Preinfection human immunodeficiency virus (HIV)-specific cytotoxic T lymphocytes failed to prevent HIV type 1 infection from strains genetically unrelated to viruses in long-term exposed partners

Journal of Virology

Volumn 83, Issue 20, 2009, Pages 10821-10829

  Liu, Yi ^b   Woodward, Amanda ^a   Zhu, Haiying ^a   Andrus, Thomas ^a   McNevin, John ^c   Lee, Jean ^c   Mullins, James I ^a,b   Corey, Lawrence ^a,b,c   McElrath, M Juliana ^b,c   Zhu, Tuofu ^a,b,c  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; NEF PROTEIN; POL PROTEIN; PROTEIN P63; PROTEOME; VIRUS GLYCOPROTEIN;

ANUS INTERCOURSE; ARTICLE; CLINICAL TRIAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DISEASE PREDISPOSITION; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INFECTION CONTROL; INFECTION RISK; MAJOR CLINICAL STUDY; MALE; MALE HOMOSEXUAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEROCONVERSION; SEXUAL BEHAVIOR; SEXUAL TRANSMISSION; STRAIN DIFFERENCE; UNSAFE SEX; VIRUS LOAD; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE;

CYTOTOXICITY, IMMUNOLOGIC; GENETIC VARIATION; HIV INFECTIONS; HIV LONG-TERM SURVIVORS; HIV SERONEGATIVITY; HIV-1; HLA-B27 ANTIGEN; HUMANS; LYMPHOCYTE ACTIVATION; MALE; SEXUAL BEHAVIOR; SEXUAL PARTNERS; T-LYMPHOCYTES, CYTOTOXIC; UNSAFE SEX;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 70349751687     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00839-09     Document Type: Article

References (67)

1. Akridge, R., F. Hladik, J. Markee, C. Alef, H. Kelley, A. Collier, A. Collier, and M. J. McElrath. 1999. Cellular immunity and target cell susceptibility in persons with repeated HIV-1 exposure. Immunol. Lett. 66:15-19.
2. Altfeld, M., E. T. Kalife, Y. Qi, H. Streeck, M. Lichterfeld, M. N. Johnston, N. Burgett, M. E. Swartz, A. Yang, G. Alter, X. G. Yu, A. Meier, J. K. Rockstroh, T. M. Allen, H. Jessen, E. S. Rosenberg, M. Carrington, and B. D. Walker. 2006. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med. 3:e403. (Pubitemid 44721824)
3. Ashley, R., A. Cent, V. Maggs, A. Nahmias, and L. Corey. 1991. Inability of enzyme immunoassays to discriminate between infections with herpes simplex virus types 1 and 2. Ann. Intern. Med. 115:520-526.
4. Ashley, R. L., J. Militoni, F. Lee, A. Nahmias, and L. Corey. 1988. Comparison of Western blot (immunoblot) and glycoprotein G-specific immunodot enzyme assay for detecting antibodies to herpes simplex virus types 1 and 2 in human sera. J. Clin. Microbiol. 26:662-667.
5. Blaak, H., A. B. van't Wout, M. Brouwer, M. Cornelissen, N. A. Kootstra, N. Albrecht-van Lent, R. P. Keet, J. Goudsmit, R. A. Coutinho, and H. Schuitemaker. 1998. Infectious cellular load in human immunodeficiency virus type 1 (HIV-1)-infected individuals and susceptibility of peripheral blood mononuclear cells from their exposed partners to non-syncytium-inducing HIV-1 as major determinants for HIV-1 transmission in homosexual couples. J. Virol. 72:218-224.
6. Corey, L., and H. H. Handsfield. 2000. Genital herpes and public health: addressing a global problem. JAMA 283:791-794. (Pubitemid 30084620)
7. Corey, L., A. Wald, C. L. Celum, and T. C. Quinn. 2004. The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission: a review of two overlapping epidemics. J. Acquir. Immune Defic. Syndr. 35:435-445.
8. Dean, M., M. Carrington, C. Winkler, G. A. Huttley, M. W. Smith, R. Allikmets, J. J. Goedert, S. P. Buchbinder, E. Vittinghoff, E. Gomperts, S. Donfield, D. Vlahov, R. Kaslow, A. Saah, C. Rinaldo, R. Detels, S. J. O'Brien, et al. 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273:1856-1862. (Pubitemid 26322495)
9. De Maria, A., C. Cirillo, and L. Moretta. 1994. Occurrence of human immunodeficiency virus type 1 (HIV-1)-specific cytolytic T cell activity in apparently uninfected children born to HIV-1-infected mothers. J. Infect. Dis. 170:1296-1299.
10. Draenert, R., S. Le Gall, K. J. Pfafferott, A. J. Leslie, P. Chetty, C. Brander, E. C. Holmes, S. C. Chang, M. E. Feeney, M. M. Addo, L. Ruiz, D. Ramduth, P. Jeena, M. Altfeld, S. Thomas, Y. Tang, C. L. Verrill, C. Dixon, J. G. Prado, P. Kiepiela, J. Martinez-Picado, B. D. Walker, and P. J. Goulder. 2004. Immune selection for altered antigen processing leads to cytotoxic T lymphocyte escape in chronic HIV-1 infection. J. Exp. Med. 199:905-915.
11. Fowke, K. R., R. Kaul, K. L. Rosenthal, J. Oyugi, J. Kimani, W. J. Rutherford, N. J. Nagelkerke, T. B. Ball, J. J. Bwayo, J. N. Simonsen, G. M. Shearer, and F. A. Plummer. 2000. HIV-1-specific cellular immune responses among HIV-1-resistant sex workers. Immunol. Cell Biol. 78:586-595.
12. Fowke, K. R., N. J. Nagelkerke, J. Kimani, J. N. Simonsen, A. O. Anzala, J. J. Bwayo, K. S. MacDonald, E. N. Ngugi, and F. A. Plummer. 1996. Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 348:1347-1351.
13. + T cells during infection. J. Virol. 78:7883-7893.
14. Gibbons, J., J. M. Cory, I. K. Hewlett, J. S. Epstein, and M. E. Eyster. 1990. Silent infections with human immunodeficiency virus type 1 are highly unlikely in multitransfused seronegative hemophiliacs. Blood 76:1624-1626.
15. Goh, W. C., J. Markee, R. E. Akridge, M. Meldorf, L. Musey, T. Karchmer, M. Krone, A. Collier, L. Corey, M. Emerman, and M. J. McElrath. 1999. Protection against human immunodeficiency virus type 1 infection in persons with repeated exposure: evidence for T cell immunity in the absence of inherited CCR5 coreceptor defects. J. Infect. Dis. 179:548-557.
16. Gonzalez, E., R. Dhanda, M. Bamshad, S. Mummidi, R. Geevarghese, G. Catano, S. A. Anderson, E. A. Walter, K. T. Stephan, M. F. Hammer, A. Mangano, L. Sen, R. A. Clark, S. S. Ahuja, M. J. Dolan, and S. K. Ahuja. 2001. Global survey of genetic variation in CCR5, RANTES, and MIP-1alpha: impact on the epidemiology of the HIV-1 pandemic. Proc. Natl. Acad. Sci. USA 98:5199-5204.
17. Hladik, F., A. Desbien, J. Lang, L. Wang, Y. Ding, S. Holte, A. Wilson, Y. Xu, M. Moerbe, S. Schmechel, and M. J. McElrath. 2003. Most highly exposed seronegative men lack HIV-1-specific, IFN-gamma-secreting T cells. J. Immunol. 171:2671-2683. (Pubitemid 37025581)
18. Hladik, F., H. Liu, E. Speelmon, D. Livingston-Rosanoff, S. Wilson, P. Sakchalathorn, Y. Hwangbo, B. Greene, T. Zhu, and M. J. McElrath. 2005. Combined effect of CCR5-Δ32 heterozygosity and the CCR5 promoter polymorphism -2459 A/G on CCR5 expression and resistance to human immunodeficiency virus type 1 transmission. J. Virol. 79:11677-11684. (Pubitemid 41279286)
19. Hoffman, T. L., R. R. MacGregor, H. Burger, R. Mick, R. W. Doms, and R. G. Collman. 1997. CCR5 genotypes in sexually active couples discordant for human immunodeficiency virus type 1 infection status. J. Infect. Dis. 176:1093-1096.
20. Huang, Y., W. A. Paxton, S. M. Wolinsky, A. U. Neumann, L. Zhang, T. He, S. Kang, D. Ceradini, Z. Jin, K. Yazdanbakhsh, K. Kunstman, D. Erickson, E. Dragon, N. R. Landau, J. Phair, D. D. Ho, and R. A. Koup. 1996. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat. Med. 2:1240-1243.
21. Imagawa, D. T., M. H. Lee, S. M. Wolinsky, K. Sano, F. Morales, S. Kwok, J. J. Sninsky, P. G. Nishanian, J. Giorgi, J. L. Fahey, et al. 1989. Human immunodeficiency virus type 1 infection in homosexual men who remain seronegative for prolonged periods. N. Engl. J. Med. 320:1458-1462.
22. Jennes, W., S. Verheyden, C. Demanet, C. A. Adje-Toure, B. Vuylsteke, J. N. Nkengasong, and L. Kestens. 2006. Cutting edge: resistance to HIV-1 infection among African female sex workers is associated with inhibitory KIR in the absence of their HLA ligands. J. Immunol. 177:6588-6592. (Pubitemid 44715020)
23. Kaslow, R. A., M. Carrington, R. Apple, L. Park, A. Munoz, A. J. Saah, J. J. Goedert, C. Winkler, S. J. O'Brien, C. Rinaldo, R. Detels, W. Blattner, J. Phair, H. Erlich, and D. L. Mann. 1996. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2:405-411.
24. Kaul, R., T. Dong, F. A. Plummer, J. Kimani, T. Rostron, P. Kiama, E. Njagi, E. Irungu, B. Farah, J. Oyugi, R. Chakraborty, K. S. MacDonald, J. B. Bwayo, A. McMichael, and S. Rowland-Jones. 2001. CD8+ lymphocytes respond to different HIV epitopes in seronegative and infected subjects. J. Clin. Investig. 107:1303-1310.
25. Kaul, R., F. Plummer, M. Clerici, M. Bomsel, L. Lopalco, and K. Broliden. 2001. Mucosal IgA in exposed, uninfected subjects: evidence for a role in protection against HIV infection. AIDS 15:431-432. (Pubitemid 32163839)
26. Kaul, R., F. A. Plummer, J. Kimani, T. Dong, P. Kiama, T. Rostron, E. Njagi, K. S. MacDonald, J. J. Bwayo, A. J. McMichael, and S. L. Rowland-Jones. 2000. HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1-resistant prostitutes in Nairobi. J. Immunol. 164:1602-1611. (Pubitemid 30067280)
27. Kaul, R., S. L. Rowland-Jones, J. Kimani, T. Dong, H. B. Yang, P. Kiama, T. Rostron, E. Njagi, J. J. Bwayo, K. S. MacDonald, A. J. McMichael, and F. A. Plummer. 2001. Late seroconversion in HIV-resistant Nairobi prostitutes despite pre-existing HIV-specific CD8+ responses. J. Clin. Investig. 107:341-349.
28. Kaul, R., S. L. Rowland-Jones, J. Kimani, K. Fowke, T. Dong, P. Kiama, J. Rutherford, E. Njagi, F. Mwangi, T. Rostron, J. Onyango, J. Oyugi, K. S. MacDonald, J. J. Bwayo, and F. A. Plummer. 2001. New insights into HIV-1 specific cytotoxic T-lymphocyte responses in exposed, persistently seronegative Kenyan sex workers. Immunol. Lett. 79:3-13.
29. Kaul, R., D. Trabattoni, J. J. Bwayo, D. Arienti, A. Zagliani, F. M. Mwangi, C. Kariuki, E. N. Ngugi, K. S. MacDonald, T. B. Ball, M. Clerici, and F. A. Plummer. 1999. HIV-1-specific mucosal IgA in a cohort of HIV-1-resistant Kenyan sex workers. AIDS 13:23-29. (Pubitemid 29078060)
30. Korber, B. 2000. HIV signature and sequence variation analysis, p. 55-72. In A. G. Rodrigo and G. H. Learn (ed.), Computational analysis of HIV molecular sequences. Kluwer Academic Publishers, Dordrecht, The Netherlands.
31. Kostrikis, L. G., A. U. Neumann, B. Thomson, B. T. Korber, P. McHardy, R. Karanicolas, L. Deutsch, Y. Huang, J. F. Lew, K. McIntosh, H. Pollack, W. Borkowsky, H. M. Spiegel, P. Palumbo, J. Oleske, A. Bardeguez, K. Luzuriaga, J. Sullivan, S. M. Wolinsky, R. A. Koup, D. D. Ho, and J. P. Moore. 1999. A polymorphism in the regulatory region of the CC-chemokine receptor 5 gene influences perinatal transmission of human immunodeficiency virus type 1 to African-American infants. J. Virol. 73:10264-10271.
32. Kulkarni, P. S., S. T. Butera, and A. C. Duerr. 2003. Resistance to HIV-1 infection: lessons learned from studies of highly exposed persistently seronegative (HEPS) individuals. AIDS Rev. 5:87-103.
33. Langlade-Demoyen, P., N. Ngo-Giang-Huong, F. Ferchal, and E. Oksenhendler. 1994. Human immunodeficiency virus (HIV) nef-specific cytotoxic T lymphocytes in noninfected heterosexual contact of HIV-infected patients. J. Clin. Investig. 93:1293-1297.
34. Le Gall, S., P. Stamegna, and B. D. Walker. 2007. Portable flanking sequences modulate CTL epitope processing. J. Clin. Investig. 117:3563-3575.
35. Lehner, T. 2003. Innate and adaptive mucosal immunity in protection against HIV infection. Vaccine 21(Suppl. 2):S68-S76. (Pubitemid 36588651)
36. Liu, H., M. Carrington, C. Wang, S. Holte, J. Lee, B. Greene, F. Hladik, D. M. Koelle, A. Wald, K. Kurosawa, C. R. Rinaldo, C. Celum, R. Detels, L. Corey, M. J. McElrath, and T. Zhu. 2006. Repeat-region polymorphisms in the gene for the dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin-related molecule: effects on HIV-1 susceptibility. J. Infect. Dis. 193:698-702.
37. Liu, H., D. Chao, E. E. Nakayama, H. Taguchi, M. Goto, X. Xin, J. K. Takamatsu, H. Saito, Y. Ishikawa, T. Akaza, T. Juji, Y. Takebe, T. Ohishi, K. Fukutake, Y. Maruyama, S. Yashiki, S. Sonoda, T. Nakamura, Y. Nagai, A. Iwamoto, and T. Shioda. 1999. Polymorphism in RANTES chemokine promoter affects HIV-1 disease progression. Proc. Natl. Acad. Sci. USA 96:4581-4585.
38. Liu, H., Y. Hwangbo, S. Holte, J. Lee, C. Wang, N. Kaupp, H. Zhu, C. Celum, L. Corey, M. J. McElrath, and T. Zhu. 2004. Analysis of genetic polymorphisms in CCR5, CCR2, stromal cell-derived factor-1, RANTES, and dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin in seronegative individuals repeatedly exposed to HIV-1. J. Infect. Dis. 190:1055-1058.
39. Liu, R., W. A. Paxton, S. Choe, D. Ceradini, S. R. Martin, R. Horuk, M. E. MacDonald, H. Stuhlmann, R. A. Koup, and N. R. Landau. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377. (Pubitemid 26272077)
40. Llewellyn, N., R. Zioni, H. Zhu, T. Andrus, Y. Xu, L. Corey, and T. Zhu. 2006. Continued evolution of HIV-1 circulating in blood monocytes with antiretroviral therapy: genetic analysis of HIV-1 in monocytes and CD4+ T cells of patients with discontinued therapy. J. Leukoc. Biol. 80:1118-1126.
41. MacDonald, K. S., K. R. Fowke, J. Kimani, V. A. Dunand, N. J. Nagelkerke, T. B. Ball, J. Oyugi, E. Njagi, L. K. Gaur, R. C. Brunham, J. Wade, M. A. Luscher, P. Krausa, S. Rowland-Jones, E. Ngugi, J. J. Bwayo, and F. A. Plummer. 2000. Influence of HLA supertypes on susceptibility and resistance to human immunodeficiency virus type 1 infection. J. Infect. Dis. 181:1581-1589.
42. Maddison, W. P., and D. R. Maddison. 2001. MacClade: analysis of phylogeny and character evolution, version 4. Sinauer Associates, Inc., Sunderland, MA.
43. Marmor, M., H. W. Sheppard, D. Donnell, S. Bozeman, C. Celum, S. Buchbinder, B. Koblin, and G. R. Seage III. 2001. Homozygous and heterozygous CCR5-delta32 genotypes are associated with resistance to HIV infection. J. Acquir. Immune Defic. Syndr. 27:472-481.
44. Martin, M. P., M. Dean, M. W. Smith, C. Winkler, B. Gerrard, N. L. Michael, B. Lee, R. W. Doms, J. Margolick, S. Buchbinder, J. J. Goedert, T. R. O'Brien, M. W. Hilgartner, D. Vlahov, S. J. O'Brien, and M. Carrington. 1998. Genetic acceleration of AIDS progression by a promoter variant of CCR5. Science 282:1907-1911. (Pubitemid 28555273)
45. Mazzoli, S., D. Trabattoni, S. Lo Caputo, S. Piconi, C. Ble, F. Meacci, S. Ruzzante, A. Salvi, F. Semplici, R. Longhi, M. Fusi, N. Tofani, M. Biasin, M. Villa, F. Mazzotta, and M. Clerici. 1997. HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat. Med. 3:1250-1257.
46. McDermott, D. H., M. J. Beecroft, C. A. Kleeberger, F. M. Al-Sharif, W. E. Ollier, P. A. Zimmerman, B. A. Boatin, S. F. Leitman, R. Detels, A. H. Hajeer, and P. M. Murphy. 2000. Chemokine RANTES promoter polymorphism affects risk of both HIV infection and disease progression in the Multicenter AIDS Cohort Study. AIDS 14:2671-2678.
47. Michael, N. L., G. Chang, L. G. Louie, J. R. Mascola, D. Dondero, D. L. Birx, and H. W. Sheppard. 1997. The role of viral phenotype and CCR-5 gene defects in HIV-1 transmission and disease progression. Nat. Med. 3:338-340.
48. Nielsen, M., C. Lundegaard, O. Lund, and C. Kesmir. 2005. The role of the proteasome in generating cytotoxic T-cell epitopes: insights obtained from improved predictions of proteasomal cleavage. Immunogenetics 57:33-41. (Pubitemid 40591245)
49. O'Brien, S. J., and J. P. Moore. 2000. The effect of genetic variation in chemokines and their receptors on HIV transmission and progression to AIDS. Immunol. Rev. 177:99-111.
50. O'Brien, S. J., G. W. Nelson, C. A. Winkler, and M. W. Smith. 2000. Polygenic and multifactorial disease gene association in man: lessons from AIDS. Annu. Rev. Genet. 34:563-591.
51. Operskalski, E. A., D. O. Stram, M. P. Busch, W. Huang, M. Harris, S. L. Dietrich, E. R. Schiff, E. Donegan, J. W. Mosley, et al. 1997. Role of viral load in heterosexual transmission of human immunodeficiency virus type 1 by blood transfusion recipients. Am. J. Epidemiol. 146:655-661.
52. Paxton, W. B., R. W. Coombs, M. J. McElrath, M. C. Keefer, J. Hughes, F. Sinangil, D. Chernoff, B. Williams, L. Demeter, and L. Corey. 1997. Longitudinal analysis of quantitative virologic measures in human immunodeficiency virus-infected subjects with ≥400 CD4 lymphocytes: implications for applying measurements to individual patients. J. Infect. Dis. 175:247-254.
53. Pedraza, M. A., J. del Romero, F. Roldan, S. Garcia, M. C. Ayerbe, A. R. Noriega, and J. Alcami. 1999. Heterosexual transmission of HIV-1 is associated with high plasma viral load levels and a positive viral isolation in the infected partner. J. Acquir. Immune Defic. Syndr. 21:120-125.
54. Quinn, T. C., M. J. Wawer, N. Sewankambo, D. Serwadda, C. Li, F. Wabwire-Mangen, M. O. Meehan, T. Lutalo, R. H. Gray, et al. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 1. N. Engl. J. Med. 342:921-929.
55. Rowland-Jones, S. L., T. Dong, L. Dorrell, G. Ogg, P. Hansasuta, P. Krausa, J. Kimani, S. Sabally, K. Ariyoshi, J. Oyugi, K. S. MacDonald, J. Bwayo, H. Whittle, F. A. Plummer, and A. J. McMichael. 1999. Broadly cross-reactive HIV-specific cytotoxic T-lymphocytes in highly-exposed persistently seronegative donors. Immunol. Lett. 66:9-14.
56. Rowland-Jones, S. L., T. Dong, K. R. Fowke, J. Kimani, P. Krausa, H. Newell, T. Blanchard, K. Ariyoshi, J. Oyugi, E. Ngugi, J. Bwayo, K. S. MacDonald, A. J. McMichael, and F. A. Plummer. 1998. Cytotoxic T cell responses to multiple conserved HIV epitopes in HIV-resistant prostitutes in Nairobi. J. Clin. Investig. 102:1758-1765.
57. Rowland-Jones, S. L., D. F. Nixon, M. C. Aldhous, F. Gotch, K. Ariyoshi, N. Hallam, J. S. Kroll, K. Froebel, and A. McMichael. 1993. HIV-specific cytotoxic T-cell activity in an HIV-exposed but uninfected infant. Lancet 341:860-861.
58. Rowland-Jones, S. L., J. Sutton, K. Ariyoshi, T. Dong, F. Gotch, S. McAdam, D. Whitby, S. Sabally, A. Gallimore, T. Corrah, M. Takiguchi, T. Schultz, A. McMichael, and H. Whittle. 1995. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat. Med. 1:59-64.
59. Samson, M., F. Libert, B. J. Doranz, J. Rucker, C. Liesnard, C. M. Farber, S. Saragosti, C. Lapoumeroulie, J. Cognaux, C. Forceille, G. Muyldermans, C. Verhofstede, G. Burtonboy, M. Georges, T. Imai, S. Rana, Y. Yi, R. J. Smyth, R. G. Collman, R. W. Doms, G. Vassart, and M. Parmentier. 1996. Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722-725. (Pubitemid 26282179)
60. Schacker, T., A. C. Collier, J. Hughes, T. Shea, and L. Corey. 1996. Clinical and epidemiologic features of primary HIV infection. Ann. Intern. Med. 125:257-264.
61. Schmechel, S. C., N. Russell, F. Hladik, J. Lang, A. Wilson, R. Ha, A. Desbien, and M. J. McElrath. 2001. Immune defence against HIV-1 infection in HIV-1-exposed seronegative persons. Immunol. Lett. 79:21-27.
62. Shankarappa, R., J. B. Margolick, S. J. Gange, A. G. Rodrigo, D. Upchurch, H. Farzadegan, P. Gupta, C. R. Rinaldo, G. H. Learn, X. He, X. L. Huang, and J. I. Mullins. 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
63. Smith, M. W., M. Dean, M. Carrington, C. Winkler, G. A. Huttley, D. A. Lomb, J. J. Goedert, T. R. O'Brien, L. P. Jacobson, R. Kaslow, S. Buchbinder, E. Vittinghoff, D. Vlahov, K. Hoots, M. W. Hilgartner, S. J. O'Brien, et al. 1997. Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Science 277:959-965.
64. Swofford, D. L. 1999. PAUP* 4.0: Phylogenetic Analysis Using Parsimony (* and other methods), 4.0b2a ed. Sinauer Associates, Inc., Sunderland, MA.
65. Yokomaku, Y., H. Miura, H. Tomiyama, A. Kawana-Tachikawa, M. Takiguchi, A. Kojima, Y. Nagai, A. Iwamoto, Z. Matsuda, and K. Ariyoshi. 2004. Impaired processing and presentation of cytotoxic-T-lymphocyte (CTL) epitopes are major escape mechanisms from CTL immune pressure in human immunodeficiency virus type 1 infection. J. Virol. 78:1324-1332. (Pubitemid 38095842)
66. Zhu, T., L. Corey, Y. Hwangbo, J. M. Lee, G. H. Learn, J. I. Mullins, and M. J. McElrath. 2003. Persistence of extraordinarily low levels of genetically homogeneous human immunodeficiency virus type 1 in exposed seronegative individuals. J. Virol. 77:6108-6116. (Pubitemid 36588382)
67. Zimbwa, P., A. Milicic, J. Frater, T. J. Scriba, A. Willis, P. J. R. Goulder, T. Pillay, H. Gunthard, J. N. Weber, H.-T. Zhang, and R. E. Phillips. 2007. Precise identification of a human immunodeficiency virus type 1 antigen processing mutant. J. Virol. 81:2031-2038. (Pubitemid 46214474)