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Biochemistry (Moscow)

, Volume 84, Issue 9, pp 1021–1027 | Cite as

Receptor Functions of Semaphorin 4D

  • E. M. KuklinaEmail author
Mini-Review
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Abstract

Semaphorin 4D (Sema4D) is a multifunctional protein widely expressed in an organism that plays an important role in the control of many physiological and pathological processes, including immunoregulation, neurogenesis, angiogenesis, and tumor progression. It was first described almost 30 years ago and has been actively studied since then. However, with rare exceptions, all studies of the Sema4D activity proceed from the assumption that semaphorin is a ligand that acts through specific receptors (CD72 and plexins) and that the main targets of Sema4D in different tissues are cells that carry these receptors on the membrane. This review analyzes the data indicating the presence of an alternative mechanism for the regulatory activity of Sema4D that involves the functioning of membrane semaphorin as a receptor ensuring the outside-in signaling. Cell signaling pathways mediated by the membrane Sema4D and their contribution to the Sema4D-dependent regulation of cell functions are discussed.

Keywords

membrane Sema4D T lymphocytes B lymphocytes NK cells neutrophils tumor cells  

Abbreviations

BCR

B cell receptor

NK cells

natural killer cells

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Notes

Funding. This work was supported by the Russian Foundation for Basic Research (project 19-015-00379) and the State Budget Project no. 01201353248.

Ethical approval. This article does not contain any studies with human participants or animals performed by the author.

References

  1. 1.
    Semaphorin Nomenclature Committee (1999) Unified nomenclature for the semaphorins/collapsins, Cell, 97, 551–552.CrossRefGoogle Scholar
  2. 2.
    Bougeret, C., Mansur, I. G., Dastot, H., Schmid, M., Mahouy, G., Bensussan, A., and Boumsell, L. (1992) Increased surface expression of a newly identified 150-kDa dimer early after human T lymphocyte activation, J. Immunol., 148, 318–323.Google Scholar
  3. 3.
    Swiercz, J. M., Kuner, R., Behrens, J., and Offermanns, S. (2002) Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology, Neuron, 35, 51–63.CrossRefGoogle Scholar
  4. 4.
    Moreau-Fauvarque, C., Kumanogoh, A., Camand, E., Jaillard, C., Barbin, G., Boquet, I., Love, C., Jones, E. Y., Kikutani, H., Lubetzki, C., Dusart, I., and Chedotal, A. (2003) The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendro-cytes and upregulated after CNS lesion, J. Neurisci., 23, 9229–9239.CrossRefGoogle Scholar
  5. 5.
    Wang, X., Kumanogoh, A., Watanabe, C., Shi, W., Yoshida, K., and Kikutani, H. (2001) Functional soluble CD100/Sema4D released from activated lymphocytes: possible role in normal and pathologic immune responses, Blood, 97, 3498–3504.CrossRefGoogle Scholar
  6. 6.
    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. (2000) Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling, Immunity, 13, 621–631.CrossRefGoogle Scholar
  7. 7.
    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. (2002) Requirement for the lymphocyte semaphorin, CD100, in the induction of antigen-specific T cells and the maturation of dendritic cells, J. Immunol., 169, 1175–1181.CrossRefGoogle Scholar
  8. 8.
    Conrotto, P., Valdembri, D., Corso, S., Serini, G., Tamagnone, L., Comoglio, P. M., Bussolino, F., and Giordano, S. (2005) Sema4D induces angiogenesis through Met recruitment by Plexin B1, Blood, 105, 4321–4329.CrossRefGoogle Scholar
  9. 9.
    Negishi-Koga, T., Shinohara, M., Komatsu, N., Bito, H., Kodama, T., Friedel, H., and Takayanagi, H. (2011) Suppression of bone formation by osteoclastic expression of semaphorin 4D, Nat. Med., 17, 1473–1480, doi:  https://doi.org/10.1038/nm.2489.CrossRefGoogle Scholar
  10. 10.
    Evans, E., Jonason, S., Bussler, H., Torno, S., Veeraraghavan, J., Reilly, C., Doherty, A., Seils, J., Winter, A., Mallow, C., Kirk, R., Howell, A., Giralico, S., Scrivens, M., Klimatcheva, K., Fisher, L., Bowers, J., Paris, M., Smith, S., and Zauderer, M. (2015) Antibody blockade of semaphorin 4D promotes immune infiltration into tumor and enhances response to other immunomodulatory therapies, Cancer Immunol. Res., 3, 689–701, doi:  https://doi.org/10.1158/2326-6066.CIR-14-0171.CrossRefGoogle Scholar
  11. 11.
    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. (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates, Cell, 99, 71–80.CrossRefGoogle Scholar
  12. 12.
    Chabbert-de Ponnat, I., Marie-Cardine, A., Pasterkamp, J., Schiavon, V., Tamagnone, L., Thomasset, N., Bensussan, A., and Boumsell, L. (2005) Soluble CD100 functions on human monocytes and immature dendritic cells require plexin C1 and plexin B1, respectively, Int. Immunol., 17, 439–447.CrossRefGoogle Scholar
  13. 13.
    Witherden, A., Watanabe, M., Garijo, O., Rieder, E., Sarkisyan, G., Cronin, J., Verdino, P., Wilson, A., Kumanogoh, A., Kikutani, H., Teyton, L., Fischer, H., and Havran, L. (2012) The CD100 receptor interacts with its plexin B2 ligand to regulate epidermal γδ T cell function, Immunity, 37, 314–325, doi:  https://doi.org/10.1016/j.immuni.2012.05.026.CrossRefGoogle Scholar
  14. 14.
    Giacobini, P., Messina, A., Morello, F., Ferraris, N., Corso, S., Penachioni, J., Giordano, S., Tamagnone, L., and Fasolo, A. (2008) Semaphorin 4D regulates gonadotropin hormone-releasing hormone-1 neuronal migration through PlexinB1–Met complex, Mol. Cell Biol., 183, 555–566.Google Scholar
  15. 15.
    Kuklina, E. M., and Nekrasova, I. V. (2017) New aspects of the Sema4D-dependent control of lymphocyte activation, Dokl. Biol. Sci., 473, 84–88, doi:  https://doi.org/10.1134/S0012496617020028.CrossRefGoogle Scholar
  16. 16.
    Herold, C., Bismuth, G., Bensussan, A., and Boumsell, L. (1995) 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., 7, 1–8.CrossRefGoogle Scholar
  17. 17.
    Granziero, L., Circosta, P., Scielzo, C., Frisaldi, E., Stella, S., Geuna, M., Giordano, S., Ghia, P., and Caligaris-Cappio, F. (2003) CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes, Blood, 101, 1962–1969.CrossRefGoogle Scholar
  18. 18.
    Mizrahi, S., Markel, G., Porgador, A., Bushkin, Y., and Mandelboim, O. (2007) CD100 on NK cells enhance IFNγ secretion and killing of target cells expressing CD72, PLoS One, 2, e818.CrossRefGoogle Scholar
  19. 19.
    He, Y., Guo, Y., Fan, C., Lei, Y., Zhou, Y., Zhang, M., Ye, C., Ji, G., Ma, L., Lian, J., Moorman, J. P., Yao, Z. Q., Wang, J., Hao, C., Zhang, Y., and Jia, Z. (2017) Interferon-α-enhanced CD100/plexin-B1/B2 interactions promote natural killer cell functions in patients with chronic hepatitis C virus infection, Front. Immunol., 8, 1435, doi:  https://doi.org/10.3389/fimmu.2017.01435 CrossRefGoogle Scholar
  20. 20.
    Nishide, M., Nojima, S., Ito, D., Takamatsu, H., Koyama, S., Kang, S., Kimura, T., Morimoto, K., Hosokawa, T., Hayama, Y., Kinehara, Y., Kato, Y., Nakatani, T., Nakanishi, Y., Tsuda, T., Park, J. H., Hirano, T., Shima, Y., Narazaki, M., Morii, E., and Kumanogoh, A. (2017) Semaphorin 4D inhibits neutrophil activation and is involved in the pathogenesis of neutrophil-mediated autoimmune vasculitis, Ann. Rheum. Dis., 76, 1440–1448, doi:  https://doi.org/10.1136/annrheumdis-2016-210706 CrossRefGoogle Scholar
  21. 21.
    Zhou, H., Kann, M. G., Mallory, E. K., Yang, Y. H., Bugshan, A., Binmadi, N. O., and Basile, J. R. (2017) Recruitment of Tiam1 to semaphorin 4D activates Rac and enhances proliferation, invasion, and metastasis in oral squamous cell carcinoma, Neoplasia, 19, 65–74, doi:  https://doi.org/10.1016/j.neo.2016.12.004.CrossRefGoogle Scholar
  22. 22.
    Li, B. J., He, Y., Zhang, Y., Guo, Y. H., Zhou, Y., Zhang, P. X., Wang, W., Zhao, J. R., Li, J. G., Zuo, W. Z., Fan, C., and Jia, Z. S. (2017) Interferon-α-induced CD100 on naive CD8+ T cells enhances antiviral responses to hepatitis C infection through CD72 signal transduction, J. Int. Med. Res., 45, 89–100, doi:  https://doi.org/10.1177/0300060516676136.CrossRefGoogle Scholar
  23. 23.
    Jiang, X., Bjorkstrom, N. K., and Melum, E. (2017) Intact CD100–CD72 interaction necessary for TCR-induced T cell proliferation, Front. Immunol., 8, 765, doi:  https://doi.org/10.3389/fimmu.2017.00765.CrossRefGoogle Scholar
  24. 24.
    Correa-Rocha, R., Lopez-Abente, J., Gutierrez, C., Perez-Fernandez, V. A., Prieto-Sanchez, A., Moreno-Guillen, S., Munoz-Fernandez, M. A., and Pion, M. (2018) CD72/CD100 and PD-1/PD-L1 markers are increased on T and B cells in HIV-1+ viremic individuals, and CD72/CD100 axis is correlated with T-cell exhaustion, PLoS One, 13, e0203419, doi: {rs 10.1371/journal.pone.0203419 DOI}.CrossRefGoogle Scholar
  25. 25.
    Eriksson, E., Jeffrey, M., Emily H., Batista, D., Holditch, J., Keh, E., Norris, J., Keating, M., Deeks, G., Hunt, P., Martin, N., Rosenberg, G., Hecht, M., and Nixon, D. (2012) Expansion of CD8+ T cells lacking Sema4D/CD100 during HIV-1 infection identifies a subset of T cells with decreased functional capacity, Blood, 119, 745–755, doi:  https://doi.org/10.1182/blood-2010-12-324848.CrossRefGoogle Scholar
  26. 26.
    Liu, B., Ma, Y., Zhang, Y., Zhang, C., Yi, J., Zhuang, R., Yu, H., Yang, A., Zhang, Y., and Jin, B. (2015) CD8low CD100– T cells identify a novel CD8 T cell subset associated with viral control during human Hantaan virus infection, J. Virol., 89, 11834–11844, doi:  https://doi.org/10.1128/JVI.01610-15.CrossRefGoogle Scholar
  27. 27.
    He, Y., Guo, Y., Zhou, Y., Zhang, Y., Fan, C., Ji, G., Wang, Y., Ma, Z., Lian, J., Hao, C., Yao, Q., and Jia, Z. (2014) CD100 up-regulation induced by interferon-α on B cells is related to hepatitis C virus infection, PLoS One, 9, e113338, doi:  https://doi.org/10.1371/journal.pone.0113338.CrossRefGoogle Scholar
  28. 28.
    Elhabazi, A., Lang, V., Herold, C., Freeman, G. J., Bensussan, A., Boumsell, L., and Bismuth, G. (1997) The human semaphorin-like leukocyte cell surface molecule CD100 associates with a serine kinase activity, J. Biol. Chem., 272, 23515–23520.CrossRefGoogle Scholar
  29. 29.
    Herold, C., Elhabazi, A., Bismuth, G., Bensussan, A., and Boumsell, L. (1996) CD100 is associated with CD45 at the surface of human T lymphocytes. Role in T cell homotypic adhesion, J. Immunol., 157, 5262–5268.Google Scholar
  30. 30.
    Billard, C., Delaire, S., Raffoux, E., Bensussan, A., and Boumsell, L. (2000) Switch in the protein tyrosine phosphatase associated with human CD100 semaphorin at terminal B-cell differentiation stage, Blood, 95, 965–972.Google Scholar
  31. 31.
    Stover, D. R., and Walsh, K. A. (1994) Protein-tyrosine phosphatase activity of CD45 is activated by sequential phosphorylation by two kinases, Mol. Cell Biol., 14, 5523–5532.CrossRefGoogle Scholar
  32. 32.
    Saunders, A. E., and Johnson, P. (2010) Modulation of immune cell signaling by the leukocyte common tyrosine phosphatase, CD45, Cell Signal., 22, 339–348, doi:  https://doi.org/10.1016/j.cellsig.2009.10.003.CrossRefGoogle Scholar
  33. 33.
    Simeoni, L. (2017) Lck activation: puzzling the pieces together, Oncotarget, 8, 102761–102762, doi:  https://doi.org/10.18632/oncotarget.22309.CrossRefGoogle Scholar
  34. 34.
    Palacios, E. H., and Weiss, A. (2004) Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation, Oncogene, 23, 7990–8000.CrossRefGoogle Scholar
  35. 35.
    Xu, Y., Harder, K. W., Huntington, N. D., Hibbs, M. L., and Tarlinton, D. M. (2005) Lyn tyrosine kinase: accentuating the positive and the negative, Immunity, 22, 9–18.Google Scholar
  36. 36.
    Irie-Sasaki, J., Sasaki, T., Matsumoto, W., Opavsky, A., Cheng, M., Welstead, G., Griffiths, E., Krawczyk, C., Richardson, C. D., Aitken, K., Iscove, N., Koretzky, G., Johnson, P., Liu, P., Rothstein, D. M., and Penninger, J. M. (2001) CD45 is a JAK phosphatase and negatively regulates cytokine receptor signaling, Nature, 409, 349–354.CrossRefGoogle Scholar
  37. 37.
    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. (2000) The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice, Immunity, 13, 633–642.CrossRefGoogle Scholar
  38. 38.
    Kuklina, E. M., Nekrasova, I. V., and Valieva, Yu. V. (2017) The involving of semaphorin Sema4D in T-dependent activation of B lymphocytes, Bull. Exp. Biol. Med., 163, 444–447, doi:  https://doi.org/10.1007/s10517-017-3825-8.CrossRefGoogle Scholar
  39. 39.
    Krzywinska, E., Cornillon, A., Allende-Vega, N., Vo, D.-N., Rene, C., Lu, Z.-Y., Pasero, C., Olive, D., Fegueux, N., Ceballos, P., Hicheri, Y., Sobecki, M., Rossi, J.-F., Cartron, G., and Villalba, M. (2016) CD45 isoform profile identifies natural killer (NK) subsets with differential activity, PLoS One, 11, e0150434, doi:  https://doi.org/10.1371/journal.pone.0150434 CrossRefGoogle Scholar
  40. 40.
    Yu, C., Yu, H. S., Sun, K. H., Hsieh, S. C., and Tsai, C. Y. (2002) Anti-CD45 isoform antibodies enhance phagocytosis and gene expression of IL-8 and TNF-α in human neutrophils by differential suppression on protein tyrosine phosphorylation and p56lck tyrosine kinase, Clin. Exp. Immunol., 129, 78–85.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.Institute of Ecology and Genetics of Microorganisms, Perm Federal Research CenterUral Branch of the Russian Academy of SciencesPermRussia

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