Comprehensive analysis of unique cases with extraordinary control over HIV replication

Blood

Volumn 119, Issue 20, 2012, Pages 4645-4655

  Mendoza, Daniel ^a   Johnson, Sarah A ^a   Peterson, Bennett A ^a   Natarajan, Ven ^b   Salgado, Maria ^c,d   Dewar, Robin L ^b   Burbelo, Peter D ^e   Doria Rose, Nicole A ^a   Graf, Erin H ^f   Greenwald, Jamieson H ^a   Hodge, Jessica N ^a   Thompson, William L ^a   Cogliano, Nancy A ^a   Chairez, Cheryl L ^a   Rehm, Catherine A ^a   Jones, Sara ^b   Hallahan, Claire W ^a   Kovacs, Joseph A ^g   Sereti, Irini ^a   Sued, Omar ^h   Peel, Sheila A ⁱ   O'Connell, Robert J ⁱ   O'Doherty, Una ^f   Chun, Tae Wook ^a   Connors, Mark ^a   Migueles, Stephen A ^a   more..

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b SAIC FREDERICK INC   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^e NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g NATIONAL INSTITUTES OF HEALTH   (United States)

^h FUNDACIÓN HUÉSPED   (Argentina)

ⁱ WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EFAVIRENZ; EMTRICITABINE; GAMMA INTERFERON; HLA ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 2; TENOFOVIR; VIRUS DNA; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ADULT; ALLELE; ANTIBODY RESPONSE; ARTICLE; CASE REPORT; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; COLONOSCOPY; CYTOKINE PRODUCTION; CYTOTOXICITY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IMMUNE RESPONSE; IMMUNOTHERAPY; LONG TERMINAL REPEAT; LYMPHOCYTE PROLIFERATION; MALE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESERVOIR; RISK FACTOR; VIREMIA; VIRUS LOAD; VIRUS REPLICATION; WESTERN BLOTTING;

EID: 84861203962     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-10-381996     Document Type: Article

References (53)

1. Migueles SA, Connors M. Long-term nonprogressive disease among untreated HIV-infected individuals: clinical implications of understanding immune control of HIV. JAMA. 2010;304(2):194-201.
2. Dinoso JB, Kim SY, Siliciano RF, Blankson JN. A comparison of viral loads between HIV-1-infected elite suppressors and individuals who receive suppressive highly active antiretroviral therapy. Clin Infect Dis. 2008;47(1):102-104. (Pubitemid 351920594)
3. Migueles SA, Osborne CM, Royce C, et al. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity. 2008;29(6):1009-1021.
4. Pereyra F, Palmer S, Miura T, et al. Persistent low-level viremia in HIV-1 elite controllers and relationship to immunologic parameters. J Infect Dis. 2009;200(6):984-990.
5. Hatano H, Delwart EL, Norris PJ, et al. Evidence for persistent low-level viremia in individuals who control human immunodeficiency virus in the absence of antiretroviral therapy. J Virol. 2009; 83(1):329-335.
6. Lambotte O, Boufassa F, Madec Y, et al. HIV controllers: a homogeneous group of HIV-1-infected patients with spontaneous control of viral replication. Clin Infect Dis. 2005;41(7):1053-1056. (Pubitemid 41368233)
7. Sajadi MM, Heredia A, Le N, Constantine NT, Redfield RR. HIV-1 natural viral suppressors: control of viral replication in the absence of therapy. AIDS. 2007;21(4):517-519.
8. Saez-Cirion A, Sinet M, Shin SY, et al. Heterogeneity in HIV suppression by CD8 T cells from HIV controllers: association with Gag-specific CD8 T cell responses. J Immunol. 2009;182(12):7828-7837.
9. Julg B, Pereyra F, Buzon MJ, et al. Infrequent recovery of HIV from but robust exogenous infection of activated CD4(+) T cells in HIV elite controllers. Clin Infect Dis. 2010;51(2):233-238.
10. Graf EH, Mexas AM, Yu JJ, et al. Elite suppressors harbor low levels of integrated HIV DNA and high levels of 2-LTR circular HIV DNA compared to HIV+ patients on and off HAART. PLoS Pathog. 2011;7(2):e1001300.
11. Saez-Cirion A, Hamimi C, Bergamaschi A, et al. Restriction of HIV-1 replication in macrophages and CD4+ T cells from HIV controllers. Blood. 2011;118(4):955-964.
12. Hersperger AR, Migueles SA, Betts MR, Connors M. Qualitative features of the HIV-specific CD8+ T-cell response associated with immunologic control. Curr Opin HIV AIDS. 2011;6(3):169-173.
13. Betts MR, Nason MC, West SM, et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood. 2006; 107(12):4781-4789. (Pubitemid 43882629)
14. Zimmerli SC, Harari A, Cellerai C, Vallelian F, Bart PA, Pantaleo G. HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc Natl Acad Sci U S A. 2005;102(20):7239-7244. (Pubitemid 40696363)
15. Saez-Cirion A, Lacabaratz C, Lambotte O, et al. HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype. Proc Natl Acad Sci U S A. 2007;104(16):6776-6781. (Pubitemid 47175577)
16. Ferre AL, Hunt PW, Critchfield JW, et al. Mucosal immune responses to HIV-1 in elite controllers: a potential correlate of immune control. Blood. 2009;113(17):3978-3989.
17. Migueles SA, Weeks KA, Nou E, et al. Defective human immunodeficiency virus-specific CD8+T-cell polyfunctionality, proliferation, and cytotoxicity are not restored by antiretroviral therapy. J Virol. 2009;83(22):11876-11889.
18. Migueles SA, Laborico AC, Shupert WL, et al. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat Immunol. 2002;3(11):1061-1068. (Pubitemid 35363659)
19. Deacon NJ, Tsykin A, Solomon A, et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science. 1995;270(5238):988-991.
20. Brockman MA, Schneidewind A, Lahaie M, et al. Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J Virol. 2007;81(22):12608-12618. (Pubitemid 350085874)
21. Navis M, Schellens I, van Baarle D, et al. Viral replication capacity as a correlate of HLA B57/B5801-associated nonprogressive HIV-1 infection. J Immunol. 2007;179(5):3133-3143.
22. Rhodes D, Solomon A, Bolton W, et al. Identification of a new recipient in the Sydney Blood Bank Cohort: a long-term HIV type 1-infected seroindeterminate individual. AIDS Res Hum Retroviruses. 1999;15(16):1433-1439. (Pubitemid 29523123)
23. Zaunders JJ, Geczy AF, Dyer WB, et al. Effect of long-term infection with nef-defective attenuated HIV type 1 on CD4+ and CD8+ T lymphocytes: increased CD45RO+CD4+ T lymphocytes and limited activation of CD8+ T lymphocytes. AIDS Res Hum Retroviruses. 1999;15(17):1519-1527.
24. Wang B, Dyer WB, Zaunders JJ, et al. Comprehensive analyses of a unique HIV-1-infected nonprogressor reveal a complex association of immunobiological mechanisms in the context of replication-incompetent infection. Virology. 2002; 304(2):246-264. (Pubitemid 36069167)
25. Ciccone EJ, Read SW, Mannon PJ, et al. Cycling of gut mucosal CD4+ T cells decreases after prolonged anti-retroviral therapy and is associated with plasma LPS levels. Mucosal Immunol. 2010; 3(2):172-181.
26. Ciccone EJ, Greenwald JH, Lee PI, et al. CD4+ T cells, including Th17 and cycling subsets, are intact in the gut mucosa of HIV-1-infected long-term nonprogressors. J Virol. 2011;85(12):5880-5888.
27. Migueles SA, Sabbaghian MS, Shupert WL, 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 U S A. 2000;97(6):2709-2714. (Pubitemid 30159236)
28. Palmer S, Wiegand AP, Maldarelli F, et al. New real-time reverse transcriptase-initiated PCR assay with single-copy sensitivity for human immunodeficiency virus type 1 RNA in plasma. J Clin Microbiol. 2003;41(10):4531-4536. (Pubitemid 37259753)
29. Glass WG, McDermott DH, Lim JK, et al. CCR5 deficiency increases risk of symptomatic West Nile virus infection. J Exp Med. 2006;203(1):35-40. (Pubitemid 43139642)
30. Elbiek T, Dewar RL, Natarajan V. Isolation and detection of human immunodeficiency virus. In: Rose NR, De Macario EC, Folds JD, Lane HC, Nakamura RM, eds. Manual of Clinical Laboratory Immunology. Washington, DC: American Society for Microbiology Press; 1997:781-787.
31. Chun TW, Nickle DC, Justement JS, et al. HIV-infected individuals receiving effective antiviral therapy for extended periods of time continually replenish their viral reservoir. J Clin Invest. 2005; 115(11):3250-3255. (Pubitemid 41567589)
32. Chun TW, Engel D, Mizell SB, et al. Effect of interleukin-2 on the pool of latently infected, resting CD4+ T cells in HIV-1-infected patients receiving highly active anti-retroviral therapy. Nat Med. 1999;5(6):651-655. (Pubitemid 29289428)
33. Rabi SA, O'Connell KA, Nikolaeva D, et al. Unstimulated primary CD4+ T cells from HIV-1-positive elite suppressors are fully susceptible to HIV-1 entry and productive infection. J Virol. 2011;85(2):979-986.
34. O'Connell KA, Rabi SA, Siliciano RF, Blankson JN. CD4+ T cells from elite suppressors are more susceptible to HIV-1 but produce fewer virions than cells from chronic progressors. Proc Natl Acad Sci U S A. 2011;108(37):E689-E698.
35. Chen H, Li C, Huang J, et al. CD4+ T cells from elite controllers resist HIV-1 infection by selective upregulation of p21. J Clin Invest. 2011;121(4): 1549-1560.
36. Buzon MJ, Seiss K, Weiss R, et al. Inhibition of HIV-1 integration in ex vivo-infected CD4 T cells from elite controllers. J Virol. 2011;85(18):9646- 9650.
37. Doria-Rose NA, Klein RM, Manion MM, et al. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J Virol. 2009;83(1):188-199.
38. Burbelo PD, Ching KH, Mattson TL, Light JS, Bishop LR, Kovacs JA. Rapid antibody quantification and generation of whole proteome antibody response profiles using LIPS (luciferase immunoprecipitation systems). Biochem Biophys Res Commun. 2007;352(4):889-895. (Pubitemid 44894369)
39. Chun TW, Nickle DC, Justement JS, et al. Persistence of HIV in gut-associated lymphoid tissue despite long-term antiretroviral therapy. J Infect Dis. 2008;197(5):714-720. (Pubitemid 351364472)
40. Yukl SA, Gianella S, Sinclair E, et al. Differences in HIV burden and immune activation within the gut of HIV-positive patients receiving suppressive antiretroviral therapy. J Infect Dis. 2010;202(10): 1553-1561.
41. Blankson JN, Bailey JR, Thayil S, et al. Isolation and characterization of replication-competent human immunodeficiency virus type 1 from a subset of elite suppressors. J Virol. 2007;81(5):2508-2518.
42. Chun TW, Carruth L, Finzi D, et al. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection [see comments]. Nature. 1997; 387(6629):183-188. (Pubitemid 27209433)
43. Bailey JR, Lassen KG, Yang HC, et al. Neutralizing antibodies do not mediate suppression of human immunodeficiency virus type 1 in elite suppressors or selection of plasma virus variants in patients on highly active antiretroviral therapy. J Virol. 2006;80(10):4758-4770.
44. Bailey JR, Williams TM, Siliciano RF, Blankson JN. Maintenance of viral suppression in HIV-1-infected HLA-B*57+ elite suppressors despite CTL escape mutations. J Exp Med. 2006;203(5):1357-1369. (Pubitemid 43736603)
45. Pereyra F, Addo MM, Kaufmann DE, et al. Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J Infect Dis. 2008;197(4):563-571. (Pubitemid 351321534)
46. Migueles SA, Rood JE, Berkley AM, et al. Trivalent adenovirus type 5 HIV recombinant vaccine primes for modest cytotoxic capacity that is greatest in humans with protective HLA class I alleles. PLoS Pathog. 2011;7(2):e1002002.
47. Chun TW, Justement JS, Murray D, et al. Rebound of plasma viremia following cessation of antiretroviral therapy despite profoundly low levels of HIV reservoir: implications for eradication. AIDS. 2010;24(18):2803-2808.
48. Ling B, Mohan M, Lackner AA, et al. The large intestine as a major reservoir for simian immunodeficiency virus in macaques with long-term, nonprogressing infection. J Infect Dis. 2010;202(12): 1846-1854.
49. Allers K, Hutter G, Hofmann J, et al. Evidence for the cure of HIV infection by CCR5Delta32/Delta32 stem cell transplantation. Blood. 2011; 117(10):2791-2799.
50. Horton H, Frank I, Baydo R, et al. Preservation of T cell proliferation restricted by protective HLA alleles is critical for immune control of HIV-1 infection. J Immunol. 2006;177:7406-7415. (Pubitemid 44715111)
51. Goujard C, Chaix ML, Lambotte O, et al. Spontaneous control of viral replication during primary HIV infection: when is "HIV controller" status established? Clin Infect Dis. 2009;49(6):982-986.
52. Okulicz JF, Marconi VC, Landrum ML, et al. Clinical outcomes of elite controllers, viremic controllers, and long-term nonprogressors in the US Department of Defense HIV natural history study. J Infect Dis. 2009;200(11):1714-1723.
53. Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature. 2011; 473(7348):523-527.