Hepatitis viruses and non-Hodgkin lymphoma: Epidemiology, mechanisms of tumorigenesis, and therapeutic opportunities

Blood

Volumn 117, Issue 6, 2011, Pages 1792-1798

  Marcucci, Fabrizio ^a,b   Mele, Alfonso ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Associazione Calabrese di Epatologia   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; CRYOGLOBULIN; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B VACCINE; HEPATITIS C VACCINE; PEGINTERFERON; RIBAVIRIN; STRESS ACTIVATED PROTEIN KINASE; VIRUS PROTEIN;

B CELL LYMPHOMA; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BURKITT LYMPHOMA; CANCER EPIDEMIOLOGY; CANCER INCIDENCE; CANCER REGISTRY; CARCINOGENESIS; CHROMOSOME TRANSLOCATION; CHRONIC LYMPHATIC LEUKEMIA; CRYOGLOBULINEMIA; DISEASE ASSOCIATION; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HODGKIN DISEASE; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOMA; MANTLE CELL LYMPHOMA; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA; PRIORITY JOURNAL; REVIEW; T CELL LYMPHOMA; VIRUS ENTRY; VIRUS GENOME; VIRUS REACTIVATION; VIRUS REPLICATION;

EID: 79951468929     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-06-275818     Document Type: Review

References (81)

1. Clarke B. Molecular virology of hepatitis C virus. J Gen Virol. 1997;78(10):2397-2410. (Pubitemid 27469980)
2. Tiollais P, Pourcel C, Dejean A. The hepatitis B virus. Nature. 1985;317(6037):489-495. (Pubitemid 16224154)
3. National Cancer Institute, Surveillance Epidemiology and End Results. Delay-adjusted SEER Incidence Rates by Year, Race and Sex: Table 19.4 - non-Hodgkin lymphoma. http://www.seer.cancer-.gov. Accessed June 10, 2010.
4. Alexander DD, Mink PJ, Adami H-O, et al. The non-Hodgkin lymphomas: a review of the epidemiologic literature. Int J Cancer. 2007;120(suppl 12):1-39. (Pubitemid 46732571)
5. Pascual M, Perrin L, Giostra E, Schifferli JA. Hepatitis C virus in patients with cryoglobulinemia type II. J Infect Dis. 1990;162(2):569-570. (Pubitemid 20239986)
6. Agnello V, Chung RT, Kaplan LM. A role for hepatitis C virus infection in type II cryoglobulinemia. N Engl J Med. 1992;327(21):1490-1495.
7. Agnello V, Zhang QX, Abel G, Knight GB. The association of hepatitis C virus infection with monoclonal rheumatoid factors bearing the WA cross-idiotype: implications for the etiopathogenesis and therapy of mixed cryoglobulinemia. Clin Exp Rheumatol. 1995;13(suppl 13):S101-S104.
8. Ferri C, Zignego AL, Pileri SA. Cryoglobulins. J Clin Pathol. 2002;55(1):4-13.
9. Monti G, Pioltelli P, Saccardo F, et al. Incidence and characteristics of non-Hodgkin lymphomas in a multicenter case file of patients with hepatitis C virus-related symptomatic mixed cryoglobulinemias. Arch Intern Med. 2005;165(1):101-105. (Pubitemid 40096090)
10. Ferri C, Caracciolo F, Zignego AL, et al. Hepatitis C virus infection in patients with non-Hodgkin's lymphoma. Br J Haematol. 1994;88(2):392-394. (Pubitemid 24318191)
11. Pozzato G, Mazzaro C, Crovatto M, et al. Lowgrade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia. Blood. 1994;84(9):3047-3053. (Pubitemid 24328097)
12. Mele A, Pulsoni A, Bianco E, et al. Hepatitis C virus and B-cell non-Hodgkin lymphomas: an Italian multicenter case-control study. Blood. 2003;102(3):996-999. (Pubitemid 36917795)
13. Duberg A-S, Nordström M, Törner A, et al. Non-Hodgkin's lymphoma and other nonhepatic malignancies in Swedish patients with hepatitis C virus infection. Hepatology. 2005;41(3):652-659. (Pubitemid 40289514)
14. Anderson LA, Pfeiffer R, Warren JL, et al. Hematopoietic malignancies associated with viral and alcoholic hepatitis. Cancer Epidemiol Biomarkers Prev. 2008;17(11):3069-75.
15. Dal Maso L, Franceschi S. Hepatitis C virus and risk of lymphoma and other lymphoid neoplasms: a meta-analysis of epidemiologic studies. Cancer Epidemiol Biomarkers Prev. 2006;15(11):2078-2085. (Pubitemid 44877029)
16. Maryak LA, Yeganeh M, Saab S. Hepatitis C and lymphoproliferative disorders: from mixed cryoglobulinemia to non-Hodgkin's lymphoma. Clin Gastroenterol Hepatol. 2009;7(8):900-905.
17. Mussini C, Ghini M, Mascia MT, et al. Monoclonal gammopathies and hepatitis C virus infection. Blood. 1995;85(4):1144-1149.
18. Silvestri F, Barillari G, Fanin R, et al. Hepatitis C virus infection among cryoglobulinemic and noncryoglobulinemic B-cell non-Hodgkin's lymphomas. Haematologica. 1997;82(3):314-317. (Pubitemid 28023307)
19. Hausfater P, Cacoub P, Sterkers Y, et al. Hepatitis C virus infection and lymphoproliferative disease: Prospective study on 1,576 patients in France. Am J Hematol. 2001;67(3):168-171. (Pubitemid 32538614)
20. Udomsakdi-Auewarakul C, Auewarakul P, Sukpanichnant S, et al. Hepatitis C virus infection in patients with non-Hodgkin lymphoma in Thailand. Blood. 2000;95(11):3640-3641. (Pubitemid 30428509)
21. Collier JD, Zanke B, Moore M, et al. No association between hepatitis C and B-cell lymphoma. Hepatology. 1999;29(4):1259-1261.
22. Galun E, Ilan Y, Livni N, et al. Hepatitis B virus infection associated with hematopoietic tumors. Am J Pathol. 1994;145(5):1001-1007. (Pubitemid 24345646)
23. Kim JH, Bang YJ, Park BJ, et al. Hepatitis B virus infection and B-cell non-Hodgkin's lymphoma in a hepatitis B endemic area: a case-control study. Jpn J Cancer Res. 2002;93(5):471-477. (Pubitemid 34752902)
24. Marcucci F, Mele A, Spada E, et al. High prevalence of hepatitis B virus infection in B cell non-Hodgkin lymphoma. Haematologica. 2006;91(4):554-557.
25. Nath A, Agarwal R, Malhotra P, Varma S. Prevalence of hepatitis B virus infection in non-Hodgkin's lymphoma. Asystematic review and meta-analysis. Intern Med J. 2010;40(9):633-641.
26. Engels EA, Cho ER, Jee SH. Hepatitis B virus infection and risk of non-Hodgkin lymphoma in South Korea: a cohort study. Lancet Oncol. 2010;11(9):827-834.
27. Bréchot C, Thiers V, Kremsdorf D, Nalpas B, Pol S, Paterlini-Bréchot P. Persistent hepatitis B virus infection in subjects without hepatitis B surface antigen: clinically significant or purely "occult"? Hepatology. 2001;34(1):194-203.
28. Yuki N, Nagaoka T, Yamashiro M, et al. Longterm histologic and virologic outcomes of acute self-limited hepatitis B. Hepatology. 2003;37(5):1172-1179. (Pubitemid 36538695)
29. Rehermann B, Ferrari C, Pasquinelli C, Chisari FV. The hepatitis B virus persists for decades after patients' recovery from acute viral hepatitis despite active maintenance of a cytotoxic T-lymphocyte response. Nat Med. 1996;2(10):1104-1108. (Pubitemid 26338629)
30. Chen MH, Hsiao LT, Chiou TJ, et al. High prevalence of occult hepatitis B virus infection in patients with B-cell non-Hodgkin's lymphoma. Ann Hematol. 2008;87(6):475-480.
31. Rossi D, Sala L, Minisini R, et al. Occult hepatitis B virus infection of peripheral blood mononuclear cells among treatment-naive patients with chronic lymphocytic leukemia. Leuk Lymphoma. 2009;50(4):604-611.
32. Wang F, Xu R-J, Han B, et al. High incidence of hepatitis B virus infection in B-cell subtype non-Hodgkin lymphoma compared with other cancers. Cancer. 2007;109(7):1360-1364. (Pubitemid 46466563)
33. Bianco E, Marcucci F, Mele A, et al. Prevalence of hepatitis C virus infection in lymphoproliferative diseases other than B-cell non-Hodgkin's lymphoma, and in myeloproliferative diseases: an Italian multi-center case-control study. Haematologica. 2004;89(1):70-76. (Pubitemid 38165857)
34. Feitelson MA, Duan LX. Hepatitis B virus x antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. Am J Pathol. 1997;150(4):1141-1157. (Pubitemid 27152632)
35. Hermine O, Lefrere F, Bronowicki JP, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med. 2002;347(2):89-94. (Pubitemid 34753478)
36. Vallisa D, Bernuzzi P, Arcaini L, et al. Role of antihepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-Hodgkin's lymphoma: A multicenter Italian experience. J Clin Oncol. 2005;23(3):468-473. (Pubitemid 46224223)
37. Gisbert JP, García-Buey L, Pajares JM, Moreno-Otero R. Systematic review: regression of lymphoproliferative disorders after treatment for hepatitis C infection. Aliment Pharmacol Ther. 2005;21(6):653-662. (Pubitemid 40468993)
38. La Mura V, De Renzo A, Perna F, et al. Antiviral therapy after complete response to chemotherapy could be efficacious in HCV-positive non-Hodgkin's lymphoma. J Hepatol. 2008;49(4):557-563.
39. Zuckerman E, Zuckerman T, Sahar D, et al. The effect of antiviral therapy on t(14;18) translocation and immunoglobulin gene rearrangement in patients with chronic hepatitis C virus infection. Blood. 2001;97(6):1555-1559. (Pubitemid 32217215)
40. Kawamura Y, Ikeda K, Arase Y, et al. Viral elimination reduces incidence of malignant lymphoma in patients with hepatitis C. Am J Med. 2007;120(12):1034-1041. (Pubitemid 350166219)
41. Stathis A, Bertonei F, Zucca E. Treatment of gastric marginal zone lymphoma of MALT type. Expert Opin Pharmacother. 2010;11(13):2141-2152.
42. Zullo A, Hassan C, Andriani A, et al. Treatment of low-grade gastric MALT-lymphoma unresponsive to Helicobacter pylori therapy: a pooled-data analysis. Med Oncol. 2010;27(2):291-295.
43. De Re V, De Vita S, Marzotto A, et al. Premalignant and malignant lymphoproliferations in an HCV-infected type II mixed cryoglobulinemic patient are sequential phases of an antigendriven pathological process. Int J Cancer. 2000;87(2):211-216. (Pubitemid 30434347)
44. Ishii K, Rosa D, Watanabe Y, et al. High titers of antibodies inhibiting the binding of envelope to human cells correlate with natural resolution of chronic hepatitis C. Hepatology. 1998;28(4):1117-1120. (Pubitemid 28450275)
45. Lesniewski R, Okasinski G, Carrick R, et al. Antibody to hepatitis C virus second envelope (HCVE2) glycoprotein: a new marker of HCV infection closely associated with viremia. J Med Virol. 1995;45(4):415-422.
46. Allander T, Drakenberg K, Beyene A, et al. Recombinant human monoclonal antibodies against different conformational epitopes of the E2 envelope glycoprotein of hepatitis C virus that inhibit its interaction with CD81. J Gen Virol. 2000;81(10):2451-2459.
47. Chan CH, Hadlock KG, Foung SKH, 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(4):1023-1026. (Pubitemid 32154288)
48. Gorevic PD, Frangione B. Mixed cryoglobulinemia cross-reactive idiotypes: implications for the relationship of MC to rheumatic and lymphoproliferative disease. Semin Hematol. 1991;28(2):79-94.
49. Ivanovski M, Silvestri F, Pozzato G, et al. Somatic hypermutation, clonal diversity, and preferential expression of the VH 51p1/VL kv325 immunoglobulin gene combination in hepatitis C virusassociated immunocytomas. Blood. 1998;91(7):2433-2442. (Pubitemid 28155518)
50. Quinn ER, Chan CH, Hadlock KG, Foung SKH, Flint M, 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(13):3745-3749.
51. Pileri P, Uematsu Y, Campagnoli S, et al. Binding of hepatitis C virus to CD81. Science. 1998;282(5390):938-941 (1998).
52. Rosa D, Saletti G, De Gregorio E, et al. Activation of naive B lymphocytes via CD81, a pathogenic mechanism for hepatitis C virus-associated B lymphocyte disorders. Proc Natl Acad Sci U S A. 2005;102(51):18544-18549. (Pubitemid 43011262)
53. Wack A, Soldaini E, Tseng C-TK, Nuti S, Klimpel GR, Abrignani S. Binding of the hepatitis C virus envelope protein E2 to CD81 provides a costimulatory signal for human T cells. Eur J Immunol. 2001;31(1):166-175.
54. Poetsch M, Weber-Matthiesen K, Plendl HJ, et al. Detection of the t(14:18) chromosomal translocation by interphase cytogenetics with yeastartificial-chromosome probe in follicular lymphoma and nonneoplastic lymphoproliferation. J Clin Oncol. 1996;14(3):963-969.
55. Tsujimoto Y, Croce CM. Analysis of the structure, transcript, and protein products of bcl-2 gene involved in follicular lymphomas. Proc Natl Acad Sci U S A. 1986;83(14):5214-5218. (Pubitemid 16051345)
56. Zignego AL, Ferri C, Giannelli F, et al. Prevalence of bcl-2 rearrangement in patients with hepatitis C virus-related mixed cryoglobulinemia with or without B-cell lymphomas. Ann Intern Med. 2002;137(7):571-580.
57. Zuckerman E, Zuckerman T, Sahar D, et al. bcl-2 and immunoglobulin gene rearrangement in patients with hepatitis C virus infection. Br J Haematol. 2001;112(2):364-369. (Pubitemid 32183478)
58. Machida K, Cheng KT, Pavio N, Sung VM, Lai MM. Hepatitis C virus E2-CD81 interaction induces hypermutation of the immunoglobulin gene in B cells. J Virol. 2005;79(13):8079-8089. (Pubitemid 40853511)
59. Inokuchi M, Ito T, Uchikoshi M, et al. Infection of B cells with hepatitis C virus for the development of lymphoproliferative disorders in patients with chronic hepatitis C. J Med Virol. 2009;81(4):619-627.
60. Zignego AL, Giannini C, Monti M, et al. Hepatitis C virus lymphotropism: lessons from a decade of studies. Dig Liver Dis. 2007;39(Suppl 1):S38-S45. (Pubitemid 47528193)
61. Sansonno D, Tucci FA, Lauletta G, et al. Hepatitis C virus productive infection in mononuclear cells from patients with cryoglobulinaemia. Clin Exp Immunol. 2007;147(2):241-248. (Pubitemid 46096001)
62. Willems M, Moshage H, Yap SH. PCR and detection of negative HCV RNA strands [letter]. Hepatology. 1993;17(3):526. (Pubitemid 23072832)
63. Landford RE, Chavez D, Chisari FV, Sureau C. Lack of detection of negative-strand hepatitis C virus RNA in peripheral blood mononuclear cells and other extrahepatic tissues by the highly strand-specific rTth reverse transcriptase PCR. J Virol. 1995;69(12):8079-8083.
64. Marukian S, Jones CT, Andrus L, et al. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology. 2008;48(6):1843-1850.
65. Evans MJ, von Hahn T, Tscherne DM, et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature. 2007;446(7137):801-805. (Pubitemid 46582027)
66. Stamataki Z, Shannon-Lowe C, Shaw J, et al. Hepatitis C virus association with peripheral blood B lymphocytes potentiates viral infection of liver-derived hepatoma cells. Blood. 2009;113(3):585-593.
67. Curry MP, Golden-Mason L, Doherty DG, et al. Expansion of innate CD5pos B cells expressing high levels of CD81 in hepatitis C virus infected liver. J Hepatol. 2003;38(5):674-676.
68. Sugawara Y, Makuuchi M, Kato N, Shimotohno K, Takada K. Enhancement of hepatitis C virus replication by Epstein-Barr virus-encoded nuclear antigen 1. EMBO J. 1999;18(20):5755-5760. (Pubitemid 29486393)
69. Bronowicki J-P, Loriot M-A, Thiers V, Grignon Y, Zignego AL, Bréchot C. Hepatitis C virus persistence in human hematopoietic cells injected into SCID mice. Hepatology. 1998;28(1):211-218. (Pubitemid 28300003)
70. Sung VMH, Shimodaira S, Doughty AL, et al. Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J Virol. 2003;77(3):2134-2146. (Pubitemid 36110026)
71. Machida K, Tsukiyama-Hohara K, Sekiguchi S, et al. Hepatitis C virus and disrupted interferon signaling promote lymphoproliferation via type II CD95 and interleukins. Gastroenterology. 2009;137(1):285-296.
72. Ishikawa T, Shibuya K, Yasui K, Mitamura K, Ueda S. Expression of hepatitis C virus core protein associated with malignant lymphoma in transgenic mice. Comp Immunol Microbiol Infect Dis. 2003;26(2):115-124. (Pubitemid 36221448)
73. Machida K, Cheng KTN, Sung VMH, et al. Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc Natl Acad Sci U S A. 2004;101(12):4262-4267. (Pubitemid 38405917)
74. Rothman KJ, Greenland S. Causation and causal inference in epidemiology. Am J Public Health. 2005;95(Suppl 1):S144-S150. (Pubitemid 41033428)
75. Fearon DT, Carroll MC. Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu Rev Immunol. 2000;18:393-422.
76. + B cells in HCV-associated mixed cryoglobulinemia. Blood. 2008;111(3):1344-1356.
77. Soulas P, Woods A, Jaulhac B, et al. Autoantigen, innate immunity, and T cells cooperate to break B cell tolerance during bacterial infection. J Clin Invest. 2005;115(8):2257-2267. (Pubitemid 41134168)
78. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 2002;416(6881):603-607. (Pubitemid 34406754)
79. Stapleton JT, Chaloner K. GB virus C infection and non-Hodgkin lymphoma: important to know but the jury is out. Int J Cancer. 2010;126(12):2759-2761.
80. Suarez F, Lortholary O, Hermine O, Lecuit M. Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood. 2006;107(8):3034-3044.
81. Gordon SC, Moonka D, Brown KA, et al. Risk for renal cell carcinoma in chronic hepatitis C infection. Cancer Epidemiol Biomarkers Prev. 2010;19(4):1066-1073.