Pathogenetic mechanisms of hepatitis C virus-induced B-Cell lymphomagenesis

Clinical and Developmental Immunology

Volumn 2012, Issue , 2012, Pages

  Forghieri, Fabio ^a   Luppi, Mario ^a   Barozzi, Patrizia ^a   Maffei, Rossana ^a   Potenza, Leonardo ^a   Narni, Franco ^a   Marasca, Roberto ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL LYMPHOMA; CARCINOGENESIS; HEPATITIS C; HUMAN; LYMPHOCYTE PROLIFERATION; LYMPHOPROLIFERATIVE DISEASE; NONHODGKIN LYMPHOMA; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; B LYMPHOCYTE; CELL PROLIFERATION; HEPATITIS C VIRUS; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; VIROLOGY;

B-LYMPHOCYTES; CELL PROLIFERATION; HEPACIVIRUS; HEPATITIS C; HUMANS; LYMPHOMA, B-CELL;

EID: 84864933834     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2012/807351     Document Type: Review

References (92)

1. Clarke B., Molecular virology of hepatitis C virus Journal of General Virology 1997 78 10 2397 2410 (Pubitemid 27469980)
2. De Beeck A. O., Cocquerel L., Dubuisson J., Biogenesis of Hepatitis C virus envelope glycoproteins Journal of General Virology 2001 82 11 2589 2595 (Pubitemid 32998636)
3. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., Weiner A. J., Houghton M., Rosa D., Grandi G., Abrignani S., Binding of hepatitis C virus to CD81 Science 1998 282 5390 938 941 (Pubitemid 28507525)
4. Lindenbach B. D., Evans M. J., Syder A. J., Wlk B., Tellinghuisen T. L., Liu C. C., Maruyama T., Hynes R. O., Burton D. R., McKeating J. A., Rice C. M., Virology: complete replication of hepatitis C virus in cell culture Science 2005 309 5734 623 626 (Pubitemid 41033648)
5. Levy S., Todd S. C., Maecker H. T., CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system Annual Review of Immunology 1998 16 89 109 (Pubitemid 28183360)
6. Ghany M. G., Strader D. B., Thomas D. L., Seeff L. B., Diagnosis, management, and treatment of hepatitis C: an update Hepatology 2009 49 4 1335 1374
7. Rosen H. R., Chronic hepatitis C infection New England Journal of Medicine 2011 364 25 2429 2438
8. Amin J., Dore G. J., O'Connell D. L., Bartlett M., Tracey E., Kaldor J. M., Law M. G., Cancer incidence in people with hepatitis B or C infection: a large community-based linkage study Journal of Hepatology 2006 45 2 197 203
9. Strauss R., Trner A., Duberg A. S., Hultcrantz R., Ekdahl K., Hepatocellular carcinoma and other primary liver cancers in hepatitis C patients in Swedena low endemic country Journal of Viral Hepatitis 2008 15 7 531 537 (Pubitemid 351798991)
10. Pozzato G., Mazzaro C., Crovatto M., Modolo M. L., Ceselli S., Mazzi G., Sulfaro S., Franzin F., Tulissi P., Moretti M., Santini G. F., Low-grade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia Blood 1994 84 9 3047 3053 (Pubitemid 24328097)
11. Agnello V., Chung R. T., Kaplan L. M., A role for hepatitis C virus infection in Type II cryoglobulinemia New England Journal of Medicine 1992 327 21 1490 1495
12. Ferri C., Zignego A. L., Pileri S. A., Cryoglobulins Journal of Clinical Pathology 2002 55 1 4 13 (Pubitemid 34081673)
13. Ferri C., Caracciolo F., Zignego A. L., La Civita L., Monti M., Longombardo G., Lombardini F., Greco F., Capochiani E., Mazzoni A., Mazzaro C., Pasero G., Hepatitis C virus infection in patients with non-Hodgkin's lymphoma British Journal of Haematology 1994 88 2 392 394 (Pubitemid 24318191)
14. Mele A., Pulsoni A., Bianco E., Musto P., Szklo A., Grazia Sanpaolo M., Lannitto E., De Renzo A., Martino B., Liso V., Andrizzi C., Pusterla S., Dore F., Maresca M., Rapicetta M., Marcucci F., Mandelli F., Franceschi S., Hepatitis C virus and B-cell non-Hodgkin lymphomas: an Italian multicenter case-control study Blood 2003 102 3 996 999 (Pubitemid 36917795)
15. Luppi M., Longo G., Ferrari M. G., Barozzi P., Marasca R., Morselli M., Valenti C., Mascia T., Vandelli L., Vallisa D., Cavanna L., Torelli G., Clinico-pathological characterization of hepatitis C virus-related B- cell non-Hodgkin's lymphomas without symptomatic cryoglobulinemia Annals of Oncology 1998 9 5 495 498 (Pubitemid 28270636)
16. Marcucci F., Mele A., Hepatitis viruses and non-Hodgkin lymphoma: epidemiology, mechanisms of tumorigenesis, and therapeutic opportunities Blood 2011 117 6 1792 1798
17. Evans A. S., Mueller N. E., Viruses and cancer. Causal associations Annals of Epidemiology 1990 1 1 71 92
18. Cocco P., Piras G., Monne M., Uras A., Gabbas A., Ennas M. G., Palmas A., Murineddu M., Collu S., Melis M., Rais M., Todde P., Cabras M. G., Angelucci E., Massarelli G., Nieters A., Risk of malignant lymphoma following viral hepatitis infection International Journal of Hematology 2008 87 5 474 483
19. Pellicelli A. M., Marignani M., Zoli V., Hepatitis C virus-related subtypes in non Hodgkins lymphoma World Journal of Hepatology 2011 3 278 284
20. Mizorogi F., Hiramoto J., Nozato A., Takekuma Y., Nagayama K., Tanaka T., Takagi K., Hepatitis C virus infection in patients with B-cell non-Hodgkin's lymphoma Internal Medicine 2000 39 2 112 117 (Pubitemid 30187234)
21. Goldman L., Ezzat S., Mokhtar N., Abdel-Hamid A., Fowler N., Gouda I., Eissa S. A. L., Abdel-Hamid M., Loffredo C. A., Viral and non-viral risk factors for non-Hodgkin's lymphoma in Egypt: heterogeneity by histological and immunological subtypes Cancer Causes and Control 2009 20 6 981 987
22. Hausfater P., Cacoub P., Sterkers Y., Thibault V., Amoura Z., Nguyen L., Ghillani P., Leblond V., Piette J. C., Hepatitis C virus infection and lymphoproliferative diseases: prospective study on 1,576 patients in France American Journal of Hematology 2001 67 3 168 171 (Pubitemid 32538614)
23. Collier J. D., Zanke B., Moore M., Kessler G., Krajden M., Shepherd F., Heathcote J., No association between hepatitis C and B-cell lymphoma Hepatology 1999 29 4 1259 1261 (Pubitemid 29168763)
24. Sy T., Jamal M. M., Epidemiology of hepatitis C virus (HCV) infection International Journal of Medical Sciences 2006 3 2 41 46
25. Gisbert J. P., Garca-Buey L., Pajares M. J., Moreno-Otero R., Prevalence of hepatitis C virus infection in B-cell non-Hodgkin's lymphoma: systematic, review and meta-analysis Gastroenterology 2003 125 6 1723 1732 (Pubitemid 37500437)
26. Luppi M., Barozzi P., Potenza L., Riva G., Morselli M., Torelli G., Is it now the time to update treatment protocols for lymphomas with new anti-virus systems? Leukemia 2004 18 10 1572 1575 (Pubitemid 39386330)
27. Dal Maso L., Franceschi S., Hepatitis C virus and risk of lymphoma and other lymphoid neoplasms: a meta-analysis of epidemiologic studies Cancer Epidemiology Biomarkers and Prevention 2006 15 11 2078 2085 (Pubitemid 44877029)
28. Matsuo K., Kusano A., Sugumar A., Nakamura S., Tajima K., Mueller N. E., Effect of hepatitis C virus infection on the risk of non-Hodgkin's lymphoma: a meta-analysis of epidemiological studies Cancer Science 2004 95 9 745 752 (Pubitemid 39335095)
29. Hartridge-Lambert S. K., Stein E. M., Markowitz A. J., Portlock C. S., Hepatitis C and non-Hodgkin lymphoma: the clinical perspective Hepatology 2012 55 634 641
30. Martyak L. A., Yeganeh M., Saab S., Hepatitis C and lymphoproliferative disorders: from mixed cryoglobulinemia to non-Hodgkin's lymphoma Clinical Gastroenterology and Hepatology 2009 7 8 900 905
31. Besson C., Cantoni D., Lepage E., Pol S., Morel P., Lederlin P., Van Hoof A., Tilly H., Gaulard P., Coiffier B., Gisselbrecht C., Brousse N., Reyes F., Hermine O., Characteristics and outcome of diffuse large B-cell lymphoma in hepatitis C virus-positive patients in LNH 93 and LNH 98 groupe d'etude des lymphomes de l'adulte programs Journal of Clinical Oncology 2006 24 6 953 960 (Pubitemid 46638850)
32. Ennishi D., Maeda Y., Niitsu N., Kojima M., Izutsu K., Takizawa J., Kusumoto S., Okamoto M., Yokoyama M., Takamatsu Y., Sunami K., Miyata A., Murayama K., Sakai A., Matsumoto M., Shinagawa K., Takaki A., Matsuo K., Kinoshita T., Tanimoto M., Hepatic toxicity and prognosis in hepatitis C virus-infected patients with diffuse large B-cell lymphoma treated with rituximab-containing chemotherapy regimens: a Japanese multicenter analysis Blood 2010 116 24 5119 5125
33. Luppi M., Ferrari M. G., Torelli G., Hepatitis C virus genotype distribution in B-cell non-Hodgkin lymphoma Annals of Internal Medicine 1998 128 7 602 (Pubitemid 28177675)
34. Torres H. A., Nevah-Rubin M., Barnett B. J., Variation of hepatitis C virus genotype distribution between geographically related patients: a retrospective multicenter Journal of Clinical Oncology 2011 29 supplement, ASCO Meeting Abstract no. 8052
35. Hermine O., Lefrre F., Bronowicki J. P., Mariette X., Jondeau K., Eclache-Saudreau V., Delmas B., Valensi F., Cacoub P., Brechot C., Varet B., Troussard X., Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection New England Journal of Medicine 2002 347 2 89 94 (Pubitemid 34753478)
36. Vallisa D., Bernuzzi P., Arcaini L., Sacchi S., Callea V., Marasca R., Lazzaro A., Trabacchi E., Anselmi E., Arcari A. L., Moroni C., Bert R., Lazzarino M., Cavanna L., Role of anti-hepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-Hodgkin's lymphoma: a multicenter Italian experience Journal of Clinical Oncology 2005 23 3 468 473 (Pubitemid 46224223)
37. Arcaini L., Vallisa D., Merli M., Hematological response to antiviral therapy in 94 patients with indolent B-cell lymphomas associated with hepatitis C virus infection: a study of the Fondazione Italiana Linfomi (FIL) Annals of Oncology 2011 22 Lugano Meeting Abstract no. 138 128 129
38. Gisbert J. P., Garca-Buey L., Pajares J. M., Moreno-Otero R., Systematic review: regression of lymphoproliferative disorders after treatment for hepatitis C infection Alimentary Pharmacology and Therapeutics 2005 21 6 653 662 (Pubitemid 40468993)
39. La Mura V., Renzo A. D., Perna F., D'Agostino D., Masarone M., Romano M., Bruno S., Torella R., Persico M., Antiviral therapy after complete response to chemotherapy could be efficacious in HCV-positive non-Hodgkin's lymphoma Journal of Hepatology 2008 49 4 557 563
40. Kawamura Y., Ikeda K., Arase Y., Yatsuji H., Sezaki H., Hosaka T., Akuta N., Kobayashi M., Suzuki F., Suzuki Y., Kumada H., Viral Elimination Reduces Incidence of Malignant Lymphoma in Patients with Hepatitis C American Journal of Medicine 2007 120 12 1034 1041 (Pubitemid 350166219)
41. Poordad F., McCone J., Bacon B. R., Bruno S., Manns M. P., Sulkowski M. S., Jacobson I. M., Reddy K. R., Goodman Z. D., Boparai N., DiNubile M. J., Sniukiene V., Brass C. A., Albrecht J. K., Bronowicki J. P., Boceprevir for untreated chronic HCV genotype 1 infection New England Journal of Medicine 2011 364 13 1195 1206
42. Jacobson I. M., McHutchison J. G., Dusheiko G., Di Bisceglie A. M., Reddy K. R., Bzowej N. H., Marcellin P., Muir A. J., Ferenci P., Flisiak R., George J., Rizzetto M., Shouval D., Sola R., Terg R. A., Yoshida E. M., Adda N., Bengtsson L., Sankoh A. J., Kieffer T. L., George S., Kauffman R. S., Zeuzem S., Telaprevir for previously untreated chronic hepatitis C virus infection New England Journal of Medicine 2011 364 25 2405 2416
43. Pawlotsky J., The results of phase III clinical trials with telaprevir and boceprevir presented at the liver meeting 2010: a new standard of care for hepatitis C virus genotype 1 infection, but with issues still pending Gastroenterology 2011 140 3 746 754
44. Nooka A., Shenoy P. J., Sinha R., Hepatitis C reactivation in patients who have diffuse large B-cell lymphoma treated with rituximab: a case report and review of literature Clinical Lymphoma Myeloma and Leukemia 2011 11 379 384
45. Merli M., Spina M., Luminari S., Prognostic models to predict survival in indolent and aggressive non-Hodgkin's lymphomas associated with hepatitis C virus infection: a multicenter Italian study on 1, 043 patients 116 Proceedings of the 52nd American Society of Hematology Annual Meeting 2010 2821
46. Vento S., Cainelli F., Mirandola F., Cosco L., Di Perri G., Solbiati M., Ferraro T., Concia E., Fulminant hepatitis on withdrawal of chemotherapy in carriers of hepatitis C virus Lancet 1996 347 8994 92 93 (Pubitemid 26017855)
47. Cox M. C., Aloe-Spiriti M. A., Cavalieri E., HCV infection, B-cell non-Hodgkins lymphoma and immunochemotherapy: evidence and open questions World Journal of Gastrointestinal Oncology 2012 15 46 53
48. Landau D. A., Saadoun D., Calabrese L. H., Cacoub P., The pathophysiology of HCV induced B-cell clonal disorders Autoimmunity Reviews 2007 6 8 581 587 (Pubitemid 47374619)
49. Stathis A., Bertoni F., Zucca E., Treatment of gastric marginal zone lymphoma of MALT type Expert Opinion on Pharmacotherapy 2010 11 13 2141 2152
50. Zullo A., Hassan C., Andriani A., Cristofari F., Bassanelli C., Spinelli G. P., Tomao S., Morini S., Treatment of low-grade gastric MALT-lymphoma unresponsive to Helicobacter pylori therapy: a pooled-data analysis Medical Oncology 2010 27 2 291 295
51. De Re V., De Vita S., Marzotto A., Pre-malignant and malignant lymphoproliferations in an HCV-infected type II mixed cryoglobulinemic patient are sequential phases of an antigen-driven pathological process International Journal of Cancer 2000 87 211 216 (Pubitemid 30434347)
52. Gorevic P. D., Frangione B., Mixed cryoglobulinemia cross-reactive idiotypes: implications for the relationship of MC to rheumatic and lymphoproliferative diseases Seminars in Hematology 1991 28 2 79 94
53. Marasca R., Vaccari P., Luppi M., Zucchini P., Castelli I., Barozzi P., Cuoghi A., Torelli G., Immunoglobulin gene mutations and frequent use of VH1-69 and VH4-34 segments in hepatitis C virus-positive and hepatitis C virus-negative nodal marginal zone B-cell lymphoma American Journal of Pathology 2001 159 1 253 261 (Pubitemid 33704210)
54. Allander T., Drakenberg K., Beyene A., Rosa D., Abrignani S., Houghton M., Widell A., Grillner L., Persson M. A. A., Recombinant human monoclonal antibodies against different conformational epitopes of the E2 envelope glycoprotein of hepatitis C virus that inhibit its interaction with CD81 Journal of General Virology 2000 81 10 2451 2459
55. Chan C. H., Hadlock K. G., Foung S. K. H., Levy S., VH1-69 gene is preferentially used 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)
56. De Re V., De Vita S., Marzotto A., Rupolo M., Gloghini A., Pivetta B., Gasparotto D., Carbone A., Boiocchi M., 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 factorn Producing cells that occur mainly in type II cryoglobulinemia Blood 2000 96 10 3578 3584
57. Lesniewski R., Okasinski G., Carrick R., Van Sant C., Desai S., Johnson R., Scheffel J., Moore B., Mushahwar I., Antibody to hepatitis C virus second envelope (HCV-E2) glycoprotein: a new marker of HCV infection closely associated with viremia Journal of Medical Virology 1995 45 4 415 422
58. Quinn E. R., Chan C. H., Hadlock K. G., Foung S. K. H., 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
59. Hermouet S., Corre I., Gassin M., Bigot-Corbel E., Sutton C. A., Casey J. W., Hepatitis C virus, human herpesvirus 8, and the development of plasma-cell leukemia New England Journal of Medicine 2003 348 2 178 179 (Pubitemid 36056732)
60. Matsumoto A. K., Martin D. R., Carter R. H., Klickstein L. B., Ahearn J. M., Fearon D. T., Functional dissection of the CD21/CD19/TAPA-1/Leu-13 complex of B lymphocytes Journal of Experimental Medicine 1993 178 4 1407 1417 (Pubitemid 23277372)
61. Carter R. H., Fearon D. T., CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes Science 1992 256 5053 105 107
62. Rosa D., Saletti G., De Gregorio E., Zorat F., Comar C., D'Oro U., Nuti S., Houghton M., Barnaba V., Pozzato G., Abrignani S., Activation of nave B lymphocytes via CD81, a pathogenetic mechanism for hepatitis C virus-associated B lymphocyte disorders Proceedings of the National Academy of Sciences of the United States of America 2005 102 51 18544 18549 (Pubitemid 43011262)
63. Wack A., Soldaini E., Tseng -TK C., Nuti S., Klimpel G. R., Abrignani S., Binding of the hepatitis C virus envelope protein E2 to CD81 provides a costimulatory signal for human T cells European Journal of Immunology 2001 31 166 175
64. Poetsch M., Weber-Matthiesen K., Plendl H. J., Grote W., Schlegelberger B., Detection of the t(14:18) chromosomal translocation by interphase cytogenetics with Yeast-artificial-chromosome probes in follicular lymphoma and nonneoplastic lymphoproliferation Journal of Clinical Oncology 1996 14 3 963 969
65. Chen Z., Zhu Y., Ren Y., Tong Y., Hua X., Zhu F., Huang L., Liu Y., Luo Y., Lu W., Zhao P., Qi Z., Hepatitis C virus protects human B lymphocytes from fas-mediated apoptosis via E2-CD81 engagement PLoS One 2011 6 4
66. Machida K., Cheng K. T. H., Pavio N., Sung V. M. H., Lai M. M. C., Hepatitis C virus E2-CD81 interaction induces hypermutation of the immunoglobulin gene in B cells Journal of Virology 2005 79 13 8079 8089 (Pubitemid 40853511)
67. Ito M., Kusunoki H., Mochida K., HCV infection and B-cell lymphomagenesis Advances in Hematology 2011 2011 8
68. Houghton M., Weiner A., Han J., Kuo G., Choo Q. L., Molecular biology of the hepatitis C viruses: implications for diagnosis, development and control of viral disease Hepatology 1991 14 2 381 388
69. Han J. H., Shyamala V., Richman K. H., Brauer M. J., Irvine B., Urdea M. S., Tekamp-Olson P., Kuo G., Choo Q. L., Houghton M., Characterization of the terminal regions of hepatitis C viral RNA: identification of conserved sequences in the 5' untranslated region and poly(A) tails at the 3' end Proceedings of the National Academy of Sciences of the United States of America 1991 88 5 1711 1715 (Pubitemid 21916295)
70. Zignego A. L., Macchia D., Monti M., Thiers V., Mazzetti M., Foschi M., Maggi E., Romagnani S., Gentilini P., Brechot C., Infection of peripheral mononuclear blood cells by hepatitis C virus Journal of Hepatology 1992 15 3 382 386
71. Ferri C., Monti M., La Civita L., Longombardo G., Greco F., Pasero G., Gentilini P., Bombardieri S., Zignego A. L., Infection of peripheral blood mononuclear cells by hepatitis C virus in mixed cryoglobulinemia Blood 1993 82 12 3701 3704 (Pubitemid 24006053)
72. Inokuchi M., Ito T., Uchikoshi M., Shimozuma Y., Morikawa K., Nozawa H., Shimazaki T., Hiroishi K., Miyakawa Y., Imawari M., Infection of B cells with hepatitis C virus for the development of lymphoproliferative disorders in patients with chronic hepatitis C Journal of Medical Virology 2009 81 4 619 627
73. Morsica G., Tambussi G., Sitia G., Novati R., Lazzarin A., Lopalco L., Mukenge S., Replication of hepatitis C virus in B lymphocytes (CD19+) Blood 1999 94 3 1138 1139 (Pubitemid 29361849)
74. Sansonno D., Iacobelli A. R., Cornacchiulo V., Iodice G., Dammacco F., Detection of hepatitis C virus (HCV) proteins by immunofluorescence and HCV RNA genomic sequences by non-isotopic in situ hybridization in bone marrow and peripheral blood mononuclear cells of chronically HCV-infected patients Clinical and Experimental Immunology 1996 103 3 414 421
75. Lanford R. E., Chavez D., Chisari F. V., 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 Journal of Virology 1995 69 12 8079 8083
76. Willems M., Moshage H., Sing Hiem Yap, PCR and detection of negative HCV RNA strands Hepatology 1993 17 3 526 (Pubitemid 23072832)
77. Marukian S., Jones C. T., Andrus L., Evans M. J., Ritola K. D., Charles E. D., Rice C. M., Dustin L. B., Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells Hepatology 2008 48 6 1843 1850
78. Stamataki Z., Shannon-Lowe C., Shaw J., Mutimer D., Rickinson A. B., Gordon J., Adams D. H., Balfe P., McKeating J. A., Hepatitis C virus association with peripheral blood B lymphocytes potentiates viral infection of liver-derived hepatoma cells Blood 2009 113 3 585 593
79. Curry M. P., Golden-Mason L., Doherty D. G., Deignan T., Norris S., Duffy M., Nolan N., Hall W., Hegarty J. E., O'Farrelly C., Expansion of innate CD5pos B cells expressing high levels of CD81 in hepatitis C virus infected liver Journal of Hepatology 2003 38 5 642 650 (Pubitemid 36560650)
80. 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 Journal 1999 18 20 5755 5760 (Pubitemid 29486393)
81. Levine A. M., Shimodaira S., Lai M. M. C., Treatment of HCV-related mantle-cell lymphoma with ribavirin and pegylated interferon alfa New England Journal of Medicine 2003 349 21 2078 2079 (Pubitemid 37448938)
82. Ohsawa M., Tomita Y., Hashimoto M., Kanno H., Aozasa K., Hepatitis C viral genome in a subset of primary hepatic lymphomas Modern Pathology 1998 11 5 471 478 (Pubitemid 28224450)
83. Sung M. H. V., Shimodaira S., Doughty A. L., Picchio G. R., Can H., Benedict Yen T. S., Lindsay K. L., Levine A. M., Lai M. M. C., Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection Journal of Virology 2003 77 3 2134 2146 (Pubitemid 36110026)
84. Caussin-Schwemling C., Schmitt C., Stoll-Keller F., Study of the infection of human blood derived monocyte/macrophages with hepatitis C virus in vitro Journal of Medical Virology 2001 65 14 22
85. Greeve J., Philipsen A., Krause K., Klapper W., Heidorn K., Castle B. E., Janda J., Marcu K. B., Parwaresch R., Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas Blood 2003 101 9 3574 3580 (Pubitemid 36857944)
86. Navas M. C., Fuchs A., Schvoerer E., Bohbot A., Aubertin A. M., Stoll-Keller F., Dendritic cell susceptibility to hepatitis C virus genotype 1 infection Journal of Medical Virology 2002 67 2 152 161 (Pubitemid 34493429)
87. Tsukiyama-Kohara K., Sekiguchi S., Kasama Y., Salem N. E., Machida K., Kohara M., Hepatitis C virus-related lymphomagenesis in a mouse model ISRN Hematology 2011 2011 8
88. Ito M., Murakami K., Suzuki T., Mochida K., Suzuki M., Ikebuchi K., Yamaguchi K., Mizuochi T., Enhanced expression of lymphomagenesis-related genes in peripheral blood B cells of chronic hepatitis C patients Clinical Immunology 2010 135 3 459 465
89. Machida K., Cheng K. T. N., Sung V. M. H., Shimodaira S., Lindsay K. L., Levinet A. M., Lai M. Y., Lai M. M. C., Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes Proceedings of the National Academy of Sciences of the United States of America 2004 101 12 4262 4267 (Pubitemid 38405917)
90. Kitay-Cohen Y., Amiel A., Hilzenrat N., Buskila D., Ashur Y., Fejgin M., Gaber E., Safadi R., Tur-Kaspa R., Lishner M., Bcl-2 rearrangement in patients with chronic hepatitis C associated with essential mixed cryoglobulinemia type II Blood 2000 96 8 2910 2912
91. Zignego A. L., Ferri C., Giannelli F., Giannini C., Caini P., Monti M., Marrocchi M. E., Di Pietro E., La Villa G., Laffi G., Gentilini P., Prevalence of bcl-2 rearrangement in patients with hepatitis C virus-related mixed cryoglobulinemia with or without B-cell lymphomas Annals of Internal Medicine 2002 137 7 571 580
92. Swaminathan S., Molecular biology of Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus Seminars in Hematology 2003 40 2 107 115 (Pubitemid 36461088)