CD8+ T-cell Cytotoxic Capacity Associated with Human Immunodeficiency Virus-1 Control Can Be Mediated through Various Epitopes and Human Leukocyte Antigen Types

EBioMedicine

Volumn 2, Issue 1, 2015, Pages 46-58

  Migueles, Stephen A ^a   Mendoza, Daniel ^a   Zimmerman, Matthew G ^a   Martins, Kelly M ^a   Toulmin, Sushila A ^a   Kelly, Elizabeth P ^a   Peterson, Bennett A ^a   Johnson, Sarah A ^a   Galson, Eric ^a   Poropatich, Kate O ^a   Patamawenu, Andy ^a   Imamichi, Hiromi ^a   Ober, Alexander ^a   Rehm, Catherine A ^a   Jones, Sara ^b   Hallahan, Claire W ^a   Follmann, Dean A ^a   Connors, Mark ^a  

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

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

CD8+ T cells; Cytotoxic capacity; Epitope specificity; Immune control; Long term nonprogressors elite controllers

Indexed keywords

AMINO ACID; EPITOPE; GAG PROTEIN; HLA ANTIGEN; LEUKOCYTE ANTIGEN; NEF PROTEIN; POL PROTEIN; VIRUS RNA;

ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CLINICAL FEATURE; CYTOTOXICITY; DISEASE COURSE; ENTROPY; FLOW CYTOMETRY; GENE FREQUENCY; GENETIC ASSOCIATION; HLA SYSTEM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNE RESPONSE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; VIRUS LOAD; AMINO ACID SEQUENCE; CHEMISTRY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; MOLECULAR GENETICS; VIROLOGY;

AMINO ACID SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; ENTROPY; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HLA ANTIGENS; HUMANS; IMMUNODOMINANT EPITOPES; MOLECULAR SEQUENCE DATA;

EID: 84927724304     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2014.12.009     Document Type: Article

References (57)

1. Allen T.M., Altfeld M., Geer S.C., Kalife E.T., Moore C., O'Sullivan K.M., Desouza I., Feeney M.E., Eldridge R.L., Maier E.L., et al. Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J. Virol. 2005, 79:13239-13249.
2. Altfeld M., Addo M.M., Rosenberg E.S., Hecht F.M., Lee P.K., Vogel M., Yu X.G., Draenert R., Johnston M.N., Strick D., et al. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 2003, 17:2581-2591.
3. Bailey J.R., Williams T.M., Siliciano R.F., Blankson J.N. Maintenance of viral suppression in HIV-1-infected HLA-B*57+ elite suppressors despite CTL escape mutations. J. Exp. Med. 2006, 203:1357-1369.
4. Bansal A., Gough E., Sabbaj S., Ritter D., Yusim K., Sfakianos G., Aldrovandi G., Kaslow R.A., Wilson C.M., Mulligan M.J., et al. CD8 T-cell responses in early HIV-1 infection are skewed towards high entropy peptides. AIDS 2005, 19:241-250.
5. Betts M.R., Ambrozak D.R., Douek D.C., Bonhoeffer S., Brenchley J.M., Casazza J.P., Koup R.A., Picker L.J. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 2001, 75:11983-11991.
6. Betts M.R., Nason M.C., West S.M., De Rosa S.C., Migueles S.A., Abraham J., Lederman M.M., Benito J.M., Goepfert P.A., Connors M., et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006, 107:4781-4789.
7. Blankson J.N., Bailey J.R., Thayil S., Yang H.C., Lassen K., Lai J., Gandhi S.K., Siliciano J.D., Williams T.M., Siliciano R.F. Isolation and characterization of replication-competent human immunodeficiency virus type 1 from a subset of elite suppressors. J. Virol. 2007, 81:2508-2518.
8. Brockman M.A., Schneidewind A., Lahaie M., Schmidt A., Miura T., Desouza I., Ryvkin F., Derdeyn C.A., Allen S., Hunter E., 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, 81:12608-12618.
9. Buckheit R.W., Allen T.G., Alme A., Salgado M., O'Connell K.A., Huculak S., Falade-Nwulia O., Williams T.M., Gallant J.E., Siliciano R.F., et al. Host factors dictate control of viral replication in two HIV-1 controller/chronic progressor transmission pairs. Nat. Commun. 2012, 3:716.
10. Buranapraditkun S., Hempel U., Pitakpolrat P., Allgaier R.L., Thantivorasit P., Lorenzen S.I., Sirivichayakul S., Hildebrand W.H., Altfeld M., Brander C., et al. A novel immunodominant CD8+ T cell response restricted by a common HLA-C allele targets a conserved region of Gag HIV-1 clade CRF01_AE infected Thais. PLoS ONE 2011, 6:e23603.
11. Crawford H., Prado J.G., Leslie A., Hue S., Honeyborne I., Reddy S., van der Stok M., Mncube Z., Brander C., Rousseau C., et al. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLA-B*5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 2007, 81:8346-8351.
12. Dinges W.L., Richardt J., Friedrich D., Jalbert E., Liu Y., Stevens C.E., Maenza J., Collier A.C., Geraghty D.E., Smith J., et al. Virus-specific CD8+ T-cell responses better define HIV disease progression than HLA genotype. J. Virol. 2010, 84:4461-4468.
13. Ferre A.L., Hunt P.W., Critchfield J.W., Young D.H., Morris M.M., Garcia J.C., Pollard R.B., Yee H.F., Martin J.N., Deeks S.G., et al. Mucosal immune responses to HIV-1 in elite controllers: a potential correlate of immune control. Blood 2009, 113:3978-3989.
14. Flores-Villanueva P.O., Yunis E.J., Delgado J.C., Vittinghoff E., Buchbinder S., Leung J.Y., Uglialoro A.M., Clavijo O.P., Rosenberg E.S., Kalams S.A., et al. Control of HIV-1 viremia and protection from AIDS are associated with HLA-Bw4 homozygosity. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5140-5145.
15. Frahm N., Adams S., Kiepiela P., Linde C.H., Hewitt H.S., Lichterfeld M., Sango K., Brown N.V., Pae E., Wurcel A.G., et al. HLA-B63 presents HLA-B57/B58-restricted cytotoxic T-lymphocyte epitopes and is associated with low human immunodeficiency virus load. J. Virol. 2005, 79:10218-10225.
16. Frahm N., Kiepiela P., Adams S., Linde C.H., Hewitt H.S., Sango K., Feeney M.E., Addo M.M., Lichterfeld M., Lahaie M.P., et al. Control of human immunodeficiency virus replication by cytotoxic T lymphocytes targeting subdominant epitopes. Nat. Immunol. 2006, 7:173-178.
17. Frahm N., Korber B.T., Adams C.M., Szinger J.J., Draenert R., Addo M.M., Feeney M.E., Yusim K., Sango K., Brown N.V., et al. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 2004, 78:2187-2200.
18. Friedrich T.C., Dodds E.J., Yant L.J., Vojnov L., Rudersdorf R., Cullen C., Evans D.T., Desrosiers R.C., Mothe B.R., Sidney J., et al. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 2004, 10:275-281.
19. Friedrich T.C., Valentine L.E., Yant L.J., Rakasz E.G., Piaskowski S.M., Furlott J.R., Weisgrau K.L., Burwitz B., May G.E., Leon E.J., et al. Subdominant CD8+ T-cell responses are involved in durable control of AIDS virus replication. J. Virol. 2007, 81:3465-3476.
20. Goulder P.J., Brander C., Annamalai K., Mngqundaniso N., Govender U., Tang Y., He S., Hartman K.E., O'Callaghan C.A., Ogg G.S., et al. Differential narrow focusing of immunodominant human immunodeficiency virus gag-specific cytotoxic T-lymphocyte responses in infected African and caucasoid adults and children. J. Virol. 2000, 74:5679-5690.
21. Goulder P.J., Bunce M., Krausa P., McIntyre K., Crowley S., Morgan B., Edwards A., Giangrande P., Phillips R.E., McMichael A.J. Novel, cross-restricted, conserved, and immunodominant cytotoxic T lymphocyte epitopes in slow progressors in HIV type 1 infection. AIDS Res. Hum. Retrovir. 1996, 12:1691-1698.
22. Goulder P.J., Phillips R.E., Colbert R.A., McAdam S., Ogg G., Nowak M.A., Giangrande P., Luzzi G., Morgan B., Edwards A., et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 1997, 3:212-217.
23. Hansen S.G., Sacha J.B., Hughes C.M., Ford J.C., Burwitz B.J., Scholz I., Gilbride R.M., Lewis M.S., Gilliam A.N., Ventura A.B., et al. Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science 2013, 340:1237874.
24. Hersperger A.R., Migueles S.A., Betts M.R., Connors M. Qualitative features of the HIV-specific CD8+ T-cell response associated with immunologic control. Curr. Opin. HIV AIDS 2011, 6:169-173.
25. Hersperger A.R., Pereyra F., Nason M., Demers K., Sheth P., Shin L.Y., Kovacs C.M., Rodriguez B., Sieg S.F., Teixeira-Johnson L., et al. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog. 2010, 6:e1000917.
26. Honeyborne I., Prendergast A., Pereyra F., Leslie A., Crawford H., Payne R., Reddy S., Bishop K., Moodley E., Nair K., et al. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. J. Virol. 2007, 81:3667-3672.
27. Horton H., Frank I., Baydo R., Jalbert E., Penn J., Wilson S., McNevin J.P., McSweyn M.D., Lee D., Huang Y., 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.
28. Kaslow R.A., Carrington M., Apple R., Park L., Munoz A., Saah A.J., Goedert J.J., Winkler C., O'Brien S.J., Rinaldo C., et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 1996, 2:405-411.
29. Kunwar P., Hawkins N., Dinges W.L., Liu Y., Gabriel E.E., Swan D.A., Stevens C.E., Maenza J., Collier A.C., Mullins J.I., et al. Superior control of HIV-1 replication by CD8+ T cells targeting conserved epitopes: implications for HIV vaccine design. PLoS ONE 2013, 8:e64405.
30. Lamine A., Caumont-Sarcos A., Chaix M.L., Saez-Cirion A., Rouzioux C., Delfraissy J.F., Pancino G., Lambotte O. Replication-competent HIV strains infect HIV controllers despite undetectable viremia (ANRS EP36 study). AIDS 2007, 21:1043-1045.
31. Lecuroux C., Saez-Cirion A., Girault I., Versmisse P., Boufassa F., Avettand-Fenoel V., Rouzioux C., Meyer L., Pancino G., Lambotte O., et al. Both HLA-B*57 and plasma HIV RNA levels contribute to the HIV-specific CD8+ T cell response in HIV controllers. J. Virol. 2014, 88:176-187.
32. Leslie A.J., Pfafferott K.J., Chetty P., Draenert R., Addo M.M., Feeney M., Tang Y., Holmes E.C., Allen T., Prado J.G., et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 2004, 10:282-289.
33. Liu M.K., Hawkins N., Ritchie A.J., Ganusov V.V., Whale V., Brackenridge S., Li H., Pavlicek J.W., Cai F., Rose-Abrahams M., et al. Vertical T cell immunodominance and epitope entropy determine HIV-1 escape. J. Clin. Investig. 2013, 123:380-393.
34. Liu Y., McNevin J., Rolland M., Zhao H., Deng W., Maenza J., Stevens C.E., Collier A.C., McElrath M.J., Mullins J.I. Conserved HIV-1 epitopes continuously elicit subdominant cytotoxic T-lymphocyte responses. J. Infect. Dis. 2009, 200:1825-1833.
35. Loffredo J.T., Maxwell J., Qi Y., Glidden C.E., Borchardt G.J., Soma T., Bean A.T., Beal D.R., Wilson N.A., Rehrauer W.M., et al. Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J. Virol. 2007, 81:8827-8832.
36. Mendoza D., Migueles S.A., Rood J.E., Peterson B., Johnson S., Doria-Rose N., Schneider D., Rakasz E., Trivett M.T., Trubey C.M., et al. Cytotoxic capacity of SIV-specific CD8(+) T cells against primary autologous targets correlates with immune control in SIV-infected rhesus macaques. PLoS Pathog. 2013, 9:e1003195.
37. Migueles S.A., Connors M. Long-term nonprogressive disease among untreated HIV-infected individuals: clinical implications of understanding immune control of HIV. JAMA 2010, 304:194-201.
38. Migueles S.A., Laborico A.C., Imamichi H., Shupert W.L., Royce C., McLaughlin M., Ehler L., Metcalf J., Liu S., Hallahan C.W., et al. The differential ability of HLA B*5701+ long-term nonprogressors and progressors to restrict human immunodeficiency virus replication is not caused by loss of recognition of autologous viral gag sequences. J. Virol. 2003, 77:6889-6898.
39. Migueles S.A., Laborico A.C., Shupert W.L., Sabbaghian M.S., Rabin R., Hallahan C.W., Van Baarle D., Kostense S., Miedema F., McLaughlin M., et al. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 2002, 3:1061-1068.
40. Migueles S.A., Osborne C.M., Royce C., Compton A.A., Joshi R.P., Weeks K.A., Rood J.E., Berkley A.M., Sacha J.B., Cogliano-Shutta N.A., et al. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 2008, 29:1009-1021.
41. Migueles S.A., Rood J.E., Berkley A.M., Guo T., Mendoza D., Patamawenu A., Hallahan C.W., Cogliano N.A., Frahm N., Duerr A., 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:e1002002.
42. Migueles S.A., Sabbaghian M.S., Shupert W.L., Bettinotti M.P., Marincola F.M., Martino L., Hallahan C.W., Selig S.M., Schwartz D., Sullivan J., 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, 97:2709-2714.
43. Migueles S.A., Weeks K.A., Nou E., Berkley A.M., Rood J.E., Osborne C.M., Hallahan C.W., Cogliano-Shutta N.A., Metcalf J.A., McLaughlin M., et al. Defective human immunodeficiency virus-specific CD8+ T-cell polyfunctionality, proliferation, and cytotoxicity are not restored by antiretroviral therapy. J. Virol. 2009, 83:11876-11889.
44. Miura T., Brockman M.A., Schneidewind A., Lobritz M., Pereyra F., Rathod A., Block B.L., Brumme Z.L., Brumme C.J., Baker B., et al. HLA-B57/B*5801 human immunodeficiency virus type 1 elite controllers select for rare gag variants associated with reduced viral replication capacity and strong cytotoxic T-lymphocyte recognition. J. Virol. 2009, 83:2743-2755.
45. Mothe B., Llano A., Ibarrondo J., Daniels M., Miranda C., Zamarreno J., Bach V., Zuniga R., Perez-Alvarez S., Berger C.T., et al. Definition of the viral targets of protective HIV-1-specific T cell responses. J. Transl. Med. 2011, 9:208.
46. Navis M., Schellens I., van Baarle D., Borghans J., van Swieten P., Miedema F., Kootstra N., Schuitemaker H. Viral replication capacity as a correlate of HLA B57/B5801-associated nonprogressive HIV-1 infection. J. Immunol. 2007, 179:3133-3143.
47. Pereyra F., Heckerman D., Carlson J.M., Kadie C., Soghoian D.Z., Karel D., Goldenthal A., Davis O.B., DeZiel C.E., Lin T., et al. HIV control is mediated in part by CD8+ T-cell targeting of specific epitopes. J. Virol. 2014, 88:12937-12948.
48. Peyerl F.W., Bazick H.S., Newberg M.H., Barouch D.H., Sodroski J., Letvin N.L. Fitness costs limit viral escape from cytotoxic T lymphocytes at a structurally constrained epitope. J. Virol. 2004, 78:13901-13910.
49. Pohlmeyer C.W., Buckheit R.W., Siliciano R.F., Blankson J.N. CD8+ T cells from HLA-B*57 elite suppressors effectively suppress replication of HIV-1 escape mutants. Retrovirology 2013, 10:152.
50. Saez-Cirion A., Lacabaratz C., Lambotte O., Vermisse P., Urrutia A., Boufassa F., Barre-Sinoussi F., Delfraissy J.-F., Sinet M., Pancino G., 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, 104:6776-6781.
51. Saez-Cirion A., Sinet M., Shin S.Y., Urrutia A., Versmisse P., Lacabaratz C., Boufassa F., Avettand-Fenoel V., Rouzioux C., Delfraissy J.F., et al. Heterogeneity in HIV suppression by CD8 T cells from HIV controllers: association with Gag-specific CD8 T cell responses. J. Immunol. 2009, 182:7828-7837.
52. Sunshine J., Kim M., Carlson J.M., Heckerman D., Czartoski J., Migueles S.A., Maenza J., McElrath M.J., Mullins J.I., Frahm N. Increased sequence coverage through combined targeting of variant and conserved epitopes correlates with control of HIV replication. J. Virol. 2014, 88:1354-1365.
53. Thomas R., Apps R., Qi Y., Gao X., Male V., O'HUigin C., O'Connor 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.
54. Yant L.J., Friedrich T.C., Johnson R.C., May G.E., Maness N.J., Enz A.M., Lifson J.D., O'Connor D.H., Carrington M., Watkins D.I. The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 2006, 80:5074-5077.
55. Yusim K., Kesmir C., Gaschen B., Addo M.M., Altfeld M., Brunak S., Chigaev A., Detours V., Korber B.T. Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation. J. Virol. 2002, 76:8757-8768.
56. Zhang Y., Peng Y., Yan H., Xu K., Saito M., Wu H., Chen X., Ranasinghe S., Kuse N., Powell T., et al. Multilayered defense in HLA-B51-associated HIV viral control. J. Immunol. 2011, 187:684-691.
57. Zimmerli S.C., Harari A., Cellerai C., Vallelian F., Bart P.A., 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, 102:7239-7244.