Hepatitis C virus association with peripheral blood B lymphocytes potentiates viral infection of liver-derived hepatoma cells

Blood

Volumn 113, Issue 3, 2009, Pages 585-593

  Stamataki, Zania ^a   Shannon Lowe, Claire ^b   Shaw, Jean ^c   Mutimer, David ^d   Rickinson, Alan B ^b   Gordon, John ^a   Adams, David H ^c   Balfe, Peter ^a   McKeating, Jane A ^a,c  

^a Division of Immunity and Infection   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d QUEEN ELIZABETH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CD81 ANTIGEN; INTERLEUKIN 4; LECTIN; SCAVENGER RECEPTOR BI; VIRUS RECEPTOR;

ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL STIMULATION; CONTROLLED STUDY; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LIVER CELL; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; VIRUS INFECTIVITY; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; DISEASE TRANSMISSION; FLOW CYTOMETRY; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PATHOGENICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; WESTERN BLOTTING;

ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; FLOW CYTOMETRY; HEPACIVIRUS; HEPATITIS C; HUMANS; LIVER NEOPLASMS; RECEPTORS, VIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 60249100063     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-05-158824     Document Type: Article

References (45)

1. Mayo MJ. Extrahepatic manifestations of hepatitis C infection. Am J Med Sci. 2003;325:135-148.
2. Agnello V, Mecucci C, Casato M. Regression of splenic lymphoma after treatment of hepatitis C virus infection. N Engl J Med. 2002;347:2168-2170.
3. De Rosa G, Gobbo ML, De Renzo A, et al. High prevalence of hepatitis C virus infection in patients with B-cell lymphoproliferative disorders in Italy. Am J Hematol. 1997;55:77-82.
4. Misiani R, Bellavita P, Fenili D, et al. Hepatitis C virus infection in patients with essential mixed cryoglobulinemia. Ann Intern Med. 1992;117:573-577.
5. Mazzaro C, Franzin F, Tulissi P, et al. Regression of monoclonal B-cell expansion in patients affected by mixed cryoglobulinemia responsive to alpha-interferon therapy. Cancer. 1996;77:2604-2613.
6. Casato M, Mecucci C, Agnello V, 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.
7. Sansonno D, Lauletta G, De Re V, et al. Intrahepatic B cell clonal expansions and extrahepatic manifestations of chronic HCV infection. Eur J Immunol. 2004;34:126-136.
8. Racanelli V, Sansonno D, Piccoli C, D'Amore FP, Tucci FA, Dammacco F. Molecular characterization of B cell clonal expansions in the liver of chronically hepatitis C virus-infected patients. J Immunol. 2001;167:21-29.
9. Lerat H, Rumin S, Habersetzer F, et al. In vivo tropism of hepatitis C virus genomic sequences in hematopoietic cells: influence of viral load, viral genotype, and cell phenotype. Blood. 1998;91: 3841-3849.
10. Valli MB, Serafino A, Crema A, et al. Transmission in vitro of hepatitis C virus from persistently infected human B-cells to hepatoma cells by cellto- cell contact. J Med Virol. 2006;78:192-201.
11. Pham TN, King D, Macparland SA, et al. Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection. Gastroenterology. 2008;134:812-822.
12. Weng WK, Levy S. Hepatitis C virus (HCV) and lymphomagenesis. Leuk Lymphoma. 2003;44: 1113-1120.
13. Bartosch B, Dubuisson J, Cosset FL. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med. 2003;197:633-642.
14. Hsu M, Zhang J, Flint M, et al. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci U S A. 2003;100:7271-7276.
15. Lindenbach BD, Evans MJ, Syder AJ, et al. Complete replication of hepatitis C virus in cell culture. Science. 2005;309:623-626.
16. Wakita T, Pietschmann T, Kato T, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med. 2005;11: 791-796.
17. Zhong J, Gastaminza P, Cheng G, et al. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A. 2005;102:9294-9299.
18. Scarselli E, Ansuini H, Cerino R, et al. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002;21:5017-5025.
19. Bartosch B, Vitelli A, Granier C, et al. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem. 2003;278: 41624-41630.
20. Pileri P, Uematsu Y, Campagnoli S, et al. Binding of hepatitis C virus to CD81. Science. 1998;282: 938-941.
21. 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;446:801-805.
22. Lozach PY, Amara A, Bartosch B, et al. C-type lectins L-SIGN and DC-SIGN capture and transmit infectious hepatitis C virus pseudotype particles. J Biol Chem. 2004;279:32035-32045.
23. von Hahn T, McKeating JA. In vitro veritas? The challenges of studying hepatitis C virus infectivity in a test tube. J Hepatol. 2007;46:355-358.
24. Shannon-Lowe C, Baldwin G, Feederle R, Bell A, Rickinson A, Delecluse HJ. Epstein-Barr virusinduced B-cell transformation: quantitating events from virus binding to cell outgrowth. J Gen Virol. 2005;86:3009-3019.
25. Lai WK, Curbishley SM, Goddard S, et al. Hepatitis C is associated with perturbation of intrahepatic myeloid and plasmacytoid dendritic cell function. J Hepatol. 2007;47:338-347.
26. Yi M, Villanueva RA, Thomas DL, Wakita T, Lemon SM. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc Natl Acad Sci U S A. 2006;103:2310-2315.
27. Shannon-Lowe CD, Neuhierl B, Baldwin G, Rickinson AB, Delecluse HJ. Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc Natl Acad Sci U S A. 2006; 103:7065-7070.
28. Rappocciolo G, Piazza P, Fuller CL, et al. DCSIGN on B lymphocytes is required for transmission of HIV-1 to T lymphocytes. PLoS Pathog. 2006;2:e70.
29. Martin G, Roy J, Barat C, Ouellet M, Gilbert C, Tremblay MJ. Human immunodeficiency virus type 1-associated CD40 ligand transactivates B lymphocytes and promotes infection of CD4+ T cells. J Virol. 2007;81:5872-5881.
30. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity. 2002;16:135-144.
31. Baker MP, Eliopoulos AG, Young LS, Armitage RJ, Gregory CD, Gordon J. Prolonged phenotypic, functional, and molecular change in group I Burkitt lymphoma cells on short-term exposure to CD40 ligand. Blood. 1998;92:2830-2843.
32. Jakubik JJ, Saifuddin M, Takefman DM, Spear GT. Immune complexes containing human immunodeficiency virus type 1 primary isolates bind to lymphoid tissue B lymphocytes and are infectious for T lymphocytes. J Virol. 2000;74:552-555.
33. Halstead SB. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res. 2003;60:421-467.
34. Barth H, Schnober EK, Neumann-Haefelin C, et al. Scavenger receptor class B is required for hepatitis C virus uptake and cross-presentation by human dendritic cells. J Virol. 2008;82:3466-3479.
35. Boisvert J, He XS, Cheung R, Keeffe EB, Wright T, Greenberg HB. Quantitative analysis of hepatitis C virus in peripheral blood and liver: replication detected only in liver. J Infect Dis. 2001;184:827-835.
36. Carr JM, Hocking H, Li P, Burrell CJ. Rapid and efficient cell-to-cell transmission of human immunodeficiency virus infection from monocyte-derived macrophages to peripheral blood lymphocytes. Virology. 1999;265:319-329.
37. Maillard P, Huby T, Andreo U, Moreau M, Chapman J, Budkowska A. The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins. FASEB J. 2006;20:735-737.
38. Barth H, Ulsenheimer A, Pape GR, et al. Uptake and presentation of hepatitis C virus-like particles by human dendritic cells. Blood. 2005;105:3605-3614.
39. 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;176:3931-3941.
40. Toubi E, Gordon S, Kessel A, et al. Elevated serum B-Lymphocyte activating factor (BAFF) in chronic hepatitis C virus infection: association with autoimmunity. J Autoimmun. 2006;27:134-139.
41. Cambi A, Koopman M, Figdor CG. How C-type lectins detect pathogens. Cell Microbiol. 2005;7: 481-488.
42. Flint M, von Hahn T, Zhang J, et al. Diverse CD81 proteins support hepatitis C virus infection. J Virol. 2006;80:11331-11342.
43. Harris HJ, Farquhar MJ, Mee CJ, et al. CD81 and claudin 1 coreceptor association: role in hepatitis C virus entry. J Virol. 2008;82:5007-5020.
44. Warren A, Le Couteur DG, Fraser R, Bowen DG, McCaughan GW, Bertolino P. T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology. 2006;44:1182-1190.
45. Benseler V, McCaughan GW, Schlitt HJ, Bishop GA, Bowen DG, Bertolino P. The liver: a special case in transplantation tolerance. Semin Liver Dis. 2007;27:194-213.