Clonal B cells of HCV-associated mixed cryoglobulinemia patients contain exhausted marginal zone-like and CD21 low cells overexpressing Stra13

European Journal of Immunology

Volumn 42, Issue 6, 2012, Pages 1468-1476

  Visentini, Marcella ^a   Cagliuso, Maria ^a   Conti, Valentina ^a   Carbonari, Maurizio ^a   Cibati, Marina ^a   Siciliano, Giulia ^a   Cristofoletti, Cristina ^b   Russo, Giandomenico ^b   Casato, Milvia ^a   Fiorilli, Massimo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Anergy; B cells; HCV; Mixed cryoglobulinemia; Stra13

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BREAKPOINT CLUSTER REGION PROTEIN; COMPLEMENT COMPONENT C3D RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE; STRA13 PROTEIN; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; CRYOGLOBULINEMIA; FEMALE; HEPATITIS C VIRUS; HEPATITIS C VIRUS ASSOCIATED MIXED CYROGLOBULINEMIA; HOMEOSTASIS; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MALE; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADULT; AGED; AGED, 80 AND OVER; B-LYMPHOCYTES; CRYOGLOBULINEMIA; DNA-BINDING PROTEINS; FEMALE; HEPATITIS C; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NUCLEAR PROTEINS; PHENOTYPE; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, COMPLEMENT 3D; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9;

EID: 84862128472     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142313     Document Type: Article

References (47)

1. Landau, D. A., Saadoun, D., Calabrese, L. H. and Cacoub, P., The pathophysiology of HCV induced B-cell clonal disorders. Autoimmun. Rev. 2007. 6: 581-587.
2. Carbonari, M., Caprini, E., Tedesco, T., Mazzetta, F., Tocco, V., Casato, M., Russo, G. et al., Hepatitis C virus drives the unconstrained monoclonal expansion of VH1-69-expressing memory B cells in type II cryoglobulinemia: a model of infection-driven lymphomagenesis. J. Immunol. 2005. 174: 6532-6539.
3. Charles, E. D., Green, R. M., Marukian, S., Talal, A. H., Lake-Bakaar, G. V., Jacobson, I. M., Rice, C. M. et al., Clonal expansion of immunoglobulin M+CD27+ B cells in HCV-associated mixed cryoglobulinemia. Blood 2008. 111: 1344-1356.
4. Chan, C. H., Hadlock, K. G., Foung, S. K. H. and Levy, S., The VH1-69 gene is preferentially used both by hepatitis C virus-associated B cell lymphomas and by normal B cells responding to the E2 viral antigen. Blood 2001. 97: 1023-1026.
5. Quinn, E. R., Chan, C. H., Hadlock, K. G., Foung, S. K., Flint, M. and Levy, S., The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis. Blood 2001. 98: 3745-3749.
6. Marcucci, F. and Mele, A., Hepatitis viruses and non-Hodgkin lymphoma: epidemiology, mechanisms of tumorigenesis and therapeutic opportunities. Blood 2011. 117: 1792-1798.
7. Hermine, O., Lefrère, F., Bronowicki, J. P., Mariette, X., Jondeau, K., Eclache-Saudreau, V., Delmas, B. et al., Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N. Engl. J. Med. 2002. 347: 89-94.
8. Casato, M., Mecucci, C., Agnello, V., Fiorilli, M., Knight, G. B., Matteucci, C., Gao, L. et al., Regression of lymphoproliferative disorder after treatment for hepatitis C virus infection in a patient with partial trisomy 3, Bcl-2 overexpression, and type II cryoglobulinemia. Blood 2002. 99: 2259-2261.
9. Matteucci, C., Bracci, M., Barba, G., Carbonari, M., Casato, M., Visentini, M., Pulsoni, A. et al., Different genomic imbalances in low- and high-grade HCV-related lymphomas. Leukemia 2008. 22: 219-222.
10. De Re, V., De Vita, S., Marzotto, A., Rupolo, M., Gloghini, A., Pivetta, B., Gasparotto, D. et al., Sequence analysis of the immunoglobulin antigen receptor of hepatitis C virus-associated non-Hodgkin lymphomas suggests that the malignant cells are derived from the rheumatoid factor-producing cells that occur mainly in type II cryoglobulinemia. Blood 2000. 96: 3578-3584.
11. Charles, E. D., Brunetti, C., Marukian, S., Ritola, K. D., Talal, A. H., Marks, K., Jacobson, I. M., et al. Clonal B cells in patients with hepatitis C virus-associated mixed cryoglobulinemia contain an expanded anergic CD21low B-cell subset. Blood 2011. 117: 5425-5437.
12. Terrier, B., Joly, F., Vazquez, T., Benech, P., Rosenzwajg, M., Carpentier, W., Garrido, M. et al., Expansion of functionally anergic CD21-/low marginal zone-like B cell clones in hepatitis C virus infection-related autoimmunity. J. Immunol. 2011. 187: 6550-6563.
13. Visentini, M., Cagliuso, M., Conti, V., Carbonari, M., Casato, M. and Fiorilli, M., The VH1-69-expressing marginal zone B cells expanded in HCV-associated mixed cryoglobulinemia display proliferative anergy irrespective of CD21low phenotype. Blood 2011. 118: 3440-3441.
14. Weller, S., Braun, M. C., Tan, B. K., Rosenwald, A., Cordier, C., Conley, M. E., Plebani, A. et al., Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 2004. 104: 3647-3654.
15. Ehrhardt, G. R., Hsu, J. T., Gartland, L., Leu, C. M., Zhang, S., Davis, R. S. and Cooper, M. D., Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J. Exp. Med. 2005. 202: 783-791.
16. Ehrhardt, G. R., Hijikata, A., Kitamura, H., Ohara, O., Wang, J. Y. and Cooper, M. D., Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 2008. 205: 1807-1817.
17. Rakhmanov, M., Keller, B., Gutenberger, S., Foerster, C., Hoenig, M., Driessen, G., van der Burg, M. et al., Circulating CD21low B cells in common variable immunodeficiency resemble tissue homing, innate-like B cells. Proc. Natl. Acad. Sci. USA 2009. 106: 13451-13456.
18. Isnardi, I., Ng, Y. S., Menard, L., Meyers, G., Saadoun, D., Srdanovic, I., Samuels, J. et al., Complement receptor 2/CD21- human naive B cells contain mostly autoreactive unresponsive clones. Blood 2010. 115: 5026-5036.
19. Visentini, M., Cagliuso, M., Conti, V., Carbonari, M., Mancaniello, D., Cibati, M., Siciliano, G. et al., Telomere-dependent replicative senescence of B and T cells from patients with type 1a common variable immunodeficiency. Eur. J. Immunol. 2011. 41: 854-862.
20. Moir, S., Ho, J., Malaspina, A., Wang, W., Di Poto, A. C., O'Shea, M. A., Roby, G. 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.
21. Kardava, L., Moir, S., Wang, W., Ho, J., Buckner, C. M., Posada, J. G., O'Shea, M. A. et al., Attenuation of HIV-associated human B cell exhaustion by siRNA downregulation of inhibitory receptors. J. Clin. Invest. 2011. 121: 2614-2624.
22. Sun, H., Lu, B., Li, R. Q., Flavell, R. A. and Taneja, R., Defective T cell activation and autoimmune disorder in Stra13-deficient mice. Nat. Immunol. 2001. 2: 1040-1047.
23. Seimiya, M., Wada, A., Kawamura, K., Sakamoto, A., Ohkubo, Y., Okada, S., Hatano, M. et al., Impaired lymphocyte development and function in Clast5/Stra13/DEC1-transgenic mice. Eur. J. Immunol. 2004. 34: 1322-1332.
24. Seimiya, M., Bahar, R., Wang, Y., Kawamura, K., Tada, Y., Okada, S., Hatano, M. et al., Clast5/Stra13 is a negative regulator of B lymphocyte activation. Biochem. Biophys. Res. Commun. 2002. 292: 121-127.
25. Bernasconi, N. L., Onai, N. and Lanzavecchia, A., A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 2003. 101: 4500-4504.
26. Persico, M., Capasso, M., Persico, E., Masarone, M., Renzo, A., Spano, D., Bruno, S. et al., Interleukin-10 - 1082 GG polymorphism influences the occurrence and the clinical characteristics of hepatitis C virus infection. J. Hepatol. 2006. 45: 779-785.
27. Mathsson, L., Tejde, A., Carlson, K., Höglund, M., Nilsson, B., Nilsson-Ekdahl, K. and Rönnelid, J., Cryoglobulin-induced cytokine production via FcgammaRIIa: inverse effects of complement blockade on the production of TNF-alpha and IL-10. Implications for the growth of malignant B-cell clones. Br. J. Haematol. 2005. 29: 830-838.
28. Rui, L., Vinuesa, C. G., Blasioli, J. and Goodnow, C. C., Resistance to CpG DNA-induced autoimmunity through tolerogenic B cell antigen receptor ERK signaling. Nat. Immunol. 2003. 4: 594-600.
29. Gauld, S. B., Benschop, R. J., Merrell, K. T. and Cambier, J. C., Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat. Immunol. 2005. 6: 1160-1167.
30. Sun, H. and Taneja, R., Stra13 expression is associated with growth arrest and represses transcription through histone deacetylase (HDAC)-dependent and HDAC-independent mechanisms. Proc. Natl. Acad. Sci. USA 2000. 97: 4058-4063.
31. Bhawal, U. K., Sato, F., Arakawa, Y., Fujimoto, K., Kawamoto, T., Tanimoto, K., Ito, Y. et al., Basic helix-loop-helix transcription factor DEC1 negatively regulates cyclin D1. J. Pathol. 2011. 224: 420-429.
32. Kin, N. W., Crawford, D. M., Liu, J., Behrens, T. W. and Kearney, J. F., DNA microarray gene expression profile of marginal zone versus follicular B cells and idiotype positive marginal zone B cells before and after immunization with Streptococcus pneumoniae. J. Immunol. 2008. 180: 6663-6674.
33. Cambier, J. C., Gauld, S. B., Merrell, K. T. and Vilen, B. J., B-cell anergy: from transgenic models to naturally occurring anergic B cells? Nat. Rev. Immunol. 2007. 7: 633-643.
34. Wong, S. C., Chew, W. K., Tan, J. E., Melendez, A. J., Francis, F. and Lam, K. P., Peritoneal CD5+ B-1 cells have signaling properties similar to tolerant B cells. J. Biol. Chem. 2002. 277: 30707-30715.
35. Holodick, N. E., Tumang, J. R. and Rothstein, T. L., Continual signaling is responsible for constitutive ERK phosphorylation in B-1a cells. Mol. Immunol. 2009. 46: 3029-3036
36. Sen, G., Wu, H. J., Bikah, G., Venkataraman, C., Robertson, D. A., Snow, E. C. and Bondada, S., Defective CD19-dependent signaling in B-1a and B-1b B lymphocyte subpopulations. Mol. Immunol. 2002. 39: 57-68.
37. Griffin, D. O., Holodick, N. E. and Rothstein, T. L., Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70- J. Exp. Med. 2011. 208: 67-80.
38. Dasu, T., Sindhava, V., Clarke, S. H. and Bondada, S., CD19 signaling is impaired in murine peritoneal and splenic B-1 B lymphocytes. Mol. Immunol. 2009. 46: 2655-2665.
39. Li, Y., Zhang, H., Xie, M., Hu, M., Ge, S., Yang, D., Wan, Y. et al., Abundant expression of Dec1/stra13/sharp2 in colon carcinoma: its antagonizing role in serum deprivation-induced apoptosis and selective inhibition of procaspase activation. Biochem. J. 2002. 367: 413-422.
40. Ehata, S., Hanyu, A., Hayashi, M., Aburatani, H., Kato, Y., Fujime, M., Saitoh, M. et al., Transforming growth factor-beta promotes survival of mammary carcinoma cells through induction of antiapoptotic transcription factor DEC1. Cancer Res. 2007. 67: 9694-9703.
41. Martin, F., Oliver, A. M. and Kearney, J. F., Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001. 14: 617-629.
42. Racine, R., Chatterjee, M. and Winslow, G. M., CD11c expression identifies a population of extrafollicular antigen-specific splenic plasmablasts responsible for CD4 T-independent antibody responses during intracellular bacterial infection. J. Immunol. 2008. 181: 1375-1385.
43. Morse, H. C., 3rd, Kearney, J. F., Isaacson, P. G., Carroll, M., Fredrickson, T. N. and Jaffe, E. S., Cells of the marginal zone-origins, function and neoplasia. Leuk. Res. 2001. 25: 169-178.
44. Suarez, F., Lortholary, O., Hermine, O. and Lecuit, M., Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood 2006. 107: 3034-3044.
45. Potter, K. N., Li, Y., Mageed, R. A., Jefferis, R. and Capra, J. D., Molecular characterization of the VH1-specific variable region determinants recognized by anti-idiotypic monoclonal antibodies G6 and G8. Scand. J. Immunol. 1999. 50:14-20.
46. Lyons, A. B., Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J. Immunol. Methods 2000. 243: 147-154.
47. Zhang, A. S., Xiong, S., Tsukamoto, H. and Enns, C. A., Localization of iron metabolism-related mRNAs in rat liver indicate that HFE is expressed predominantly in hepatocytes. Blood 2004. 103: 1509-1514.