1887

Abstract

Both rhesus and cynomolgus macaques have been used as animal models for measles vaccination and immunopathogenesis studies. A number of studies have suggested that experimental measles virus (MV) infection induces more-characteristic clinical features in rhesus than in cynomolgus monkeys. In the present study, both macaque species were infected with two different wild-type MV strains and clinical, virological and immunological parameters were compared. The viruses used were a genotype C2 virus isolated in The Netherlands in 1991 (MV-Bil) and a genotype B3 virus isolated from a severe measles case in Sudan in 1997 (MV-Sudan). Following infection, all rhesus monkeys developed a skin rash and conjunctivitis, which were less obvious in cynomolgus monkeys. Fever was either mild or absent in both species. Virus reisolation profiles from peripheral blood mononuclear cells and broncho-alveolar lavage cells and the kinetics of MV-specific IgM and IgG responses were largely identical in the two animal species. However, in animals infected with MV-Sudan, viraemia appeared earlier and lasted longer than in animals infected with MV-Bil. This was also reflected by the earlier appearance of MV-specific serum IgM antibodies after infection with MV-Sudan. Collectively, these data show that cynomolgus and rhesus macaques are equally susceptible to wild-type MV infection, although infection in the skin seems to follow a different course in rhesus macaques. MV-Sudan proved more pathogenic for non-human primates than MV-Bil, which may render it more suitable for use in future pathogenesis studies.

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2007-07-01
2019-11-17
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References

  1. Andres, O., Obojes, K., Kim, K. S., Ter Meulen, V. & Schneider-Schaulies, J. ( 2003; ). CD46- and CD150-independent endothelial cell infection with wild-type measles viruses. J Gen Virol 84, 1189–1197.[CrossRef]
    [Google Scholar]
  2. Auwaerter, P. G., Kaneshima, H., McCune, J. M., Wiegand, G. & Griffin, D. E. ( 1996; ). Measles virus infection of thymic epithelium in the SCID-hu mouse leads to thymocyte apoptosis. J Virol 70, 3734–3740.
    [Google Scholar]
  3. Auwaerter, P. G., Rota, P. A., Elkins, W. R., Adams, R. J., DeLozier, T., Shi, Y., Bellini, W. J., Murphy, B. R. & Griffin, D. E. ( 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.[CrossRef]
    [Google Scholar]
  4. Bennett, J. V., Fernandez de Castro, J., Valdespino-Gomez, J. L., De Lourdes Garcia-Garcia, M., Islas-Romero, R., Echaniz-Aviles, G., Jimenez-Corona, A. & Sepulveda-Amor, J. ( 2002; ). Aerosolized measles and measles-rubella vaccines induce better measles antibody booster responses than injected vaccines: randomized trials in Mexican schoolchildren. Bull World Health Organ 80, 806–812.
    [Google Scholar]
  5. De Swart, R. L., Vos, H. W., UytdeHaag, F. G. C. M., Osterhaus, A. D. M. E. & Van Binnendijk, R. S. ( 1998; ). Measles virus fusion protein- and hemagglutinin-transfected cell lines are a sensitive tool for the detection of specific antibodies by a FACS-measured immunofluorescence assay. J Virol Methods 71, 35–44.[CrossRef]
    [Google Scholar]
  6. De Swart, R. L., Wertheim-van Dillen, P. M. E., Van Binnendijk, R. S., Muller, C. P., Frenkel, J. & Osterhaus, A. D. M. E. ( 2000; ). Measles in a Dutch hospital introduced by an immunocompromised infant from Indonesia infected with a new genotype virus. Lancet 355, 201–202.[CrossRef]
    [Google Scholar]
  7. De Swart, R. L., Kuiken, T., Fernandez de Castro, J., Papania, M. J., Bennett, J. V., Valdespino, J. L., Minor, P., Witham, C., Yüksel, S. & other authors ( 2006; ). Aerosol measles vaccination in macaques: preclinical studies of immune responses and safety. Vaccine 24, 6424–6436.[CrossRef]
    [Google Scholar]
  8. Duke, T. & Mgone, C. S. ( 2003; ). Measles: not just another viral exanthem. Lancet 361, 763–773.[CrossRef]
    [Google Scholar]
  9. El Mubarak, H. S., Van de Bildt, M. W. G., Mustafa, O. A., Vos, H. W., Mukhtar, M. M., Groen, J., El Hassan, A. M., Niesters, H. G. M., Ibrahim, S. A. & other authors ( 2000; ). Serological and virological characterization of clinically diagnosed cases of measles in suburban Khartoum. J Clin Microbiol 38, 987–991.
    [Google Scholar]
  10. El Mubarak, H. S., Ibrahim, S. A., Vos, H. W., Mukhtar, M. M., Mustafa, O. A., Wild, T. F., Osterhaus, A. D. M. E. & De Swart, R. L. ( 2004; ). Measles virus protein-specific IgM, IgA, and IgG subclass responses during the acute and convalescent phase of infection. J Med Virol 72, 290–298.[CrossRef]
    [Google Scholar]
  11. Griffin, D. E. ( 2001; ). Measles virus. In Fields Virology, 4th edn, pp. 1401–1441. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
  12. Hashimoto, K., Ono, N., Tatsuo, H., Minagawa, H., Takeda, M., Takeuchi, K. & Yanagi, Y. ( 2002; ). SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J Virol 76, 6743–6749.[CrossRef]
    [Google Scholar]
  13. Ibrahim, S. A., Mustafa, O. M., Mukhtar, M. M., Saleh, E. A., El Mubarak, H. S., Abdallah, A., El Hassan, A. M., Osterhaus, A. D. M. E., Groen, J. & other authors ( 2002; ). Measles in suburban Khartoum: an epidemiological and clinical study. Trop Med Int Health 7, 442–449.[CrossRef]
    [Google Scholar]
  14. Kobune, F., Takahashi, H., Terao, K., Ohkawa, T., Ami, Y., Suzaki, Y., Nagata, N., Sakata, H., Yamanouchi, K. & Kai, C. ( 1996; ). Nonhuman primate models of measles. Lab Anim Sci 46, 315–320.
    [Google Scholar]
  15. McChesney, M. B., Miller, C. J., Rota, P. A., Zhu, Y., Antipa, L., Lerche, N. W., Ahmed, R. & Bellini, W. J. ( 1997; ). Experimental measles. I. Pathogenesis in the normal and the immunized host. Virology 233, 74–84.[CrossRef]
    [Google Scholar]
  16. Naniche, D., Varior-Krishnan, G., Cervoni, F., Wild, T. F., Rossi, B., Rabourdin-Combe, C. & Gerlier, D. ( 1993; ). Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67, 6025–6032.
    [Google Scholar]
  17. Niewiesk, S. ( 2001; ). Studying experimental measles virus vaccines in the presence of maternal antibodies in the cotton rat model (Sigmodon hispidus). Vaccine 19, 2250–2253.[CrossRef]
    [Google Scholar]
  18. Orenstein, W. A., Hinman, A. R. & Strebel, P. J. ( 2006; ). Measles: the need for 2 opportunities for prevention. Clin Infect Dis 42, 320–321.[CrossRef]
    [Google Scholar]
  19. Polack, F. P., Auwaerter, P. G., Lee, S. H., Nousari, H. C., Valsamakis, A., Leiferman, K. M., Diwan, A., Adams, R. J. & Griffin, D. E. ( 1999; ). Production of atypical measles in rhesus macaques: evidence for disease mediated by immune complex formation and eosinophils in the presence of fusion-inhibiting antibody. Nat Med 5, 629–634.[CrossRef]
    [Google Scholar]
  20. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  21. Rimmelzwaan, G. F., Kuiken, T., Van Amerongen, G., Bestebroer, T. M., Fouchier, R. A. M. & Osterhaus, A. D. M. E. ( 2001; ). Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol 75, 6687–6691.[CrossRef]
    [Google Scholar]
  22. Sellin, C. I., Davoust, N., Guillaume, V., Baas, D., Belin, M. F., Buckland, R., Wild, T. F. & Horvat, B. ( 2006; ). High pathogenicity of wild-type measles virus infection in CD150 (SLAM) transgenic mice. J Virol 80, 6420–6429.[CrossRef]
    [Google Scholar]
  23. Stittelaar, K. J., Wyatt, L. S., De Swart, R. L., Vos, H. W., Groen, J., Van Amerongen, G., Van Binnendijk, R. S., Rozenblatt, S., Moss, B. & Osterhaus, A. D. M. E. ( 2000; ). Protective immunity in macaques vaccinated with a modified vaccinia virus Ankara-based measles virus vaccine in the presence of passively acquired antibodies. J Virol 74, 4236–4243.[CrossRef]
    [Google Scholar]
  24. Stittelaar, K. J., De Swart, R. L. & Osterhaus, A. D. M. E. ( 2002; ). Vaccination against measles: a neverending story. Expert Rev Vaccines 1, 151–159.[CrossRef]
    [Google Scholar]
  25. Stittelaar, K. J., Van Amerongen, G., Kondova, I., Kuiken, T., van Lavieren, R. F., Pistoor, F. H. M., Niesters, H. G. M., van Doornum, G., van der Zeijst, B. A. M. & other authors ( 2005; ). Modified vaccinia virus Ankara protects macaques against respiratory challenge with monkeypox virus. J Virol 79, 7845–7851.[CrossRef]
    [Google Scholar]
  26. Tatsuo, H., Ono, N., Tanaka, K. & Yanagi, Y. ( 2000; ). SLAM (CDw150) is a cellular receptor for measles virus. Nature 406, 893–897.[CrossRef]
    [Google Scholar]
  27. Van Binnendijk, R. S., Van der Heijden, R. W. J., Van Amerongen, G., UytdeHaag, F. G. C. M. & Osterhaus, A. D. M. E. ( 1994; ). Viral replication and development of specific immunity in macaques after infection with different measles virus strains. J Infect Dis 170, 443–448.[CrossRef]
    [Google Scholar]
  28. Van Binnendijk, R. S., Van der Heijden, R. W. J. & Osterhaus, A. D. M. E. ( 1995; ). Monkeys in measles research. In Measles Virus, pp. 135–148. Edited by V. Ter Meulen & M. A. Billeter. Berlin: Springer-Verlag.
  29. Welstead, G. G., Iorio, C., Draker, R., Bayani, J., Squire, J., Vongpunsawad, S., Cattaneo, R. & Richardson, C. D. ( 2005; ). Measles virus replication in lymphatic cells and organs of CD150 (SLAM) transgenic mice. Proc Natl Acad Sci U S A 102, 16415–16420.[CrossRef]
    [Google Scholar]
  30. WHO ( 1998; ). Expanded Programme on Immunization (EPI). Standardization of the nomenclature for describing the genetic characteristics of wild-type measles viruses. Wkly Epidemiol Rec 73, 265–272.
    [Google Scholar]
  31. WHO ( 2004; ). Measles vaccines. Wkly Epidemiol Rec 79, 130–142.
    [Google Scholar]
  32. WHO ( 2005; ). New genotype of measles virus and update on global distribution of measles genotypes. Wkly Epidemiol Rec 80, 347–351.
    [Google Scholar]
  33. WHO ( 2006; ). Progress in reducing global measles deaths: 1999–2004. Wkly Epidemiol Rec 81, 90–94.
    [Google Scholar]
  34. Wyde, P. R., Ambrose, M. W., Voss, T. G., Meyer, H. L. & Gilbert, B. E. ( 1992; ). Measles virus replication in lungs of hispid cotton rats after intranasal inoculation. Proc Soc Exp Biol Med 201, 80–87.[CrossRef]
    [Google Scholar]
  35. Yanagi, Y., Takeda, M., Ohno, S. & Seki, F. ( 2006; ). Measles virus receptors and tropism. Jpn J Infect Dis 59, 1–5.
    [Google Scholar]
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