DOI QR코드

DOI QR Code

Involvement of lymphoid inducer cells in the development of secondary and tertiary lymphoid structure

  • Evans, Isabel (MRC Centre for Immune Regulation, Institute for Biomedical Research, Birmingham Medical School) ;
  • Kim, Mi-Yeon (Department of Bioinformatics and Life Science, The College of Natural Science, Soongsil University)
  • Published : 2009.04.30

Abstract

During development lymphoid tissue inducer (LTi) cells are the first hematopoietic cells to enter the secondary lymphoid anlagen and induce lymphoid tissue neogenesis. LTi cells induce lymphoid tissue neogensis by expressing a wide range of proteins that are associated with lymphoid organogenesis. Among these proteins, membrane-bound lymphotoxin (LT) $\alpha1\beta2$ has been identified as a critical component to this process. LT$\alpha1\beta2$ interacts with the LT$\beta$-receptor on stromal cells and this interaction induces up-regulation of adhesion molecules and production of chemokines that are necessary for the attraction, retention and organization of other cell types. Constitutive expression of LT$\alpha1\beta2$ in adult LTi cells can result in the formation of a lymphoid-like structure called tertiary lymphoid tissue. In this review, we summarize the function of fetal and adult LTi cells and their involvement in secondary and tertiary lymphoid tissue development in murine models.

Keywords

References

  1. Mebius, R. E., Rennert, P. and Weissman, I. L. (1997) Developing lymph nodes collect CD4+CD3- LTbeta+cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7, 493-504 https://doi.org/10.1016/S1074-7613(00)80371-4
  2. Finke, D., Acha-Orbea, H., Mattis, A., Lipp, M. and Kraehenbuhl, J. (2002) CD4+CD3- cells induce Peyer's patch development: role of alpha4beta1 integrin activation by CXCR5. Immunity 17, 363-373 https://doi.org/10.1016/S1074-7613(02)00395-3
  3. Mebius, R. E. (2003) Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3, 292-303 https://doi.org/10.1038/nri1054
  4. Fukuyama, S., Hiroi, T., Yokota, Y., Rennert, P. D., Yanagita, M., Kinoshita, N., Terawaki, S., Shikina, T., Yamamoto, M., Kurono, Y. and Kiyono, H. (2002) Initiation of NALT organogenesis is independent of the IL-7R, LTbetaR, and NIK signaling pathways but requires the Id2 gene and CD3(-)CD4(+)CD45(+) cells. Immunity 17, 31-40 https://doi.org/10.1016/S1074-7613(02)00339-4
  5. Yoshida, H., Naito, A., Inoue, J., Satoh, M., Santee-Cooper, S. M., Ware, C. F., Togawa, A. and Nishikawa, S. (2002) Different cytokines induce surface lymphotoxin-alphabeta on IL-7 receptor-alpha cells that differentially engender lymph nodes and Peyer's patches. Immunity 17, 823-833 https://doi.org/10.1016/S1074-7613(02)00479-X
  6. Kim, D., Mebius, R. E., MacMicking, J. D., Jung, S., Cupedo, T., Castellanos, Y., Rho, J., Wong, B. R., Josien, R., Kim, N., Rennert, P. D. and Choi, Y. (2000) Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J. Exp. Med. 192, 1467-1478 https://doi.org/10.1084/jem.192.10.1467
  7. Cupedo, T., Jansen, W., Kraal, G. and Mebius, R. E. (2004) Induction of secondary and tertiary lymphoid structures in the skin. Immunity 21, 655-667 https://doi.org/10.1016/j.immuni.2004.09.006
  8. Sun, Z., Unutmaz, D., Zou, Y. R., Sunshine, M. J., Pierani, A., Brenner-Morton, S., Mebius, R. E. and Littman, D. R. (2000) Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 288, 2369-2373 https://doi.org/10.1126/science.288.5475.2369
  9. Drayton, D. L., Ying, X., Lee, J., Lesslauer, W. and Ruddle, N. H. (2003) Ectopic LT alpha beta directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J. Exp. Med. 197, 1153-1163 https://doi.org/10.1084/jem.20021761
  10. Wu, Q., Salomon, B., Chen, M., Wang, Y., Hoffman, L. M., Bluestone, J. A. and Fu, Y. X. (2001) Reversal of spontaneous autoimmune insulitis in nonobese diabetic mice by soluble lymphotoxin receptor. J. Exp. Med. 193, 1327-1332 https://doi.org/10.1084/jem.193.11.1327
  11. Adachi, S., Yoshida, H., Kataoka, H. and Nishikawa, S. (1997) Three distinctive steps in Peyer's patch formation of murine embryo. Int. Immunol. 9, 507-514 https://doi.org/10.1093/intimm/9.4.507
  12. Dejardin, E., Droin, N. M., Delhase, M., Haas, E., Cao, Y., Makris, C., Li, Z. W., Karin, M., Ware, C. F. and Green, D. R. (2002) The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 17, 525-535 https://doi.org/10.1016/S1074-7613(02)00423-5
  13. Honda, K., Nakano, H., Yoshida, H., Nishikawa, S., Rennert, P., Ikuta, K., Tamechika, M., Yamaguchi, K., Fukumoto, T., Chiba, T. and Nishikawa, S.I. (2001) Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J. Exp. Med. 193, 621-630 https://doi.org/10.1084/jem.193.5.621
  14. Luther, S. A., Ansel, K. M. and Cyster, J. G. (2003) Overlapping roles of CXCL13, interleukin 7 receptor alpha, and CCR7 ligands in lymph node development. J. Exp. Med. 197, 1191-1198 https://doi.org/10.1084/jem.20021294
  15. Kim, M. Y., Gaspal, F. M., Wiggett, H. E., McConnell, F. M., Gulbranson-Judge, A., Raykundalia, C., Walker, L. S., Goodall, M. D. and Lane, P. J. (2003) CD4(+)CD3(-) accessory cells costimulate primed CD4 T cells through OX40 and CD30 at sites where T cells collaborate with B cells. Immunity 18, 643-654 https://doi.org/10.1016/S1074-7613(03)00110-9
  16. Gaspal, F. M., Kim, M. Y., McConnell, F. M., Raykundalia, C., Bekiaris, V. and Lane, P. J. (2005) Mice deficient in OX40 and CD30 signals lack memory antibody responses because of deficient CD4 T cell memory. J. Immunol. 174, 3891-3896 https://doi.org/10.4049/jimmunol.174.7.3891
  17. Lane, P. J., Gaspal, F. M. and Kim, M. Y. (2005) Two sides of a cellular coin: CD4(+)CD3- cells regulate memory responses and lymph-node organization. Nat. Rev. Immunol. 5, 655-660 https://doi.org/10.1038/nri1665
  18. Kim, M. Y. (2008) Roles of embryonic and adult lymphoid tissue inducer cells in primary and secondary lymphoid tissues. Yonsei Med. J. 49, 352-356 https://doi.org/10.3349/ymj.2008.49.3.352
  19. Gaspal, F., Bekiaris, V., Kim, M. Y., Withers, D. R., Bobat, S., MacLennan, I. C., Anderson, G., Lane, P. J. and Cunningham, A. F. (2008) Critical synergy of CD30 and OX40 signals in CD4 T cell homeostasis and Th1 immunity to Salmonella. J. Immunol. 180, 2824-2829 https://doi.org/10.4049/jimmunol.180.5.2824
  20. Kim, M. Y., Anderson, G., White, A., Jenkinson, E., Arlt, W., Martensson, I. L., Erlandsson, L. and Lane, P. J. (2005) OX40 ligand and CD30 ligand are expressed on adult but not neonatal CD4+CD3- inducer cells: evidence that IL-7 signals regulate CD30 ligand but not OX40 ligand expression. J. Immunol. 174, 6686-6691 https://doi.org/10.4049/jimmunol.174.11.6686
  21. Kim, M. Y., McConnell, F. M., Gaspal, F. M., White, A., Glanville, S. H., Bekiaris, V., Walker, L. S., Caamano, J., Jenkinson, E., Anderson, G. and Lane, P. J. (2007) Function of CD4+CD3- cells in relation to B- and T-zone stroma in spleen. Blood 109, 1602-1610 https://doi.org/10.1182/blood-2006-04-018465
  22. Fu, Y. X., Molina, H., Matsumoto, M., Huang, G., Min, J. and Chaplin, D. D. (1997) Lymphotoxin-alpha (LTalpha) supports development of splenic follicular structure that is required for IgG responses. J. Exp. Med. 18, 2111-2120
  23. Hsu, S. and Dickinson, D. (2006) A new approach to managing oral manifestations of Sjogren's syndrome and skin manifestations of lupus. J. Biochem. Mol. Biol. 39, 229-239 https://doi.org/10.5483/BMBRep.2006.39.3.229
  24. Weyand, C. M., Kurtin, P. J. and Goronzy, J. J. (2001) Ectopic lymphoid organogenesis: a fast track for autoimmunity. Am. J. Pathol. 159, 787-793 https://doi.org/10.1016/S0002-9440(10)61751-8
  25. Luther, S. A., Lopez, T., Bai, W., Hanahan, D. and Cyster, J. G. (2000) BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 12, 471-481 https://doi.org/10.1016/S1074-7613(00)80199-5
  26. Takemura, S., Braun, A., Crowson, C., Kurtin, P. J., Cofield, R. H., O'Fallon, W. M., Goronzy, J. J. and Weyand, C. M. (2001) Lymphoid neogenesis in rheumatoid synovitis. J. Immunol. 167, 1072-1080 https://doi.org/10.4049/jimmunol.167.2.1072
  27. Salomonsson, S., Larsson, P., Tengner, P., Mellquist, E., Hjelmstrom, P. and Wahren-Herlenius, M. (2002) Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjogren's syndrome. Scand. J. Immunol. 55, 336-342
  28. Hjelmstrom, P., Fjell, J., Nakagawa, T., Sacca, R., Cuff, C. A. and Ruddle, N. H. (2000) Lymphoid tissue homing chemokines are expressed in chronic inflammation. Am. J. Pathol. 156, 1133-1138 https://doi.org/10.1016/S0002-9440(10)64981-4
  29. Picarella, D. E., Kratz, A., Li, C. B., Ruddle, N. H. and Flavell, R. A. (1992) Insulitis in transgenic mice expressing tumor necrosis factor beta (lymphotoxin) in the pancreas. Proc. Natl. Acad. Sci. U S A. 89, 10036-10040 https://doi.org/10.1073/pnas.89.21.10036
  30. Green, E. A. and Flavell, R. A. (1999) Tumor necrosis factor- alpha and the progression of diabetes in non-obese diabetic mice. Immunol. Rev. 169, 11-22 https://doi.org/10.1111/j.1600-065X.1999.tb01302.x
  31. Nishikawa, S. I., Hashi, H., Honda, K., Fraser, S. and Yoshida, H. (2000) Inflammation, a prototype for organogenesis of the lymphopoietic/hematopoietic system. Curr. Opin. Immunol. 12, 342-345 https://doi.org/10.1016/S0952-7915(00)00097-2
  32. Iwanaga, S. and Lee, B. L. (2005) Recent advances in the innate immunity of invertebrate animals. J. Biochem. Mol. Biol. 38, 128-150 https://doi.org/10.5483/BMBRep.2005.38.2.128
  33. Delovitch, T. L. and Singh, B. (1997) The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 7, 727-738 https://doi.org/10.1016/S1074-7613(00)80392-1
  34. McMillan, S. J. and Lloyd, C. M. (2004) Prolonged allergen challenge in mice leads to persistent airway remodelling. Clin. Exp. Allergy 34, 497-507 https://doi.org/10.1111/j.1365-2222.2004.01895.x

Cited by

  1. Potential of Cells and Cytokines/Chemokines to Regulate Tertiary Lymphoid Structures in Human Diseases vol.16, pp.5, 2016, https://doi.org/10.4110/in.2016.16.5.271
  2. High cell density cultivation of human leukemia T cells (Jurkat cells) in semipermeable polyelectrolyte microcapsules vol.15, pp.4, 2015, https://doi.org/10.1002/elsc.201400186
  3. Synthesis of artificial lymphoid tissue with immunological function vol.31, pp.11, 2010, https://doi.org/10.1016/j.it.2010.09.002
  4. Short-term inhibition of p53 combined with keratinocyte growth factor improves thymic epithelial cell recovery and enhances T-cell reconstitution after murine bone marrow transplantation vol.115, pp.5, 2010, https://doi.org/10.1182/blood-2009-05-223198