Measles virus infects and suppresses proliferation of T lymphocytes from transgenic mice bearing human signaling lymphocytic activation molecule

Journal of Virology

Volumn 77, Issue 6, 2003, Pages 3505-3515

  Hahm, Bumsuk ^a   Arbour, Nathalie ^a   Naniche, Denise ^a   Homann, Dirk ^a   Manchester, Marianne ^a   Oldstone, Michael B A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GLYCOPROTEIN; MEMBRANE COFACTOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIVISION; CONTROLLED STUDY; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MEASLES; MEASLES VIRUS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSGENIC MOUSE; VIRUS INFECTION;

ANIMALS; ANTIGENS, CD; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; GLYCOPROTEINS; HUMANS; IMMUNOGLOBULINS; IMMUNOSUPPRESSION; LYMPHOCYTE ACTIVATION; MEASLES; MEASLES VIRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, CELL SURFACE; SPLEEN; THYMUS GLAND; TRANSGENES;

EID: 0037333887     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.6.3505-3515.2003     Document Type: Article

References (57)

1. Auwaerter, P. G., H. Kaneshima, J. M. McCune, G. Wiegand, and D. E. Griffin. 1996. Measles virus infection of thymic epithelium in the SCID-hu mouse leads to thymocyte apoptosis. J. Virol. 70:3734-3740.
2. Aversa, G., J. Carballido, J. Punnonen, C.-C. J. Chang, T. Hauser, B. G. Cocks, and J. E. de Vries. 1997. SLAM and its role in T cell activation and Th cell responses. Immunol. Celt Biol. 75:202-205.
3. Chaffin, K. E., C. R. Beals, T. M. Wilkie, K. A. Forbush, M. I. Simon, and R. M. Perlmutter. 1990. Dissection of thymocyte signaling pathways by in vivo expression of pertussis toxin ADP-ribosyltransferase. EMBO J. 9:3821-3829.
4. Cocks, B. G., C.-C. J. Chang, J. M. Carballido, H. Yssel, J. E. de Vries, and G. Aversa. 1995. A novel receptor involved in T-cell activation. Nature 376:260-263.
5. Davis, S. J., S. Ikemizu, M. K. Wild, and P. A. van der Merwe. 1998. CD2 and the nature of protein interactions mediating cell-cell recognition. Immunol. Rev. 163:217-236.
6. Dorig, R., A. Marcel, A. Chopra, and C. D. Richardson. 1993. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75:295-305.
7. Enders, J. F., and T. C. Peebles. 1954. Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc. Soc. Exp. Biol. Med. 86:277-286.
8. Erlenhofer, C., W. P. Duprex, B. K. Rima, V. ter Menlen, and J. Schneider-Schaulies. 2002. Analysis of receptor (CD46, CD150) usage by measles virus. J. Gen. Virol. 83:1431-1436.
9. Erlenhoefer, C., W. J. Wurzer, S. Löffler, S. Schneider-Schaulies, V. ter Menlen, and J. Schneider-Schaulies. 2001. CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J. Virol. 75:4499-4505.
10. Fraser, C. C., D. Howie, M. Morra, Y. Qiu, C. Murphy, Q. Shen, J. C. Gutierrez-Ramos, A. Coyle, G. A. Kingsbury, and C. Terhorst. 2002. Identification and characterization of SF2000 and SF2001, two new members of the immune receptor SLAM/CD2 family. Immunogenetics 53:843-850.
11. Fugier-Vivier, I., C. Servet-Delprat, P. Rivailler, M. C. Rissoan, Y. J. Liu, and C. Rabourdin-Combe. 1997. Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J. Exp. Med. 186:813-823.
12. Griffin, D. E. 1995. Immune responses during measles virus infection, p.117-134. In M. Billeter and V. ter Meulen (ed.), Measles virus. Springer, Berlin, Germany.
13. Griffin, D. E., and B. J. Ward. 1993. Differential CD4 T cell activation in measles. J. Infect. Dis. 168:275-281.
14. Grosjean, I., C. Caux, C. Bella, I. Berger, F. Wild, J. Banchereau, and D. Kaiserlian. 1997. Measles virus infects human dendritic cells and blocks their allostimulatory properties for CD4+ T cells. J. Exp. Med. 186:801-812.
15. Hamalainen, H., S. Meissner, and R. Lahesmaa. 2000. Signaling lymphocytic activation molecule is differentially expressed in human Thl and Th2 cells. J. Immunol. Methods 242:9-19.
16. Horvat, B., P. Rivailler, G. Varior-Krishnan, A. Cardoso, D. Gerlier, and C. Rabourdin-Combe. 1996. Transgenic mice expressing human measles virus (MV) receptor provide cells exhibiting different permissivities to MV infection. J. Virol. 70:6673-6681.
17. Howie, D., M. Simarro, J. Sayos, M. Guirado, J. Sancho, and C. Terhorst. 2002. Molecular dissection of the signaling and costimulatory functions of CD150 (SLAM): CD150/SAP binding and CD150-mediated costimulation. Blood 99:957-965.
18. Hsu, E. C., C. Iorio, F. Sarangi, A. A. Khine, and C. D. Richardson. 2001. CDw150 (SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279:9-21.
19. Hyypia, T., P. Korkiamaki, and R. Vainionpaa. 1985. Replication of measles virus in human lymphocytes. J. Exp. Med. 161:1261-1271.
20. Katz, S. L., M. V. Milovanovic, and J. F. Enders. 1958. Propagation of measles virus in cultures of chicken embryo cells. Proc. Soc. Exp. Biol. Med. 97:23-29.
21. Kobune, F., H. Sakata, and A. Sugiura. 1990, Marmoset lymphoblastoid cells as a sensitive host for isolation of measles virus. J. Virol. 64:700-705.
22. Latour, S., G. Gish, C. D. Helgason, R. K. Humphries, T. Pawson, and A. Veillette. 2001. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat. Immunol. 2:681-690.
23. Lawrence, D. M. P., M. M. Vaughn, A. R. Belman, J. S. Cole, and G. F. Rail. 1999. Immune response-mediated protection of adult but not neonatal mice from neuron-restricted measles virus infection and central nervous system disease. J. Virol. 73:1795-1801.
24. Liebert, U. G., and D. Finke. 1995. Measles virus infections in rodents. Curr. Top. Microbiol. Immunol. 191:149-166.
25. Manchester, M., D. S. Eto, A. Valsamakis, P. B. Liton, R. Fernandez-Munoz, P. A. Rota, W. J. Bellini, D. N. Forthal, and M. B. A. Oldstone. 2000. Clinical isolates of measles virus use CD46 as a cellular receptor. J. Virol. 74:3967-3974.
26. Manchester, M., M. K. Liszewski, J. P. Atkinson, and M. B. A. Oldstone. 1994. Multiple isoforms of CD46 (membrane cofactor protein) serve as receptors for measles virus. Proc. Natl. Acad. Sci. USA 91:2161-2165.
27. McChesney, M. B., A. Altman, and M. B. A. Oldstone. 1988. Suppression of T lymphocyte function by measles virus is due to cell cycle arrest in G1. J. Immunol. 140:1269-1273.
28. McChesney, M. B., and M. B. A. Oldstone. 1989. Virus-induced immunosuppression: infections with measles virus and human immunodeficiency virus. Adv. Immunol. 45:335-380.
29. McQuaid, S., and S. L. Cosby. 2002. An immunohistochemical study of the distribution of the measles virus receptors, CD46 and SLAM, in normal human tissues and subacute sclerosing panencephalitis. Lab. Investig. 82: 403-409.
30. Minagawa, H., K. Tanaka, N. Ono, H. Tatsuo, and Y. Yanagi. 2001. Induction of the measles virus receptor SLAM (CD150) on monocytes. J. Gen. Virol. 82:2913-2917.
31. Moench, T. R., D. E. Griffin, C. Obriecht, A. Vaisberg, and R. T. Johnson. 1988. Acute measles in patients with and without neurological involvement: distribution of measles virus antigen and RNA. J. Infect. Dis. 158:433-437.
32. 0-like block leads to suppression of retinoblastoma protein expression. J. Virol. 73:1894-1901.
33. Naniche, D., G. Varior-Krishnan, F. Cervino, T. F. Wild, B. Rossi, C. Rabourdin-Combe, and D. Gerlier. 1993. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J. Virol. 67:6025-6032.
34. Niewiesk, S., M. Gotzelmann, and V. ter Meulen. 2000. Selective in vivo suppression of T lymphocyte responses in experimental measles virus infection. Proc. Natl. Acad. Sci. USA 97:4251-4255.
35. Nozawa, Y., N. Ono, M. Abe, H. Sakuma, and H. Wakasa. 1994. An immunohistochemical study of Warthlin-Finkeldey cells in measles. Pathol. Int. 44:442-447.
36. Oldstone, M. B. A., H. Lewicki, D. Thomas, A. Tishon, S. Dales, J. Patterson, M. Manchester, D. Homann, D. Naniche, and A. Holz. 1999. Measles virus infection in a transgenic model: virus-induced central nervous system disease and immunosuppression. Cell 98:629-640.
37. Ono, N., H. Tatsuo, Y. Hidaka, T. Aoki, H. Minagawa, and Y. Yanagi. 2001. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J. Virol. 75:4399-4401.
38. Ono, N., H. Tatsuo, K. Tanaka, H. Minagawa, and Y. Yanagi. 2001. V domain of human SLAM (CDw150) is essential for its function as a measles virus receptor. J. Virol. 75:1594-1600.
39. Patterson, C. E., D. M. Lawrence, L. A. Echols, and G. F. Rall. 2002. Immune-mediated protection from measles virus-induced central nervous system disease is noncytolytic and gamma interferon dependent. J. Virol. 76:4497-4506.
40. Punnonen, J., B. G. Cocks, J. M. Carballido, B. Bennett, D. Peterson, G. Aversa, and J. E. de Vries. 1997. Soluble and membrane-bound forms of signaling lymphocytic activation molecule (SLAM) induce proliferation and Ig synthesis by activated human B lymphocytes. J. Exp. Med. 185:993-1004.
41. Rail, G. F., M. Manchester, L. R. Daniels, E. Callahan, A. Belman, and M. B. A. Oldstone. 1997. A transgenic mouse model for measles virus infection of the brain. Proc. Natl. Acad. Sci. USA 94:4659-4663.
42. Sayos, J., C. Wu, M. Morra, N. Wang, X. Xang, D. Allen, S. van Schaik, L. Notarangelo, R. Geha, M. G. Roncarolo, H. Ottegen, J. E. De Vries, G. Aversa, and C. Terhorst. 1998. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395:462-469.
43. Schlender, J., J. J. Schnorr, P. Spielhoffer, T. Cathomen, R. Cattaneo, M. A. Billeter, V. ter Meulen, and S. Schneider-Schaulies. 1996. Interaction of measles virus glycoproteins with the surface of uninfected peripheral blood lymphocytes induces immunosuppression in vitro. Proc. Natl. Acad. Sci. USA 93:13194-13199.
44. Schneider, U., V. von Messling, P. Devaux, and R. Cattaneo. 2002. Efficiency of measles virus entry and dissemination through different receptors. J. Virol. 76:7460-7467.
45. Schnorr, J. J., S. Xanthakos, P. Keikavoussi, E. Kampgen, V. ter Meulen, and S. Schneider-Schaulies. 1997. Induction of maturation of human blood dendritic cell precursors by measles virus is associated with immunosuppression. Proc. Natl. Acad. Sci. USA 94:5326-5331.
46. Servet-Delprat, C., P. O. Vidalain, H. Bausinger, S. Manie, F. Le Deist, O. Azoear, D. Hanau, A. Fischer, and C. Rabourdin-Combe. 2000. Measles virus induces abnormal differentiation of CD40L-activated human dendritic cells. J. Immunol. 164:1753-1760.
47. Shimizu, C., H. Kawamoto, M. Yamashita, M. Kimura, E. Kondou, Y. Kaneko, S. Okada, T. Tokuhisa, M. Yokoyama, M. Taniguchi, Y. Katsura, and T. Nakayama. 2001. Progression of T cell lineage restriction in the earliest subpopulation of murine adult thymus visualized by the expression of lck proximal promoter activity. Int. Immunol. 13:105-117.
48. Shlapatska, L. M., S. V. Mikhalap, A. G. Berdova, O. M. Zelensky, T. J. Yun, K. E. Nichols, E. A. Clark, and S. P. Sodorenko. 2001. CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J. Immunol. 166:5480-5487.
49. Sidorenko, S. P., and E. A. Clark. 1993. Characterization of a cell surface glycoprotein IPO-3, expressed on activated human B and T lymphocytes. J. Immunol. 151:4614-4624.
50. Sullivan, J. L., D. W. Barry, S. J. Lucas, and P. Albrecht. 1975. Measles infection of human mononuclear cells. I. Acute infection of peripheral blood lymphocytes and monocytes. J. Exp. Med. 142:773-784.
51. Tanaka, K., H. Minagawa, M. F. Xie, and Y. Yanagi. 2002. The measles virus hemagglutinin downregulates the cellular receptor SLAM (CD150). Arch. Virol. 147:195-203.
52. Tatsuo, H., N. Ono, K. Tanaka, and Y. Yanagi. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897.
53. ter Meulen, V., J. R. Stephenson, and H. W. Kreth. 1983. Subacute sclerosing panencephalitis. In H. Fraenkel-Conrat and R. R. Wagner (ed.), The viruses, vol. 18. Plenum Press, New York, N.Y.
54. Tsujimura, A., K. Shida, M. Kitamura, M. Nomura, J. Takeda, H. Tanaka, M. Matsumoto, K. Matsumiya, A. Okuyama, Y. Nishimune, M. Okabe, and T. Seya. 1998. Molecular cloning of a murine homologue of membrane cofactor protein (CD46): preferential expression in testicular germ cells. Biochem. J. 330:163-168.
55. Vydelingum, S., K. Suryanarayana, R. G. Marusyk, and A. A. Salmi. 1995. Replication of measles virus in human monocytes and T cells. Can. J. Microbiol. 41:620-623.
56. Weidmann, A., A. Maisner, W. Garten, M. Seufert, V. ter Meulen, and S. Schneider-Schaulies. 2000. Proteolytic cleavage of the fusion protein but not membrane fusion is required for measles virus-induced immunosuppression in vitro. J. Virol. 74:1985-1993.
57. Yannoutsos, N., J. N. Ijzermans, C. Harkes, F. Bonthuis, C. Y. Zhou, D. White, R. L. Marquet, and F. Grosveld. 1996. A membrane cofactor protein transgenic mouse model for the study of discordant xenograft rejection. Genes Cells 1:409-419.