Clear and independent associations of several HLA-DRB1 alleles with diVerential antibody responses to hepatitis B vaccination in youth

Human Genetics

Volumn 126, Issue 5, 2009, Pages 685-696

  Li, Yufeng ^a   Ni, Rong ^a   Song, Wei ^b   Shao, Wenshuo ^b   Shrestha, Sadeep ^b   Ahmad, Sushma ^c   Cunningham, Coleen K ^d   Flynn, Patricia M ^e   Kapogiannis, Bill G ^f   Wilson, Craig M ^b   Tang, Jianming ^g  

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

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c WESTAT   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^g University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATITIS B ANTIBODY; HEPATITIS B VACCINE; HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DR ANTIGEN; HLA D ANTIGEN; HLA-DRB1 ANTIGEN;

ADOLESCENT; ADULT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CHILD; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENETIC ASSOCIATION; HEPATITIS B; HISPANIC; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RACE DIFFERENCE; SCHOOL CHILD; VACCINATION; ANALYSIS OF VARIANCE; ANTIBODY PRODUCTION; BRAZIL; CAUCASIAN; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; IMMUNOLOGY; MULTIVARIATE ANALYSIS; NEGRO; SERODIAGNOSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SOUTH AFRICA; UNITED STATES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADOLESCENT; AFRICAN CONTINENTAL ANCESTRY GROUP; ANALYSIS OF VARIANCE; ANTIBODY FORMATION; BRAZIL; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC VARIATION; HAPLOTYPES; HEPATITIS B VACCINES; HISPANIC AMERICANS; HIV SERONEGATIVITY; HLA-D ANTIGENS; HLA-DR ANTIGENS; HUMANS; MALE; MULTIVARIATE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; SOUTH AFRICA; UNITED STATES; YOUNG ADULT;

EID: 73949120502     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-009-0720-z     Document Type: Article

References (64)

1. Agrawal S, Khan F, Bharadwaj U (2007) Human genetic variation studies and HLA class II loci. Int J Immunogenet 34:247-252
2. Bashirova AA, Martin MP, McVicar DW, Carrington M (2006) The killer immunoglobulin-like receptor gene cluster: tuning the genome for defense. Annu Rev Genomics Hum Genet 7:277-300
3. Belloni C, Orsolini P, Martinetti M, Chirico G, Cerbo RM, Comolli G, Maccarini U, Barlassina C, Togni C, Polatti F et al (1993) Control of hepatitis B: evaluation of two different vaccinal schedules in new-borns from HBsAg negative mothers. New Microbiol 16:237-244
4. Bergstrom TF, Erlandsson R, Engkvist H, Josefsson A, Erlich HA, Gyllensten U (1999) Phylogenetic history of hominoid DRB loci and alleles inferred from intron sequences. Immunol Rev 167:351-365
5. Caillat-Zucman S, Gimenez JJ, Albouze G, Lebkiri B, Naret C, Jungers P, Bach JF (1993) HLA genetic heterogeneity of hepatitis B vaccine response in hemodialyzed patients. Kidney Int Suppl 41:S157-S160
6. Caillat-Zucman S, Gimenez JJ, Wambergue F, Albouze G, Lebkiri B, Naret C, Moynot A, Jungers P, Bach JF (1998) Distinct HLA class II alleles determine antibody response to vaccination with hepatitis B surface antigen. Kidney Int 53:1626-1630
7. Catano G, Kulkarni H, He W, Marconi VC, Agan BK, Landrum M, Anderson S, Delmar J, Telles V, Song L, Castiblanco J, Clark RA, Dolan MJ, Ahuja SK (2008) HIV-1 disease-influencing effects associated with ZNRD1, HCP5 and HLA-C alleles are attributable mainly to either HLA-A10 or HLA-B*57 alleles. PLoS ONE 3:e3636
8. Collier AC, Corey L, Murphy VL, Handsfield HH (1988) Antibody to human immunodeficiency virus (HIV) and suboptimal response to hepatitis B vaccination. Ann Intern Med 109:101-105
9. Cooper CL, Angel JB, Seguin I, Davis HL, Cameron DW (2008) CPG 7909 adjuvant plus hepatitis B virus vaccination in HIV-infected adults achieves long-term seroprotection for up to 5 years. Clin Infect Dis 46:1310-1314
10. Cornejo-Juarez P, Volkow-Fernandez P, Escobedo-Lopez K, Vilar-Compte D, Ruiz-Palacios G, Soto-Ramirez LE (2006) Randomized controlled trial of hepatitis B virus vaccine in HIV-1-in-fected patients comparing two different doses. AIDS Res Ther 3:9
11. Craven DE, Awdeh ZL, Kunches LM, Yunis EJ, Dienstag JL, Werner BG, Polk BF, Syndman DR, Platt R, Crumpacker CS et al (1986) Nonresponsiveness to hepatitis B vaccine in health care workers. Results of revaccination and genetic typings. Ann Intern Med 105:356-360
12. Cruciani M, Mengoli C, Serpelloni G, Lanza A, Gomma M, Nardi S, Rimondo C, Bricolo F, Consolaro S, Trevisan M, Bosco O (2009) Serologic response to hepatitis B vaccine with high dose and increasing number of injections in HIV infected adult patients. Vaccine 27:17-22
13. Custer B, Sullivan SD, Hazlet TK, Iloeje U, Veenstra DL, Kowdley KV (2004) Global epidemiology of hepatitis B virus. J Clin Gas-troenterol 38:S158-S168
14. Dalmasso C, Carpentier W, Meyer L, Rouzioux C, Goujard C, Chaix ML, Lambotte O, Avettand-Fenoel V, Le Clerc S, de Senneville LD, Deveau C, Boufassa F, Debre P, Delfraissy JF, Broet P, Theodorou I (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
15. de Bakker PI, McVean G, Sabeti PC, Miretti MM, Green T, Marchini J, Ke X, Monsuur AJ, Whittaker P, Delgado M, Morrison J, Richardson A, Walsh EC, Gao X, Galver L, Hart J, Hafler DA, Pericak-Vance M, Todd JA, Daly MJ, Trowsdale J, Wijmenga C, Vyse TJ, Beck S, Murray SS, Carrington M, Gregory S, Deloukas P, Rioux JD (2006) A high-resolution HLA and SNP haplotype map for disease association studies in the extended human MHC. Nat Genet 38:1166-1172
16. de Vries-Sluijs TE, Hansen BE, van Doornum GJ, Springeling T, Evertsz NM, de Man RA, van der Ende ME (2008) A prospective open study of the efficacy of high-dose recombinant hepatitis B rechallenge vaccination in HIV-infected patients. J Infect Dis 197:292-294
17. del Canho R, de Vries RR, Schalm SW (1993) Human leucocyte antigens (HLA) in neonates with an inadequate response to hepatitis B vaccination. Vaccine 11:983
18. Dienstag JL (2008) hepatitis B virus infection. N Engl J Med 359:1486-1500
19. Donaldson PT, Baragiotta A, Heneghan MA, Floreani A, Venturi C, Underhill JA, Jones DE, James OF, Bassendine MF (2006) HLA class II alleles, enotypes, haplotypes, and amino acids in primary biliary cirrhosis: a large-scale study. Hepatology 44:667-674
20. Dorak MT, Shao W, Machulla HK, Lobashevsky ES, Tang J, Park MH, Kaslow RA (2006) Conserved extended haplotypes of the major histocompatibility complex: further characterization. Genes Immun 7:450-467
21. Fattovich G, Bortolotti F, Donato F (2008) Natural history of chronic hepatitis B: special emphasis on disease progression and prognostic factors. J Hepatol 48:335-352
22. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, Zhang K, Gumbs C, Castagna A, Cossarizza A, Cozzi-Lepri A, De Luca A, Easterbrook P, Francioli P, Mallal S, Martinez-Picado J, Miro JM, Obel N, Smith JP, Wyniger J, Descombes P, Anton-arakis SE, Letvin NL, McMichael AJ, Haynes BF, Telenti A, Goldstein DB (2007) A whole-genome association study of major determinants for host control of HIV-1. Science 317:944-947
23. Fonseca MO, Pang LW, de Paula Cavalheiro N, Barone AA, Heloisa Lopes M (2005) Randomized trial of recombinant hepatitis B vaccine in HIV-infected adult patients comparing a standard dose to a double dose. Vaccine 23:2902-2908
24. Hafler DA, Compston A, Sawcer S, Lander ES, Daly MJ, De Jager PL, de Bakker PI, Gabriel SB, Mirel DB, Ivinson AJ, Pericak-Vance MA, Gregory SG, Rioux JD, McCauley JL, Haines JL, Barcellos LF, Cree B, Oksenberg JR, Hauser SL (2007) Risk alleles for multiple sclerosis identified by a genomewide study. N Engl J Med 357:851-862
25. Hatae K, Kimura A, Okubo R, Watanabe H, Erlich HA, Ueda K, Nishimura Y, Sasazuki T (1992) Genetic control of nonrespon-siveness to hepatitis B virus vaccine by an extended HLA haplotype. Eur J Immunol 22:1899-1905
26. Hohjoh H, Ohashi J, Takasu M, Nishioka T, Ishida T, Tokunaga K (2003) Recent divergence of the HLA-DRB1*04 allelic lineage from the DRB1*0701 lineage after the separation of the human and chimpanzee species. Immunogenetics 54:856-861
27. Hohler T, Meyer CU, Notghi A, Stradmann-Bellinghausen B, Schneider PM, Starke R, Zepp F, Sanger R, Clemens R, Meyer zum Buschen-felde KH, Rittner C (1998) The influence of major histocompatibility complex class II genes and T-cell Vβ repertoire on response to immunization with HBsAg. Hum Immunol 59:212-218
28. Hohler T, Reuss E, Evers N, Dietrich E, Rittner C, Freitag CM, Vollmar J, Schneider PM, Fimmers R (2002a) Differential genetic determination of immune responsiveness to hepatitis B surface antigen and to hepatitis A virus: a vaccination study in twins. Lancet 360:991-995
29. Hohler T, Stradmann-Beilinghausen B, Starke R, Sanger R, Victor A, Rittner C, Schneider PM (2002b) C4A deficiency and nonre-sponse to hepatitis B vaccination. J Hepatol 37:387-392
30. Jones EY, Fugger L, Strominger JL, Siebold C (2006) MHC class II proteins and disease: a structural perspective. Nat Rev Immunol 6:271-282
31. Kramer A, Herth D, von Keyserlingk HJ, Ludwig WD, Hampl H, Sommer D, Hahn EG, Riecken EO (1988) Non-responsiveness to hepatitis-B vaccination: revaccination and immunogenetic typing. Klin Wochenschr 66:670-674
32. Kuniholm MH (2007) Replicating genome-wide association studies. Science 318:390-391, author reply 390-391
33. Lai CL, Yuen MF (2008) Chronic hepatitis B - new goals, new treatment. N Engl J Med 359:2488-2491
34. Limou S, Le Clerc S, Coulonges C, Carpentier W, Dina C, Delaneau O, Labib T, Taing L, Sladek R, Deveau C, Ratsimandresy R, Montes M, Spadoni JL, Lelievre JD, Levy Y, Therwath A, Schachter F, Matsuda F, Gut I, Froguel P, Delfraissy JF, Hercberg S, Zagury JF (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
35. Listgarten J, Brumme Z, Kadie C, Xiaojiang G, Walker B, Carrington M, Goulder P, Heckerman D (2008) Statistical resolution of ambiguous HLA typing data. PLoS Comput Biol 4:el000016
36. Martinetti M, Cuccia M, Daielli C, Ambroselli F, Gatti C, Pizzochero C, Belloni C, Orsolini P, Salvaneschi L (1995) Anti-HBV neonatal immunization with recombinant vaccine. Part II. Molecular basis of the impaired alloreactivity. Vaccine 13:555-560
37. Martinetti M, De Silvestri A, Belloni C, Pasi A, Tinelli C, Pistorio A, Salvaneschi L, Rondini G, Avanzini MA, Cuccia M (2000) Humoral response to recombinant hepatitis B virus vaccine at birth: role of HLA and beyond. Clin Immunol 97:234-240
38. McDermott AB, Zuckerman JN, Sabin CA, Marsh SG, Madrigal JA (1997) Contribution of human leukocyte antigens to the antibody response to hepatitis B vaccination. Tissue Antigens 50:8-14
39. McGovern BH (2007) The epidemiology, natural history and prevention of hepatitis B: implications of HIV coinfection. Antivir Ther 12(Suppl 3):H3-H13
40. Miretti MM, Walsh EC, Ke X, Delgado M, Griffiths M, Hunt S, Morrison J, Whittaker P, Lander ES, Cardon LR, Bentley DR, Rioux JD, Beck S, Deloukas P (2005) A high-resolution linkage-disequilibrium map of the human major histocompatibility complex and first generation of tag single-nucleotide polymorphisms. Am J Hum Genet 76:634-646
41. O'Brien SJ, Nelson GW (2004) Human genes that limit AIDS. Nat Genet 36:565-574
42. Ovsyannikova IG, Jacobson RM, Vierkant RA, Shane Pankratz V, Jacobsen SJ, Poland GA (2004) Associations between human leukocyte antigen (HLA) alleles and very high levels of measles antibody following vaccination. Vaccine 22:1914-1920
43. Ovsyannikova IG, Pankratz VS, Vierkant RA, Jacobson RM, Poland GA (2006) Human leukocyte antigen haplotypes in the genetic control of immune response to measles-mumps-rubella vaccine. J Infect Dis 193:655-663
44. Parham P (2005) Influence of KIR diversity on human immunity. Adv Exp Med Biol 560:47-50
45. Pasricha N, Datta U, Chawla Y, Singh S, Arora SK, Sud A, Minz RW, Saikia B, Singh H, James I, Sehgal S (2006) Immune responses in patients with HIV infection after vaccination with recombinant hepatitis B virus vaccine. BMC Infect Dis 6:65
46. Peces R, de la Torre M, Alcazar R, Urra JM (1997) Prospective analysis of the factors influencing the antibody response to hepatitis B vaccine in hemodialysis patients. Am J Kidney Dis 29:239-245
47. Qian Y, Zhang L, Liang XM, Hou JL, Luo KX (2002) Association of immune response to hepatitis B vaccine with HLA-DRB1*02, 07, 09 genes in the population of Han nationality in Guangdong Province. Di Yi Jun Yi Da Xue Xue Bao 22:67-69
48. Rey D, Krantz V, Partisani M, Schmitt MP, Meyer P, Libbrecht E, Wendling MJ, Vetter D, Nicolle M, Kempf-Durepaire G, Lang JM (2000) Increasing the number of hepatitis B vaccine injections augments anti-HBs response rate in HIV-infected patients. Effects on HIV-1 viral load. Vaccine 18:1161-1165
49. Robinson J, Waller MJ, Fail SC, Marsh SG (2006) The IMGT/HLA and IPD databases. Hum Mutat 27:1192-1199
50. Sasaki MG, Foccacia R, de Messias-Reason IJ (2003) Efficacy of granulocyte-macrophage colony-stimulating factor (GM-CSF) as a vaccine adjuvant for hepatitis B virus in patients with HIV infection. Vaccine 21:4545-4549
51. Schreuder GM, Hurley CK, Marsh SG, Lau M, Fernandez-Vina MA, Noreen HJ, Setterholm M, Maiers M (2005) HLA dictionary 2004: summary of HLA-A, -B, -C, -DRB1/3/4/5, -DQB1 alleles and their association with serologically defined HLA-A, -B, -C, -DR, and -DQ antigens. Hum Immunol 66:170-210
52. Shao W, Tang J, Dorak MT, Song W, Lobashevsky E, Cobbs CS, Wrensch MR, Kaslow RA (2004) Molecular typing of human leukocyte antigen and related polymorphisms following whole genome amplification. Tissue Antigens 64:286-292
53. Shrestha S, Aissani B, Song W, Wilson CM, Kaslow RA, Tang J (2009) Host genetics and HIV-1 viral set-point in African Americans. AIDS 23:673-677
54. Stachowski J, Kramer J, Fust G, Maciejewski J, Baldamus CA, Petranyi GG (1995) Relationship between the reactivity to hepatitis B virus vaccination and the frequency of MHC class I, II and III alleles in haemodialysis patients. Scand J Immunol 42:60-65
55. Tang J, Kaslow RA (2003) The impact of host genetics on HIV infection and disease progression in the era of highly active antiretro-viral therapy. AIDS 17:S51-S60
56. Tang J, Penman-Aguilar A, Lobashevsky E, Allen S, Kaslow R, Zambia-UAB HIV Research Project (2004) HLA-DRB1 and -DQB1 alleles and haplotypes in Zambian couples and their associations with heterosexual transmission of human immunodeficiency virus type 1. J Infect Dis 189:1696-1704
57. Tang J, Shao W, Yoo YJ, Brill I, Mulenga J, Allen S, Hunter E, Kaslow RA (2008) Human leukocyte antigen class I genotypes in relation to heterosexual HIV type 1 transmission within discordant couples. J Immunol 181:2626-2635
58. Thio CL, Thomas DL, Karacki P, Gao X, Marti D, Kaslow RA, Goedert JJ, Hilgartner M, Strathdee SA, Duggal P, O'Brien SJ, Astemborski J, Carrington M (2003) Comprehensive analysis of class I and class II HLA antigens and chronic hepatitis B virus infection. J Virol 77:12083-12087
59. van Manen D, Kootstra NA, Boeser-Nunnink B, Handulle MAM, van't Wout AB, Schuitemaker H (2009) Association of HLA-C and HCP5 gene regions with the clinical course of HIV-1 infection. AIDS 23:19-28
60. Wang C, Tang J, Song W, Lobashevsky E, Wilson CM, Kaslow RA (2004) Human leukocyte antigen and cytokine gene polymorphisms are independently associated with responses to hepatitis B vaccination. Hepatology 39:978-988
61. Watanabe H, Matsushita S, Kamikawaji N, Hirayama K, Okumura M, Sasazuki T (1988) Immune suppression gene on HLA-Bw54-DR4-DRw53 haplotype controls nonresponsiveness in humans to hepatitis B surface antigen via CD8+ suppressor T-cells. Hum Immunol 22:9-17
62. Weissman JY, Tsuchiyose MM, Tong MJ, Co R, Chin K, Ettenger RB (1988) Lack of response to recombinant hepatitis B vaccine in nonresponders to the plasma vaccine. JAMA 260:1734-1738
63. Wilson CM, Ellenberg JH, Sawyer MK, Belzer M, Crowley-Nowick PA, Puga A, Futterman DC, Peralta L (2001) Serologic response to hepatitis B vaccine in HIV infected and high-risk HIV uninfected adolescents in the REACH cohort. Reaching for Excellence in Adolescent Care and Health. J Adolesc Health 29:123-129
64. Zuin G, Principi N, Tornaghi R, Paccagnini S, Re M, Massironi E, Ragni MC (1992) Impaired response to hepatitis B vaccine in HIV infected children. Vaccine 10:857-860