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HIV-associated immune dysfunction and viral infection: role in the pathogenesis of AIDS-related lymphoma

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Abstract

HIV infection is associated with a much higher risk for the development of non-Hodgkin lymphoma (AIDS-NHL). The principal causes of lymphomagenesis in HIV-infected individuals are thought to be the loss of immune function seen in HIV infection, which results in the loss of immunoregulation of Epstein–Barr virus-infected B cells, as well as HIV infection-associated immune dysregulation, including chronic B-cell activation. In this review, we discuss recent reports that further support the importance of these factors, and we highlight emerging evidence of different mechanisms that potentially drive lymphomagenesis in HIV-infected individuals.

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References

  1. Grulich AE, van Leeuwen MT, Falster MO, et al. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet. 2007;370:59–67.

    Article  PubMed  Google Scholar 

  2. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR Recomm Rep. 1992;41:1–19.

  3. Raphaël M, Said J, Borish B, et al. Lymphomas associated with HIV infection. In: Swerdlow SH, Campo E, Harris NL, et al., editors. WHO classification of tumors of the haematopoietic and lymphoid tissues. Lyon: IARC; 2008.

    Google Scholar 

  4. Carbone A, Cesarman E, Spina M, et al. HIV-associated lymphomas and gamma-herpesviruses. Blood. 2009;113:1213–24.

    Article  PubMed  CAS  Google Scholar 

  5. Klein G, Klein E, Kashuba E. Interaction of Epstein-Barr virus (EBV) with human B-lymphocytes. Biochem Biophys Res Commun. 2010;396:67–73.

    Article  PubMed  CAS  Google Scholar 

  6. Bornkamm GW. Epstein-Barr virus and the pathogenesis of Burkitt’s lymphoma: more questions than answers. Int J Cancer. 2009;124:1745–55.

    Article  PubMed  CAS  Google Scholar 

  7. Klapproth K, Wirth T. Advances in the understanding of MYC-induced lymphomagenesis. Br J Haematol. 2010;149:484–97.

    Article  PubMed  CAS  Google Scholar 

  8. Polo JM, Juszczynski P, Monti S, et al. Transcriptional signature with differential expression of BCL6 target genes accurately identifies BCL6-dependent diffuse large B cell lymphomas. Proc Natl Acad Sci USA. 2007;104:3207–12.

    Article  PubMed  CAS  Google Scholar 

  9. Deffenbacher KE, Iqbal J, Liu Z, et al. Recurrent chromosomal alterations in molecularly classified AIDS-related lymphomas: an integrated analysis of DNA copy number and gene expression. J Acquir Immune Defic Syndr. 2010;54:18–26.

    Article  PubMed  Google Scholar 

  10. Martinez-Maza O, Crabb E, Mitsuyasu RT, et al. Infection with the human immunodeficiency virus (HIV) is associated with an in vivo increase in B lymphocyte activation and immaturity. J Immunol. 1987;138:3720–4.

    PubMed  CAS  Google Scholar 

  11. Pasqualucci L, Bhagat G, Jankovic M, et al. AID is required for germinal center-derived lymphomagenesis. Nat Genet. 2008;40:108–12.

    Article  PubMed  CAS  Google Scholar 

  12. Robbiani DF, Bunting S, Feldhahn N, et al. AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol Cell. 2009;36:631–41.

    Article  PubMed  CAS  Google Scholar 

  13. Epeldegui M, Breen EC, Hung YP, et al. Elevated expression of activation induced cytidine deaminase in peripheral blood mononuclear cells precedes AIDS-NHL diagnosis. AIDS. 2007;21:2265–70.

    Article  PubMed  CAS  Google Scholar 

  14. Landgren O, Goedert JJ, Rabkin CS, et al. Circulating serum free light chains as predictive markers of AIDS-related lymphoma. J Clin Oncol. 2010;28:773–9.

    Article  PubMed  CAS  Google Scholar 

  15. Gottenberg JE, Aucouturier F, Goetz J, et al. Serum immunoglobulin free light chain assessment in rheumatoid arthritis and primary Sjogren’s syndrome. Ann Rheum Dis. 2007;66:23–7.

    Article  PubMed  CAS  Google Scholar 

  16. Martin W, Abraham R, Shanafelt T, et al. Serum-free light chain-a new biomarker for patients with B-cell non-Hodgkin lymphoma and chronic lymphocytic leukemia. Transl Res. 2007;149:231–5.

    Article  PubMed  CAS  Google Scholar 

  17. Terrier B, Sene D, Saadoun D, et al. Serum-free light chain assessment in hepatitis C virus-related lymphoproliferative disorders. Ann Rheum Dis. 2009;68:89–93.

    Article  PubMed  CAS  Google Scholar 

  18. Breen EC, Fatahi S, Epeldegui M, et al. Elevated serum soluble CD30 precedes the development of AIDS-associated non-Hodgkin’s B cell lymphoma. Tumour Biol. 2006;27:187–94.

    Article  PubMed  CAS  Google Scholar 

  19. Widney D, Gundapp G, Said JW, et al. Aberrant expression of CD27 and soluble CD27 (sCD27) in HIV infection and in AIDS-associated lymphoma. Clin Immunol. 1999;93:114–23.

    Article  PubMed  CAS  Google Scholar 

  20. Chiarle R, Podda A, Prolla G, et al. CD30 in normal and neoplastic cells. Clin Immunol. 1999;90:157–64.

    Article  PubMed  CAS  Google Scholar 

  21. van Oers MH, Pals ST, Evers LM, et al. Expression and release of CD27 in human B-cell malignancies. Blood. 1993;82:3430–6.

    PubMed  Google Scholar 

  22. De Milito A, Morch C, Sonnerborg A, et al. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS. 2001;15:957–64.

    Article  PubMed  Google Scholar 

  23. Breen EC, Epeldegui M, Boscardin WJ, et al. Elevated levels of soluble CD44 precede the development of AIDS-associated non-Hodgkin’s B-cell lymphoma. Aids. 2005;19:1711–2.

    Article  PubMed  Google Scholar 

  24. Navarro JT, Ribera JM, Vaquero M, et al. Increased serum levels of CD44s and CD44v6 in patients with AIDS-related non-Hodgkin’s lymphoma. AIDS. 2000;14:1460–1.

    Article  PubMed  CAS  Google Scholar 

  25. Yawetz S, Cumberland WG, van der Meyden M, et al. Elevated serum levels of soluble CD23 (sCD23) precede the appearance of acquired immunodeficiency syndrome–associated non-Hodgkin’s lymphoma. Blood. 1995;85:1843–9.

    PubMed  CAS  Google Scholar 

  26. Schroeder JR, Saah AJ, Hoover DR, et al. Serum soluble CD23 level correlates with subsequent development of AIDS-related non-Hodgkin’s lymphoma. Cancer Epidemiol Biomarkers Prev. 1999;8:979–84.

    PubMed  CAS  Google Scholar 

  27. Schroeder JR, Saah AJ, Ambinder RF, et al. Serum sCD23 level in patients with AIDS-related non-Hodgkin’s lymphoma is associated with absence of Epstein-Barr virus in tumor tissue. Clin Immunol. 1999;93:239–44.

    Article  PubMed  CAS  Google Scholar 

  28. Gordon J, Millsum MJ, Flores-Romo L, et al. Regulation of resting and cycling human B lymphocytes via surface IgM and the accessory molecules interleukin-4, CD23 and CD40. Immunology. 1989;68:526–31.

    PubMed  CAS  Google Scholar 

  29. Gordon J, Flores-Romo L, Cairns JA, et al. CD23: a multi-functional receptor/lymphokine? Immunol Today. 1989;10:153–7.

    Article  PubMed  CAS  Google Scholar 

  30. Herbelin A, Elhadad S, Ouaaz F, et al. Soluble CD23 potentiates interleukin-1-induced secretion of interleukin-6 and interleukin-1 receptor antagonist by human monocytes. Eur J Immunol. 1994;24:1869–73.

    Article  PubMed  CAS  Google Scholar 

  31. Breen EC, van der Meijden M, Cumberland W, et al. The development of AIDS-associated Burkitt’s/small noncleaved cell lymphoma is preceded by elevated serum levels of interleukin 6. Clin Immunol. 1999;92:293–9.

    Article  PubMed  CAS  Google Scholar 

  32. Pluda JM, Venzon DJ, Tosato G, et al. Parameters affecting the development of non-Hodgkin’s lymphoma in patients with severe human immunodeficiency virus infection receiving antiretroviral therapy. J Clin Oncol. 1993;11:1099–107.

    PubMed  CAS  Google Scholar 

  33. Burdin N, Van Kooten C, Galibert L, et al. Endogenous IL-6 and IL-10 contribute to the differentiation of CD40-activated human B lymphocytes. J Immunol. 1995;154:2533–44.

    PubMed  CAS  Google Scholar 

  34. Widney DP, Breen EC, Boscardin WJ, et al. Serum levels of the homeostatic B cell chemokine, CXCL13, are elevated during HIV infection. J Interferon Cytokine Res. 2005;25:702–6.

    Article  PubMed  CAS  Google Scholar 

  35. Cagigi A, Mowafi F, Phuong Dang LV, et al. Altered expression of the receptor-ligand pair CXCR5/CXCL13 in B cells during chronic HIV-1 infection. Blood. 2008;112:4401–10.

    Article  PubMed  CAS  Google Scholar 

  36. Widney DP, Gui D, Popoviciu LM, et al. Expression of the B cell chemokine, CXCL13, in AIDS-associated non-Hodgkin’s lymphoma. AIDS Res Treat. 2010 (in press).

  37. Hussain SK, Widney D, Jacobson L, et al. Elevated serum levels of CXCL13 precede HIV-associated non Hodgkin’s lymphoma: 12th international conference on malignancies in aids and other acquired immunodeficiencies (ICMAOI). Bethesda, Maryland: National Cancer Institute; 2010.

  38. Fischer L, Korfel A, Pfeiffer S, et al. CXCL13 and CXCL12 in central nervous system lymphoma patients. Clin Cancer Res. 2009;15:5968–73.

    Article  PubMed  CAS  Google Scholar 

  39. Levin LI, Breen EC, Kitchen CR, et al. Elevated serum levels of CXCL13 precede the diagnosis of B cells non-Hodgkin lymphoma (NHL): the future of molecular epidemiology: new tools, biomarkers, and opportunities. Miami, FL: American Association for Cancer Research; 2010, 45 PR41.

  40. Breen EC, Boscardin WJ, Detels R, et al. Non-Hodgkin’s B cell lymphoma in persons with acquired immunodeficiency syndrome is associated with increased serum levels of IL10, or the IL10 promoter-592 C/C genotype. Clin Immunol. 2003;109:119–29.

    Article  PubMed  CAS  Google Scholar 

  41. Wong HL, Breen EC, Pfeiffer RM, et al. Cytokine signaling pathway polymorphisms and AIDS-related non-Hodgkin lymphoma risk in the multicenter AIDS cohort study. AIDS. 2010;24:1025–33.

    Article  PubMed  CAS  Google Scholar 

  42. Sasson SC, Smith S, Seddiki N, et al. IL-7 receptor is expressed on adult pre-B-cell acute lymphoblastic leukemia and other B-cell derived neoplasms and correlates with expression of proliferation and survival markers. Cytokine. 2010;50:58–68.

    Article  PubMed  CAS  Google Scholar 

  43. Aissani B, Ogwaro KM, Shrestha S, et al. The major histocompatibility complex conserved extended haplotype 8.1 in AIDS-related non-Hodgkin lymphoma. J Acquir Immune Defic Syndr. 2009;52:170–9.

    Article  PubMed  CAS  Google Scholar 

  44. Patke CL, Shearer WT. gp120- and TNF-alpha-induced modulation of human B cell function: proliferation, cyclic AMP generation, Ig production, and B-cell receptor expression. J Allergy Clin Immunol. 2000;105:975–82.

    Article  PubMed  CAS  Google Scholar 

  45. Romagnani S, Maggi E, Liotta F, et al. Properties and origin of human Th17 cells. Mol Immunol. 2009;47:3–7.

    Article  PubMed  CAS  Google Scholar 

  46. Takagi R, Higashi T, Hashimoto K, et al. B cell chemoattractant CXCL13 is preferentially expressed by human Th17 cell clones. J Immunol. 2008;181:186–9.

    PubMed  CAS  Google Scholar 

  47. Kryczek I, Wei S, Zou L, et al. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J Immunol. 2007;178:6730–3.

    PubMed  CAS  Google Scholar 

  48. Ekstrom Smedby K, Vajdic CM, Falster M, et al. Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph Consortium. Blood. 2008;111:4029–38.

    Article  PubMed  CAS  Google Scholar 

  49. Croft M. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol. 2003;3:609–20.

    Article  PubMed  CAS  Google Scholar 

  50. Romagnani S. Th1/Th2 cells. Inflamm Bowel Dis. 1999;5:285–94.

    Article  PubMed  CAS  Google Scholar 

  51. Fiorentino DF, Bond MW, Mosmann TR. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med. 1989;170:2081–95.

    Article  PubMed  CAS  Google Scholar 

  52. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med. 2007;13:139–45.

    Article  PubMed  CAS  Google Scholar 

  53. Ji Y, Zhang W. Th17 cells: positive or negative role in tumor? Cancer Immunol Immunother. 2010;59:979–87.

    Article  PubMed  Google Scholar 

  54. Kim CH, Lim HW, Kim JR, et al. Unique gene expression program of human germinal center T helper cells. Blood. 2004;104:1952–60.

    Article  PubMed  CAS  Google Scholar 

  55. Vissers JL, Hartgers FC, Lindhout E, et al. BLC (CXCL13) is expressed by different dendritic cell subsets in vitro and in vivo. Eur J Immunol. 2001;31:1544–9.

    Article  PubMed  CAS  Google Scholar 

  56. Huysentruyt LC, McGrath MS. The role of macrophages in the development and progression of AIDS-related non-Hodgkin lymphoma. J Leukoc Biol. 2010;87:627–32.

    Article  PubMed  CAS  Google Scholar 

  57. van Baarle D, Hovenkamp E, Callan MF, et al. Dysfunctional Epstein-Barr virus (EBV)-specific CD8(+) T lymphocytes and increased EBV load in HIV-1 infected individuals progressing to AIDS-related non-Hodgkin lymphoma. Blood. 2001;98:146–55.

    Article  PubMed  Google Scholar 

  58. Kinlen L. Immunosuppression and cancer. In: Vainio H, Magee PN, McGregor DB, McMichael AJ, editors. Mechanisms of carcinogenesis in risk identification. Lyon: International Agency for Research on Cancer; 1992. p. 237–53.

    Google Scholar 

  59. Vajdic CM, McDonald SP, McCredie MR, et al. Cancer incidence before and after kidney transplantation. JAMA. 2006;296:2823–31.

    Article  PubMed  CAS  Google Scholar 

  60. Gaidano G, Capello D, Carbone A. The molecular basis of acquired immunodeficiency syndrome-related lymphomagenesis. Semin Oncol. 2000;27:431–41.

    PubMed  CAS  Google Scholar 

  61. Biggar RJ, Chaturvedi AK, Goedert JJ, et al. AIDS-related cancer and severity of immunosuppression in persons with AIDS. J Natl Cancer Inst. 2007;99:962–72.

    Article  PubMed  Google Scholar 

  62. Klein U, Klein G, Ehlin-Henriksson B, et al. Burkitt’s lymphoma is a malignancy of mature B cells expressing somatically mutated V region genes. Mol Med. 1995;1:495–505.

    PubMed  CAS  Google Scholar 

  63. Chapman CJ, Wright D, Stevenson FK. Insight into Burkitt’s lymphoma from immunoglobulin variable region gene analysis. Leuk Lymphoma. 1998;30:257–67.

    PubMed  CAS  Google Scholar 

  64. Bellan C, Lazzi S, Hummel M, et al. Immunoglobulin gene analysis reveals 2 distinct cells of origin for EBV-positive and EBV-negative Burkitt lymphomas. Blood. 2005;106:1031–6.

    Article  PubMed  CAS  Google Scholar 

  65. Kurth J, Hansmann ML, Rajewsky K, et al. Epstein-Barr virus-infected B cells expanding in germinal centers of infectious mononucleosis patients do not participate in the germinal center reaction. Proc Natl Acad Sci USA. 2003;100:4730–5.

    Article  PubMed  CAS  Google Scholar 

  66. Kurth J, Spieker T, Wustrow J, et al. EBV-infected B cells in infectious mononucleosis: viral strategies for spreading in the B cell compartment and establishing latency. Immunity. 2000;13:485–95.

    Article  PubMed  CAS  Google Scholar 

  67. Bornkamm GW. Epstein-Barr virus and its role in the pathogenesis of Burkitt’s lymphoma: an unresolved issue. Semin Cancer Biol. 2009;19:351–65.

    Article  PubMed  CAS  Google Scholar 

  68. Souza TA, Stollar BD, Sullivan JL, et al. Influence of EBV on the peripheral blood memory B cell compartment. J Immunol. 2007;179:3153–60.

    PubMed  CAS  Google Scholar 

  69. Souza TA, Stollar BD, Sullivan JL, et al. Peripheral B cells latently infected with Epstein-Barr virus display molecular hallmarks of classical antigen-selected memory B cells. Proc Natl Acad Sci USA. 2005;102:18093–8.

    Article  PubMed  CAS  Google Scholar 

  70. Epeldegui M, Hung YP, McQuay A, et al. Infection of human B cells with Epstein-Barr virus results in the expression of somatic hypermutation-inducing molecules and in the accrual of oncogene mutations. Mol Immunol. 2007;44:934–42.

    Article  PubMed  CAS  Google Scholar 

  71. He B, Raab-Traub N, Casali P, et al. EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching. J Immunol. 2003;171:5215–24.

    PubMed  CAS  Google Scholar 

  72. Gil Y, Levy-Nabot S, Steinitz M, et al. Somatic mutations and activation-induced cytidine deaminase (AID) expression in established rheumatoid factor-producing lymphoblastoid cell line. Mol Immunol. 2007;44:494–505.

    Article  PubMed  CAS  Google Scholar 

  73. Tobollik S, Meyer L, Buettner M, et al. Epstein-Barr virus nuclear antigen 2 inhibits AID expression during EBV-driven B-cell growth. Blood. 2006;108:3859–64.

    Article  PubMed  CAS  Google Scholar 

  74. Canaan A, Haviv I, Urban AE, et al. EBNA1 regulates cellular gene expression by binding cellular promoters. Proc Natl Acad Sci USA. 2009;106:22421–6.

    Article  PubMed  Google Scholar 

  75. De Falco G, Antonicelli G, Onnis A, et al. Role of EBV in microRNA dysregulation in Burkitt lymphoma. Semin Cancer Biol. 2009;19:401–6.

    Article  PubMed  CAS  Google Scholar 

  76. Mrazek J, Kreutmayer SB, Grasser FA, et al. Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res. 2007;35:73.

    Article  CAS  Google Scholar 

  77. Cai X, Schafer A, Lu S, et al. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2006;2:23.

    Article  CAS  Google Scholar 

  78. Grundhoff A, Sullivan CS, Ganem D. A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA. 2006;12:733–50.

    Article  PubMed  CAS  Google Scholar 

  79. Xia T, O’Hara A, Araujo I, et al. EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1–3. Cancer Res. 2008;68:1436–42.

    Article  PubMed  CAS  Google Scholar 

  80. Leucci E, Onnis A, Cocco M, et al. B-cell differentiation in EBV-positive Burkitt lymphoma is impaired at posttranscriptional level by miRNA-altered expression. Int J Cancer. 2010;126:1316–26.

    PubMed  CAS  Google Scholar 

  81. Yang R, Murillo FM, Delannoy MJ, et al. B lymphocyte activation by human papillomavirus-like particles directly induces Ig class switch recombination via TLR4-MyD88. J Immunol. 2005;174:7912–9.

    PubMed  CAS  Google Scholar 

  82. Machida K, Cheng KT, Sung VM, et al. Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc Natl Acad Sci USA. 2004;101:4262–7.

    Article  PubMed  CAS  Google Scholar 

  83. Zuckerman E, Zuckerman T, Levine AM, et al. Hepatitis C virus infection in patients with B-cell non-Hodgkin lymphoma. Ann Intern Med. 1997;127:423–8.

    PubMed  CAS  Google Scholar 

  84. Ito M, Mizoroki F, Takai K, et al. Functional phenotypes and gene expression profiles of peripheral blood mononuclear cells in chronic hepatitis C patients who developed non-Hodgkin’s B-cell lymphoma. Biochem Biophys Res Commun. 2009;390:269–72.

    Article  PubMed  CAS  Google Scholar 

  85. Chaturvedi AK, Kleinerman RA, Hildesheim A, et al. Second cancers after squamous cell carcinoma and adenocarcinoma of the cervix. J Clin Oncol. 2009;27:967–73.

    Article  PubMed  Google Scholar 

  86. Zoufaly A, Stellbrink HJ, Heiden MA, et al. Cumulative HIV viremia during highly active antiretroviral therapy is a strong predictor of AIDS-related lymphoma. J Infect Dis. 2009;200:79–87.

    Article  PubMed  Google Scholar 

  87. Schnittman SM, Lane HC, Higgins SE, et al. Direct polyclonal activation of human B lymphocytes by the acquired immune deficiency syndrome virus. Science. 1986;233:1084–6.

    Article  PubMed  CAS  Google Scholar 

  88. 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.

    PubMed  CAS  Google Scholar 

  89. Kundu RK, Sangiorgi F, Wu LY, et al. Expression of the human immunodeficiency virus-Tat gene in lymphoid tissues of transgenic mice is associated with B-cell lymphoma. Blood. 1999;94:275–82.

    PubMed  CAS  Google Scholar 

  90. Martin G, Roy J, Barat C, et al. Human immunodeficiency virus type 1-associated CD40 ligand transactivates B lymphocytes and promotes infection of CD4+ T cells. J Virol. 2007;81:5872–81.

    Article  PubMed  CAS  Google Scholar 

  91. Epeldegui M, Thapa DR, Kitchen S, et al. CD40 ligand (CD154) incorporated into HIV virions induces activation-induced cytidine deaminase (AID) expression in human B lymphocytes. PLos One. 2010;5:e11448.

    Article  PubMed  CAS  Google Scholar 

  92. Kolar GR, Mehta D, Pelayo R, et al. A novel human B cell subpopulation representing the initial germinal center population to express AID. Blood. 2007;109:2545–52.

    Article  PubMed  CAS  Google Scholar 

  93. Ott DE. Cellular proteins in HIV virions. Rev Med Virol. 1997;7:167–80.

    Article  PubMed  CAS  Google Scholar 

  94. Meerloo T, Parmentier HK, Osterhaus AD, et al. Modulation of cell surface molecules during HIV-1 infection of H9 cells. An immunoelectron microscopic study. Aids. 1992;6:1105–16.

    Article  PubMed  CAS  Google Scholar 

  95. Scholl PR, Geha RS. MHC class II signaling in B-cell activation. Immunol Today. 1994;15:418–22.

    Article  PubMed  CAS  Google Scholar 

  96. Palacios R, Martinez-Maza O, Guy K. Monoclonal antibodies against HLA-DR antigens replace T helper cells in activation of B lymphocytes. Proc Natl Acad Sci USA. 1983;80:3456–60.

    Article  PubMed  CAS  Google Scholar 

  97. Esser MT, Graham DR, Coren LV, et al. Differential incorporation of CD45, CD80 (B7–1), CD86 (B7–2), and major histocompatibility complex class I and II molecules into human immunodeficiency virus type 1 virions and microvesicles: implications for viral pathogenesis and immune regulation. J Virol. 2001;75:6173–82.

    Article  PubMed  CAS  Google Scholar 

  98. Widney D, Boscardin WJ, Kasravi A, et al. Expression and function of CD28 on Epstein-Barr virus-positive B cell lines and AIDS-associated non-Hodgkin’s lymphoma cell lines. Tumour Biol. 2003;24:82–93.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Microbiology, Immunology & Molecular Genetics, UCLA AIDS Institute, Los Angeles, CA, USA

    Marta Epeldegui & Otoniel Martínez-Maza

  2. Department of Obstetrics & Gynecology, David Geffen School of Medicine at UCLA, UCLA AIDS Institute, Los Angeles, CA, USA

    Elena Vendrame & Otoniel Martínez-Maza

  3. Department of Epidemiology, UCLA School of Public Health, UCLA AIDS Institute, Los Angeles, CA, USA

    Otoniel Martínez-Maza

  4. BSRB 173, 615 Charles E. Young Drive South, Los Angeles, CA, 90095-7363, USA

    Otoniel Martínez-Maza

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  1. Marta Epeldegui
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  2. Elena Vendrame
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  3. Otoniel Martínez-Maza
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Correspondence to Otoniel Martínez-Maza.

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Marta Epeldegui and Elena Vendrame contributed equally to this work.

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Epeldegui, M., Vendrame, E. & Martínez-Maza, O. HIV-associated immune dysfunction and viral infection: role in the pathogenesis of AIDS-related lymphoma. Immunol Res 48, 72–83 (2010). https://doi.org/10.1007/s12026-010-8168-8

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