Reappraisal of the relationship between the HIV-1-protective single-nucleotide polymorphism 35 kilobases upstream of the HLA-C gene and surface HLA-C expression

Journal of Virology

Volumn 85, Issue 7, 2011, Pages 3367-3374

  Corrah, Tumena W ^a   Goonetilleke, Nilu ^a   Kopycinski, Jakub ^b   Deeks, Steven G ^c   Cohen, Myron S ^d   Borrow, Persephone ^e   McMichael, Andrew ^a   Brackenridge, Simon ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HLA B ANTIGEN; HLA C ANTIGEN;

ALLELE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENOTYPE; HLA C GENE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS LOAD;

GENE EXPRESSION; HIV-1; HLA-C ANTIGENS; HUMANS; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; REGULATORY ELEMENTS, TRANSCRIPTIONAL; VIRAL LOAD;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79952603435     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02276-10     Document Type: Article

References (56)

1. Adnan, S., et al. 2006. Nef interference with HIV-1-specific CTL antiviral activity is epitope specific. Blood 108:3414-3419.
2. Altfeld, M., et al. 2003. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17:2581-2591. (Pubitemid 38402336)
3. Barnstable, C. J., et al. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens - new tools for genetic analysis. Cell 14:9-20. (Pubitemid 8340429)
4. Bihl, F., et al. 2006. Impact of HLA-B alleles, epitope binding affinity, functional avidity, and viral coinfection on the immunodominance of virusspecific CTL responses. J. Immunol. 176:4094-4101. (Pubitemid 44264388)
5. Bonaparte, M. I., and E. Barker. 2004. Killing of human immunodeficiency virus-infected primary T-cell blasts by autologous natural killer cells is dependent on the ability of the virus to alter the expression of major histocompatibility complex class I molecules. Blood 104:2087-2094. (Pubitemid 39297862)
6. Braud, V. M., et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795-799.
7. Braud, V. M., D. S. Allan, D. Wilson, and A. J. McMichael. 1998. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8:1-10.
8. Carrington, M., et al. 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283:1748-1752.
9. Carrington, M., and S. J. O'Brien. 2003. The influence of HLA genotype on AIDS. Annu. Rev. Med. 54:535-551.
10. Catano, G., et al. 2008. HIV-1 disease-influencing effects associated with ZNRD1, HCP5 and HLA-C alleles are attributable mainly to either HLAA10 or HLA-B*57 alleles. PLoS One 3:e3636.
11. Cohen, G. B., et al. 1999. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661-671. (Pubitemid 29302919)
12. Collins, K. L., and D. Baltimore. 1999. HIV's evasion of the cellular immune response. Immunol. Rev. 168:65-74.
13. Collins, K. L., B. K. Chen, S. A. Kalams, B. D. Walker, and D. Baltimore. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401. (Pubitemid 28093515)
14. Coupel, S., et al. 2007. Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood 109:2806-2814. (Pubitemid 46482075)
15. Dalmasso, C., et al. 2008. Distinct genetic loci control plasma HIV-RNA and cellular HIV-DNA levels in HIV-1 infection: the ANRS Genome Wide Association 01 study. PLoS One 3:e3907.
16. Dickson, S. P., K. Wang, I. Krantz, H. Hakonarson, and D. B. Goldstein. Rare variants create synthetic genome-wide associations. PLoS Biol. 8:e1000294.
17. Fellay, J., et al. 2009. Common genetic variation and the control of HIV-1 in humans. PLoS Genet. 5:e1000791.
18. Fellay, J., et al. 2007. A whole-genome association study of major determinants for host control of HIV-1. Science 317:944-947. (Pubitemid 47301321)
19. Frazer, K. A., S. S. Murray, N. J. Schork, and E. J. Topol. 2009. Human genetic variation and its contribution to complex traits. Nat. Rev. Genet. 10:241-251.
20. Goldstein, D. B. 2009. Common genetic variation and human traits. N. Engl. J. Med. 360:1696-1698.
21. Goulder, P. J., and D. I. Watkins. 2008. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8:619-630.
22. Hunt, P. W., et al. 2003. T cell activation is associated with lower CD4+ T cell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy. J. Infect. Dis. 187:1534-1543.
23. Johnson, D. R. 2000. Differential expression of human major histocompatibility class I loci: HLA-A, -B, and -C. Hum. Immunol. 61:389-396.
24. Kaslow, R. A., et al. 1990. A1, Cw7, B8, DR3 HLA antigen combination associated with rapid decline of T-helper lymphocytes in HIV-1 infection. A report from the Multicenter AIDS Cohort Study. Lancet 335:927-930.
25. Kiepiela, P., et al. 2004. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432:769-775.
26. Kiepiela, P., et al. 2007. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
27. Kosmrlj, A., et al. Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 465:350-354.
28. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-274.
29. Lee, N., D. R. Goodlett, A. Ishitani, H. Marquardt, and D. E. Geraghty. 1998. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol. 160:4951-4960.
30. Leslie, A., et al. 2010. Additive contribution of HLA class I alleles in the immune control of HIV-1 infection. J. Virol. 84:9879-9888.
31. Limou, S., et al. 2009. Genomewide association study of an AIDS-nonprogression cohort emphasizes the role played by HLA genes (ANRS Genomewide Association Study 02). J. Infect. Dis. 199:419-426.
32. Lo Monaco, E., et al. 2008. HLA-E: strong association with beta2-microglobulin and surface expression in the absence of HLA class I signal sequence- derived peptides. J. Immunol. 181:5442-5450.
33. McCutcheon, J. A., J. Gumperz, K. D. Smith, C. T. Lutz, and P. Parham. 1995. Low HLA-C expression at cell surfaces correlates with increased turnover of heavy chain mRNA. J. Exp. Med. 181:2085-2095.
34. McMichael, A. J., P. Borrow, G. D. Tomaras, N. Goonetilleke, and B. F. Haynes. The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 10:11-23.
35. McNeil, A. J., et al. 1996. Association of HLA types A1-B8-DR3 and B27 with rapid and slow progression of HIV disease. QJM 89:177-185. (Pubitemid 26086136)
36. Mellors, J. W., et al. 2007. Prognostic value of HIV-1 RNA, CD4 cell count, and CD4 cell count slope for progression to AIDS and death in untreated HIV-1 infection. JAMA 297:2349-2350. (Pubitemid 46883761)
37. Mellors, J. W., et al. 1997. Plasma viral load and CD4+ lymphocytes as prognostic markers of HIV-1 infection. Ann. Intern. Med. 126:946-954.
38. Menier, C., et al. 2003. Characterization of monoclonal antibodies recognizing HLA-G or HLA-E: new tools to analyze the expression of nonclassical HLA class I molecules. Hum. Immunol. 64:315-326.
39. Middleton, D., L. Menchaca, H. Rood, and R. Komerofsky. 2003. New allele frequency database: http://www.allelefrequencies.net. Tissue Antigens 61:403-407.
40. Migueles, S. A., et al. 2000. 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. 97:2709-2714.
41. Nattermann, J., et al. 2005. HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir. Ther. 10:95-107.
42. O'Brien, S. J., X. Gao, and M. Carrington. 2001. HLA and AIDS: a cautionary tale. Trends Mol. Med. 7:379-381.
43. Olerup, O., and H. Zetterquist. 1992. HLA-DR typing by PCR amplification with sequence-specific primers (PCR-SSP) in 2 hours: an alternative to serological DR typing in clinical practice including donor-recipient matching in cadaveric transplantation. Tissue Antigens 39:225-235.
44. Palmisano, G. L., et al. 2005. HLA-E surface expression is independent of the availability of HLA class I signal sequence-derived peptides in human tumor cell lines. Hum. Immunol. 66:1-12.
45. Parham, P. 2005. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5:201-214.
46. Pei, R., J. H. Lee, N. J. Shih, M. Chen, and P. I. Terasaki. 2003. Single human leukocyte antigen flow cytometry beads for accurate identification of human leukocyte antigen antibody specificities. Transplantation 75:43-49.
47. Pelak, K., et al. Host determinants of HIV-1 control in African Americans. J. Infect. Dis. 201:1141-1149.
48. Pereyra, F., et al. 2010. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551-1557.
49. Shrestha, S., et al. 2009. Host genetics and HIV-1 viral load set-point in African-Americans. AIDS 23:673-677.
50. Snary, D., C. J. Barnstable, W. F. Bodmer, and M. J. Crumpton. 1977. Molecular structure of human histocompatibility antigens: the HLA-C series. Eur. J. Immunol. 7:580-585.
51. Stranger, B. E., et al. 2005. Genome-wide associations of gene expression variation in humans. PLoS Genet. 1:e78.
52. Thomas, R., et al. 2009. HLA-C cell surface expression and control of HIV/AIDS correlate with a variant upstream of HLA-C. Nat. Genet. 41: 1290-1294.
53. Trachtenberg, E., et al. 2009. The HLA-B/-C haplotype block contains major determinants for host control of HIV. Genes Immun. 10:673-677.
54. Turnbull, E. L., et al. 2006. HIV-1 epitope-specific CD8+ T cell responses strongly associated with delayed disease progression cross-recognize epitope variants efficiently. J. Immunol. 176:6130-6146.
55. van Manen, D., et al. 2009. Association of HLA-C and HCP5 gene regions with the clinical course of HIV-1 infection. AIDS 23:19-28.
56. Williams, M., et al. 2002. Direct binding of human immunodeficiency virus type 1 Nef to the major histocompatibility complex class I (MHC-I) cytoplasmic tail disrupts MHC-I trafficking. J. Virol. 76:12173-12184. (Pubitemid 35304315)