Lentivirus infections and mechanisms of disease resistance in chimpanzees

Frontiers in Bioscience

Volumn 8, Issue , 2003, Pages

  Rutjens, Erik ^a   Balla Jhagjhoorsingh, Sunita ^a   Verschoor, Ernst ^a   Bogers, Willy ^a   Koopman, Gerrit ^a   Heeney, Jonathan ^a  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

Author keywords

AIDS; Chimpanzee; HIV; Immunity; Resistance; Review; SIVcpz; T helper response

Indexed keywords

BIOCHEMICAL MARKER; CHEMOKINE; CYTOKINE; DNA VACCINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; CELLULAR IMMUNITY; CHIMPANZEE; CYTOTOXIC T LYMPHOCYTE; DISEASE COURSE; DISEASE RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMORAL IMMUNITY; IMMUNE RESPONSE; MOLECULAR DYNAMICS; NONHUMAN; RETROVIRUS INFECTION; REVIEW; VIRUS ISOLATION; VIRUS STRAIN;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS; MACACA; MACACA MULATTA; PAN (APE); PAN TROGLODYTES; PRIMATES; UNIDENTIFIED RETROVIRUS;

EID: 3242715285     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: None     Document Type: Review

References (96)

1. Olson M.V. & A. Varki: Sequencing the chimpanzee genome: insights into human evolution and disease. Nat Rev Genet 4, 1 20-8 (2003)
2. Wildman D.E.: A map of the common chimpanzee genome. Bioessays 24, 6 490-3 (2002)
3. Alter H.J., J.W. Eichberg, H. Masur, W.C. Saxinger, R. Gallo, A.M. Macher, H.C. Lane & A.S. Fauci: Transmission of HTLV-III infection from human plasma to chimpanzees: an animal model for AIDS. Science 226, 4674 549-52 (1984)
4. Fultz P.N., H.M. McClure, H. Daugharty, A. Brodie, C.R. McGrath, B. Swenson & D.P. Francis: Vaginal transmission of human immunodeficiency virus (HIV) to a chimpanzee. J Infect Dis 154, 5 896-900 (1986)
5. Fultz P.N., C. Greene, W. Switzer, B. Swenson, D. Anderson & H.M. McClure: Lack of transmission of human immunodeficiency virus from infected to uninfected chimpanzees. J Med Primatol 16, 6 341-7 (1987)
6. Fultz P.N., A. Srinivasan, C.R. Greene, D. Butler, R.B. Swenson & H.M. McClure: Superinfection of a chimpanzee with a second strain of human immunodeficiency virus. J Virol 61, 12 4026-9 (1987)
7. Pischinger K., K. Zimmermann, M.M. Eibl & J.W. Mannhalter: Comparison of early events during infection of human and chimpanzee peripheral blood mononuclear cells with HIV-1. Arch Virol 143, 11 2065-76 (1998)
8. Goudsmit J., L. Smit, W.J. Krone, M. Bakker, J. van der Noordaa, C.J. Gibbs, L.G. Epstein & D.C. Gajdusek: IgG response to human immunodeficiency virus in experimentally infected chimpanzees mimics the IgG response in humans. J Infect Dis 155, 2 327-31 (1987)
9. Nara P.L., W.G. Robey, L.O. Arthur, D.M. Asher, A.V. Wolff, C.J. Gibbs, Jr., D.C. Gajdusek & P.J. Fischinger: Persistent infection of chimpanzees with human immunodeficiency virus: serological responses and properties of reisolated viruses. J Virol 61, 10 3173-80 (1987)
10. Nara P.L., W.G. Robey, M.A. Gonda, S.G. Carter & P.J. Fischinger: Absence of cytotoxic antibody to human immunodeficiency virus-infected cells in humans and its induction in animals after infection or immunization with purified envelope glycoprotein gp120. Proc Natl Acad Sci U S A 84, 11 3797-801 (1987)
11. Arthur L.O., S.W. Pyle, P.L. Nara, J.W. Bess, Jr., M.A. Gonda, J.C. Kelliher, R.V. Gilden, W.G. Robey, D.P. Bolognesi, R.C. Gallo & et al.: Serological responses in chimpanzees inoculated with human immunodeficiency virus glycoprotein (gp120) subunit vaccine. Proc Natl Acad Sci U S A 84, 23 8583-7 (1987)
12. Hu S.L., P.N. Fultz, H.M. McClure, J.W. Eichberg, E.K. Thomas, J. Zarling, M.C. Singhal, S.G. Kosowski, R.B. Swenson, D.C. Anderson & et al.: Effect of immunization with a vaccinia-HIV env recombinant on HIV infection of chimpanzees. Nature 328, 6132 721-3 (1987)
13. Prince A.M., B. Horowitz, L. Baker, R.W. Shulman, H. Ralph, J. Valinsky, A. Cundell, B. Brotman, W. Boehle, F. Rey & et al.: Failure of a human immunodeficiency virus (HIV) immune globulin to protect chimpanzees against experimental challenge with HIV. Proc Natl Acad Sci U S A 85, 18 6944-8 (1988)
14. Goudsmit J., M. Bakker, L. Smit & R.H. Meloen: Specificity of chimpanzee antibodies binding a strain-specific HIV-1 neutralization epitope of the external envelope. J Med Primatol 18, 3-4 357-62 (1989)
15. Berman P.W., T.J. Gregory, L. Riddle, G.R. Nakamura, M.A. Champe, J.P. Porter, F.M. Wurm, R.D. Hershberg, E.K. Cobb & J.W. Eichberg: Protection of chimpanzees from infection by HIV-1 after vaccination with recombinant glycoprotein gp120 but not gp160. Nature 345, 6276 622-5 (1990)
16. Emini E.A., W.A. Schleif, J.H. Nunberg, A.J. Conley, Y. Eda, S. Tokiyoshi, S.D. Putney, S. Matsushita, K.E. Cobb, C.M. Jett & et al.: Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 355, 6362 728-30 (1992)
17. Goudsmit J., C. Debouck, R.H. Meloen, L. Smit, M. Bakker, D.M. Asher, A.V. Wolff, C.J. Gibbs, Jr. & D.C. Gajdusek: Human immunodeficiency virus type 1 neutralization epitope with conserved architecture elicits early type-specific antibodies in experimentally infected chimpanzees. Proc Natl Acad Sci U S A 85, 12 4478-82 (1988)
18. Ferrari G., C.A. Place, P.M. Ahearne, S.M. Nigida, Jr., L.O. Arthur, D.P. Bolognesi & K.J. Weinhold: Comparison of anti-HIV-1 ADCC reactivities in infected humans and chimpanzees. J Acquir Immune Defic Syndr 7, 4 325-31 (1994)
19. Broliden K., J. Hinkula, T. Tolfvenstam, H. Niphuis & J. Heeney: Antibody-dependent cellular cytotoxicity to clinical isolates of HIV-1 and SIVcpz: comparison of human and chimpanzees. Aids 10, 11 1199-204 (1996)
20. Gibbs C.J., Jr., R. Peters, M. Gravell, B.K. Johnson, F.C. Jensen, D.J. Carlo & J. Salk: Observations after human immunodeficiency virus immunization and challenge of human immunodeficiency virus seropositive and seronegative chimpanzees. Proc Natl Acad Sci U S A 88, 8 3348-52 (1991)
21. Israel Z.R. & P.A. Marx: Nonclassical mucosal antibodies predominate in genital secretions of HIV-1 infected chimpanzees. J Med Primatol 24, 2 53-60 (1995)
22. Bruck C., C. Thiriart, L. Fabry, M. Francotte, P. Pala, O. Van-Opstal, J. Culp, M. Rosenberg, M. DeWilde, P. Heidt & a. et: HIV-1 envelope-elicited neutralizing antibody titres correlate with protection and virus load in chimpanzees. Vaccine 12, 12 1141-8 (1994)
23. Cho M.W., M.K. Lee, C.H. Chen, T. Matthews & M.A. Martin: Identification of gp120 regions targeted by a highly potent neutralizing antiserum elicited in a chimpanzee inoculated with a primary human immunodeficiency virus type 1 isolate. J Virol 74, 20 9749-54 (2000)
24. Eichberg J.W., J.M. Zarling, H.J. Alter, J.A. Levy, P.W. Berman, T. Gregory, L.A. Lasky, J. McClure, K.E. Cobb, P.A. Moran & et al.: T-cell responses to human immunodeficiency virus (HIV) and its recombinant antigens in HIV-infected chimpanzees. J Virol 61, 12 3804-8 (1987)
25. Van Eendenburg J.P., M. Yagello, M. Girard, M.P. Kieny, J.P. Lecocq, E. Muchmore, P.N. Fultz, Y. Riviere, L. Montagnier & J.C. Gluckman: Cell-mediated immune proliferative responses to HIV-1 of chimpanzees vaccinated with different vaccinia recombinant viruses. AIDS Res Hum Retroviruses 5, 1 41-50 (1989)
26. Zarling J.M., J.A. Ledbetter, J. Sias, P. Fultz, J. Eichberg, G. Gjerset & P.A. Moran: HIV-infected humans, but not chimpanzees, have circulating cytotoxic T lymphocytes that lyse uninfected CD4+ cells. J Immunol 144, 8 2992-8 (1990)
27. Castro B.A., C.M. Walker, J.W. Eichberg & J.A. Levy: Suppression of human immunodeficiency virus replication by CD8+ cells from infected and uninfected chimpanzees. Cell Immunol 132, 1 246-55 (1991)
28. Schuitemaker H., L. Meyaard, N.A. Kootstra, R. Dubbes, S.A. Otto, M. Tersmette, J.L. Heeney & F. Miedema: Lack of T cell dysfunction and programmed cell death in human immunodeficiency virus type 1-infected chimpanzees correlates with absence of monocytotropic variants. J Infect Dis 168, 5 1140-7. (1993)
29. Boyer J.D., M. Chattergoon, A. Shah, R. Ginsberg, R.R. MacGregor & D.B. Weiner: HIV-1 DNA based vaccine induces a CD8 mediated cross-clade CTL response. Dev Biol Stand 95, 147-53 (1998)
30. Balla-Jhagjhoorsingh S.S., G. Koopman, P. Mooij, T.G. Haaksma, V.J. Teeuwsen, R.E. Bontrop & J.L. Heeney: Conserved CTL epitopes shared between HIV-infected human long-term survivors and chimpanzees. J Immunol 162, 4 2308-14. (1999)
31. Balla-Jhagjhoorsingh S., P. Mooij, G. Koopman, T. Haaksma, V. Teeuwsen, J. Heeney & R. Bontrop: Differential cytotoxic T-lymphocyte (CTL) responses in HIV-1 immunised sibling chimpanzees with shared MHC haplotypes. Immunol Lett 66, 1-3 61-7. (1999)
32. Santra S., P.N. Fultz & N.L. Letvin: Virus-specific cytotoxic T lymphocytes in human immunodeficiency virus type 1-infected chimpanzees. J Virol 73, 8 7065-9 (1999)
33. Koopman G., A.G. Haaksma, J. ten Velden, C.E. Hack & J.L. Heeney: The relative resistance of HIV type 1-infected chimpanzees to AIDS correlates with the maintenance of follicular architecture and the absence of infiltration by CD8+ cytotoxic T lymphocytes. AIDS Res Hum Retroviruses 15, 4 365-73 (1999)
34. Balla-Jhagjhoorsingh S.S., P. Mooij, P.J. ten Haaft, W.M. Bogers, V.J. Teeuwsen, G. Koopman & J.L. Heeney: Protection from secondary human immunodeficiency virus type 1 infection in chimpanzees suggests the importance of antigenic boosting and a possible role for cytotoxic T cells. J Infect Dis 184, 2 136-43 (2001)
35. Heeney J.L.: The critical role of CD4(+) T-cell help in immunity to HIV. Vaccine 20, 15 1961-3 (2002)
36. Ohnimus H., M. Heinkelein, J.L. Heeney, C.M. Walker & C. Jassoy: Lysis of HIV envelope glycoprotein-expressing cells by CD4+ T lymphocytes from chimpanzees. J Acquir Immune Defic Syndr Hum Retrovirol 20, 2 207-13 (1999)
37. Castro B.A., J. Homsy, E. Lennette, K.K. Murthy, J.W. Eichberg & J.A. Levy: HIV-1 expression in chimpanzees can be activated by CD8+ cell depletion or CMV infection. Clin Immunol Immunopathol 65, 3 227-33 (1992)
38. Watanabe M., D.J. Ringler, P.N. Fultz, J.J. MacKey, J.E. Boyson, C.G. Levine & N.L. Letvin: A chimpanzee-passaged human immunodeficiency virus isolate is cytopathic for chimpanzee cells but does not induce disease. J Virol 65, 6 3344-8 (1991)
39. Gendelman H.E., G.D. Ehrlich, L.M. Baca, S. Conley, J. Ribas, D.C. Kalter, M.S. Meltzer, B.J. Poiesz & P. Nara: The inability of human immunodeficiency virus to infect chimpanzee monocytes can be overcome by serial viral passage in vivo. J Virol 65, 7 3853-63 (1991)
40. Heeney J., R. Jonker, W. Koornstra, R. Dubbes, H. Niphuis, A.M. Di Rienzo, M.L. Gougeon & L. Montagnier: The resistance of HIV-infected chimpanzees to progression to AIDS correlates with absence of HIV-related T-cell dysfunction. J Med Primatol 22, 2-3 194-200 (1993)
41. Clerici M. & G.M. Shearer: A TH1 - >TH2 switch is a critical step in the etiology of HIV infection. Immunol Today 14, 3 107-11 (1993)
42. Clerici M. & G.M. Shearer: The Th1-Th2 hypothesis of HIV infection: new insights. Immunol Today 15, 12 575-81 (1994)
43. Heeney J.L.: AIDS: a disease of impaired Th-cell renewal? Immunol Today 16, 11 515-20 (1995)
44. Kestens L., J. Vingerhoets, M. Peeters, G. Vanham, C. Vereecken, G. Penne, H. Niphuis, P. van Eerd, G. van der Groen, P. Gigase & et al.: Phenotypic and functional parameters of cellular immunity in a chimpanzee with a naturally acquired simian immunodeficiency virus infection. J Infect Dis 172, 4 957-63 (1995)
45. Ferrari G., J. Ottinger, C. Place, S.M. Nigida, Jr., L.O. Arthur & K.J. Weinhold: The impact of HIV-1 infection on phenotypic and functional parameters of cellular immunity in chimpanzees. AIDS Res Hum Retroviruses 9, 7 647-56 (1993)
46. Ferrari G., C.A. Place, P.M. Ahearne, S. Nigida, Jr., L.O. Arthur, D.P. Bolognesi & K.J. Weinhold: Comparison of anti-HIV-1 ADCC reactivities in infected humans and chimpanzees. J Acquir Immune Defic Syndr 7, 4 325-31 (1994)
47. Walker C.M., D.J. Moody, D.P. Stites & J.A. Levy: CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234, 4783 1563-6 (1986)
48. Husch B., M.M. Eibl & J.W. Mannhalter: CD3, CD8 double-positive cells from HIV-1-infected chimpanzees show group-specific inhibition of HIV-1 replication. AIDS Res Hum Retroviruses 9, 5 405-13 (1993)
49. Walker C.M.: Non-cytolytic control of HIV replication by CD8+ T cells. Semin Immunol 5, 3 195-201 (1993)
50. Mackewicz C.E., L.C. Yang, J.D. Lifson & J.A. Levy: Non-cytolytic CD8 T-cell anti-HIV responses in primary HIV-1 infection. Lancet 344, 8938 1671-3 (1994)
51. Moriuchi H., M. Moriuchi, C. Combadiere, P.M. Murphy & A.S. Fauci: CD8+ T-cell-derived soluble factor(s), but not beta-chemokines RANTES, MIP-1 alpha, and MIP-1 beta, suppress HIV-1 replication in monocyte/macrophages. Proc Natl Acad Sci U S A 93, 26 15341-5 (1996)
52. Barker E.: CD8+ cell-derived anti-human immunodeficiency virus inhibitory factor. J Infect Dis 179 Suppl 3, S485-8 (1999)
53. Ondoa P., J. Vingerhoets, C. Vereecken, G. van der Groen, J.L. Heeney & L. Kestens: In vitro replication of SIVcpz is suppressed by beta-chemokines and CD8+ T cells but not by natural killer cells of infected chimpanzees. AIDS Res Hum Retroviruses 18, 5 373-82 (2002)
54. Zhang L., W. Yu, T. He, J. Yu, R.E. Caffrey, E.A. Dalmasso, S. Fu, T. Pham, J. Mei, J.J. Ho, W. Zhang, P. Lopez & D.D. Ho: Contribution of human alpha-defensin 1, 2, and 3 to the anti-HIV-1 activity of CD8 antiviral factor. Science 298, 5595 995-1000 (2002)
55. Tersmette M., R.A. Gruters, F. de Wolf, R.E. de Goede, J.M. Lange, P.T. Schellekens, J. Goudsmit, H.G. Huisman & F. Miedema: Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. J Virol 63, 5 2118-25 (1989)
56. De Wolf F., E. Hogervorst, J. Goudsmit, E.M. Fenyo, H. Rubsamen-Waigmann, H. Holmes, B. Galvao-Castro, E. Karita, C. Wasi, S.D. Sempala & et al.: Syncytium-inducing and non-syncytium-inducing capacity of human immunodeficiency virus type 1 subtypes other than B: phenotypic and genotypic characteristics. WHO Network for HIV Isolation and Characterization. AIDS Res Hum Retroviruses 10, 11 1387-400 (1994)
57. Doms R.W.: Chemokine receptors and HIV entry. Aids 15 Suppl 1, S34-5 (2001)
58. Berger E.A.: HIV entry and tropism: the chemokine receptor connection. Aids 11 Suppl A, S3-16 (1997)
59. Berger E.A., P.M. Murphy & J.M. Farber: Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17, 657-700 (1999)
60. Cocchi F., A.L. DeVico, A. Garzino-Demo, A. Cara, R.C. Gallo & P. Lusso: The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nat Med 2, 11 1244-7 (1996)
61. Scarlatti G., E. Tresoldi, A. Bjorndal, R. Fredriksson, C. Colognesi, H.K. Deng, M.S. Malnati, A. Plebani, A.G. Siccardi, D.R. Littman, E.M. Fenyo & P. Lusso: In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat Med 3, 11 1259-65 (1997)
62. Broder C.C. & D.S. Dimitrov: HIV and the 7-transmembrane domain receptors. Pathobiology 64, 4 171-9 (1996)
63. Ditzel H.J., M.M. Rosenkilde, P. Garred, M. Wang, K. Koefoed, C. Pedersen, D.R. Burton & T.W. Schwartz: The CCR5 receptor acts as an alloantigen in CCR5Delta32 homozygous individuals: identification of chemokineand HIV-1-blocking human antibodies. Proc Natl Acad Sci U S A 95, 9 5241-5 (1998)
64. Heeney J.L., V.J.P. Teeuwsen, M. van Gils, W.M.J.M. Bogers, C. de Giuli Morghen, A. Radaelli, S. Barnett, B. Morein, L. Akerblom, Y. Wang, T. Lehner & D. Davis: β-chemokines and neutralizing antibody titers correlate with sterilizing immunity generated in HIV-1 vaccinated macaques. Proc Natl Acad Sci U S A 95, 10803-10808 (1998)
65. Bogers W., W. Koornstra, R. Dubbes, P. Nara, L. Buijs & J. Heeney: Potent HIV-1 inhibiting soluble factor from chimpanzee peripheral blood cells. HIV and Cytokines 211-215 (1997)
66. Heeney J., W. Bogers, L. Buijs, R. Dubbes, P. ten Haaft, W. Koornstra, H. Niphuis, P. Nara & V. Teeuwsen: Immune strategies utilized by lentivirus infected chimpanzees to resist progression to AIDS. Immunol Lett 51, 1-2 45-52 (1996)
67. Peeters M., C. Honore, T. Huet, L. Bedjabaga, S. Ossari, P. Bussi, R.W. Cooper & E. Delaporte: Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. Aids 3, 10 625-30 (1989)
68. Huet T., R. Cheynier, A. Meyerhans, G. Roelants & S. Wain-Hobson: Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345, 6273 356-9 (1990)
69. Peeters M., K. Fransen, E. Delaporte, M. Van den Haesevelde, G.M. Gershy-Damet, L. Kestens, G. van der Groen & P. Piot: Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. Aids 6, 5 447-51 (1992)
70. Nyambi P.N., P. Lewi, M. Peeters, W. Janssens, L. Heyndrickx, K. Fransen, K. Andries, M. Vanden Haesevelde, J. Heeney, P. Piot & G. van der Groen: Study of the dynamics of neutralization escape mutants in a chimpanzee naturally infected with the simian immunodeficiency virus SIVcpz-ant. J Virol 71, 3 2320-30 (1997)
71. Peeters M., W. Janssens, M. Vanden Haesevelde, K. Fransen, B. Willems, L. Heyndrickx, L. Kestens, P. Piot, G. Van der Groen & J. Heeney: Virologic and serologic characteristics of a natural chimpanzee lentivirus infection. Virology 211, 1 312-5 (1995)
72. Gao F., E. Bailes, D.L. Robertson, Y. Chen, C.M. Rodenburg, S.F. Michael, L.B. Cummins, L.O. Arthur, M. Peeters, G.M. Shaw, P.M. Sharp & B.H. Hahn: Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397, 6718 436-41 (1999)
73. Berry N., C. Davis, A. Jenkins, D. Wood, P. Minor, G. Schild, M. Bottiger, H. Holmes & N. Almond: Vaccine safety. Analysis of oral polio vaccine CHAT stocks. Nature 410, 6832 1046-7 (2001)
74. Plotkin S.A. & H. Koprowski: No evidence to link polio vaccine with HIV. Nature 407, 6807 941 (2000)
75. Dickson D.: Tests fail to support claims for origin of AIDS in polio vaccine. Nature 407, 6801 117 (2000)
76. Poinar H., M. Kuch & S. Paabo: Molecular analyses of oral polio vaccine samples. Science 292, 5517 743-4 (2001)
77. Peeters M., V. Courgnaud, B. Abela, P. Auzel, X. Pourrut, F. Bibollet-Ruche, S. Loul, F. Liegeois, C. Butel, D. Koulagna, E. Mpoudi-Ngole, G.M. Shaw, B.H. Hahn & E. Delaporte: Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg Infect Dis 8, 5 451-7 (2002)
78. Hahn B.H., G.M. Shaw, K.M. De Cock & P.M. Sharp: AIDS as a zoonosis: scientific and public health implications. Science 287, 5453 607-14 (2000)
79. Korber B., M. Muldoon, J. Theiler, F. Gao, R. Gupta, A. Lapedes, B.H. Hahn, S. Wolinsky & T. Bhattacharya: Timing the ancestor of the HIV-1 pandemic strains. Science 288, 5472 1789-96 (2000)
80. Salemi M., K. Strimmer, W.W. Hall, M. Duffy, E. Delaporte, S. Mboup, M. Peeters & A.M. Vandamme: Dating the common ancestor of SIVcpz and HIV-1 group M and the origin of HIV-1 subtypes using a new method to uncover clock-like molecular evolution. Faseb J 15, 2 276-8 (2001)
81. Santiago M.L., C.M. Rodenburg, S. Kamenya, F. Bibollet-Ruche, F. Gao, E. Bailes, S. Meleth, S.J. Soong, J.M. Kilby, Z. Moldoveanu, B. Fahey, M.N. Muller, A. Ayouba, E. Nerrienet, H.M. McClure, J.L. Heeney, A.E. Pusey, D.A. Collins, C. Boesch, R.W. Wrangham, J. Goodall, P.M. Sharp, G.M. Shaw & B.H. Hahn: SIVcpz in wild chimpanzees. Science 295, 5554 465 (2002)
82. Barre-Sinoussi F., J.C. Chermann, F. Rey, M.T. Nugeyre, S. Chamaret, J. Gruest, C. Dauguet, C. Axler-Blin, F. Vezinet-Brun, C. Rouzioux, W. Rozenbaum & L. Montagnier: Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220, 4599 868-71 (1983)
83. Chermann J.C., F. Barre-Sinoussi, C. Dauguet, F. Brun-Vezinet, C. Rouzioux, W. Rozenbaum & L. Montagnier: Isolation of a new retrovirus in a patient at risk for acquired immunodeficiency syndrome. Antibiot Chemother 32, 48-53 (1983)
84. ten Haaft P., K. Murthy, M. Salas, H. McClure, R. Dubbes, W. Koornstra, H. Niphuis, D. Davis, G. van der Groen & J. Heeney: Differences in early virus loads with different phenotypic variants of HIV-1 and SIV(cpz) in chimpanzees. Aids 15, 16 2085-92 (2001)
85. Copeland K.F. & J.L. Heeney: T helper cell activation and human retroviral pathogenesis. Microbiol Rev 60, 4 722-42. (1996)
86. Gougeon M.L., S. Garcia, J. Heeney, R. Tschopp, H. Lecoeur, D. Guetard, V. Rame, C. Dauguet & L. Montagnier: Programmed cell death in AIDS-related HIV and SIV infections. AIDS Res Hum Retroviruses 9, 6 553-63 (1993)
87. Gougeon M.L., H. Lecoeur, A. Dulioust, M.G. Enouf, M. Crouvoiser, C. Goujard, T. Debord & L. Montagnier: Programmed cell death in peripheral lymphocytes from HIV-infected persons: increased susceptibility to apoptosis of CD4 and CD8 T cells correlates with lymphocyte activation and with disease progression. J Immunol 156, 9 3509-20. (1996)
88. Davis I.C., M. Girard & P.N. Fultz: Loss of CD4+ T cells in human immunodeficiency virus type 1-infected chimpanzees is associated with increased lymphocyte apoptosis. J Virol 72, 6 4623-32 (1998)
89. Novembre F.J., M. Saucier, D.C. Anderson, S.A. Klumpp, S.P. O'Neil, C.R. Brown, 2nd, C.E. Hart, P.C. Guenthner, R.B. Swenson & H.M. McClure: Development of AIDS in a chimpanzee infected with human immunodeficiency virus type 1. J Virol 71, 5 4086-91 (1997)
90. O'Neil S.P., F.J. Novembre, A.B. Hill, C. Suwyn, C.E. Hart, T. Evans-Strickfaden, D.C. Anderson, J. deRosayro, J.G. Herndon, M. Saucier & H.M. McClure: Progressive infection in a subset of HIV-1-positive chimpanzees. J Infect Dis 182, 4 1051-62 (2000)
91. ten Haaft P., B. Verstrepen, K. Uberla, B. Rosenwirth & J. Heeney: A pathogenic threshold of virus load defined in simian immunodeficiency virus- or simian-human immunodeficiency virus-infected macaques. J Virol 72, 12 10281-5 (1998)
92. Ondoa P., C. Vereecken, K. Fransen, R. Colebunders, G. Van Der Groen, J.L. Heeney & L. Kestens: Human and simian immunodeficiency virus-infected chimpanzees do not have increased intracellular levels of beta-chemokines in contrast to infected humans. J Med Virol 69, 3 297-305 (2003)
93. Ondoa P, D. Davis, L. Kestens, K. Vereecken, S. Garcia Ribas, K. Fransen, J. Heeney & G. van der Groen: In vitro susceptibility to infection with SIVcpz and HIV-1 is lower in chimpanzee than in human peripheral blood mononuclear cells. J Med Virol 67, 3 301-311 (2002)
94. de Groot N.G., N. Otting, G.G. Doxiadis, S.S. Balla-Jhagjhoorsingh, J.L. Heeney, J.J. van Rood, P. Gagneux & R.E. Bontrop: Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc Natl Acad Sci U S A 99, 18 11748-53 (2002)
95. Balla-Jhagjhoorsingh S., E. Verschoor, N.G. de Groot, V. Teeuwsen, R. Bontrop & J. Heeney: Specific Nature of cellular immune responses elicited by chimpanzees against HIV-1. hum immunol (2003)
96. Champagne P., G.S. Ogg, A.S. King, C. Knabenhans, K. Ellefsen, M. Nobile, V. Appay, G.P. Rizzardi, S. Fleury, M. Lipp, R. Forster, S. Rowland-Jones, R.P. Sekaly, A.J. McMichael & G. Pantaleo: Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410, 6824 106-11 (2001)