Decreased mutation frequencies among immunoglobulin G variable region genes during viremic HIV-1 infection

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Bowers, Elisabeth ^a,c   Scamurra, Ronald W ^d   Asrani, Anil ^d   Beniguel, Lydie ^e   MaWhinney, Samantha ^a,b   Keays, Kathryne M ^a   Thurn, Joseph R ^d   Janoff, Edward N ^a,c  

^a UNIVERSITY OF COLORADO   (United States)

^b Global Health and Health Disparities   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITÉ JEAN MONNET   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; AMINO ACID; COMPLEMENTARY DNA; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; MESSENGER RNA; NUCLEOTIDE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE;

ADULT; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CLINICAL ARTICLE; CLONE; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA SEQUENCE; FEMALE; GENE AMPLIFICATION; GENE FREQUENCY; GENE SEQUENCE; GENE SWITCHING; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOGLOBULIN PRODUCTION; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOPATHOGENESIS; MALE; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SOMATIC HYPERMUTATION; VIREMIA;

ADULT; AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; CASE-CONTROL STUDIES; COMPLEMENTARITY DETERMINING REGIONS; FEMALE; GENE EXPRESSION; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN VARIABLE REGION; MALE; MIDDLE AGED; MUTATION; MUTATION RATE; VIREMIA; YOUNG ADULT;

EID: 84896925239     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081913     Document Type: Article

References (54)

1. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, et al. (1983) Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. New Eng J Med 309: 453-458. (Pubitemid 13041485)
2. Terpstra FG, Al BJ, Roos MT, De Wolf F, Goudsmit J, et al. (1989) Longitudinal study of leukocyte functions in homosexual men seroconverted for HIV: rapid and persistent loss of B cell function after HIV infection. Eur J Immunol 19: 667-673. (Pubitemid 19152934)
3. Obaro SK, Pugatch D, Luzuriaga K (2004) Immunogenicity and efficacy of childhood vaccines in HIV-1-infected children. Lancet Infect Dis 4: 510-518. (Pubitemid 39077921)
4. Pancharoen C, Ananworanich J, Thisyakorn U (2004) Immunization for persons infected with human immunodeficiency virus. Curr HIV Res 2: 293-299. (Pubitemid 39242959)
5. Rivas P, Herrero MD, Puente S, Ramirez-Olivencia G, Soriano V (2007) Immunizations in HIV-infected adults. AIDS Rev 9: 173-187. (Pubitemid 350010542)
6. Scamurra RW, Miller DJ, Dahl L, Abrahamsen M, Kapur V, et al. (2000) Impact of HIV-1 infection on VH3 gene repertoire of naive human B cells. J Immunol 164: 5482-5491. (Pubitemid 30305233)
7. Berek C, Berger A, Apel M (1991) Maturation of the immune response in germinal centers. Cell 67: 1121-1129. (Pubitemid 121001525)
8. Janoff EN, Jackson S, Wahl SM, Thomas K, Peterman JH, et al. (1994) Intestinal mucosal immunoglobulins during human immunodeficiency virus type 1 infection. J Infec Dis 170: 299-307. (Pubitemid 24226355)
9. Fogelman I, Davey V, Ochs HD, Elashoff M, Feinberg MB, et al. (2000) Evaluation of CD4+ T cell function In vivo in HIV-infected patients as measured by bacteriophage phiX174 immunization. J Infec Dis 182: 435-441. (Pubitemid 30651039)
10. Matsuda F, Ishii K, Bourvagnet P, Kuma K, Hayashida H, et al. (1998) The complete nucleotide sequence of the human immunoglobulin heavy chain variable region locus. J Exp Med 188: 2151-2162. (Pubitemid 28562531)
11. Abadi J, Friedman J, Mageed RA, Jefferis R, Rodriguez-Barradas MC, et al. (1998) Human antibodies elicited by a pneumococcal vaccine express idiotypic determinants indicative of VH3 gene segment usage. J Infec Dis 178: 707-716. (Pubitemid 28397218)
12. Adderson EE, Shackelford PG, Quinn A, Wilson PM, Cunningham MW, et al. (1993) Restricted immunoglobulin VH usage and VDJ combinations in the human response to Haemophilus influenzae type b capsular polysaccharide. Nucleotide sequences of monospecific anti-Haemophilus antibodies and polyspecific antibodies cross-reacting with self antigens. J Clin Invest 91: 2734-2743. (Pubitemid 23182530)
13. Pirofski L, Lui R, DeShaw M, Kressel AB, Zhong Z (1995) Analysis of human monoclonal antibodies elicited by vaccination with a Cryptococcus neoformans glucuronoxylomannan capsular polysaccharide vaccine. Infect Immun 63: 3005-3014.
14. French N, Nakiyingi J, Carpenter LM, Lugada E, Watera C, et al. (2000) 23-valent pneumococcal polysaccharide vaccine in HIV-1-infected Ugandan adults: double-blind, randomised and placebo controlled trial. Lancet 355(9221): 2106-2111. (Pubitemid 30364659)
15. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C (1991) Sequences of proteins of immunological interest. U.S. Department of Health and Human Services, Bethesda.
16. Owens GP, Ritchie AM, Burgoon MP, Williamson RA, Corboy JR, et al. (2003) Single-cell repertoire analysis demonstrates that clonal expansion is a prominent feature of the B cell response in multiple sclerosis cerebrospinal fluid. J Immunol 171(5): 2725-2733. (Pubitemid 37025586)
17. Kristiansen SV, Pascual V, Lipsky PE (1994) Staphylococcal protein A induces biased production of Ig by VH3-expressing B lymphocytes. J Immunol 153: 2974-2982.
18. Mortari F, Wang JY, Schroeder HW (1993) Human cord blood antibody repertoire. Mixed population of VH gene segments and CDR3 distribution in the expressed C alpha and C gamma repertoires. J Immunol 150: 1348-1357. (Pubitemid 23127424)
19. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
20. Eisenberg D (1984) Three-dimensional structure of membrane and surface proteins. Annu Rev Biochem 53: 595-623.
21. Lefranc MP, Giudicelli V, Ginestoux C, Jabado-Michaloud J, Folch G, et al. (2009) IMGT®, the international ImMunoGeneTics information system®. Nuc Acids Res 37: D1006-D1012.
22. Souto-Carneiro MM, Longo NS, Russ DE, Sun H, Lipsky PE (2004) Characterization of the human immunoglobulin heavy chain antigen binding complementarity determining region 3 using a newly-developed software algorithm, JOINSOLVER®. J Immunol 172(11): 6790-6802. (Pubitemid 38669117)
23. H gene repertoire. J Clin Invest 99: 2488-2501.
24. Wu X, Feng J, Komori A, Kim EC, Zan H, et al. (2003) Immunoglobulin somatic hypermutation: double-strand DNA breaks, AID and error-prone DNA repair. J Clin Immunol 23: 235-246. (Pubitemid 36870666)
25. Rogosch T, Kerzel S, Hoss K, Hoersch G, Zemlin C, et al. (2012). IgA response in preterm neonates shows little evidence of antigen-driven selection. J Immunol 189(11): 5449-5456.
26. Karray S, Juompan L, Maroun RC, Isenberg D, Silverman GJ, et al. (1998) Structural basis of the gp120 superantigen-binding site on human immunoglobulins. J Immunol 161: 6681-6688. (Pubitemid 28562210)
27. Spencer J, Dunn-Walters DK (2005) Hypermutation at A-T base pairs: the A nucleotide replacement spectrum is affected by adjacent nucleotides and there is no reverse complementarity of sequences flanking mutated A and T nucleotides. J Immunol 175: 5170-5177. (Pubitemid 41456401)
28. Luo Z, Ronai D, Scharff MD (2004) The role of activation-induced cytidine deaminase in antibody diversification, immunodeficiency, and B-cell malignancies. J Allergy Clin Immunol 114: 726-735; quiz 736.
29. Neuberger MS, Di Noia JM, Beale RC, Williams GT, Yang Z, et al. (2005) Somatic hypermutation at A.T pairs: polymerase error versus dUTP incorporation. Nat Rev Immunol 5(2): 171-178. (Pubitemid 40208906)
30. Casali P, Pal Z, Xu Z, Zan H (2006) DNA repair in antibody somatic hypermutation. Trends Immunol 27: 313-321. (Pubitemid 43963473)
31. Seki M, Gearhart PJ, Wood RD (2005) DNA polymerases and somatic hypermutation of immunoglobulin genes. EMBO Rep 12: 1143-1148. (Pubitemid 41741697)
32. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, et al. (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 337: 585-596. (Pubitemid 38326879)
33. Langlois MA, Beale RC, Conticello SG, Neuberger MS (2005) Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nuc Acids Res 33: 1913-1923. (Pubitemid 41748336)
34. Subramaniam K, French N, Pirofsky LA (2005) Cryptococcus neoformans-reactive and total immunoglobulin profiles of human immunodeficiency virus-infected and uninfected Ugandans. Clin Diagn Lab Immunol 12(10): 1168-1176. (Pubitemid 41475825)
35. Nair N, Moss WJ, Scott S, Mugala N, Ndhlovu ZM, et al. (2009) HIV-1 Infection in Zambian Children Impairs the Development and Avidity Maturation of Measles Virus-Specific Immunoglobulin G after Vaccination and Infection. J Infec Dis 200: 1031-8.
36. Brunell PA, Vimal V, Sandu M, Courville TM, Daar E, et al. (1995) Abnormalities of measles antibody response in human immunodeficiency virus type 1 (HIV-1) infection. J Acquir Immune Defic Syndr Hum Retrovirol 10: 540-8.
37. Ballet JJ, Sulcebe G, Couderc LJ, Danon F, Rabian C, et al. (1987) Impaired anti-pneumococcal antibody response in patients with AIDS-related persistent generalized lymphadenopathy. Clin Exp Immunol 68: 479-487. (Pubitemid 17077133)
38. French N, Gilks CF, Mujugira A, Fasching C, O'Brien J, et al. (1998) Pneumococcal vaccination in HIV-1-infected adults in Uganda: humoral response and two vaccine failures. AIDS (London, England) 12: 1683-1689. (Pubitemid 28418340)
39. Janoff EN, Fasching C, Ojoo JC, O'Brien J, Gilks CF (1997) Responsiveness of human immunodeficiency virus type 1-infected Kenyan women with or without prior pneumococcal disease to pneumococcal vaccine. J Infec Dis 175: 975-978. (Pubitemid 27142981)
40. Berberian L, Goodglick L, Kipps TJ, Braun J (1993) Immunoglobulin VH3 gene products: natural ligands for HIV gp120. Science 261: 1588-1591. (Pubitemid 23319603)
41. Haase AT, Henry K, Zupancic M, Sedgewick G, Faust RA, et al. (1996) Quantitative image analysis of HIV-1 infection in lymphoid tissue. Science 274: 985-989. (Pubitemid 26398421)
42. He B, Qiao X, Klasse PJ, Chiu A, Chadburn A, et al. (2006) HIV-1 envelope triggers polyclonal Ig class switch recombination through a CD40-independent mechanism involving BAFF and C-type lectin receptors. J Immunol 176(7): 3931-3941. (Pubitemid 44264370)
43. Moir S, Fauci AS (2009) B cells in HIV infection and disease. Nat Rev Immunol 9(4): 235-245.
44. Pham P, Zhang K, Goodman MF (2008) Hypermutation at A/T Sites During G.U Mismatch Repair in vitro by Human B-cell Lysates. J Biol Chem 283(46): 31754-31762.
45. Epeldegui M, Thapa DR, De La Cruz J, Kitchen S, Zack JA, et al. (2010) CD40 Ligand (CD154) Incorporated into HIV Virions Induces Activated-Induced Cytidine Deaminase (AID) Expression in Human B Lympocytes. PLoS ONE 5(7).
46. Epeldegui M, Breen EC, Hung YP, Boscardin WJ, Detels R, et al. (2007) Elevated expression of activation induced cytidine deaminase in peripheral blood mononuclear cells precedes AIDS-NHL diagnosis. AIDS (London, England) 21: 2265-2270. (Pubitemid 350287452)
47. Cagigi A, Du L, Dang LV, Grutzmeier S, Atlas A, et al. (2009) CD27(-) B-cells produce class switched and somatically hyper-mutated antibodies during chronic HIV-1 infection. PLoS ONE 4(5): e5427.
48. Muto T, Okazaki IM, Yamada S, Tanaka Y, Kinoshita K, et al. (2006) Negative regulation of activation-induced cytidine deaminase in B cells. PNAS 103(8): 2752-2757.
49. Santa-Marta M, Aires da Silva F, Fonseca AM, Rato S, Goncalves J (2007) HIV-1 Vif protein blocks the cytidine deaminase activity of B-cell specific AID in E. coli by a similar mechanism of action. Mol Immunol 44: 583-590. (Pubitemid 44287042)
50. Qiao X, He B, Chiu A, Knowles DM, Chadburn A, et al. (2006). Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol 7(3): 302-310.
51. Kolar GR, Mehta D, Wilson PC, Capra JD (2006) Diversity of the Ig repertoire is maintained with age in spite of reduced germinal centre cells in human tonsil lymphoid tissue. Scand J Immunol 64: 314-324. (Pubitemid 44215122)
52. Chong Y, Ikematsu H, Yamaji K, Nishimura M, Kashiwagi S, et al. (2003) Age-related accumulation of Ig V(H) gene somatic mutations in peripheral B cells from aged humans. Clin Exp Immunol 133: 59-66. (Pubitemid 36791943)
53. Wu Y, Kipling D, Dunn-Walters DK (2012) Age-related changes in human peripheral blood IGH repertoire following vaccination. Front Immunol 3: 193. doi: 10.3389/fimmu.2012.00193.
54. Jiang N, He J, Weinstein JA, Penland L, Sasaki S, et al. (2013) Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci Transl Med 5(171): doi: 10.1126/scitranslmed.3004794.