Maturational characteristics of HIV-specific antibodies in viremic individuals

JCI Insight

Volumn 1, Issue 3, 2016, Pages

  Meffre, Eric ^a   Louie, Aaron ^b   Bannock, Jason ^a   Kim, Leo J Y ^b   Ho, Jason ^b   Frear, Cody C ^b   Kardava, Lela ^b   Wang, Wei ^b   Buckner, Clarisa M ^b   Wang, Yimeng ^c   Fankuchen, Olivia R ^b   Gittens, Kathleen R ^b   Chun, Tae Wook ^b   Li, Yuxing ^b,c   Fauci, Anthony S ^b   Moir, Susan ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84981158037     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.84610     Document Type: Article

References (74)

1. Moir S, Fauci AS. B-cell exhaustion in HIV infection: the role of immune activation. Curr Opin HIV AIDS. 2014;9(5):472–477.
2. Moir S, Fauci AS. Insights into B cells and HIV-specific B-cell responses in HIV-infected individuals. Immunol Rev. 2013;254(1):207–224.
3. Amu S, Ruffin N, Rethi B, Chiodi F. Impairment of B-cell functions during HIV-1 infection. AIDS. 2013;27(15):2323–2334.
4. Buckner CM, et al. Characterization of plasmablasts in the blood of HIV-infected viremic individuals: evidence for nonspecific immune activation. J Virol. 2013;87(10):5800–5811.
5. Stacey AR, et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol. 2009;83(8):3719–3733.
6. Malaspina A, et al. Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7. Proc Natl Acad Sci U S A. 2006;103(7):2262–2267.
7. Moir S, et al. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy. Blood. 2010;116(25):5571–5579.
8. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med. 1998;188(9):1679–1689.
9. Tangye SG, Liu YJ, Aversa G, Phillips JH, de Vries JE. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J Exp Med. 1998;188(9):1691–1703.
10. Tangye SG, Ma CS, Brink R, Deenick EK. The good, the bad and the ugly — TFH cells in human health and disease. Nat Rev Immunol. 2013;13(6):412–426.
11. Tangye SG, Tarlinton DM. Memory B cells: effectors of long-lived immune responses. Eur J Immunol. 2009;39(8):2065–2075.
12. Tarlinton D, Good-Jacobson K. Diversity among memory B cells: origin, consequences, and utility. Science. 2013;341(6151):1205–1211.
13. Wu YC, Kipling D, Dunn-Walters DK. The relationship between CD27 negative and positive B cell populations in human peripheral blood. Front Immunol. 2011;2:81.
14. + B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J Immunol. 2006;177(6):3728–3736.
15. Kaminski DA, Wei C, Qian Y, Rosenberg AF, Sanz I. Advances in human B cell phenotypic profiling. Front Immunol. 2012;3:302.
16. Ehrhardt GR, et al. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J Exp Med. 2005;202(6):783–791.
17. Moir S, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med. 2008;205(8):1797–1805.
18. Wherry EJ, et al. Molecular signature of CD8(+) T cell exhaustion during chronic viral infection. Immunity. 2007;27(4):670–684.
19. Isnardi I, et al. Complement receptor 2/CD21-human naive B cells contain mostly autoreactive unresponsive clones. Blood. 2010;115(24):5026–5036.
20. low B-cell subset. Blood. 2011;117(20):5425–5437.
21. Weiss GE, et al. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol. 2009;183(3):2176–2182.
22. low B cells in common variable immunodeficiency resemble tissue homing, innate-like B cells. Proc Natl Acad Sci U S A. 2009;106(32):13451–13456.
23. Doi H, Tanoue S, Kaplan DE. Peripheral CD27(–)CD21(–) B-cells represent an exhausted lymphocyte population in hepatitis C cirrhosis. Clin Immunol. 2014;150(2):184–191.
24. –/low B cells in Sjogren’s syndrome-associated lymphoproliferation. Arthritis Rheum. 2013;65(4):1085–1096.
25. Castiello MC, et al. Wiskott-Aldrich Syndrome protein deficiency perturbs the homeostasis of B-cell compartment in humans. J Autoimmun. 2014;50:42–50.
26. Kuehn HS, et al. Immune dysregulation in human subjects with heterozygous germline mutations in CTLA4. Science. 2014;345(6204):1623–1627.
27. Schubert D, et al. Autosomal dominant immune dysregulation syndrome in humans with CTLA4 mutations. Nat Med. 2014;20(12):1410–1416.
28. Kardava L, et al. Abnormal B cell memory subsets dominate HIV-specific responses in infected individuals. J Clin Invest. 2014;124(7):3252–3262.
29. Berkowska MA, et al. Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways. Blood. 2011;118(8):2150–2158.
30. van Zelm MC, Szczepanski T, van der Burg M, van Dongen JJ. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J Exp Med. 2007;204(3):645–655.
31. Kardava L, et al. Attenuation of HIV-associated human B cell exhaustion by siRNA downregulation of inhibitory receptors. J Clin Invest. 2011;121(7):2614–2624.
32. Gitlin AD, Shulman Z, Nussenzweig MC. Clonal selection in the germinal centre by regulated proliferation and hypermutation. Nature. 2014;509(7502):637–640.
33. Kolhatkar NS, et al. Altered BCR and TLR signals promote enhanced positive selection of autoreactive transitional B cells in Wiskott-Aldrich syndrome. J Exp Med. 2015;212(10):1663–1677.
34. Pugh-Bernard AE, et al. Regulation of inherently autoreactive VH4-34 B cells in the maintenance of human B cell tolerance. J Clin Invest. 2001;108(7):1061–1070.
35. Kobie JJ, et al. 9G4 autoreactivity is increased in HIV-infected patients and correlates with HIV broadly neutralizing serum activity. PLoS One. 2012;7(4):e35356.
36. Sundling C, et al. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci Transl Med. 2012;4(142):142ra96.
37. Scheid JF, et al. A method for identification of HIV gp140 binding memory B cells in human blood. J Immunol Methods. 2009;343(2):65–67.
38. Bonsignori M, et al. HIV-1 antibodies from infection and vaccination: insights for guiding vaccine design. Trends Microbiol. 2012;20(11):532–539.
39. Lynch RM, et al. The development of CD4 binding site antibodies during HIV-1 infection. J Virol. 2012;86(14):7588–7595.
40. Scheid JF, et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature. 2009;458(7238):636–640.
41. Mascola JR, Haynes BF. HIV-1 neutralizing antibodies: understanding nature’s pathways. Immunol Rev. 2013;254(1):225–244.
42. Li Y, Svehla K, Mathy NL, Voss G, Mascola JR, Wyatt R. Characterization of antibody responses elicited by human immunodeficiency virus type 1 primary isolate trimeric and monomeric envelope glycoproteins in selected adjuvants. J Virol. 2006;80(3):1414–1426.
43. Dey B, et al. Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathog. 2009;5(5):e1000445.
44. Mouquet H, et al. Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature. 2010;467(7315):591–595.
45. Klein F, et al. Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell. 2013;153(1):126–138.
46. Liao HX, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. 2013;496(7446):469–476.
47. Scheid JF, et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science. 2011;333(6049):1633–1637.
48. Wu X, et al. Maturation and diversity of the VRC01-antibody lineage over 15 years of chronic HIV-1 infection. Cell. 2015;161(3):470–485.
49. Wu X, et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science. 2011;333(6049):1593–1602.
50. Victora GD, Nussenzweig MC. Germinal centers. Annu Rev Immunol. 2012;30:429–457.
51. Wu X, et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science. 2010;329(5993):856–861.
52. Zhou T, et al. Structural repertoire of HIV-1-neutralizing antibodies targeting the CD4 supersite in 14 donors. Cell. 2015;161(6):1280–1292.
53. Binley JM, et al. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J Virol. 2008;82(23):11651–11668.
54. Walker LM, et al. A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog. 2010;6(8):e1001028.
55. Li Y, et al. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat Med. 2007;13(9):1032–1034.
56. Muellenbeck MF, et al. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. J Exp Med. 2013;210(2):389–399.
57. Zinocker S, et al. The V gene repertoires of classical and atypical memory B cells in malaria-susceptible West African children. J Immunol. 2015;194(3):929–939.
58. Weiss GE, et al. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog. 2010;6(5):e1000912.
59. Portugal S, et al. Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. Elife. 2015;4.
60. Perreau M, et al. Follicular helper T cells serve as the major CD4 T cell compartment for HIV-1 infection, replication, and production. J Exp Med. 2013;210(1):143–156.
61. Cubas RA, et al. Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nat Med. 2013;19(4):494–499.
62. Tangye SG. Advances in IL-21 biology-enhancing our understanding of human disease. Curr Opin Immunol. 2015;34:107–115.
63. Naradikian MS, et al. IL-4 and IL-21 reciprocally regulate T-BET expression in activated B cells. Presented at: Keystone Symposia: The Golden Anniversary of B Cell Discovery; March 23, 2015; Banff, Alberta, Canada.
64. Snapper CM, Paul WE. Interferon-γ and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 1987;236(4804):944–947.
65. Terrier B, et al. Expansion of functionally anergic CD21-/low marginal zone-like B cell clones in hepatitis C virus infection-related autoimmunity. J Immunol. 2011;187(12):6550–6563.
66. Kurosaki T, Kometani K, Ise W. Memory B cells. Nat Rev Immunol. 2015;15(3):149–159.
67. Rubtsova K, Rubtsov AV, Cancro MP, Marrack P. Age-associated B cells: A T-bet-dependent effector with roles in protective and pathogenic immunity. J Immunol. 2015;195(5):1933–1937.
68. Wherry EJ, Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 2015;15(8):486–499.
69. Xiao M, Prabakaran P, Chen W, Kessing B, Dimitrov DS. Deep sequencing and Circos analyses of antibody libraries reveal antigen-driven selection of Ig VH genes during HIV-1 infection. Exp Mol Pathol. 2013;95(3):357–363.
70. Moir S, et al. CD40-Mediated induction of CD4 and CXCR4 on B lymphocytes correlates with restricted susceptibility to human immunodeficiency virus type 1 infection: potential role of B lymphocytes as a viral reservoir. J Virol. 1999;73(10):7972–7980.
71. Moir S, et al. Humans with chronic granulomatous disease maintain humoral immunologic memory despite low frequencies of circulating memory B cells. Blood. 2012;120(24):4850–4858.
72. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. Predominant autoantibody production by early human B cell precursors. Science. 2003;301(5638):1374–1377.
73. Li M, et al. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol. 2005;79(16):10108–10125.
74. Montezuma-Rusca JM, et al. Bone marrow plasma cells are a primary source of serum HIV-1-specific antibodies in chronically infected individuals. J Immunol. 2015;194(6):2561–2568.