Canine distemper virus selectively inhibits apoptosis progression in infected immune cells

Journal of Virology

Volumn 83, Issue 12, 2009, Pages 6279-6287

  Pillet, Stéphane ^a   Von Messling, Veronika ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW; CANINE DISTEMPER MORBILLIVIRUS; CELL CYCLE; CELL DIVISION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; FERRET; IMMUNOCOMPETENT CELL; IN VITRO STUDY; LEUKOPENIA; MALE; MESENTERY LYMPH NODE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SPLEEN; THYMUS; VIRUS CULTURE; VIRUS INFECTION; ANIMAL; CELL LINE; CELL SURVIVAL; DOG; DOG DISEASE; IMMUNOLOGY; LYMPH NODE; MONONUCLEAR CELL; TIME; VIROLOGY;

CANINE DISTEMPER VIRUS; MORBILLIVIRUS; MUSTELA;

ANIMALS; APOPTOSIS; BONE MARROW; CELL CYCLE; CELL LINE; CELL SURVIVAL; DISTEMPER; DISTEMPER VIRUS, CANINE; DOGS; FERRETS; LEUKOCYTES, MONONUCLEAR; LEUKOPENIA; LYMPH NODES; MALE; SPLEEN; THYMUS GLAND; TIME FACTORS;

EID: 66149126522     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00050-09     Document Type: Article

References (42)

1. Albert, M. L. 2004. Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat. Rev. Immunol. 4:223-231.
2. Auwaerter, P. G., P. A. Rota, W. R. Elkins, R. J. Adams, T. DeLozier, Y. Shi, W. J. Bellini, B. R. Murphy, and D. E. Griffin. 1999. Measles virus infection in rhesus macaques: altered immune responses and comparison of the virulence of six different virus strains. J. Infect. Dis. 180:950-958.
3. Barrett, T. 1999. Morbillivirus infections, with special emphasis on morbilliviruses of carnivores. Vet. Microbiol. 69:3-13.
4. Beckford, A. P., R. O. Kaschula, and C. Stephen. 1985. Factors associated with fatal cases of measles. A retrospective autopsy study. S. Afr. Med. J. 68:858-863.
5. Beineke, A., C. Puff, F. Seehusen, and W. Baumgartner. 2009. Pathogenesis and immunopathology of systemic and nervous canine distemper. Vet. Immunol. Immunopathol. 127:1-18.
6. Benedict, C. A., P. S. Norris, and C. F. Ware. 2002. To kill or be killed: viral evasion of apoptosis. Nat. Immunol. 3:1013-1018.
7. Cruz, C. D., H. Palosaari, J. P. Parisien, P. Devaux, R. Cattaneo, T. Ouchi, and C. M. Horvath. 2006. Measles virus V protein inhibits p53 family member p73. J. Virol. 80:5644-5650. (Pubitemid 43752811)
8. de Swart, R. L., M. Ludlow, L. de Witte, Y. Yanagi, G. van Amerongen, S. McQuaid, S. Yuksel, T. B. Geijtenbeek, W. P. Duprex, and A. D. Osterhaus. 2007. Predominant infection of CD150+ lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog. 3:1771-1781. (Pubitemid 350291611)
9. Engelking, O., L. M. Fedorov, R. Lilischkis, V. ter Meulen, and S. Schneider-Schaulies. 1999. Measles virus-induced immunosuppression in vitro is associated with deregulation of G1 cell cycle control proteins. J. Gen. Virol. 80:1599-1608.
10. Esolen, L. M., S. W. Park, J. M. Hardwick, and D. E. Griffin. 1995. Apoptosis as a cause of death in measles virus-infected cells. J. Virol. 69:3955-3958.
11. Fadok, V. A., D. L. Bratton, D. M. Rose, A. Pearson, R. A. Ezekewitz, and P. M. Henson. 2000. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85-90. (Pubitemid 30321820)
12. 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.
13. Gauvrit, A., S. Brandler, C. Sapede-Peroz, N. Boisgerault, F. Tangy, and M. Gregoire. 2008. Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumor-specific CD8 response. Cancer Res. 68:4882-4892.
14. Grais, R. F., C. Dubray, S. Gerstl, J. P. Guthmann, A. Djibo, K. D. Nargaye, J. Coker, K. P. Alberti, A. Cochet, C. Ihekweazu, N. Nathan, L. Payne, K. Porten, D. Sauvageot, B. Schimmer, F. Fermon, M. E. Burny, B. S. Hersh, and P. J. Guerin. 2007. Unacceptably high mortality related to measles epidemics in Niger, Nigeria, and Chad. PLoS Med. 4:e16.
15. Griffin, D. E. 2001. Measles virus, p. 1401-1441. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol.1. Lippincott Williams & Wilkins, Philadelphia, PA.
16. Ito, M., T. Yamamoto, M. Watanabe, T. Ihara, H. Kamiya, and M. Sakurai. 1996. Detection of measles virus-induced apoptosis of human monocytic cell line (THP-1) by DNA fragmentation ELISA. FEMS Immunol. Med. Microbiol. 15:115-122.
17. Jacobson, M. D., J. F. Burne, and M. C. Raff. 1994. Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J. 13:1899-1910. (Pubitemid 24124523)
18. Kajita, M., H. Katayama, T. Murata, C. Kai, M. Hori, and H. Ozaki. 2006. Canine distemper virus induces apoptosis through caspase-3 and -8 activation in vero cells. J. Vet. Med. B 53:273-277.
19. Laine, D., J. M. Bourhis, S. Longhi, M. Flacher, L. Cassard, B. Canard, C. Sautes-Fridman, C. Rabourdin-Combe, and H. Valentin. 2005. Measles virus nucleoprotein induces cell-proliferation arrest and apoptosis through NTAIL-NR and NCORE-FcgammaRIIB1 interactions, respectively. J. Gen. Virol. 86:1771-1784.
20. Laine, D., M. C. Trescol-Biemont, S. Longhi, G. Libeau, J. C. Marie, P. O. Vidalain, O. Azocar, A. Diallo, B. Canard, C. Rabourdin-Combe, and H. Valentin. 2003. Measles virus (MV) nucleoprotein binds to a novel cell surface receptor distinct from FcγRII via its C-terminal domain: role in MV-induced immunosuppression. J. Virol. 77:11332-11346. (Pubitemid 37271632)
21. Liu, T. C., and D. Kirn. 2008. Gene therapy progress and prospects cancer: oncolytic viruses. Gene Ther. 15:877-884. (Pubitemid 351791475)
22. McChesney, M. B., A. Altman, and M. B. Oldstone. 1988. Suppression of T lymphocyte function by measles virus is due to cell cycle arrest in G1. J. Immunol. 140:1269-1273. (Pubitemid 18088600)
23. Niewiesk, S., H. Ohnimus, J. J. Schnorr, M. Gotzelmann, S. Schneider-Schaulies, C. Jassoy, and V. ter Meulen. 1999. Measles virus-induced immunosuppression in cotton rats is associated with cell cycle retardation in uninfected lymphocytes. J. Gen. Virol. 80:2023-2029.
24. Ohno, S., N. Ono, F. Seki, M. Takeda, S. Kura, T. Tsuzuki, and Y. Yanagi. 2007. Measles virus infection of SLAM (CD150) knock-in mice reproduces tropism and immunosuppression in human infection. J. Virol. 81:1650-1659. (Pubitemid 46214440)
25. Okada, H., F. Kobune, T. A. Sato, T. Kohama, Y. Takeuchi, T. Abe, N. Takayama, T. Tsuchiya, and M. Tashiro. 2000. Extensive lymphopenia due to apoptosis of uninfected lymphocytes in acute measles patients. Arch. Virol. 145:905-920.
26. Ryon, J. J., W. J. Moss, M. Monze, and D. E. Griffin. 2002. Functional and phenotypic changes in circulating lymphocytes from hospitalized zambian children with measles. Clin. Diagn. Lab. Immunol. 9:994-1003.
27. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965-975.
28. 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.
29. Schneider-Schaulies, J., and S. Schneider-Schaulies. 2008. Receptor interactions, tropism, and mechanisms involved in morbillivirus-induced immunomodulation. Adv. Virus Res. 71:173-205.
30. Schnorr, J. J., M. Seufert, J. Schlender, J. Borst, I. C. Johnston, V. ter Meulen, and S. Schneider-Schaulies. 1997. Cell cycle arrest rather than apoptosis is associated with measles virus contact-mediated immunosuppression in vitro. J. Gen. Virol. 78:3217-3226.
31. Schobesberger, M., A. Summerfield, M. G. Doherr, A. Zurbriggen, and C. Griot. 2005. Canine distemper virus-induced depletion of uninfected lymphocytes is associated with apoptosis. Vet. Immunol. Immunopathol. 104:33-44.
32. Servet-Delprat, C., P. O. Vidalain, H. Valentin, and C. Rabourdin-Combe. 2003. Measles virus and dendritic cell functions: how specific response cohabits with immunosuppression. Curr. Top. Microbiol. Immunol. 276:103-123.
33. Stolte, M., L. Haas, H. M. Wamwayi, T. Barrett, and P. Wohlsein. 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.
34. Sun, M., T. A. Rothermel, L. Shuman, J. A. Aligo, S. Xu, Y. Lin, R. A. Lamb, and B. He. 2004. Conserved cysteine-rich domain of paramyxovirus simian virus 5 V protein plays an important role in blocking apoptosis. J. Virol. 78:5068-5078.
35. Takeuchi, K., T. Komatsu, Y. Kitagawa, K. Sada, and B. Gotoh. 2008. Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J. Virol. 82:10102-10110.
36. Tatsuo, H., N. Ono, and Y. Yanagi. 2001. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 75: 5842-5850. (Pubitemid 32553114)
37. Thot, A. M., P. Devaux, R. Cattaneo, and C. E. Samuel. 2009. Protein kinase PKR mediates the apoptosis induction and growth restriction phenotypes of C protein-deficient measles virus. J. Virol. 83:961-968.
38. von Messling, V., D. Milosevic, and R. Cattaneo. 2004. Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc. Natl. Acad. Sci. USA 101:14216-14221.
39. von Messling, V., C. Springfeld, P. Devaux, and R. Cattaneo. 2003. A ferret model of canine distemper virus virulence and immunosuppression. J. Virol. 77:12579-12591. (Pubitemid 37430654)
40. von Messling, V., N. Svitek, and R. Cattaneo. 2006. Receptor (SLAM [CD150]) recognition and the V protein sustain swift lymphocyte-based invasion of mucosal tissue and lymphatic organs by a morbillivirus. J. Virol. 80:6084-6092. (Pubitemid 43849186)
41. Vuorinen, T., P. Peri, and R. Vainionpaa. 2003. Measles virus induces apoptosis in uninfected bystander T cells and leads to granzyme B and caspase activation in peripheral blood mononuclear cell cultures. Eur. J. Clin. Investig. 33:434-442.
42. Wilson, R. L., S. M. Fuentes, P. Wang, E. C. Taddeo, A. Klatt, A. J. Henderson, and B. He. 2006. Function of small hydrophobic proteins of paramyxovirus. J. Virol. 80:1700-1709.