HIV-1 Dynamics: A reappraisal of host and viral factors, as well as methodological issues

Viruses

Volumn 4, Issue 10, 2012, Pages 2080-2096

  Prentice, Heather A ^a   Tang, Jianming ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Correlates; Genetics; HIV 1; Viral load

Indexed keywords

HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2;

ALLELE; CHEMOKINE LIGAND GENE; CHEMOKINE RECEPTOR GENE; GENE; GENETIC ASSOCIATION; GENOTYPE; HERITABILITY; HLA ANTIGEN CLASS 1 GENE; HLA ANTIGEN CLASS 2 GENE; HOST; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR GENE; MOLECULAR EVOLUTION; NONHUMAN; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL; VIRAL GENETICS; VIRAL PHENOMENA AND FUNCTIONS; VIREMIA; VIRUS CELL INTERACTION; VIRUS DYNAMICS; VIRUS LOAD; VIRUS MUTATION; VIRUS REPLICATION;

ADAPTATION, BIOLOGICAL; ALLELES; DISEASE PROGRESSION; GENES, MHC CLASS I; GENES, MHC CLASS II; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; VIRAL LOAD; VIREMIA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84868129312     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v4102080     Document Type: Review

References (115)

1. Gottlieb, G.S.; Heath, L.; Nickle, D.C.; Wong, K.G.; Leach, S.E.; Jacobs, B.; Gezahegne, S.; van 't Wout, A.B.; Jacobson, L.P.; Margolick, J.B.; et al. HIV-1 variation before seroconversion in men who have sex with men, analysis of acute/early HIV infection in the multicenter AIDS cohort study. J. Infect. Dis. 2008, 197, 1011-1015.
2. Keele, B.F.; Giorgi, E.E.; Salazar-Gonzalez, J.F.; Decker, J.M.; Pham, K.T.; Salazar, M.G.; Sun, C.; Grayson, T.; Wang, S.; Li, H.; et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 2008, 105, 7552-7557.
3. Abrahams, M.R.; Anderson, J.A.; Giorgi, E.E.; Seoighe, C.; Mlisana, K.; Ping, L.H.; Athreya, G.S.; Treurnicht, F.K.; Keele, B.F.; Wood, N. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J. Virol. 2009, 83, 3556-3567.
4. Haaland, R.E.; Hawkins, P.A.; Salazar-Gonzalez, J.; Johnson, A.; Tichacek, A.; Karita, E.; Manigart, O.; Mulenga, J.; Keele, B.F.; Shaw, G.M.; et al. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 2009, 5, e1000274.
5. Kearney, M.; Maldarelli, F.; Shao, W.; Margolick, J.B.; Daar, E.S.; Mellors, J.W.; Rao, V.; Coffin, J.M.; Palmer, S. Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J. Virol. 2009, 83, 2715-2727.
6. Walker, B.D.; Korber, B.T. Immune control of HIV, the obstacles of HLA and viral diversity. Nat. Immunol. 2001, 2, 473-475.
7. Korber, B.; Muldoon, M.; Theiler, J.; Gao, F.; Gupta, R.; Lapedes, A.; Hahn, B.H.; Wolinsky, S.; Bhattacharya, T. Timing the ancestor of the HIV-1 pandemic strains. Science 2000, 288, 1789-1796.
8. Tebit, D.M.; Arts, E.J. Tracking a century of global expansion and evolution of HIV to drive understanding and to combat disease. Lancet Infect Dis 2011, 11, 45-56.
9. Boutwell, C.L.; Rolland, M.M.; Herbeck, J.T.; Mullins, J.I.; Allen, T.M. Viral evolution and escape during acute HIV-1 infection. J. Infect. Dis. 2010, 202, S309-314.
10. Mellors, J.W.; Rinaldo, C.R.J.; Gupta, P.; White, R.M.; Todd, J.A.; Kingsley, L.A. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 1996, 272, 1167-1170.
11. Mellors, J.W.; Muñoz, A.; Giorgi, J.V.; Margolick, J.B.; Tassoni, C.J.; Gupta, P.; Kingsley, L.A.; Todd, J.A.; Saah, A.J.; Detels, R.; et al. Plasma viral load and CD4+ lymphocytes as prognostic markers of HIV-1 infection. Ann Intern Med 1997, 126, 946-954.
12. de Wolf, F.; Spijkerman, I.; Schellekens, P.T.; Langendam, M.; Kuiken, C.; Bakker, M.; Roos, M.; Coutinho, R.; Miedema, F.; Goudsmit, J. AIDS prognosis based on HIV-1 RNA, CD4+ T-cell count and function, markers with reciprocal predictive value over time after seroconversion. AIDS 1997, 11, 1799-1806.
13. Mann, D.L.; Garner, R.P.; Dayoff, D.E.; Cao, K.; Fernandez-Vina, M.A.; Davis, C.; Aronson, N.; Ruiz, N.; Birx, D.L.; Michael, N.L. Major histocompatibility complex genotype is associated with disease progression and virus load levels in a cohort of human immunodeficiency virus type 1-infected Caucasians and African Americans. J. Infect. Dis. 1998, 178, 1799-1802.
14. Lyles, R.H.; Muñoz, A.; Yamashita, T.E.; Bazmi, H.; Detels, R.; Rinaldo, C.R.; Margolick, J.B.; Phair, J.P.; Mellors, J.W. Natural history of human immunodeficiency virus type 1 viremia after seroconversion and proximal to AIDS in a large cohort of homosexual men. Multicenter AIDS Cohort Study. J. Infect. Dis. 2000, 181, 872-880.
15. Gottlieb, G.S.; Sow, P.S.; Hawes, S.E.; Ndoye, I.; Redman, M.; Coll-Seck, A.M.; Faye-Niang, M.A.; Diop, A.; Kuypers, J.M.; Critchlow, C.W.; et al. Equal plasma viral loads predict a similar rate of CD4+ T cell decline in human immunodeficiency virus (HIV) type 1-and HIV-2-infected individuals from Senegal, West Africa. J. Infect. Dis. 2002, 185, 905-914.
16. Mellors, J.W.; Margolick, J.B.; Phair, J.P.; Rinaldo, C.R.; Detels, R.; Jacobson, L.P.; Muñoz, A. Prognostic value of HIV-1 RNA, CD4 cell count, and CD4 Cell count slope for progression to AIDS and death in untreated HIV-1 infection. JAMA 2007, 297, 2349-2350.
17. Lavreys, L.; Baeten, J.M.; Chohan, V.; McClelland, R.S.; Hassan, W.M.; Richardson, B.A.; Mandaliya, K.; Ndinya-Achola, J.O.; Overbaugh, J. Higher set point plasma viral load and more-severe acute HIV type 1 (HIV-1) illness predict mortality among high-risk HIV-1-infected African women. Clin Infect Dis 2006, 42, 1333-1339.
18. Quinn, T.C.; Wawer, M.J.; Sewankambo, N.; Serwadda, D.; Li, C.; Wabwire-Mangen, F.; Meehan, M.O.; Lutalo, T.; Gray, R.H. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Eng J Med 2000, 342, 921-929.
19. Fideli, U.S.; Allen, S.A.; Musonda, R.; Trask, S.; Hahn, B.H.; Weiss, H.; Mulenga, J.; Kasolo, F.; Vermund, S.H.; Aldrovandi, G.M. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Res Hum Retroviruses 2001, 17, 901-910.
20. Daar, E.S.; Moudgil, T.; Meyer, R.D.; Ho, D.D. Transient high levels of viremia in patients with primary HIV-1 infection. N Engl J Med 1991, 324, 961-964.
21. Geskus, R.B.; Prins, M.; Hubert, J.B.; Miedema, F.; Berkhout, B.; Rouzioux, C.; Delfraissy, J.F.; Meyer, L. The HIV RNA setpoint theory revisited. Retrovirology 2007, 4, 65.
22. National Institute of Allergy and Infectious Diseases. What are HIV and AIDS? In, HIV/AIDS. Bethesda, National Institues of Health; 2008.
23. Egger, M.; May, M.; Chêne, G.; Phillips, A.N.; Ledergerber, B.; Dabis, F.; Costagliola, D.; D'Arminio Monforte, A.; de Wolf, F.; Reiss, P.; et al. Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy, a collaborative analysis of prospective studies. Lancet 2002, 360, 119-129.
24. Langford, S.E.; Ananworanich, J.; Cooper, D.A. Predictors of disease progression in HIV infection, a review. AIDS Res Ther 2007, 4, 11.
25. Tang, J.; Kaslow, R.A. The impact of host genetics on HIV infection and disease progression in the era of highly active antiretroviral therapy. AIDS 2003, 17, S51-S60.
26. Carrington, M.; O'Brien, S.J. The influence of HLA genotype on AIDS. Annu Rev Med 2003, 54, 535-551.
27. Streeck, H.; Jolin, J.S.; Qi, Y.; Yassine-Diab, B.; Johnson, R.C.; Kwon, D.S.; Addo, M.M.; Brumme, C.; Routy, J.P.; Little, S.; et al. Human immunodeficiency virus type 1-specific CD8+ T-cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J. Virol. 2009, 83, 7641-7648.
28. Horton, R.; Wilming, L.; Rand, V.; Lovering, R.C.; Bruford, E.A.; Khodiyar, V.K.; Lush, M.J.; Povey, S.; Talbot, C.C.J.; Wright, M.W.; et al. Gene map of the extended human MHC. Nat Rev Genet 2004, 5, 889-899.
29. Carrington, M.; Martin, M.P.; van Bergen, J. KIR-HLA intercourse in HIV disease. Trends Microbiol 2008, 16, 620-627.
30. O'Callaghan, C.A.; Bell, J.I. Structure and function of the human MHC class Ib molecules HLA-E, HLA-F and HLA-G. Immunol Rev 1998, 163, 129-138.
31. Yunis, E.J.; Romero, V.; Diaz-Giffero, F.; Zuniga, J.; Koka, P. Natural killer cell receptor NKG2A/HLA-E interaction dependent differential thymopoiesis of hematopoietic progenitor cells influences the outcome of HIV infection. J Stem Cells 2007, 2, 237-248.
32. Gao, X.; O'Brien, T.R.; Welzel, T.M.; Marti, D.; Qi, Y.; Goedert, J.J.; Phair, J.; Pfeiffer, R.; Carrington, M. HLA-B alleles associate consistently with HIV heterosexual transmission, viral load, and progression to AIDS, but not to susceptability to infection. AIDS 2010, 24, 1835-1840.
33. Leslie, A.; Matthews, P.C.; Listgarten, J.; Carlson, J.M.; Kadie, C.; Ndung'u, T.; Brander, C.; Coovadia, H.; Walker, B.D.; Heckerman, D.; et al. Additive contribution of HLA class I alleles in the immune control of HIV-1 infection. J. Virol. 2010, 84, 9879-9888.
34. Tang, J.; Malhotra, R.; Song, W.; Brill, I.; Hu, L.; Farmer, P.K.; Mulenga, J.; Allen, S.; Hunter, E.; Kaslow, R.A. Human leukocyte antigens and HIV type 1 viral load in early and chronic infections, predominance of evolving relationships. PLoS One 2010, 5, e9629.
35. Lazaryan, A.; Song, W.; Lobashevsky, E.; Tang, J.; Shrestha, S.; Zhang, K.; McNicholl, J.M.; Gardner, L.I.; Wilson, C.M.; Klein, R.S.; et al. The influence of human leukocyte antigen class I alleles and their population frequencies on human immunodeficiency virus type 1 control among African Americans. Hum Immunol 2011, 72, 312-318.
36. Tang, J.; Cormier, E.; Gilmour, J.; Price, M.A.; Prentice, H.A.; Song, W.; Kamali, A.; Karita, E.; Lakhi, S.; Sanders, E.J.; et al. Human leukocyte antigen variants B*44 and B*57 are consistently favorable during two distinct phases of primary HIV-1 infection in sub-Saharan Africans with several viral subtypes. J. Virol. 2011, 85, 8894-8902.
37. Tang, J.; Tang, S.; Lobashevsky, E.; Myracle, A.D.; Fideli, U.; Aldrovandi, G.; Allen, S.; Musonda, R.; Kaslow, R.A.; Zambia-UAB HIV Research Project. Favorable and unfavorable HLA class I alleles and haplotypes in Zambians predominantly infected with clade C human immunodeficiency virus type 1. J. Virol. 2002, 76, 8276-8284.
38. Trachtenberg, E.; Korber, B.; Sollars, C.; Kepler, T.B.; Hraber, P.T.; Hayes, E.; Funkhouser, R.; Fugate, M.; Theiler, J.; Hsu, Y.S.; et al. Advantage of rare HLA supertype in HIV disease progression. Nat Med 2003, 9, 928-935.
39. Matthews, P.C.; Adland, E.; Listgarten, J.; Leslie, A.; Mkhwanazi, N.; Carlson, J.M.; Harndahl, M.; Stryhn, A.; Payne, R.P.; Ogwu, A.; et al. HLA-A*7401-mediated control of HIV viremia is independent of its linkage disequilibrium with HLA-B*5703. J Immunol 2011, 186, 5675-5686.
40. Tang, J.; Shao, W.; Yoo, Y.J.; Brill, I.; Mulenga, J.; Allen, S.; Hunter, E.; Kaslow, R.A. Human leukocyte antigen class I genotypes in relation to heterosexual HIV type 1 transmission within discordant couples. J Immunol 2008, 181, 2626-2635.
41. Julg, B.; Moodley, E.S.; Qi, Y.; Ramduth, D.; Reddy, S.; Mncube, Z.; Gao, X.; Goulder, P.J.; Detels, R.; Ndung'u, T.; et al. Possession of HLA class II DRB1*1303 associates with reduced viral loads in chronic HIV-1 clade C and B infection. J. Infect. Dis. 2011, 203, 803-809.
42. Pereyra, F.; International HIV Controllers Study. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 2010, 330, 1551-1557.
43. Kloverpris, H.N.; Stryhn, A.; Harndahl, M.; van der Stok, M.; Payne, R.P.; Matthews, P.C.; Chen, F.; Riddell, L.; Walker, B.D.; Ndung'u, T.; et al. HLA-B*57 micropolymorphism shapes HLA allele-specific epitope immunogenicity, selection pressure, and HIV immune control. J. Virol. 2012, 86, 919-929.
44. Pelak, K.; Need, A.C.; Fellay, J.; Shianna, K.V.; Feng, S.; Urban, T.J.; Ge, D.; De Luca, A.; Martinez-Picado, J.; Wolinsky, S.M.; et al. Copy number variation of KIR genes influences HIV-1 control. PLoS Biol 2011, 9, e1001208.
45. van Manen, D.; Gras, L.; Boeser-Nunnink, B.D.; van Sighem, A.I.; Mangas Ruiz, M.M.; Harskamp, A.M.; Steingrover, R.; Prins, J.M.; de Wolf, F.; van't Wout, A.B.; et al. Rising HIV-1 viral load set point at a population level coincides with a fading impact of host genetic factors on HIV-1 control. AIDS 2011, 25, 2217-2226.
46. Malhotra, R.; Hu, L.; Song, W.; Brill, I.; Mulenga, J.; Allen, S.; Hunter, E.; Shrestha, S.; Tang, J.; Kaslow, R.A. Association of chemokine receptor gene (CCR2-CCR5) haplotypes with acquisition and control of HIV-1 infection in Zambians. Retrovirology 2011, 8, 22.
47. Hu, L.; Song, W.; Brill, I.; Mulenga, J.; Allen, S.; Hunter, E.; Shrestha, S.; Tang, J.; Kaslow, R.A. Genetic variations and heterosexual HIV-1 infection, analysis of clustered genes encoding CC-motif chemokine ligands. Genes Immun 2012, 13, 202-205.
48. Xu, L.; Li, Q.; Ye, H.; Zhang, Q.; Chen, H.; Huang, F.; Chen, R.; Zhou, R.; Zhou, W.; Xia, P.; et al. The nine-repeat DC-SIGNR isoform is associated with increased HIV-RNA loads and HIV sexual transmission. J Clin Immunol 2010, 30, 402-407.
49. Evangelou, E.; Fellay, J.; Colombo, S.; Martinez-Picado, J.; Obel, N.; Goldstein, D.B.; Telenti, A.; Ioannidis, J.P. Impact of phenotype definition on genome-wide association signals, empirical evaluation in human immunodeficiency virus type 1 infection. Am J Epidemiol 2011, 173, 1336-1342.
50. Pelak, K.; Goldstein, D.B.; Walley, N.M.; Fellay, J.; Ge, D.; Shianna, K.V.; Gumbs, C.; Gao, X.; Maia, J.M.; Cronin, K.D.; et al. Host determinants of HIV-1 control in African Americans. J. Infect. Dis. 2010, 201, 1141-1149.
51. Lingappa, J.R.; Petrovski, S.; Kahle, E.; Fellay, J.; Shianna, K.; McElrath, M.J.; Thomas, K.K.; Baeten, J.M.; Celum, C.; Wald, A.; et al. Genomewide association study for determinants of HIV-1 acquisition and viral set point in HIV-1 serodiscordant couples with quantified virus exposure. PLoS One 2011, 6, e28632.
52. Silva, E.M.; Acosta, A.X.; Santos, E.J.; Netto, E.M.; Lemaire, D.C.; Oliveira, A.S.; Barbosa, C.M.; Bendicho, M.T.; Galvão-Castro, B.; Brites, C. HLA-Bw4-B*57 and Cw*18 alleles are associated with plasma viral load modulation in HIV-1 infected individuals in Salvador, Brazil. Braz J. Infect. Dis. 2010, 14, 468-475.
53. Merino, A.; Malhotra, R.; Morton, M.; Mulenga, J.; Allen, S.; Hunter, E.; Tang, J.; Kaslow, R.A. Impact of a functional KIR2DS4 allele on heterosexual HIV-1 transmission among discordant Zambian couples. J. Infect. Dis. 2011, 203, 487-495.
54. McLaren, P.J.; Ripke, S.; Pelak, K.; Weintrob, A.C.; Patsopoulos, N.A.; Jia, X.; Erlich, R.L.; Lennon, N.J.; Kadie, C.M.; Heckerman, D.; et al. Fine-mapping classical HLA variation associated with durable host control of HIV-1 infection in African Americans. Hum Mol Genet 2012, in press.
55. Koup, R.A.; Graham, B.S.; Douek, D.C. The quest for a T cell-based immune correlate of protection against HIV, a story of trials and errors. Nat Rev Immunol 2011, 11, 65-70.
56. Rousseau, C.M.; Daniels, M.G.; Carlson, J.M.; Kadie, C.; Crawford, H.; Prendergast, A.; Matthews, P.; Payne, R.; Rolland, M.; Raugi, D.N.; et al. HLA class I-driven evolution of human immunodeficiency virus type 1 subtype c proteome, immune escape and viral load. J. Virol. 2008, 82, 6434-6446.
57. Qi, Y.; Martin, M.P.; Gao, X.; Jacobson, L.; Goedert, J.J.; Buchbinder, S.; Kirk, G.D.; O'Brien, S.J.; Trowsdale, J.; Carrington, M. KIR/HLA pleiotropism, protection against both HIV and opportunistic infections. PLoS Pathog 2006, 2, e79.
58. Vilches, C.; Parham, P. KIR, diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 2002, 20, 217-251.
59. Martin, M.P.; Qi, Y.; Gao, X.; Yamada, E.; Martin, J.N.; Pereyra, F.; Colombo, S.; Brown, E.E.; Shupert, W.L.; Phair, J.; et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007, 39, 733-740.
60. Gaudieri, S.; DeSantis, D.; McKinnon, E.; Moore, C.; Nolan, D.; Witt, C.S.; Mallal, S.A.; Christiansen, F.T. Killer immunoglobulin-like receptors and HLA act both independently and synergistically to modify HIV disease progression. Genes Immun 2005, 6, 683-690.
61. Kaslow, R.A.; Dorak, T.; Tang, J.J. Influence of Host Genetic Variation on Susceptibility to HIV Type 1 Infection. J. Infect. Dis. 2005,191, S68-77.
62. Evangelou, E.; Fellay, J.; Colombo, S.; Martinez-Picado, J.; Obel, N.; Goldstein, D.B.; Telenti, A.; Ioannidis, J.P. Impact of phenotype definition on genome-wide association signals, empirical evaluation in human immunodeficiency virus type 1 infection. Am J Epidemiol 2011, 173, 1336-1342.
63. Pelak, K.; Goldstein, D.B.; Walley, N.M.; Fellay, J.; Ge, D.; Shianna, K.V.; Gumbs, C.; Gao, X.; Maia, J.M.; Cronin, K.D.; et al. Host determinants of HIV-1 control in African Americans. J. Infect. Dis. 2010, 201, 1141-1149.
64. Lingappa, J.R.; Petrovski, S.; Kahle, E.; Fellay, J.; Shianna, K.; McElrath, M.J.; Thomas, K.K.; Baeten, J.M.; Celum, C.; Wald, A.; et al. Genomewide association study for determinants of HIV-1 acquisition and viral set point in HIV-1 serodiscordant couples with quantified virus exposure. PLoS One 2011, 6, e28632.
65. Silva, E.M.; Acosta, A.X.; Santos, E.J.; Netto, E.M.; Lemaire, D.C.; Oliveira, A.S.; Barbosa, C.M.; Bendicho, M.T.; Galvão-Castro, B.; Brites, C. HLA-Bw4-B*57 and Cw*18 alleles are associated with plasma viral load modulation in HIV-1 infected individuals in Salvador, Brazil. Braz J. Infect. Dis. 2010, 14, 468-475.
66. Merino, A.; Malhotra, R.; Morton, M.; Mulenga, J.; Allen, S.; Hunter, E.; Tang, J.; Kaslow, R.A. Impact of a functional KIR2DS4 allele on heterosexual HIV-1 transmission among discordant Zambian couples. J. Infect. Dis. 2011, 203, 487-495.
67. McLaren, P.J.; Ripke, S.; Pelak, K.; Weintrob, A.C.; Patsopoulos, N.A.; Jia, X.; Erlich, R.L.; Lennon, N.J.; Kadie, C.M.; Heckerman, D.; et al. Fine-mapping classical HLA variation associated with durable host control of HIV-1 infection in African Americans. Hum Mol Genet 2012, in press.
68. Koup, R.A.; Graham, B.S.; Douek, D.C. The quest for a T cell-based immune correlate of protection against HIV, a story of trials and errors. Nat Rev Immunol 2011, 11, 65-70.
69. Rousseau, C.M.; Daniels, M.G.; Carlson, J.M.; Kadie, C.; Crawford, H.; Prendergast, A.; Matthews, P.; Payne, R.; Rolland, M.; Raugi, D.N.; et al. HLA class I-driven evolution of human immunodeficiency virus type 1 subtype c proteome, immune escape and viral load. J. Virol. 2008, 82, 6434-6446.
70. Qi, Y.; Martin, M.P.; Gao, X.; Jacobson, L.; Goedert, J.J.; Buchbinder, S.; Kirk, G.D.; O'Brien, S.J.; Trowsdale, J.; Carrington, M. KIR/HLA pleiotropism, protection against both HIV and opportunistic infections. PLoS Pathog 2006, 2, e79.
71. Vilches, C.; Parham, P. KIR, diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 2002, 20, 217-251.
72. Martin, M.P.; Qi, Y.; Gao, X.; Yamada, E.; Martin, J.N.; Pereyra, F.; Colombo, S.; Brown, E.E.; Shupert, W.L.; Phair, J.; et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007, 39, 733-740.
73. Gaudieri, S.; DeSantis, D.; McKinnon, E.; Moore, C.; Nolan, D.; Witt, C.S.; Mallal, S.A.; Christiansen, F.T. Killer immunoglobulin-like receptors and HLA act both independently and synergistically to modify HIV disease progression. Genes Immun 2005, 6, 683-690.
74. Kaslow, R.A.; Dorak, T.; Tang, J.J. Influence of Host Genetic Variation on Susceptibility to HIV Type 1 Infection. J. Infect. Dis. 2005,191, S68-77. Viruses 2012, 4 2093
75. Tang, J.; Shelton, B.; Makhatadze, N.J.; Zhang, Y.; Schaen, M.; Louie, L.G.; Goedert, J.J.; Seaberg, E.C.; Margolick, J.B.; Mellors, J.; et al. Distribution of chemokine receptor CCR2 and CCR5 genotypes and their relative contribution to human immunodeficiency virus type 1 (HIV-1) seroconversion, early HIV-1 RNA concentration in plasma, and later disease progression. J. Virol. 2002, 76, 662-672.
76. Katzenstein, T.L.; Eugen-Olsen, J.; Hofmann, B.; Benfield, T.; Pedersen, C.; Iversen, A.K.; Sørensen, A.M.; Garred, P.; Koppelhus, U.; Svejgaard, A.; et al. HIV-infected individuals with the CCR delta32/CCR5 genotype have lower HIV RNA levels and higher CD4 cell counts in the early years of the infection than do patients with the wild type. Copenhagen AIDS Cohort Study Group. J Acquir Immune Defic Syndr Hum Retrovirol 1997, 16, 10-14.
77. Meyer, L.; Magierowska, M.; Hubert, J.B.; Rouzioux, C.; Deveau, C.; Sanson, F.; Debre, P.; Delfraissy, J.F.; Theodorou, I. Early protective effect of CCR-5 delta 32 heterozygosity on HIV-1 disease progression, relationship with viral load. The SEROCO Study Group. AIDS 1997, 11, F73-78.
78. Ioannidis, J.P.; Rosenberg, P.S.; Goedert, J.J.; Ashton, L.J.; Benfield, T.L.; Buchbinder, S.P.; Coutinho, R.A.; Eugen-Olsen, J.; Gallart, T.; Katzenstein, T.L.; et al. Effects of CCR5-Delta32, CCR2-64I, and SDF-1 3'A alleles on HIV-1 disease progression, An international meta-analysis of individual-patient data. Ann Intern Med 2001, 135, 782-795.
79. Shrestha, S.; Tang, J.; Kaslow, R.A. Gene copy number, learning to count past two. Nat Med 2009, 15, 1127-1129.
80. Liu, H.; Carrington, M.; Wang, C.; Holte, S.; Lee, J.; Greene, B.; Hladik, F.; Koelle, D.M.; Wald, A.; Kurosawa, K.; et al. 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. 2006, 193, 698-702.
81. Geijtenbeek, T.B.; van Duijnhoven, G.C.; van Vliet, S.J.; Krieger, E.; Vriend, G.; Figdor, C.G.; van Kooyk, Y. Identification of different binding sites in the dendritic cell-specific receptor DC-SIGN for intercellular adhesion molecule 3 and HIV-1. J Biol Chem 2002, 277, 11314-11320.
82. Fellay, J.; Shianna, K.V.; Ge, D.; Colombo, S.; Ledergerber, B.; Weale, M.; Zhang, K.; Gumbs, C.; Castagna, A.; Cossarizza, A.; et al. A whole-genome association study of major determinants for host control of HIV-1. Science 2007, 317, 944-947.
83. Dalmasso, C.; Carpentier, W.; Meyer, L.; Rouzioux, C.; Goujard, C.; Chaix, M.L.; Lambotte, O.; Avettand-Fenoel, V.; Le Clerc, S.; de Senneville, L.D.; et al. Distinct genetic loci control plasma HIV-RNA and cellular HIV-DNA levels in HIV-1 infection, the ANRS genome wide association 01 study. PLoS One 2008, 3, e3907.
84. Catano, G.; Kulkarni, H.; He, W.; Marconi, V.C.; Agan, B.K.; Landrum, M.; Anderson, S.; Delmar, J.; Telles, V.; Song, L.; et al. HIV-1 disease-influencing effects associated with ZNRD1, HCP5 and HLA-C alleles are attributable mainly to either HLA-A10 or HLA-B*57 alleles. PLoS One 2008, 3, e3636.
85. Fellay, J.; Ge, D.; Shianna, K.V.; Colombo, S.; Ledergerber, B.; Cirulli, E.T.; Urban, T.J.; Zhang, K.; Gumbs, C.; Smith, J.P.; et al. Common genetic variation and the control of HIV-1 in humans. PLoS Genet 2009, 5, e1000791.
86. Thomas, R.; Apps, R.; Qi, Y.; Gao, X.; Male, V.; O'hUiqin, C.; O'Conner, G.; Ge, D.; Fellay, J.; Martin, J.N.; et al. HLA-C cell surface expression and control of HIV/AIDS correlate with a variant upstream of HLA-C. Nat Genet 2009, 41, 1290-1294.
87. van Manen, D.; Kootstra, N.A.; Boeser-Nunnink, B.; Handulle, M.A.M.; van't Wout, A.B.; Schuitemaker, H. Association of HLA-C and HCP5 gene regions with the clinical course of HIV-1 infection. AIDS 2009, 23, 19-28.
88. Guergnon, J.; Theodorou, I. What did we learn on host's genetics by studying large cohorts of HIV-1-infected patients in the genome-wide association era? Current Opinion in HIV and AIDS 2011, 6, 290-296.
89. Aouizerat, B.E.; Pearce, C.L.; Miaskowski, C. The search for host genetic factors of HIV/AIDS pathogenesis in the post-genome era, progress to date and new avenues for discovery. Curr HIV/AIDS Rep 2011, 8, 38-44.
90. Kulkarni, S.; Savan, R.; Qi, Y.; Gao, X.; Yuki, Y.; Bass, S.E.; Martin, M.P.; Hunt, P.; Deeks, S.G.; Telenti, A.; et al. Differential microRNA regulation of HLA-C expression and its association with HIV control. Nature 2011, 472, 495-498.
91. Shrestha, S.; Aissani, B.; Song, W.; Wilson, C.M.; Kaslow, R.A.; Tang, J. Host genetics and HIV-1 viral load set-point in African Americans. AIDS 2009, 23, 673-677.
92. Trachtenberg, E.; Bhattacharya, T.; Ladner, M.; Phair, J.; Erlich, H.; Wolinsky, S. The HLA-B/C haplotype block contains major determinants for host control of HIV. Genes Immun 2009, 10, 673-677.
93. Learmont, J.C.; Geczy, A.F.; Mills, J.; Ashton, L.J.; Raynes-Greenow, C.H.; Garsia, R.J.; Dyer, W.B.; McIntyre, L.; Oelrichs, R.B.; Rhodes, D.I.; et al. Immunologic and virologic status after 14 to 18 years of infection with an attenuated strain of HIV-1. A report from the Sydney Blood Bank Cohort. N Engl J Med 1999, 340, 1715-1722.
94. Zaunders, J.; Dyer, W.B.; Churchill, M. The Sydney Blood Bank Cohort, implications for viral fitness as a cause of elite control. Curr Opin HIV AIDS 2011, 6, 151-156.
95. Bailey, J.R.; O'Connell, K.; Yang, H.C.; Han, Y.; Xu, J.; Jilek, B.; Williams, T.M.; Ray, S.C.; Siliciano, R.F.; Blankson, J.N. Transmission of human immunodeficiency virus type 1 from a patient who developed AIDS to an elite suppressor. J. Virol. 2008, 82, 7395-7410.
96. Hollingsworth, T.D.; Laeyendecker, O.; Shirreff, G.; Donnelly, C.A.; Serwadda, D.; Wawer, M.J.; Kiwanuka, N.; Nalugoda, F.; Collinson-Streng, A.; Ssempijja, V.; et al. HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda. PLoS Pathog 2010, 6, e1000876.
97. Alizon, S.; von Wyl, V.; Stadler, T.; Kouyos, R.D.; Yerly, S.; Hirschel, B.; Boni, J.; Shah, C.; Klimkait, T.; Furrer, H.; et al. Phylogenetic approach reveals that virus genotype largely determines HIV set-point viral load. PLoS Pathog 2010, 6, e1001123.
98. Tang, J.; Tang, S.; Lobashevsky, E.; Zulu, I.; Aldrovandi, G.; Allen, S.; Kaslow, R.A.; Zambia-UAB HIV Research Project. HLA allele sharing and HIV type 1 viremia in seroconverting Zambians with known transmitting partners. AIDS Res Hum Retroviruses 2004, 20, 19-25.
99. Novitsky, V.; Gilbert, P.; Peter, T.; McLane, M.F.; Gaolekwe, S.; Rybak, N.; Thior, I.; Ndung'u, T.; Marlink, R.; Lee, T.H.; et al. Association between virus-specific T-cell responses and plasma viral load in human immunodeficiency virus type 1 subtype C infection. J. Virol. 2003, 77, 882-890.
100. Mei, Y.; Wang, L.; Holte, S.E. A comparison of methods for determining HIV viral set point. Stat Med 2008, 27, 121-139.
101. Mellors, J.W.; Kingsley, L.A.; Rinaldo, C.R.J.; Todd, J.A.; Hoo, B.S.; Kokka, R.P.; Gupta, P. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann Intern Med 1995, 122, 573-579.
102. Hubert, J.B.; Burgard, M.; Dussaix, E.; Tamalet, C.; Deveau, C.; Le Chenadec, J.; Chaix, M.L.; Marchadier, E.; Vildé, J.L.; Delfraissy, J.F.; et al. Natural history of serum HIV-1 RNA levels in 330 patients with a known date of infection. The SEROCO Study Group. AIDS 2000, 14, 123-131.
103. Dorrucci, M.; Rezza, G.; Porter, K.; Phillips, A.; Concerted Action on Seroconversion to AIDS and Death in Europe Collaboration. Temporal trends in postseroconversion CD4 cell count and HIV load, the Concerted Action on Seroconversion to AIDS and Death in Europe Collaboration, 1985-2002. J. Infect. Dis. 2007, 195, 525-534.
104. Gras, L.; Jurriaans, S.; Bakker, M.; van Sighem, A.; Bezemer, D.; Fraser, C.; Lange, J.; Prins, J.M.; Berkhout, B.; de Wolf, F. Viral load levels measured at set-point have risen over the last decade of the HIV epidemic in the Netherlands. PLoS One 2009, 4, e7365.
105. Müller, V.; Maggiolo, F.; Suter, F.; Ladisa, N.; De Luca, A.; Antinori, A.; Sighinolfi, L.; Quiros-Roldan, E.; Carosi, G.; Torti, C. Increasing clinical virulence in two decades of the Italian HIV epidemic. PLoS One 2009, 5, e1000454.
106. Müller, V.; Ledergerber, B.; Perrin, L.; Klimkait, T.; Furrer, H.; Telenti, A.; Bernasconi, E.; Vernazza, P.; Günthard, H.F.; Bonhoeffer, S.; et al. Stable virulence levels in the HIV epidemic of Switzerland over two decades. AIDS 2006, 20, 889-894.
107. Potard, V.; Weiss, L.; Lamontagne, F.; Rouveix, E.; Beck-Wirth, G.; Drogoul-Vey, M.P.; Souala, M.F.; Costagliola, D.; French Hospital Database on HIV ANRS CO4. Trends in post-infection CD4 cell counts and plasma HIV-1 RNA levels in HIV-1-infected patients in France between 1997 and 2005. J Acquir Immune Defic Syndr 2009, 52, 422-426.
108. Troude, P.; Chaix, M.L.; Tran, L.; Deveau, C.; Seng, R.; Delfraissy, J.F.; Rouzioux, C.; Goujard, C.; Meyer, L.; ANRS Primo Cohort. No evidence of a change in HIV-1 virulence since 1996 in France. AIDS 2009, 23, 1261-1267.
109. Herbeck, J.T.; Muller, V.; Maust, B.S.; Ledergerber, B.; Torti, C.; Di Giambenedetto, S.; Gras, L.; Gunthard, H.F.; Jacobson, L.P.; Mullins, J.I.; et al. Is the virulence of HIV changing? A meta-analysis of trends in prognostic markers of HIV disease progression and transmission. AIDS 2012, 26, 193-205.
110. Moore, C.B.; John, M.; James, I.R.; Christiansen, F.T.; Witt, C.S.; Mallal, S. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 2002, 296, 1439-1443.
111. Koga, M.; Kawana-Tachikawa, A.; Heckerman, D.; Odawara, T.; Nakamura, H.; Koibuchi, T.; Fujii, T.; Miura, T.; Iwamoto, A. Changes in impact of HLA class I allele expression on HIV-1 plasma virus loads at a population level over time. Microbiol Immunol 2010, 54, 196-205.
112. Kawashima, Y.; Pfafferott, K.; Frater, J.; Matthews, P.; Payne, R.; Addo, M.; Gatanaga, H.; Fujiwara, M.; Hachiya, A.; Koizumi, H.; et al. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009, 458, 641-645.
113. Peeters, M. The genetic variability of HIV-1 and its implications. Transfus Clin Biol 2001, 8, 222-225.
114. Eberle, J.; Gurtler, L. HIV types, groups, subtypes and recombinant forms, errors in replication, selection pressure and quasispecies. Intervirology 2012, 55, 79-83.
115. Saah, A.J.; Hoover, D.R.; Weng, S.; Carrington, M.; Mellors, J.; Rinaldo, C.R.J.; Mann, D.; Apple, R.; Phair, J.P.; Detels, R.; et al. Association of HLA profiles with early plasma viral load, CD4+ cell count and rate of progression to AIDS following acute HIV-1 infection. Multicenter AIDS Cohort Study. AIDS 1998, 12, 2107-2113.