HLA-B signal peptide polymorphism influences the rate of HIV-1 acquisition but not viral load

Journal of Infectious Diseases

Volumn 205, Issue 12, 2012, Pages 1797-1805

  Merino, Aimee M ^a,b   Song, Wei ^a   He, Dongning ^a   Mulenga, Joseph ^d   Allen, Susan ^d,e   Hunter, Eric ^f   Tang, Jianming ^a,b   Kaslow, Richard A ^a,b,c  

^a UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d Rwanda Zambia HIV 1 Research Group   (Zambia)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; HLA E ANTIGEN; SIGNAL PEPTIDE;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE; HOMOZYGOSITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN POLYMORPHISM; SEROCONVERSION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS LOAD;

ADULT; COHORT STUDIES; FEMALE; HIV INFECTIONS; HIV-1; HLA-B27 ANTIGEN; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, GENETIC; PROTEIN SORTING SIGNALS; RWANDA; VIRAL LOAD; ZAMBIA;

EID: 84861554024     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jis275     Document Type: Article

References (50)

1. Carrington M, Martin MP, van Bergen J. KIR-HLA intercourse in HIV disease. Trends Microbiol 2008; 16:620-7.
2. Berger CT, Frahm N, Price DA, et al. High-functional-avidity cytotoxic T lymphocyte responses to HLA-B-restricted Gag-derived epitopes associated with relative HIV control. J Virol 2011; 85:9334-45.
3. Pereyra F, Jia X, McLaren PJ, et al. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 2010; 330:1551-7.
4. Petrie EJ, Clements CS, Lin J, et al. CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J Exp Med 2008; 205:725-35.
5. Vales-Gomez M, Reyburn HT, Erskine RA, Lopez-Botet M, Strominger JL. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 1999; 18:4250-60.
6. Kaiser BK, Barahmand-Pour F, Paulsene W, Medley S, Geraghty DE, Strong RK. Interactions between NKG2x immunoreceptors and HLAE ligands display overlapping affinities and thermodynamics. J Immunol 2005; 174:2878-84.
7. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J Exp Med 1998; 187:813-8.
8. Strong RK, Holmes MA, Li P, Braun L, Lee N, Geraghty DE. HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J Biol Chem 2003; 278:5082-90.
9. 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.
10. Llano M, Lee N, Navarro F, et al. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 1998; 28:2854-63.
11. Braud V, Jones EY, McMichael A. The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur J Immunol 1997; 27:1164-9.
12. Miller JD, Weber DA, Ibegbu C, Pohl J, Altman JD, Jensen PE. Analysis of HLA-E peptide-binding specificity and contact residues in bound peptide required for recognition by CD94/NKG2. J Immunol 2003; 171:1369-75.
13. Stevens J, Joly E, Trowsdale J, Butcher GW. Peptide binding characteristics of the non-classical class Ib MHC molecule HLA-E assessed by a recombinant random peptide approach. BMC Immunol 2001; 2:5.
14. Natarajan K, Dimasi N, Wang J, Mariuzza RA, Margulies DH. Structure and function of natural killer cell receptors: multiple molecular solutions to self, nonself discrimination. Annu Rev Immunol 2002; 20:853-85.
15. Gumperz JE, Barber LD, Valiante NM, et al. Conserved and variable residues within the Bw4 motif of HLA-B make separable contributions to recognition by the NKB1 killer cell-inhibitory receptor. J Immunol 1997; 158:5237-41.
16. Carr WH, Pando MJ, Parham P. KIR3DL1 polymorphisms that affect NK cell inhibition by HLA-Bw4 ligand. J Immunol 2005; 175:5222-9.
17. Cella M, Longo A, Ferrara GB, Strominger JL, Colonna M. NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J Exp Med 1994; 180:1235-42.
18. Flores-Villanueva PO, Yunis EJ, Delgado JC, et al. Control of HIV-1 viremia and protection from AIDS are associated with HLA-Bw4 homozygosity. Proc Natl Acad Sci USA 2001; 98:5140-5.
19. Welzel TM, Gao X, Pfeiffer RM, et al. HLA-B Bw4 alleles and HIV-1 transmission in heterosexual couples. AIDS 2007; 21:225-9.
20. Martin MP, Qi Y, Gao X, et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007; 39:733-40.
21. Liu K, Kao KJ. Mechanisms for genetically predetermined differential quantitative expression of HLA-A and-B antigens. Hum Immunol 2000; 61:799-807.
22. Yunis EJ, Romero V, Diaz-Giffero F, Zuniga J, Koka P. Natural killer cell receptor NKG2A/HLA-E interaction dependent differential thymopoiesis of hematopoietic progenitor cells influences the outcome of HIV infection. J Stem Cells 2007; 2:237-48.
23. Tang J, Tang S, Lobashevsky E, et al. Favorable and unfavorable HLA class I alleles and haplotypes in Zambians predominantly infected with clade C human immunodeficiency virus type 1. J Virol 2002; 76:8276-84.
24. Tang J, Penman-Aguilar A, Lobashevsky E, Allen S, Kaslow RA. HLA-DRB1 and-DQB1 alleles and haplotypes in Zambian couples and their associations with heterosexual transmission of HIV type 1. J Infect Dis 2004; 189:1696-704.
25. Tang J, Shao W, Yoo YJ, et al. Human leukocyte antigen class I genotypes in relation to heterosexual HIV type 1 transmission within discordant couples. J Immunol 2008; 181:2626-35.
26. Tang J, Tang S, Lobashevsky E, et al. HLA allele sharing and HIV type 1 viremia in seroconverting Zambians with known transmitting partners. AIDS Res Hum Retroviruses 2004; 20:19-25.
27. Lazaryan A, Lobashevsky E, Mulenga J, et al. Human leukocyte antigen B58 supertype and human immunodeficiency virus type 1 infection in native Africans. J Virol 2006; 80:6056-60.
28. Fideli US, Allen SA, Musonda R, et al. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Res Hum Retroviruses 2001; 17:901-10.
29. Allen S, Meinzen-Derr J, Kautzman M, et al. Sexual behavior of HIV discordant couples after HIV counseling and testing. AIDS 2003; 17:733-40.
30. Trask SA, Derdeyn CA, Fideli U, et al. Molecular epidemiology of human immunodeficiency virus type 1 transmission in a heterosexual cohort of discordant couples in Zambia. J Virol 2002; 76:397-405.
31. Merino A, Malhotra R, Morton M, et al. Impact of a functional KIR2DS4 allele on heterosexual HIV-1 transmission among discordant Zambian couples. J Infect Dis 2011; 203:487-95.
32. Robinson J, Waller MJ, Fail SC, et al. The IMGT/HLA database. Nucleic Acids Res 2009; 37:D1013-7.
33. Paquay MM, Schellekens J, Tilanus MG. A high-throughput Taqman approach for the discrimination of HLA-E alleles. Tissue Antigens 2009; 74:514-9.
34. Song W, He D, Brill I, et al. Disparate associations of HLA class I markers with HIV-1 acquisition and control of viremia in an African population. PLoS One 2011; 6:e23469.
35. Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol 1998; 160:4951-60.
36. Ulbrecht M, Martinozzi S, Grzeschik M, et al. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 2000; 164:5019-22.
37. Tomasec P, Braud VM, Rickards C, et al. Surface expression of HLAE, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000; 287:1031.
38. Nattermann J, Nischalke HD, Hofmeister V, et al. HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir Ther 2005; 10:95-107.
39. Boucraut J, Guillaudeux T, Alizadeh M, et al. HLA-E is the only class I gene that escapes CpG methylation and is transcriptionally active in the trophoblast-derived human cell line JAR. Immunogenetics 1993; 38:117-30.
40. Houlihan JM, Biro PA, Harper HM, Jenkinson HJ, Holmes CH. The human amnion is a site of MHC class Ib expression: evidence for the expression of HLA-E and HLA-G. J Immunol 1995; 154:5665-74.
41. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 1998; 391:397-401.
42. Cohen GB, Gandhi RT, Davis DM, et al. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 1999; 10:661-71.
43. Braud VM, Allan DS, O'Callaghan CA, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998; 391:795-9.
44. Michaelsson J, Teixeira de Matos C, Achour A, Lanier LL, Karre K, Soderstrom K. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 2002; 196:1403-14.
45. Ulbrecht M, Couturier A, Martinozzi S, et al. Cell surface expression of HLA-E: interaction with human beta2-microglobulin and allelic differences. Eur J Immunol 1999; 29:537-47.
46. Barbour JD, Sriram U, Caillier SJ, Levy JA, Hecht FM, Oksenberg JR. Synergy or independence? Deciphering the interaction of HLA Class I and NK cell KIR alleles in early HIV-1 disease progression. PLoS Pathog 2007; 3:e43.
47. Martin MP, Gao X, Lee JH, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 2002; 31:429-34.
48. Carrington M, O'Brien SJ. The influence of HLA genotype on AIDS. Annu Rev Med 2003; 54:535-51.
49. Parsons MS, Boulet S, Song R, et al. Mind the gap: lack of association between KIR3DL1*004/HLA-Bw4-induced natural killer cell function and protection from HIV infection. J Infect Dis 2010; 202(Suppl 3): S356-60.
50. Stern M, Ruggeri L, Capanni M, Mancusi A, Velardi A. Human leukocyte antigens A23, A24, and A32 but not A25 are ligands for KIR3DL1. Blood 2008; 112:708-10.