Role of Lymphatic Vessels in Tumor Immunity: Passive Conduits or Active Participants? (original) (raw)
Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell. 2010;140(4):460–76. ArticlePubMedCAS Google Scholar
Itano AA, McSorley SJ, Reinhardt RL, Ehst BD, Ingulli E, Rudensky AY, et al. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity. 2003;19(1):47–57. ArticlePubMedCAS Google Scholar
Pape KA, Catron DM, Itano AA, Jenkins MK. The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity. 2007;26(4):491–502. ArticlePubMedCAS Google Scholar
Wilson NS, El-Sukkari D, Belz GT, Smith CM, Steptoe RJ, Heath WR, et al. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood. 2003;102(6):2187–94. ArticlePubMedCAS Google Scholar
Randolph GJ, Angeli V, Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005;5(8):617–28. ArticlePubMedCAS Google Scholar
Förster R, Davalos-Misslitz A, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol. 2008;8(5):362–71. ArticlePubMedCAS Google Scholar
Reynoso ED, Lee JW, Turley SJ. Peripheral tolerance induction by lymph node stroma. Adv Exp Med Biol. 2009;633:113–27. ArticlePubMed Google Scholar
Cohen JN, Guidi CJ, Tewalt EF, Qiao H, Rouhani SJ, Ruddell A, et al. Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J Exp Med. 2010;207(4):681–8. ArticlePubMedCAS Google Scholar
Kraal G, Samsom JN, Mebius RE. The importance of regional lymph nodes for mucosal tolerance. Immunol Rev. 2006;213:119–30. ArticlePubMed Google Scholar
Ji RC. Lymphatic endothelial cells, inflammatory lymphangiogenesis, and prospective players. Curr Med Chem. 2007;14(22):2359–68. ArticlePubMedCAS Google Scholar
Patel SP, Dana R. Corneal lymphangiogenesis: implications in immunity. Semin Ophthalmol. 2009;24(3):135–8. ArticlePubMed Google Scholar
Kerjaschki D, Regele HM, Moosberger I, Nagy-Bojarski K, Watschinger B, Soleiman A, et al. Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J Am Soc Nephrol. 2004;15(3):603–12. ArticlePubMedCAS Google Scholar
Nasr IW, Reel M, Oberbarnscheidt MH, Mounzer RH, Baddoura FK, Ruddle NH, et al. Tertiary lymphoid tissues generate effector and memory T cells that lead to allograft rejection. Am J Transplant. 2007;7(5):1071–9. ArticlePubMedCAS Google Scholar
Angeli V, Ginhoux F, Llodra J, Quemeneur L, Frenette PS, Skobe M, et al. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity. 2006;24(2):203–15. ArticlePubMedCAS Google Scholar
Jell G, Kerjaschki D, Revell P, Al-Saffar N. Lymphangiogenesis in the bone-implant interface of orthopedic implants: importance and consequence. J Biomed Mater Res A. 2006;77A(1):119–27. ArticleCAS Google Scholar
Halin C, Tobler NE, Vigl B, Brown LF, Detmar M. VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood. 2007;110(9):3158–67. ArticlePubMedCAS Google Scholar
Achen MG, McColl BK, Stacker SA. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell. 2005;7(2):121–7. ArticlePubMedCAS Google Scholar
Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood. 2007;109(3):1010–7. ArticlePubMedCAS Google Scholar
Hirakawa S, Detmar M, Kerjaschki D, Nagamatsu S, Matsuo K, Tanemura A, et al. Nodal lymphangiogenesis and metastasis role of tumor-induced lymphatic vessel activation in extramammary paget’s disease. Am J Pathol. 2009;175(5):2235–48. ArticlePubMed Google Scholar
Skobe M, Hamberg LM, Hawighorst T, Schirner M, Wolf GL, Alitalo K, et al. Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol. 2001;159(3):893–903. PubMedCAS Google Scholar
Liersch R, Biermann C, Mesters RM, Berdel WE. Lymphangiogenesis in cancer: current perspectives. Recent Results Cancer Res. 2010;180:115–35. ArticlePubMedCAS Google Scholar
Ohtani O, Shao XJ, Saitoh M, Ohtani Y. Lymphatics of the rat mammary gland during virgin, pregnant, lactating and post-weaning periods. Ital J Anat Embryol. 1998;103(4 Suppl 1):335–42. PubMedCAS Google Scholar
Raharison F, Sautet J. The topography of the lymph vessels of mammary glands in female cats. Anat Histol Embryol. 2007;36(6):442–52. ArticlePubMedCAS Google Scholar
Heath TJ, Kerlin RL. Lymph drainage from the mammary gland in sheep. J Anat. 1986;144:61–70. PubMedCAS Google Scholar
Mylona E, Alexandrou P, Mpakali A, Giannopoulou I, Liapis G, Markaki S, et al. Clinicopathological and prognostic significance of vascular endothelial growth factors (VEGF)-C and -D and VEGF receptor 3 in invasive breast carcinoma. Eur J Surg Oncol. 2007;33(3):294–300. ArticlePubMedCAS Google Scholar
Pereira CT, Rahal SC, de Carvalho Balieiro JC, Ribeiro AA. Lymphatic drainage on healthy and neoplasic mammary glands in female dogs: can it really be altered? Anat Histol Embryol. 2003;32(5):282–90. ArticlePubMedCAS Google Scholar
Ran S, Volk L, Hall K, Flister MJ. Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology. 2010;17(4):229–51. ArticlePubMed Google Scholar
Maby-El Hajjami H, Petrova TV. Developmental and pathological lymphangiogenesis: from models to human disease. Histochem Cell Biol. 2008;130(6):1063–78. ArticlePubMedCAS Google Scholar
Wick N, Saharinen P, Saharinen J, Gurnhofer E, Steiner CW, Raab I, et al. Transcriptomal comparison of human dermal lymphatic endothelial cells ex vivo and in vitro. Physiol Genomics. 2007;28(2):179–92. PubMedCAS Google Scholar
Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, et al. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med. 2007;204(10):2349–62. ArticlePubMedCAS Google Scholar
Tammela T, Saaristo A, Holopainen T, Lyytikka J, Kotronen A, Pitkonen M, et al. Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat Med. 2007;13(12):1458–66. ArticlePubMedCAS Google Scholar
Schmid-Schonbein GW. The second valve system in lymphatics. Lymphat Res Biol. 2003;1(1):25–9. discussion 29-31. ArticlePubMed Google Scholar
Schmid-Schonbein GW. Microlymphatics and lymph flow. Physiol Rev. 1990;70(4):987–1028. PubMedCAS Google Scholar
Zawieja DC. Contractile physiology of lymphatics. Lymphat Res Biol. 2009;7(2):87–96. ArticlePubMed Google Scholar
Bazigou E, Xie S, Chen C, Weston A, Miura N, Sorokin L, et al. Integrin-alpha9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Dev Cell. 2009;17(2):175–86. ArticlePubMedCAS Google Scholar
Quick CM, Venugopal AM, Gashev AA, Zawieja DC, Stewart RH. Intrinsic pump-conduit behavior of lymphangions. Am J Physiol Regul Integr Comp Physiol. 2007;292(4):R1510–8. PubMedCAS Google Scholar
Wick N, Haluza D, Gurnhofer E, Raab I, Kasimir MT, Prinz M, et al. Lymphatic precollectors contain a novel, specialized subpopulation of podoplanin(low), CCL27-expressing lymphatic endothelial cells. Am J Pathol. 2008;173(4):1202–9. ArticlePubMedCAS Google Scholar
Baluk P, Yao LC, Feng J, Romano T, Jung SS, Schreiter JL, et al. TNF-alpha drives remodeling of blood vessels and lymphatics in sustained airway inflammation in mice. J Clin Invest. 2009;119(10):2954–64. PubMedCAS Google Scholar
Kim KE, Koh YJ, Jeon BH, Jang C, Han J, Kataru RP, et al. Role of CD11b+ macrophages in intraperitoneal lipopolysaccharide-induced aberrant lymphangiogenesis and lymphatic function in the diaphragm. Am J Pathol. 2009;175(4):1733–45. ArticlePubMedCAS Google Scholar
Miteva DO, Rutkowski JM, Dixon JB, Kilarski W, Shields JD, Swartz MA. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ Res. 2010;106(5):920–31. ArticlePubMedCAS Google Scholar
Tomei AA, Siegert S, Britschgi MR, Luther SA, Swartz MA. Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J Immunol. 2009;183(7):4273–83. ArticlePubMedCAS Google Scholar
Shields JD, Fleury ME, Yong C, Tomei AA, Randolph GJ, Swartz MA. Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell. 2007;11(6):526–38. ArticlePubMedCAS Google Scholar
Fleury ME, Boardman KC, Swartz MA. Autologous morphogen gradients by subtle interstitial flow and matrix interactions. Biophys J. 2006;91(1):113–21. ArticlePubMedCAS Google Scholar
Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, Mebius RE, et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity. 2009;30(2):264–76. ArticlePubMedCAS Google Scholar
Boardman KC, Swartz MA. Interstitial flow as a guide for lymphangiogenesis. Circ Res. 2003;92(7):801–8. ArticlePubMedCAS Google Scholar
Rutkowski JM, Boardman KC, Swartz MA. Characterization of lymphangiogenesis in a model of adult skin regeneration. Am J Physiol Heart Circ Physiol. 2006;291(3):H1402–10. ArticlePubMedCAS Google Scholar
Ng CP, Helm CL, Swartz MA. Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro. Microvasc Res. 2004;68(3):258–64. ArticlePubMed Google Scholar
Helm CL, Fleury ME, Zisch AH, Boschetti F, Swartz MA. Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism. Proc Natl Acad Sci USA. 2005;102(44):15779–84. ArticlePubMedCAS Google Scholar
Helm CL, Zisch A, Swartz MA. Engineered blood and lymphatic capillaries in 3-D VEGF-fibrin-collagen matrices with interstitial flow. Biotechnol Bioeng. 2007;96(1):167–76. ArticlePubMedCAS Google Scholar
Rutkowski JM, Moya M, Johannes J, Goldman J, Swartz MA. Secondary lymphedema in the mouse tail: Lymphatic hyperplasia, VEGF-C upregulation, and the protective role of MMP-9. Microvasc Res. 2006;72(3):161–71. ArticlePubMedCAS Google Scholar
Angeli V, Randolph GJ. Inflammation, lymphatic function, and dendritic cell migration. Lymphat Res Biol. 2006;4(4):217–28. ArticlePubMedCAS Google Scholar
Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 2009;21(2):154–65. ArticlePubMedCAS Google Scholar
Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol. 2007;8(6):464–78. ArticlePubMedCAS Google Scholar
Pytowski B, Goldman J, Persaud K, Wu Y, Witte L, Hicklin DJ, et al. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst. 2005;97(1):14–21. ArticlePubMedCAS Google Scholar
Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature. 2005;438(7070):946–53. ArticlePubMedCAS Google Scholar
Bajenoff M, Germain RN. B-cell follicle development remodels the conduit system and allows soluble antigen delivery to follicular dendritic cells. Blood. 2009;114(24):4989–97. ArticlePubMedCAS Google Scholar
Sixt M, Kanazawa N, Selg M, Samson T, Roos G, Reinhardt DP, et al. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity. 2005;22(1):19–29. ArticlePubMedCAS Google Scholar
Schumann K, Lammermann T, Bruckner M, Legler DF, Polleux J, Spatz JP, et al. Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity. 2010;32(5):703–13. ArticlePubMedCAS Google Scholar
Stachowiak AN, Wang Y, Huang YC, Irvine DJ. Homeostatic lymphoid chemokines synergize with adhesion ligands to trigger T and B lymphocyte chemokinesis. J Immunol. 2006;177(4):2340–8. PubMedCAS Google Scholar
Angel CE, Chen CJ, Horlacher OC, Winkler S, John T, Browning J, et al. Distinctive localization of antigen-presenting cells in human lymph nodes. Blood. 2009;113(6):1257–67. ArticlePubMedCAS Google Scholar
Mebius RE, Streeter PR, Breve J, Duijvestijn AM, Kraal G. The influence of afferent lymphatic vessel interruption on vascular addressin expression. J Cell Biol. 1991;115(1):85–95. ArticlePubMedCAS Google Scholar
Drayton DL, Liao S, Mounzer RH, Ruddle NH. Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol. 2006;7(4):344–53. ArticlePubMedCAS Google Scholar
Mori S, Nakano H, Aritomi K, Wang CR, Gunn MD, Kakiuchi T. Mice lacking expression of the chemokines CCL21-ser and CCL19 (plt mice) demonstrate delayed but enhanced T cell immune responses. J Exp Med. 2001;193(2):207–18. ArticlePubMedCAS Google Scholar
Luther SA, Bidgol A, Hargreaves DC, Schmidt A, Xu Y, Paniyadi J, et al. Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J Immunol. 2002;169(1):424–33. PubMedCAS Google Scholar
Ohl L, Henning G, Krautwald S, Lipp M, Hardtke S, Bernhardt G, et al. Cooperating mechanisms of CXCR5 and CCR7 in development and organization of secondary lymphoid organs. J Exp Med. 2003;197(9):1199–204. ArticlePubMedCAS Google Scholar
Mueller SN, Ahmed R. Lymphoid stroma in the initiation and control of immune responses. Immunol Rev. 2008;224:284–94. ArticlePubMedCAS Google Scholar
Pabst O, Wahl B, Bernhardt G, Hammerschmidt SI. Mesenteric lymph node stroma cells in the generation of intestinal immune responses. J Mol Med. 2009;87(10):945–51. ArticlePubMed Google Scholar
Hammerschmidt SI, Ahrendt M, Bode U, Wahl B, Kremmer E, Forster R, et al. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J Exp Med. 2008;205(11):2483–90. ArticlePubMedCAS Google Scholar
Davalos-Misslitz AC, Rieckenberg J, Willenzon S, Worbs T, Kremmer E, Bernhardt G, et al. Generalized multi-organ autoimmunity in CCR7-deficient mice. Eur J Immunol. 2007;37(3):613–22. ArticlePubMedCAS Google Scholar
Achtman AH, Hopken UE, Bernert C, Lipp M. CCR7-deficient mice develop atypically persistent germinal centers in response to thymus-independent type 2 antigens. J Leukoc Biol. 2009;85(3):409–17. ArticlePubMedCAS Google Scholar
Henning G, Ohl L, Junt T, Reiterer P, Brinkmann V, Nakano H, et al. CC chemokine receptor 7-dependent and -independent pathways for lymphocyte homing: modulation by FTY720. J Exp Med. 2001;194(12):1875–81. ArticlePubMedCAS Google Scholar
Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A, Williams LT, et al. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med. 1999;189(3):451–60. ArticlePubMedCAS Google Scholar
Nakano H, Mori S, Yonekawa H, Nariuchi H, Matsuzawa A, Kakiuchi T. A novel mutant gene involved in T-lymphocyte-specific homing into peripheral lymphoid organs on mouse chromosome 4. Blood. 1998;91(8):2886–95. PubMedCAS Google Scholar
Stein JV, Rot A, Luo Y, Narasimhaswamy M, Nakano H, Gunn MD, et al. The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function-associated antigen 1-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J Exp Med. 2000;191(1):61–76. ArticlePubMedCAS Google Scholar
Warnock RA, Campbell JJ, Dorf ME, Matsuzawa A, McEvoy LM, Butcher EC. The role of chemokines in the microenvironmental control of T versus B cell arrest in Peyer’s patch high endothelial venules. J Exp Med. 2000;191(1):77–88. ArticlePubMedCAS Google Scholar
Hofmann J, Greter M, Du Pasquier L, Becher B. B-cells need a proper house, whereas T-cells are happy in a cave: the dependence of lymphocytes on secondary lymphoid tissues during evolution. Trends Immunol. 2010;31(4):144–53. ArticlePubMedCAS Google Scholar
Ochando JC, Yopp AC, Yang Y, Garin A, Li Y, Boros P, et al. Lymph node occupancy is required for the peripheral development of alloantigen-specific Foxp3+ regulatory T cells. J Immunol. 2005;174(11):6993–7005. PubMedCAS Google Scholar
Menning A, Hopken UE, Siegmund K, Lipp M, Hamann A, Huehn J. Distinctive role of CCR7 in migration and functional activity of naive- and effector/memory-like Treg subsets. Eur J Immunol. 2007;37(6):1575–83. ArticlePubMedCAS Google Scholar
Schneider MA, Meingassner JG, Lipp M, Moore HD, Rot A. CCR7 is required for the in vivo function of CD4+ CD25+ regulatory T cells. J Exp Med. 2007;204(4):735–45. ArticlePubMedCAS Google Scholar
Zhang N, Schroppel B, Lal G, Jakubzick C, Mao X, Chen D, et al. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity. 2009;30(3):458–69. ArticlePubMedCAS Google Scholar
Ueha S, Yoneyama H, Hontsu S, Kurachi M, Kitabatake M, Abe J, et al. CCR7 mediates the migration of Foxp3+ regulatory T cells to the paracortical areas of peripheral lymph nodes through high endothelial venules. J Leukoc Biol. 2007;82(5):1230–8. ArticlePubMedCAS Google Scholar
Eller K, Weber T, Pruenster M, Wolf AM, Mayer G, Rosenkranz AR, et al. CCR7 deficiency exacerbates injury in acute nephritis due to aberrant localization of regulatory T cells. J Am Soc Nephrol. 2010;21(1):42–52. ArticlePubMedCAS Google Scholar
Jin Y, Chauhan SK, Saban DR, Dana R. Role of CCR7 in facilitating direct allosensitization and regulatory T-cell function in high-risk corneal transplantation. Invest Ophthalmol Vis Sci. 2010;51(2):816–21. ArticlePubMed Google Scholar
Ahrendt M, Hammerschmidt SI, Pabst O, Pabst R, Bode U. Stromal cells confer lymph node-specific properties by shaping a unique microenvironment influencing local immune responses. J Immunol. 2008;181(3):1898–907. PubMedCAS Google Scholar
Wolvers DA, Coenen-de Roo CJ, Mebius RE, van der Cammen MJ, Tirion F, Miltenburg AM, et al. Intranasally induced immunological tolerance is determined by characteristics of the draining lymph nodes: studies with OVA and human cartilage gp-39. J Immunol. 1999;162(4):1994–8. PubMedCAS Google Scholar
Lee JW, Epardaud M, Sun J, Becker JE, Cheng AC, Yonekura AR, et al. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat Immunol. 2007;8(2):181–90. ArticlePubMedCAS Google Scholar
Kyewski B, Klein L. A central role for central tolerance. Annu Rev Immunol. 2006;24:571–606. ArticlePubMedCAS Google Scholar
Collier AY, Lee JW, Turley SJ. Self-encounters of the third kind: lymph node stroma promotes tolerance to peripheral tissue antigens. Mucosal Immunol. 2008;1(4):248–51. ArticlePubMedCAS Google Scholar
Fletcher AL, Lukacs-Kornek V, Reynoso ED, Pinner SE, Bellemare-Pelletier A, Curry MS, et al. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J Exp Med. 2010;207(4):689–97. ArticlePubMedCAS Google Scholar
Turley SJ, Lee JW, Dutton-Swain N, Mathis D, Benoist C. Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc Natl Acad Sci USA. 2005;102(49):17729–33. ArticlePubMedCAS Google Scholar
Shrestha B, Hashiguchi T, Ito T, Miura N, Takenouchi K, Oyama Y, et al. B cell-derived vascular endothelial growth factor a promotes lymphangiogenesis and high endothelial venule expansion in lymph nodes. J Immunol. 2010;184(9):4819–26. ArticlePubMedCAS Google Scholar
Liao S, Ruddle NH. Synchrony of high endothelial venules and lymphatic vessels revealed by immunization. J Immunol. 2006;177(5):3369–79. PubMedCAS Google Scholar
Vondenhoff MF, Greuter M, Goverse G, Elewaut D, Dewint P, Ware CF, et al. LTbetaR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J Immunol. 2009;182(9):5439–45. ArticlePubMedCAS Google Scholar
Ruddle NH, Akirav EM. Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response. J Immunol. 2009;183(4):2205–12. ArticlePubMedCAS Google Scholar
Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol. 2006;6(3):205–17. ArticlePubMedCAS Google Scholar
Martin AP, Coronel EC, Sano G, Chen SC, Vassileva G, Canasto-Chibuque C, et al. A novel model for lymphocytic infiltration of the thyroid gland generated by transgenic expression of the CC chemokine CCL21. J Immunol. 2004;173(8):4791–8. PubMedCAS Google Scholar
Heller F, Lindenmeyer MT, Cohen CD, Brandt U, Draganovici D, Fischereder M, et al. The contribution of B cells to renal interstitial inflammation. Am J Pathol. 2007;170(2):457–68. ArticlePubMedCAS Google Scholar
Fan L, Reilly CR, Luo Y, Dorf ME, Lo D. Cutting edge: ectopic expression of the chemokine TCA4/SLC is sufficient to trigger lymphoid neogenesis. J Immunol. 2000;164(8):3955–9. PubMedCAS Google Scholar
Chen SC, Vassileva G, Kinsley D, Holzmann S, Manfra D, Wiekowski MT, et al. Ectopic expression of the murine chemokines CCL21a and CCL21b induces the formation of lymph node-like structures in pancreas, but not skin, of transgenic mice. J Immunol. 2002;168(3):1001–8. PubMedCAS Google Scholar
Thaunat O, Kerjaschki D, Nicoletti A. Is defective lymphatic drainage a trigger for lymphoid neogenesis? Trends Immunol. 2006;27(10):441–5. ArticlePubMedCAS Google Scholar
Flister MJ, Wilber A, Hall KL, Iwata C, Miyazono K, Nisato RE, et al. Inflammation induces lymphangiogenesis through up-regulation of VEGFR-3 mediated by NF-kappaB and Prox1. Blood. 2009;115(2):418–29. ArticlePubMedCAS Google Scholar
Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, Hicklin DJ, et al. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest. 2005;115(2):247–57. PubMedCAS Google Scholar
Watari K, Nakao S, Fotovati A, Basaki Y, Hosoi F, Bereczky B, et al. Role of macrophages in inflammatory lymphangiogenesis: enhanced production of vascular endothelial growth factor C and D through NF-kappaB activation. Biochem Biophys Res Commun. 2008;377(3):826–31. ArticlePubMedCAS Google Scholar
Kajiya K, Detmar M. An important role of lymphatic vessels in the control of UVB-induced edema formation and inflammation. J Invest Dermatol. 2006;126(4):919–21. ArticlePubMedCAS Google Scholar
Kunstfeld R, Hirakawa S, Hong YK, Schacht V, Lange-Asschenfeldt B, Velasco P, et al. Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-A transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood. 2004;104(4):1048–57. ArticlePubMedCAS Google Scholar
Leong TT, Fearon U, Veale DJ. Angiogenesis in psoriasis and psoriatic arthritis: clues to disease pathogenesis. Curr Rheumatol Rep. 2005;7(4):325–9. ArticlePubMedCAS Google Scholar
Danese S, Sans M, de la Motte C, Graziani C, West G, Phillips MH, et al. Angiogenesis as a novel component of inflammatory bowel disease pathogenesis. Gastroenterology. 2006;130(7):2060–73. ArticlePubMedCAS Google Scholar
Schonthaler HB, Huggenberger R, Wculek SK, Detmar M, Wagner EF. Systemic anti-VEGF treatment strongly reduces skin inflammation in a mouse model of psoriasis. Proc Natl Acad Sci USA. 2009;106(50):21264–9. ArticlePubMedCAS Google Scholar
Yao LC, Baluk P, Feng J, McDonald DM. Steroid-resistant lymphatic remodeling in chronically inflamed mouse airways. Am J Pathol. 2010;176(3):1525–41. ArticlePubMedCAS Google Scholar
Stuht S, Gwinner W, Franz I, Schwarz A, Jonigk D, Kreipe H, et al. Lymphatic neoangiogenesis in human renal allografts: results from sequential protocol biopsies. Am J Transplant. 2007;7(2):377–84. ArticlePubMedCAS Google Scholar
Ling S, Qi C, Li W, Xu J, Kuang W. Crucial role of corneal lymphangiogenesis for allograft rejection in alkali-burned cornea bed. Clin Experiment Ophthalmol. 2009;37(9):874–83. ArticlePubMed Google Scholar
Ling S, Qi C, Li W, Xu J, Kuang W. The expression of vascular endothelial growth factor C in transplanted corneas. Curr Eye Res. 2009;34(7):553–61. ArticlePubMedCAS Google Scholar
Chung ES, Saban DR, Chauhan SK, Dana R. Regulation of blood vessel versus lymphatic vessel growth in the cornea. Invest Ophthalmol Vis Sci. 2009;50(4):1613–8. ArticlePubMed Google Scholar
Nathanson SD. Insights into the mechanisms of lymph node metastasis. Cancer. 2003;98(2):413–23. ArticlePubMed Google Scholar
Amioka T, Kitadai Y, Tanaka S, Haruma K, Yoshihara M, Yasui W, et al. Vascular endothelial growth factor-C expression predicts lymph node metastasis of human gastric carcinomas invading the submucosa. Eur J Cancer. 2002;38(10):1413–9. ArticlePubMedCAS Google Scholar
Arinaga M, Noguchi T, Takeno S, Chujo M, Miura T, Uchida Y. Clinical significance of vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 in patients with nonsmall cell lung carcinoma. Cancer. 2003;97(2):457–64. ArticlePubMedCAS Google Scholar
Clarijs R, Schalkwijk L, Ruiter DJ, de Waal RM. Lack of lymphangiogenesis despite coexpression of VEGF-C and its receptor Flt-4 in uveal melanoma. Invest Ophthalmol Vis Sci. 2001;42(7):1422–8. PubMedCAS Google Scholar
Leu AJ, Berk DA, Lymboussaki A, Alitalo K, Jain RK. Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res. 2000;60(16):4324–7. PubMedCAS Google Scholar
Padera TP, Kadambi A, di Tomaso E, Carreira CM, Brown EB, Boucher Y, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science. 2002;296(5574):1883–6. ArticlePubMedCAS Google Scholar
Issa A, Le TX, Shoushtari AN, Shields JD, Swartz MA. Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumor cell-lymphatic cross-talk promote invasive phenotype. Cancer Res. 2009;69(1):349–57. ArticlePubMedCAS Google Scholar
Sipos B, Kojima M, Tiemann K, Klapper W, Kruse ML, Kalthoff H, et al. Lymphatic spread of ductal pancreatic adenocarcinoma is independent of lymphangiogenesis. J Pathol. 2005;207(3):301–12. ArticlePubMedCAS Google Scholar
Wong SY, Haack H, Crowley D, Barry M, Bronson RT, Hynes RO. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res. 2005;65(21):9789–98. ArticlePubMedCAS Google Scholar
Kataru RP, Jung K, Jang C, Yang H, Schwendener RA, Baik JE, et al. Critical role of CD11b+ macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood. 2009;113(22):5650–9. ArticlePubMedCAS Google Scholar
Jennbacken K, Vallbo C, Wang WZ, et al. Expression of vascular endothelial growth factor C (VEGF‐C) and VEGF receptor‐3 in human prostate cancer is associated with regional lymph node metastasis. Prostate. 2005;65(2):110–116. Google Scholar
Jenny B, Harrison JA, Baetens D, et al. Expression and localization of VEGF‐C and VEGFR‐3 in glioblastomas and haemangioblastomas. J Pathol. 2006;209(1):34–43. Google Scholar
Li J, Hong M, Pan T. Clinical significance of VEGF‐C and VEGFR‐3 expression in non‐small cell lung cancer. J Huazhong Univ Sci Technolog Med Sci. 2006;26(5):587–90. Google Scholar
Filho AL, Martins A, Costa SMA, et al. VEGFR‐3 expression in breast cancer tissue is not restricted to lymphatic vessels. Pathology Research and Practice. 2005;201(2):93–99. Google Scholar
Su JL, Yang PC, Shih JY, et al. The VEGF‐C/Flt‐4 axis promotes invasion and metastasis of cancer cells. Cancer Cell. 2006;9(3):209–23. Google Scholar
Shields JD, Kourtis IC, Tomei AA, et al. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science. 2010;328(5979):749–52. ArticlePubMedCAS Google Scholar
Harrell MI, Iritani BM, Ruddell A. Tumor‐induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol. 2007;170(2):774–86. Google Scholar
Ruddell RG, Knight B, Tirnitz‐Parker JE, et al. Lymphotoxin‐beta receptor signaling regulates hepatic stellate cell function and wound healing in a murine model of chronic liver injury. Hepatology. 2009;49(1):227–39. Google Scholar
Ruddell A, Harrell MI, Minoshima S, et al. Dynamic contrast‐enhanced magnetic resonance imaging of tumor‐induced lymph flow. Neoplasia. 2008;10(7):706–U4. Google Scholar
Herber DL, Cao W, Nefedova Y, et al. Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med. 2010;16(8):880–6. ArticlePubMedCAS Google Scholar