Heterogeneity in vaccine immune response: The role of immunogenetics and the emerging field of vaccinomics

Clinical Pharmacology and Therapeutics

Volumn 82, Issue 6, 2007, Pages 653-664

  Poland, G A ^a,b   Ovsyannikova, I G ^a,b   Jacobson, R M ^a,b   Smith, D I ^b  

^a Mayo Clinic   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CYTOKINE; HEPATITIS A VACCINE; HEPATITIS B VACCINE; HLA ANTIGEN; RUBELLA VACCINE;

CELLULAR IMMUNITY; COMPARATIVE GENOMIC HYBRIDIZATION; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; GENOMICS; HAPLOTYPE; HETEROZYGOSITY; HIGH THROUGHPUT SCREENING; HLA SYSTEM; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENETICS; MICROARRAY ANALYSIS; PHARMACOGENETICS; PRIORITY JOURNAL; RECEPTOR GENE; REVIEW;

ANIMALS; ANTIBODY FORMATION; BIOMETRY; COMPUTATIONAL BIOLOGY; CYTOKINES; EPIGENESIS, GENETIC; GENOMICS; HAPLOTYPES; HETEROZYGOTE; HLA ANTIGENS; HUMANS; IMMUNOGENETICS; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHARMACOGENETICS; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CELL SURFACE; SEQUENCE ANALYSIS, DNA; TWIN STUDIES AS TOPIC; VACCINES; VIRAL VACCINES;

EID: 36148964050     PISSN: 00099236     EISSN: 15326535     Source Type: Journal    
DOI: 10.1038/sj.clpt.6100415     Document Type: Review

References (87)

1. Weinshilboum, R. Inheritance and drug response. N. Engl. J. Med. 348, 529-537 (2003).
2. Dean, M., Carrington, M. & O'Brien, S.J. Balanced polymorphism selected by genetic versus infectious human disease. Annu. Rev. Genomics Hum. Genet. 3, 263-292 (2002).
3. Hill, A.V. The genomics and genetics of human infectious disease susceptibility. Annu. Rev. Genomics Hum. Genet. 2, 373-400 (2001).
4. Poland, G.A. & Jacobson, R.M. The genetic basis for variation in antibody response to vaccines. Curr. Opin. Pediatr. 10, 208-215 (1998).
5. Poland, G.A. Variability in immune response to pathogens: using measles vaccine to probe immunogenetic determinants of response. Am. J. Hum. Genet. 62, 215-220 (1998).
6. Poland, G.A., Ovsyannikova, I.G. & Jacobson, R.M. Genetic influences on the immune response to vaccines. In Genetic Susceptibility to Infectious Diseases (ed. Kaslow R.A.) (Oxford Univ. Press, Oxford, 2006) pp 414-429.
7. Tan, P.-L., Jacobson, R.M., Poland, G.A., Jacobsen, S.J. & Pankratz, S.V. Twin studies of immunogenicity - determining the genetic contribution to vaccine failure. Vaccine 19, 2434-2439 (2001).
8. Jacobson, R.M., Ovsyannikova, I.G., Targonski, P.V. & Poland, G.A. Studies of twins in vaccinology. Vaccine 25, 3160-3164 (2007).
9. Hohler, T. et al. 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 (2002).
10. Newport, M.J. et al. Genetic regulation of immune responses to vaccines in early life. Genes Immun. 5, 122-129 (2004).
11. Newport, M.J., Goetghebuer, T. & Marchant, A. Hunting for immune response regulatory genes: vaccination studies in infant twins. Expert Rev. Vaccines 4, 739-746 (2005).
12. Hohler, T., Reuss, E., Freitag, C.M. & Schneider, P.M. A functional polymorphism in the IL-10 promoter influences the response after vaccination with HBsAg and hepatitis A. Hepatology 42, 72-76 (2005).
13. Sinha, P., Snyder, J.A., Kim, E.Y. & Moudgil, K.D. The major histocompatibility complex haplotypes dictate and the background genes fine-tune the dominant versus the cryptic response profile of a T-cell determinant within a native antigen: relevance to disease susceptibility and vaccination. Scand. J. Immunol. 65, 158-165 (2007).
14. Haldane, J.B.S. Disease and evolution. Supplem. La Ricerca Scientifica. 19, 68-76 (1949).
15. Poland, G.A., Jacobson, R.M., Schaid, D.J., Moore, S.B. & Jacobsen, S.J. The association between HLA class I alleles and measles vaccine-induced antibody response: evidence of a significant association. Vaccine 16, 1869-1871 (1998).
16. Ovsyannikova, I.G., Jacobson, R.M. & Poland, G.A. Variation in vaccine response in normal populations. Pharmacogenomics 5, 417-427 (2004).
17. Ovsyannikova, I.G., Dhiman, N., Jacobson, R.M. & Poland, G.A. Human leukocyte antigen polymorphisms: variable humoral immune responses to viral vaccines. Expert Rev. Vaccines 5, 33-43 (2006).
18. Jacobson, R.M. et al. The association of class I HLA alleles and antibody levels following a single dose of measles vaccine. Hum. Immunol. 64, 103-109 (2003).
19. Poland, G.A. et al. Identification of an association between HLA class II alleles and low antibody levels after measles immunization. Vaccine 20, 430-438 (2001).
20. Ovsyannikova, I.G. et al. Associations between human leukocyte antigen (HLA) alleles and very high levels of measles antibody following vaccination. Vaccine 22, 1914-1920 (2004).
21. Ovsyannikova, I.G. et al. The contribution of HLA class I antigens in immune status following two doses of rubella vaccination. Hum. Immunol. 65, 1506-1515 (2004).
22. Ovsyannikova, I.G. et al. Human leukocyte antigen class II alleles and rubella-specific humoral and cell-mediated immunity following measles-mumps-rubella-II vaccination. J. Infect. Dis. 191, 515-519 (2005).
23. Ovsyannikova, I.G. et al. Relationship between HLA polymorphisms and gamma interferon and INterleukin-10 cytokine production in healthy individuals after rubella vaccination. Clin. Vaccine Immunol. 14, 115-122 (2007).
24. Gelder, C.M. et al. Associations between human leukocyte antigens and nonresponsiveness to influenza vaccine. J. Infect. Dis. 185, 114-117 (2002).
25. Lambkin, R., Novelli, P., Oxford, J. & Gelder, C. Human genetics and responses to influenza vaccination: clinical implications. Am. J. Pharmacogenomics 4, 293-298 (2004).
26. Alper, C.A. et al. Genetic prediction of nonresponse to hepatitis B vaccine. N. Engl. J. Med. 321, 708-712 (1989).
27. Desombere, I., Willems, A. & Leroux-Roels, G. Response to hepatitis B vaccine: multiple HLA genes are involved. Tissue Antigens 51, 593-604 (1998).
28. Wang, C. et al. HLA and cytokine gene polymorphisms are independently associated with responses to hepatitis B vaccination. Hepatology 39, 978-988 (2004).
29. Ovsyannikova, I.G., Pankratz, S.V., Vierkant, R., Jacobson, R.M. & Poland, G.A. Human leukocyte antigen haplotypes in the genetic control of immune response to measles-mumps-rubella vaccine. J. Infect. Dis. 193, 655-663 (2006).
30. Sette, A. & Fikes, J. Epitope-based vaccines: an update on epitope identification, vaccine design and delivery. Curr. Opin. Immunol. 15, 461-470 (2003).
31. Sette, A. & Sidney, J. HLA supertypes and supermotifs: a functional perspective on HLA polymorphism. Curr. Opin. Immunol. 10, 478-482 (1998).
32. Sette, A. et al. Class I molecules with similar peptide-binding specificities are the result of both common ancestry and convergent evolution. Immunogenetics 54, 830-841 (2003).
33. Ovsyannikova, I.G., Jacobson, R.M., Vierkant, R.A., Pankratz, V.S. & Poland, G.A. HLA supertypes and immune responses to measles-mumps-rubella viral vaccine: findings and implications for vaccine design. Vaccine 25, 3090-3100 (2007).
34. St Sauver, J.L. et al. Associations between human leukocyte antigen homozygosity and antibody levels to measles vaccine. J. Infect. Dis. 185, 1545-1549 (2002).
35. St Sauver, J.L. et al. Extinction of the human leukocyte antigen homozygosity effect after two doses of the measles-mumps-rubella vaccine. Hum. Immunol. 66, 788-798 (2005).
36. Ovsyannikova, I.G. et al. HLA homozygosity does not adversely effect measles vaccine-induced cytokine responses. Virology 364, 87-94 (2007).
37. Kaslow, R.A. et al. Polymorphisms in HLA class I genes associated with both favorable prognosis of human immunodeficiency virus (HIV) type 1 infection and positive cytotoxic T-lymphocyte responses to ALVAC-HIV recombinant canarypox vaccines. J. Virol. 75, 8681-8689 (2001).
38. Ovsyannikova, I.G. et al. Immunologic significance of HLA class I genes in measles virus-specific IFN-gamma and IL-4 cytokine immune responses. Immunogenetics 57, 828-836 (2005).
39. Ovsyannikova, I.G. et al. HLA class II alleles and measles virus-specific cytokine immune response following two doses of measles vaccine. Immunogenetics 56, 798-807 (2005).
40. Ovsyannikova, I.G. et al. Human leukocyte antigen and interleukin 2, 10 and 12p40 cytokine responses to measles: is there evidence of the HLA effect? Cytokine 36, 173-179 (2006).
41. Dhiman, N. et al. Associations between measles vaccine immunity and single nucleotide polymorphisms in cytokine and cytokine receptor genes. J. Infect. Dis. 195, 21-29 (2007).
42. Yilmaz, V., Yentur, S.P. & Saruhan-Direskeneli, G. IL-12 and IL-10 polymorphisms and their effects on cytokine production. Cytokine 30, 188-194 (2005).
43. Stanley, S.L. Jr. et al. The immunogenetics of smallpox vaccination. J. Infect. Dis. 196, 212-219 (2007).
44. Dhiman, N. et al. Variations in measles vaccine-specific humoral immunity by polymorphisms in SLAM and CD46 measles virus receptors. J. Allergy Clin. Immunol. 120, 666-672 (2007).
45. Dhiman, N., Jacobson, R.M. & Poland, G.A. Measles virus receptors: SLAM and CD46. Rev. Med. Virol. 14, 217-229 (2004).
46. Rassa, J.C. & Ross, S.R. Viruses and Toll-like receptors. Microbes Infect. 5, 961-968 (2003).
47. Bowie, A.G. & Haga, I.R. The role of Toll-like receptors in the host response to viruses. Mol. Immunol. 42, 859-867 (2005).
48. Bieback, K. et al. Hemagglutinin protein of wild-type measles virus activates Toll-like receptor 2 signaling. J. Virol. 76, 8729-8736 (2002).
49. Bowie, A.G. Translational mini-review series on Toll-like receptors: recent advances in understanding the role of Toll-like receptors in anti-viral immunity. Clin. Exp. Immunol. 147, 217-226 (2007).
50. Bowie, A. et al. A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 97, 10162-10167 (2000).
51. Harte, M.T. et al. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J. Exp. Med. 197, 343-351 (2003).
52. Murabayashi, N. et al. Susceptibility of human dendritic cells (DCs) to measles virus (MV) depends on their activation stages in conjunction with the level of CDw150: role of Toll stimulators in DC maturation and MV amplification. Microbes Infect. 4, 785-794 (2002).
53. Tanabe, M. et al. Mechanism of up-regulation of human Toll-like receptor 3 secondary to infection of measles virus-attenuated strains. Biochem. Biophys. Res. Commun. 311, 39-48 (2003).
54. Hahm, B., Cho, J.H. & Oldstone, M.B. Measles virus-dendritic cell interaction via SLAM inhibits innate immunity: selective signaling through TLR4 but not other TLRs mediates suppression of IL-12 synthesis. Virology 358, 251-257 (2006).
55. Schlender, J. et al. Inhibition of Toll-like receptor 7- and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79, 5507-5515 (2005).
56. ten Oever, B.R., Servant, M.J., Grandvaux, N., Lin, R. & Hiscott, J. Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J. Virol. 76, 3659-3669 (2002).
57. Manger, I.D. & Relman, D.A. How the host "sees" pathogens: global gene expression responses to infection. Curr. Opin. Immunol. 12, 215-218 (2000).
58. Jin, P. & Wang, E. Polymorphism in clinical immunology - from HLA typing to immunogenetic profiling. J. Transl. Med. 1, 8 (2003).
59. Keen, L.J. The extent and analysis of cytokine and cytokine receptor gene polymorphism. Transpl. Immunol. 10, 143-146 (2002).
60. Agrawal, A.A. Phenotypic plasticity in the interactions and evolution of species. Science 294, 321-326 (2001).
61. Taylor, P.D. et al. The evolutionary consequences of plasticity in host-pathogen interactions. Theor. Popul. Biol. 69, 323-331 (2006).
62. Giacomini, K.M. et al. The pharmacogenetics research network: from SNP discovery to clinical drug response. Clin. Pharmacol. Ther. 81, 328-345 (2007).
63. Sellick, G.S. et al. Genomewide linkage searches for Mendelian disease loci can be efficiently conducted using high-density SNP genotyping arrays. Nucleic Acids Res. 32, e164 (2004).
64. Shelling, A.N. & Ferguson, L.R. Genetic variation in human disease and a new role for copy number variants. Mutat. Res. 622, 33-41 (2007).
65. Cheng, J. et al. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308, 1149-1154 (2005).
66. Birney, E. et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799-816 (2007).
67. Pinkel, D. et al. High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat. Genet. 20, 207-211 (1998).
68. Pinkel, D. & Albertson, D.G. Comparative genomic hybridization. Annu. Rev. Genomics Hum. Genet. 6, 331-354 (2005).
69. Venter, J.C. et al. The sequence of the human genome. Science 291, 1304-1351 (2001).
70. Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
71. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380 (2005).
72. Halassy, B. et al. Immunogenicity of peptides of measles virus origin and influence of adjuvants. Vaccine 24, 185-194 (2006).
73. Sleijffers, A. et al. Cytokine polymorphisms play a role in susceptibility to ultraviolet B-induced modulation of immune responses after hepatitis B vaccination. J. Immunol. 170, 3423-3428 (2003).
74. Yucesoy, B. et al. IL-1beta gene polymorphisms influence hepatitis B vaccination. Vaccine 20, 3193-3196 (2002).
75. Ovsyannikova, I.G., Johnson, K.L., Muddiman, D.C., Vierkant, R.A. & Poland, G.A. Identification and characterization of novel, naturally processed measles virus class II HLA-DRB1 peptides. J. Virol. 78, 42-51 (2004).
76. Putz, M.M., Ammerlaan, W., Schneider, F., Jung, G. & Muller, C.P. Humoral immune responses to a protective peptide-conjugate against measles after different prime-boost regimens. Vaccine 22, 4173-4182 (2004).
77. Spielberg, S.P. Therapeutics and toxicology. Curr. Opin. Pediatr. 10, 201-202 (1998).
78. Vandenbroeck, K. & Goris, A. Cytokine gene polymorphisms in multifactorial diseases: gateways to novel targets for immunotherapy? Trends Pharmacol. Sci. 24, 284-289 (2003).
79. Kim, M.-J. et al. Revaccination of healthy nonresponders with hepatitis B vaccine and prediction of seroprotection response. Vaccine 21, 1174-1179 (2003).
80. Lee, H.G. et al. Peptide-specific CTL induction in HBV-seropositive PBMC by stimulation with peptides in vitro: novel epitopes identified from chronic carriers. Virus Res. 50, 185-194 (1997).
81. Poland, G.A., Ovsyannikova, I.G., Johnson, K.L. & Naylor, S. The role of mass spectrometry in vaccine development. Vaccine 19, 2692-2700 (2001).
82. Johnson, K.L., Ovsyannikova, I.G., Poland, G. & Muddiman, D.C. Identification of class II HLA-DRB1*03-bound measles virus peptides by 2D-liquid chromatography tandem mass spectrometry. J. Proteome Res. 4, 2243-2249 (2005).
83. Ovsyannikova, I.G., Poland, G.A., Easler, N.J. & Vierkant, R.A. Influence of HLA-DRB1 alleles on lymphoproliferative responses to a naturally processed and presented measles virus phosphoprotein in measles immunized individuals. Hum. Immunol. 65, 209-217 (2004).
84. Ovsyannikova, I.G., Vierkant, R.A. & Poland, G.A. Importance of HLA-DQ and HLA-DP polymorphisms in cytokine response to naturally processed HLA-DR-derived measles virus peptides. Vaccine 24, 5381-5389 (2006).
85. Ovsyannikova, I.G., Johnson, K.L., Naylor, S. & Poland, G.A. Identification of HLA-DRB1-bound self-peptides following measles virus infection. J. Immunol. Methods 297, 153-167 (2005).
86. Ota, M.O. et al. Hemagglutinin protein is a primary target of the measles virus-specific HLA-A2-restricted CD8+ T cell response during measles and after vaccination. J. Infect. Dis. 195, 1799-1807 (2007).
87. Perera, L.P. et al. Development of smallpox vaccine candidates with integrated IL-15 that demonstrate superior immunogenicity, efficacy and safety in mice. J. Virol. 18, 8774-8783 (2007).