Immune activation and increased IL-21R expression are associated with the loss of memory B cells during HIV-1 infection

Journal of Internal Medicine

Volumn 272, Issue 5, 2012, Pages 492-503

  Ruffin, N ^a   Lantto, R ^a   Pensieroso, S ^a   Sammicheli, S ^a   Hejdeman, B ^b   Rethi, B ^a   Chiodi, F ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STOCKHOLM SÖDER HOSPITAL   (Sweden)

Author keywords

Apoptosis; Human immunodeficiency virus type 1; IL 21 receptor; Immune activation; Microbial translocation

Indexed keywords

CD14 ANTIGEN; CD38 ANTIGEN; INTERLEUKIN 21 RECEPTOR; LIPOPOLYSACCHARIDE; PROTEIN BCL 2; TOLL LIKE RECEPTOR;

APOPTOSIS; ARTICLE; BACTERIAL TRANSLOCATION; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOLOGICAL MEMORY; LYMPHOCYTE COUNT; MEMORY CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

AGE FACTORS; APOPTOSIS; B-LYMPHOCYTES; BACTERIAL TRANSLOCATION; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOCYTE ACTIVATION; RECEPTORS, INTERLEUKIN-21; SWEDEN;

EID: 84867907413     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/j.1365-2796.2012.02550.x     Document Type: Article

References (46)

1. Titanji K, De Milito A, Cagigi A et al. Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 2006; 108: 1580-7.
2. Geretti AM, Doyle T. Immunization for HIV-positive individuals. Curr Opin Infect Dis 2010; 23: 32-8.
3. Cagigi A, Nilsson A, Pensieroso S, Chiodi F. Dysfunctional B-cell responses during HIV-1 infection: implication for influenza vaccination and highly active antiretroviral therapy. Lancet Infect Dis 2010; 10: 499-503.
4. Moir S, Malaspina A, Ogwaro KM et al. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Nat Acad Sci USA 2001; 98: 10362-7.
5. 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: 453-8.
6. Muro-Cacho CA, Pantaleo G, Fauci AS. Analysis of apoptosis 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 1995; 154: 5555-66.
7. 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: 1031-8.
8. Moir S, Malaspina A, Pickeral OK 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: 587-99.
9. Moir S, Ho J, Malaspina A 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: 1797-805.
10. Shen X, Tomaras GD. Alterations of the B-cell response by HIV-1 replication. Curr HIV/AIDS Rep 2011; 8: 23-30.
11. He B, Qiao X, Klasse PJ 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: 3931-41.
12. 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: 302-10.
13. Brenchley JM, Price DA, Schacker TW et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12: 1365-71.
14. Marchetti G, Cozzi-Lepri A, Merlini E et al. Microbial translocation predicts disease progression of HIV-infected antiretroviral-naive patients with high CD4+ cell count. AIDS 2011; 25: 1385-94.
15. Moir S, Chun TW, Fauci AS. Pathogenic mechanisms of HIV disease. Annu Rev Pathol 2011; 6: 223-48.
16. Finkel TH, Tudor-Williams G, Banda NK et al. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1995; 1: 129-34.
17. Groux H, Torpier G, Monte D, Mouton Y, Capron A, Ameisen JC. Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med 1992; 175: 331-40.
18. Meyaard L, Otto SA, Jonker RR, Mijnster MJ, Keet RP, Miedema F. Programmed death of T cells in HIV-1 infection. Science 1992; 257: 217-9.
19. Sousa AE, Carneiro J, Meier-Schellersheim M, Grossman Z, Victorino RM. CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J Immunol 2002; 169: 3400-6.
20. Leng Q, Borkow G, Weisman Z, Stein M, Kalinkovich A, Bentwich Z. Immune activation correlates better than HIV plasma viral load with CD4 T-cell decline during HIV infection. J Acquir Immune Defic Syndr 2001; 27: 389-97.
21. Hunt PW, Brenchley J, Sinclair E et al. Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 2008; 197: 126-33.
22. Schacker TW, Nguyen PL, Martinez E et al. Persistent abnormalities in lymphoid tissues of human immunodeficiency virus-infected patients successfully treated with highly active antiretroviral therapy. J Infect Dis 2002; 186: 1092-7.
23. Badley AD, Parato K, Cameron DW et al. Dynamic correlation of apoptosis and immune activation during treatment of HIV infection. Cell Death Differ 1999; 6: 420-32.
24. Giorgi JV, Hultin LE, McKeating JA 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: 859-70.
25. Kuller LH, Tracy R, Belloso W et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 2008; 5: e203.
26. Yue FY, Lo C, Sakhdari A et al. 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 2010; 185: 498-506.
27. Chtanova T, Tangye SG, Newton R et al. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J Immunol 2004; 173: 68-78.
28. Konforte D, Simard N, Paige CJ. IL-21: an executor of B cell fate. J Immunol 2009; 182: 1781-7.
29. Good KL, Bryant VL, Tangye SG. Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J Immunol 2006; 177: 5236-47.
30. Avery DT, Deenick EK, Ma CS et al. B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J Exp Med 2010; 207: 155-71.
31. Ettinger R, Sims GP, Fairhurst AM et al. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 2005; 175: 7867-79.
32. Iannello A, Boulassel MR, Samarani S et al. Dynamics and consequences of IL-21 production in HIV-infected individuals: a longitudinal and cross-sectional study. J Immunol 2010; 184: 114-26.
33. Brenchley JM, Douek DC. The mucosal barrier and immune activation in HIV pathogenesis. Curr Opin HIV AIDS 2008; 3: 356-61.
34. Titanji K, Chiodi F, Bellocco R et al. Primary HIV-1 infection sets the stage for important B lymphocyte dysfunctions. AIDS 2005; 19: 1947-55.
35. De Milito A, Morch C, Sonnerborg A, Chiodi F. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 2001; 15: 957-64.
36. Iannello A, Tremblay C, Routy JP, Boulassel MR, Toma E, Ahmad A. Decreased levels of circulating IL-21 in HIV-infected AIDS patients: correlation with CD4+ T-cell counts. Viral Immunol 2008; 21: 385-8.
37. Lund FE, Cockayne DA, Randall TD, Solvason N, Schuber F, Howard MC. CD38: a new paradigm in lymphocyte activation and signal transduction. Immunol Rev 1998; 161: 79-93.
38. O'Connor L, Strasser A, O'Reilly LA et al. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J 1998; 17: 384-95.
39. Gowda A, Roda J, Hussain SR et al. IL-21 mediates apoptosis through up-regulation of the BH3 family member BIM and enhances both direct and antibody-dependent cellular cytotoxicity in primary chronic lymphocytic leukemia cells in vitro. Blood 2008; 111: 4723-30.
40. Chiodi F. New therapy to revert dysfunctional antibody responses during HIV-1 infection. J Clin Invest 2010; 120: 3810-3.
41. van Grevenynghe J, Cubas RA, Noto A et al. Loss of memory B cells during chronic HIV infection is driven by Foxo3a- and TRAIL-mediated apoptosis. J Clin Invest 2011; 121: 3877-88.
42. Mascola JR, Montefiori DC. The role of antibodies in HIV vaccines. Annu Rev Immunol 2010; 28: 413-44.
43. Lewis GK. Challenges of antibody-mediated protection against HIV-1. Expert Rev Vaccines 2010; 9: 683-7.
44. Ettinger R, Kuchen S, Lipsky PE. The role of IL-21 in regulating B-cell function in health and disease. Immunol Rev 2008; 223: 60-86.
45. Bessa J, Kopf M, Bachmann MF. Cutting edge: IL-21 and TLR signaling regulate germinal center responses in a B cell-intrinsic manner. J Immunol 2010; 184: 4615-9.
46. Pantaleo G, Graziosi C, Demarest JF et al. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 1993; 362: 355-8.