Skip to content
1887

Journal of General Virology header logo Journal of General Virology

Volume 76, Issue 11

Efficient replication of human immunodeficiency virus type 1 and measles virus in a human-to-mouse graft versus host disease model permits immunization research No Access

Abstract

An acute graft versus host disease (GvHD) murine model was developed to study the pathogenic and protective mechanisms against viruses that replicate in cells of the human immune system. The model allowed efficient replication of lymphotropic, macrophage and amphitropic strains of human immunodeficiency virus type 1 (HIV-1) and measles virus (MV). Cytopathic lymphotropic strains of HIV-1 and a wild-type MV strain replicated in a ‘burst’-like manner, whereas a non-cytopathic lymphotropic HIV-1 strain and all macrophage-tropic HIV-1 strains caused persistent infection of the graft. The replication kinetics of infection with these viruses were highly reproducible and were very similar to those observed in natural infection of humans. Infection with these viruses, with the exception of HIV-1, led to a significant delay and abrogation of the GvHD, indicating a direct immunosuppressive effect. Interestingly, infection with the lymphotropic HIV-1 strain was rapidly and spontaneously abrogated. The model was also shown to be suitable for the evaluation of passive immunization strategies. Administration of a combination of antibodies against the HIV-1 V3 loop and the HIV-1 CD4 binding sites prevented subsequent infection with HIV-1. In contrast, administration of CD4 binding site specific human monoclonal antibody at a concentration that would neutralize the virus enhanced infection with HIV-1. The model also allowed evaluation of immunization studies. Immunization with a live attenuated measles vaccine resulted in protection from a wild-type MV challenge, whereas immunization with a subunit candidate vaccine appeared to give partial protection.

  • Received:
  • Accepted:
  • Published Online:
© Journal of General Virology 1995
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-76-11-2707
1995-11-01
2025-03-21
Loading full text...

Full text loading...

References

  1. Ada G. 1993; Towards phase III trials for candidate vaccine. Nature 364:489–490
     [Google Scholar]
  2. Aldrovandi G. M., Feuer G., Gao L., Jamieson B., Kristeva M., Chen I. S., Zack J. A. 1993; The SCID-hu mouse as a model for HIV-1 infection. Nature 363:732–736
     [Google Scholar]
  3. Bonyhadi M. L., Rabin L., Salimi S., Brown D. A., Kosek J., McCune J. M., Kaneshima H. 1993; HIV induces thymus depletion in vivo . Nature 363:728–732
     [Google Scholar]
  4. Cheng-Mayer C., Quiroga M., Tung J. W., Dina D., Levy J. A. 1990; Viral determinants of human immunodeficiency virus type 1 T cell macrophage tropism, cytopathogenicity, and CD4 antigen modulation. Journal of Virology 64:4390–4398
     [Google Scholar]
  5. Devash Y., Matthews T. J., Drummond J. E., Javaherian K., Waters D. J., Arthur L. O., Blattner W. A., Rusche J. R. 1990; C-terminal fragments of gpl20 and synthetic peptides from five HTLV-III strains: prevalence of antibodies to the HTLV-III-MN isolate in infected individuals. AIDS Research and Human Retroviruses 6:307–316
     [Google Scholar]
  6. Embretson J., Zupancic M., Ribas J. L., Burke A., Racz P., Tenner-Racz K., Haase A. T. 1993; Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 362:359–362
     [Google Scholar]
  7. Gallo R. C., Salahuddin S. Z., Popovic M., Sheared G. M., Kaplan M., Haynes B. F., Palker T. J., Redfield R., Oleske J., Safai B., White G., Foster P., Markham P. D. 1984; Fragment detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk from AIDS. Science 224:500–503
     [Google Scholar]
  8. Gorny M. K., Xu J. Y., Karwowska S., Buchbinder A., Zolla-Pazner S. 1993; Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. Journal of Immunology 150:635–643
     [Google Scholar]
  9. Groenink M., Fouchier R. A., Degoede R. E., Dewolf F., Gruters R. A., Cuypers H. T., Huisman H. G., Tersmette M. 1990; Phenotypic heterogeneity in a panel of infectious molecular human immunodeficiency virus type 1 clones derived from a single individual. Journal of Virology 65:1968–1975
     [Google Scholar]
  10. Hesselton R. M., Koup R. A., Cromwell M. A., Graham B. S., Johns M., Sullivan J. L. 1993; Human peripheral blood xenografts in the SCID mouse: characterization of immunologic reconstitution. Journal of Infectious Diseases 168:630–640
     [Google Scholar]
  11. Hoffmann-Fezer G., Kranz B., Gall C., Thierfelder S. 1992; Peritoneal sanctuary for human lymphopoiesis in SCID mice injected with human peripheral blood lymphocytes from Epstein-Barr virus-negative donors. European Journal of Immunology 22:3161–3166
     [Google Scholar]
  12. Hoffmann-Fezer G., Gall C., Zengerle U., Kranz B., Thierfelder S. 1993; Immunohistology and immunocytology of human T-cell chimerism and graft-versus-host disease in SCID mice. Blood 12:3440–3448
     [Google Scholar]
  13. Huppes W., Degeus B., Zurcher C., VanBekkum D. W. 1992; Acute human vs. mouse graft vs-host disease in normal and immunodeficient mice. European Journal of Immunology 22:197–206
     [Google Scholar]
  14. Huppes W., Fickenscher H., ’tHart B. A., Fleckenstein B. 1994; Cytokine dependence of human to mouse graft vs-host disease. Scandinavian Journal of Immunology 40:26–36
     [Google Scholar]
  15. Krowka J. F., Sarin S., Namikawa R., McCune J. M., Kaneshima H. 1991; Characteristics of human lymphocytes in the peripheral blood of SCID-hu mice. Journal of Immunology 146:3751–3756
     [Google Scholar]
  16. McCune J. M., Péault B., Streeter P. R., Rabin L. 1991; Preclinical evaluation of human hematolymphoid function in the SCID-hu mouse. Immunological Reviews 124:45–63
     [Google Scholar]
  17. Mosier D. E., Gulizia R. J., Baird S. M., Wilson D. B. 1988; Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature 335:256–259
     [Google Scholar]
  18. Mosier D. E., Gulizia R. J., Baird S. M., Wilson D. B., Spector D. H., Spector S. A. 1991; Human immunodeficiency virus infection of human-PBL-SCID mice. Science 251:791–794
     [Google Scholar]
  19. Mosier D. E., Gulizia R. J., MacIsaac P. D., Torbett B. E., Levy J. A. 1993a; Rapid loss of CD4+T cells in human-PBL-SCID mice by noncytopathogenic HIV isolates. Science 260:689
     [Google Scholar]
  20. Mosier D. E., Gulizia R. J., MacIsaac P. D., Corey L., Greenberg P. D. 1993b; Resistance to human immunodeficiency virus 1 infection of SCID mice reconstituted with peripheral blood leukocytes from donors vaccinated with vaccinia gpl60 and recombinant gpl60. Proceedings of the National Academy of Sciences, USA 90:2443–2447
     [Google Scholar]
  21. Namikawa R., Kaneshima H., Lieberman M., Weissman I. L., McCune J. M. 1988; Infection of the SCID-hu mouse by HIV-1. Science 242:1684–1686
     [Google Scholar]
  22. Nara P., Hatch W., Kessler J., Kelliher J., Carter S. 1989; The biology of human immunodeficiency virus-1 IIIB infection in the chimpanzee: in vivo and in vitro correlation. Journal of Medical Primatology 18:343–355
     [Google Scholar]
  23. Nick S., Fickenscher H., Biesinger B., Born G., Jahn G., Fleckenstein B. 1993; Herpes virus saimiri transformed human T cell lines: a permissive system for human immunodeficiency viruses. Virology 194:875–877
     [Google Scholar]
  24. Nonoyama S., Smith F. O., Ochs H. D. 1993; Specific antibody production to a recall or a neoantigen by SCID mice reconstituted with human peripheral blood lymphocytes. Journal of Immunology 151:3894–901
     [Google Scholar]
  25. Popovic M., Sarngadharan M. G., Read E., Gallo R. C. 1984; Detection, isolation, and continous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 224:497–500
     [Google Scholar]
  26. Prince A. M., Horowitz B., Baker L., Shulman R. W., Ralph H., Valinsky J., Cundell A., Brotman B., Boehle W., Rey F., Reesink H., Lelie N., Tersmette M., Miedema F., Barbosa L., Nmeo G., Nastala C. L., Langlois A. J., Allan J. S., Lee D. R., Eichberg J. W. 1988; Failure of a human immunodeficiency virus (HIV) immune globulin to protect chimpanzees against experimental challenge with HIV. Proceedings of the National Academy of Sciences, USA 85:6944–6948
     [Google Scholar]
  27. Prince A. M., Reesink H., Pascual D., Horowitz B., Hewlett I., Murthy K. K., Cobb K. E., Eichberg J. W. 1991; Prevention of HIV infection by passive immunization with HIV immunoglobulin. Aids Research and Human Retroviruses 12:971–973
     [Google Scholar]
  28. Safrit J. T., Fung M. S., Andrews C. A., Braun D. G., Sun W. N., Chang T. W., Koup R. A. 1993; Hu-PBL-SCID mice can be protected from HIV-1 infection by passive transfer of monoclonal antibody to the principal neutralizing determinant of envelope gpl20. AIDS 7:15–21
     [Google Scholar]
  29. Saxinger C., Alter H. J., Eichberg J. W., Fauci A. S., Robey W. G., Gallo R. C. 1987; Stages in the progression of HIV infection in chimpanzees. AIDS Research and Human Retroviruses 3:375–385
     [Google Scholar]
  30. Schuitemaker G. H., Groenink M., Meyaard L., Kootstra N. A., Fouchier R. A. M., Gruters R. A., Huisman H. G., Tersmette M., Miedema F. 1993a; Early replication steps but not cell type-specific signalling of the viral long terminal repeat determine HIV-1 monocytotropism. AIDS Research and Human Retroviruses 9:669–675
     [Google Scholar]
  31. Schuitemaker G. H., Meyaard L., Kootstra N. A., Dubbes R., Otto S. A., Tersmette M., Heeney J. L., Miedema F. 1993b; Lack of T cell dysfunction and programmed cell death in human immunodeficiency virus type 1-infected chimpanzees correlates with absence of monocytotropic variants. Journal of Infectious Diseases 168:1140–1147
     [Google Scholar]
  32. Schutten M., McKnight A., Huisman R. C., Thali M., McKeating J. A., Sodroski J., Goudsmit J., Osterhaus A. D. M. E. 1993; Further characterization of an antigenic site of HIV-1 gpl20 recognized by virus neutralizing human monoclonal antibodies. AIDS 7:919–923
     [Google Scholar]
  33. Simpson E., Farrant J., Chandler P. 1991; Phenotypic and functional studies of human peripheral blood lymphocytes engrafted in SCID mice. Immunological Reviews 124:197–113
     [Google Scholar]
  34. Spear G. T., Sullivan B. L., Takefman D. M., Landay A. L., Lint T. F. 1991; Human immunodeficiency virus (HlV)-infected cells and free virus directly activate the classical complement pathway in rabbit, mouse and guinea-pig sera: activation results in virus neutralization by virolysis. Immunology 73:377–382
     [Google Scholar]
  35. Tary-Lehmann M., Saxon A. 1992; Human mature T cells that are anergic in vivo prevail in SCID mice reconstituted with human peripheral blood. Journal of Experimental Medicine 175:503–516
     [Google Scholar]
  36. Teeuwsen V. J., Siebelink K. H., Crush-Stanton S., Swerdlow B., Schalken J. J., Goudsmit J., Vandenakker R., Stukart M. J., UytdeHaag F. G. C. M., Osterhaus A. D. M. E. 1990; Production and characterization of a human monoclonal antibody, reactive with a conserved epitope on gp41 of human immunodeficiency virus type 1. AIDS Research and Human Retroviruses 6:381–392
     [Google Scholar]
  37. Torbett B. E., Picchio G., Mosier D. E. 1991; Hu-PBL-SCID mice: a model for human immune function, AIDS and lympho-magenesis. Immunological Reviews 124:139–165
     [Google Scholar]
  38. VanBinnendijk R. S., Poelen M. C. M., Kuijpers K. C., Osterhaus A. D. M. E., UytdeHaag F. G. C. M. 1990; The predominance of CD8+ T cells after infection with measles virus suggests a role for CD8+ class I MHC-restricted cytotoxic T lymphocytes (CTL) in recovery from measles. Clonal analyses of human CD8+ class I MHC-restricted CTL. Journal of Immunology 144:2394–2399
     [Google Scholar]
  39. VanBinnendijk R. S., VanBaalen C. A., Poelen M. C. M., DeVries P., Boes J., Cerundolo V., Osterhaus A. D. M. E., UytdeHaag F. G. C. M. 1992; Measles virus transmembrane fusion protein synthesized de novo or presented in immuno-stimulating complexes is endogenously processed for HLA class I- and class Il-restricted cytotoxic T cell recognition. Journal of Experimental Medicine 176:119–128
     [Google Scholar]
  40. VanBinnendijk R. S., Heijden R. W. J., VanAmerongen G., UytdeHaag F. G. C. M., Osterhaus A. D. M. E. 1994; Virus replication and development of specific immunity in macaques after infection with different measles strains. Journal of Infectious Diseases 170:443–447
     [Google Scholar]
  41. VanDeGriend R. J., VanKrimpen B. A., Bol S J. L., Thompson A., Bolhuis R. L. H. 1984; Rapid expansion of human T cell clones: growth promotion by a heat labile serum component and by various types of feeder cells. Journal of Immunological Methods 66:285–298
     [Google Scholar]
  42. Vittecoq D., Mattlinger B., Barre-Sinoussi F., Courouce A. M., Rouzioux C., Doinel C., Bary M., Viard J. P., Bach J. F., Rouger P., Lefrere J. J. 1992; Passive immunotherapy in AIDS: a randomized trial of human immunodeficiency virus-positive transfusions of plasma rich in p24 antibodies versus transfusions of seronegative plasma. Journal of Infectious Diseases 165:364–368
     [Google Scholar]
  43. Williams S. S., Umemoto T., Kida H., Repasky E. A., Bankert R. B. 1992; Engraftment of human peripheral blood leukocytes into severe combined immunodeficient mice results in the long term and dynamic production of human xenoreactive antibodies. Journal of Immunology 149:2830–2836
     [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-76-11-2707
Loading
Efficient replication of human immunodeficiency virus type 1 and measles virus in a human-to-mouse graft versus host disease model permits immunization research
J. Gen. Virol. 76, 2707 (1995); https://doi.org/10.1099/0022-1317-76-11-2707
/content/journal/jgv/10.1099/0022-1317-76-11-2707
/content/journal/jgv/10.1099/0022-1317-76-11-2707
Loading

Data & Media loading...

Most cited 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