Structure and function of the immune semaphorin CD100/SEMA4D

Critical Reviews in Immunology

Volumn 23, Issue 1-2, 2003, Pages 65-81

  Elhabazi, Abdellah ^a   Marie Cardine, Anne ^a   Chabbert de Ponnat, Isabelle ^a   Bensussan, Armand ^a   Boumsell, Laurence ^a  

^a FACULTÉ DE MÉDECINE   (France)

Author keywords

B cells; CD100; CD72; Immune response; Monocytes; Plexin B1; Semaphorin; T cells

Indexed keywords

CD100 ANTIGEN; CD45 ANTIGEN; CD72 ANTIGEN; CHEMOKINE; PLEXIN B1; PROTEIN SEMA4D; PROTEIN SERINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RECEPTOR; SEMAPHORIN; T LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; B LYMPHOCYTE; CELL MIGRATION; CELL SURVIVAL; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; MEMBRANE BINDING; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SOLUBILITY; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD; B-LYMPHOCYTES; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MONOCYTES; SEMAPHORINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0037777666     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevImmunol.v23.i12.40     Document Type: Review

References (65)

1. Tessier-Lavigne, M., and Goodman, C.S., The molecular biology of axon guidance. Science 1996; 27:1123-1133.
2. Kolodkin, A.L., Mathes, D.J., and Goodman, C.S., The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993; 75:1389-1399.
3. Miao, H.Q., Soker, S., Feiner, L., Alonso, J.L., Raper, J.A., and Klagsbrun M., Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J Cell Biol 1999; 146:233-242.
4. Behar, O., Golden, J.A., Mashimo, H., Schoen, F.J., and Fishman, M.C., Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 1996; 383:525-528.
5. Christensen, C.R., Klingelhofer, J., Tarabykina, S., Hulgaard, E.F., Kramerov, D., and Lukanidin, E., Transcription of a novel mouse semaphorin gene, M-semaH, correlates with the metastatic ability of mouse tumor cell lines. Cancer Res 1998; 58:1238-1244.
6. Semaphorin Nomenclature Committee, Unified nomenclature for the semaphorins/collapsins. Cell 1999; 97:551-552.
7. Bougeret, C., Mansur, I.G., Dastot, H., Schmid, M., Mahouy, G., Bensussan, A., and Boumsell, L., Increased surface expression of a newly identified 150 kDa dimer early after human T lymphocyte activation. J Immunol 1992; 148:318-323.
8. Hérold, C., Bismuth, G., Bensussan, A. and Boumsell, L., Activation signals are delivered through two distinct epitopes of CD100, a unique 150 kDa human lymphocyte surface structure previously defined by BB18 mAb. Int Immunol 1995; 7:1-8.
9. Hall, K.T., Boumsell, L., Schultze, J.L., Boussiotis, V.A., Dorfman, D.M., Cardoso, A.A., Bensussan, A., Nadler, L.M., and Freeman, G., CD100, a novel human leucocyte semaphorin involved in germinal center development. Proc Natl Acad Sci U S A 1995; 9:11780-11785.
10. Elhabazi, A., Delaire, S., Bensussan, A., Boumsell, L., and Bismuth, G., Biological activity of soluble CD100. I. The extracellular region of CD100 is released from the surface of T lymphocytes by regulated proteolysis. J Immunol 2001; 166:4341-4347.
11. Furuyama, T., Inagaki, S., Kosugi, A., Noda, S., Saitoh, S., Ogata, M., Iwahashi, Y., Miyazaki, N., Hamaoka, T., and Tohyama, M., Identification of a novel transmembrane semaphorin expressed on lymphocytes. J Biol Chem 1996; 271:33376-33381.
12. Hérold, C., Elhabazi, A., Bismuth, G., Bensussan, A., and Boumsell, L., CD100 is associated with CD45 at the surface of human T lymphocytes. Role in T cell homotypic adhesion. J Immunol 1996; 157:5262-5268.
13. Watanabe, C., Kumanogoh, A., Shi, W., Suzuki, K., Yamada, S., Okabe, M., Yoshida, K., and Kikutani, H., Enhanced immune responses in transgenic mice expressing a truncated form of the lymphocyte semaphorin CD100. J Immunol 2001; 167:4321-4328.
14. Adams, R.H., Lohrum, M., Klostermann, A., Betz, H., and Puschel, A.W., The chemorepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing. EMBO J 1997; 16:6077-6086.
15. Koppel, A.M., and Raper, J.A., Collapsin-1 covalently dimerizes, and dimerization is necessary for collapsing activity. J Biol Chem 1998; 273:15708-15713.
16. Hérold, C., Elhabazi, A., Bensussan, A., and Boumsell, L., "Molécules "CD" et transmission des signaux d'activation aux lymphocytes T". Med Sci 1995; 11:669-680 (in French).
17. Wagner, N., Engel, P., and Tedder, T.F., Regulation of the tyrosine kinase-dependent adhesion pathway in human lymphocytes through CD45. J Immunol 1993; 150:4887-4899.
18. Chan, A.C., Desai, D.M., and Weiss, A., The role of protein tyrosine kinases and protein tyrosine phosphatases in T cell antigen receptor signal transduction. Annu Rev Immunol 1994; 12:555-592.
19. Schraven, B., Samstag, Y., Altevogt, P., and Meuer, S.C., Association of CD2 and CD45 on human T, lymphocytes. Nature 1990; 345:71-74.
20. Billard, C., Delaire, S., Raffoux, E., Bensussan, A., and Boumsell, L., Switch in the protein tyrosine phosphatase associated with human CD100 semaphorin at terminal B-cell differentiation stage. Blood 2000; 95:965-972.
21. Elhabazi, A., Lang, V., Hérold, C., Freeman, G.J., Bensussan, A, Boumsell L., and Bismuth, G., The human semaphorin-like leukocyte cell surface molecule CD100 associates with a serine kinase activity. J Biol Chem 1997; 272:23515-23521.
22. Elhabazi, A., Hérold, C., Bensussan, A., Boumsell, L., and Bismuth, G., Human CD100 associates with a serine kinase activity differently recruited through its epitopes NL-056 (BB18) and NL-057 (BD16). In: Kishimoto, T., Kikutani, H., von dem Borne, A. E. G. Kr., Goyert, S. M., Mason, D. Y., Miyasaka, M., Moretta, L., Okumura, K., Shaw, S., Springer, T. A., Sagamura, K., and Zola, H., editors. Leucocyte Typing VI. New York, London: Garland Publishing, 1997:537-539.
23. Stover, D.R., and Walsh, K.A., Protein-tyrosine phosphatase activity of CD45 is activated by sequential phosphorylation by two kinases. Mol Cell Biol 1994;14:5523-5532.
24. Delaire, S., Billard, C., Tordjman, R., Chedotal, A., Elhabazi, A., Bensussan, A., and Boumsell, L., Biological activity of soluble CD100. II. Soluble CD100, similarly to H-SemaIII, inhibits immune cell migration. J Immunol 2001; 166:4348-4354.
25. Kumanogoh, A., Watanabe, C., Lee, I., Wang, X., Shi, W., Araki, H., Hirata, H., Iwahori, K., Uchida, J., Yasui, T., Matsumoto, M., Yoshida, K., Yakura, H., Pan, C., Parnes, J.R., and Kikutani, H., Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity 2000; 13:621-631.
26. Wang, X., Kumanogoh, A., Watanabe, C., Shi, W., Yoshida, K., and Kikutani, H., Functional soluble CD100/Sema4D released from activated lymphocytes: possible role in normal and pathologic immune responses. Blood 2000; 97:3498-3504.
27. Shi, W., Kumanogoh, A., Watanabe, C., Uchida, J., Wang, X., Yasui, T., Yukawa, K., Ikawa, M., Okabe, M., Parnes, J.R., Yoshida, K., and Kikutani, H., The class IV semaphorin CD100 plays non-redundant roles in the immune system: defective B and T cell activation in CD100-deficient mice. Immunity 2000; 13:633-642.
28. Kumanogoh, A., Suzuki, K., Ch'ng, E., Watanabe, C., Marukawa, S., Takegahara, N., Ishida, I., Sato, T., Habu, S., Yoshida, K., Shi, W., and Kikutani H., Requirement for the lymphocyte semaphorin, CD100, in the induction of antigen-specific T cells and the maturation of dendritic cells. J Immunol 2002; 169:1175-1181.
29. Kumanogoh, A., and Kikutani, H., The CD100-CD72 interaction: a novel mechanism of immune regulation. Trends Immunol 2001; 22:670-676.
30. Tamagnone, L., Artigiani. S., Chen, H., He, Z., Ming, G.I., Song, H., Chedotal, A., Winberg, M.L., Goodman, C.S., Poo, M., Tessier-Lavigne, M., and Comoglio, P.M., Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999; 99:71-80.
31. Tamagnone, L., and Comoglio, P.M., Signaling by semaphorin receptors: cell guidance and beyond. Trends Cell Biol 2000; 10:377-383.
32. Maestrini, E., Tamagnone, L., Longati, P., Cremona, O., Gulisano, M., Bione, S., Tamanini, F., Neel, B.G., Toniolo, D., and Comoglio, P.M., A family of transmembrane proteins with homology to the MET-hepatocyte growth factor receptor. Proc Natl Acad Sci U S A 1996; 93:674-678.
33. Granziero, L., Circosta, P., Scielzo, C., Frisaldi, E., Stella, S., Geuna, M., Giordano, S., Ghia, P., and Caligaris-Cappio, F., CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes. Blood 2002 (pre-published online October 24, 2002; DOI 10.1182/blood-2002-05-1339).
34. Giordano, S., Corso, S., Conrotto, P., Artigiani, S., Gilestro, G., Barberis, D., Tamagnone, L., and Comoglio, P.M., The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat Cell Biol 2002; 4:720-724.
35. Swiercz, J.M., Kuner, R., Behrens, J., and Offermanns, S., Plexin-B1 directly interacts with PDZ-RhoGEF/ LARG to regulate RhoA and growth cone morphology. Neuron 2002; 35:51-63.
36. Bismuth, G., and Boumsell, L., Controlling the immune system through semaphorins. Sci STKE 2002; 128:RE4.
37. Delaire, S., Elhabazi, A., Bensussan, A., and Boumsell, L., CD100 is a leukocyte semaphorin. Cell Mol Life Sci 1998; 54:1265-1276.
38. Naramura, M., Jang, I.K., Kole, H., Huang, F., Haines, D., and Gu, H., c-Cbl and Cbl-b regulate T cell responsiveness by promoting ligand-induced TCR down-modulation. Nat Immunol 2002; 3:1192-1199.
39. Carriere, D., Arcier, J.M., Derocq, J.M., Fontaine, C., and Richer, G., Antigenic modulation induced by four monoclonal antibodies adsorbed on gold particles (specificity anti-CD4, anti-CD5, anti-CD7, and anti-150-kDa antigen): relationship between modulation and cytotoxic activity of immunotoxins. Exp Cell Res 1989; 182:114-128.
40. Tonks, N.K., and Neel, B.G., From form to function: signaling by protein tyrosine phosphatases. Cell 1996; 87:365-368.
41. Liu, B.P., and Strittmatter, S.M., Semaphorin-mediated axonal guidance via Rho-related G proteins. Curr Opin Cell Biol 2001; 13:619-626.
42. Nakamura, F., Kalb, R.G., and Strittmatter, S.M., Molecular basis of semaphorin-mediated axon guidance. J Neurobiol 2000; 44:219-229.
43. Takahashi, T., Fournier, A., Nakamura, F., Wang, L.H., Murakami, Y., Kalb, R.G., Fujisawa, H., and Strittmatter, S.M., Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 1999; 99:59-69.
44. Vikis, H.G., Li, W., and Guan, K.L., The plexin-B1/ Rac interaction inhibits PAK activation and enhances Sema4D ligand binding. Genes Dev 2002; 16:836-845.
45. Hall, A., Rho GTPases and the actin cytoskeleton. Science 1998; 279:509-514.
46. Driessens, M.H., Hu, H., Nobes, C.D., Self, A., Jordens, I., Goodman, C.S., and Hall, A., Plexin-B semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr Biol 2001; 11:339-344.
47. Vikis, H.G., Li, W., He, Z., and Guan, K.L., The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc Natl Acad Sci U S A 2000; 97:12457-12462.
48. Aurandt, J., Vikis, H.G., Gutkind, J.S., Ahn, N., and Guan, K.L., The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc Natl Acad Sci U S A 2002; 99:12085-12090.
49. Hirotani, M., Ohoka, Y., Yamamoto, T., Nirasawa, H., Furuyama, T., Kogo, M., Matsuya, T., and Inagaki, S., Interaction of plexin-B1 with PDZ domain-containing Rho guanine nucleotide exchange factors. Biochem Biophys Res Commun 2002; 297:32-37.
50. Comeau, M.R., Johnson, R., DuBose, R.F., Petersen, M., Gearing, P., VandenBos, T., Park, L., Farrah, T., Buller, R.M., Cohen, J.I., Strockbine, L.D., Rauch, C., and Spriggs, M.K., A poxvirus-encoded semaphorin induces cytokine production from monocytes and binds to a novel cellular semaphorin receptor, VESPR. Immunity 1998; 8:473-482.
51. Spriggs, M.K., Shared resources between the neural and immune systems: semaphorinsjoin the ranks. Curr Opin Immunol 1999; 11:387-391.
52. Spriggs, M.K., One step ahead of the game: viral immunomodulatory molecules. Annu Rev Immunol 1996; 14:101-130.
53. Yamada, A., Kubo, K., Takeshita, T., Harashima, N., Kawano, K., Mine, T., Sagawa, K., Sugamura, K., and Itoh, K., Molecular cloning of a glycosylphosphatidylinositol-anchored molecule CDw108. J Immunol 1999; 162:4094-4100.
54. Xu, X., Ng, S., Wu, Z.L., Nguyen, D., Homburger, S., Seidel-Dugan, C., Ebens, A., and Luo, Y., Human semaphorin K1 is glycosylphosphatidyhnositol-linked and defines a new subfamily of viral-related semaphorins. J Biol Chem 1998; 273:22428-22434.
55. Mine, T., Harada, K., Matsumoto, T., Yamana, H., Shirouzu, K., Itoh, K., and Yamada, A., CDw108 expression during T-cell development. Tissue Antigens 2000; 55:429-436.
56. Holmes, S., Downs, A.M., Fosberry, A., Hayes, P.D., Michalovich, D., Murdoch, P., Moores, K., Fox, J., Deen, K., Pettman, G., Wattam, T., and Lewis, C., Sema7A is a potent monocyte stimulator. Scand J Immunol 2002; 56:270-275.
57. Frank, I., Stoiber, H., Godar, S., Stockinger, H., Steindl, F., Katinger, H.W., and Dierich, M.P., Acquisition of host cell-surface-derived molecules by HIV-1. AIDS 1996; 10:1611-1620.
58. Kumanogoh, A., Marukawa, S., Suzuki, K., Takegahara, N., Watanabe, C., Ch'ng, E., Ishida, I., Fujimura, H., Sakoda, S., Yoskida, K., and Kikutani, H., Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2. Nature 2002; 419:629-633.
59. Monney, L., Sabatos, C.A., Gaglia, J.L., Ryu, A., Waldner, H., Chernova, T., Manning, S., Greenfield, E.A., Coyle, A.J., Sobel, R.A., Freeman, G.J., and Kuchroo, V.K., Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 2002; 415:536-41.
60. Delon, J., and Germain, R.N., Information transfer at the immunological synapse. Curr Biol 2000; 10: R923-R933.
61. Tordjman, R., Lepelletier, Y., Lemarchandel, V., Cambot, M., Gaulard, P., Hermine, O., and Romeo, P.H., A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nat Immunol 2002; 3:477-482.
62. Goshima, Y., Ito, T., Sasaki, Y., and Nakamura, F., Semaphorins as signals for cell repulsion and invasion. J Clin Invest 2002; 109:993-998.
63. Terman, J.R., Mao, T., Pasterkamp, R.J., Yu, H.H., and Kolodkin, A.L., MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 2002; 109:887-900.
64. Weigent, D.A., and Blalock, J.E., Interactions between the neuroendocrine and immune systems: common hormones and receptors. Immunol Rev 1987; 100:79-108.
65. Song, H., Ming, G., He, Z., Lehmann, M., McKerracher, L., Tessier-Lavigne, M., and Poo, M., Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 1998; 281:1515-1518.