Mechanisms of human natural resistance to HIV: A summary of ten years of research in the Colombian population
Keywords:
HIV, acquired immunodeficiency syndrome, infection control, HLA antigens, receptors, CCR5, killer cells, natural, apoptosis, defensins
Abstract
The natural history of human immunodeficiency virus type-1 (HIV-1) infection is a complex and variable process that, similarly to other infections, has clearly demonstrated the existence of mechanisms of human natural resistance. The resistance either inhibits the establishment of infection or delays disease progression. When there is continuous exposure to infectious viral particles, several genetic and immunological mechanisms are essential to lead to resistance to HIV-1 infection/progression. The objective of this manuscript was to review the different mechanisms so far proposed to be responsible for HIV-1 resistance and to present the main results derived from 10 years of research in this area among Colombian subjects. In particular, this review focuses on determining the mechanisms involved in the protection of a group of individuals repeatedly exposed to the virus but who remained exempt of serological and clinical evidence of HIV-1 infection. Although the studies carried out in our research group corroborated the protective role of some of the previously proposed mechanisms of protection, ongoing research worldwide has made it clear that the phenomenon of human natural resistance depends on multiple factors with an important genetic influence, and only multicenter studies involving individuals with different genetic backgrounds may determine more universal mechanisms of resistance. Increasing our knowledge in this field will contribute to the development of novel preventive and therapeutic measures.Downloads
Download data is not yet available.
References
1. UNAIDS, WHO. Colombia: Epidemiological fact sheets on HIV/AIDS and sexually transmitted infections. Geneva: UNAIDS; 2004.
2. Summers T. Public policy for health care workers infected with the human immunodeficiency virus. JAMA. 2001;285:882.
3. Shattock RJ, Moore JP. Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol. 2003;1:25-34.
4. Mann JM, Tarantola DJ. HIV 1998: The global picture. Sci Am. 1998;279:82-3.
5. Kedzierska K, Crowe SM. The role of monocytes and macrophages in the pathogenesis of HIV-1 infection. Curr Med Chem. 2002;9:1893-903.
6. MacDougall TH, Shattock RJ, Madsen C, Chain BM, Katz DR. Regulation of primary HIV-1 isolate replication in dendritic cells. Clin Exp Immunol. 2002;127:66-71.
7. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 1996;381:661-6.
8. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, et al. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature. 1996;381:667-73.
9. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity. 2002;16:135-44.
10. Lambert AA, Gilbert C, Richard M, Beaulieu AD, Tremblay MJ. The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood. 2008;112:1299-307.
11. Trujillo JR, Rogers R, Molina RM, Dangond F, McLane MF, Essex M, et al. Noninfectious entry of HIV-1 into peripheral and brain macrophages mediated by the mannose receptor. Proc Natl Acad Sci USA. 2007;104:5097-102.
12. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, Southern PJ, et al. Glycerol monolaurate prevents mucosal SIV transmission. Nature. 2009;458:1034-8.
13. Buchbinder SP, Katz MH, Hessol NA, O'Malley PM, Holmberg SD. Long-term HIV-1 infection without immunologic progression. AIDS. 1994;8:1123-8.
14. Cao Y, Qin L, Zhang L, Safrit J, Ho DD. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med. 1995;332:201-8.
15. Paxton WA, Martin SR, Tse D, O'Brien TR, Skurnick J, VanDevanter NL, et al. Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposure. Nat Med. 1996;2:412-7.
16. Goh WC, Markee J, Akridge RE, Meldorf M, Musey L, Karchmer T, et al. 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. 1999;179:548-57.
17. Stranford SA, Skurnick J, Louria D, Osmond D, Chang SY, Sninsky J, et al. Lack of infection in HIV-exposed individuals is associated with a strong CD8(+) cell noncytotoxic anti-HIV response. Proc Natl Acad Sci USA. 1999;96:1030-5.
18. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, et al. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature. 1996;382:722-5.
19. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, et al. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell. 1996;86:367-77.
20. Huang Y, Paxton WA, Wolinsky SM, Neumann AU, Zhang L, He T, et al. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med. 1996;2:1240-3.
21. Rugeles MT, Solano F, Díaz FJ, Bedoya VI, Patino PJ. Molecular characterization of the CCR 5 gene in seronegative individuals exposed to human immunodeficiency virus (HIV). J Clin Virol. 2002;23:161-9.
22. Smith MW, Dean M, Carrington M, Winkler C, Huttley GA, Lomb DA, et al. Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study. Science. 1997;277:959-65.
23. Winkler C, Modi W, Smith MW, Nelson GW, Wu X, Carrington M, et al. Genetic restriction of AIDS pathogenesis by an SDF-1 chemokine gene variant. ALIVE Study, Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC). Science. 1998;279:389-93.
24. MacDonald KS, Fowke KR, Kimani J, Dunand VA, Nagelkerke NJ, Ball TB, et al. Influence of HLA supertypes on susceptibility and resistance to human immunodeficiency virus type 1 infection. J Infect Dis. 2000;181:1581-9.
25. Mikhail M, Wang B, Saksena NK. Mechanisms involved in non-progressive HIV disease. AIDS Rev. 2003;5:230-44.
26. Hildeman D, Jorgensen T, Kappler J, Marrack P. Apoptosis and the homeostatic control of immune responses. Curr Opin Immunol. 2007;19:516-21.
27. Rojas M, Barrera LF, Puzo G, García LF. Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages: role of nitric oxide and mycobacterial products. J Immunol. 1997;159:1352-61.
28. Clem RJ, Fechheimer M, Miller LK. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science. 1991;254:1388-90.
29. Clouston WM, Kerr JF. Apoptosis, lymphocytotoxicity and the containment of viral infections. Med Hypotheses. 1985;18:399-404.
30. Wallace M, Malkovsky M, Carding SR. Gamma/delta T lymphocytes in viral infections. J Leukoc Biol. 1995;58:277-83.
31. Welsh RM, Lin MY, Lohman BL, Varga SM, Zarozinski CC, Selin LK. Alpha beta and gamma delta T-cell networks and their roles in natural resistance to viral infections. Immunol Rev. 1997;159:79-93.
32. Selin LK, Santolucito PA, Pinto AK, Szomolanyi-Tsuda E, Welsh RM. Innate immunity to viruses: Control of vaccinia virus infection by gamma delta T cells. J Immunol. 2001;166:6784-94.
33. DeVico AL, Gallo RC. Control of HIV-1 infection by soluble factors of the immune response. Nat Rev Microbiol. 2004;2:401-13.
34. Sierra S, Kupfer B, Kaiser R. Basics of the virology of HIV-1 and its replication. J Clin Virol. 2005;34:233-44.
35. Cheng-Mayer C, Liu R, Landau NR, Stamatatos L. Macrophage tropism of human immunodeficiency virus type 1 and utilization of the CC-CKR5 coreceptor. J Virol. 1997;71:1657-61.
36. Gonzalez E, Bamshad M, Sato N, Mummidi S, Dhanda R, Catano G, et al. Race-specific HIV-1 disease-modifying effects associated with CCR5 haplotypes. Proc Natl Acad Sci USA. 1999;96:12004-9.
37. Díaz FJ, Vega JA, Patino PJ, Bedoya G, Nagles J, Villegas C, et al. Frequency of CCR5 delta-32 mutation in human immunodeficiency virus (HIV)-seropositive and HIV-exposed seronegative individuals and in general population of Medellin, Colombia. Mem Inst Oswaldo Cruz. 2000;95:237-42.
38. O'Brien SJ, Gao X, Carrington M. HLA and AIDS: a cautionary tale. Trends Mol Med. 2001;7:379-81.
39. Hendel H, Caillat-Zucman S, Lebuanec H, Carrington M, O'Brien S, Andrieu JM, et al. New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. J Immunol. 1999;162:6942-6.
40. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med. 1996;2:405-11.
41. Gillespie GM, Kaul R, Dong T, Yang HB, Rostron T, Bwayo JJ, et al. Cross-reactive cytotoxic T lymphocytes against a HIV-1 p24 epitope in slow progressors with B*57. AIDS. 2002;16:961-72.
42. Migueles SA, Sabbaghian MS, Shupert WL, Bettinotti MP, Marincola FM, Martino L, et al. HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc Natl Acad Sci USA. 2000;97:2709-14.
43. MacDonald KS, Embree J, Njenga S, Nagelkerke NJ, Ngatia I, Mohammed Z, et al. Mother-child class I HLA concordance increases perinatal human immunodeficiency virus type 1 transmission. J Infect Dis. 1998;177:551-6.
44. Rugeles MT, Shearer GM. Alloantigen recognition in utero: Dual advantage for the fetus? Trends Immunol. 2004;25:348-52.
45. MacDonald KS, Embree JE, Nagelkerke NJ, Castillo J, Ramhadin S, Njenga S, et al. The HLA A2/6802 supertype is associated with reduced risk of perinatal human immunodeficiency virus type 1 transmission. J Infect Dis. 2001;183:503-6.
46. Bedoya VI, Jaimes FA, Delgado JC, Rugeles C, Usuga X, Zapata W, et al. Fetal-maternal HLA-A and -B discordance is associated with placental RNase expression and anti-HIV-1 activity. Curr HIV Res. 2008;6:380-7.
47. O'Brien V. Viruses and apoptosis. J Gen Virol. 1998;79:1833-45.
48. Benedict CA, Norris PS, Ware CF. To kill or be killed: Viral evasion of apoptosis. Nat Immunol. 2002;3:1013-8.
49. Fesq H, Bacher M, Nain M, Gemsa D. Programmed cell death (apoptosis) in human monocytes infected by influenza A virus. Immunobiology. 1994;190:175-82.
50. Jelachich ML, Lipton HL. Theiler's murine encephalomyelitis virus kills restrictive but not permissive cells by apoptosis. J Virol. 1996;70:6856-61.
51. Crowe SM, Sonza S. HIV-1 can be recovered from a variety of cells including peripheral blood monocytes of patients receiving highly active antiretroviral therapy: A further obstacle to eradication. J Leukoc Biol. 2000;68:345-50.
52. Lewin SR, Kirihara J, Sonza S, Irving L, Mills J, Crowe SM. HIV-1 DNA and mRNA concentrations are similar in peripheral blood monocytes and alveolar macrophages in HIV-1-infected individuals. AIDS.1998;12:719-27.
53. Cassol E, Alfano M, Biswas P, Poli G. Monocyte-derived macrophages and myeloid cell lines as targets of HIV-1 replication and persistence. J Leukoc Biol. 2006;80: 1018-30.
54. Rich EA, Chen IS, Zack JA, Leonard ML, O'Brien WA. Increased susceptibility of differentiated mononuclear phagocytes to productive infection with human immuno- deficiency virus-1 (HIV-1). J Clin Invest. 1992;89:176-83.
55. Sonza S, Maerz A, Uren S, Violo A, Hunter S, Boyle W, et al. Susceptibility of human monocytes to HIV type 1 infection in vitro is not dependent on their level of CD4 expression. AIDS Res Hum Retroviruses. 1995;11:769-76.
56. Lewin SR, Lambert P, Deacon NJ, Mills J, Crowe SM. Constitutive expression of p50 homodimer in freshly isolated human monocytes decreases with in vitro and in vivo differentiation: A possible mechanism influencing human immunodeficiency virus replication in monocytes and mature macrophages. J Virol. 1997;71:2114-9.
57. Naif HM, Li S, Alali M, Sloane A, Wu L, Kelly M, et al. CCR5 expression correlates with susceptibility of maturing monocytes to human immunodeficiency virus type 1 infection. J Virol. 1998;72:830-6.
58. Velilla PA, Hoyos A, Rojas M, Patino PJ, Vélez LA, Rugeles MT. Apoptosis as a mechanism of natural resistance to HIV-1 infection in an exposed but uninfected population. J Clin Virol. 2005;32:329-35.
59. Lehner T, Wang Y, Pido-López J, Whittall T, Bergmeier LA, Babaahmady K. The emerging role of innate immunity in protection against HIV-1 infection. Vaccine. 2008;26:2997-3001.
60. Medzhitov R, Janeway C Jr. Innate immunity. N Engl J Med. 2000;343:338-44.
61. Levy JA, Scott I, Mackewicz C. Protection from HIV/AIDS: The importance of innate immunity. Clin Immunol. 2003;108:167-74.
62. Donaghy H, Pozniak A, Gazzard B, Qazi N, Gilmour J, Gotch F, et al. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood. 2001;98:2574-6.
63. Motsinger A, Haas DW, Stanic AK, van Kaer L, Joyce S, Unutmaz D. CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J Exp Med. 2002;195:869-79.
64. Soumelis V, Scott I, Gheyas F, Bouhour D, Cozon G, Cotte L, et al. Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients. Blood. 2001;98:906-12.
65. Sandberg JK, Fast NM, Palacios EH, Fennelly G, Dobroszycki J, Palumbo P, et al. Selective loss of innate CD4(+) V alpha 24 natural killer T cells in human immunodeficiency virus infection. J Virol. 2002;76:7528-34.
66. Montoya CJ, Velilla PA, Chougnet C, Landay AL, Rugeles MT. Increased IFN-gamma production by NK and CD3+/CD56+ cells in sexually HIV-1-exposed but uninfected individuals. Clin Immunol. 2006;120:138-46.
67. Clerici M. Cell-mediated immunity in HIV infection. AIDS. 1993;7 (Suppl.1):S135-40.
68. Mazzoli S, Trabattoni D, Lo Caputo S, Piconi S, Ble C, Meacci F, et al. HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat Med. 1997;3:1250-7.
69. Rowland-Jones SL, Nixon DF, Aldhous MC, Gotch F, Ariyoshi K, Hallam N, et al. HIV-specific cytotoxic T-cell activity in an HIV-exposed but uninfected infant. Lancet. 1993;341:860-1.
70. Kuhn L, Meddows-Taylor S, Gray G, Tiemessen C. Human immunodeficiency virus (HIV)-specific cellular immune responses in newborns exposed to HIV in utero. Clin Infect Dis. 2002;34:267-76.
71. Rowland-Jones S, Sutton J, Ariyoshi K, Dong T, Gotch F, McAdam S, et al. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat Med. 1995;1:59-64.
72. Rowland-Jones SL, Dong T, Dorrell L, Ogg G, Hansasuta P, Krausa P, et al. Broadly cross-reactive HIV-specific cytotoxic T-lymphocytes in highly-exposed persistently seronegative donors. Immunol Lett. 1999;66:9-14.
73. Pinto LA, Sullivan J, Berzofsky JA, Clerici M, Kessler HA, Landay AL, et al. ENV-specific cytotoxic T lymphocyte responses in HIV seronegative health care workers occupationally exposed to HIV-contaminated body fluids. J Clin Invest. 1995;96:867-76.
74. Schenal M, Lo Caputo S, Fasano F, Vichi F, Saresella M, Pierotti P, et al. Distinct patterns of HIV-specific memory T lymphocytes in HIV-exposed uninfected individuals and in HIV-infected patients. AIDS. 2005;19:653-61.
75. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science. 1995;270:1811-5.
76. Walker CM, Moody DJ, Stites DP, Levy JA. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 1986;234:1563-6.
77. Alfano M, Poli G. Role of cytokines and chemokines in the regulation of innate immunity and HIV infection. Mol Immunol. 2005;42:161-82.
78. Patterson BK, Behbahani H, Kabat WJ, Sullivan Y, O'Gorman MR, Landay A, et al. Leukemia inhibitory factor inhibits HIV-1 replication and is upregulated in placentae from nontransmitting women. J Clin Invest. 2001;107:287-94.
79. Lee-Huang S, Huang PL, Sun Y, Kung HF, Blithe DL, Chen HC. Lysozyme and RNases as anti-HIV components in beta-core preparations of human chorionic gonadotropin. Proc Natl Acad Sci U S A. 1999;96:2678-81.
80. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, Rangel HR, et al. Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. AIDS. 2003;17:F39-48.
81. Chang TL, Vargas J Jr, Del Portillo A, Klotman ME. Dual role of alpha-defensin-1 in anti-HIV-1 innate immunity. J Clin Invest. 2005;115:765-73.
82. Garcia JR, Krause A, Schulz S, Rodríguez-Jiménez FJ, Kluver E, Adermann K, et al. Human beta-defensin 4: A novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J. 2001;15:1819-21.
83. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol. 2000;1:113-8.
84. Valore EV, Park CH, Quayle AJ, Wiles KR, McCray PB Jr., Ganz T. Human beta-defensin-1: an antimicrobial peptide of urogenital tissues. J Clin Invest. 1998;101:1633-42.
85. Trabattoni D, Caputo SL, Maffeis G, Vichi F, Biasin M, Pierotti P, et al. Human alpha defensin in HIV-exposed but uninfected individuals. J Acquir Immune Defic Syndr. 2004;35:455-63.
86. Ganz T. Defensins:A peptides of vertebrates. C R Biol. 2004;327:539-49.
87. Schutte BC, Mitros JP, Bartlett JA, Walters JD, Jia HP, Welsh MJ, et al. Discovery of five conserved beta -defensin gene clusters using a computational search strategy. Proc Natl Acad Sci USA. 2002;99:2129-33.
88. Jurevic RJ, Bai M, Chadwick RB, White TC, Dale BA. Single-nucleotide polymorphisms (SNPs) in human beta-defensin 1: High-throughput SNP assays and association with Candida carriage in type I diabetics and nondiabetic controls. J Clin Microbiol. 2003;41:90-6.
89. Jurevic RJ, Chrisman P, Mancl L, Livingston R, Dale BA. Single-nucleotide polymorphisms and haplotype analysis in beta-defensin genes in different ethnic populations. Genet Test. 2002;6:261-9.
90. Zapata W, Rodríguez B, Weber J, Estrada H, Quinones-Mateu ME, Zimermman PA, et al. Increased levels of human beta-defensins mRNA in sexually HIV-1 exposed but uninfected individuals. Curr HIV Res. 2008;6:531-8
2. Summers T. Public policy for health care workers infected with the human immunodeficiency virus. JAMA. 2001;285:882.
3. Shattock RJ, Moore JP. Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol. 2003;1:25-34.
4. Mann JM, Tarantola DJ. HIV 1998: The global picture. Sci Am. 1998;279:82-3.
5. Kedzierska K, Crowe SM. The role of monocytes and macrophages in the pathogenesis of HIV-1 infection. Curr Med Chem. 2002;9:1893-903.
6. MacDougall TH, Shattock RJ, Madsen C, Chain BM, Katz DR. Regulation of primary HIV-1 isolate replication in dendritic cells. Clin Exp Immunol. 2002;127:66-71.
7. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 1996;381:661-6.
8. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, et al. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature. 1996;381:667-73.
9. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity. 2002;16:135-44.
10. Lambert AA, Gilbert C, Richard M, Beaulieu AD, Tremblay MJ. The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood. 2008;112:1299-307.
11. Trujillo JR, Rogers R, Molina RM, Dangond F, McLane MF, Essex M, et al. Noninfectious entry of HIV-1 into peripheral and brain macrophages mediated by the mannose receptor. Proc Natl Acad Sci USA. 2007;104:5097-102.
12. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, Southern PJ, et al. Glycerol monolaurate prevents mucosal SIV transmission. Nature. 2009;458:1034-8.
13. Buchbinder SP, Katz MH, Hessol NA, O'Malley PM, Holmberg SD. Long-term HIV-1 infection without immunologic progression. AIDS. 1994;8:1123-8.
14. Cao Y, Qin L, Zhang L, Safrit J, Ho DD. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med. 1995;332:201-8.
15. Paxton WA, Martin SR, Tse D, O'Brien TR, Skurnick J, VanDevanter NL, et al. Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposure. Nat Med. 1996;2:412-7.
16. Goh WC, Markee J, Akridge RE, Meldorf M, Musey L, Karchmer T, et al. 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. 1999;179:548-57.
17. Stranford SA, Skurnick J, Louria D, Osmond D, Chang SY, Sninsky J, et al. Lack of infection in HIV-exposed individuals is associated with a strong CD8(+) cell noncytotoxic anti-HIV response. Proc Natl Acad Sci USA. 1999;96:1030-5.
18. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, et al. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature. 1996;382:722-5.
19. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, et al. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell. 1996;86:367-77.
20. Huang Y, Paxton WA, Wolinsky SM, Neumann AU, Zhang L, He T, et al. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med. 1996;2:1240-3.
21. Rugeles MT, Solano F, Díaz FJ, Bedoya VI, Patino PJ. Molecular characterization of the CCR 5 gene in seronegative individuals exposed to human immunodeficiency virus (HIV). J Clin Virol. 2002;23:161-9.
22. Smith MW, Dean M, Carrington M, Winkler C, Huttley GA, Lomb DA, et al. Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study. Science. 1997;277:959-65.
23. Winkler C, Modi W, Smith MW, Nelson GW, Wu X, Carrington M, et al. Genetic restriction of AIDS pathogenesis by an SDF-1 chemokine gene variant. ALIVE Study, Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC). Science. 1998;279:389-93.
24. MacDonald KS, Fowke KR, Kimani J, Dunand VA, Nagelkerke NJ, Ball TB, et al. Influence of HLA supertypes on susceptibility and resistance to human immunodeficiency virus type 1 infection. J Infect Dis. 2000;181:1581-9.
25. Mikhail M, Wang B, Saksena NK. Mechanisms involved in non-progressive HIV disease. AIDS Rev. 2003;5:230-44.
26. Hildeman D, Jorgensen T, Kappler J, Marrack P. Apoptosis and the homeostatic control of immune responses. Curr Opin Immunol. 2007;19:516-21.
27. Rojas M, Barrera LF, Puzo G, García LF. Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages: role of nitric oxide and mycobacterial products. J Immunol. 1997;159:1352-61.
28. Clem RJ, Fechheimer M, Miller LK. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science. 1991;254:1388-90.
29. Clouston WM, Kerr JF. Apoptosis, lymphocytotoxicity and the containment of viral infections. Med Hypotheses. 1985;18:399-404.
30. Wallace M, Malkovsky M, Carding SR. Gamma/delta T lymphocytes in viral infections. J Leukoc Biol. 1995;58:277-83.
31. Welsh RM, Lin MY, Lohman BL, Varga SM, Zarozinski CC, Selin LK. Alpha beta and gamma delta T-cell networks and their roles in natural resistance to viral infections. Immunol Rev. 1997;159:79-93.
32. Selin LK, Santolucito PA, Pinto AK, Szomolanyi-Tsuda E, Welsh RM. Innate immunity to viruses: Control of vaccinia virus infection by gamma delta T cells. J Immunol. 2001;166:6784-94.
33. DeVico AL, Gallo RC. Control of HIV-1 infection by soluble factors of the immune response. Nat Rev Microbiol. 2004;2:401-13.
34. Sierra S, Kupfer B, Kaiser R. Basics of the virology of HIV-1 and its replication. J Clin Virol. 2005;34:233-44.
35. Cheng-Mayer C, Liu R, Landau NR, Stamatatos L. Macrophage tropism of human immunodeficiency virus type 1 and utilization of the CC-CKR5 coreceptor. J Virol. 1997;71:1657-61.
36. Gonzalez E, Bamshad M, Sato N, Mummidi S, Dhanda R, Catano G, et al. Race-specific HIV-1 disease-modifying effects associated with CCR5 haplotypes. Proc Natl Acad Sci USA. 1999;96:12004-9.
37. Díaz FJ, Vega JA, Patino PJ, Bedoya G, Nagles J, Villegas C, et al. Frequency of CCR5 delta-32 mutation in human immunodeficiency virus (HIV)-seropositive and HIV-exposed seronegative individuals and in general population of Medellin, Colombia. Mem Inst Oswaldo Cruz. 2000;95:237-42.
38. O'Brien SJ, Gao X, Carrington M. HLA and AIDS: a cautionary tale. Trends Mol Med. 2001;7:379-81.
39. Hendel H, Caillat-Zucman S, Lebuanec H, Carrington M, O'Brien S, Andrieu JM, et al. New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. J Immunol. 1999;162:6942-6.
40. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med. 1996;2:405-11.
41. Gillespie GM, Kaul R, Dong T, Yang HB, Rostron T, Bwayo JJ, et al. Cross-reactive cytotoxic T lymphocytes against a HIV-1 p24 epitope in slow progressors with B*57. AIDS. 2002;16:961-72.
42. Migueles SA, Sabbaghian MS, Shupert WL, Bettinotti MP, Marincola FM, Martino L, et al. HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc Natl Acad Sci USA. 2000;97:2709-14.
43. MacDonald KS, Embree J, Njenga S, Nagelkerke NJ, Ngatia I, Mohammed Z, et al. Mother-child class I HLA concordance increases perinatal human immunodeficiency virus type 1 transmission. J Infect Dis. 1998;177:551-6.
44. Rugeles MT, Shearer GM. Alloantigen recognition in utero: Dual advantage for the fetus? Trends Immunol. 2004;25:348-52.
45. MacDonald KS, Embree JE, Nagelkerke NJ, Castillo J, Ramhadin S, Njenga S, et al. The HLA A2/6802 supertype is associated with reduced risk of perinatal human immunodeficiency virus type 1 transmission. J Infect Dis. 2001;183:503-6.
46. Bedoya VI, Jaimes FA, Delgado JC, Rugeles C, Usuga X, Zapata W, et al. Fetal-maternal HLA-A and -B discordance is associated with placental RNase expression and anti-HIV-1 activity. Curr HIV Res. 2008;6:380-7.
47. O'Brien V. Viruses and apoptosis. J Gen Virol. 1998;79:1833-45.
48. Benedict CA, Norris PS, Ware CF. To kill or be killed: Viral evasion of apoptosis. Nat Immunol. 2002;3:1013-8.
49. Fesq H, Bacher M, Nain M, Gemsa D. Programmed cell death (apoptosis) in human monocytes infected by influenza A virus. Immunobiology. 1994;190:175-82.
50. Jelachich ML, Lipton HL. Theiler's murine encephalomyelitis virus kills restrictive but not permissive cells by apoptosis. J Virol. 1996;70:6856-61.
51. Crowe SM, Sonza S. HIV-1 can be recovered from a variety of cells including peripheral blood monocytes of patients receiving highly active antiretroviral therapy: A further obstacle to eradication. J Leukoc Biol. 2000;68:345-50.
52. Lewin SR, Kirihara J, Sonza S, Irving L, Mills J, Crowe SM. HIV-1 DNA and mRNA concentrations are similar in peripheral blood monocytes and alveolar macrophages in HIV-1-infected individuals. AIDS.1998;12:719-27.
53. Cassol E, Alfano M, Biswas P, Poli G. Monocyte-derived macrophages and myeloid cell lines as targets of HIV-1 replication and persistence. J Leukoc Biol. 2006;80: 1018-30.
54. Rich EA, Chen IS, Zack JA, Leonard ML, O'Brien WA. Increased susceptibility of differentiated mononuclear phagocytes to productive infection with human immuno- deficiency virus-1 (HIV-1). J Clin Invest. 1992;89:176-83.
55. Sonza S, Maerz A, Uren S, Violo A, Hunter S, Boyle W, et al. Susceptibility of human monocytes to HIV type 1 infection in vitro is not dependent on their level of CD4 expression. AIDS Res Hum Retroviruses. 1995;11:769-76.
56. Lewin SR, Lambert P, Deacon NJ, Mills J, Crowe SM. Constitutive expression of p50 homodimer in freshly isolated human monocytes decreases with in vitro and in vivo differentiation: A possible mechanism influencing human immunodeficiency virus replication in monocytes and mature macrophages. J Virol. 1997;71:2114-9.
57. Naif HM, Li S, Alali M, Sloane A, Wu L, Kelly M, et al. CCR5 expression correlates with susceptibility of maturing monocytes to human immunodeficiency virus type 1 infection. J Virol. 1998;72:830-6.
58. Velilla PA, Hoyos A, Rojas M, Patino PJ, Vélez LA, Rugeles MT. Apoptosis as a mechanism of natural resistance to HIV-1 infection in an exposed but uninfected population. J Clin Virol. 2005;32:329-35.
59. Lehner T, Wang Y, Pido-López J, Whittall T, Bergmeier LA, Babaahmady K. The emerging role of innate immunity in protection against HIV-1 infection. Vaccine. 2008;26:2997-3001.
60. Medzhitov R, Janeway C Jr. Innate immunity. N Engl J Med. 2000;343:338-44.
61. Levy JA, Scott I, Mackewicz C. Protection from HIV/AIDS: The importance of innate immunity. Clin Immunol. 2003;108:167-74.
62. Donaghy H, Pozniak A, Gazzard B, Qazi N, Gilmour J, Gotch F, et al. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood. 2001;98:2574-6.
63. Motsinger A, Haas DW, Stanic AK, van Kaer L, Joyce S, Unutmaz D. CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J Exp Med. 2002;195:869-79.
64. Soumelis V, Scott I, Gheyas F, Bouhour D, Cozon G, Cotte L, et al. Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients. Blood. 2001;98:906-12.
65. Sandberg JK, Fast NM, Palacios EH, Fennelly G, Dobroszycki J, Palumbo P, et al. Selective loss of innate CD4(+) V alpha 24 natural killer T cells in human immunodeficiency virus infection. J Virol. 2002;76:7528-34.
66. Montoya CJ, Velilla PA, Chougnet C, Landay AL, Rugeles MT. Increased IFN-gamma production by NK and CD3+/CD56+ cells in sexually HIV-1-exposed but uninfected individuals. Clin Immunol. 2006;120:138-46.
67. Clerici M. Cell-mediated immunity in HIV infection. AIDS. 1993;7 (Suppl.1):S135-40.
68. Mazzoli S, Trabattoni D, Lo Caputo S, Piconi S, Ble C, Meacci F, et al. HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat Med. 1997;3:1250-7.
69. Rowland-Jones SL, Nixon DF, Aldhous MC, Gotch F, Ariyoshi K, Hallam N, et al. HIV-specific cytotoxic T-cell activity in an HIV-exposed but uninfected infant. Lancet. 1993;341:860-1.
70. Kuhn L, Meddows-Taylor S, Gray G, Tiemessen C. Human immunodeficiency virus (HIV)-specific cellular immune responses in newborns exposed to HIV in utero. Clin Infect Dis. 2002;34:267-76.
71. Rowland-Jones S, Sutton J, Ariyoshi K, Dong T, Gotch F, McAdam S, et al. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat Med. 1995;1:59-64.
72. Rowland-Jones SL, Dong T, Dorrell L, Ogg G, Hansasuta P, Krausa P, et al. Broadly cross-reactive HIV-specific cytotoxic T-lymphocytes in highly-exposed persistently seronegative donors. Immunol Lett. 1999;66:9-14.
73. Pinto LA, Sullivan J, Berzofsky JA, Clerici M, Kessler HA, Landay AL, et al. ENV-specific cytotoxic T lymphocyte responses in HIV seronegative health care workers occupationally exposed to HIV-contaminated body fluids. J Clin Invest. 1995;96:867-76.
74. Schenal M, Lo Caputo S, Fasano F, Vichi F, Saresella M, Pierotti P, et al. Distinct patterns of HIV-specific memory T lymphocytes in HIV-exposed uninfected individuals and in HIV-infected patients. AIDS. 2005;19:653-61.
75. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science. 1995;270:1811-5.
76. Walker CM, Moody DJ, Stites DP, Levy JA. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 1986;234:1563-6.
77. Alfano M, Poli G. Role of cytokines and chemokines in the regulation of innate immunity and HIV infection. Mol Immunol. 2005;42:161-82.
78. Patterson BK, Behbahani H, Kabat WJ, Sullivan Y, O'Gorman MR, Landay A, et al. Leukemia inhibitory factor inhibits HIV-1 replication and is upregulated in placentae from nontransmitting women. J Clin Invest. 2001;107:287-94.
79. Lee-Huang S, Huang PL, Sun Y, Kung HF, Blithe DL, Chen HC. Lysozyme and RNases as anti-HIV components in beta-core preparations of human chorionic gonadotropin. Proc Natl Acad Sci U S A. 1999;96:2678-81.
80. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, Rangel HR, et al. Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. AIDS. 2003;17:F39-48.
81. Chang TL, Vargas J Jr, Del Portillo A, Klotman ME. Dual role of alpha-defensin-1 in anti-HIV-1 innate immunity. J Clin Invest. 2005;115:765-73.
82. Garcia JR, Krause A, Schulz S, Rodríguez-Jiménez FJ, Kluver E, Adermann K, et al. Human beta-defensin 4: A novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J. 2001;15:1819-21.
83. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol. 2000;1:113-8.
84. Valore EV, Park CH, Quayle AJ, Wiles KR, McCray PB Jr., Ganz T. Human beta-defensin-1: an antimicrobial peptide of urogenital tissues. J Clin Invest. 1998;101:1633-42.
85. Trabattoni D, Caputo SL, Maffeis G, Vichi F, Biasin M, Pierotti P, et al. Human alpha defensin in HIV-exposed but uninfected individuals. J Acquir Immune Defic Syndr. 2004;35:455-63.
86. Ganz T. Defensins:A peptides of vertebrates. C R Biol. 2004;327:539-49.
87. Schutte BC, Mitros JP, Bartlett JA, Walters JD, Jia HP, Welsh MJ, et al. Discovery of five conserved beta -defensin gene clusters using a computational search strategy. Proc Natl Acad Sci USA. 2002;99:2129-33.
88. Jurevic RJ, Bai M, Chadwick RB, White TC, Dale BA. Single-nucleotide polymorphisms (SNPs) in human beta-defensin 1: High-throughput SNP assays and association with Candida carriage in type I diabetics and nondiabetic controls. J Clin Microbiol. 2003;41:90-6.
89. Jurevic RJ, Chrisman P, Mancl L, Livingston R, Dale BA. Single-nucleotide polymorphisms and haplotype analysis in beta-defensin genes in different ethnic populations. Genet Test. 2002;6:261-9.
90. Zapata W, Rodríguez B, Weber J, Estrada H, Quinones-Mateu ME, Zimermman PA, et al. Increased levels of human beta-defensins mRNA in sexually HIV-1 exposed but uninfected individuals. Curr HIV Res. 2008;6:531-8
How to Cite
1.
Rugeles MT, Velilla PA, Montoya CJ. Mechanisms of human natural resistance to HIV: A summary of ten years of research in the Colombian population. biomedica [Internet]. 2011 Mar. 7 [cited 2024 May 16];31(2):269-80. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/309
Some similar items:
- Iveth J. González, Metacaspases and their role in the life cycle of human protozoan parasites , Biomedica: Vol. 29 No. 3 (2009)
- María Elena Maldonado, Souad Bousserouel, Francine Gossé, Annelise Lobstein, Francis Raul, Implication of NF-κB and p53 in the expression of TRAIL-death receptors and apoptosis by apple procyanidins in human metastatic SW620 cells , Biomedica: Vol. 30 No. 4 (2010)
- Jaime E. Castellanos, José I. Neissa, Sigrid J. Camacho, Dengue virus induces apoptosis in SH-SY5Y human neuroblastoma cells , Biomedica: Vol. 36 (2016): Suplemento 2, Enfermedades virales
- Claudia Viviana Barbosa, Carlos Enrique Muskus, Luz Yaneth Orozco, Adriana Pabón, Mutagenicity, genotoxicity and gene expression of Rad51C, Xiap, P53 and Nrf2 induced by antimalarial extracts of plants collected from the middle Vaupés region, Colombia , Biomedica: Vol. 37 No. 3 (2017)
- Benny Weiss-Steider, Yolanda Córdova, Itzen Aguiñiga-Sánchez, Edgar Ledesma-Martínez, Vanihamin Domínguez-Meléndez, Edelmiro Santiago-Osorio, Sodium caseinate and alfa-casein inhibit proliferation of the mouse myeloid cell line 32D clone 3 (32Dcl3) via TNF-α , Biomedica: Vol. 39 No. 2 (2019)
- Iman Fathy Abou-El-Naga, Rasha Fadly Mady, Nermine Mogahed Fawzy Hussien Mogahed, In vitro effectivity of three approved drugs and their synergistic interaction against Leishmania infantum , Biomedica: Vol. 40 No. Supl. 1 (2020): Mayo, Infecciones en el trópico
Issue
Section
Topic review
| Article metrics | |
|---|---|
| Abstract views | |
| Galley vies | |
| PDF Views | |
| HTML views | |
| Other views | |
