Impact of a functional KIR2DS4 allele on heterosexual HIV-1 transmission among discordant Zambian couples

Journal of Infectious Diseases

Volumn 203, Issue 4, 2011, Pages 487-495

  Merino, Aimee ^a,b   Malhotra, Rakhi ^c   Morton, Matt ^c   Mulenga, Joseph ^d   Allen, Susan ^d,e   Hunter, Eric ^f   Tang, Jianming ^a,b   Kaslow, Richard A ^a,b,c  

^a University of Alabama at Birmingham   (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

HLA ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL4; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL5A; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL5B; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DP1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS4; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS5; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DP1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DS1; UNCLASSIFIED DRUG;

ADULT; ALLELE; ARTICLE; COITUS; CONTROLLED STUDY; FEMALE; GENETIC VARIABILITY; GENITAL ULCER; HETEROSEXUALITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MAJOR CLINICAL STUDY; MALE; NATURAL KILLER CELL; PRIORITY JOURNAL; PROSPECTIVE STUDY; SEROCONVERSION; SEXUAL INTERCOURSE; SEXUAL TRANSMISSION; VIRUS LOAD; VIRUS TRANSMISSION; ZAMBIA;

ADULT; FAMILY CHARACTERISTICS; FEMALE; GENE FREQUENCY; HETEROSEXUALITY; HIV INFECTIONS; HIV-1; HUMANS; MALE; RECEPTORS, KIR; VIRAL LOAD; ZAMBIA;

EID: 79751518166     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jiq075     Document Type: Article

References (50)

1. Raulet DH. Recognition events that inhibit and activate natural killer cells. Curr Opin Immunol 1996; 8:372-7. (Pubitemid 26229659)
2. Norman PJ, Cook MA, Carey BS, et al. SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics 2004; 56:225-37. (Pubitemid 39119277)
3. Katz G, Markel G, Mizrahi S, Arnon TI, Mandelboim O. Recognition of HLA-Cw4 but not HLA-Cw6 by the NK cell receptor killer cell Ig-like receptor two-domain short tail number 4. J Immunol 2001; 166: 7260-7. (Pubitemid 32525600)
4. Christensen MD, Geisler C. Recruitment of SHP-1 protein tyrosine phosphatase and signalling by a chimeric T-cell receptor-killer inhibitory receptor. Scand J Immunol 2000; 51:557-64. (Pubitemid 30353364)
5. Chwae YJ, Chang MJ, Park SM, et al. Molecular mechanism of the activation-induced cell death inhibition mediated by a p70 inhibitory killer cell Ig-like receptor in Jurkat T cells. J Immunol 2002; 169: 3726-35.
6. Biassoni R, Cantoni C, Falco M, et al. The human leukocyte antigen (HLA)-C-specific "activatory" or "inhibitory" natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions. J Exp Med 1996; 183:645-50.
7. Schellekens J, Rozemuller EH, Petersen EJ, et al. Patients benefit from the addition of KIR repertoire data to the donor selection procedure for unrelated haematopoietic stem cell transplantation. Mol Immunol 2008; 45:981-9. (Pubitemid 350016341)
8. Lu Z, Zhang B, Chen S, et al. Association of KIR genotypes and haplotypes with susceptibility to chronic hepatitis B virus infection in Chinese Han population. Cell Mol Immunol 2008; 5:457-63.
9. 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. (Pubitemid 35154456)
10. Long BR, Ndhlovu LC, Oksenberg JR, et al. Conferral of enhanced natural killer cell function by KIR3DS1 in early human immunodeficiency virus type 1 infection. J Virol 2008; 82:4785-92. (Pubitemid 351657040)
11. Alter G, Rihn S, Walter K, et al. HLA class I subtype-dependent expansion of KIR3DS1+ and KIR3DL1+ NK cells during acute human immunodeficiency virus type 1 infection. J Virol 2009; 83:6798-805.
12. Carrington M, Martin MP, van Bergen J. KIR-HLA intercourse in HIV disease. Trends Microbiol 2008; 16:620-7.
13. Agarwal SK, Gourh P, Shete S, et al. Association of interleukin 23 receptor polymorphisms with anti-topoisomerase-I positivity and pulmonary hypertension in systemic sclerosis. J Rheumatol 2009; 36:2715-23.
14. Butler DM, Smith DM, Cachay ER, et al. Herpes simplex virus 2 serostatus and viral loads of HIV-1 in blood and semen as risk factors for HIV transmission among men who have sex with men. AIDS 2008; 22:1667-71.
15. Paz-Bailey G, Sternberg M, Puren AJ, et al. Determinants. of HIV type 1 shedding from genital ulcers among men in South Africa. Clin Infect Dis 2010; 50:1060-7.
16. Jin F, Prestage GP, Imrie J, et al. Anal sexually transmitted infections and risk of HIV infection in homosexual men. J Acquir Immune Defic Syndr 2010; 53:144-9.
17. Bernstein KT, Marcus JL, Nieri G, Philip SS, Klausner JD. Rectal gonorrhea and chlamydia reinfection is associated with increased risk of HIV seroconversion. J Acquir Immune Defic Syndr 2010; 53:537-43.
18. 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.
19. 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. (Pubitemid 43849183)
20. 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. (Pubitemid 38147173)
21. 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. (Pubitemid 34809082)
22. 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. (Pubitemid 32881333)
23. 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. (Pubitemid 33139024)
24. Yoo YJ, Tang J, Kaslow RA, Zhang K. Haplotype inference for present-absent genotype data using previously identified haplotypes and haplotype patterns. Bioinformatics 2007; 23:2399-406. (Pubitemid 47423837)
25. Gao X, Becker LC, Becker DM, Starmer JD, Province MA. Avoiding the high Bonferroni penalty in genome-wide association studies. Genet Epidemiol 2010; 34:100-5.
26. Martin MP, Single RM, Wilson MJ, Trowsdale J, Carrington M. KIR haplotypes defined by segregation analysis in 59 Centre d'Etude Polymorphisme Humain (CEPH) families. Immunogenetics 2008; 60:767-74.
27. Chewning JH, Gudme CN, Hsu KC, Selvakumar A, Dupont B. KIR2DS1-positive NK cells mediate alloresponse against the C2 HLA-KIR ligand group in vitro. J Immunol 2007; 179:854-68.
28. Graef T, Moesta AK, Norman PJ, et al. KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J Exp Med 2009; 206: 2557-72.
29. Uyar FA, Dorak MT, Saruhan-Direskeneli G. Human leukocyte antigen-A, -B and -C alleles and human leukocyte antigen haplotypes in Turkey: Relationship to other populations. Tissue Antigens 2004; 64:180-7.
30. Rose MJ, Brooks AG, Stewart LA, Nguyen TH, Schwarer AP. Killer Iglike receptor ligand mismatch directs NK cell expansion in vitro. J Immunol 2009; 183:4502-8.
31. 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. (Pubitemid 46848586)
32. Jennes W, Verheyden S, Demanet C, et al. 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. (Pubitemid 44715020)
33. Boulet S, Sharafi S, Simic N, et al. Increased proportion of KIR3DS1 homozygotes in HIV-exposed uninfected individuals. AIDS 2008; 22:595-9. (Pubitemid 351640592)
34. Gagne K, Busson M, Bignon JD, et al. Donor KIR3DL1/3DS1 gene and recipient Bw4 KIR ligand as prognostic markers for outcome in unrelated hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2009; 15:1366-75.
35. Katz G, Gazit R, Arnon TI, et al. MHC class I-independent recognition of NK-activating receptor KIR2DS4. J Immunol 2004; 173:1819-25. (Pubitemid 38971615)
36. Maxwell LD, Wallace A, Middleton D, Curran MD. A common KIR2DS4 deletion variant in the human that predicts a soluble KIR molecule analogous to the KIR1D molecule observed in the rhesus monkey. Tissue Antigens 2002; 60:254-8. (Pubitemid 35398828)
37. Middleton D, Gonzalez A, Gilmore PM. Studies on the expression of the deleted KIR2DS4*003 gene product and distribution of KIR2DS4 deleted and nondeleted versions in different populations. Hum Immunol 2007; 68:128-34. (Pubitemid 46282218)
38. Crawford H, Lumm W, Leslie A, et al. Evolution of HLA-B*5703 HIV-1 escape mutations in HLA-B*5703-positive individuals and their transmission recipients. J Exp Med 2009; 206:909-21.
39. Gumbi PP, Nkwanyana NN, Bere A, et al. Impact of mucosal inflammation on cervical human immunodeficiency virus (HIV-1)-specific CD8 T-cell responses in the female genital tract during chronic HIV infection. J Virol 2008; 82:8529-36.
40. Cummins JE, Christensen L, Lennox JL, et al. Mucosal innate immune factors in the female genital tract are associated with vaginal HIV-1 shedding independent of plasma viral load. AIDS Res Hum Retroviruses 2006; 22:788-95. (Pubitemid 44735006)
41. Zuckerman RA, Whittington WL, Celum CL, et al. Higher concentration of HIV RNA in rectal mucosa secretions than in blood and seminal plasma, among men who have sex with men, independent of antiretroviral therapy. J Infect Dis 2004; 190:156-61. (Pubitemid 38858416)
42. Nkwanyana NN, Gumbi PP, Roberts L, et al. Impact of human immunodeficiency virus 1 infection and inflammation on the composition and yield of cervical mononuclear cells in the female genital tract. Immunology 2009; 128:e746-57.
43. Martin MP, Nelson G, Lee JH, et al. Cutting edge: susceptibility to psoriatic arthritis: influence of activating killer Ig-like receptor genes in the absence of specific HLA-C alleles. J Immunol 2002; 169:2818-22. (Pubitemid 35013118)
44. Bao XJ, Hou LH, Sun AN, et al. The. impact of KIR2DS4 alleles and the expression of KIR in the development of acute GVHD after unrelated allogeneic hematopoietic SCT. BoneMarrow Transplant 2010; 45:1435-41.
45. Norman PJ, Stephens HA, Verity DH, Chandanayingyong D, Vaughan RW. Distribution of natural killer cell immunoglobulin-like receptor sequences in three ethnic groups. Immunogenetics 2001; 52:195-205. (Pubitemid 32142806)
46. Estefania E, Gómez-Lozano N, Portero F, et al. Influence of KIR gene diversity on the course of HSV-1 infection: Resistance to the disease is associated with the absence of KIR2DL2 and KIR2DS2. Tissue Antigens 2007; 70:34-41. (Pubitemid 46890276)
47. Long BR, Erickson AE, Chapman JM, et al. Increased. number and function of natural killer cells in human immunodeficiency virus 1-positive subjects co-infected with herpes simplex virus 2. Immunology 2010; 129:186-96.
48. Fan QR, Wiley DC. Structure of human histocompatibility leukocyte antigen (HLA)-Cw4, a ligand for the KIR2D natural killer cell inhibitory receptor. J Exp Med 1999; 190:113-23. (Pubitemid 29330128)
49. Wagtmann N, Biassoni R, Cantoni C, et al. Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity 1995; 2:439-49.
50. Hsu KC, Liu XR, Selvakumar A, Mickelson E, O'Reilly RJ, Dupont B. Killer Ig-like receptor haplotype analysis by gene content: Evidence for genomic diversity with a minimum of 6 basic framework haplotypes, each with multiple subsets. J Immunol 2002; 169:5118-29. (Pubitemid 35217181)