The impact of inflammation and immune activation on B cell differentiation during HIV-1 infection

Frontiers in Immunology

Volumn 2, Issue JAN, 2012, Pages

  Ruffin, Nicolas ^a   HongThang, Pham ^a,b   Rethi, Bence ^a   Nilsson, Anna ^a   Chiodi, Francesca ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL INSTITUTE OF HYGIENE AND EPIDEMIOLOGY   (Viet Nam)

Author keywords

B cells; Germinal center; Hiv 1; Immune activation; Serological memory

Indexed keywords

EID: 84874044347     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.00090     Document Type: Article

References (64)

1. Alos, L., Navarrete, P., Morente, V., Garcia, F., Garrido, M., Plana, M., Mozos, A., Lopez, A., Gil, C., Pumarola, T., Caballero, M., Blanch, J. L., Fumero, E., Miro, J. M., Gal-lart, T., Gatell, J. M., and Campo, E. (2005). Immunoarchitecture of lymphoid tissue in HIV-infection during antiretroviral therapy correlates with viral persistence. Mod. Pathol. 18, 127-136.
2. Avery, D. T., Deenick, E. K., Ma, C. S., Suryani, S., Simpson, N., Chew, G. Y., Chan, T. D., Palendira, U., Busta-mante, J., Boisson-Dupuis, S., Choo, S., Bleasel, K. E., Peake, J., King, C., French, M. A., Engelhard, D., Al-Hajjar, S., Al-Muhsen, S., Mag-dorf, K., Roesler, J., Arkwright, P. D., Hissaria, P., Riminton, D. S., Wong, M., Brink, R., Fulcher, D. A., Casanova, J. L., Cook, M. C., and Tangye, S. G. (2010). B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J. Exp. Med. 207, 155-171.
3. Badr, G., Borhis, G., Lefevre, E. A., Chaoul, N., Deshayes, F., Dessirier, V., Lapree, G., Tsapis, A., and Richard, Y. (2008). BAFF enhances chemotaxis of primary human B cells: a particular synergy between BAFF and CXCL13 on memory B cells. Blood 111, 2744-2754.
4. Berkowska, M. A., Driessen, G. J., Bikos, V., Grosserichter-Wagener, C., Stam-atopoulos, K., Cerutti, A., He, B., Biermann, K., Lange, J. F., Van Der Burg, M., Van Dongen, J. J., and Van Zelm, M. C. (2011). Human memory B cells originate from three distinct germinal center-dependent and -independent maturation pathways. Blood 118, 2150-2158.
5. Bessa, J., Kopf, M., and Bachmann, M. E (2010). Cutting edge: IL-21 and TLR signaling regulate germinal center responses in a B cell-intrinsic manner. J. Immunol. 184, 4615-4619.
6. Brenchley, J. M., Price, D. A., Schacker, T. W., Asher, T. E., Silvestri, G., Rao, S., Kazzaz, Z., Bornstein, E., Lam-botte, O., Altmann, D., Blazar, B. R., Rodriguez, B., Teixeira-Johnson, L., Landay, A., Martin, J. N., Hecht, E M., Picker, L. J., Lederman, M. M., Deeks, S. G., and Douek, D. C. (2006). Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12, 1365-1371.
7. Brink, R. (2006). Regulation of B cell self-tolerance by BAFF. Semin. Immunol. 18, 276-283.
8. Cagigi, A., Mowafi, F., Phuong Dang, L. V., Tenner-Racz, K., Atlas, A., Grutzmeier, S., Racz, P., Chiodi, E, and Nilsson, A. (2008). Altered expression of the receptor-ligand pair CXCR5/CXCL13 in B cells during chronic HIV-1 infection. Blood 112, 4401-4410.
9. Cagigi, A., Nilsson, A., Pensieroso, S., and Chiodi, E (2010). Dysfunctional B-cell responses during HIV-1 infection: implication for influenza vaccination and highly active antiretroviral therapy. Lancet Infect. Dis. 10, 499-503.
10. Chiodi, E (2010). New therapy to revert dysfunctional antibody responses during HIV-1 infection. J. Clin. Invest. 120, 3810-3813.
11. Chu, V T., Beller, A., Nguyen, T. T., Steinhauser, G., and Berek, C. (2011). The long-term survival of plasma cells. Scand. J. Immunol. 73, 508-511.
12. Dandekar, S., George, M. D., and Baum-ler, A. J. (2010). Th17 cells, HIV and the gut mucosal barrier. Curr. Opin. HIV AIDS 5, 173-178.
13. Estes, J. D., Haase, A. T., and Schacker, T. W. (2008). The role of collagen deposition in depleting CD4+ T cells and limiting reconstitution in HIV-1 and SIV infections through damage to the secondary lymphoid organ niche. Semin. Immunol. 20, 181-186.
14. Ettinger, R., Kuchen, S., and Lipsky, P. E. (2008). The role of IL-21 in regulating B-cell function in health and disease. Immunol. Rev. 223, 60-86.
15. Ettinger, R., Sims, G. P., Fairhurst, A. M., Robbins, R., Da Silva, Y. S., Spol-ski, R., Leonard, W. J., and Lipsky, P. E. (2005). IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J. Immunol. 175, 7867-7879.
16. Fontaine, J., Chagnon-Choquet, J., Val-cke, H. S., Poudrier, J., and Roger, M. (2011). High expression levels of B lymphocyte stimulator (BLyS) by dendritic cells correlate with HIV-related B-cell disease progression in humans. Blood 117, 145-155.
17. Geretti, A. M., and Doyle, T. (2010). Immunization for HIV-positive individuals. Curr. Opin. Infect. Dis. 23, 32-38.
18. Good-Jacobson, K. L., Szumilas, C. G., Chen, L., Sharpe, A. H., Tomayko, M. M., and Shlomchik, M. J. (2010). PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 11, 535-542.
19. Harigai, M., Kawamoto, M., Hara, M., Kubota, T., Kamatani, N., and Miyasaka, N. (2008). Excessive production of IFN-gamma in patients with systemic lupus erythemato-sus and its contribution to induction of B lymphocyte stimulator/B cell-activating factor/TNF ligand superfamily-13B. J. Immunol. 181, 2211-2219.
20. Haynes, N. M., Allen, C. D., Lesley, R., Ansel, K. M., Killeen, N., and Cys-ter, J. G. (2007). Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopula-tion. J. Immunol. 179, 5099-5108.
21. He, B., Qiao, X., Klasse, P. J., Chiu, A., Chadburn, A., Knowles, D. M., Moore, J. P., and Cerutti, A. (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, 3931-3941.
22. Ho, J., Moir, S., Wang, W., Posada, J. G., Gu, W., Rehman, M. T., Dewar, R., Kovacs, C., Sneller, M. C., Chun, T. W., Follmann, D. A., and Fauci, A. S. (2011). Enhancing effects of adjuvanted 2009 pandemic H1N1 influenza A vaccine on memory B-cell responses in HIV-infected individuals. AIDS 25, 295-302.
23. Huang, K. H., Bonsall, D., Katzourakis, A., Thomson, E. C., Fidler, S. J., Main, J., Muir, D., Weber, J. N., Frater, A. J., Phillips, R. E., Pybus, O. G., Goul-der, P. J., Mcclure, M. O., Cooke, G. S., and Klenerman, P. (2010). B-cell depletion reveals a role for antibodies in the control of chronic HIV-1 infection. Nat. Commun. 1, 102.
24. Iannello, A., Boulassel, M. R., Sama-rani, S., Debbeche, O., Trem-blay, C., Toma, E., Routy, J. P., and Ahmad, A. (2010). Dynamics and consequences of IL-21 production in HIV-infected individuals: a longitudinal and cross-sectional study. J. Immunol. 184, 114-126.
25. Iannello, A., Tremblay, C., Routy, J. P., Boulassel, M. R., Toma, E., and Ahmad, A. (2008). Decreased levels of circulating IL-21 in HIV-infected AIDS patients: correlation with CD4+ T-cell counts. Viral Immunol. 21, 385-388.
26. Kalled, S. L. (2006). Impact of the BAFF/BR3 axis on B cell survival, germinal center maintenance and antibody production. Semin. Immunol. 18, 290-296.
27. Klatt, N. R., Vinton, C. L., Lynch, R. M., Canary, L. A., Ho, J., Darrah, P. A., Estes, J. D., Seder, R. A., Moir, S. L., and Brenchley, J. M. (2011). SIV infection of rhesus macaques results in dysfunctional T- and B-cell responses to neo and recall Leish-mania major vaccination. Blood 118, 5803-5812.
28. Lane, H. C., Masur, H., Edgar, L. C., Whalen, G., Rook, A. H., and Fauci, A. S. (1983). Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 309, 453-458.
29. Lanzavecchia, A., andSallusto, F. (2009). Human B cell memory. Curr. Opin. Immunol. 21, 298-304.
30. Lederman, M. M., and Margolis, L. (2008). The lymph node in HIV pathogenesis. Semin. Immunol. 20, 187-195.
31. Lewis, G. K. (2010). Challenges of antibody-mediated protection against HIV-1. Expert Rev. Vaccines 9, 683-687.
32. Li, Q., Duan, L., Estes, J. D., Ma, Z. M., Rourke, T., Wang, Y., Reilly, C., Carlis, J., Miller, C. J., and Haase, A. T. (2005). Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434, 1148-1152.
33. Linterman, M. A., Beaton, L., Yu, D., Ramiscal, R. R., Srivastava, M., Hogan, J. J., Verma, N. K., Smyth, M. J., Rigby, R. J., and Vinuesa, C. G. (2010). IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207, 353-363.
34. Linterman, M. A., Pierson, W., Lee, S. K., Kallies, A., Kawamoto, S., Rayner, T. F., Srivastava, M., Divekar, D. P., Beaton, L., Hogan, J. J., Fagarasan, S., Liston, A., Smith, K. G., and Vinuesa, C. G. (2011). Foxp3+ follicular regulatory T cells control the germinal center response. Nat. Med. 17, 975-982.
35. Macias, J., Japon, M. A., Leal, M., Saez, C., Pineda, J. A., Segura, D. I., Ortega, J., and Lissen, E. (2001). Structural normalization of the lymphoid tissue in asymptomatic HIV-infected patients after 48 weeks of potent antiretroviral therapy. AIDS 15, 2371-2378.
36. Mackay, F., and Leung, H. (2006). The role of the BAFF/APRIL system on T cell function. Semin. Immunol. 18, 284-289.
37. Mackay, F., and Schneider, P. (2009). Cracking the BAFF code. Nat. Rev. Immunol. 9, 491-502.
38. Mascola, J. R., and Montefiori, D. C. (2010). The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28, 413-444.
39. Mehandru, S., Poles, M. A., Tenner-Racz, K., Horowitz, A., Hurley, A., Hogan, C., Boden, D., Racz, P., and Markowitz, M. (2004). Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200, 761-770.
40. Miedema, E (2011). Grand challenges in the immunology of HIV and AIDS. Front. Immunol. 2:20. doi:10.3389/fimmu.2011.00020.
41. 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. (2008). Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 205, 1797-1805.
42. 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. (2001). HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc. Natl. Acad. Sci. U.S.A. 98, 10362-10367.
43. Muro-Cacho, C. A., Pantaleo, G., and Fauci, A. S. (1995). Analysis of apop-tosis in lymph nodes of HIV-infected persons. Intensity of apoptosis correlates with the general state of activation of the lymphoid tissue and not with stage of disease or viral burden. J.Immunol. 154, 5555-5566.
44. Nilsson, J., Kinloch-De-Loes, S., Granath, A., Sonnerborg, A., Goh, L. E., and Andersson, J. (2007). Early immune activation in gut-associated and peripheral lymphoid tissue during acute HIV infection. AIDS 21, 565-574.
45. Nutt, S. L., and Tarlinton, D. M. (2011). Germinal center B and follicular helper T cells: siblings, cousins or just good friends? Nat. Immunol. 12, 472-477.
46. Pallikkuth, S., Rogers, K., Villinger, F., Dosterii, M., Vaccari, M., Franchini, G., Pahwa, R., and Pahwa, S. (2011). Interleukin-21 administration to rhesus macaques chronically infected with simian immunodeficiency virus increases cytotoxic effector molecules in T cells and NK cells and enhances B cell function without increasing immune activation or viral replication. Vaccine 29, 9229-9238.
47. Pariani, E., Boschini, A., Amendola, A., Poletti, R., Anselmi, G., Beg-nini, M., Ranghiero, A., Cecconi, G., and Zanetti, A. R. (2011). Response to 2009 pandemic and seasonal influenza vaccines co-administered to HIV-infected and HIV-uninfected former drug users living in a rehabilitation community in Italy. Vaccine 29, 9209-9213.
48. Pelletier, N., Mcheyzer-Williams, L. J., Wong, K. A., Urich, E., Fazilleau, N., and Mcheyzer-Williams, M. G. (2010). Plasma cells negatively regulate the follicular helper T cell program. Nat. Immunol. 11, 1110-1118.
49. Qiao, X., He, B., Chiu, A., Knowles, D. M., Chadburn, A., and Cerutti, A. (2006). Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat. Immunol. 7, 302-310.
50. Rankin, A. L., Macleod, H., Keegan, S., Andreyeva, T., Lowe, L., Bloom, L., Collins, M., Nickerson-Nutter, C., Young, D., and Guay, H. (2011). IL-21 receptor is critical for the development of memory B cell responses. J. Immunol. 186, 667-674.
51. Rodriguez, B., Valdez, H., Freimuth, W., Butler, T., Asaad, R., and Lederman, M. M. (2003). Plasma levels of B-lymphocyte stimulator increase with HIV disease progression. AIDS 17, 1983-1985.
52. Samuelsson, A., Sonnerborg, A., Heuts, N., Coster, J., and Chiodi, F. (1997). Progressive B cell apoptosis and expression of Fas ligand during human immunodeficiency virus type 1 infection. AIDS Res. Hum. Retroviruses 13, 1031-1038.
53. Scheid, J. F., Mouquet, H., Feldhahn, N., Seaman, M. S., Velinzon, K., Piet-zsch, J., Ott, R. G., Anthony, R. M., Zebroski, H., Hurley, A., Phogat, A., Chakrabarti, B., Li, Y., Connors, M., Pereyra, F., Walker, B. D., Warde-mann, H., Ho, D., Wyatt, R. T., Mascola, J. R., Ravetch, J. V., and Nussenzweig, M. C. (2009). Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458, 636-640.
54. Stohl, W., Cheema, G. S., Briggs, W. S., Xu, D., Sosnovtseva, S., Roschke, V., Ferrara, D. E., Labat, K., Sat-tler, E R., Pierangeli, S. S., and Hilbert, D. M. (2002). B lymphocyte stimulator protein-associated increase in circulating autoantibody levels may require CD4+ T cells: lessons from HIV-infected patients. Clin. Immunol. 104, 115-122.
55. Swingler, S., Zhou, J., Swingler, C., Dauphin, A., Greenough, T., Joli-coeur, P., and Stevenson, M. (2008). Evidence for a pathogenic determinant in HIV-1 Nef involved in B cell dysfunction in HIV/AIDS. Cell Host Microbe 4, 63-76.
56. Thang, P. H., Ruffin, N., Brodin, D., Rethi, B., Cam, P. D., Hien, N. T., Lopalco, L., Vivar, N., and Chiodi, E (2010). The role of IL-1beta in reduced IL-7 production by stro-mal and epithelial cells: a model for impaired T-cell numbers in the gut during HIV-1 infection. J. Intern. Med. 268, 181-193.
57. Titanji, K., De Milito, A., Cagigi, A., Thorstensson, R., Grutzmeier, S., Atlas, A., Hejdeman, B., Kroon, F. P., Lopalco, L., Nilsson, A., and Chiodi, E (2006). Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 108, 1580-1587.
58. Titanji, K., Velu, V., Chennareddi, L., Vijay-Kumar, M., Gewirtz, A. T., Freeman, G. J., and Amara, R. R. (2010). Acute depletion of activated memory B cells involves the PD-1 pathway in rapidly progressing SIV-infected macaques. J. Clin. Invest. 120, 3878-3890.
59. Tokoyoda, K., Hauser, A. E., Nakayama, T., and Radbruch, A. (2010). Organization of immunological memory by bone marrow stroma. Nat. Rev. Immunol. 10, 193-200.
60. Van Grevenynghe, J., Halwani, R., Chomont, N., Ancuta, P., Peretz, Y., Tanel, A., Procopio, E A., Shi, Y., Said, E. A., Haddad, E. K., and Sekaly, R. P. (2008). Lymph node architecture collapse and consequent modulation of FOXO3a pathway on memory T- and B-cells during HIV infection. Semin. Immunol. 20, 196-203.
61. Velu, V., Titanji, K., Zhu, B., Husain, S., Pladevega, A., Lai, L., Vander-ford, T. H., Chennareddi, L., Silvestri, G., Freeman, G. J., Ahmed, R., and Amara, R. R. (2009). Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458, 206-210.
62. Yue, E Y., Lo, C., Sakhdari, A., Lee, E. Y., Kovacs, C. M., Benko, E., Liu, J., Song, H., Jones, R. B., Sheth, P., Chege, D., Kaul, R., and Ostrowski, M. A. (2010). HIV-specific IL-21 producing CD4+ T cells are induced in acute and chronic progressive HIV infection and are associated with relative viral control. J. Immunol. 185, 498-506.
63. Zeng, M., Smith, A. J., Wietgrefe, S. W., Southern, P. J., Schacker, T. W., Reilly, C. S., Estes, J. D., Burton, G. F., Sil-vestri, G., Lifson, J. D., Carlis, J. V., and Haase, A. T. (2011). Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J. Clin. Invest. 121, 998-1008.
64. Zotos, D., Coquet, J. M., Zhang, Y., Light, A., D'Costa, K., Kallies, A., Corcoran, L. M., Godfrey, D. I., Toellner, K. M., Smyth, M. J., Nutt, S. L., and Tar-linton, D. M. (2010). IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207, 365-378.