Phagocyte partnership during the onset and resolution of inflammation (original) (raw)

• Nathan, C. Neutrophils and immunity: challenges and opportunities. Nature Rev. Immunol. 6, 173–182 (2006).
  Article CAS Google Scholar
• Ingersoll, M. A. et al. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 115, e10–e19 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Ziegler-Heitbrock, L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 81, 584–592 (2007).
  Article CAS PubMed Google Scholar
• Auffray, C. et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317, 666–670 (2007). The first paper to show the potential importance of non-classical monocytes during the start of an inflammatory response in the mouse.
  Article CAS PubMed Google Scholar
• Nahrendorf, M. et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204, 3037–3047 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Zhao, C. et al. Identification of novel functional differences in monocyte subsets using proteomic and transcriptomic methods. J. Proteome Res. 8, 4028–4038 (2009).
  Article CAS PubMed Google Scholar
• Frankenberger, M., Sternsdorf, T., Pechumer, H., Pforte, A. & Ziegler-Heitbrock, H. W. Differential cytokine expression in human blood monocyte subpopulations: a polymerase chain reaction analysis. Blood 87, 373–377 (1996).
  CAS PubMed Google Scholar
• Belge, K. U. et al. The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J. Immunol. 168, 3536–3542 (2002).
  Article CAS PubMed Google Scholar
• Tacke, F. et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117, 185–194 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• An, G. et al. P-selectin glycoprotein ligand-1 is highly expressed on Ly-6Chi monocytes and a major determinant for Ly-6Chi monocyte recruitment to sites of atherosclerosis in mice. Circulation 117, 3227–3237 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Soehnlein, O. & Weber, C. Myeloid cells in atherosclerosis: initiators and decision shapers. Semin. Immunopathol. 31, 35–47 (2009).
  Article CAS PubMed Google Scholar
• Geissmann, F., Jung, S. & Littman, D. R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71–82 (2003). This paper proves the existence of two mouse monocyte subsets with phenotypical and functional differences.
  Article CAS PubMed Google Scholar
• Yona, S. & Jung, S. Monocytes: subsets, origins, fates and functions. Curr. Opin. Hematol. 17, 53–59 (2010).
  Article PubMed Google Scholar
• Kaufmann, S. H. Immunology's foundation: the 100-year anniversary of the Nobel Prize to Paul Ehrlich and Elie Metchnikoff. Nature Immunol. 9, 705–712 (2008).
  Article CAS Google Scholar
• Dale, D. C., Boxer, L. & Liles, W. C. The phagocytes: neutrophils and monocytes. Blood 112, 935–945 (2008).
  Article CAS PubMed Google Scholar
• Kantari, C., Pederzoli-Ribeil, M. & Witko-Sarsat, V. The role of neutrophils and monocytes in innate immunity. Contrib. Microbiol. 15, 118–146 (2008).
  Article CAS PubMed Google Scholar
• Akashi, K., Traver, D., Miyamoto, T. & Weissman, I. L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404, 193–197 (2000).
  Article CAS PubMed Google Scholar
• Ma, Q., Jones, D. & Springer, T. A. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10, 463–471 (1999).
  Article CAS PubMed Google Scholar
• Suratt, B. T. et al. Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104, 565–571 (2004).
  Article CAS PubMed Google Scholar
• Serbina, N. V. & Pamer, E. G. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nature Immunol. 7, 311–317 (2006).
  Article CAS Google Scholar
• Martin, C. et al. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19, 583–593 (2003).
  Article CAS PubMed Google Scholar
• Swirski, F. K. et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325, 612–616 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Nathan, C. & Shiloh, M. U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl Acad. Sci. USA 97, 8841–8848 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Kono, H. & Rock, K. L. How dying cells alert the immune system to danger. Nature Rev. Immunol. 8, 279–289 (2008).
  Article CAS Google Scholar
• Medzhitov, R. Recognition of microorganisms and activation of the immune response. Nature 449, 819–826 (2007).
  Article CAS PubMed Google Scholar
• Passlick, B., Flieger, D. & Ziegler-Heitbrock, H. W. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74, 2527–2534 (1989).
  CAS PubMed Google Scholar
• Auffray, C., Sieweke, M. H. & Geissmann, F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27, 669–692 (2009).
  Article CAS PubMed Google Scholar
• Soehnlein, O., Lindbom, L. & Weber, C. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 114, 4613–4623 (2009).
  Article CAS PubMed Google Scholar
• Yamasaki, S., Ishikawa, E., Sakuma, M., Hara, H., Ogata, K. & Saito, T. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nature Immunol. 9, 1179–1188 (2008). This paper describes a new mechanism linking cell necrosis to inflammation, whereby necrotic cell-derived SAP130 ligates CLEC4E on myeloid cell resulting in transcription of pro-inflammatory signals.
  Article CAS Google Scholar
• Hara, H. et al. The adaptor protein CARD9 is essential for the activation of myeloid cells through ITAM-associated and Toll-like receptors. Nature Immunol. 8, 619–629 (2007).
  Article CAS Google Scholar
• Scaffidi, P., Misteli, T. & Bianchi, M. E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191–195 (2002).
  Article CAS PubMed Google Scholar
• Bianchi, M. E. HMGB1 loves company. J. Leukoc. Biol. 86, 573–576 (2009).
  Article CAS PubMed Google Scholar
• Tian, J. et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nature Immunol. 8, 487–496 (2007).
  Article CAS Google Scholar
• Yanai, H. et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462, 99–103 (2009).
  Article CAS PubMed Google Scholar
• Chen, G. Y., Tang, J., Zheng, P. & Liu, Y. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 323, 1722–1725 (2009). This study elucidates a new mechanism by which the immune system discriminates between infection and tissue injury.
  Article CAS PubMed PubMed Central Google Scholar
• Liu, Y., Chen, G. Y. & Zheng, P. CD24-Siglec G/10 discriminates danger- from pathogen-associated molecular patterns. Trends Immunol. 30, 557–561 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• García-Ramallo, E. et al. Resident cell chemokine expression serves as the major mechanism for leukocyte recruitment during local inflammation. J. Immunol. 169, 6467–6473 (2002).
  Article PubMed Google Scholar
• Beck-Schimmer, B. et al. Alveolar macrophages regulate neutrophil recruitment in endotoxin-induced lung injury. Respir. Res. 6, 61 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Cailhier, J. F. et al. Conditional macrophage ablation demonstrates that resident macrophages initiate acute peritoneal inflammation. J. Immunol. 174, 2336–2342 (2005).
  Article CAS PubMed Google Scholar
• Cailhier, J. F. et al. Resident pleural macrophages are key orchestrators of neutrophil recruitment in pleural inflammation. Am. J. Respir. Crit. Care. Med. 173, 540–547 (2006).
  Article CAS PubMed Google Scholar
• Ajuebor, M. N. et al. Role of resident peritoneal macrophages and mast cells in chemokine production and neutrophil migration in acute inflammation: evidence for an inhibitory loop involving endogenous IL-10. J. Immunol. 162, 1685–1691 (1999).
  CAS PubMed Google Scholar
• Yamamoto, S. et al. TRPM2-mediated Ca2+ influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nature Med. 14, 738–747 (2008).
  Article CAS PubMed Google Scholar
• Van den Steen, P. E., Proost, P., Wuyts, A., Van Damme, J. & Opdenakker, G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-α and leaves RANTES and MCP-2 intact. Blood 96, 2673–2681 (2000).
  CAS PubMed Google Scholar
• Tester, A. M. et al. LPS responsiveness and neutrophil chemotaxis in vivo require PMN MMP-8 activity. PLoS ONE 2, e312 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Funk, C. D. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871–1875 (2001).
  Article CAS PubMed Google Scholar
• Dahlén, S. E. et al. Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc. Natl Acad. Sci. USA 78, 3887–3891 (1981).
  Article PubMed PubMed Central Google Scholar
• Schoenberger, S. P. BLT for speed. Nature Immunol. 4, 937–939 (2003).
  Article CAS Google Scholar
• Tager, A. M. & Luster, A. D. BLT1 and BLT2: the leukotriene B4 receptors. Prostaglandins Leukot. Essent. Fatty Acids. 69, 123–134 (2003).
  Article CAS PubMed Google Scholar
• Borregaard, N. & Cowland, J. B. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89, 3503–3521 (1997).
  CAS PubMed Google Scholar
• Faurschou, M. & Borregaard, N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5, 1317–1327 (2003).
  Article CAS PubMed Google Scholar
• Gautam, N., Herwald, H., Hedqvist, P. & Lindbom, L. Signaling via β2 integrins triggers neutrophil-dependent alteration in endothelial barrier function. J. Exp. Med. 191, 1829–1839 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Gautam, N. et al. Heparin-binding protein (HBP/CAP37): a missing link in neutrophil-evoked alteration of vascular permeability. Nature Med. 7, 1123–1127 (2001).
  Article CAS PubMed Google Scholar
• Herwald, H. et al. M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116, 367–379 (2004).
  Article CAS PubMed Google Scholar
• Soehnlein, O. et al. Neutrophil degranulation mediates severe lung damage triggered by streptococcal M1 protein. Eur. Respir. J. 32, 405–412 (2008).
  Article CAS PubMed Google Scholar
• Soehnlein, O. et al. Neutrophil-derived heparin-binding protein (HBP/CAP37) deposited on endothelium enhances monocyte arrest under flow conditions. J. Immunol. 174, 6399–6405 (2005).
  Article CAS PubMed Google Scholar
• Soehnlein, O. & Lindbom, L. Neutrophil-derived azurocidin alarms the immune system. J. Leukoc. Biol. 85, 344–351 (2009).
  Article CAS PubMed Google Scholar
• Lee, T. D., Gonzalez, M. L., Kumar, P., Grammas, P. & Pereira, H. A. CAP37, a neutrophil-derived inflammatory mediator, augments leukocyte adhesion to endothelial monolayers. Microvasc. Res. 66, 38–48 (2003).
  Article CAS PubMed Google Scholar
• Lacy, P. & Eitzen, G. Control of granule exocytosis in neutrophils. Front. Biosci. 13, 5559–5570 (2008).
  Article CAS PubMed Google Scholar
• Gombart, A. F. & Koeffler, H. P. Neutrophil specific granule deficiency and mutations in the gene encoding transcription factor C/EBPɛ. Curr. Opin. Hematol. 9, 36–42 (2002).
  Article PubMed Google Scholar
• De Yang. et al. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192, 1069–1074 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Yang, D., de la Rosa, G., Tewary, P. & Oppenheim, J. J. Alarmins link neutrophils and dendritic cells. Trends Immunol. 30, 531–537 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Chertov, O. et al. Identification of human neutrophil-derived cathepsin G. and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J. Exp. Med. 186, 739–747 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Ye, R. D. et al. International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev. 61, 119–161 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Sun, R. et al. Identification of neutrophil granule protein cathepsin G. as a novel chemotactic agonist for the G. protein-coupled formyl peptide receptor. J. Immunol. 173, 428–436 (2004).
  Article CAS PubMed Google Scholar
• Soehnlein, O. et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 112, 1461–1471 (2008). This work highlights the importance of neutrophil-derived LL-37 and azurocidin in extravasation of classical, inflammatory monocytes.
  Article CAS PubMed PubMed Central Google Scholar
• Soehnlein, O., Weber, C. & Lindbom, L. Neutrophil granule proteins tune monocytic cell function. Trends Immunol. 30, 538–546 (2009).
  Article CAS PubMed Google Scholar
• Ley, K., Laudanna, C., Cybulsky, M. I. & Nourshargh, S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nature Rev. Immunol. 7, 678–689 (2007).
  Article CAS Google Scholar
• Romano, M. et al. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6, 315–325 (1997).
  Article CAS PubMed Google Scholar
• Taga, T. et al. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 58, 573–581 (1989).
  Article CAS PubMed Google Scholar
• Hurst, S. M. et al. Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 14, 705–714 (2001).
  Article CAS PubMed Google Scholar
• Chalaris, A. et al. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 110, 1748–1755 (2007).
  Article CAS PubMed Google Scholar
• Taekema-Roelvink, M. E. et al. Proteinase 3 enhances endothelial monocyte chemoattractant protein-1 production and induces increased adhesion of neutrophils to endothelial cells by upregulating intercellular cell adhesion molecule-1. J. Am. Soc. Nephrol. 12, 932–940 (2001).
  CAS PubMed Google Scholar
• Påhlman, L. I. et al. Streptococcal M protein: a multipotent and powerful inducer of inflammation. J. Immunol. 177, 1221–1228 (2006).
  Article PubMed Google Scholar
• Berahovich, R. D. et al. Proteolytic activation of alternative CCR1 ligands in inflammation. J. Immunol. 174, 7341–7351 (2005).
  Article CAS PubMed Google Scholar
• Borregaard, N., Sørensen, O. E. & Theilgaard-Mönch, K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 28, 340–345 (2007).
  Article CAS PubMed Google Scholar
• Gerszten, R. E. et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 398, 718–723 (1999).
  Article CAS PubMed Google Scholar
• Kasama, T., Strieter, R. M., Standiford, T. J., Burdick, M. D. & Kunkel, S. L. Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1α. J. Exp. Med. 178, 63–72 (1993).
  Article CAS PubMed Google Scholar
• Pelletier, M. et al. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115, 335–343 (2010).
  Article CAS PubMed Google Scholar
• Scapini, P. et al. Neutrophils produce biologically active macrophage inflammatory protein-3α (MIP-3α)/CCL20 and MIP-3β/CCL19. Eur. J. Immunol. 31, 1981–1988 (2001).
  Article CAS PubMed Google Scholar
• Le Borgne, M. et al. Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo. Immunity 24, 191–201 (2006).
  Article CAS PubMed Google Scholar
• Wittamer, V. et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J. Exp. Med. 198, 977–985 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Zabel, B. A. et al. Chemerin activation by serine proteases of the coagulation, fibrinolytic, and inflammatory cascades. J. Biol. Chem. 280, 34661–34666 (2005).
  Article CAS PubMed Google Scholar
• Soehnlein, O. et al. Neutrophil primary granule proteins HBP and HNP1–3 boost bacterial phagocytosis by human and murine macrophages. J. Clin. Invest. 118, 3491–3502 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Soehnlein, O. Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins. J. Mol. Med. 87, 1157–1164 (2009).
  Article CAS PubMed Google Scholar
• Silva, M. T. When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J. Leukoc. Biol. 87, 93–106 (2010).
  Article CAS PubMed Google Scholar
• Serhan, C. N., Chiang, N. & Van Dyke, T. E. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Rev. Immunol. 8, 349–361 (2008).
  Article CAS Google Scholar
• Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K. & Serhan, C. N. Lipid mediator class switching during acute inflammation: signals in resolution. Nature Immunol. 2, 612–619 (2001). The first study showing the presence of predominantly pro-inflammatory lipid mediators such as leukotriene B 4 and PGE 2 in inflammatory exudates at early stages, and anti-inflammatory lipid mediators such as lipoxin A4 dominates at later stages.
  Article CAS Google Scholar
• Freire-de-Lima, C. G. et al. Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J. Biol. Chem. 281, 38376–38384 (2006).
  Article CAS PubMed Google Scholar
• Maddox, J. F. et al. Lipoxin A4 stable analogs are potent mimetics that stimulate human monocytes and THP-1 cells via a G.-protein-linked lipoxin A4 receptor. J. Biol. Chem. 272, 6972–6978 (1997).
  Article CAS PubMed Google Scholar
• Chiang, N. et al. The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo. Pharmacol. Rev. 58, 463–487 (2006).
  Article CAS PubMed Google Scholar
• József, L., Zouki, C., Petasis, N. A., Serhan, C. N. & Filep, J. G. Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit peroxynitrite formation, NF-κB and AP-1 activation, and IL-8 gene expression in human leukocytes. Proc. Natl Acad. Sci. USA 99, 13266–13271 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Serhan, C. N. et al. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J. Exp. Med. 192, 1197–1204 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Arita, M. et al. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J. Immunol. 178, 3912–3917 (2007).
  Article CAS PubMed Google Scholar
• Arita, M. et al. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med. 201, 713–722 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Serhan, C. N. et al. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J. Exp. Med. 206, 15–23 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Perretti, M. & D'Acquisto, F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nature Rev. Immunol. 9, 62–70 (2009).
  Article CAS Google Scholar
• Perretti, M. et al. Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nature Med. 2, 1259–1262 (1996).
  Article CAS PubMed Google Scholar
• Scannell, M. et al. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol. 178, 4595–4605 (2007).
  Article CAS PubMed Google Scholar
• Cash, J. L. et al. Synthetic chemerin-derived peptides suppress inflammation through ChemR23. J. Exp. Med. 205, 767–775 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Cash, J. L., Christian, A. R. & Greaves, D. R. Chemerin peptides promote phagocytosis in a ChemR23- and Syk-dependent manner. J. Immunol. 184, 5315–5324 (2010).
  Article CAS PubMed Google Scholar
• Ariel, A. et al. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nature Immunol. 7, 1209–1216 (2006).
  Article CAS Google Scholar
• Dean, R. A. et al. Macrophage-specific metalloelastase (MMP-12) truncates and inactivates ELR+ CXC chemokines and generates CCL2, -7, -8, and -13 antagonists: potential role of the macrophage in terminating polymorphonuclear leukocyte influx. Blood 112, 3455–3464 (2008).
  Article CAS PubMed Google Scholar
• McQuibban, G. A. et al. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289, 1202–1206 (2000).
  Article CAS PubMed Google Scholar
• McQuibban, G. A. et al. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100, 1160–1167 (2002).
  CAS PubMed Google Scholar
• van den Berg, J. M., Weyer, S., Weening, J. J., Roos, D. & Kuijpers, T. W. Divergent effects of tumor necrosis factor α on apoptosis of human neutrophils. J. Leukoc. Biol. 69, 467–473 (2001).
  CAS PubMed Google Scholar
• Allenbach, C. et al. Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major. J. Immunol. 176, 6656–6664 (2006).
  Article CAS PubMed Google Scholar
• Meszaros, A. J., Reichner, J. S. & Albina, J. E. Macrophage-induced neutrophil apoptosis. J. Immunol. 165, 435–441 (2000).
  Article CAS PubMed Google Scholar
• Bournazou, I. et al. Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin. J. Clin. Invest. 119, 20–32 (2009). This report identifies lactoferrin from apoptotic cells as an important mediator for blocking the further influx of neutrophils.
  CAS PubMed Google Scholar
• de la Rosa, G., Yang, D., Tewary, P., Varadhachary, A. & Oppenheim, J. J. Lactoferrin acts as an alarmin to promote the recruitment and activation of APCs and antigen-specific immune responses. J. Immunol. 180, 6868–6876 (2008).
  Article CAS PubMed Google Scholar
• Brinkmann, V. et al. Neutrophil extracellular traps kill bacteria. Science 303, 1532–1535 (2004).
  Article CAS PubMed Google Scholar
• Papayannopoulos, V. & Zychlinsky, A. NETs: a new strategy for using old weapons. Trends Immunol. 30, 513–521 (2009).
  Article CAS PubMed Google Scholar
• Stark, M. A. et al. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285–294 (2005).
  Article CAS PubMed Google Scholar
• Ley, K., Smith, E. & Stark, M. A. IL-17A-producing neutrophil-regulatory Tn lymphocytes. Immunol. Res. 34, 229–242 (2006).
  Article CAS PubMed Google Scholar
• Lauber, K. et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113, 717–730 (2003). In this study, the authors identify lysophosphatidylcholine released from apoptotic cells as an important 'find me' signal.
  Article CAS PubMed Google Scholar
• Kim, S. J., Gershov, D., Ma, X., Brot, N. & Elkon, K. B. I-PLA2 activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J. Exp. Med. 196, 655–665 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Peter, C. et al. Migration to apoptotic “find-me” signals is mediated via the phagocyte receptor G2A. J. Biol. Chem. 283, 5296–5305 (2008).
  Article CAS PubMed Google Scholar
• Elliott, M. R. et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461, 282–286 (2009). This report highlights the importance of the nucleotides ATP and UTP secreted from apoptotic cells in recruiting monocytes and macrophages.
  Article CAS PubMed PubMed Central Google Scholar
• Truman, L. A. et al. CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis. Blood 112, 5026–5036 (2008).
  Article CAS PubMed Google Scholar
• Zhao, M. et al. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN. Nature 442, 457–460 (2006).
  Article CAS PubMed Google Scholar
• Voll, R. E. et al. Immunosuppressive effects of apoptotic cells. Nature 390, 350–351 (1997).
  Article CAS PubMed Google Scholar
• Fadok, V. A. et al. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890–898 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Bellingan, G. J., Caldwell, H., Howie, S. E., Dransfield, I. & Haslett, C. In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J. Immunol. 157, 2577–2585 (1996). References 121 and 122 are classical studies on the clearance of apoptotic neutrophils by macrophages, subsequent macrophage reprogramming and emigration to the draining lymph nodes.
  CAS PubMed Google Scholar
• Grimsley, C. & Ravichandran, K. S. Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals. Trends Cell. Biol. 13, 648–656 (2003).
  Article CAS PubMed Google Scholar
• Li, M. O., Sarkisian, M. R., Mehal, W. Z., Rakic, P. & Flavell, R. A. Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302, 1560–1563 (2003).
  Article CAS PubMed Google Scholar
• Greenberg, M. E. et al. Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J. Exp. Med. 203, 2613–2625 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Miyanishi, M. et al. Identification of Tim4 as a phosphatidylserine receptor. Nature 450, 435–439 (2007).
  Article CAS PubMed Google Scholar
• Mevorach, D., Mascarenhas, J. O., Gershov, D. & Elkon, K. B. Complement-dependent clearance of apoptotic cells by human macrophages. J. Exp. Med. 188, 2313–2320 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kennedy, A. D. & DeLeo, F. R. Neutrophil apoptosis and the resolution of infection. Immunol. Res. 43, 25–61 (2009).
  Article PubMed Google Scholar
• Freire-de-Lima, C. G. et al. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403, 199–203 (2000).
  Article CAS PubMed Google Scholar
• Medeiros, A. I., Serezani, C. H., Lee, S. P. & Peters-Golden, M. Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling. J. Exp. Med. 206, 61–68 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Scott, M. G. et al. An anti-infective peptide that selectively modulates the innate immune response. Nature Biotechnol. 25, 465–472 (2007).
  Article CAS Google Scholar
• Koenen, R. R. et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nature Med. 15, 97–103 (2009).
  Article CAS PubMed Google Scholar
• Koenen, R. R. & Weber, C. Therapeutic targeting of chemokine interactions in atherosclerosis. Nature Rev. Drug Discov. 9, 141–153 (2010).
  Article CAS Google Scholar
• Rossi, A. G. et al. Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nature Med. 12, 1056–1064 (2006).
  Article CAS PubMed Google Scholar
• Schwab, J. M., Chiang, N., Arita, M. & Serhan, C. N. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447, 869–874 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Spite, M. et al. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461, 1287–1291 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Mosser, D. M. & Edwards, J. P. Exploring the full spectrum of macrophage activation. Nature Rev. Immunol. 8, 958–969 (2008).
  Article CAS Google Scholar