Abnormal B cell memory subsets dominate HIV-specific responses in infected individuals

Journal of Clinical Investigation

Volumn 124, Issue 7, 2014, Pages 3252-3262

  Kardava, Lela ^a   Moir, Susan ^a   Shah, Naisha ^a   Wang, Wei ^a   Wilson, Richard ^b   Buckner, Clarisa M ^a   Santich, Brian H ^a,f   Kim, Leo J Y ^a,g   Spurlin, Emily E ^a,h   Nelson, Amy K ^a   Wheatley, Adam K ^a   Harvey, Christopher J ^c   McDermott, Adrian B ^a   Wucherpfennig, Kai W ^c,d   Chun, Tae Wook ^a   Tsang, John S ^a,e   Li, Yuxing ^a,b   Fauci, Anthony S ^a  

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

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

^f Mount Sinai Graduate School of Biological Sciences   (United States)

^g CASE WESTERN RESERVE UNIVERSITY   (United States)

^h UNIVERSITY OF SOUTH ALABAMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CORECEPTOR; EPITOPE; GLYCOPROTEIN GP 140; RECEPTOR; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL MEMORY; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; PRIORITY JOURNAL; VIREMIA; VIRUS ENVELOPE;

ACUTE DISEASE; ANTI-HIV AGENTS; ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTE SUBSETS; CHRONIC DISEASE; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HUMANS; IMMUNOLOGIC MEMORY; TRANSCRIPTOME; VIRAL LOAD;

EID: 84903765782     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI74351     Document Type: Article

References (59)

1. Corti D, et al. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One. 2010;5(1):e8805.
2. Walker LM, et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science. 2009;326(5950):285- 289.
3. Wu X, et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science. 2010;329(5993):856-861.
4. Scheid JF, et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science. 2011;333(6049):1633-1637.
5. Wu X, et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science. 2011;333(6049):1593-1602.
6. Walker LM, et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature. 2011;477(7365):466-470.
7. Burton DR, et al. A blueprint for HIV vaccine discovery. Cell Host Microbe. 2012;12(4):396-407.
8. Moir S, Malaspina A, Fauci AS. Prospects for an HIV vaccine: leading B cells down the right path. Nat Struct Mol Biol. 2011;18(12):1317-1321.
9. Kwong PD, Mascola JR. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity. 2012;37(3):412-425.
10. McCoy LE, Weiss RA. Neutralizing antibodies to HIV-1 induced by immunization. J Exp Med. 2013; 210(2):209-223.
11. Klein F, Mouquet H, Dosenovic P, Scheid JF, Scharf L, Nussenzweig MC. Antibodies in HIV-1 vaccine development and therapy. Science. 2013;341(6151):1199-1204.
12. Bonsignori M, et al. HIV-1 antibodies from infection and vaccination: insights for guiding vaccine design. Trends Microbiol. 2012;20(11):532-539.
13. Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, Stamatatos L. Characteristics of the earliest crossneutralizing antibody response to HIV-1. PLoS Pathog. 2011;7(1):e1001251.
14. Liao HX, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. 2013;496(7446):469-476.
15. 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.
16. Georgiev IS, et al. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science. 2013;340(6133):751-756.
17. Labrijn AF, et al. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1. J Virol. 2003; 77(19):10557-10565.
18. Chen W, Zhu Z, Feng Y, Dimitrov DS. Human domain antibodies to conserved sterically restricted regions on gp120 as exceptionally potent crossreactive HIV-1 neutralizers. Proc Natl Acad Sci U S A. 2008;105(44):17121-17126.
19. Li Y, et al. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J Virol. 2011;85(17):8954-8967.
20. Li Y, et al. HIV-1 neutralizing antibodies display dual recognition of the primary and coreceptor binding sites and preferential binding to fully cleaved envelope glycoproteins. J Virol. 2012;86(20):11231-11241.
21. 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.
22. Amu S, Ruffin N, Rethi B, Chiodi F. Impairment of B cell functions during HIV-1 infection. AIDS. 2013;27(15):2323-2334.
23. Moir S, et al. B cells of HIV-1-infected patients bind virions through CD21-complement interactions and transmit infectious virus to activated T cells. J Exp Med. 2000;192(5):637-646.
24. He B, et al. HIV-1 envelope triggers polyclonal Ig class switch recombination through a CD40-independent mechanism involving BAFF and C-type lectin receptors. J Immunol. 2006;176(7):3931-3941.
25. Silverman GJ, Goodyear CS. Confounding B cell defences: lessons from a staphylococcal superantigen. Nat Rev Immunol. 2006;6(6):465-475.
26. Rappocciolo G, et al. DC-SIGN on B lymphocytes is required for transmission of HIV-1 to T lymphocytes. PLoS Pathog. 2006;2(7):e70.
27. Haas A, Zimmermann K, Oxenius A. Antigen-dependent and-independent mechanisms of T and B cell hyperactivation during chronic HIV-1 infection. J Virol. 2011;85(23):12102-12113.
28. Klasse PJ, Sanders RW, Cerutti A, Moore JP. How can HIV-type-1-Env immunogenicity be improved to facilitate antibody-based vaccine development? AIDS Res Hum Retroviruses. 2012;28(1):1-15.
29. Jelicic K, et al. The HIV-1 envelope protein gp120 impairs B cell proliferation by inducing TGF-beta1 production and FcRL4 expression. Nat Immunol. 2013;14(12):1256-1265.
30. 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.
31. 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.
32. Scheid JF, et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature. 2009;458(7238):636-640.
33. Lynch RM, et al. The development of CD4 binding site antibodies during HIV-1 infection. J Virol. 2012;86(14):7588-7595.
34. 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.
35. Kaminski DA, Wei C, Qian Y, Rosenberg AF, Sanz I. Advances in human B cell phenotypic profiling. Front Immunol. 2012;3:302.
36. 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.
37. Lackner AA, Lederman MM, Rodriguez B. HIV pathogenesis: the host. Cold Spring Harb Perspect Med. 2012;2(9):a007005.
38. Whittle JR, et al. Flow cytometry reveals that H5N1 vaccination elicits cross-reactive stem-directed antibodies from multiple Ig heavy chain lineages. J Virol. 2014;88(8):4047-4057.
39. Franz B, May KF Jr, Dranoff G, Wucherpfennig K. Ex vivo characterization and isolation of rare memory B cells with antigen tetramers. Blood. 2011;118(2):348-357.
40. Ehrhardt GR, Hijikata A, Kitamura H, Ohara O, Wang JY, Cooper MD. Discriminating gene expression profiles of memory B cell subpopulations. J Exp Med. 2008;205(8):1807-1817.
41. 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.
42. Charles ED, et al. Clonal B cells in patients with hepatitis C virus-associated mixed cryoglobulinemia contain an expanded anergic CD21low B cell subset. Blood. 2011;117(20):5425-5437.
43. Isnardi I, et al. Complement receptor 2/CD21-human naive B cells contain mostly autoreactive unresponsive clones. Blood. 2010;115(24):5026-5036.
44. 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.
45. Wherry EJ, et al. Molecular Signature of CD8(+) T Cell Exhaustion during Chronic Viral Infection. Immunity. 2007;27(4):670-684.
46. Tarlinton D, Good-Jacobson K. Diversity among memory B cells: origin, consequences, and utility. Science. 2013;341(6151):1205-1211.
47. Conge AM, et al. Impairment of B-lymphocyte differentiation induced by dual triggering of the B cell antigen receptor and CD40 in advanced HIV-1-disease. AIDS. 1998;12(12):1437-1449.
48. De Milito A, et al. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood. 2004;103(6):2180-2186.
49. Moir S, et al. Decreased survival of B cells of HIVviremic patients mediated by altered expression of receptors of the TNF superfamily. J Exp Med. 2004;200(5):587-599.
50. van Grevenynghe J, et al. Loss of memory B cells during chronic HIV infection is driven by Foxo3aand TRAIL-mediated apoptosis. J Clin Invest. 2011;121(10):3877-3888.
51. Titanji K, et al. Low frequency of plasma nervegrowth factor detection is associated with death of memory B lymphocytes in HIV-1 infection. Clin Exp Immunol. 2003;132(2):297-303.
52. Samuelsson A, Brostrom C, van Dijk N, Sonnerborg A, Chiodi F. Apoptosis of CD4+ and CD19+ cells during human immunodeficiency virus type 1 infection-correlation with clinical progression, viral load, and loss of humoral immunity. Virology. 1997;238(2):180-188.
53. 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.
54. Li Y, et al. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J Virol. 2009;83(2):1045-1059.
55. Dosenovic P, et al. Selective expansion of HIV-1 envelope glycoprotein-specific B cell subsets recognizing distinct structural elements following immunization. J Immunol. 2009; 183(5):3373-3382.
56. Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc B Met. 1995;57(1):289-300.
57. Warnes GR, Bolker B, Lumley T. gplots: Various R Programming Tools For Plotting Data. R package version 2.6.0. CRAN; 2014.
58. Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22(12):1540-1542.
59. Rousseeuw PJ. Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math. 1987;20:53-65.