Expansion of cortical and medullary sinuses restrains lymph node hypertrophy during prolonged inflammation

Journal of Immunology

Volumn 188, Issue 8, 2012, Pages 4065-4080

  Tan, Kar Wai ^a   Yeo, Kim Pin ^a   Wong, Fiona H S ^a   Lim, Hwee Ying ^a   Khoo, Kai Ling ^b   Abastado, Jean Pierre ^b   Angeli, Véronique ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN A; VASCULOTROPIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CORTICAL SINUS; DENDRITIC CELL; EXPERIMENTAL MODEL; FEMALE; FIBROBLAST; IMMUNOCOMPETENT CELL; INFLAMMATION; LYMPH NODE; LYMPH NODE HYPERTROPHY; LYMPHADENOPATHY; LYMPHANGIOGENESIS; LYMPHOCYTE; MEDULLARY SINUS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETICULUM CELL; STEADY STATE; STROMA CELL;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, NEUTRALIZING; CELL COMMUNICATION; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; FEMALE; HYPERTROPHY; INFLAMMATION; INJECTIONS, INTRAPERITONEAL; LYMPH NODES; LYMPHANGIOGENESIS; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84860320665     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101854     Document Type: Article

References (55)

1. Palframan, R. T., S. Jung, G. Cheng, W. Weninger, Y. Luo, M. Dorf, D. R. Littman, B. J. Rollins, H. Zweerink, A. Rot, and U. H. von Andrian. 2001. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 194: 1361-1373. (Pubitemid 33055053)
2. Cahill, R. N., H. Frost, and Z. Trnka. 1976. The effects of antigen on the migration of recirculating lymphocytes through single lymph nodes. J. Exp. Med. 143: 870-888.
3. Mackay, C. R., W. Marston, and L. Dudler. 1992. Altered patterns of T cell migration through lymph nodes and skin following antigen challenge. Eur. J. Immunol. 22: 2205-2210.
4. Hall, J. G., and B. Morris. 1965. The immediate effect of antigens on the cell output of a lymph node. Br. J. Exp. Pathol. 46: 450-454.
5. Young, A. J. 1999. The physiology of lymphocyte migration through the single lymph node in vivo. Semin. Immunol. 11: 73-83. (Pubitemid 29201813)
6. Shiow, L. R., D. B. Rosen, N. Brdicková, Y. Xu, J. An, L. L. Lanier, J. G. Cyster, and M. Matloubian. 2006. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440: 540-544.
7. Pham, T. H., T. Okada, M. Matloubian, C. G. Lo, and J. G. Cyster. 2008. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 28: 122-133.
8. Drayton, D. L., S. Liao, R. H. Mounzer, and N. H. Ruddle. 2006. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7: 344-353.
9. Mueller, S. N., and R. N. Germain. 2009. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat. Rev. Immunol. 9: 618-629.
10. Randolph, G. J., V. Angeli, and M. A. Swartz. 2005. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5: 617-628. (Pubitemid 41113193)
11. Webster, B., E. H. Ekland, L. M. Agle, S. Chyou, R. Ruggieri, and T. T. Lu. 2006. Regulation of lymph node vascular growth by dendritic cells. J. Exp. Med. 203: 1903-1913. (Pubitemid 44188465)
12. Soderberg, K. A., G. W. Payne, A. Sato, R. Medzhitov, S. S. Segal, and A. Iwasaki. 2005. Innate control of adaptive immunity via remodeling of lymph node feed arteriole. Proc. Natl. Acad. Sci. USA 102: 16315-16320. (Pubitemid 41688911)
13. Katakai, T., T. Hara, M. Sugai, H. Gonda, and A. Shimizu. 2004. Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J. Exp. Med. 200: 783-795. (Pubitemid 39299464)
14. Scandella, E., B. Bolinger, E. Lattmann, S. Miller, S. Favre, D. R. Littman, D. Finke, S. A. Luther, T. Junt, and B. Ludewig. 2008. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat. Immunol. 9: 667-675. (Pubitemid 351712637)
15. Angeli, V., F. Ginhoux, J. Llodrà, L. Quemeneur, P. S. Frenette, M. Skobe, R. Jessberger, M. Merad, and G. J. Randolph. 2006. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 24: 203-215. (Pubitemid 43214589)
16. Junt, T., E. Scandella, and B. Ludewig. 2008. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 8: 764-775.
17. Halin, C., M. L. Scimone, R. Bonasio, J. M. Gauguet, T. R. Mempel, E. Quackenbush, R. L. Proia, S. Mandala, and U. H. von Andrian. 2005. The S1P-analog FTY720 differentially modulates T-cell homing via HEV: T-cell-expressed S1P1 amplifies integrin activation in peripheral lymph nodes but not in Peyer patches. Blood 106: 1314-1322. (Pubitemid 41129595)
18. Lo, C. G., Y. Xu, R. L. Proia, and J. G. Cyster. 2005. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 201: 291-301. (Pubitemid 40189438)
19. Pytowski, B., J. Goldman, K. Persaud, Y. Wu, L. Witte, D. J. Hicklin, M. Skobe, K. C. Boardman, and M. A. Swartz. 2005. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J. Natl. Cancer Inst. 97: 14-21.
20. Nakao, S., S. Zandi, Y. Hata, S. Kawahara, R. Arita, A. Schering, D. Sun, M. I. Melhorn, Y. Ito, N. Lara-Castillo, et al. 2011. Blood vessel endothelial VEGFR-2 delays lymphangiogenesis: an endogenous trapping mechanism links lymph- and angiogenesis. Blood 117: 1081-1090.
21. Halin, C., N. E. Tobler, B. Vigl, L. F. Brown, and M. Detmar. 2007. VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 110: 3158-3167. (Pubitemid 350106307)
22. Robbiani, D. F., R. A. Finch, D. Jäger, W. A. Muller, A. C. Sartorelli, and G. J. Randolph. 2000. The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 103: 757-768.
23. Matloubian, M., C. G. Lo, G. Cinamon, M. J. Lesneski, Y. Xu, V. Brinkmann, M. L. Allende, R. L. Proia, and J. G. Cyster. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427: 355-360. (Pubitemid 38133663)
24. Mandala, S., R. Hajdu, J. Bergstrom, E. Quackenbush, J. Xie, J. Milligan, R. Thornton, G. J. Shei, D. Card, C. Keohane, et al. 2002. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296: 346-349. (Pubitemid 34303689)
25. Kataru, R. P., K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh. 2009. Critical role of CD11b+ macro-phages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood 113: 5650-5659.
26. Huggenberger, R., S. Ullmann, S. T. Proulx, B. Pytowski, K. Alitalo, and M. Detmar. 2010. Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J. Exp. Med. 207: 2255-2269.
27. Chyou, S., E. H. Ekland, A. C. Carpenter, T. C. Tzeng, S. Tian, M. Michaud, J. A. Madri, and T. T. Lu. 2008. Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J. Immunol. 181: 3887-3896.
28. Nicander, L., P. Nafstad, T. Landsverk, and R. H. Engebretsen. 1991. A study of modified lymphatics in the deep cortex of ruminant lymph nodes. J. Anat. 178: 203-212.
29. Sinha R. K., C. Park, I. Y. Hwang, M. D. Davis, and J. H. Kehrl. 2009. B lymphocytes exit lymph nodes through cortical lymphatic sinusoids by a mechanism independent of sphingosine-1-phosphate-mediated chemotaxis. Immunity 30: 434-446.
30. Grigorova, I. L., S. R. Schwab, T. G. Phan, T. H. Pham, T. Okada, and J. G. Cyster. 2009. Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat. Immunol. 10: 58-65.
31. Wei, S. H., H. Rosen, M. P. Matheu, M. G. Sanna, S. K. Wang, E. Jo, C. H. Wong, I. Parker, and M. D. Cahalan. 2005. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat. Immunol. 6: 1228-1235. (Pubitemid 43045634)
32. Söderström, N., and A. Stenström. 1969. Outflow paths of cells from the lymph node parenchyma to the efferent lymphatics - observations in thin section histology. Scand. J. Haematol. 6: 186-196.
33. Bélisle, C., and G. Sainte-Marie. 1981. Tridimensional study of the deep cortex of the rat lymph node. III. Morphology of the deep cortex units. Anat. Rec. 199: 213-226. (Pubitemid 11108950)
34. Grigorova, I. L., M. Panteleev, and J. G. Cyster. 2010. Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc. Natl. Acad. Sci. USA 107: 20447-20452.
35. Debes, G. F., C. N. Arnold, A. J. Young, S. Krautwald, M. Lipp, J. B. Hay, and E. C. Butcher. 2005. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat. Immunol. 6: 889-894. (Pubitemid 43090443)
36. Bromley, S. K., S. Y. Thomas, and A. D. Luster. 2005. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat. Immunol. 6: 895-901. (Pubitemid 43090444)
37. Cyster, J. G. 2005. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu. Rev. Immunol. 23: 127-159. (Pubitemid 40563167)
38. Braun, A., T. Worbs, G. L. Moschovakis, S. Halle, K. Hoffmann, J. Bölter, A. Münk, and R. Förster. 2011. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat. Immunol. 12: 879-887.
39. Phan, T. G., J. A. Green, E. E. Gray, Y. Xu, and J. G. Cyster. 2009. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 10: 786-793.
40. Gonzalez, S. F., V. Lukacs-Kornek, M. P. Kuligowski, L. A. Pitcher, S. E. Degn, Y. A. Kim, M. J. Cloninger, L. Martinez-Pomares, S. Gordon, S. J. Turley, and M.C. Carroll. 2010. Captureofinfluenza bymedullary dendritic cells via SIGN-R1 is essential forhumoralimmunityindraining lymphnodes. Nat. Immunol. 11: 427-434.
41. Boardman, K. C., and M. A. Swartz. 2003. Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 92: 801-808. (Pubitemid 36457646)
42. Goldman, J., K. A. Conley, A. Raehl, D. M. Bondy, B. Pytowski, M. A. Swartz, J. M. Rutkowski, D. B. Jaroch, and E. L. Ongstad. 2007. Regulation of lymphatic capillary regeneration by interstitial flow in skin. Am. J. Physiol. Heart Circ. Physiol. 292: H2176-H2183. (Pubitemid 47084597)
43. Tomei, A. A., S. Siegert, M. R. Britschgi, S. A. Luther, and M. A. Swartz. 2009. Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J. Immunol. 183: 4273-4283.
44. Angeli, V., J. Llodrá, J. X. Rong, K. Satoh, S. Ishii, T. Shimizu, E. A. Fisher, and G. J. Randolph. 2004. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity 21: 561-574. (Pubitemid 39370511)
45. Hay, J. B., and B. B. Hobbs. 1977. The flow of blood to lymph nodes and its relation to lymphocyte traffic and the immune response. J. Exp. Med. 145: 31-44. (Pubitemid 8010090)
46. von Andrian, U. H., and T. R. Mempel. 2003. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3: 867-878. (Pubitemid 37411716)
47. Mueller, S. N., K. A. Hosiawa-Meagher, B. T. Konieczny, B. M. Sullivan, M. F. Bachmann, R. M. Locksley, R. Ahmed, and M. Matloubian. 2007. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 317: 670-674. (Pubitemid 47229967)
48. Link, A., T. K. Vogt, S. Favre, M. R. Britschgi, H. Acha-Orbea, B. Hinz, J. G. Cyster, and S. A. Luther. 2007. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8: 1255-1265. (Pubitemid 350011765)
49. Luther, S. A., H. L. Tang, P. L. Hyman, A. G. Farr, and J. G. Cyster. 2000. Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc. Natl. Acad. Sci. USA 97: 12694-12699.
50. Ansel, K. M., V. N. Ngo, P. L. Hyman, S. A. Luther, R. Förster, J. D. Sedgwick, J. L. Browning, M. Lipp, and J. G. Cyster. 2000. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406: 309-314. (Pubitemid 30604409)
51. Gretz, J. E., C. C. Norbury, A. O. Anderson, A. E. Proudfoot, and S. Shaw. 2000. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J. Exp. Med. 192: 1425-1440.
52. Ferrara, N., H. P. Gerber, and J. LeCouter. 2003. The biology of VEGF and its receptors. Nat. Med. 9: 669-676. (Pubitemid 36749215)
53. Schwab, S. R., J. P. Pereira, M. Matloubian, Y. Xu, Y. Huang, and J. G. Cyster. 2005. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309: 1735-1739. (Pubitemid 41285945)
54. Pappu, R., S. R. Schwab, I. Cornelissen, J. P. Pereira, J. B. Regard, Y. Xu, E. Camerer, Y. W. Zheng, Y. Huang, J. G. Cyster, and S. R. Coughlin. 2007. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316: 295-298. (Pubitemid 46633109)
55. Sanna, M. G., S. K. Wang, P. J. Gonzalez-Cabrera, A. Don, D. Marsolais, M. P. Matheu, S. H. Wei, I. Parker, E. Jo, W. C. Cheng, et al. 2006. Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat. Chem. Biol. 2: 434-441. (Pubitemid 44114922)