Impairment of B-cell functions during HIV-1 infection

AIDS

Volumn 27, Issue 15, 2013, Pages 2323-2334

  Amu, Sylvie ^a   Ruffin, Nicolas ^a,b   Rethi, Bence ^a   Chiodi, Francesca ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INSERM U955   (France)

Author keywords

Apoptosis; B cells; B cell subpopulations; HIV; Intrinsic defects; Regulatory functions

Indexed keywords

CYTOKINE;

B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL FUNCTION; CELL POPULATION; CELL SURFACE; CELL SURVIVAL; GERMINAL CENTER; HOMEOSTASIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; MEMORY CELL; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; B-LYMPHOCYTES; CYTOKINES; HIV INFECTIONS; HIV-1; HUMANS; T-LYMPHOCYTES;

EID: 84884499482     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e328361a427     Document Type: Review

References (102)

1. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narvaez AB, et al. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 2004; 104:942-947.
2. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 1999; 179:859-870.
3. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, Fauci AS. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 1983; 309:453-458.
4. Moir S, Malaspina A, Ogwaro KM, Donoghue ET, Hallahan CW, Ehler LA, et al. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Natl Acad Sci U S A 2001; 98:10362-10367.
5. Nagase H, Agematsu K, Kitano K, Takamoto M, Okubo Y, Komiyama A, et al. Mechanism of hypergammaglobulinemia by HIV infection: circulating memory B-cell reduction with plasmacytosis. Clin Immunol 2001; 100:250-259.
6. Jacobson DL, McCutchan JA, Spechko PL, Abramson I, Smith RS, Bartok A, et al. The evolution of lymphadenopathy and hypergammaglobulinemia are evidence for early and sustained polyclonal B lymphocyte activation during human immunodeficiency virus infection. J Infect Dis 1991; 163: 240-246.
7. Titanji K, Chiodi F, Bellocco R, Schepis D, Osorio L, Tassandin C, et al. Primary HIV-1 infection sets the stage for important B lymphocyte dysfunctions. AIDS 2005; 19:1947-1955.
8. Petrovas C, Yamamoto T, Gerner MY, Boswell KL, Wloka K, Smith EC, et al. CD4 T follicular helper cell dynamics during SIV infection. J Clin Invest 2012; 122:3281-3294.
9. Lindqvist M, van Lunzen J, Soghoian DZ, Kuhl BD, Ranasinghe S, Kranias G, et al. Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J Clin Invest 2012; 122:3271-3280.
10. Vinuesa CG. HIV and T follicular helper cells: a dangerous relationship. J Clin Invest 2012; 122:3059-3062.
11. Sammicheli S, Ruffin N, Lantto R, Vivar N, Chiodi F, Rethi B. IL-7 modulates B cells survival and activation by inducing BAFF and CD70 expression in T cells. J Autoimmun 2012; 38:304-314.
12. Perreau M, Savoye AL, De Crignis E, Corpataux JM, Cubas R, Haddad EK, 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; 210:143-156.
13. Notermans DW, de Jong JJ, Goudsmit J, Bakker M, Roos MT, Nijholt L, et al. Potent antiretroviral therapy initiates normalization of hypergammaglobulinemia and a decline in HIV type 1-specific antibody responses. AIDS Res Hum Retroviruses 2001; 17:1003-1008.
14. Fondere JM, Huguet MF, Yssel H, Baillat V, Reynes J, van de Perre P, et al. Detection of peripheral HIV-1-specific memory B cells in patients untreated or receiving highly active antiretroviral therapy. AIDS 2003; 17:2323-2330.
15. He B, Qiao X, Klasse PJ, Chiu A, Chadburn A, Knowles DM, 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; 176:3931-3941.
16. Swingler S, Zhou J, Swingler C, Dauphin A, Greenough T, Jolicoeur P, et al. Evidence for a pathogenic determinant in HIV-1 Nef involved in B cell dysfunction in HIV/AIDS. Cell Host Microbe 2008; 4:63-76.
17. Qiao X, He B, Chiu A, Knowles DM, Chadburn A, Cerutti A. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol 2006; 7:302-310.
18. Malaspina A, Moir S, Ho J, Wang W, Howell ML, O'Shea MA, et al. Appearance of immature/transitional B cells in HIVinfected individuals with advanced disease: correlation with increased IL-7. Proc Natl Acad SciUS A 2006; 103:2262-2267.
19. Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010; 32:129-140.
20. Del Nagro CJ, Otero DC, Anzelon AN, Omori SA, Kolla RV, Rickert RC. CD19 function in central and peripheral B-cell development. Immunol Res 2005; 31:119-131.
21. Perosa F, Favoino E, Caragnano MA, Prete M, Dammacco F. CD20: a target antigen for immunotherapy of autoimmune diseases. Autoimmun Rev 2005; 4:526-531.
22. Roozendaal R, Carroll MC. Complement receptors CD21 and CD35 in humoral immunity. Immunol Rev 2007; 219:157-166.
23. Palanichamy A, Barnard J, Zheng B, Owen T, Quach T, Wei C, et al. Novel human transitional B cell populations revealed by B cell depletion therapy. J Immunol 2009; 182:5982-5993.
24. Borst J, Hendriks J, Xiao Y. CD27 and CD70 in T cell and B cell activation. Curr Opin Immunol 2005; 17:275-281.
25. Deaglio S, Aydin S, Vaisitti T, Bergui L, Malavasi F. CD38 at the junction between prognostic marker and therapeutic target. Trends Mol Med 2008; 14:210-218.
26. Caraux A, Klein B, Paiva B, Bret C, Schmitz A, Fuhler GM, et al. Circulating human B and plasma cells. Age-associated changes in counts and detailed characterization of circulating normal CD138- and CD138+ plasma cells. Haematologica 2010; 95:1016-1020.
27. Kaminski DA, Wei C, Qian Y, Rosenberg AF, Sanz I. Advances in human B cell phenotypic profiling. Front Immunol 2012; 3:302.
28. Cagigi A, Palma P, Nilsson A, Di Cesare S, Pensieroso S, Kakoulidou M, et al. The impact of active HIV-1 replication on the physiological age-related decline of immature-transitional B-cells in HIV-1 infected children. AIDS 2010; 24:2075-2080.
29. Moir S, Buckner CM, Ho J, Wang W, Chen J, Waldner AJ, 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; 116:5571-5579.
30. Suryani S, Fulcher DA, Santner-Nanan B, Nanan R, Wong M, Shaw PJ, et al. Differential expression of CD21 identifies developmentally and functionally distinct subsets of human transitional B cells. Blood 2010; 115:519-529.
31. Ho J, Moir S, Malaspina A, Howell ML, Wang W, DiPoto AC, et al. Two overrepresented B cell populations in HIV-infected individuals undergo apoptosis by different mechanisms. Proc Natl Acad Sci U S A 2006; 103:19436-19441.
32. Zeng M, Smith AJ, Wietgrefe SW, Southern PJ, Schacker TW, Reilly CS, et al. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J Clin Invest 2011; 121:998-1008.
33. Rethi B, Vivar N, Sammicheli S, Chiodi F. Limited efficiency of endogenous interleukin-7 levels in T cell reconstitution during HIV-1 infection: will exogenous interleukin-7 therapy work? AIDS 2009; 23:745-755.
34. Titanji K, De Milito A, Cagigi A, Thorstensson R, Grutzmeier S, Atlas A, et al. Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 2006; 108:1580-1587.
35. De Milito A, Morch C, Sonnerborg A, Chiodi F. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 2001; 15:957-964.
36. De Milito A, Nilsson A, Titanji K, Thorstensson R, Reizenstein E, Narita M, et al. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood 2004; 103:2180-2186.
37. Pensieroso S, Cagigi A, Palma P, Nilsson A, Capponi C, Freda E, et al. Timing of HAART defines the integrity of memory B cells and the longevity of humoral responses in HIV-1 vertically-infected children. Proc Natl Acad Sci U S A 2009; 106:7939-7944.
38. D'Orsogna LJ, Krueger RG, McKinnon EJ, French MA. Circulating memory B-cell subpopulations are affected differently by HIV infection and antiretroviral therapy. AIDS 2007; 21:1747-1752.
39. Pensieroso S, Galli L, Nozza S, Ruffin N, Castagna A, Tambussi G, et al. B-cell subset alterations and correlated factors in HIV-1 infection. AIDS 2013 [Epub ahead of print].
40. Titanji K, Velu V, Chennareddi L, Vijay-Kumar M, Gewirtz AT, Freeman GJ, et al. Acute depletion of activated memory B cells involves the PD-1 pathway in rapidly progressing SIV-infected macaques. J Clin Invest 2010; 120:3878-3890.
41. Ruffin N, Lantto R, Pensieroso S, Sammicheli S, Hejdeman B, Rethi B, et al. Immune activation and increased IL-21R expression are associated with the loss of memory B cells during HIV-1 infection. J Intern Med 2012; 272:492-503.
42. Rethi B, Sammicheli S, Amu S, Pensieroso S, Hejdeman B, Schepis D, et al. Concerted effect of lymphopenia, viremia and T cell activation on Fas expression of peripheral B cells in HIV-1 infected patients. AIDS 2013; 27:155-162.
43. Cagigi A, Mowafi F, Phuong Dang LV, Tenner-Racz K, Atlas A, Grutzmeier S, et al. Altered expression of the receptor-ligand pair CXCR5/CXCL13 in B cells during chronic HIV-1 infection. Blood 2008; 112:4401-4410.
44. Moir S, Malaspina A, Li Y, Chun TW, Lowe T, Adelsberger J, 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; 192:637-646.
45. Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, O'Shea MA, 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; 205:1797-1805.
46. Kardava L, Moir S, Wang W, Ho J, Buckner CM, Posada JG, et al. Attenuation of HIV-associated human B cell exhaustion by siRNA downregulation of inhibitory receptors. J Clin Invest 2011; 121:2614-2624.
47. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443:350-354.
48. Chiodi F.Newtherapy to revert dysfunctional antibody responses during HIV-1 infection. J Clin Invest 2010; 120:3810-3813.
49. Kubo S, Yamada T, Osawa Y, Ito Y, Narita N, Fujieda S. Cytosine-phosphate-guanosine-DNA induces CD274 expression in human B cells and suppresses T helper type 2 cytokine production in pollen antigen-stimulated CD4-positive cells. Clin Exp Immunol 2012; 169:1-9.
50. Moir S, Malaspina A, Pickeral OK, Donoghue ET, Vasquez J, Miller NJ, et al. Decreased survival of B cells of HIV-viremic patients mediated by altered expression of receptors of the TNF superfamily. J Exp Med 2004; 200:587-599.
51. van Grevenynghe J, Cubas RA, Noto A, DaFonseca S, He Z, Peretz Y, et al. Loss of memory B cells during chronic HIV infection is driven by Foxo3a- and TRAIL-mediated apoptosis. J Clin Invest 2011; 121:3877-3888.
52. Macias J, Japon MA, Leal M, Saez C, Pineda JA, Segura DI, et al. Structural normalization of the lymphoid tissue in asymptomatic HIV-infected patients after 48 weeks of potent antiretroviral therapy. AIDS 2001; 15:2371-2378.
53. Alos L, Navarrete P, Morente V, Garcia F, Garrido M, Plana M, et al. Immunoarchitecture of lymphoid tissue in HIV-infection during antiretroviral therapy correlates with viral persistence. Mod Pathol 2005; 18:127-136.
54. Huang KH, Bonsall D, Katzourakis A, Thomson EC, Fidler SJ, Main J, et al. B-cell depletion reveals a role for antibodies in the control of chronic HIV-1 infection. Nat Commun 2010; 1:102.
55. Sammicheli S, Dang VP, Ruffin N, Pham HT, Lantto R, Vivar N, et al. IL-7 promotes CD95-induced apoptosis in B cells via the IFN-gamma/STAT1 pathway. PLoS One 2011; 6:e28629.
56. Maurer D, Fischer GF, Fae I, Majdic O, Stuhlmeier K, Von Jeney N, et al. IgM and IgG but not cytokine secretion is restricted to the CD27+ B lymphocyte subset. J Immunol 1992; 148:3700-3705.
57. Wolthers KC, Otto SA, Lens SM, Kolbach DN, van Lier RA, Miedema F, et al. Increased expression of CD80, CD86 and CD70 on T cells from HIV-infected individuals upon activation in vitro: regulation by CD4+ T cells. Eur J Immunol 1996; 26:1700-1706.
58. Fontaine J, Chagnon-Choquet J, Valcke HS, Poudrier J, Roger M. High expression levels of B lymphocyte stimulator (BLyS) by dendritic cells correlate with HIV-related B-cell disease progression in humans. Blood 2011; 117:145-155.
59. Sanz I. Indications of rituximab in autoimmune diseases. Drug Discov Today Ther Strateg 2009; 6:13-19.
60. De Keersmaecker B, Thielemans K, Aerts JL. Fighting with the enemy's weapons? The role of costimulatory molecules in HIV. Curr Mol Med 2011; 11:172-196.
61. Legendre C, Raphael M, Gras G, Lefevre EA, Feuillard J, Dormont D, et al. CD80 expression is decreased in hyperplastic lymph nodes of HIV+ patients. Int Immunol 1998; 10:1847-1851.
62. Malaspina A, Moir S, Kottilil S, Hallahan CW, Ehler LA, Liu S, et al. Deleterious effect of HIV-1 plasma viremia on B cell costimulatory function. J Immunol 2003; 170:5965-5972.
63. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200:749-759.
64. Estaquier J, Tanaka M, Suda T, Nagata S, Golstein P, Ameisen JC. Fas-mediated apoptosis of CD4+ and CD8+ T cells from human immunodeficiency virus-infected persons: differential in vitro preventive effect of cytokines and protease antagonists. Blood 1996; 87:4959-4966.
65. Quaranta MG, Mattioli B, Giordani L, Viora M. HIV-1 Nef equips dendritic cells to reduce survival and function of CD8+ T cells: a mechanism of immune evasion. FASEB J 2004; 18:1459-1461.
66. Strauss G, Lindquist JA, Arhel N, Felder E, Karl S, Haas TL, et al. CD95 co-stimulation blocks activation of naive T cells by inhibiting T cell receptor signaling. J Exp Med 2009; 206:1379-1393.
67. Samuelsson A, Sonnerborg A, Heuts N, Coster J, Chiodi F. Progressive B cell apoptosis and expression of Fas ligand during human immunodeficiency virus type 1 infection. AIDS Res Hum Retroviruses 1997; 13:1031-1038.
68. Rethi B, Vivar N, Sammicheli S, Fluur C, Ruffin N, Atlas A, et al. Priming of T cells to Fas-mediated proliferative signals by interleukin-7. Blood 2008; 112:1195-1204.
69. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, Heitman J, 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; 83:3719-3733.
70. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, Gray-Owen SD, et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 2010; 6:e1000852.
71. Kfutwah AK, Mary JY, Nicola MA, Blaise-Boisseau S, Barre-Sinoussi F, Ayouba A, et al. Tumour necrosis factor-alpha stimulates HIV-1 replication in single-cycle infection of human term placental villi fragments in a time, viral dose and envelope dependent manner. Retrovirology 2006; 3:36.
72. Clerici M, Wynn TA, Berzofsky JA, Blatt SP, Hendrix CW, Sher A, et al. Role of interleukin-10 in T helper cell dysfunction in asymptomatic individuals infected with the human immunodeficiency virus. J Clin Invest 1994; 93:768-775.
73. Alter G, Kavanagh D, Rihn S, Luteijn R, Brooks D, Oldstone M, et al. IL-10 induces aberrant deletion of dendritic cells by natural killer cells in the context of HIV infection. J Clin Invest 2010; 120:1905-1913.
74. Devadas K, Hardegen NJ, Wahl LM, Hewlett IK, Clouse KA, Yamada KM, et al. Mechanisms for macrophage-mediated HIV-1 induction. J Immunol 2004; 173:6735-6744.
75. Merrill JE, Koyanagi Y, Chen IS. Interleukin-1 and tumor necrosis factor alpha can be induced from mononuclear phagocytes by human immunodeficiency virus type 1 binding to the CD4 receptor. J Virol 1989; 63:4404-4408.
76. Kaul M, Garden GA, Lipton SA. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 2001; 410:988-994.
77. Villinger F, Ansari AA. Role of IL-12 in HIV infection and vaccine. Eur Cytokine Netw 2010; 21:215-218.
78. Rieckmann P, Poli G, Fox CH, Kehrl JH, Fauci AS. Recombinant gp120 specifically enhances tumor necrosis factor-alpha production and Ig secretion in B lymphocytes from HIVinfected individuals but not from seronegative donors. J Immunol 1991; 147:2922-2927.
79. Muller F, Aukrust P, Nordoy I, Froland SS. Possible role of interleukin-10 (IL-10) and CD40 ligand expression in the pathogenesis of hypergammaglobulinemia in human immunodeficiency virus infection: modulation of IL-10 and Ig production after intravenous Ig infusion. Blood 1998; 92:3721-3729.
80. Weimer R, Zipperle S, Daniel V, Zimmermann R, Schimpf K, Opelz G. HIV-induced IL-6/IL-10 dysregulation of CD4 cells is associated with defective B cell help and autoantibody formation against CD4 cells. Clin Exp Immunol 1998; 111:20-29.
81. Boue F, Wallon C, Goujard C, Barre-Sinoussi F, Galanaud P, Delfraissy JF. HIV induces IL-6 production by human B lymphocytes. Role of IL-4. J Immunol 1992; 148:3761-3767.
82. Muraguchi A, Hirano T, Tang B, Matsuda T, Horii Y, Nakajima K, et al. The essential role of B cell stimulatory factor 2 (BSF-2/IL-6) for the terminal differentiation of B cells. J Exp Med 1988; 167:332-344.
83. Shive CL, Biancotto A, Funderburg NT, Pilch-Cooper HA, Valdez H, Margolis L, et al. HIV-1 is not a major driver of increased plasma IL-6 levels in chronic HIV-1 disease. J Acquir Immune Defic Syndr 2012; 61:145-152.
84. Regidor DL, Detels R, Breen EC, Widney DP, Jacobson LP, Palella F, et al. Effect of highly active antiretroviral therapy on biomarkers of B-lymphocyte activation and inflammation. AIDS 2011; 25:303-314.
85. Barr TA, Shen P, Brown S, Lampropoulou V, Roch T, Lawrie S, et al. B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J Exp Med 2012; 209:1001-1010.
86. Fujimoto M, Nakano M, Terabe F, Kawahata H, Ohkawara T, Han Y, et al. The influence of excessive IL-6 production in vivo on the development and function of Foxp3+ regulatory T cells. J Immunol 2011; 186:32-40.
87. Fujimoto M, Serada S, Mihara M, Uchiyama Y, Yoshida H, Koike N, et al. Interleukin-6 blockade suppresses autoimmune arthritis in mice by the inhibition of inflammatory Th17 responses. Arthritis Rheum 2008; 58:3710-3719.
88. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, Asher TE, et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008; 112:2826-2835.
89. Nilsson J, Boasso A, Velilla PA, Zhang R, Vaccari M, Franchini G, et al. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood 2006; 108:3808-3817.
90. Mackewicz CE, Ortega H, Levy JA. Effect of cytokines on HIV replication in CD4+ lymphocytes: lack of identity with the CD8+ cell antiviral factor. Cell Immunol 1994; 153:329-343.
91. Barker E, Mackewicz CE, Levy JA. Effects of TH1 and TH2 cytokines on CD8+ cell response against human immunodeficiency virus: implications for long-term survival. Proc Natl Acad Sci U S A 1995; 92:11135-11139.
92. Chernoff AE, Granowitz EV, Shapiro L, Vannier E, Lonnemann G, Angel JB, et al. A randomized, controlled trial of IL-10 in humans. Inhibition of inflammatory cytokine production and immune responses. J Immunol 1995; 154:5492-5499.
93. Villacres MC, Kono N, Mack WJ, Nowicki MJ, Anastos K, Augenbraun M, et al. Interleukin 10 responses are associated with sustained CD4 T-cell counts in treated HIV infection. J Infect Dis 2012; 206:780-789.
94. Brockman MA, Kwon DS, Tighe DP, Pavlik DF, Rosato PC, Sela J, et al. IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virus-specific T cells. Blood 2009; 114:346-356.
95. Bouaziz JD, Le Buanec H, Saussine A, Bensussan A, Bagot M. IL-10 producing regulatory B cells in mice and humans: state of the art. Curr Mol Med 2012; 12:519-527.
96. Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz-Suano A, Kamanaka M, et al. Mice lacking endogenous IL-10-producing regulatoryB cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol 2011; 186:5569-5579.
97. DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 2010; 1183:38-57.
98. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011; 117:530-541.
99. Andersson J, Boasso A, Nilsson J, Zhang R, Shire NJ, Lindback S, et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J Immunol 2005; 174:3143-3147.
100. Schulze Zur Wiesch J, Thomssen A, Hartjen P, Toth I, Lehmann C, Meyer-Olson D, et al. Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3+ T regulatory cells correlates with progressive disease. J Virol 2011; 85:1287-1297.
101. Li C, Toth I, Schulze Zur Wiesch J, Pereyra F, Rychert J, Rosenberg ES, et al. Functional characterization of HLAG (+) regulatory T cells in HIV-1 infection. PLoS Pathog 2013; 9:e1003140.
102. 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; 85:12102-12113.