Decreased survival of B cells of HIV-viremic patients mediated by altered expression of receptors of the TNF superfamily

Journal of Experimental Medicine

Volumn 200, Issue 5, 2004, Pages 587-599

  Moir, Susan ^a   Malaspina, Angela ^a   Pickeral, Oxana K ^b   Donoghue, Eileen T ^a   Vasquez, Joshua ^a   Miller, Natalie J ^a   Krishnan, Surekha R ^b   Planta, Marie A ^a   Turney, John F ^a   Justement, J Shawn ^a   Kottilil, Shyamasundaran ^a   Dybul, Mark ^a   Mican, JoAnn M ^a   Kovacs, Colin ^c   Chun, Tae Wook ^a   Birse, Charles E ^b   Fauci, Anthony S ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b GLAXOSMITHKLINE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Gene expression; Immune activation; Interferon; Microarray; Terminal differentiation

Indexed keywords

COMPLEMENT COMPONENT C3D RECEPTOR; FAS ANTIGEN; INTERFERON; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR; B CELL ACTIVATING FACTOR RECEPTOR; B CELL MATURATION ANTIGEN; MEMBRANE PROTEIN; TNFRSF13C PROTEIN, HUMAN; TNFRSF17 PROTEIN, HUMAN;

ANTIGENICITY; ARTICLE; B LYMPHOCYTE; CELL DEATH; CELL DENSITY; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA MICROARRAY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VIREMIA; VIRUS REPLICATION; APOPTOSIS; BIOSYNTHESIS; BLOOD; CELL MEMBRANE; COMPARATIVE STUDY; GENE EXPRESSION PROFILING; IMMUNOLOGY; METABOLISM; VIROLOGY;

ADP-RIBOSYL CYCLASE; ANTIGENS, CD; ANTIGENS, CD38; ANTIGENS, CD95; APOPTOSIS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MEMBRANE; CELL SEPARATION; FLOW CYTOMETRY; HIV INFECTIONS; HIV SEROPOSITIVITY; HUMANS; INTERFERONS; MEMBRANE GLYCOPROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; RECEPTORS, COMPLEMENT 3D; UP-REGULATION; B-CELL ACTIVATION FACTOR RECEPTOR; B-CELL MATURATION ANTIGEN; GENE EXPRESSION PROFILING; MEMBRANE PROTEINS; RECEPTORS, TUMOR NECROSIS FACTOR;

EID: 4544264445     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20032236     Document Type: Article

References (71)

1. Grossman, Z., M. Meier-Schellersheim, A.E. Sousa, R.M. Victorino, and W.E. Paul. 2002. CD41 T-cell depletion in HIV infection: are we closer to understanding the cause? Nat. Med. 8:319-323.
2. Hazenberg, M.D., D. Hamann, H. Schuitemaker, and F. Miedema. 2000. T cell depletion in HIV-1 infection: how CD4+ T cells go out of stock. Nat. Immunol. 1:285-289.
3. Pantaleo, G., and A.S. Fauci. 1995. New concepts in the immunopathogenesis of HIV infection. Annu. Rev. Immunol. 13:487-512.
4. Moir, S., A. Malaspina, Y. Li, T.W. Chun, T. Lowe, J. Adelsberger, M. Baseler, L.A. Ehler, S. Liu, R.T. Davey, et al. 2000. B cells of HIV-1-infected patients bind virions through CD21-complement interactions and transmit infectious virus to activated T cells. J. Exp. Med. 192:637-646.
5. Pahwa, R., R.A. Good, and S. Pahwa. 1987. Prematurity, hypogammaglobulinemia, and neuropathology with human immunodeficiency virus (HIV) infection. Proc. Natl. Acad. Sci. USA. 84:3826-3830.
6. Morris, L., J.M. Binley, B.A. Clas, S. Bonhoeffer, T.P. Astill, R. Kost, A. Hurley, Y. Cao, M. Markowitz, D.D. Ho, and J.P. Moore. 1998. HIV-1 antigen-specific and -nonspecific B cell responses are sensitive to combination antiretroviral therapy. J. Exp. Med. 188:233-245.
7. Shirai, A., M. Cosentino, S.F. Leitman-Klinman, and D.M. Klinman. 1992. Human immunodeficiency virus infection induces both polyclonal and virus-specific B cell activation. J. Clin. Invest. 89:561-566.
8. Forster, R., G. Schweigard, S. Johann, T. Emrich, E. Kremmer, C. Nerl, and M. Lipp. 1997. Abnormal expression of the B-cell homing chemokine receptor BLR1 during the progression of acquired immunodeficiency syndrome. Blood. 90:520-525.
9. Moir, S., A. Malaspina, K.M. Ogwaro, E.T. Donoghue, C.W. Hallahan, L.A. Ehler, S. Liu, J. Adelsberger, R. Lapointe, P. Hwu, et al. 2001. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc. Natl. Acad. Sci. USA. 98:10362-10367.
10. Malaspina, A., S. Moir, S. Kottilil, C.W. Hallahan, L.A. Ehler, S. Liu, M.A. Planta, T.W. Chun, and A.S. Fauci. 2003. Deleterious effect of HIV-1 plasma viremia on B cell costimulatory function. J. Immunol. 170:5965-5972.
11. Amadori, A., A. De Rossi, G.P. Faulkner-Valle, and L. Chieco-Bianchi. 1988. Spontaneous in vitro production of virus-specific antibody by lymphocytes from HIV-infected subjects. Clin. Immunol. Immunopathol. 46:342-351.
12. Lane, H.C., H. Masur, L.C. Edgar, G. Whalen, A.H. Rook, and A.S. Fauci. 1983. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 309:453-458.
13. Miedema, F., A.J. Petit, F.G. Terpstra, J.K. Schattenkerk, F. de Wolf, B.J. Al, M. Roos, J.M. Lange, S.A. Danner, J. Goudsmit, et al. 1988. Immunological abnormalities in human immunodeficiency virus (HIV)-infected asymptomatic homosexual men. HIV affects the immune system before CD41 T helper cell depletion occurs. J. Clin. Invest. 82:1908-1914.
14. Ballet, J.J., G. Sulcebe, L.J. Couderc, F. Danon, C. Rabian, M. Lathrop, J.P. Clauvel, and M. Seligmann. 1987. Impaired anti-pneumococcal antibody response in patients with AIDS-related persistent generalized lymphadenopathy. Clin. Exp. Immunol. 68:479-487.
15. Conge, A.M., K. Tarte, J. Reynes, M. Segondy, J. Gerfaux, M. Zembala, and J.P. Vendrell. 1998. Impairment of B-lymphocyte differentiation induced by dual triggering of the B-cell antigen receptor and CD40 in advanced HIV-1-disease. AIDS. 12:1437-1449.
16. Moir, S., K.M. Ogwaro, A. Malaspina, J. Vasquez, E.T. Donoghue, C.W. Hallahan, S. Liu, L.A. Ehler, M.A. Planta, S. Kottilil, et al. 2003. Perturbations in B cell responsiveness to CD41 T cell help in HIV-infected individuals. Proc. Natl. Acad. Sci. USA. 100:6057-6062.
17. Muro-Cacho, C.A., G. Pantaleo, and A.S. Fauci. 1995. 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. 154:5555-5566.
18. Samuelsson, A., A. Sonnerborg, N. Heuts, J. Coster, and F. Chiodi. 1997. Progressive B cell apoptosis and expression of Fas ligand during human immunodeficiency virus type 1 infection. AIDS Res. Hum. Retroviruses. 13:1031-1038.
19. Jacobson, M.A., H. Khayam-Bashi, J.N. Martin, D. Black, and V. Ng. 2002. Effect of long-term highly active antiretroviral therapy in restoring HIV-induced abnormal B-lymphocyte function. J Acquir. Immune Defic. Syndr. 31:472-477.
20. Horvath, A., D. Banhegyi, A. Biro, E. Ujhelyi, A. Veres, L. Horvath, Z. Prohaszka, A. Bacsi, V. Tarjan, L. Romics, et al. 2001. High level of anticholesterol antibodies (ACHA) in HIV patients. Normalization of serum ACHA concentration after introduction of HAART. Immunobiology. 203:756-768.
21. Notermans, D.W., J.J. de Jong, J. Goudsmit, M. Bakker, M.T. Roos, L. Nijholt, J. Cremers, J.A. Hellings, S.A. Danner, and A. de Ronde. 2001. Potent antiretroviral therapy initiates normalization of hypergammaglobulinemia and a decline in HIV type 1-specific antibody responses. AIDS Res. Hum. Retroviruses. 17:1003-1008.
22. Taoufik, Y., I. Peguillet, M.G. de Goer, M. Lambert, B. Gubler, A. Trylesinski, J.F. Delfraissy, and O. Lantz. 2001. Effect of highly active antiretroviral therapy on expression of interleukin-10 and interleukin-12 in HIV-infected patients. J. Acquir. Immune Defic. Syndr. 26:303-304.
23. De Milito, A., A. Nilsson, K. Titanji, R. Thorstensson, E. Reizenstein, M. Narita, S. Grutzmeier, A. Sonnerborg, and F. Chiodi. 2003. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood. 103:2180-2186.
24. Tedder, T.F., L.T. Clement, and M.D. Cooper. 1984. Expression of C3d receptors during human B cell differentiation: immunofluorescence analysis with the HB-5 monoclonal antibody. J. Immunol. 133:678-683.
25. Makar, K.W., C.T. Pham, M.H. Dehoff, S.M. O'Connor, S.M. Jacobi, and V.M. Holers. 1998. An intronic silencer regulates B lymphocyte cell- and stage-specific expression of the human complement receptor type 2 (CR2, CD21) gene. J. Immunol. 160:1268-1278.
26. Sung, C., B. Nardelli, D.W. LaFleur, E. Blatter, M. Corcoran, H.S. Olsen, C.E. Birse, O.K. Pickeral, J. Zhang, D. Shah, et al. 2003. An IFN-beta-albumin fusion protein that displays improved pharmacokinetic and pharmacodynamic properties in nonhuman primates. J. Interferon Cytokine Res. 23:25-36.
27. Neale, G.A., and G.R. Kitchingman. 1991. mRNA transcripts initiating within the human immunoglobulin mu heavy chain enhancer region contain a non-translatable exon and are extremely heterogeneous at the 59 end. Nucleic Acids Res. 19:2427-2433.
28. Klein, U., Y. Tu, G.A. Stolovitzky, J.L. Keller, J. Haddad Jr., V. Miljkovic, G. Cattoretti, A. Califano, and R. Dalla-Favera. 2003. Transcriptional analysis of the B cell germinal center reaction. Proc. Natl. Acad. Sci. USA. 100:2639-2644.
29. Meffre, E., F. Papavasiliou, P. Cohen, O. de Bouteiller, D. Bell, H. Karasuyama, C. Schiff, J. Banchereau, Y.J. Liu, and M.C. Nussenzweig. 1998. Antigen receptor engagement turns off the V(D)J recombination machinery in human tonsil B cells. J. Exp. Med. 188:765-772.
30. Li, S.C., P.B. Rothman, J. Zhang, C. Chan, D. Hirsh, and F.W. Alt. 1994. Expression of I mu-C gamma hybrid germline transcripts subsequent to immunoglobulin heavy chain class switching. Int. Immunol. 6:491-497.
31. Porton, B., H.T. Kao, and P. Greengard. 1999. Characterization of transcripts from the synapsin III gene locus. J. Neurochem. 73:2266-2271.
32. Biron, C.A., K.B. Nguyen, G.C. Pien, L.P. Cousens, and T.P. Salazar-Mather. 1999. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17:189-220.
33. Der, S.D., A. Zhou, B.R. Williams, and R.H. Silverman. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA. 95:15623-15628.
34. Bennett, L., A.K. Palucka, E. Arce, V. Cantrell, J. Borvak, J. Banchereau, and V. Pascual. 2003. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197:711-723.
35. Rich, S.A., and T.R. Owens. 1984. Purified recombinant human leukocyte interferons IFLrA and IFLrD induce human lupus inclusions in Raji and Daudi cells. J. Interferon Res. 4:335-345.
36. Orenstein, J.M., O.T. Preble, P. Kind, and R. Schulof. 1987. The relationship of serum alpha-interferon and ultrastructural markers in HIV-seropositive individuals. Ultrastruct. Pathol. 11:673-679.
37. Claudio, J.O., E. Masih-Khan, H. Tang, J. Goncalves, M. Voralia, Z.H. Li, V. Nadeem, E. Cukennan, O. Francisco-Pabalan, C.C. Liew, et al. 2002. A molecular compendium of genes expressed in multiple myeloma. Blood. 100:2175-2186.
38. Medina, F., C. Segundo, A. Campos-Caro, I. Gonzalez-Garcia, and J.A. Brieva. 2002. The heterogeneity shown by human plasma cells from tonsil, blood, and bone marrow reveals graded stages of increasing maturity, but local profiles of adhesion molecule expression. Blood. 99:2154-2161.
39. Kunkel, E.J., and E.C. Butcher. 2003. Plasma-cell homing. Nat. Rev. Immunol. 3:822-829.
40. Avery, D.T., S.L. Kalled, J.I. Ellyard, C. Ambrose, S.A. Bixler, M. Thien, R. Brink, F. Mackay, P.D. Hodgkin, and S.G. Tangye. 2003. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J. Clin. Invest. 112:286-297.
41. Mackay, F., P. Schneider, P. Rennert, and J. Browning. 2003. BAFF AND APRIL: a tutorial on B cell survival. Annu. Rev. Immunol. 21:231-264.
42. Terstappen, L.W., S. Johnsen, I.M. Segers-Nolten, and M.R. Loken. 1990. Identification and characterization of plasma cells in normal human bone marrow by high-resolution flow cytometry. Blood. 76:1739-1747.
43. Krammer, P.H. 2000. CD95's deadly mission in the immune system. Nature. 407:789-795.
44. Rothstein, T.L., J.K. Wang, D.J. Panka, L.C. Foote, Z. Wang, B. Stanger, H. Cui, S.T. Ju, and A. Marshak-Rothstein. 1995. Protection against Fas-dependent Th1-mediated apoptosis by antigen receptor engagement in B cells. Nature. 374:163-165.
45. Prado, J.G., A. Shintani, M. Bofill, B. Clotet, L. Ruiz, and J. Martinez-Picado. 2004. Lack of longitudinal intrapatient correlation between p24 antigenemia and levels of human immunodeficiency virus (HIV) type 1 RNA in patients with chronic hiv infection during structured treatment interruptions. J. Clin. Microbiol. 42:1620-1625.
46. Pelletier, M., J.S. Thompson, F. Qian, S.A. Bixler, D. Gong, T. Cachero, K. Gilbride, E. Day, M. Zafari, C. Benjamin, et al. 2003. Comparison of soluble decoy IgG fusion proteins of BAFF-R and BCMA as antagonists for BAFF. J. Biol. Chem. 278:33127-33133.
47. Do, R.K., E. Hatada, H. Lee, M.R. Tourigny, D. Hilbert, and S. Chen-Kiang. 2000. Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med. 192:953-964.
48. Defrance, T., M. Casamayor-Palleja, and P.H. Krammer. 2002. The life and death of a B cell. Adv. Cancer Res. 86:195-225.
49. Kovacs, J.A., R.A. Lempicki, I.A. Sidorov, J.W. Adelsberger, B. Herpin, J.A. Metcalf, I. Sereti, M.A. Polis, R.T. Davey, J. Tavel, et al. 2001. Identification of dynamically distinct sub-populations of T lymphocytes that are differentially affected by HIV. J. Exp. Med. 194:1731-1741.
50. De Boer, R.J., H. Mohri, D.D. Ho, and A.S. Perelson. 2003. Turnover rates of B cells, T cells, and NK cells in simian immunodeficiency virus-infected and uninfected rhesus macaques. J. Immunol. 170:2479-2487.
51. Dybul, M., E. Nies-Kraske, M. Daucher, K. Hertogs, C.W. Hallahan, G. Csako, C. Yoder, L. Ehler, P.A. Sklar, M. Belson, et al. 2003. Long-cycle structured intermittent versus continuous highly active antiretroviral therapy for the treatment of chronic infection with human immunodeficiency virus: effects on drug toxicity and on immunologic and virologic parameters. J. Infect. Dis. 188:388-396.
52. Mackay, F., and C. Ambrose. 2003. The TNF family members BAFF and APRIL: the growing complexity. Cytokine Growth Factor Rev. 14:311-324.
53. Schneider, P., and J. Tschopp. 2003. BAFF and the regulation of B cell survival. Immunol. Lett. 88:57-62.
54. Thompson, J.S., S.A. Bixler, F. Qian, K. Vora, M.L. Scott, T.G. Cachero, C. Hession, P. Schneider, I.D. Sizing, C. Mullen, et al. 2001. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science. 293:2108-2111.
55. Xu, S., and K.P. Lam. 2001. B-cell maturation protein, which binds the tumor necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses. Mol. Cell. Biol. 21:4067-4074.
56. von Bulow, G.U., J.M. van Deursen, and R.J. Bram. 2001. Regulation of the T-independent humoral response by TACI. Immunity. 14:573-582.
57. Yan, M., H. Wang, B. Chan, M. Roose-Girma, S. Erickson, T. Baker, D. Tumas, I.S. Grewal, and V.M. Dixit. 2001. Activation and accumulation of B cells in TACI-deficient mice. Nat. Immunol. 2:638-643.
58. Seshasayee, D., P. Valdez, M. Yan, V.M. Dixit, D. Tumas, and I.S. Grewal. 2003. Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor. Immunity. 18:279-288.
59. Yan, M., J.R. Brady, B. Chan, W.P. Lee, B. Hsu, S. Harless, M. Cancro, I.S. Grewal, and V.M. Dixit. 2001. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr. Biol. 11:1547-1552.
60. Hauser, A.E., G.F. Debes, S. Arce, G. Cassese, A. Hamann, A. Radbruch, and R.A. Manz. 2002. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J. Immunol. 169:1277-1282.
61. Horst, A., N. Hunzelmann, S. Arce, M. Herber, R.A. Manz, A. Radbruch, R. Nischt, J. Schmitz, and M. Assenmacher. 2002. Detection and characterization of plasma cells in peripheral blood: correlation of IgE+ plasma cell frequency with IgE serum titre. Clin. Exp. Immunol. 130:370-378.
62. Nagase, H., K. Agematsu, K. Kitano, M. Takamoto, Y. Okubo, A. Komiyama, and K. Sugane. 2001. Mechanism of hypergammaglobulinemia by HIV infection: circulating memory B-cell reduction with plasmacytosis. Clin. Immunol. Immunopathol. 100:250-259.
63. De Milito, A., C. Morch, A. Sonnerborg, and F. Chiodi. 2001. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS. 15:957-964.
64. Calame, K.L., K.I. Lin, and C. Tunyaplin. 2003. Regulatory mechanisms that determine the development and function of plasma cells. Annu. Rev. Immunol. 21:205-230.
65. Tarte, K., F. Zhan, J. De Vos, B. Klein, and J. Shaughnessy, Jr. 2003. Gene expression profiling of plasma cells and plasmablasts: toward a better understanding of the late stages of B-cell differentiation. Blood. 102:592-600.
66. Zhan, F., E. Tian, K. Bumm, R. Smith, B. Barlogie, and J. Shaughnessy, Jr. 2003. Gene expression profiling of human plasma cell differentiation and classification of multiple myeloma based on similarities to distinct stages of late-stage B-cell development. Blood. 101:1128-1140.
67. Shaffer, A.L., A. Rosenwald, E.M. Hurt, J.M. Giltnane, L.T. Lam, O.K. Pickeral, and L.M. Staudt. 2001. Signatures of the immune response. Immunity. 15:375-385.
68. Marquart, H.V., A. Svendsen, J.M. Rasmussen, C.H. Nielsen, P. Junker, S.E. Svehag, and R.G. Leslie. 1995. Complement receptor expression and activation of the complement cascade on B lymphocytes from patients with systemic lupus erythematosus (SLE). Clin. Exp. Immunol. 101:60-65.
69. Illges, H., M. Braun, H.H. Peter, and I. Melchers. 2000. Reduced expression of the complement receptor type 2 (CR2, CD21) by synovial fluid B and T lymphocytes. Clin. Exp. Immunol. 122:270-276.
70. Ni, J., E. Hembrador, A.M. Di Bisceglie, I.M. Jacobson, A.H. Talal, D. Butera, C.M. Rice, T.J. Chambers, and L.B. Dustin. 2003. Accumulation of B lymphocytes with a naive, resting phenotype in a subset of hepatitis C patients. J. Immunol. 170:3429-3439.
71. Bockus, D., F. Remington, J.Y. Luu, M. Bean, and S. Hammar. 1988. Induction of cylindrical confronting cistemae (AIDS inclusions) in Daudi lymphoblastoid cells by recombinant alpha-interferon. Hum. Pathol. 19:78-82.