Inflammatory Cell Migration in Rheumatoid Arthritis: A Comprehensive Review (original) (raw)
References
Parkes M, Cortes A, van Heel DA, Brown MA (2013) Genetic insights into common pathways and complex relationships among immune-mediated diseases. Nat Rev Genet 14(9):661–673. doi:10.1038/nrg3502 ArticleCASPubMed Google Scholar
Roadmap Epigenomics C, Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, Heravi-Moussavi A, Kheradpour P, Zhang Z, Wang J, Ziller MJ, Amin V, Whitaker JW, Schultz MD, Ward LD, Sarkar A, Quon G, Sandstrom RS, Eaton ML, Wu YC, Pfenning AR, Wang X, Claussnitzer M, Liu Y, Coarfa C, Harris RA, Shoresh N, Epstein CB, Gjoneska E, Leung D, Xie W, Hawkins RD, Lister R, Hong C, Gascard P, Mungall AJ, Moore R, Chuah E, Tam A, Canfield TK, Hansen RS, Kaul R, Sabo PJ, Bansal MS, Carles A, Dixon JR, Farh KH, Feizi S, Karlic R, Kim AR, Kulkarni A, Li D, Lowdon R, Elliott G, Mercer TR, Neph SJ, Onuchic V, Polak P, Rajagopal N, Ray P, Sallari RC, Siebenthall KT, Sinnott-Armstrong NA, Stevens M, Thurman RE, Wu J, Zhang B, Zhou X, Beaudet AE, Boyer LA, De Jager PL, Farnham PJ, Fisher SJ, Haussler D, Jones SJ, Li W, Marra MA, McManus MT, Sunyaev S, Thomson JA, Tlsty TD, Tsai LH, Wang W, Waterland RA, Zhang MQ, Chadwick LH, Bernstein BE, Costello JF, Ecker JR, Hirst M, Meissner A, Milosavljevic A, Ren B, Stamatoyannopoulos JA, Wang T, Kellis M (2015) Integrative analysis of 111 reference human epigenomes. Nature 518(7539):317–330. doi:10.1038/nature14248 ArticleCAS Google Scholar
Farh KK, Marson A, Zhu J, Kleinewietfeld M, Housley WJ, Beik S, Shoresh N, Whitton H, Ryan RJ, Shishkin AA, Hatan M, Carrasco-Alfonso MJ, Mayer D, Luckey CJ, Patsopoulos NA, De Jager PL, Kuchroo VK, Epstein CB, Daly MJ, Hafler DA, Bernstein BE (2015) Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 518(7539):337–343. doi:10.1038/nature13835 ArticleCASPubMed Google Scholar
van Beers JJ, Schwarte CM, Stammen-Vogelzangs J, Oosterink E, Bozic B, Pruijn GJ (2013) The rheumatoid arthritis synovial fluid citrullinome reveals novel citrullinated epitopes in apolipoprotein E, myeloid nuclear differentiation antigen, and beta-actin. Arthritis Rheum 65(1):69–80. doi:10.1002/art.37720 ArticlePubMedCAS Google Scholar
Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, Sundin U, van Venrooij WJ (2003) Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum 48(10):2741–2749. doi:10.1002/art.11223 ArticlePubMedCAS Google Scholar
Nielen MM, van Schaardenburg D, Reesink HW, van de Stadt RJ, van der Horst-Bruinsma IE, de Koning MH, Habibuw MR, Vandenbroucke JP, Dijkmans BA (2004) Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum 50(2):380–386. doi:10.1002/art.20018 ArticlePubMed Google Scholar
Hyun Sohn D, Rhodes C, Onuma K, Zhao X, Sharpe O, Gazitt T, Shiao R, Fert-Bober J, Cheng D, Lahey LJ, Wong HH, Van Eyk J, Robinson WH, Sokolove J (2015) Local joint inflammation and histone citrullination provides a murine model for the transition from preclinical autoimmunity to inflammatory arthritis. Arthritis Rheumatol. doi:10.1002/art.39283 Google Scholar
Bevaart L, Vervoordeldonk MJ, Tak PP (2010) Evaluation of therapeutic targets in animal models of arthritis: how does it relate to rheumatoid arthritis? Arthritis Rheum 62(8):2192–2205. doi:10.1002/art.27503 ArticleCASPubMed Google Scholar
Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D (1996) Organ-specific disease provoked by systemic autoimmunity. Cell 87(5):811–822 ArticleCASPubMed Google Scholar
Matsumoto I, Maccioni M, Lee DM, Maurice M, Simmons B, Brenner M, Mathis D, Benoist C (2002) How antibodies to a ubiquitous cytoplasmic enzyme may provoke joint-specific autoimmune disease. Nat Immunol 3(4):360–365. doi:10.1038/ni772 ArticleCASPubMed Google Scholar
Maccioni M, Zeder-Lutz G, Huang H, Ebel C, Gerber P, Hergueux J, Marchal P, Duchatelle V, Degott C, van Regenmortel M, Benoist C, Mathis D (2002) Arthritogenic monoclonal antibodies from K/BxN mice. J Exp Med 195(8):1071–1077 ArticleCASPubMedPubMed Central Google Scholar
Mandik-Nayak L, Wipke BT, Shih FF, Unanue ER, Allen PM (2002) Despite ubiquitous autoantigen expression, arthritogenic autoantibody response initiates in the local lymph node. Proc Natl Acad Sci USA 99(22):14368–14373. doi:10.1073/pnas.182549099 ArticleCASPubMedPubMed Central Google Scholar
Li J, Kuzin I, Moshkani S, Proulx ST, Xing L, Skrombolas D, Dunn R, Sanz I, Schwarz EM, Bottaro A (2010) Expanded CD23(+)/CD21(hi) B cells in inflamed lymph nodes are associated with the onset of inflammatory-erosive arthritis in TNF-transgenic mice and are targets of anti-CD20 therapy. J Immunol 184(11):6142–6150. doi:10.4049/jimmunol.0903489 ArticleCASPubMedPubMed Central Google Scholar
Li J, Ju Y, Bouta EM, Xing L, Wood RW, Kuzin I, Bottaro A, Ritchlin CT, Schwarz EM (2013) Efficacy of B cell depletion therapy for murine joint arthritis flare is associated with increased lymphatic flow. Arthritis Rheum 65(1):130–138. doi:10.1002/art.37709 ArticlePubMedPubMed CentralCAS Google Scholar
Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T (2004) Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 350(25):2572–2581. doi:10.1056/NEJMoa032534 ArticleCASPubMed Google Scholar
Pape KA, Catron DM, Itano AA, Jenkins MK (2007) The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity 26(4):491–502. doi:10.1016/j.immuni.2007.02.011 ArticleCASPubMed Google Scholar
Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, Mebius RE, von Andrian UH, Carroll MC (2009) Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 30(2):264–276. doi:10.1016/j.immuni.2008.12.014 ArticleCASPubMedPubMed Central Google Scholar
Sixt M, Kanazawa N, Selg M, Samson T, Roos G, Reinhardt DP, Pabst R, Lutz MB, Sorokin L (2005) The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 22(1):19–29. doi:10.1016/j.immuni.2004.11.013 ArticleCASPubMed Google Scholar
Carrasco YR, Batista FD (2007) B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 27(1):160–171. doi:10.1016/j.immuni.2007.06.007 ArticleCASPubMed Google Scholar
Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, Boes M, Fink K, Henrickson SE, Shayakhmetov DM, Di Paolo NC, van Rooijen N, Mempel TR, Whelan SP, von Andrian UH (2007) Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450(7166):110–114. doi:10.1038/nature06287 ArticleCASPubMed Google Scholar
Phan TG, Grigorova I, Okada T, Cyster JG (2007) Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat Immunol 8(9):992–1000. doi:10.1038/ni1494 ArticleCASPubMed Google Scholar
Phan TG, Green JA, Gray EE, Xu Y, Cyster JG (2009) Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol 10(7):786–793. doi:10.1038/ni.1745 ArticleCASPubMedPubMed Central Google Scholar
Itoh J, Kinjoh K, Ohyama A, Nose M, Kyogoku M (1992) Application of two-color immunofluorescence staining to demonstration of T-cells and HLA-DR-bearing cells in rheumatoid synovitis. J Histochem Cytochemi Off J Histochem Soc 40(11):1675–1683 ArticleCAS Google Scholar
van Dinther-Janssen AC, Pals ST, Scheper R, Breedveld F, Meijer CJ (1990) Dendritic cells and high endothelial venules in the rheumatoid synovial membrane. J Rheumatol 17(1):11–17 PubMed Google Scholar
de Vere TA, Knight SC, Edwards AJ, Clarke JB (1983) Veiled (dendritic) cells in synovial fluid. Lancet 1(8322):472–473 Google Scholar
Zvaifler NJ, Steinman RM, Kaplan G, Lau LL, Rivelis M (1985) Identification of immunostimulatory dendritic cells in the synovial effusions of patients with rheumatoid arthritis. J Clin Invest 76(2):789–800. doi:10.1172/JCI112036 ArticleCASPubMedPubMed Central Google Scholar
Thomas R, Davis LS, Lipsky PE (1994) Rheumatoid synovium is enriched in mature antigen-presenting dendritic cells. J Immunol 152(5):2613–2623 CASPubMed Google Scholar
Page G, Lebecque S, Miossec P (2002) Anatomic localization of immature and mature dendritic cells in an ectopic lymphoid organ: correlation with selective chemokine expression in rheumatoid synovium. J Immunol 168(10):5333–5341 ArticleCASPubMed Google Scholar
Cavanagh LL, Boyce A, Smith L, Padmanabha J, Filgueira L, Pietschmann P, Thomas R (2005) Rheumatoid arthritis synovium contains plasmacytoid dendritic cells. Arthritis Res Ther 7(2):R230–240. doi:10.1186/ar1467 ArticlePubMedPubMed Central Google Scholar
Lande R, Giacomini E, Serafini B, Rosicarelli B, Sebastiani GD, Minisola G, Tarantino U, Riccieri V, Valesini G, Coccia EM (2004) Characterization and recruitment of plasmacytoid dendritic cells in synovial fluid and tissue of patients with chronic inflammatory arthritis. J Immunol 173(4):2815–2824 ArticleCASPubMed Google Scholar
Van Krinks CH, Matyszak MK, Gaston JS (2004) Characterization of plasmacytoid dendritic cells in inflammatory arthritis synovial fluid. Rheumatology 43(4):453–460. doi:10.1093/rheumatology/keh115 ArticlePubMed Google Scholar
Gatto D, Paus D, Basten A, Mackay CR, Brink R (2009) Guidance of B cells by the orphan G protein-coupled receptor EBI2 shapes humoral immune responses. Immunity 31(2):259–269. doi:10.1016/j.immuni.2009.06.016 ArticleCASPubMed Google Scholar
Hannedouche S, Zhang J, Yi T, Shen W, Nguyen D, Pereira JP, Guerini D, Baumgarten BU, Roggo S, Wen B, Knochenmuss R, Noel S, Gessier F, Kelly LM, Vanek M, Laurent S, Preuss I, Miault C, Christen I, Karuna R, Li W, Koo DI, Suply T, Schmedt C, Peters EC, Falchetto R, Katopodis A, Spanka C, Roy MO, Detheux M, Chen YA, Schultz PG, Cho CY, Seuwen K, Cyster JG, Sailer AW (2011) Oxysterols direct immune cell migration via EBI2. Nature 475(7357):524–527. doi:10.1038/nature10280 ArticleCASPubMedPubMed Central Google Scholar
Liu C, Yang XV, Wu J, Kuei C, Mani NS, Zhang L, Yu J, Sutton SW, Qin N, Banie H, Karlsson L, Sun S, Lovenberg TW (2011) Oxysterols direct B-cell migration through EBI2. Nature 475(7357):519–523. doi:10.1038/nature10226 ArticleCASPubMed Google Scholar
Gatto D, Wood K, Caminschi I, Murphy-Durland D, Schofield P, Christ D, Karupiah G, Brink R (2013) The chemotactic receptor EBI2 regulates the homeostasis, localization and immunological function of splenic dendritic cells. Nat Immunol 14(5):446–453. doi:10.1038/ni.2555 ArticleCASPubMed Google Scholar
Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B (1980) Immunisation against heterologous type II collagen induces arthritis in mice. Nature 283(5748):666–668 ArticleCASPubMed Google Scholar
LaBranche TP, Hickman-Brecks CL, Meyer DM, Storer CE, Jesson MI, Shevlin KM, Happa FA, Barve RA, Weiss DJ, Minnerly JC, Racz JL, Allen PM (2010) Characterization of the KRN cell transfer model of rheumatoid arthritis (KRN-CTM), a chronic yet synchronized version of the K/BxN mouse. Am J Pathol 177(3):1388–1396. doi:10.2353/ajpath.2010.100195 ArticleCASPubMedPubMed Central Google Scholar
Burmester GR, Stuhlmuller B, Keyszer G, Kinne RW (1997) Mononuclear phagocytes and rheumatoid synovitis. Mastermind or workhorse in arthritis? Arthritis Rheum 40(1):5–18 ArticleCASPubMed Google Scholar
Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, Meinders AE, Breedveld FC (1997) Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum 40(2):217–225 ArticleCASPubMed Google Scholar
Mulherin D, Fitzgerald O, Bresnihan B (1996) Synovial tissue macrophage populations and articular damage in rheumatoid arthritis. Arthritis Rheum 39(1):115–124 ArticleCASPubMed Google Scholar
Wipke BT, Allen PM (2001) Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 167(3):1601–1608 ArticleCASPubMed Google Scholar
Eyles JL, Hickey MJ, Norman MU, Croker BA, Roberts AW, Drake SF, James WG, Metcalf D, Campbell IK, Wicks IP (2008) A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood 112(13):5193–5201. doi:10.1182/blood-2008-02-139535 ArticleCASPubMed Google Scholar
Penna G, Sozzani S, Adorini L (2001) Cutting edge: selective usage of chemokine receptors by plasmacytoid dendritic cells. J Immunol 167(4):1862–1866 ArticleCASPubMed Google Scholar
Burman A, Haworth O, Hardie DL, Amft EN, Siewert C, Jackson DG, Salmon M, Buckley CD (2005) A chemokine-dependent stromal induction mechanism for aberrant lymphocyte accumulation and compromised lymphatic return in rheumatoid arthritis. J Immunol 174(3):1693–1700 ArticleCASPubMedPubMed Central Google Scholar
Blades MC, Ingegnoli F, Wheller SK, Manzo A, Wahid S, Panayi GS, Perretti M, Pitzalis C (2002) Stromal cell-derived factor 1 (CXCL12) induces monocyte migration into human synovium transplanted onto SCID Mice. Arthritis Rheum 46(3):824–836. doi:10.1002/art.10102 ArticleCASPubMed Google Scholar
Bradfield PF, Amft N, Vernon-Wilson E, Exley AE, Parsonage G, Rainger GE, Nash GB, Thomas AM, Simmons DL, Salmon M, Buckley CD (2003) Rheumatoid fibroblast-like synoviocytes overexpress the chemokine stromal cell-derived factor 1 (CXCL12), which supports distinct patterns and rates of CD4+ and CD8+ T cell migration within synovial tissue. Arthritis Rheum 48(9):2472–2482. doi:10.1002/art.11219 ArticleCASPubMed Google Scholar
Jacobs JP, Ortiz-Lopez A, Campbell JJ, Gerard CJ, Mathis D, Benoist C (2010) Deficiency of CXCR2, but not other chemokine receptors, attenuates autoantibody-mediated arthritis in a murine model. Arthritis Rheum 62(7):1921–1932. doi:10.1002/art.27470 CASPubMedPubMed Central Google Scholar
Barsante MM, Cunha TM, Allegretti M, Cattani F, Policani F, Bizzarri C, Tafuri WL, Poole S, Cunha FQ, Bertini R, Teixeira MM (2008) Blockade of the chemokine receptor CXCR2 ameliorates adjuvant-induced arthritis in rats. Br J Pharmacol 153(5):992–1002. doi:10.1038/sj.bjp.0707462 ArticleCASPubMed Google Scholar
Podolin PL, Bolognese BJ, Foley JJ, Schmidt DB, Buckley PT, Widdowson KL, Jin Q, White JR, Lee JM, Goodman RB, Hagen TR, Kajikawa O, Marshall LA, Hay DW, Sarau HM (2002) A potent and selective nonpeptide antagonist of CXCR2 inhibits acute and chronic models of arthritis in the rabbit. J Immunol 169(11):6435–6444 ArticleCASPubMed Google Scholar
Grespan R, Fukada SY, Lemos HP, Vieira SM, Napimoga MH, Teixeira MM, Fraser AR, Liew FY, McInnes IB, Cunha FQ (2008) CXCR2-specific chemokines mediate leukotriene B4-dependent recruitment of neutrophils to inflamed joints in mice with antigen-induced arthritis. Arthritis Rheum 58(7):2030–2040. doi:10.1002/art.23597 ArticleCASPubMed Google Scholar
Wang B, Zinselmeyer BH, Runnels HA, LaBranche TP, Morton PA, Kreisel D, Mack M, Nickerson-Nutter C, Allen PM, Miller MJ (2012) In vivo imaging implicates CCR2(+) monocytes as regulators of neutrophil recruitment during arthritis. Cell Immunol 278(1-2):103–112. doi:10.1016/j.cellimm.2012.07.005 ArticleCASPubMedPubMed Central Google Scholar
Snir O, Backlund J, Bostrom J, Andersson I, Kihlberg J, Buckner JH, Klareskog L, Holmdahl R, Malmstrom V (2012) Multifunctional T cell reactivity with native and glycosylated type II collagen in rheumatoid arthritis. Arthritis Rheum 64(8):2482–2488. doi:10.1002/art.34459 ArticleCASPubMedPubMed Central Google Scholar
Janson PC, Linton LB, Bergman EA, Marits P, Eberhardson M, Piehl F, Malmstrom V, Winqvist O (2011) Profiling of CD4+ T cells with epigenetic immune lineage analysis. J Immunol 186(1):92–102. doi:10.4049/jimmunol.1000960 ArticleCASPubMed Google Scholar
Qin S, Rottman JB, Myers P, Kassam N, Weinblatt M, Loetscher M, Koch AE, Moser B, Mackay CR (1998) The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest 101(4):746–754. doi:10.1172/JCI1422 ArticleCASPubMedPubMed Central Google Scholar
Ruth JH, Rottman JB, Katschke KJ Jr, Qin S, Wu L, LaRosa G, Ponath P, Pope RM, Koch AE (2001) Selective lymphocyte chemokine receptor expression in the rheumatoid joint. Arthritis Rheum 44(12):2750–2760 ArticleCASPubMed Google Scholar
Nanki T, Hayashida K, El-Gabalawy HS, Suson S, Shi K, Girschick HJ, Yavuz S, Lipsky PE (2000) Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J Immunol 165(11):6590–6598 ArticleCASPubMed Google Scholar
Mohan K, Issekutz TB (2007) Blockade of chemokine receptor CXCR3 inhibits T cell recruitment to inflamed joints and decreases the severity of adjuvant arthritis. J Immunol 179(12):8463–8469 ArticleCASPubMed Google Scholar
Moret FM, Hack CE, van der Wurff-Jacobs KM, de Jager W, Radstake TR, Lafeber FP, van Roon JA (2013) Intra-articular CD1c-expressing myeloid dendritic cells from rheumatoid arthritis patients express a unique set of T cell-attracting chemokines and spontaneously induce Th1, Th17 and Th2 cell activity. Arthritis Res Ther 15(5):R155. doi:10.1186/ar4338 ArticlePubMedPubMed CentralCAS Google Scholar
Rossol M, Pierer M, Arnold S, Keysser G, Burkhardt H, Baerwald C, Wagner U (2009) Negative association of the chemokine receptor CCR5 d32 polymorphism with systemic inflammatory response, extra-articular symptoms and joint erosion in rheumatoid arthritis. Arthritis Res Ther 11(3):R91. doi:10.1186/ar2733 ArticlePubMedPubMed CentralCAS Google Scholar
Pokorny V, McQueen F, Yeoman S, Merriman M, Merriman A, Harrison A, Highton J, McLean L (2005) Evidence for negative association of the chemokine receptor CCR5 d32 polymorphism with rheumatoid arthritis. Ann Rheum Dis 64(3):487–490. doi:10.1136/ard.2004.023333 ArticleCASPubMed Google Scholar
Zapico I, Coto E, Rodriguez A, Alvarez C, Torre JC, Alvarez V (2000) CCR5 (chemokine receptor-5) DNA-polymorphism influences the severity of rheumatoid arthritis. Genes Immun 1(4):288–289. doi:10.1038/sj.gene.6363673 ArticleCASPubMed Google Scholar
Lindner E, Nordang GB, Melum E, Flato B, Selvaag AM, Thorsby E, Kvien TK, Forre OT, Lie BA (2007) Lack of association between the chemokine receptor 5 polymorphism CCR5delta32 in rheumatoid arthritis and juvenile idiopathic arthritis. BMC Med Genet 8:33. doi:10.1186/1471-2350-8-33 ArticlePubMedPubMed CentralCAS Google Scholar
Kohem CL, Brenol JC, Xavier RM, Bredemeier M, Brenol CV, Dedavid e Silva TL, de Castilhos Mello A, de Canedo AD, Neves AG, Chies JA (2007) The chemokine receptor CCR5 genetic polymorphism and expression in rheumatoid arthritis patients. Scand J Rheumatol 36(5):359–364. doi:10.1080/03009740701393999 ArticleCASPubMed Google Scholar
Quinones MP, Ahuja SK, Jimenez F, Schaefer J, Garavito E, Rao A, Chenaux G, Reddick RL, Kuziel WA, Ahuja SS (2004) Experimental arthritis in CC chemokine receptor 2-null mice closely mimics severe human rheumatoid arthritis. J Clin Invest 113(6):856–866. doi:10.1172/JCI20126 ArticleCASPubMedPubMed Central Google Scholar
Chung SH, Seki K, Choi BI, Kimura KB, Ito A, Fujikado N, Saijo S, Iwakura Y (2010) CXC chemokine receptor 4 expressed in T cells plays an important role in the development of collagen-induced arthritis. Arthritis Res ther 12(5):R188. doi:10.1186/ar3158 ArticlePubMedPubMed CentralCAS Google Scholar
Nanki T, Imai T, Nagasaka K, Urasaki Y, Nonomura Y, Taniguchi K, Hayashida K, Hasegawa J, Yoshie O, Miyasaka N (2002) Migration of CX3CR1-positive T cells producing type 1 cytokines and cytotoxic molecules into the synovium of patients with rheumatoid arthritis. Arthritis Rheum 46(11):2878–2883. doi:10.1002/art.10622 ArticleCASPubMed Google Scholar
Blaschke S, Koziolek M, Schwarz A, Benohr P, Middel P, Schwarz G, Hummel KM, Muller GA (2003) Proinflammatory role of fractalkine (CX3CL1) in rheumatoid arthritis. J Rheumatol 30(9):1918–1927 CASPubMed Google Scholar
Yano R, Yamamura M, Sunahori K, Takasugi K, Yamana J, Kawashima M, Makino H (2007) Recruitment of CD16+ monocytes into synovial tissues is mediated by fractalkine and CX3CR1 in rheumatoid arthritis patients. Acta Med Okayama 61(2):89–98 CASPubMed Google Scholar
Nanki T, Urasaki Y, Imai T, Nishimura M, Muramoto K, Kubota T, Miyasaka N (2004) Inhibition of fractalkine ameliorates murine collagen-induced arthritis. J Immunol 173(11):7010–7016 ArticleCASPubMed Google Scholar
Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, Sugimoto N, Yamaguchi T, Nomura T, Ito H, Nakamura T, Sakaguchi N, Sakaguchi S (2007) Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med 204(12):2803–2812. doi:10.1084/jem.20071397 ArticleCASPubMedPubMed Central Google Scholar
Matsui T, Akahoshi T, Namai R, Hashimoto A, Kurihara Y, Rana M, Nishimura A, Endo H, Kitasato H, Kawai S, Takagishi K, Kondo H (2001) Selective recruitment of CCR6-expressing cells by increased production of MIP-3 alpha in rheumatoid arthritis. Clin Exp Immunol 125(1):155–161 ArticleCASPubMedPubMed Central Google Scholar
Tsunemi S, Iwasaki T, Kitano S, Imado T, Miyazawa K, Sano H (2010) Effects of the novel immunosuppressant FTY720 in a murine rheumatoid arthritis model. Clin Immunol 136(2):197–204. doi:10.1016/j.clim.2010.03.428 ArticleCASPubMed Google Scholar
Wang F, Tan W, Guo D, He S (2007) Reduction of CD4 positive T cells and improvement of pathological changes of collagen-induced arthritis by FTY720. Eur J Pharmacol 573(1-3):230–240. doi:10.1016/j.ejphar.2007.07.029 ArticleCASPubMed Google Scholar
Matsuura M, Imayoshi T, Okumoto T (2000) Effect of FTY720, a novel immunosuppressant, on adjuvant- and collagen-induced arthritis in rats. Int J Immunopharmacol 22(4):323–331 ArticleCASPubMed Google Scholar
Kitano M, Hla T, Sekiguchi M, Kawahito Y, Yoshimura R, Miyazawa K, Iwasaki T, Sano H, Saba JD, Tam YY (2006) Sphingosine 1-phosphate/sphingosine 1-phosphate receptor 1 signaling in rheumatoid synovium: regulation of synovial proliferation and inflammatory gene expression. Arthritis Rheum 54(3):742–753. doi:10.1002/art.21668 ArticleCASPubMed Google Scholar
Lai WQ, Irwan AW, Goh HH, Howe HS, Yu DT, Valle-Onate R, McInnes IB, Melendez AJ, Leung BP (2008) Anti-inflammatory effects of sphingosine kinase modulation in inflammatory arthritis. J Immunol 181(11):8010–8017 ArticleCASPubMed Google Scholar
Edwards JC, Cambridge G (2001) Sustained improvement in rheumatoid arthritis following a protocol designed to deplete B lymphocytes. Rheumatology 40(2):205–211 ArticleCASPubMed Google Scholar
Cohen SB, Emery P, Greenwald MW, Dougados M, Furie RA, Genovese MC, Keystone EC, Loveless JE, Burmester GR, Cravets MW, Hessey EW, Shaw T, Totoritis MC, Group RT (2006) Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum 54(9):2793–2806. doi:10.1002/art.22025 ArticleCASPubMed Google Scholar
van Gaalen FA, Linn-Rasker SP, van Venrooij WJ, de Jong BA, Breedveld FC, Verweij CL, Toes RE, Huizinga TW (2004) Autoantibodies to cyclic citrullinated peptides predict progression to rheumatoid arthritis in patients with undifferentiated arthritis: a prospective cohort study. Arthritis Rheum 50(3):709–715. doi:10.1002/art.20044 ArticlePubMedCAS Google Scholar
Amara K, Steen J, Murray F, Morbach H, Fernandez-Rodriguez BM, Joshua V, Engstrom M, Snir O, Israelsson L, Catrina AI, Wardemann H, Corti D, Meffre E, Klareskog L, Malmstrom V (2013) Monoclonal IgG antibodies generated from joint-derived B cells of RA patients have a strong bias toward citrullinated autoantigen recognition. J Exp Med 210(3):445–455. doi:10.1084/jem.20121486 ArticleCASPubMedPubMed Central Google Scholar
Nanki T, Takada K, Komano Y, Morio T, Kanegane H, Nakajima A, Lipsky PE, Miyasaka N (2009) Chemokine receptor expression and functional effects of chemokines on B cells: implication in the pathogenesis of rheumatoid arthritis. Arthritis Res ther 11(5):R149. doi:10.1186/ar2823 ArticlePubMedPubMed CentralCAS Google Scholar
Sellam J, Rouanet S, Hendel-Chavez H, Miceli-Richard C, Combe B, Sibilia J, Le Loet X, Tebib J, Jourdan R, Dougados M, Taoufik Y, Mariette X (2013) CCL19, a B cell chemokine, is related to the decrease of blood memory B cells and predicts the clinical response to rituximab in patients with rheumatoid arthritis. Arthritis Rheum 65(9):2253–2261. doi:10.1002/art.38023 ArticleCASPubMed Google Scholar
Pickens SR, Chamberlain ND, Volin MV, Pope RM, Talarico NE, Mandelin AM 2nd, Shahrara S (2012) Role of the CCL21 and CCR7 pathways in rheumatoid arthritis angiogenesis. Arthritis Rheum 64(8):2471–2481. doi:10.1002/art.34452 ArticleCASPubMedPubMed Central Google Scholar
Shi K, Hayashida K, Kaneko M, Hashimoto J, Tomita T, Lipsky PE, Yoshikawa H, Ochi T (2001) Lymphoid chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients. J Immunol 166(1):650–655 ArticleCASPubMed Google Scholar
Bugatti S, Caporali R, Manzo A, Sakellariou G, Rossi S, Montecucco C (2012) Ultrasonographic and MRI characterisation of the palindromic phase of rheumatoid arthritis. Ann Rheum Dis 71(4):625–626. doi:10.1136/annrheumdis-2011-200077 ArticlePubMed Google Scholar
Conaghan PG, O'Connor P, McGonagle D, Astin P, Wakefield RJ, Gibbon WW, Quinn M, Karim Z, Green MJ, Proudman S, Isaacs J, Emery P (2003) Elucidation of the relationship between synovitis and bone damage: a randomized magnetic resonance imaging study of individual joints in patients with early rheumatoid arthritis. Arthritis Rheum 48(1):64–71. doi:10.1002/art.10747 ArticlePubMed Google Scholar
Boyesen P, Haavardsholm EA, Ostergaard M, van der Heijde D, Sesseng S, Kvien TK (2011) MRI in early rheumatoid arthritis: synovitis and bone marrow oedema are independent predictors of subsequent radiographic progression. Ann Rheum Dis 70(3):428–433. doi:10.1136/ard.2009.123950 ArticlePubMed Google Scholar
McQueen FM, Benton N, Perry D, Crabbe J, Robinson E, Yeoman S, McLean L, Stewart N (2003) Bone edema scored on magnetic resonance imaging scans of the dominant carpus at presentation predicts radiographic joint damage of the hands and feet six years later in patients with rheumatoid arthritis. Arthritis Rheum 48(7):1814–1827. doi:10.1002/art.11162 ArticlePubMed Google Scholar
Hayashida K, Ochi T, Fujimoto M, Owaki H, Shimaoka Y, Ono K, Matsumoto K (1992) Bone marrow changes in adjuvant-induced and collagen-induced arthritis. Interleukin-1 and interleukin-6 activity and abnormal myelopoiesis. Arthritis Rheum 35(2):241–245 ArticleCASPubMed Google Scholar
Proulx ST, Kwok E, You Z, Papuga MO, Beck CA, Shealy DJ, Calvi LM, Ritchlin CT, Awad HA, Boyce BF, Xing L, Schwarz EM (2008) Elucidating bone marrow edema and myelopoiesis in murine arthritis using contrast-enhanced magnetic resonance imaging. Arthritis Rheum 58(7):2019–2029. doi:10.1002/art.23546 ArticlePubMedPubMed Central Google Scholar
Wyllie JC (1983) Histopathology of the subchondral bone lesion in rheumatoid arthritis. J Rheumatol Suppl 11:26–28 CASPubMed Google Scholar
Watson WC, Tooms RE, Carnesale PG, Dutkowsky JP (1994) A case of germinal center formation by CD45RO T and CD20 B lymphocytes in rheumatoid arthritic subchondral bone: proposal for a two-compartment model of immune-mediated disease with implications for immunotherapeutic strategies. Clin Immunol Immunopathol 73(1):27–37 ArticleCASPubMed Google Scholar
O'Connell JX, Nielsen GP, Rosenberg AE (1999) Subchondral acute inflammation in severe arthritis: a sterile osteomyelitis? Am J Surg Pathol 23(2):192–197 ArticlePubMed Google Scholar
Kaneko M, Tomita T, Nakase T, Ohsawa Y, Seki H, Takeuchi E, Takano H, Shi K, Takahi K, Kominami E, Uchiyama Y, Yoshikawa H, Ochi T (2001) Expression of proteinases and inflammatory cytokines in subchondral bone regions in the destructive joint of rheumatoid arthritis. Rheumatology 40(3):247–255 ArticleCASPubMed Google Scholar
Bromley M, Woolley DE (1984) Chondroclasts and osteoclasts at subchondral sites of erosion in the rheumatoid joint. Arthritis Rheum 27(9):968–975 ArticleCASPubMed Google Scholar
Bugatti S, Caporali R, Manzo A, Vitolo B, Pitzalis C, Montecucco C (2005) Involvement of subchondral bone marrow in rheumatoid arthritis: lymphoid neogenesis and in situ relationship to subchondral bone marrow osteoclast recruitment. Arthritis Rheum 52(11):3448–3459. doi:10.1002/art.21377 ArticleCASPubMed Google Scholar
McQueen FM, Stewart N, Crabbe J, Robinson E, Yeoman S, Tan PL, McLean L (1998) Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals a high prevalence of erosions at four months after symptom onset. Ann Rheum Dis 57(6):350–356 ArticleCASPubMedPubMed Central Google Scholar
Gravallese EM, Harada Y, Wang JT, Gorn AH, Thornhill TS, Goldring SR (1998) Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis. Am J Pathol 152(4):943–951 CASPubMedPubMed Central Google Scholar
Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, Wong T, Campagnuolo G, Moran E, Bogoch ER, Van G, Nguyen LT, Ohashi PS, Lacey DL, Fish E, Boyle WJ, Penninger JM (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402(6759):304–309. doi:10.1038/46303 ArticleCASPubMed Google Scholar
Romas E, Sims NA, Hards DK, Lindsay M, Quinn JW, Ryan PF, Dunstan CR, Martin TJ, Gillespie MT (2002) Osteoprotegerin reduces osteoclast numbers and prevents bone erosion in collagen-induced arthritis. Am J Pathol 161(4):1419–1427. doi:10.1016/S0002-9440(10)64417-3 ArticleCASPubMedPubMed Central Google Scholar
Lubberts E, Oppers-Walgreen B, Pettit AR, Van Den Bersselaar L, Joosten LA, Goldring SR, Gravallese EM, Van Den Berg WB (2002) Increase in expression of receptor activator of nuclear factor kappaB at sites of bone erosion correlates with progression of inflammation in evolving collagen-induced arthritis. Arthritis Rheum 46(11):3055–3064. doi:10.1002/art.10607 ArticleCASPubMed Google Scholar
Pettit AR, Ji H, von Stechow D, Muller R, Goldring SR, Choi Y, Benoist C, Gravallese EM (2001) TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol 159(5):1689–1699. doi:10.1016/S0002-9440(10)63016-7 ArticleCASPubMedPubMed Central Google Scholar
Redlich K, Hayer S, Ricci R, David JP, Tohidast-Akrad M, Kollias G, Steiner G, Smolen JS, Wagner EF, Schett G (2002) Osteoclasts are essential for TNF-alpha-mediated joint destruction. J Clin Invest 110(10):1419–1427. doi:10.1172/JCI15582 ArticleCASPubMedPubMed Central Google Scholar
Redlich K, Hayer S, Maier A, Dunstan CR, Tohidast-Akrad M, Lang S, Turk B, Pietschmann P, Woloszczuk W, Haralambous S, Kollias G, Steiner G, Smolen JS, Schett G (2002) Tumor necrosis factor alpha-mediated joint destruction is inhibited by targeting osteoclasts with osteoprotegerin. Arthritis Rheum 46(3):785–792. doi:10.1002/art.10097 ArticleCASPubMed Google Scholar
Schett G, Stolina M, Bolon B, Middleton S, Adlam M, Brown H, Zhu L, Feige U, Zack DJ (2005) Analysis of the kinetics of osteoclastogenesis in arthritic rats. Arthritis Rheum 52(10):3192–3201. doi:10.1002/art.21343 ArticlePubMed Google Scholar
Walsh NC, Reinwald S, Manning CA, Condon KW, Iwata K, Burr DB, Gravallese EM (2009) Osteoblast function is compromised at sites of focal bone erosion in inflammatory arthritis. J Bone Miner Res 24(9):1572–1585. doi:10.1359/jbmr.090320 ArticleCASPubMed Google Scholar
Jimenez-Boj E, Redlich K, Turk B, Hanslik-Schnabel B, Wanivenhaus A, Chott A, Smolen JS, Schett G (2005) Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J Immunol 175(4):2579–2588 ArticleCASPubMed Google Scholar
Gortz B, Hayer S, Redlich K, Zwerina J, Tohidast-Akrad M, Tuerk B, Hartmann C, Kollias G, Steiner G, Smolen JS, Schett G (2004) Arthritis induces lymphocytic bone marrow inflammation and endosteal bone formation. J Bone Miner Res 19(6):990–998. doi:10.1359/JBMR.040205 ArticleCASPubMed Google Scholar
Arai F, Miyamoto T, Ohneda O, Inada T, Sudo T, Brasel K, Miyata T, Anderson DM, Suda T (1999) Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J Exp Med 190(12):1741–1754 ArticleCASPubMedPubMed Central Google Scholar
Charles JF, Hsu LY, Niemi EC, Weiss A, Aliprantis AO, Nakamura MC (2012) Inflammatory arthritis increases mouse osteoclast precursors with myeloid suppressor function. J Clin Invest 122(12):4592–4605. doi:10.1172/JCI60920 ArticleCASPubMedPubMed Central Google Scholar
Jacome-Galarza CE, Lee SK, Lorenzo JA, Aguila HL (2013) Identification, characterization, and isolation of a common progenitor for osteoclasts, macrophages, and dendritic cells from murine bone marrow and periphery. J Bone Miner Res 28(5):1203–1213. doi:10.1002/jbmr.1822 ArticleCASPubMedPubMed Central Google Scholar
Jacquin C, Gran DE, Lee SK, Lorenzo JA, Aguila HL (2006) Identification of multiple osteoclast precursor populations in murine bone marrow. J Bone Miner Res 21(1):67–77. doi:10.1359/JBMR.051007 ArticlePubMed Google Scholar
Hettinger J, Richards DM, Hansson J, Barra MM, Joschko AC, Krijgsveld J, Feuerer M (2013) Origin of monocytes and macrophages in a committed progenitor. Nat Immunol 14(8):821–830. doi:10.1038/ni.2638 ArticleCASPubMed Google Scholar
Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93(2):165–176 ArticleCASPubMed Google Scholar
Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ, Penninger JM (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397(6717):315–323. doi:10.1038/16852 ArticleCASPubMed Google Scholar
Hsu H, Lacey DL, Dunstan CR, Solovyev I, Colombero A, Timms E, Tan HL, Elliott G, Kelley MJ, Sarosi I, Wang L, Xia XZ, Elliott R, Chiu L, Black T, Scully S, Capparelli C, Morony S, Shimamoto G, Bass MB, Boyle WJ (1999) Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc Natl Acad Sci USA 96(7):3540–3545 ArticleCASPubMedPubMed Central Google Scholar
Udagawa N, Takahashi N, Akatsu T, Tanaka H, Sasaki T, Nishihara T, Koga T, Martin TJ, Suda T (1990) Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proc Natl Acad Sci USA 87(18):7260–7264 ArticleCASPubMedPubMed Central Google Scholar
Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17(10):1231–1234. doi:10.1038/nm.2452 ArticleCASPubMed Google Scholar
Mundy GR, Varani J, Orr W, Gondek MD, Ward PA (1978) Resorbing bone is chemotactic for monocytes. Nature 275(5676):132–135 ArticleCASPubMed Google Scholar
Nevius E, Pinho F, Dhodapkar M, Jin H, Nadrah K, Horowitz MC, Kikuta J, Ishii M, Pereira JP (2015) Oxysterols and EBI2 promote osteoclast precursor migration to bone surfaces and regulate bone mass homeostasis. J Exp Med 212(11):1931-1946. doi:10.1084/jem.20150088 ArticleCASPubMedPubMed Central Google Scholar
Jacquelin S, Licata F, Dorgham K, Hermand P, Poupel L, Guyon E, Deterre P, Hume DA, Combadiere C, Boissonnas A (2013) CX3CR1 reduces Ly6Chigh-monocyte motility within and release from the bone marrow after chemotherapy in mice. Blood 122(5):674–683. doi:10.1182/blood-2013-01-480749 ArticlePubMed Google Scholar
Rahimi P, Wang CY, Stashenko P, Lee SK, Lorenzo JA, Graves DT (1995) Monocyte chemoattractant protein-1 expression and monocyte recruitment in osseous inflammation in the mouse. Endocrinology 136(6):2752–2759. doi:10.1210/endo.136.6.7750500 CASPubMed Google Scholar
Williams SR, Jiang Y, Cochran D, Dorsam G, Graves DT (1992) Regulated expression of monocyte chemoattractant protein-1 in normal human osteoblastic cells. Am J Physiol 263(1 Pt 1):C194–199 CASPubMed Google Scholar
Zhu JF, Valente AJ, Lorenzo JA, Carnes D, Graves DT (1994) Expression of monocyte chemoattractant protein 1 in human osteoblastic cells stimulated by proinflammatory mediators. J Bone Miner Res 9(7):1123–1130. doi:10.1002/jbmr.5650090721 ArticleCASPubMed Google Scholar
Kim MS, Day CJ, Selinger CI, Magno CL, Stephens SR, Morrison NA (2006) MCP-1-induced human osteoclast-like cells are tartrate-resistant acid phosphatase, NFATc1, and calcitonin receptor-positive but require receptor activator of NFkappaB ligand for bone resorption. J Biol Chem 281(2):1274–1285. doi:10.1074/jbc.M510156200 ArticleCASPubMed Google Scholar
Kim MS, Magno CL, Day CJ, Morrison NA (2006) Induction of chemokines and chemokine receptors CCR2b and CCR4 in authentic human osteoclasts differentiated with RANKL and osteoclast like cells differentiated by MCP-1 and RANTES. J Cell Biochem 97(3):512–518. doi:10.1002/jcb.20649 ArticleCASPubMed Google Scholar
Li X, Qin L, Bergenstock M, Bevelock LM, Novack DV, Partridge NC (2007) Parathyroid hormone stimulates osteoblastic expression of MCP-1 to recruit and increase the fusion of pre/osteoclasts. J Biol Chem 282(45):33098–33106. doi:10.1074/jbc.M611781200 ArticleCASPubMed Google Scholar
Binder NB, Niederreiter B, Hoffmann O, Stange R, Pap T, Stulnig TM, Mack M, Erben RG, Smolen JS, Redlich K (2009) Estrogen-dependent and C-C chemokine receptor-2-dependent pathways determine osteoclast behavior in osteoporosis. Nat Med 15(4):417–424. doi:10.1038/nm.1945 ArticleCASPubMed Google Scholar
Yamada Y, Ando F, Niino N, Shimokata H (2002) Association of a polymorphism of the CC chemokine receptor-2 gene with bone mineral density. Genomics 80(1):8–12 ArticleCASPubMed Google Scholar
Lee B, Doranz BJ, Rana S, Yi Y, Mellado M, Frade JM, Martinez AC, O'Brien SJ, Dean M, Collman RG, Doms RW (1998) Influence of the CCR2-V64I polymorphism on human immunodeficiency virus type 1 coreceptor activity and on chemokine receptor function of CCR2b, CCR3, CCR5, and CXCR4. J Virol 72(9):7450–7458 CASPubMedPubMed Central Google Scholar
Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7(3):311–317. doi:10.1038/ni1309 ArticleCASPubMed Google Scholar
Shi C, Jia T, Mendez-Ferrer S, Hohl TM, Serbina NV, Lipuma L, Leiner I, Li MO, Frenette PS, Pamer EG (2011) Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands. Immunity 34(4):590–601. doi:10.1016/j.immuni.2011.02.016 ArticleCASPubMedPubMed Central Google Scholar
Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF (2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117(4):902–909. doi:10.1172/JCI29919 ArticleCASPubMedPubMed Central Google Scholar
Kikuta J, Nevius E, Ishii M, Pereira JP (2015) Trafficking of osteoclast precursors. In: Lorenzo J (ed) Osteoimmunology: interactions of the immune and skeletal systems, 2 edn. Elsevier, pp 25–40
Hoshino A, Iimura T, Ueha S, Hanada S, Maruoka Y, Mayahara M, Suzuki K, Imai T, Ito M, Manome Y, Yasuhara M, Kirino T, Yamaguchi A, Matsushima K, Yamamoto K (2010) Deficiency of chemokine receptor CCR1 causes osteopenia due to impaired functions of osteoclasts and osteoblasts. J Biol Chem 285(37):28826–28837. doi:10.1074/jbc.M109.099424 ArticleCASPubMedPubMed Central Google Scholar
Koizumi K, Saitoh Y, Minami T, Takeno N, Tsuneyama K, Miyahara T, Nakayama T, Sakurai H, Takano Y, Nishimura M, Imai T, Yoshie O, Saiki I (2009) Role of CX3CL1/fractalkine in osteoclast differentiation and bone resorption. J Immunol 183(12):7825–7831. doi:10.4049/jimmunol.0803627 ArticleCASPubMed Google Scholar
Hoshino A, Ueha S, Hanada S, Imai T, Ito M, Yamamoto K, Matsushima K, Yamaguchi A, Iimura T (2013) Roles of chemokine receptor CX3CR1 in maintaining murine bone homeostasis through the regulation of both osteoblasts and osteoclasts. J Cell Sci 126(Pt 4):1032–1045. doi:10.1242/jcs.113910 ArticleCASPubMed Google Scholar
Han KH, Ryu JW, Lim KE, Lee SH, Kim Y, Hwang CS, Choi JY, Han KO (2014) Vascular expression of the chemokine CX3CL1 promotes osteoclast recruitment and exacerbates bone resorption in an irradiated murine model. Bone 61:91–101. doi:10.1016/j.bone.2013.12.032 ArticleCASPubMed Google Scholar
Jenne CN, Enders A, Rivera R, Watson SR, Bankovich AJ, Pereira JP, Xu Y, Roots CM, Beilke JN, Banerjee A, Reiner SL, Miller SA, Weinmann AS, Goodnow CC, Lanier LL, Cyster JG, Chun J (2009) T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J Exp Med 206(11):2469–2481. doi:10.1084/jem.20090525 ArticleCASPubMedPubMed Central Google Scholar
Walzer T, Chiossone L, Chaix J, Calver A, Carozzo C, Garrigue-Antar L, Jacques Y, Baratin M, Tomasello E, Vivier E (2007) Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat Immunol 8(12):1337–1344. doi:10.1038/ni1523 ArticleCASPubMed Google Scholar
Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, Vacher J, Proia RL, Germain RN (2009) Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 458(7237):524–528. doi:10.1038/nature07713 ArticleCASPubMedPubMed Central Google Scholar
Ishii M, Kikuta J, Shimazu Y, Meier-Schellersheim M, Germain RN (2010) Chemorepulsion by blood S1P regulates osteoclast precursor mobilization and bone remodeling in vivo. J Exp Med 207(13):2793–2798. doi:10.1084/jem.20101474 ArticleCASPubMedPubMed Central Google Scholar
Grassi F, Piacentini A, Cristino S, Toneguzzi S, Cavallo C, Facchini A, Lisignoli G (2003) Human osteoclasts express different CXC chemokines depending on cell culture substrate: molecular and immunocytochemical evidence of high levels of CXCL10 and CXCL12. Histochem Cell Biol 120(5):391–400. doi:10.1007/s00418-003-0587-3 ArticleCASPubMed Google Scholar
Wright LM, Maloney W, Yu X, Kindle L, Collin-Osdoby P, Osdoby P (2005) Stromal cell-derived factor-1 binding to its chemokine receptor CXCR4 on precursor cells promotes the chemotactic recruitment, development and survival of human osteoclasts. Bone 36(5):840–853. doi:10.1016/j.bone.2005.01.021 ArticleCASPubMed Google Scholar
Semerad CL, Christopher MJ, Liu F, Short B, Simmons PJ, Winkler I, Levesque JP, Chappel J, Ross FP, Link DC (2005) G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 106(9):3020–3027. doi:10.1182/blood-2004-01-0272 ArticleCASPubMedPubMed Central Google Scholar
Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977–988. doi:10.1016/j.immuni.2006.10.016 ArticleCASPubMed Google Scholar
Yu X, Huang Y, Collin-Osdoby P, Osdoby P (2003) Stromal cell-derived factor-1 (SDF-1) recruits osteoclast precursors by inducing chemotaxis, matrix metalloproteinase-9 (MMP-9) activity, and collagen transmigration. J Bone Miner Res 18(8):1404–1418. doi:10.1359/jbmr.2003.18.8.1404 ArticleCASPubMed Google Scholar
Zhou BO, Yue R, Murphy MM, Peyer JG, Morrison SJ (2014) Leptin-Receptor-Expressing Mesenchymal Stromal Cells Represent the Main Source of Bone Formed by Adult Bone Marrow. Cell Stem Cell. doi:10.1016/j.stem.2014.06.008 Google Scholar
Omatsu Y, Sugiyama T, Kohara H, Kondoh G, Fujii N, Kohno K, Nagasawa T (2010) The Essential Functions of Adipo-osteogenic Progenitors as the Hematopoietic Stem and Progenitor Cell Niche. Immunity 33(3):387–399. doi:10.1016/j.immuni.2010.08.017 ArticleCASPubMed Google Scholar
Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829–834. doi:10.1038/nature09262 ArticleCASPubMedPubMed Central Google Scholar
Ding L, Morrison SJ (2013) Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature. doi:10.1038/nature11885 Google Scholar
Hirbe AC, Rubin J, Uluckan O, Morgan EA, Eagleton MC, Prior JL, Piwnica-Worms D, Weilbaecher KN (2007) Disruption of CXCR4 enhances osteoclastogenesis and tumor growth in bone. Proc Natl Acad Sci USA 104(35):14062–14067. doi:10.1073/pnas.0705203104 ArticleCASPubMedPubMed Central Google Scholar
Pandey R, Mousawy K, Nagarkatti M, Nagarkatti P (2009) Endocannabinoids and immune regulation. Pharmacol Res Off J Italian Pharmacol Soc 60(2):85–92. doi:10.1016/j.phrs.2009.03.019 CAS Google Scholar
Pereira JP, An J, Xu Y, Huang Y, Cyster JG (2009) Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids. Nat Immunol 10(4):403–411 ArticleCASPubMedPubMed Central Google Scholar
Idris AI, Sophocleous A, Landao-Bassonga E, van't Hof RJ, Ralston SH (2008) Regulation of bone mass, osteoclast function, and ovariectomy-induced bone loss by the type 2 cannabinoid receptor. Endocrinology 149(11):5619–5626. doi:10.1210/en.2008-0150 ArticleCASPubMed Google Scholar
Ofek O, Karsak M, Leclerc N, Fogel M, Frenkel B, Wright K, Tam J, Attar-Namdar M, Kram V, Shohami E, Mechoulam R, Zimmer A, Bab I (2006) Peripheral cannabinoid receptor, CB2, regulates bone mass. Proc Natl Acad Sci USA 103(3):696–701. doi:10.1073/pnas.0504187103 ArticleCASPubMedPubMed Central Google Scholar
Karsak M, Cohen-Solal M, Freudenberg J, Ostertag A, Morieux C, Kornak U, Essig J, Erxlebe E, Bab I, Kubisch C, de Vernejoul MC, Zimmer A (2005) Cannabinoid receptor type 2 gene is associated with human osteoporosis. Hum Mol Genet 14(22):3389–3396. doi:10.1093/hmg/ddi370 ArticleCASPubMed Google Scholar
Yamada Y, Ando F, Shimokata H (2007) Association of candidate gene polymorphisms with bone mineral density in community-dwelling Japanese women and men. Int J Mol Med 19(5):791–801 CASPubMed Google Scholar
Keffer J, Probert L, Cazlaris H, Georgopoulos S, Kaslaris E, Kioussis D, Kollias G (1991) Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J 10(13):4025–4031 CASPubMedPubMed Central Google Scholar
Yao Z, Li P, Zhang Q, Schwarz EM, Keng P, Arbini A, Boyce BF, Xing L (2006) Tumor necrosis factor-alpha increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-Fms expression. J Biol Chem 281(17):11846–11855. doi:10.1074/jbc.M512624200 ArticleCASPubMed Google Scholar
Speziani C, Rivollier A, Gallois A, Coury F, Mazzorana M, Azocar O, Flacher M, Bella C, Tebib J, Jurdic P, Rabourdin-Combe C, Delprat C (2007) Murine dendritic cell transdifferentiation into osteoclasts is differentially regulated by innate and adaptive cytokines. Eur J Immunol 37(3):747–757. doi:10.1002/eji.200636534 ArticleCASPubMed Google Scholar
Rivollier A, Mazzorana M, Tebib J, Piperno M, Aitsiselmi T, Rabourdin-Combe C, Jurdic P, Servet-Delprat C (2004) Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 104(13):4029–4037. doi:10.1182/blood-2004-01-0041 ArticleCASPubMed Google Scholar
Fumoto T, Takeshita S, Ito M, Ikeda K (2014) Physiological functions of osteoblast lineage and T cell-derived RANKL in bone homeostasis. J Bone Miner Res 29(4):830–842. doi:10.1002/jbmr.2096 ArticleCASPubMed Google Scholar
Onal M, Xiong J, Chen X, Thostenson JD, Almeida M, Manolagas SC, O'Brien CA (2012) Receptor activator of nuclear factor kappaB ligand (RANKL) protein expression by B lymphocytes contributes to ovariectomy-induced bone loss. J Biol Chem 287(35):29851–29860. doi:10.1074/jbc.M112.377945 ArticleCASPubMedPubMed Central Google Scholar
Horwood NJ, Kartsogiannis V, Quinn JM, Romas E, Martin TJ, Gillespie MT (1999) Activated T lymphocytes support osteoclast formation in vitro. Biochem Biophys Res Commun 265(1):144–150. doi:10.1006/bbrc.1999.1623 ArticleCASPubMed Google Scholar
Takayanagi H, Iizuka H, Juji T, Nakagawa T, Yamamoto A, Miyazaki T, Koshihara Y, Oda H, Nakamura K, Tanaka S (2000) Involvement of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum 43(2):259–269. doi:10.1002/1529-0131(200002)43:2<259::AID-ANR4>3.0.CO;2-W ArticleCASPubMed Google Scholar
Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-hora M, Kodama T, Tanaka S, Bluestone JA, Takayanagi H (2014) Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med 20(1):62–68. doi:10.1038/nm.3432 ArticleCASPubMed Google Scholar
Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, Tanaka S, Kodama T, Akira S, Iwakura Y, Cua DJ, Takayanagi H (2006) Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 203(12):2673–2682. doi:10.1084/jem.20061775 ArticleCASPubMedPubMed Central Google Scholar
Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103(9):1345–1352. doi:10.1172/JCI5703 ArticleCASPubMedPubMed Central Google Scholar
Adamopoulos IE, Chao CC, Geissler R, Laface D, Blumenschein W, Iwakura Y, McClanahan T, Bowman EP (2010) Interleukin-17A upregulates receptor activator of NF-kappaB on osteoclast precursors. Arthritis Res Ther 12(1):R29. doi:10.1186/ar2936 ArticlePubMedPubMed CentralCAS Google Scholar
Adamopoulos IE, Suzuki E, Chao CC, Gorman D, Adda S, Maverakis E, Zarbalis K, Geissler R, Asio A, Blumenschein WM, McClanahan T, De Waal MR, Gershwin ME, Bowman EP (2015) IL-17A gene transfer induces bone loss and epidermal hyperplasia associated with psoriatic arthritis. Ann Rheum Dis 74(6):1284–1292. doi:10.1136/annrheumdis-2013-204782 ArticlePubMed Google Scholar
Tyagi AM, Srivastava K, Mansoori MN, Trivedi R, Chattopadhyay N, Singh D (2012) Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: a new candidate in the pathogenesis of osteoporosis. PLoS One 7(9):e44552. doi:10.1371/journal.pone.0044552 ArticleCASPubMedPubMed Central Google Scholar
Danks L, Komatsu N, Guerrini MM, Sawa S, Armaka M, Kollias G, Nakashima T, Takayanagi H (2015) RANKL expressed on synovial fibroblasts is primarily responsible for bone erosions during joint inflammation. Ann Rheum Dis. doi:10.1136/annrheumdis-2014-207137 PubMed Google Scholar
Cohen SB, Dore RK, Lane NE, Ory PA, Peterfy CG, Sharp JT, van der Heijde D, Zhou L, Tsuji W, Newmark R, Denosumab Rheumatoid Arthritis Study G (2008) Denosumab treatment effects on structural damage, bone mineral density, and bone turnover in rheumatoid arthritis: a twelve-month, multicenter, randomized, double-blind, placebo-controlled, phase II clinical trial. Arthritis Rheum 58(5):1299–1309. doi:10.1002/art.23417 ArticleCASPubMed Google Scholar
Kikuta J, Wada Y, Kowada T, Wang Z, Sun-Wada GH, Nishiyama I, Mizukami S, Maiya N, Yasuda H, Kumanogoh A, Kikuchi K, Germain RN, Ishii M (2013) Dynamic visualization of RANKL and Th17-mediated osteoclast function. J Clin Invest 123(2):866–873. doi:10.1172/JCI65054 CASPubMedPubMed Central Google Scholar
Kobayashi K, Takahashi N, Jimi E, Udagawa N, Takami M, Kotake S, Nakagawa N, Kinosaki M, Yamaguchi K, Shima N, Yasuda H, Morinaga T, Higashio K, Martin TJ, Suda T (2000) Tumor necrosis factor alpha stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction. J Exp Med 191(2):275–286 ArticleCASPubMedPubMed Central Google Scholar
Yokota K, Sato K, Miyazaki T, Kitaura H, Kayama H, Miyoshi F, Araki Y, Akiyama Y, Takeda K, Mimura T (2014) Combination of tumor necrosis factor alpha and interleukin-6 induces mouse osteoclast-like cells with bone resorption activity both in vitro and in vivo. Arthritis Rheumatol 66(1):121–129. doi:10.1002/art.38218 ArticleCASPubMed Google Scholar
Kim N, Kadono Y, Takami M, Lee J, Lee SH, Okada F, Kim JH, Kobayashi T, Odgren PR, Nakano H, Yeh WC, Lee SK, Lorenzo JA, Choi Y (2005) Osteoclast differentiation independent of the TRANCE-RANK-TRAF6 axis. J Exp Med 202(5):589–595. doi:10.1084/jem.20050978 ArticleCASPubMedPubMed Central Google Scholar
Haringman JJ, Gerlag DM, Zwinderman AH, Smeets TJ, Kraan MC, Baeten D, McInnes IB, Bresnihan B, Tak PP (2005) Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 64(6):834–838. doi:10.1136/ard.2004.029751 ArticleCASPubMed Google Scholar
Harre U, Georgess D, Bang H, Bozec A, Axmann R, Ossipova E, Jakobsson PJ, Baum W, Nimmerjahn F, Szarka E, Sarmay G, Krumbholz G, Neumann E, Toes R, Scherer HU, Catrina AI, Klareskog L, Jurdic P, Schett G (2012) Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 122(5):1791–1802. doi:10.1172/JCI60975 ArticleCASPubMedPubMed Central Google Scholar
Harre U, Lang SC, Pfeifle R, Rombouts Y, Fruhbeisser S, Amara K, Bang H, Lux A, Koeleman CA, Baum W, Dietel K, Grohn F, Malmstrom V, Klareskog L, Kronke G, Kocijan R, Nimmerjahn F, Toes RE, Herrmann M, Scherer HU, Schett G (2015) Glycosylation of immunoglobulin G determines osteoclast differentiation and bone loss. Nat Commun 6:6651. doi:10.1038/ncomms7651 ArticleCASPubMedPubMed Central Google Scholar
Li P, Schwarz EM, O'Keefe RJ, Ma L, Boyce BF, Xing L (2004) RANK signaling is not required for TNFalpha-mediated increase in CD11(hi) osteoclast precursors but is essential for mature osteoclast formation in TNFalpha-mediated inflammatory arthritis. J Bone Miner Res 19(2):207–213. doi:10.1359/JBMR.0301233 ArticleCASPubMed Google Scholar
Ritchlin CT, Haas-Smith SA, Li P, Hicks DG, Schwarz EM (2003) Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest 111(6):821–831. doi:10.1172/JCI16069 ArticleCASPubMedPubMed Central Google Scholar
Koch AE, Kunkel SL, Harlow LA, Johnson B, Evanoff HL, Haines GK, Burdick MD, Pope RM, Strieter RM (1992) Enhanced production of monocyte chemoattractant protein-1 in rheumatoid arthritis. J Clin Invest 90(3):772–779. doi:10.1172/JCI115950 ArticleCASPubMedPubMed Central Google Scholar
Akahoshi T, Wada C, Endo H, Hirota K, Hosaka S, Takagishi K, Kondo H, Kashiwazaki S, Matsushima K (1993) Expression of monocyte chemotactic and activating factor in rheumatoid arthritis. Regulation of its production in synovial cells by interleukin-1 and tumor necrosis factor. Arthritis Rheum 36(6):762–771 ArticleCASPubMed Google Scholar
Gong JH, Ratkay LG, Waterfield JD, Clark-Lewis I (1997) An antagonist of monocyte chemoattractant protein 1 (MCP-1) inhibits arthritis in the MRL-lpr mouse model. J Exp Med 186(1):131–137 ArticleCASPubMedPubMed Central Google Scholar
Plater-Zyberk C, Hoogewerf AJ, Proudfoot AE, Power CA, Wells TN (1997) Effect of a CC chemokine receptor antagonist on collagen induced arthritis in DBA/1 mice. Immunol Lett 57(1-3):117–120 ArticleCASPubMed Google Scholar
Bruhl H, Cihak J, Schneider MA, Plachy J, Rupp T, Wenzel I, Shakarami M, Milz S, Ellwart JW, Stangassinger M, Schlondorff D, Mack M (2004) Dual role of CCR2 during initiation and progression of collagen-induced arthritis: evidence for regulatory activity of CCR2+ T cells. J Immunol 172(2):890–898 ArticlePubMed Google Scholar
Rampersad RR, Tarrant TK, Vallanat CT, Quintero-Matthews T, Weeks MF, Esserman DA, Clark J, Di Padova F, Patel DD, Fong AM, Liu P (2011) Enhanced Th17-cell responses render CCR2-deficient mice more susceptible for autoimmune arthritis. PLoS One 6(10):e25833. doi:10.1371/journal.pone.0025833 ArticleCASPubMedPubMed Central Google Scholar
Koch AE, Kunkel SL, Harlow LA, Mazarakis DD, Haines GK, Burdick MD, Pope RM, Strieter RM (1994) Macrophage inflammatory protein-1 alpha. A novel chemotactic cytokine for macrophages in rheumatoid arthritis. J Clin Invest 93(3):921–928. doi:10.1172/JCI117097 ArticleCASPubMedPubMed Central Google Scholar
Volin MV, Shah MR, Tokuhira M, Haines GK, Woods JM, Koch AE (1998) RANTES expression and contribution to monocyte chemotaxis in arthritis. Clin Immunol Immunopathol 89(1):44–53 ArticleCASPubMed Google Scholar
Lebre MC, Vergunst CE, Choi IY, Aarrass S, Oliveira AS, Wyant T, Horuk R, Reedquist KA, Tak PP (2011) Why CCR2 and CCR5 blockade failed and why CCR1 blockade might still be effective in the treatment of rheumatoid arthritis. PLoS One 6(7):e21772. doi:10.1371/journal.pone.0021772 ArticleCASPubMedPubMed Central Google Scholar
Vallet S, Raje N, Ishitsuka K, Hideshima T, Podar K, Chhetri S, Pozzi S, Breitkreutz I, Kiziltepe T, Yasui H, Ocio EM, Shiraishi N, Jin J, Okawa Y, Ikeda H, Mukherjee S, Vaghela N, Cirstea D, Ladetto M, Boccadoro M, Anderson KC (2007) MLN3897, a novel CCR1 inhibitor, impairs osteoclastogenesis and inhibits the interaction of multiple myeloma cells and osteoclasts. Blood 110(10):3744–3752. doi:10.1182/blood-2007-05-093294 ArticleCASPubMedPubMed Central Google Scholar
Vergunst CE, Gerlag DM, Lopatinskaya L, Klareskog L, Smith MD, van den Bosch F, Dinant HJ, Lee Y, Wyant T, Jacobson EW, Baeten D, Tak PP (2008) Modulation of CCR2 in rheumatoid arthritis: a double-blind, randomized, placebo-controlled clinical trial. Arthritis Rheum 58(7):1931–1939. doi:10.1002/art.23591 ArticleCASPubMed Google Scholar
Vergunst CE, Gerlag DM, von Moltke L, Karol M, Wyant T, Chi X, Matzkin E, Leach T, Tak PP (2009) MLN3897 plus methotrexate in patients with rheumatoid arthritis: safety, efficacy, pharmacokinetics, and pharmacodynamics of an oral CCR1 antagonist in a phase IIa, double-blind, placebo-controlled, randomized, proof-of-concept study. Arthritis Rheum 60(12):3572–3581. doi:10.1002/art.24978 ArticleCASPubMed Google Scholar
Gerlag DM, Hollis S, Layton M, Vencovsky J, Szekanecz Z, Braddock M, Tak PP, Group ES (2010) Preclinical and clinical investigation of a CCR5 antagonist, AZD5672, in patients with rheumatoid arthritis receiving methotrexate. Arthritis Rheum 62(11):3154–3160. doi:10.1002/art.27652 ArticleCASPubMed Google Scholar
van Kuijk AW, Vergunst CE, Gerlag DM, Bresnihan B, Gomez-Reino JJ, Rouzier R, Verschueren PC, van der Leij C, Maas M, Kraan MC, Tak PP (2010) CCR5 blockade in rheumatoid arthritis: a randomised, double-blind, placebo-controlled clinical trial. Ann Rheum Dis 69(11):2013–2016. doi:10.1136/ard.2010.131235 ArticlePubMedCAS Google Scholar
Hayashida K, Nanki T, Girschick H, Yavuz S, Ochi T, Lipsky PE (2001) Synovial stromal cells from rheumatoid arthritis patients attract monocytes by producing MCP-1 and IL-8. Arthritis Res 3(2):118–126 ArticleCASPubMedPubMed Central Google Scholar
Fukuda S, Kohsaka H, Takayasu A, Yokoyama W, Miyabe C, Miyabe Y, Harigai M, Miyasaka N, Nanki T (2014) Cannabinoid receptor 2 as a potential therapeutic target in rheumatoid arthritis. BMC Musculoskelet Disord 15:275. doi:10.1186/1471-2474-15-275 ArticlePubMedPubMed CentralCAS Google Scholar
Ha J, Choi HS, Lee Y, Kwon HJ, Song YW, Kim HH (2010) CXC chemokine ligand 2 induced by receptor activator of NF-kappa B ligand enhances osteoclastogenesis. J Immunol 184(9):4717–4724. doi:10.4049/jimmunol.0902444 ArticleCASPubMed Google Scholar
Coelho FM, Pinho V, Amaral FA, Sachs D, Costa VV, Rodrigues DH, Vieira AT, Silva TA, Souza DG, Bertini R, Teixeira AL, Teixeira MM (2008) The chemokine receptors CXCR1/CXCR2 modulate antigen-induced arthritis by regulating adhesion of neutrophils to the synovial microvasculature. Arthritis Rheum 58(8):2329–2337. doi:10.1002/art.23622 ArticlePubMed Google Scholar
Kasama T, Strieter RM, Lukacs NW, Lincoln PM, Burdick MD, Kunkel SL (1995) Interleukin-10 expression and chemokine regulation during the evolution of murine type II collagen-induced arthritis. J Clin Invest 95(6):2868–2876. doi:10.1172/JCI117993 ArticleCASPubMedPubMed Central Google Scholar
Heinig M, Petretto E, Wallace C, Bottolo L, Rotival M, Lu H, Li Y, Sarwar R, Langley SR, Bauerfeind A, Hummel O, Lee YA, Paskas S, Rintisch C, Saar K, Cooper J, Buchan R, Gray EE, Cyster JG, Erdmann J, Hengstenberg C, Maouche S, Ouwehand WH, Rice CM, Samani NJ, Schunkert H, Goodall AH, Schulz H, Roider HG, Vingron M, Blankenberg S, Munzel T, Zeller T, Szymczak S, Ziegler A, Tiret L, Smyth DJ, Pravenec M, Aitman TJ, Cambien F, Clayton D, Todd JA, Hubner N, Cook SA (2010) A trans-acting locus regulates an anti-viral expression network and type 1 diabetes risk. Nature 467(7314):460–464. doi:10.1038/nature09386 ArticleCASPubMedPubMed Central Google Scholar
Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, Essers J, Mitrovic M, Ning K, Cleynen I, Theatre E, Spain SL, Raychaudhuri S, Goyette P, Wei Z, Abraham C, Achkar JP, Ahmad T, Amininejad L, Ananthakrishnan AN, Andersen V, Andrews JM, Baidoo L, Balschun T, Bampton PA, Bitton A, Boucher G, Brand S, Buning C, Cohain A, Cichon S, D'Amato M, De Jong D, Devaney KL, Dubinsky M, Edwards C, Ellinghaus D, Ferguson LR, Franchimont D, Fransen K, Gearry R, Georges M, Gieger C, Glas J, Haritunians T, Hart A, Hawkey C, Hedl M, Hu X, Karlsen TH, Kupcinskas L, Kugathasan S, Latiano A, Laukens D, Lawrance IC, Lees CW, Louis E, Mahy G, Mansfield J, Morgan AR, Mowat C, Newman W, Palmieri O, Ponsioen CY, Potocnik U, Prescott NJ, Regueiro M, Rotter JI, Russell RK, Sanderson JD, Sans M, Satsangi J, Schreiber S, Simms LA, Sventoraityte J, Targan SR, Taylor KD, Tremelling M, Verspaget HW, De Vos M, Wijmenga C, Wilson DC, Winkelmann J, Xavier RJ, Zeissig S, Zhang B, Zhang CK, Zhao H, International IBDGC, Silverberg MS, Annese V, Hakonarson H, Brant SR, Radford-Smith G, Mathew CG, Rioux JD, Schadt EE, Daly MJ, Franke A, Parkes M, Vermeire S, Barrett JC, Cho JH (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491(7422):119–124. doi:10.1038/nature11582 ArticleCASPubMedPubMed Central Google Scholar
Wallace C, Rotival M, Cooper JD, Rice CM, Yang JH, McNeill M, Smyth DJ, Niblett D, Cambien F, Cardiogenics C, Tiret L, Todd JA, Clayton DG, Blankenberg S (2012) Statistical colocalization of monocyte gene expression and genetic risk variants for type 1 diabetes. Hum Mol Genet 21(12):2815–2824. doi:10.1093/hmg/dds098 ArticleCASPubMedPubMed Central Google Scholar
Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA (2010) Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature 465(7299):793–797. doi:10.1038/nature09135 ArticleCASPubMedPubMed Central Google Scholar
Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A (2009) IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458(7240):904–908. doi:10.1038/nature07815 ArticleCASPubMed Google Scholar
Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, Offner S, Dunant CF, Eshkind L, Bockamp E, Lio P, Macdonald HR, Trumpp A (2008) Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135(6):1118–1129. doi:10.1016/j.cell.2008.10.048 ArticleCASPubMed Google Scholar
Lawlor KE, Campbell IK, Metcalf D, O'Donnell K, van Nieuwenhuijze A, Roberts AW, Wicks IP (2004) Critical role for granulocyte colony-stimulating factor in inflammatory arthritis. Proc Natl Acad Sci USA 101(31):11398–11403. doi:10.1073/pnas.0404328101 ArticleCASPubMedPubMed Central Google Scholar