HLA-B27-mediated protection in HIV and hepatitis C virus infection and pathogenesis in spondyloarthritis: Two sides of the same coin?

Current Opinion in Rheumatology

Volumn 25, Issue 4, 2013, Pages 426-433

  Neumann Haefelin, Christoph ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

CD8p T cell; hepatitis C virus; HIV; HLA B*27; HLA B27; immunodominance; viral escape

Indexed keywords

AMINOPEPTIDASE; ENDOPLASMATIC RETICULUM AMINOPEPTIDASE 1; EPITOPE; HLA A3 ANTIGEN; HLA B27 ANTIGEN; HLA B51 ANTIGEN; HLA B57 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; TRYPTOPHAN; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; CD8+ T LYMPHOCYTE; DISEASE ASSOCIATION; GENOTYPE; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION RISK; JAUNDICE; LYMPHOCYTE FUNCTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; REGULATORY T LYMPHOCYTE; REVIEW; SPONDYLARTHRITIS; VIRUS LOAD;

CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; HEPATITIS C; HIV INFECTIONS; HIV LONG-TERM SURVIVORS; HLA-B27 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; SPONDYLARTHRITIS; VIRAL LOAD;

EID: 84879883126     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0b013e328362018f     Document Type: Review

References (62)

1. Gomard E, Sitbon M, Toubert A, et al. HLA-B27, a dominant restricting element in antiviral responses? Immunogenetics 1984; 20:197-204. (Pubitemid 14058353)
2. Nixon DF, Townsend AR, Elvin JG, et al. HIV-1 gag-specific cytotoxic T lymphocytes defined with recombinant vaccinia virus and synthetic peptides. Nature 1988; 336:484-487.
3. Kaslow RA, Carrington M, Apple R, et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 1996; 2:405-411. (Pubitemid 26193012)
4. Goulder PJ, Walker BD. HIV and HLA class I: an evolving relationship. Immunity 2012; 37:426-440.
5. Pereyra F, Jia X, McLaren PJ, et al. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 2010; 330:1551-1557.
6. Hraber P, Kuiken C, Yusim K. Evidence for human leukocyte antigen heterozygote advantage against hepatitis C virus infection. Hepatology 2007; 46:1713-1721.
7. McKiernan SM, Hagan R, Curry M, et al. Distinct MHC class I and II alleles are associated with hepatitis C viral clearance, originating from a single source. Hepatology 2004; 40:108-114. (Pubitemid 38877575)
8. Mustonen J, Partanen J, Kanerva M, et al. Association of HLA B27 with benign clinical course of nephropathia epidemica caused by Puumala hantavirus. Scand J Immunol 1998; 47:277-279. (Pubitemid 28153406)
9. Kim AY, Kuntzen T, Timm J, et al. Spontaneous control of HCV is associated with expression of HLA-B-57 and preservation of targeted epitopes. Gastroenterology 2011; 140:686-696.
10. Kuniholm MH, Kovacs A, Gao X, et al. Specific human leukocyte antigen class I and II alleles associated with hepatitis C virus viremia. Hepatology 2010; 51:1514-1522.
11. Thio CL, Gao X, Goedert JJ, et al. HLA-Cw-04 and hepatitis C virus persistence. J Virol 2002; 76:4792-4797.
12. Altfeld M, Kalife ET, Qi Y, et al. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(p) T cell response against HIV-1. PLoS Med 2006; 3:e403.
13. Streeck H, Jolin JS, Qi Y, et al. Human immunodeficiency virus type 1-specific CD8p T-cell responses during primary infection are major determinants of the viral set point and loss of CD4p T cells. J Virol 2009; 83:7641-7648.
14. Feeney ME, Tang Y, Roosevelt KA, et al. Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-term-nonprogressing child. J Virol 2004; 78:8927-8930. (Pubitemid 39025159)
15. Schellens IM, Kesmir C, Miedema F, et al. An unanticipated lack of consensus cytotoxic T lymphocyte epitopes in HIV-1 databases: the contribution of prediction programs. AIDS 2008; 22:33-37. (Pubitemid 350294875)
16. Neumann-Haefelin C, McKiernan S, Ward S, et al. Dominant influence of an HLA-B27 restricted CD8p T cell response in mediating HCV clearance and evolution. Hepatology 2006; 43:563-572.
17. Dazert E, Neumann-Haefelin C, Bressanelli S, et al. Loss of viral fitness and cross-recognition by CD8p T cells limit HCV escape from a protective HLA-B27-restricted human immune response. J Clin Invest 2009; 119:376-386.
18. Neumann-Haefelin C, Timm J, Schmidt J, et al. Protective effect of human leukocyte antigen B27 in hepatitis C virus infection requires the presence of a genotype-specific immunodominant CD8p T-cell epitope. Hepatology 2010; 51:54-62.
19. Ziegler S, Ruhl M, Tenckhoff H, et al. Susceptibility to chronic hepatitis C virus infection is influenced by sequence differences in immunodominant CD8p T cell epitopes. J Hepatol 2013; 58:24-30.
20. McMichael AJ. Triple bypass: complicated paths to HIV escape. J Exp Med 2007; 204:2785-2788.
21. Lichterfeld M, Kavanagh DG, Williams KL, et al. A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomonocytic cells. J Exp Med 2007; 204:2813-2824. (Pubitemid 350179552)
22. Goulder PJ, Brander C, Tang Y, et al. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 2001; 412:334-338. (Pubitemid 32694384)
23. Goulder PJ, Phillips RE, Colbert RA, et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 1997; 3:212-217. (Pubitemid 27064707)
24. Kelleher AD, Long C, Holmes EC, et al. Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J Exp Med 2001; 193:375-386.
25. Schneidewind A, Brockman MA, Sidney J, et al. Structural and functional constraints limit options for CTL escape in the immunodominant HLAB27 restricted epitope in HIV-1 capsid. J Virol 2008; 82:5594-5605. (Pubitemid 351705266)
26. Schneidewind A, Brockman MA, Yang R, et al. Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J Virol 2007; 81:12382-12393. (Pubitemid 350085852)
27. Neumann-Haefelin C, Oniangue-Ndza C, Kuntzen T, et al. Human leukocyte antigen B27 selects for rare escape mutations that significantly impair hepatitis C virus replication and require compensatory mutations. Hepatology 2011; 54:1157-1166.
28. Crawford H, Prado JG, Leslie A, et al. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLA-B-5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J Virol 2007; 81:8346-8351. (Pubitemid 47101520)
29. Martinez-Picado J, Prado JG, Fry EE, et al. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J Virol 2006; 80:3617-3623.
30. Boutwell CL, Carlson JM, Lin TH, et al. Frequent and variable cytotoxic-Tlymphocyte escape-associated fitness costs in the human immunodeficiency virus type 1 subtype B gag proteins. J Virol 2013; 87:3952-3965.
31. Oniangue-Ndza C, Kuntzen T, Kemper M, et al. Compensatory mutations restore the replication defects caused by cytotoxic T lymphocyte escape mutations in hepatitis C virus polymerase. J Virol 2011; 85:11883-11890.
32. Fitzmaurice K, Petrovic D, Ramamurthy N, et al. Molecular footprints reveal the impact of the protective HLA-A-03 allele in hepatitis C virus infection. Gut 2011; 60:1563-1571.
33. Gaudieri S, Rauch A, Park LP, et al. Evidence of viral adaptation to HLA class Irestricted immune pressure in chronic hepatitis C virus infection. J Virol 2006; 80:11094-11104. (Pubitemid 44706550)
34. Kiepiela P, Leslie AJ, Honeyborne I, et al. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 2004; 432:769-775.
35. Neumann-Haefelin C, Timm J, Spangenberg HC, et al. Virological and immunological determinants of intrahepatic virus-specific CD8p T-cell failure in chronic hepatitis C virus infection. Hepatology 2008; 47:1824-1836. (Pubitemid 351945550)
36. Ruhl M, Knuschke T, Schewior K, et al. CD8p T-cell response promotes evolution of hepatitis C virus nonstructural proteins. Gastroenterology 2011; 140:2064-2073.
37. Mudd PA, Martins MA, Ericsen AJ, et al. Vaccine-induced CD8p T cells control AIDS virus replication. Nature 2012; 491:129-133.
38. Almeida JR, Price DA, Papagno L, et al. Superior control of HIV-1 replication by CD8p T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 2007; 204:2473-2485. (Pubitemid 47529331)
39. Harari A, Cellerai C, Enders FB, et al. Skewed association of polyfunctional antigen-specific CD8 T cell populations with HLA-B genotype. Proc Natl Acad Sci U S A 2007; 104:16233-16238. (Pubitemid 350099390)
40. 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; 85:9334-9345.
41. Mothe B, Llano A, Ibarrondo J, et al. CTL responses of high functional avidity and broad variant cross-reactivity are associated with HIV control. PLoS One 2012; 7:e29717.
42. Yerly D, Heckerman D, Allen TM, et al. Increased cytotoxic T-lymphocyte epitope variant cross-recognition and functional avidity are associated with hepatitis C virus clearance. J Virol 2008; 82:3147-3153. (Pubitemid 351329204)
43. Payne RP, Kloverpris H, Sacha JB, et al. Efficacious early antiviral activity of HIV Gag- and Pol-specific HLA-B 2705-restricted CD8pT cells. J Virol 2010; 84:10543-10557.
44. Schmidt J, Iversen AK, Tenzer S, et al. Rapid antigen processing and presentation of a protective and immunodominant HLA-B-27-restricted hepatitis C virus-specific CD8p T-cell epitope. PLoS Pathog 2012; 8:e1003042.
45. Kosmrlj A, Read EL, Qi Y, et al. Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 2010; 465:350-354.
46. Chen H, Ndhlovu ZM, Liu D, et al. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat Immunol 2012; 13:691-700.
47. Hersperger AR, Pereyra F, Nason M, et al. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog 2010; 6:e1000917.
48. Feinberg MB, Ahmed R. Born this way? Understanding the immunological basis of effective HIV control. Nat Immunol 2012; 13:632-634.
49. Meyer-Olson D, Shoukry NH, Brady KW, et al. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J Exp Med 2004; 200:307-319. (Pubitemid 39031250)
50. Miles JJ, Thammanichanond D, Moneer S, et al. Antigen-driven patterns of TCR bias are shared across diverse outcomes of human hepatitis C virus infection. J Immunol 2011; 186:901-912.
51. Iglesias MC, Briceno O, Gostick E, et al. Immunodominance of HLA-B27- restricted HIV KK10-specific CD8(p) T-cells is not related to naive precursor frequency. Immunol Lett 2013; 149:119-122.
52. Tenzer S, Wee E, Burgevin A, et al. Antigen processing influences HIVspecific cytotoxic T lymphocyte immunodominance. Nat Immunol 2009; 10:636-646.
53. Elahi S, Dinges WL, Lejarcegui N, et al. Protective HIV-specific CD8p T cells evade Treg cell suppression. Nat Med 2011; 17:989-995.
54. Chessman D, Kostenko L, Lethborg T, et al. Human leukocyte antigen class Irestricted activation of CD8p T cells provides the immunogenetic basis of a systemic drug hypersensitivity. Immunity 2008; 28:822-832. (Pubitemid 351784513)
55. Illing PT, Vivian JP, Dudek NL, et al. Immune self-reactivity triggered by drugmodified HLA-peptide repertoire. Nature 2012; 486:554-558.
56. Illing PT, Vivian JP, Purcell AW, et al. Human leukocyte antigen-associated drug hypersensitivity. Curr Opin Immunol 2013; 25:81-89.
57. Ostrov DA, Grant BJ, Pompeu YA, et al. Drug hypersensitivity caused by alteration of the MHC-presented self-peptide repertoire. Proc Natl Acad Sci U S A 2012; 109:9959-9964.
58. Pineton de Chambrun M, Wechsler B, Geri G, et al. New insights into the pathogenesis of Behcet's disease. Autoimmun Rev 2012; 11:687-698.
59. Yamaguchi A, Tsuchiya N, Mitsui H, et al. Association of HLA-B39 with HLAB27- negative ankylosing spondylitis and pauciarticular juvenile rheumatoid arthritis in Japanese patients. Evidence for a role of the peptide-anchoring B pocket. Arthritis Rheum 1995; 38:1672-1677.
60. Burton PR, Clayton DG, Cardon LR, et al. Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet 2007; 39:1329-1337. (Pubitemid 350041542)
61. EvansDM, Spencer CC, Pointon JJ, et al. Interaction between ERAP1 and HLAB27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat Genet 2011; 43:761-767.
62. Reveille JD, Sims AM, Danoy P, et al. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat Genet 2010; 42:123-127. Interreg IV Oberrhein)