Loss of HIV-specific memory B-cells as a potential mechanism for the dysfunction of the humoral immune response against HIV

Virology

Volumn 397, Issue 1, 2010, Pages 7-13

  Bussmann, Bianca M ^a   Reiche, Sven ^a   Bieniek, Bernhard ^b   Krznaric, Ivanka ^c   Ackermann, Frank ^d   Jassoy, Christian ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b PraxisCityOst   (Germany)

^c Practice Dupke/Carganico/Baumgarten   (Germany)

^d Medcenter Leipzig   (Germany)

Author keywords

Antibody; B cell Elispot; Env; Gag; HIV; Memory B cell

Indexed keywords

ANTIRETROVIRUS AGENT; GAG PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; TETANUS TOXOID;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; CD4 LYMPHOCYTE COUNT; CELL LOSS; CONTROLLED STUDY; DISEASE COURSE; DRUG TREATMENT FAILURE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOPATHOGENESIS; IMMUNOPATHOLOGY; INFLUENZA; MEMORY CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS CELL INTERACTION;

ANTI-RETROVIRAL AGENTS; ANTIBODIES, BACTERIAL; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CD4 LYMPHOCYTE COUNT; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV; HIV ANTIBODIES; HIV INFECTIONS; HUMANS; IMMUNOLOGIC MEMORY; INFLUENZA, HUMAN; TETANUS TOXOID;

EID: 73949138822     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.11.003     Document Type: Article

References (35)

1. Binley J.M., Klasse P.J., Cao Y., Jones I., Markowitz M., Ho D.D., and Moore J.P. Differential regulation of the antibody responses to Gag and Env proteins of human immunodeficiency virus type 1. J. Virol. 71 4 (1997) 2799-2809
2. Bonsignori M., Moody M.A., Parks R.J., Holl T.M., Kelsoe G., Hicks C.B., Vandergrift N., Tomaras G.D., and Haynes B.F. HIV-1 envelope induces memory B cell responses that correlate with plasma antibody levels after envelope gp120 protein vaccination or HIV-1 infection. J. Immunol. 183 4 (2009) 2708-2717
3. Brown A.E., Vahey M.T., Zhou S.Y., Chung R.C., Ruiz N.M., Hofheinz D., Lane J.R., and Mayers D.L. Quantitative relationship of circulating p24 antigen with human immunodeficiency virus (HIV) RNA and specific antibody in HIV-infected subjects receiving antiretroviral therapy. The RV43 Study Group. J. Infect. Dis. 172 4 (1995) 1091-1095
4. Cagigi A., Nilsson A., De Milito A., and Chiodi F. B cell immunopathology during HIV-1 infection: lessons to learn for HIV-1 vaccine design. Vaccine 26 24 (2008) 3016-3025
5. Cheingsong-Popov R., Panagiotidi C., Bowcock S., Aronstam A., Wadsworth J., and Weber J. Relation between humoral responses to HIV gag and env proteins at seroconversion and clinical outcome of HIV infection. BMJ 302 6767 (1991) 23-26
6. Crotty S., and Ahmed R. Immunological memory in humans. Semin. Immunol. 16 3 (2004) 197-203
7. De Milito A., Morch C., Sonnerborg A., and Chiodi F. Loss of memory (CD27) B lymphocytes in HIV-1 infection. Aids 15 8 (2001) 957-964
8. Douek D.C., Brenchley J.M., Betts M.R., Ambrozak D.R., Hill B.J., Okamoto Y., Casazza J.P., Kuruppu J., Kunstman K., Wolinsky S., Grossman Z., Dybul M., Oxenius A., Price D.A., Connors M., and Koup R.A. HIV preferentially infects HIV-specific CD4+ T cells. Nature 417 6884 (2002) 95-98
9. Fondere J.M., Huguet M.F., Yssel H., Baillat V., Reynes J., van de Perre P., and Vendrell J.P. Detection of peripheral HIV-1-specific memory B cells in patients untreated or receiving highly active antiretroviral therapy. Aids 17 16 (2003) 2323-2330
10. Fournier A.M., Fondere J.M., Alix-Panabieres C., Merle C., Baillat V., Huguet M.F., Taib J., Ohayon V., Zembala M., Reynes J., and Vendrell J.P. Spontaneous secretion of immunoglobulins and anti-HIV-1 antibodies by in vivo activated B lymphocytes from HIV-1-infected subjects: monocyte and natural killer cell requirement for in vitro terminal differentiation into plasma cells. Clin. Immunol. 103 1 (2002) 98-109
11. Gourley T.S., Wherry E.J., Masopust D., and Ahmed R. Generation and maintenance of immunological memory. Semin. Immunol. 16 5 (2004) 323-333
12. Guan Y., Sajadi M.M., Kamin-Lewis R., Fouts T.R., Dimitrov A., Zhang Z., Redfield R.R., DeVico A.L., Gallo R.C., and Lewis G.K. Discordant memory B cell and circulating anti-Env antibody responses in HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 106 10 (2009) 3952-3957
13. Hart M., Steel A., Clark S.A., Moyle G., Nelson M., Henderson D.C., Wilson R., Gotch F., Gazzard B., and Kelleher P. Loss of discrete memory B cell subsets is associated with impaired immunization responses in HIV-1 infection and may be a risk factor for invasive pneumococcal disease. J. Immunol. 178 12 (2007) 8212-8220
14. He B., Qiao X., Klasse P.J., Chiu A., Chadburn A., Knowles D.M., Moore J.P., and Cerutti A. 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 (2006) 3931-3941
15. Janoff E.N., Hardy W.D., Smith P.D., and Wahl S.M. Humoral recall responses in HIV infection. Levels, specificity, and affinity of antigen-specific IgG. J. Immunol. 147 7 (1991) 2130-2135
16. Jiang W., Lederman M.M., Mohner R.J., Rodriguez B., Nedrich T.M., Harding C.V., and Sieg S.F. Impaired naive and memory B-cell responsiveness to TLR9 stimulation in human immunodeficiency virus infection. J. Virol. 82 16 (2008) 7837-7845
17. Kroon F.P., van Dissel J.T., de Jong J.C., Zwinderman K., and van Furth R. Antibody response after influenza vaccination in HIV-infected individuals: a consecutive 3-year study. Vaccine 18 26 (2000) 3040-3049
18. Lane H.C., Masur H., Edgar L.C., Whalen G., Rook A.H., and Fauci A.S. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 309 8 (1983) 453-458
19. Malaspina A., Moir S., Orsega S.M., Vasquez J., Miller N.J., Donoghue E.T., Kottilil S., Gezmu M., Follmann D., Vodeiko G.M., Levandowski R.A., Mican J.M., and Fauci A.S. Compromised B cell responses to influenza vaccination in HIV-infected individuals. J. Infect. Dis. 191 9 (2005) 1442-1450
20. Malaspina A., Moir S., DiPoto A.C., Ho J., Wang W., Roby G., O'Shea M.A., and Fauci A.S. CpG oligonucleotides enhance proliferative and effector responses of B Cells in HIV-infected individuals. J. Immunol. 181 2 (2008) 1199-1206
21. Moir S., Malaspina A., Ogwaro K.M., Donoghue E.T., Hallahan C.W., Ehler L.A., Liu S., Adelsberger J., Lapointe R., Hwu P., Baseler M., Orenstein J.M., Chun T.W., Mican J.A., and Fauci A.S. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc. Natl. Acad. Sci. U.S.A. 98 18 (2001) 10362-10367
22. Moir S., Ho J., Malaspina A., Wang W., DiPoto A.C., O'Shea M.A., Roby G., Kottilil S., Arthos J., Proschan M.A., Chun T.W., and Fauci A.S. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 205 8 (2008) 1797-1805
23. Moir S., Malaspina A., Ho J., Wang W., Dipoto A.C., O'Shea M.A., Roby G., Mican J.M., Kottilil S., Chun T.W., Proschan M.A., and Fauci A.S. Normalization of B cell counts and subpopulations after antiretroviral therapy in chronic HIV disease. J. Infect. Dis. 197 4 (2008) 572-579
24. Morris L., Binley J.M., Clas B.A., Bonhoeffer S., Astill T.P., Kost R., Hurley A., Cao Y., Markowitz M., Ho D.D., and Moore J.P. HIV-1 antigen-specific and -nonspecific B cell responses are sensitive to combination antiretroviral therapy. J. Exp. Med. 188 2 (1998) 233-245
25. Nagase H., Agematsu K., Kitano K., Takamoto M., Okubo Y., Komiyama A., and Sugane K. Mechanism of hypergammaglobulinemia by HIV infection: circulating memory B-cell reduction with plasmacytosis. Clin. Immunol. 100 2 (2001) 250-259
26. Pitcher C.J., Quittner C., Peterson D.M., Connors M., Koup R.A., Maino V.C., and Picker L.J. HIV-1-specific CD4+ T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat. Med. 5 5 (1999) 518-525
27. Reiche S., Bussmann B.M., Dwai Y., and Jassoy C. Antibody-mediated binding of fluorescent HIV Gag and influenza nucleoprotein tetramers to blood cells. Immunobiology (2009)
28. doi:10.1016/j.imbio.2009.02.004.
29. Rosenberg E.S., Billingsley J.M., Caliendo A.M., Boswell S.L., Sax P.E., Kalams S.A., and Walker B.D. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278 5342 (1997) 1447-1450
30. Scheid J.F., Mouquet H., Feldhahn N., Seaman M.S., Velinzon K., Pietzsch J., Ott R.G., Anthony R.M., Zebroski H., Hurley A., Phogat A., Chakrabarti B., Li Y., Connors M., Pereyra F., Walker B.D., Wardemann H., Ho D., Wyatt R.T., Mascola J.R., Ravetch J.V., and Nussenzweig M.C. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458 7238 (2009) 636-640
31. Shirai A., Cosentino M., Leitman-Klinman S.F., and Klinman D.M. Human immunodeficiency virus infection induces both polyclonal and virus-specific B cell activation. J. Clin. Invest. 89 2 (1992) 561-566
32. Strathdee S.A., Frank J.W., McLaughlin J., Leblanc M., Major C., O'Shaughnessy M.V., and Read S.E. Quantitative measures of human immunodeficiency virus-specific antibodies predict progression to AIDS. J. Infect. Dis. 172 5 (1995) 1375-1379
33. Terpstra F.G., Al B.J., Roos M.T., De Wolf F., Goudsmit J., Schellekens P.T., and Miedema F. 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 4 (1989) 667-673
34. Titanji K., Chiodi F., Bellocco R., Schepis D., Osorio L., Tassandin C., Tambussi G., Grutzmeier S., Lopalco L., and De Milito A. Primary HIV-1 infection sets the stage for important B lymphocyte dysfunctions. Aids 19 17 (2005) 1947-1955
35. Zwart G., van der Hoek L., Valk M., Cornelissen M.T., Baan E., Dekker J., Koot M., Kuiken C.L., and Goudsmit J. Antibody responses to HIV-1 envelope and gag epitopes in HIV-1 seroconverters with rapid versus slow disease progression. Virology 201 2 (1994) 285-293