1887

Abstract

Measles virus (MV) nucleoprotein (N) is a cytosolic protein that is released into the extracellular compartment after apoptosis and/or secondary necrosis of MV-infected cells . Thus, MV-N becomes accessible to inhibitory cell-surface receptors: FcRIIB and an uncharacterized nucleoprotein receptor (NR). MV-N is composed of two domains: N (aa 1–400) and N (aa 401–525). To assess the contribution of MV-N domains and of these two receptors in suppression of cell proliferation, a human melanoma HT144 cell line expressing (HT144IIB1) or lacking FcRIIB1 was used as a model. Specific and exclusive N–FcRIIB1 and N–NR interactions were shown. Moreover, N binding to human NR predominantly led to suppression of cell proliferation by arresting cells in the G/G phases of the cell cycle, rather than to apoptosis. N binding to HT144IIB1 cells primarily triggered caspase-3 activation, in contrast to HT144IIB1/IC cells lacking the FcRIIB1 intra-cytoplasmic tail, thus demonstrating the specific inhibitory effect of the N–FcRIIB1 interaction. MV-N- and N-mediated apoptosis through FcRIIB1 was inhibited by the pan-caspase inhibitor zVAD-FMK, indicating that apoptosis was dependent on caspase activation. By using N deletion proteins, it was also shown that the region of N responsible for binding to human NR and for cell growth arrest maps to one of the three conserved boxes (Box1, aa 401–420) found in N of . This work unveils novel mechanisms by which distinct domains of MV-N may display different immunosuppressive activities, thus contributing to our comprehension of the immunosuppressive state associated with MV infection. Finally, MV-N domains may be good tools to target tumour cell proliferation and/or apoptosis.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80791-0
2005-06-01
2021-10-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/6/vir861771.html?itemId=/content/journal/jgv/10.1099/vir.0.80791-0&mimeType=html&fmt=ahah

References

  1. Avota E., Avots A., Niewiesk S., Kane L. P., Bommhardt U., ter Meulen V., Schneider-Schaulies S. 2001; Disruption of Akt kinase activation is important for immunosuppression induced by measles virus. Nat Med 7:725–731 [CrossRef]
    [Google Scholar]
  2. Bankamp B., Horikami S. M., Thompson P. D., Huber M., Billeter M., Moyer S. A. 1996; Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 216:272–277 [CrossRef]
    [Google Scholar]
  3. Beckford A. P., Kaschula R. O., Stephen C. 1985; Factors associated with fatal cases of measles. A retrospective autopsy study. S Afr Med J 68:858–863
    [Google Scholar]
  4. Bourhis J., Johansson K., Receveur-Bréchot V., Oldfield C. J., Dunker K. A., Canard B., Longhi S. 2004; The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their physiological partner. Virus Res 99:157–167 [CrossRef]
    [Google Scholar]
  5. Buckland R., Giraudon P., Wild F. 1989; Expression of measles virus nucleoprotein in Escherichia coli : use of deletion mutants to locate the antigenic sites. J Gen Virol 70:435–441 [CrossRef]
    [Google Scholar]
  6. Cassard L., Cohen-Solal J. F., Galinha A. 7 other authors 2002; Modulation of tumor growth by inhibitory Fc γ receptor expressed by human melanoma cells. J Clin Invest 110:1549–1557 [CrossRef]
    [Google Scholar]
  7. Choi K.-S., Nah J.-J., Ko Y.-J., Choi C.-U., Kim J.-H., Kang S.-Y., Joo Y.-S. 2003; Characterization of antigenic sites on the rinderpest virus N protein using monoclonal antibodies. J Vet Sci 4:57–65
    [Google Scholar]
  8. Choi K.-S., Nah J.-J., Ko Y.-J., Kang S.-Y., Yoon K.-J., Joo Y.-S. 2004; Characterization of immunodominant linear B-cell epitopes on the carboxy terminus of the rinderpest virus nucleocapsid protein. Clin Diagn Lab Immunol 11:658–664
    [Google Scholar]
  9. Cohen-Solal J. F., Cassard L., Fridman W. H., Sautes-Fridman C. 2004; Fc γ receptors. Immunol Lett 92:199–205 [CrossRef]
    [Google Scholar]
  10. Curran J., Kolakofsky D. 1999; Replication of paramyxoviruses. Adv Virus Res 54:403–422
    [Google Scholar]
  11. Curran J., Homann H., Buchholz C., Rochat S., Neubert W., Kolakofsky D. 1993; The hypervariable C-terminal tail of the Sendai paramyxovirus nucleocapsid protein is required for template function but not for RNA encapsidation. J Virol 67:4358–4364
    [Google Scholar]
  12. Diallo A., Barrett T., Barbron M., Meyer G., Lefevre P. C. 1994; Cloning of the nucleocapsid protein gene of peste-des-petits-ruminants virus: relationship to other morbilliviruses. J Gen Virol 75:233–237 [CrossRef]
    [Google Scholar]
  13. Etchart N., Desmoulins P. O., Chemin K., Maliszewski C., Dubois B., Wild F., Kaiserlian D. 2001; Dendritic cells recruitment and in vivo priming of CD8+ CTL induced by a single topical or transepithelial immunization via the buccal mucosa with measles virus nucleoprotein. J Immunol 167:384–391 [CrossRef]
    [Google Scholar]
  14. Fujinami R. S., Sun X., Howell J. M., Jenkin J. C., Burns J. B. 1998; Modulation of immune system function by measles virus infection: role of soluble factor and direct infection. J Virol 72:9421–9427
    [Google Scholar]
  15. Gerlier D., Valentin H., Laine D., Rabourdin-Combe C., Servet-Delprat C. 2005; Subversion of the immune system by measles virus: a model for the intricate interplay between a virus and the immune system. In Microbial Subversion of Host Immunity pp  1–81 Edited by Lachmman P., Oldstone M. B. Norfolk: Horizon Scientific Press;
    [Google Scholar]
  16. Giraudon P., Wild T. F. 1981; Monoclonal antibodies against measles virus. J Gen Virol 54:325–332 [CrossRef]
    [Google Scholar]
  17. Giraudon P., Jacquier M. F., Wild T. F. 1988; Antigenic analysis of African measles virus field isolates: identification and localization of one conserved and two variable epitope sites on the NP protein. Virus Res 10:137–152 [CrossRef]
    [Google Scholar]
  18. Graves M., Griffin D. E., Johnson R. T., Hirsch R. L., de Soriano I. L., Roedenbeck S., Vaisberg A. 1984; Development of antibody to measles virus polypeptides during complicated and uncomplicated measles virus infections. J Virol 49:409–412
    [Google Scholar]
  19. Grazia Cappiello M., Sutterwala F. S., Trinchieri G., Mosser D. M., Ma X. 2001; Suppression of IL-12 transcription in macrophages following Fc γ receptor ligation. J Immunol 166:4498–4506 [CrossRef]
    [Google Scholar]
  20. Griffin D. E. 1995; Immune responses during measles virus infection. Curr Top Microbiol Immunol 191:117–134
    [Google Scholar]
  21. Hahm B., Arbour N., Naniche D., Homann D., Manchester M., Oldstone M. B. 2003; Measles virus infects and suppresses proliferation of T lymphocytes from transgenic mice bearing human signaling lymphocytic activation molecule. J Virol 77:3505–3515 [CrossRef]
    [Google Scholar]
  22. Harty R. N., Palese P. 1995; Measles virus phosphoprotein (P) requires the NH2- and COOH-terminal domains for interactions with the nucleoprotein (N) but only the COOH terminus for interactions with itself. J Gen Virol 76:2863–2867 [CrossRef]
    [Google Scholar]
  23. Heaney J., Barrett T., Cosby S. L. 2002; Inhibition of in vitro leukocyte proliferation by morbilliviruses. J Virol 76:3579–3584 [CrossRef]
    [Google Scholar]
  24. Ilonen J., Makela M. J., Ziola B., Salmi A. A. 1990; Cloning of human T cells specific for measles virus haemagglutinin and nucleocapsid. Clin Exp Immunol 81:212–217
    [Google Scholar]
  25. Jacobson S., Sekaly R. P., Jacobson C. L., McFarland H. F., Long E. O. 1989; HLA class II-restricted presentation of cytoplasmic measles virus antigens to cytotoxic T cells. J Virol 63:1756–1762
    [Google Scholar]
  26. Johansson K., Bourhis J. M., Campanacci V., Cambillau C., Canard B., Longhi S. 2003; Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J Biol Chem 278:44567–44573 [CrossRef]
    [Google Scholar]
  27. Karlin D., Longhi S., Canard B. 2002; Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 302:420–432 [CrossRef]
    [Google Scholar]
  28. Karlin D., Ferron F., Canard B., Longhi S. 2003; Structural disorder and modular organization in Paramyxovirinae N and P. J Gen Virol 84:3239–3252 [CrossRef]
    [Google Scholar]
  29. Laine D., Trescol-Biemont M. C., Longhi S. 8 other authors 2003; Measles virus (MV) nucleoprotein binds to a novel cell surface receptor distinct from Fc γ RII via its C-terminal domain: role in MV-induced immunosuppression. J Virol 77:11332–11346 [CrossRef]
    [Google Scholar]
  30. Liston P., Batal R., DiFlumeri C., Briedis D. J. 1997; Protein interaction domains of the measles virus nucleocapsid protein (NP). Arch Virol 142:305–321 [CrossRef]
    [Google Scholar]
  31. Longhi S., Receveur-Brechot V., Karlin D., Johansson K., Darbon H., Bhella D., Yeo R., Finet S., Canard B. 2003; The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J Biol Chem 278:18638–18648 [CrossRef]
    [Google Scholar]
  32. Malbec O., Fridman W. H., Daeron M. 1999; Negative regulation of hematopoietic cell activation and proliferation by Fc γ RIIB. Curr Top Microbiol Immunol 244:13–27
    [Google Scholar]
  33. Marie J. C., Kehren J., Trescol-Biemont M. C. 8 other authors 2001; Mechanism of measles virus-induced suppression of inflammatory immune responses. Immunity 14:69–79 [CrossRef]
    [Google Scholar]
  34. McChesney M. B., Kehrl J. H., Valsamakis A., Fauci A. S., Oldstone M. B. 1987; Measles virus infection of B lymphocytes permits cellular activation but blocks progression through the cell cycle. J Virol 61:3441–3447
    [Google Scholar]
  35. McChesney M. B., Altman A., Oldstone M. B. 1988; Suppression of T lymphocyte function by measles virus is due to cell cycle arrest in G1. J Immunol 140:1269–1273
    [Google Scholar]
  36. Miller D. L. 1964; Frequency of complications of measles; 1963; Report on a national inquiry by the Public Health Laboratory Service in collaboration with the Society of Medical Officers of Health. Br Med J 5401:75–78
    [Google Scholar]
  37. Mondal B., Sreenivasa B. P., Dhar P., Singh R. P., Bandyopadhyay S. K. 2001; Apoptosis induced by peste des petits ruminants virus in goat peripheral blood mononuclear cells. Virus Res 73:113–119 [CrossRef]
    [Google Scholar]
  38. Moss W. J., Polack F. P. 2001; Immune responses to measles and measles vaccine: challenges for measles control. Viral Immunol 14:297–309 [CrossRef]
    [Google Scholar]
  39. Naniche D., Reed S. I., Oldstone M. B. 1999; Cell cycle arrest during measles virus infection: a G0-like block leads to suppression of retinoblastoma protein expression. J Virol 73:1894–1901
    [Google Scholar]
  40. Niewiesk S., Eisenhuth I., Fooks A., Clegg J. C., Schnorr J. J., Schneider-Schaulies S., ter Meulen V. 1997; Measles virus-induced immune suppression in the cotton rat ( Sigmodon hispidus ) model depends on viral glycoproteins. J Virol 71:7214–7219
    [Google Scholar]
  41. Norrby E., Gollmar Y. 1972; Appearance and persistence of antibodies against different virus components after regular measles infections. Infect Immun 6:240–247
    [Google Scholar]
  42. Okada H., Kobune F., Sato T. A., Kohama T., Takeuchi Y., Abe T., Takayama N., Tsuchiya T., Tashiro M. 2000; Extensive lymphopenia due to apoptosis of uninfected lymphocytes in acute measles patients. Arch Virol 145:905–920 [CrossRef]
    [Google Scholar]
  43. Okada H., Sato T. A., Katayama A. 8 other authors 2001; Comparative analysis of host responses related to immunosuppression between measles patients and vaccine recipients with live attenuated measles vaccines. Arch Virol 146:859–874 [CrossRef]
    [Google Scholar]
  44. Olszewska W., Erume J., Ripley J., Steward M. W., Partidos C. D. 2001; Immune responses and protection induced by mucosal and systemic immunization with recombinant measles nucleoprotein in a mouse model of measles virus-induced encephalitis. Arch Virol 146:293–302 [CrossRef]
    [Google Scholar]
  45. Pearse R. N., Kawabe T., Bolland S., Guinamard R., Kurosaki T., Ravetch J. V. 1999; SHIP recruitment attenuates Fc γ RIIB-induced B cell apoptosis. Immunity 10:753–760 [CrossRef]
    [Google Scholar]
  46. Pfeuffer J., Puschel K., Meulen V., Schneider-Schaulies J., Niewiesk S. 2003; Extent of measles virus spread and immune suppression differentiates between wild-type and vaccine strains in the cotton rat model ( Sigmodon hispidus ). J Virol 77:150–158 [CrossRef]
    [Google Scholar]
  47. Planz O., Pleschka S., Oesterle K., Berberich-Siebelt F., Ehrhardt C., Stitz L., Ludwig S. 2003; Borna disease virus nucleoprotein interacts with the CDC2–cyclin B1 complex. J Virol 77:11186–11192 [CrossRef]
    [Google Scholar]
  48. Pulford K., Ralfkiaer E., MacDonald S. M., Erber W. N., Falini B., Gatter K. C., Mason D. Y. 1986; A new monoclonal antibody (KB61) recognizing a novel antigen which is selectively expressed on a subpopulation of human B lymphocytes. Immunology 57:71–76
    [Google Scholar]
  49. Ravanel K., Castelle C., Defrance T., Wild T. F., Charron D., Lotteau V., Rabourdin-Combe C. 1997; Measles virus nucleocapsid protein binds to Fc γ RII and inhibits human B cell antibody production. J Exp Med 186:269–278 [CrossRef]
    [Google Scholar]
  50. Ravetch J. V., Bolland S. 2001; IgG Fc receptors. Annu Rev Immunol 19:275–290 [CrossRef]
    [Google Scholar]
  51. Realdon S., Gerotto M., Dal Pero F., Marin O., Granato A., Basso G., Muraca M., Alberti A. 2004; Proapoptotic effect of hepatitis C virus CORE protein in transiently transfected cells is enhanced by nuclear localization and is dependent on PKR activation. J Hepatol 40:77–85
    [Google Scholar]
  52. Reth M. 1989; Antigen receptor tail clue. Nature 338:383–384
    [Google Scholar]
  53. Sanchez-Lanier M., Guerin P., McLaren L. C., Bankhurst A. D. 1988; Measles virus-induced suppression of lymphocyte proliferation. Cell Immunol 116:367–381 [CrossRef]
    [Google Scholar]
  54. Schlender J., Schnorr J. J., Spielhoffer P., Cathomen T., Cattaneo R., Billeter M. A., ter Meulen V., Schneider-Schaulies S. 1996; Interaction of measles virus glycoproteins with the surface of uninfected peripheral blood lymphocytes induces immunosuppression in vitro . Proc Natl Acad Sci U S A 93:13194–13199 [CrossRef]
    [Google Scholar]
  55. Schneider-Schaulies S., ter Meulen V. 2002; Modulation of immune functions by measles virus. Springer Semin Immunopathol 24:127–148 [CrossRef]
    [Google Scholar]
  56. Schobesberger M., Summerfield A., Doherr M. G., Zurbriggen A., Griot C. 2005; Canine distemper virus-induced depletion of uninfected lymphocytes is associated with apoptosis. Vet Immunol Immunopathol 104:33–44 [CrossRef]
    [Google Scholar]
  57. Servet-Delprat C., Vidalain P.-O., Valentin H., Rabourdin-Combe C. 2003; Measles virus and dendritic cell functions: how specific response cohabits with immunosuppression. Curr Top Microbiol Immunol 276:103–123
    [Google Scholar]
  58. Stolte M., Haas L., Wamwayi H. M., Barrett T., Wohlsein P. 2002; Induction of apoptotic cellular death in lymphatic tissues of cattle experimentally infected with different strains of rinderpest virus. J Comp Pathol 127:14–21 [CrossRef]
    [Google Scholar]
  59. Sun X., Burns J. B., Howell J. M., Fujinami R. S. 1998; Suppression of antigen-specific T cell proliferation by measles virus infection: role of a soluble factor in suppression. Virology 246:24–33 [CrossRef]
    [Google Scholar]
  60. tenOever B. R., Servant M. J., Grandvaux N., Lin R., Hiscott J. 2002; Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J Virol 76:3659–3669 [CrossRef]
    [Google Scholar]
  61. Toba K., Winton E. F., Koike T., Shibata A. 1995; Simultaneous three-color analysis of the surface phenotype and DNA–RNA quantitation using 7-amino-actinomycin D and pyronin Y. J Immunol Methods 182:193–207 [CrossRef]
    [Google Scholar]
  62. Tsubata T. 1999; Co-receptors on B lymphocytes. Curr Opin Immunol 11:249–255 [CrossRef]
    [Google Scholar]
  63. Valentin H., Azocar O., Horvat B., Williems R., Garrone R., Evlashev A., Toribio M. L., Rabourdin-Combe C. 1999; Measles virus infection induces terminal differentiation of human thymic epithelial cells. J Virol 73:2212–2221
    [Google Scholar]
  64. van Binnendijk R. S., Poelen M. C., de Vries P., Voorma H. O., Osterhaus A. D., Uytdehaag F. G. 1989; Measles virus-specific human T cell clones. Characterization of specificity and function of CD4+ helper/cytotoxic and CD8+ cytotoxic T cell clones. J Immunol 142:2847–2854
    [Google Scholar]
  65. Wang M., Libbey J. E., Tsunoda I., Fujinami R. S. 2003; Modulation of immune system function by measles virus infection. II. Infection of B cells leads to the production of a soluble factor that arrests uninfected B cells in G0/G1 . Viral Immunol 16:45–55 [CrossRef]
    [Google Scholar]
  66. Yao Z. Q., Eisen-Vandervelde A., Ray S., Hahn Y. S. 2003; HCV core/gC1qR interaction arrests T cell cycle progression through stabilization of the cell cycle inhibitor p27Kip1. Virology 314:271–282 [CrossRef]
    [Google Scholar]
  67. Zhang X., Glendening C., Linke H., Parks C. L., Brooks C., Udem S. A., Oglesbee M. 2002; Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J Virol 76:8737–8746 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80791-0
Loading
/content/journal/jgv/10.1099/vir.0.80791-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error