Evidence for the innate immune response as a correlate of protection in human immunodeficiency virus (HIV)-1 highly exposed seronegative subjects (HESN)

Clinical and Experimental Immunology

Volumn 164, Issue 2, 2011, Pages 158-169

  Tomescu, C ^a   Abdulhaqq, S ^a   Montaner, L J ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

Dendritic cells; HIV 1 exposed seronegative; Intravenous drug user; Natural killer cells

Indexed keywords

ALPHA DEFENSIN; ALPHA INTERFERON; CD94 ANTIGEN; CHEMOKINE; DEFENSIN; ELAFIN; EOTAXIN; HLA ANTIGEN; HLA B ANTIGEN; HLA E ANTIGEN; HLA G ANTIGEN; HUMORAL ANTIBODY; IMMUNOGLOBULIN A; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 21; INTERLEUKIN 8; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DS1; LACTOFERRIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; NATURAL KILLER CELL RECEPTOR NKG2A; RANTES; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNINDEXED DRUG;

CELL ACTIVITY; CORRELATION ANALYSIS; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMORAL IMMUNITY; IMMUNE RESPONSE; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROENVIRONMENT; NATURAL KILLER CELL; PRIORITY JOURNAL; REVIEW; SEXUAL TRANSMISSION; TARGET CELL; VERTICAL TRANSMISSION; VIRUS ENTRY; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS TRANSMISSION;

ADULT; ANIMALS; CHEMOKINES; DEFENSINS; DENDRITIC CELLS; DISEASE SUSCEPTIBILITY; FEMALE; HIV ANTIBODIES; HIV INFECTIONS; HIV SERONEGATIVITY; HIV-1; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; INFANT, NEWBORN; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; KILLER CELLS, NATURAL; MACACA MULATTA; NEEDLE SHARING; OCCUPATIONAL EXPOSURE; PREGNANCY; RISK-TAKING; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIRUS REPLICATION;

EID: 79953804550     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2011.04379.x     Document Type: Review

References (139)

1. Fowke KR, Nagelkerke NJ, Kimani J etal. Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 1996; 348:1347-51.
2. Jennes W, Verheyden S, Demanet C etal. 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 2006; 177:6588-92.
3. Beretta A, Furci L, Burastero S etal. HIV-1-specific immunity in persistently seronegative individuals at high risk for HIV infection. Immunol Lett 1996; 51:39-43.
4. Clerici M, Giorgi JV, Chou CC etal. Cell-mediated immune response to human immunodeficiency virus (HIV) type 1 in seronegative homosexual men with recent sexual exposure to HIV-1. J Infect Dis 1992; 165:1012-9.
5. Mazzoli S, Trabattoni D, Lo Caputo S etal. HIV-specific mucosal and cellular immunity in HIV-seronegative partners of HIV-seropositive individuals. Nat Med 1997; 3:1250-7.
6. 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.
7. Pallikkuth S, Wanchu A, Bhatnagar A, Sachdeva RK, Sharma M. Human immunodeficiency virus (HIV) gag antigen-specific T-helper and granule-dependent CD8 T-cell activities in exposed but uninfected heterosexual partners of HIV type 1-infected individuals in North India. Clin Vaccine Immunol 2007; 14:1196-202.
8. Promadej-Lanier N, Hanson DL, Srinivasan P etal. Resistance to simian HIV infection is associated with high plasma interleukin-8, RANTES and eotaxin in a macaque model of repeated virus challenges. J Acquir Immune Defic Syndr 2010; 53:574-81.
9. Letvin NL, Rao SS, Dang V etal. No evidence for consistent virus-specific immunity in simian immunodeficiency virus-exposed, uninfected rhesus monkeys. J Virol 2007; 81:12368-74.
10. Ballan WM, Vu BA, Long BR etal. Natural killer cells in perinatally HIV-1-infected children exhibit less degranulation compared to HIV-1-exposed uninfected children and their expression of KIR2DL3, NKG2C, and NKp46 correlates with disease severity. J Immunol 2007; 179:3362-70.
11. Clerici M, Sison AV, Berzofsky JA etal. Cellular immune factors associated with mother-to-infant transmission of HIV. AIDS 1993; 7:1427-33.
12. Tiemessen CT, Shalekoff S, Meddows-Taylor S etal. Cutting edge: unusual NK cell responses to HIV-1 peptides are associated with protection against maternal-infant transmission of HIV-1. J Immunol 2009; 182:5914-8.
13. Winchester R, Pitt J, Charurat M etal. Mother-to-child transmission of HIV-1: strong association with certain maternal HLA-B alleles independent of viral load implicates innate immune mechanisms. J Acquir Immune Defic Syndr 2004; 36:659-70.
14. Pinto LA, Sullivan J, Berzofsky JA etal. 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.
15. Kroner BL, Rosenberg PS, Aledort LM, Alvord WG, Goedert JJ. HIV-1 infection incidence among persons with hemophilia in the United States and Western Europe, 1978-1990. Multicenter Hemophilia Cohort Study. J Acquir Immune Defic Syndr 1994; 7:279-86.
16. Salkowitz JR, Purvis SF, Meyerson H etal. Characterization of high-risk HIV-1 seronegative hemophiliacs. Clin Immunol 2001; 98:200-11.
17. Boulet S, Sharafi S, Simic N etal. Increased proportion of KIR3DS1 homozygotes in HIV-exposed uninfected individuals. AIDS 2008; 22:595-9.
18. Follezou JY, Lan NY, Lien TX etal. Clinical and biological characteristics of human immunodeficiency virus-infected and uninfected intravascular drug users in Ho Chi Minh City, Vietnam. Am J Trop Med Hyg 1999; 61:420-4.
19. Scott-Algara D, Truong LX, Versmisse P etal. Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users. J Immunol 2003; 171:5663-7.
20. Tomescu C, Duh FM, Lanier MA etal. Increased plasmacytoid dendritic cell maturation and natural killer cell activation in HIV-1 exposed, uninfected intravenous drug users. AIDS 2010; 24:2151-60.
21. Horton RE, McLaren PJ, Fowke K, Kimani J, Ball TB. Cohorts for the study of HIV-1-exposed but uninfected individuals: benefits and limitations. J Infect Dis 2010; 202 (Suppl. 3):S377-81.
22. Boileau C, Bruneau J, Al-Nachawati H, Lamothe F, Vincelette J. A prognostic model for HIV seroconversion among injection drug users as a tool for stratification in clinical trials. J Acquir Immune Defic Syndr 2005; 39:489-95.
23. Ranki A, Mattinen S, Yarchoan R etal. T-cell response towards HIV in infected individuals with and without zidovudine therapy, and in HIV-exposed sexual partners. AIDS 1989; 3:63-9.
24. Clerici M, Levin JM, Kessler HA etal. HIV-specific T-helper activity in seronegative health care workers exposed to contaminated blood. JAMA 1994; 271:42-6.
25. Alimonti JB, Kimani J, Matu L etal. Characterization of CD8 T-cell responses in HIV-1-exposed seronegative commercial sex workers from Nairobi, Kenya. Immunol Cell Biol 2006; 84:482-5.
26. Erickson AL, Willberg CB, McMahan V etal. Potentially exposed but uninfected individuals produce cytotoxic and polyfunctional human immunodeficiency virus type 1-specific CD8(+) T-cell responses which can be defined to the epitope level. Clin Vaccine Immunol 2008; 15:1745-8.
27. Restrepo C, Rallon NI, del Romero J etal. Low-level exposure to HIV induces virus-specific T cell responses and immune activation in exposed HIV-seronegative individuals. J Immunol 2010; 185:982-9.
28. Boulet S, Kleyman M, Kim JY etal. A combined genotype of KIR3DL1 high expressing alleles and HLA-B*57 is associated with a reduced risk of HIV infection. AIDS 2008; 22:1487-91.
29. Lacap PA, Huntington JD, Luo M etal. Associations of human leukocyte antigen DRB with resistance or susceptibility to HIV-1 infection in the Pumwani Sex Worker Cohort. AIDS 2008; 22:1029-38.
30. Killian MS, Johnson C, Teque F, Fujimura S, Levy JA. Natural suppression of human immunodeficiency virus type 1 replication is mediated by transitional memory CD8+ T cells. J Virol 2011; 85:1696-705.
31. Betts MR, Nason MC, West SM etal. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006; 107:4781-9.
32. Boaz MJ, Waters A, Murad S, Easterbrook PJ, Vyakarnam A. Presence of HIV-1 Gag-specific IFN-gamma+IL-2+ and CD28+IL-2+ CD4 T cell responses is associated with nonprogression in HIV-1 infection. J Immunol 2002; 169:6376-85.
33. McElrath MJ, De Rosa SC, Moodie Z etal. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 2008; 372:1894-905.
34. Sekaly RP. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J Exp Med 2008; 205:7-12.
35. Buchbinder SP, Mehrotra DV, Duerr A etal. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008; 372:1881-93.
36. Addo MM, Altfeld M, Brainard DM etal. Lack of detectable HIV-1-specific CD8+ T cell responses in Zambian HIV-1-exposed seronegative partners of HIV-1-positive individuals. J Infect Dis 2011; 203:258-62.
37. Kaul R, Rowland-Jones SL, Kimani J etal. New insights into HIV-1 specific cytotoxic T-lymphocyte responses in exposed, persistently seronegative Kenyan sex workers. Immunol Lett 2001; 79:3-13.
38. Kaul R, MacDonald KS, Nagelkerke NJ etal. HIV viral set point and host immune control in individuals with HIV-specific CD8+ T-cell responses prior to HIV acquisition. AIDS 2010; 24:1449-54.
39. Kaul R, Rowland-Jones SL, Kimani J etal. Late seroconversion in HIV-resistant Nairobi prostitutes despite pre-existing HIV-specific CD8+ responses. J Clin Invest 2001; 107:341-9.
40. Liu Y, Woodward A, Zhu H etal. 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. J Virol 2009; 83:10821-9.
41. Lederman MM, Alter G, Daskalakis DC etal. Determinants of protection among HIV-exposed seronegative persons: an overview. J Infect Dis 2011; 202 (Suppl. 3):S333-8.
42. Miyazawa M, Lopalco L, Mazzotta F, Lo Caputo S, Veas F, Clerici M. The 'immunologic advantage' of HIV-exposed seronegative individuals. AIDS 2009; 23:161-75.
43. Piacentini L, Fenizia C, Naddeo V, Clerici M. Not just sheer luck! Immune correlates of protection against HIV-1 infection. Vaccine 2008; 26:3002-7.
44. Broliden K, Hinkula J, Devito C etal. Functional HIV-1 specific IgA antibodies in HIV-1 exposed, persistently IgG seronegative female sex workers. Immunol Lett 2001; 79:29-36.
45. Kaul R, Plummer F, Clerici M, Bomsel M, Lopalco L, Broliden K. Mucosal IgA in exposed, uninfected subjects: evidence for a role in protection against HIV infection. AIDS 2001; 15:431-2.
46. Kaul R, Trabattoni D, Bwayo JJ etal. HIV-1-specific mucosal IgA in a cohort of HIV-1-resistant Kenyan sex workers. AIDS 1999; 13:23-9.
47. Mazzoli S, Lopalco L, Salvi A etal. Human immunodeficiency virus (HIV)-specific IgA and HIV neutralizing activity in the serum of exposed seronegative partners of HIV-seropositive persons. J Infect Dis 1999; 180:871-5.
48. Hirbod T, Kaul R, Reichard C etal. HIV-neutralizing immunoglobulin A and HIV-specific proliferation are independently associated with reduced HIV acquisition in Kenyan sex workers. AIDS 2008; 22:727-35.
49. Hasselrot K, Saberg P, Hirbod T etal. Oral HIV-exposure elicits mucosal HIV-neutralizing antibodies in uninfected men who have sex with men. AIDS 2009; 23:329-33.
50. Perez CL, Hasselrot K, Bratt G, Broliden K, Karlsson AC. Induction of systemic HIV-1-specific cellular immune responses by oral exposure in the uninfected partner of discordant couples. AIDS 2010; 24:969-74.
51. Farquhar C, VanCott T, Bosire R etal. Salivary human immunodeficiency virus (HIV)-1-specific immunoglobulin A in HIV-1-exposed infants in Kenya. Clin Exp Immunol 2008; 153:37-43.
52. Dorrell L, Hessell AJ, Wang M etal. Absence of specific mucosal antibody responses in HIV-exposed uninfected sex workers from The Gambia. AIDS 2000; 14:1117-22.
53. Clerici M, Barassi C, Devito C etal. Serum IgA of HIV-exposed uninfected individuals inhibit HIV through recognition of a region within the alpha-helix of gp41. AIDS 2002; 16:1731-41.
54. Devito C, Broliden K, Kaul R etal. Mucosal and plasma IgA from HIV-1-exposed uninfected individuals inhibit HIV-1 transcytosis across human epithelial cells. J Immunol 2000; 165:5170-6.
55. Tudor D, Derrien M, Diomede L etal. HIV-1 gp41-specific monoclonal mucosal IgAs derived from highly exposed but IgG-seronegative individuals block HIV-1 epithelial transcytosis and neutralize CD4(+) cell infection: an IgA gene and functional analysis. Mucosal Immunol 2009; 2:412-26.
56. Herr AB, White CL, Milburn C, Wu C, Bjorkman PJ. Bivalent binding of IgA1 to FcalphaRI suggests a mechanism for cytokine activation of IgA phagocytosis. J Mol Biol 2003; 327:645-57.
57. Raghavan M, Bjorkman PJ. Fc receptors and their interactions with immunoglobulins. Annu Rev Cell Dev Biol 1996; 12:181-220.
58. Nguyen M, Pean P, Lopalco L etal. HIV-specific antibodies but not T-cell responses are associated with protection in seronegative partners of HIV-1-infected individuals in Cambodia. J Acquir Immune Defic Syndr 2006; 42:412-9.
59. Mestecky J, Wright PF, Lopalco L etal. Scarcity or absence of humoral immune responses in the plasma and cervicovaginal lavage fluids of heavily HIV-1-exposed but persistently seronegative women. AIDS Res Hum Retroviruses 2010; Epub ahead of print.
60. Horton RE, Ball TB, Wachichi C etal. Cervical HIV-specific IgA in a population of commercial sex workers correlates with repeated exposure but not resistance to HIV. AIDS Res Hum Retroviruses 2009; 25:83-92.
61. Fonck K, Kaul R, Keli F etal. Sexually transmitted infections and vaginal douching in a population of female sex workers in Nairobi, Kenya. Sex Transm Infect 2001; 77:271-5.
62. Hirbod T, Broliden K. Mucosal immune responses in the genital tract of HIV-1-exposed uninfected women. J Intern Med 2007; 262:44-58.
63. Iqbal SM, Kaul R. Mucosal innate immunity as a determinant of HIV susceptibility. Am J Reprod Immunol 2008; 59:44-54.
64. Suresh P, Wanchu A, Bhatnagar A, Sachdeva RK, Sharma M. Spontaneous and antigen-induced chemokine production in exposed but uninfected partners of HIV type 1-infected individuals in North India. AIDS Res Hum Retroviruses 2007; 23:261-8.
65. Furci L, Scarlatti G, Burastero S etal. Antigen-driven C-C chemokine-mediated HIV-1 suppression by CD4(+) T cells from exposed uninfected individuals expressing the wild-type CCR-5 allele. J Exp Med 1997; 186:455-60.
66. Hasselrot K, Bratt G, Duvefelt K, Hirbod T, Sandstrom E, Broliden K. HIV-1 exposed uninfected men who have sex with men have increased levels of salivary CC-chemokines associated with sexual behavior. AIDS 2010; 24:1569-75.
67. Iqbal SM, Ball TB, Kimani J etal. Elevated T cell counts and RANTES expression in the genital mucosa of HIV-1-resistant Kenyan commercial sex workers. J Infect Dis 2005; 192:728-38.
68. Malnati MS, Tambussi G, Clerici E etal. Increased plasma levels of the C-C chemokine RANTES in patients with primary HIV-1 infection. J Biol Regul Homeost Agents 1997; 11:40-2.
69. McNeely TB, Dealy M, Dripps DJ, Orenstein JM, Eisenberg SP, Wahl SM. Secretory leukocyte protease inhibitor: a human saliva protein exhibiting anti-human immunodeficiency virus 1 activity in vitro. J Clin Invest 1995; 96:456-64.
70. Groot F, Geijtenbeek TB, Sanders RW etal. Lactoferrin prevents dendritic cell-mediated human immunodeficiency virus type 1 transmission by blocking the DC-SIGN-gp120 interaction. J Virol 2005; 79:3009-15.
71. Harmsen MC, Swart PJ, de Bethune MP, Pauwels R, De Clercq E. The TH, Meijer DK. Antiviral effects of plasma and milk proteins: lactoferrin shows potent activity against both human immunodeficiency virus and human cytomegalovirus replication in vitro. J Infect Dis 1995; 172:380-8.
72. Viani RM, Gutteberg TJ, Lathey JL, Spector SA. Lactoferrin inhibits HIV-1 replication in vitro and exhibits synergy when combined with zidovudine. AIDS 1999; 13:1273-4.
73. Novak RM, Donoval BA, Graham PJ etal. Cervicovaginal levels of lactoferrin, secretory leukocyte protease inhibitor, and RANTES and the effects of coexisting vaginoses in human immunodeficiency virus (HIV)-seronegative women with a high risk of heterosexual acquisition of HIV infection. Clin Vaccine Immunol 2007; 14:1102-7.
74. Iqbal SM, Ball TB, Levinson P etal. Elevated elafin/trappin-2 in the female genital tract is associated with protection against HIV acquisition. AIDS 2009; 23:1669-77.
75. Weinberg A, Quinones-Mateu ME, Lederman MM. Role of human beta-defensins in HIV infection. Adv Dent Res 2006; 19:42-8.
76. Kuhn L, Trabattoni D, Kankasa C etal. Alpha-defensins in the prevention of HIV transmission among breastfed infants. J Acquir Immune Defic Syndr 2005; 39:138-42.
77. Quinones-Mateu ME, Lederman MM, Feng Z etal. Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. AIDS 2003; 17:F39-48.
78. Rodriguez-Garcia M, Climent N, Oliva H etal. Increased alpha-defensins 1-3 production by dendritic cells in HIV-infected individuals is associated with slower disease progression. PLoS ONE 2010; 5:e9436.
79. Trabattoni D, Caputo SL, Maffeis G etal. Human alpha defensin in HIV-exposed but uninfected individuals. J Acquir Immune Defic Syndr 2004; 35:455-63.
80. Zapata W, Rodriguez B, Weber J etal. Increased levels of human beta-defensins mRNA in sexually HIV-1 exposed but uninfected individuals. Curr HIV Res 2008; 6:531-8.
81. Levinson P, Kaul R, Kimani J etal. Levels of innate immune factors in genital fluids: association of alpha defensins and LL-37 with genital infections and increased HIV acquisition. AIDS 2009; 23:309-17.
82. Bosire R, John-Stewart GC, Mabuka JM etal. Breast milk alpha-defensins are associated with HIV type 1 RNA and CC chemokines in breast milk but not vertical HIV type 1 transmission. AIDS Res Hum Retroviruses 2007; 23:198-203.
83. Biassoni R, Cantoni C, Pende D etal. Human natural killer cell receptors and co-receptors. Immunol Rev 2001; 181:203-14.
84. Long EO, Burshtyn DN, Clark WP etal. Killer cell inhibitory receptors: diversity, specificity, and function. Immunol Rev 1997; 155:135-44.
85. Boyton RJ, Altmann DM. Natural killer cells, killer immunoglobulin-like receptors and human leucocyte antigen class I in disease. Clin Exp Immunol 2007; 149:1-8.
86. Altfeld M, Kalife ET, Qi Y etal. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med 2006; 3:e403.
87. Martin MP, Qi Y, Gao X etal. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007; 39:733-40.
88. Long BR, Ndhlovu LC, Oksenberg JR etal. KIR3DS1 conferral of enhanced natural killer cell function in early HIV-1 infection. J Virol 2008; 82:4785-92.
89. Alter G, Martin MP, Teigen N etal. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 2007; 204:3027-36.
90. Lajoie J, Hargrove J, Zijenah LS, Humphrey JH, Ward BJ, Roger M. Genetic variants in nonclassical major histocompatibility complex class I human leukocyte antigen (HLA)-E and HLA-G molecules are associated with susceptibility to heterosexual acquisition of HIV-1. J Infect Dis 2006; 193:298-301.
91. Ravet S, Scott-Algara D, Bonnet E etal. Distinctive NK-cell receptor repertoires sustain high-level constitutive NK-cell activation in HIV-exposed uninfected individuals. Blood 2007; 109:4296-305.
92. Tomescu C, Chehimi J, Maino VC, Montaner LJ. Retention of viability, cytotoxicity, and response to IL-2, IL-15, or IFN-{alpha} by human NK cells after CD107a degranulation. J Leukoc Biol 2009; 85:871-6.
93. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 1999; 17:189-220.
94. Waldmann T. The contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for the immunotherapy of rheumatological diseases. Arthritis Res 2002; 4 (Suppl. 3):S161-7.
95. Trinchieri G, Wysocka M, D'Andrea A etal. Natural killer cell stimulatory factor (NKSF) or interleukin-12 is a key regulator of immune response and inflammation. Prog Growth Factor Res 1992; 4:355-68.
96. Muller-Trutwin M, Hosmalin A. Role for plasmacytoid dendritic cells in anti-HIV innate immunity. Immunol Cell Biol 2005; 83:578-83.
97. Smit JJ, Rudd BD, Lukacs NW. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J Exp Med 2006; 203:1153-9.
98. Yoneyama H, Matsuno K, Toda E etal. Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J Exp Med 2005; 202:425-35.
99. Bandyopadhyay S, Perussia B, Trinchieri G, Miller DS, Starr SE. Requirement for HLA-DR+ accessory cells in natural killing of cytomegalovirus-infected fibroblasts. J Exp Med 1986; 164:180-95.
100. Feldman M, Howell D, Fitzgerald-Bocarsly P. Interferon-alpha-dependent and -independent participation of accessory cells in natural killer cell-mediated lysis of HSV-1-infected fibroblasts. J Leukoc Biol 1992; 52:473-82.
101. Fitzgerald-Bocarsly P, Feldman M, Curl S, Schnell J, Denny T. Positively selected Leu-11a (CD16+) cells require the presence of accessory cells or factors for the lysis of herpes simplex virus-infected fibroblasts but not herpes simplex virus-infected Raji. J Immunol 1989; 143:1318-26.
102. Oh SH, Bandyopadhyay S, Miller DS, Starr SE. Cooperation between CD16(Leu-11b)+ NK cells and HLA-DR+ cells in natural killing of herpesvirus-infected fibroblasts. J Immunol 1987; 139:2799-802.
103. Perussia B, Fanning V, Trinchieri G. A leukocyte subset bearing HLA-DR antigens is responsible for in vitro alpha interferon production in response to viruses. Nat Immun Cell Growth Regul 1985; 4:120-37.
104. Tomescu C, Chehimi J, Maino VC, Montaner LJ. NK Cell lysis of HIV-1-infected autologous CD4 primary T cells: requirement for IFN-mediated NK activation by plasmacytoid dendritic cells. J Immunol 2007; 179:2097-104.
105. Evans DT, Serra-Moreno R, Singh RK, Guatelli JC. BST-2/tetherin: a new component of the innate immune response to enveloped viruses. Trends Microbiol 2010; 18:388-96.
106. Tokarev A, Skasko M, Fitzpatrick K, Guatelli J. Antiviral activity of the interferon-induced cellular protein BST-2/tetherin. AIDS Res Hum Retroviruses 2009; 25:1197-210.
107. Argyris EG, Acheampong E, Wang F etal. The interferon-induced expression of APOBEC3G in human blood-brain barrier exerts a potent intrinsic immunity to block HIV-1 entry to central nervous system. Virology 2007; 367:440-51.
108. Tanaka Y, Marusawa H, Seno H etal. Anti-viral protein APOBEC3G is induced by interferon-alpha stimulation in human hepatocytes. Biochem Biophys Res Commun 2006; 341:314-9.
109. Li Q, Estes JD, Schlievert PM etal. Glycerol monolaurate prevents mucosal SIV transmission. Nature 2009; 458:1034-8.
110. Biasin M, Piacentini L, Lo Caputo S etal. TLR activation pathways in HIV-1-exposed seronegative individuals. J Immunol 2010; 184:2710-7.
111. Herbeuval JP, Shearer GM. HIV-1 immunopathogenesis: how good interferon turns bad. Clin Immunol 2007; 123:121-8.
112. Sirianni MC, Mezzaroma I, Aiuti F, Moretta A. Analysis of the cytolytic activity mediated by natural killer cells from acquired immunodeficiency syndrome patients in response to phytohemagglutinin or anti-CD16 monoclonal antibody. Eur J Immunol 1994; 24:1874-8.
113. Hu PF, Hultin LE, Hultin P etal. Natural killer cell immunodeficiency in HIV disease is manifest by profoundly decreased numbers of CD16+CD56+ cells and expansion of a population of CD16dimCD56- cells with low lytic activity. J Acquir Immune Defic Syndr Hum Retrovirol 1995; 10:331-40.
114. Lucia B, Jennings C, Cauda R, Ortona L, Landay AL. Evidence of a selective depletion of a CD16+ CD56+ CD8+ natural killer cell subset during HIV infection. Cytometry 1995; 22:10-5.
115. Ullum H, Gotzsche PC, Victor J, Dickmeiss E, Skinhoj P, Pedersen BK. Defective natural immunity: an early manifestation of human immunodeficiency virus infection. J Exp Med 1995; 182:789-99.
116. Brunetta E, Fogli M, Varchetta S etal. The decreased expression of Siglec-7 represents an early marker of dysfunctional natural killer-cell subsets associated with high levels of HIV-1 viremia. Blood 2009; 114:3822-30.
117. Brunetta E, Hudspeth KL, Mavilio D. Pathologic natural killer cell subset redistribution in HIV-1 infection: new insights in pathophysiology and clinical outcomes. J Leukoc Biol 2010; 88:1119-30.
118. Hong HS, Eberhard JM, Keudel P etal. Phenotypically and functionally distinct subsets contribute to the expansion of CD56-/CD16+ natural killer cells in HIV infection. AIDS 2010; 24:1823-34.
119. De Maria A, Fogli M, Costa P etal. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 2003; 33:2410-8.
120. Mavilio D, Benjamin J, Daucher M etal. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci USA 2003; 100:15011-6.
121. Fogli M, Costa P, Murdaca G etal. Significant NK cell activation associated with decreased cytolytic function in peripheral blood of HIV-1-infected patients. Eur J Immunol 2004; 34:2313-21.
122. Alter G, Altfeld M. NK cell function in HIV-1 infection. Curr Mol Med 2006; 6:621-9.
123. Vieillard V, Fausther-Bovendo H, Samri A, Debre P. Specific phenotypic and functional features of natural killer cells from HIV-infected long-term nonprogressors and HIV controllers. J Acquir Immune Defic Syndr 2010; 53:564-73.
124. O'Connell KA, Han Y, Williams TM, Siliciano RF, Blankson JN. Role of natural killer cells in a cohort of elite suppressors: low frequency of the protective KIR3DS1 allele and limited inhibition of human immunodeficiency virus type 1 replication in vitro. J Virol 2009; 83:5028-34.
125. Martin MP, Gao X, Lee JH etal. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 2002; 31:429-34.
126. Liu J, Keele BF, Li H etal. Low-dose mucosal simian immunodeficiency virus infection restricts early replication kinetics and transmitted virus variants in rhesus monkeys. J Virol 2010; 84:10406-12.
127. Kramer HB, Lavender KJ, Qin L etal. Elevation of intact and proteolytic fragments of acute phase proteins constitutes the earliest systemic antiviral response in HIV-1 infection. PLoS Pathog 2010; 6:e1000893.
128. Stacey AR, Norris PJ, Qin L etal. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 2009; 83:3719-33.
129. Nelson PW, Mittler JE, Perelson AS. Effect of drug efficacy and the eclipse phase of the viral life cycle on estimates of HIV viral dynamic parameters. J Acquir Immune Defic Syndr 2001; 26:405-12.
130. Biasin M, Clerici M, Piacentini L. Innate immunity in resistance to HIV infection. J Infect Dis 2010; 202 (Suppl. 3):S361-5.
131. Ganusov VV, De Boer RJ. Estimating costs and benefits of CTL escape mutations in SIV/HIV infection. PLoS Comput Biol 2006; 2:e24.
132. Lopez M, Soriano V, Benito JM. Escape mutations in HIV infection and its impact on CD8+ T cell responses. Curr Mol Med 2007; 7:446-58.
133. McNeil AC, Shupert WL, Iyasere CA etal. High-level HIV-1 viremia suppresses viral antigen-specific CD4(+) T cell proliferation. Proc Natl Acad Sci USA 2001; 98:13878-83.
134. Selliah N, Shackelford J, Wang JF, Traynor F, Yin J, Finkel TH. T cell signaling and apoptosis in HIV disease. Immunol Res 2003; 27:247-60.
135. Finkel TH, Banda NK. Indirect mechanisms of HIV pathogenesis: how does HIV kill T cells? Curr Opin Immunol 1994; 6:605-15.
136. Finkel TH, Tudor-Williams G, Banda NK etal. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1995; 1:129-34.
137. Giri MS, Nebozyhn M, Raymond A etal. Circulating monocytes in HIV-1-infected viremic subjects exhibit an antiapoptosis gene signature and virus- and host-mediated apoptosis resistance. J Immunol 2009; 182:4459-70.
138. Muthumani K, Choo AY, Premkumar A etal. Human immunodeficiency virus type 1 (HIV-1) Vpr-regulated cell death: insights into mechanism. Cell Death Differ 2005; 12 (Suppl. 1):962-70.
139. Reynolds MR, Rakasz E, Skinner PJ etal. CD8+ T-lymphocyte response to major immunodominant epitopes after vaginal exposure to simian immunodeficiency virus: too late and too little. J Virol 2005; 79:9228-35.