Soluble CD27 induces IgG production through activation of antigen-primed B cells

Journal of Internal Medicine

Volumn 271, Issue 3, 2012, Pages 282-293

  Dang, L V P ^a   Nilsson, A ^a   Ingelman Sundberg, H ^a   Cagigi, A ^b   Gelinck, L B S ^c   Titanji, K ^d   De Milito, A ^a   Grutzmeier, S ^e   Hedlund, J ^b   Kroon, F P ^f   Chiodi, F ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e STOCKHOLM SÖDER HOSPITAL   (Sweden)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

B cells; HIV 1; IgG production; SCD27

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD27 ANTIGEN; CD40 LIGAND; CD70 ANTIGEN; IMMUNOGLOBULIN G; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 6; LYMPHOCYTE ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RECOMBINANT CD27 ANTIGEN; RECOMBINANT CYTOKINE; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ADULT; AGED; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CD4 LYMPHOCYTE COUNT; CELL DIFFERENTIATION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOGLOBULIN PRODUCTION; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MEMORY CELL; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TH2 CELL; UPREGULATION; VIRUS LOAD;

ADULT; AGED; ANTIGENS, CD27; ANTIGENS, CD70; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; B-LYMPHOCYTES; CASE-CONTROL STUDIES; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; SOLUBILITY; YOUNG ADULT;

EID: 84857624737     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/j.1365-2796.2011.02444.x     Document Type: Article

References (61)

1. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig) M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 1998; 9: 1679-89.
2. van Lier RA, Borst J, Vroom TM et al. Tissue distribution and biochemical and functional properties of Tp55 (CD27), a novel T cell differentiation antigen. J Immunol 1987; 139: 1589-96.
3. Sugita K, Robertson MJ, Torimoto Y, Ritz J, Schlossman SF, Morimoto C. Participation of the CD27 antigen in the regulation of IL-2-activated human natural killer cells. J Immunol 1992; 149: 1199-203.
4. Wiesmann A, Phillips RL, Mojica M et al. Expression of CD27 on murine hematopoietic stem and progenitor cells. Immunity 2000; 12: 193-9.
5. Oshima H, Nakano H, Nohara C et al. Characterization of murine CD70 by molecular cloning and mAb. Int Immunol 1998; 10: 517-26.
6. Tesselaar K, Xiao Y, Arens R et al. Expression of the murine CD27 ligand CD70 in vitro and in vivo. J Immunol 2003; 170: 33-40.
7. Maurer D, Fischer GF, Fae I et al. IgM and IgG but not cytokine secretion is restricted to the CD27+ B lymphocyte subset. J Immunol 1992; 148: 3700-5.
8. Nagumo H, Agematsu K. Synergistic augmentative effect of interleukin-10 and CD27/CD70 interactions on B-cell immunoglobulin synthesis. Immunology 1998; 94: 388-94.
9. Ranheim EA, Cantwell MJ, Kipps TJ. Expression of CD27 and its ligand, CD70, on chronic lymphocytic leukemia B-cells. Blood 1995; 85: 3556-65.
10. Nilsson A, de Milito A, Mowafi F et al. Expression of CD27-CD70 on early B cell progenitors in the bone marrow: implication for diagnosis and therapy of childhood ALL. Exp Hematol 2005; 33: 1500-7.
11. Stein H, Herbst H, Anagnostopoulos I, Niedobitek G, Dallenbach F, Kratzsch HC. The nature of Hodgkin and Reed-Sternberg cells, their association with EBV, and their relationship to anaplastic large-cell lymphoma. Ann Oncol 1991; 2(Suppl 2): 33-8.
12. Lens SM, Drillenburg P, den Drijver BF et al. Aberrant expression and reverse signalling of CD70 on malignant B cells. Br J Haematol 1999; 106: 491-503.
13. Arens R, Nolte MA, Tesselaar K et al. Signaling through CD70 regulates B cell activation and IgG production. J Immunol 2004; 173: 3901-8.
14. Kato K, Chu P, Takahashi S, Hamada H, Kipps TJ. Metalloprotease inhibitors block release of soluble CD27 and enhance the immune stimulatory activity of chronic lymphocytic leukemia cells. Exp Hematol 2007; 35: 434-42.
15. Loenen WA, De Vries E, Gravestein LA, Hintzen RQ, Van Lier RA, Borst J. The CD27 membrane receptor, a lymphocyte-specific member of the nerve growth factor receptor family, gives rise to a soluble form by protein processing that does not involve receptor endocytosis. Eur J Immunol 1992; 22: 447-55.
16. Hintzen RQ, de Jong R, Hack CE et al. A soluble form of the human T cell differentiation antigen CD27 is released after triggering of the TCR/CD3 complex. J Immunol 1991; 147: 29-35.
17. Bohnhorst JO, Bjorgan MB, Thoen JE, Jonsson R, Natvig JB, Thompsson KM. Abnormal B cell differentiation in primary Sjogrens syndrome results in a depressed percentage of circulating memory B cells and elevated levels of soluble CD27 that correlate with serum IgG concentration. Clin Immunol 2002; 103: 79-88.
18. Font J, Pallares L, Martorell J et al. Elevated sCD27 levels in serum of patients with systemic lupus erytematosus. Clin Immunol Immunopathol 1996; 81: 239-43.
19. van Oers MH, Pals ST, Evers LM et al. Expression and release of CD27 in human B-cell malignancies. Blood 1993; 82: 3430-6.
20. Portegies P, Godfried MH, Hintzen RQ et al. Low levels of specific T cell activation marker CD27 accompanied by elevated levels of markers for non-specific immune activation in the cerebrospinal fluid of patients with AIDS dementia complex. J Neuroimmunol 1993; 48: 241-7.
21. 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.
22. Messele T, Brouwer M, Girma M et al. Plasma levels of viro-immunological markers in HIV-infected and non-infected Ethiopians: correlation with cell surface activation markers. Clin Immunol 2001; 98: 212-9.
23. De Milito A, Aleman S, Marenzi R, Sönnerborg A, Zazzi M, Chiodi F. Plasma level of soluble CD27: a simple marker to monitor immune activation during potent antiretriviral therapy in HIV-1 infected subjects. Clin Exp Immunol 2002; 127: 486-94.
24. Atlas A, Thanh Ha TT, Lindstrom A et al. Effects of potent antiretroviral therapy on the immune activation marker soluble CD27 in patients infected with HIV-1 subtypes A-D. J Med Virol 2004; 72: 345-51.
25. De Milito A. B lymphocyte dysfunctions in HIV infection. Curr HIV Res 2004; 2: 11-21.
26. Moir S, Malaspina A, Ogwaro KM 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: 10362-7.
27. Morris L, Binley JM, Clas BA et al. HIV-1 antigen-specific and -nonspecific B cell responses are sensitive to combination antiretroviral therapy. J Exp Med 1998; 188: 233-45.
28. 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.
29. 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.
30. 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.
31. Samuelsson A, Yari F, Hinkula J, Ersoy O, Norrby E, Persson MA. Human antibodies from phage libraries: neutralizing activity against human immunodeficiency virus type 1 equally improved after expression as Fab and IgG in mammalian cells. Eur J Immunol 1996; 26: 3029-34.
32. Agematsu K, Kobata T, Sugita K et al. Role of CD27 in T cell immune response. Analysis by recombinant soluble CD27. J Immunol 1994; 153: 1421-9.
33. Cagigi A, Du L, Dang LV et al. CD27(-) B-cells produce class switched and somatically hyper-mutated antibodies during chronic HIV-1 infection. PLoS ONE 2009; 4: e5427.
34. Fauci AS, Pratt KR. Human bone marrow lymphocytes. III. Polyclonal activation of B lymphocytes in human bone marrow measured by a direct plaque-forming cell assay. J Immunol 1977; 118: 1150-3.
35. Kindler V, Zubler RH. Memory, but not naive, peripheral blood B lymphocytes differentiate into Ig-secreting cells after CD40 ligation and costimulation with IL-4 and the differentiation factors IL-2, IL-10, and IL-3. J Immunol 1997; 159: 2085-90.
36. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002; 298: 2199-202.
37. Arpin C, Dechanet J, Van Kooten C et al. Generation of memory B cells and plasma cells in vitro. Science 1995; 268: 720-2.
38. Lens SM, Baars PA, Hooibrink B, van Oers MH, van Lier RA. Antigen-presenting cell-derived signals determine expression levels of CD70 on primed T cells. Immunology 1997; 90: 38-45.
39. Lens SMA, de Jong R, Hooibrink B et al. Phenotype and function of human B cells expressing CD70. Eur J Immunol 1996; 26: 2964-71.
40. Stavnezer J, Guikema JE, Schrader CE. Mechanism and regulation of class switch recombination. Annu Rev Immunol 2008; 26: 261-92.
41. Reimold AM, Iwakoshi NN, Manis J et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001; 412: 300-7.
42. Turner CA Jr, Mack DH, Davis MM. Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 1994; 77: 297-306.
43. Hintzen RQ, van Lier RAW, Kuijpers KC et al. Elevated levels of a soluble form of the T cell activation antigen CD27 in cerebrospinal fluid of multiple sclerosis patients. J Neuroimmunol 1991; 35: 211-7.
44. 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.
45. Shirai A, Cosentino M, Leitman-Klinman SF, Klinman DM. Human immunodeficiency virus infection induces both polyclonal and virus-specific B cell activation. J Clin Invest 1992; 89: 561-6.
46. Terpstra FG, Al BJ, Roos MT et al. Longitudinal study of leukocyte functions in homosexual men seroconverted for HIV: rapid and persistent loss of B cell function after HIV infection. Eur J Immunol 1989; 19: 667-73.
47. De Milito A, Nilsson A, Titanji K et al. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood 2004; 103: 2180-6.
48. Malaspina A, Moir S, Ho J et al. Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7. Proc Natl Acad Sci U S A 2006; 103: 2262-7.
49. 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.
50. Doria-Rose NA, Klein RM, Manion MM et al. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J Virol 2009; 83: 188-99.
51. Nagase H, Agematsu K, Kitano K et al. Mechanism of hypergammaglobulinemia by HIV infection: circulating memory B-cell reduction with plasmacytosis. Clin Immunol 2001; 100: 250-9.
52. Xiao Y, Hendriks J, Langerak P, Jacobs H, Borst J. CD27 is acquired by primed B cells at the centroblast stage and promotes germinal center formation. J Immunol 2004; 172: 7432-41.
53. Lens SMA, Tesselaar K, van Oers M, van Lier RAW. Control of lymphocyte function through CD27-CD70 interactions. Seminars in Immunol 1998; 10: 491-9.
54. Hintzen RQ, de Jong R, Lens SMA, van Lier RAW. CD27; a marker and mediator of T-cell activation. Immunol Today 1994; 15: 307-11.
55. Ho AW, Hatjiharissi E, Ciccarelli BT et al. CD27-CD70 interactions in the pathogenesis of Waldenstrom macroglobulinemia. Blood 2008; 112: 4683-9.
56. Ruprecht CR, Lanzavecchia A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol 2006; 36: 810-6.
57. Shapiro-Shelef M, Lin KI, Savitsky D, Liao J, Calame K. Blimp-1 is required for maintenance of long-lived plasma cells in the bone marrow. J Exp Med 2005; 202: 1471-6.
58. Calame KL, Lin KI, Tunyaplin C. Regulatory mechanisms that determine the development and function of plasma cells. Annu Rev Immunol 2003; 21: 205-30.
59. Iwakoshi NN, Lee AH, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 2003; 4: 321-9.
60. Kallies A, Hasbold J, Fairfax K et al. Initiation of plasma-cell differentiation is independent of the transcription factor Blimp-1. Immunity 2007; 26: 555-66.
61. De Milito A, Morch C, Sonnerborg A, Chiodi F. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 2001; 15: 957-64.