Specialization of hepatitis C virus envelope glycoproteins for B-lymphocytes in chronically infected patients

Journal of Virology

Volumn 90, Issue 2, 2016, Pages 992-1008

  Douam, Florian ^{a,b,c,d,e,f,h}   Bobay, Louis Marie ^e,i   Maurin, Guillemette ^a,b,c,d,e   Fresquet, Judith ^a,b,c,d,e   Calland, Noémie ^a,b,c,d,e   Maisse, Carine ^e   Durand, Tony ^e   Cosset, François Loïc ^a,b,c,d,e,f   Féray, Cyrille ^g   Lavillette, Dimitri ^a,b,c,d,e,j  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITÉ LYON 1   (France)

^e INSERM   (France)

^f UNIVERSITÉ DE LYON   (France)

^g HENRI MONDOR HOSPITAL   (France)

^h PRINCETON UNIVERSITY   (United States)

ⁱ UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^j INSTITUTE PASTEUR OF SHANGHAI   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E1; GLYCOPROTEIN E2; VIRUS PROTEIN; VIRUS RNA; E1 PROTEIN, HEPATITIS C VIRUS; GLYCOPROTEIN E2, HEPATITIS C VIRUS; VIRUS ENVELOPE PROTEIN;

ARTICLE; B LYMPHOCYTE; CELLS BY BODY ANATOMY; CLINICAL ARTICLE; CONTROLLED STUDY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYLOGENY; PRIORITY JOURNAL; RNA ISOLATION; VIRION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS PARTICLE; VIRUS REPLICATION; CELL LINE; CHRONIC HEPATITIS C; GENETIC TRANSDUCTION; HEPACIVIRUS; ISOLATION AND PURIFICATION; LIVER CELL; METABOLISM; PHYSIOLOGY; VIRAL TROPISM; VIROLOGY;

B-LYMPHOCYTES; CELL LINE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HEPATOCYTES; HUMANS; TRANSDUCTION, GENETIC; VIRAL ENVELOPE PROTEINS; VIRAL TROPISM; VIRUS INTERNALIZATION;

EID: 84954110412     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02516-15     Document Type: Article

References (43)

1. Koike K. 2009. Steatosis, liver injury, and hepatocarcinogenesis in hepatitis C viral infection. J Gastroenterol 44(Suppl 19):S82-S88.
2. Ferri C, Monti M, La Civita L, Longombardo G, Greco F, Pasero G, Gentilini P, Bombardieri S, Zignego AL. 1993. Infection of peripheral blood mononuclear cells by hepatitis C virus in mixed cryoglobulinemia. Blood 82:3701-3704.
3. Zignego AL, Craxi A. 2008. Extrahepatic manifestations of hepatitis C virus infection. Clin Liver Dis 12:611-636, ix. http://dx.doi.org/10.1016/j.cld.2008.03.012.
4. Blackard JT, Kemmer N, Sherman KE. 2006. Extrahepatic replication of HCV: insights into clinical manifestations and biological consequences. Hepatology 44:15-22. http://dx.doi.org/10.1002/hep.21283.
5. Ploss A, Evans MJ. 2012. Hepatitis C virus host cell entry. Curr Opin Virol 2:14-19. http://dx.doi.org/10.1016/j.coviro.2011.12.007.
6. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S. 1998. Binding of hepatitis C virus to CD81. Science 282:938-941. http://dx.doi.org/10.1126/science.282.5390.938.
7. Dao Thi VL, Granier C, Zeisel MB, Guerin M, Mancip J, Granio O, Penin F, Lavillette D, Bartenschlager R, Baumert TF, Cosset FL, Dreux M. 2012. Characterization of hepatitis C virus particle subpopulations reveals multiple usage of the scavenger receptor BI for entry steps. J Biol Chem 287:31242-31257. http://dx.doi.org/10.1074/jbc.M112.365924.
8. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wolk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801-805. http://dx.doi.org/10.1038/nature05654.
9. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, de Jong YP, Rice CM. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882-886. http://dx.doi.org/10.1038/nature07684.
10. Pham TN, Michalak TI. 2008. Occult persistence and lymphotropism of hepatitisCvirus infection. World J Gastroenterol 14:2789-2793. http://dx.doi.org/10.3748/wjg.14.2789.
11. Blackard JT, Smeaton L, Hiasa Y, Horiike N, Onji M, Jamieson DJ, Rodriguez I, Mayer KH, Chung RT. 2005. Detection of hepatitis C virus (HCV) in serum and peripheral-blood mononuclear cells from HCVmonoinfected and HIV/HCV-coinfected persons. J Infect Dis 192:258-265. http://dx.doi.org/10.1086/430949.
12. Durand T, Di Liberto G, Colman H, Cammas A, Boni S, Marcellin P, Cahour A, Vagner S, Feray C. 2010. Occult infection of peripheral B cells by hepatitis C variants which have low translational efficiency in cultured hepatocytes. Gut 59:934-942. http://dx.doi.org/10.1136/gut.2009.192088.
13. Di Liberto G, Roque-Afonso AM, Kara R, Ducoulombier D, Fallot G, Samuel D, Feray C. 2006. Clinical and therapeutic implications of hepatitis C virus compartmentalization. Gastroenterology 131:76-84. http://dx.doi.org/10.1053/j.gastro.2006.04.016.
14. Lerat H, Berby F, Trabaud MA, Vidalin O, Major M, Trepo C, Inchauspe G. 1996. Specific detection of hepatitis C virus minus strand RNA in hematopoietic cells. J Clin Invest 97:845-851. http://dx.doi.org/10.1172/JCI118485.
15. Pal S, Sullivan DG, Kim S, Lai KK, Kae J, Cotler SJ, Carithers RL, Jr, Wood BL, Perkins JD, Gretch DR. 2006. Productive replication of hepatitis C virus in perihepatic lymph nodes in vivo: implications of HCV lymphotropism. Gastroenterology 130:1107-1116. http://dx.doi.org/10.1053/j.gastro.2005.12.039.
16. Morsica G, Tambussi G, Sitia G, Novati R, Lazzarin A, Lopalco L, Mukenge S. 1999. Replication of hepatitis C virus in B lymphocytes (CD19+). Blood 94:1138-1139.
17. Ducoulombier D, Roque-Afonso AM, Di Liberto G, Penin F, Kara R, Richard Y, Dussaix E, Feray C. 2004. Frequent compartmentalization of hepatitis C virus variants in circulating B cells and monocytes. Hepatology 39:817-825. http://dx.doi.org/10.1002/hep.20087.
18. Roque-Afonso AM, Ducoulombier D, Di Liberto G, Kara R, Gigou M, Dussaix E, Samuel D, Feray C. 2005. Compartmentalization of hepatitis C virus genotypes between plasma and peripheral blood mononuclear cells. J Virol 79:6349-6357. http://dx.doi.org/10.1128/JVI.79.10.6349-6357.2005.
19. Mizutani T, Kato N, Ikeda M, Sugiyama K, Shimotohno K. 1996. Long-term human T-cell culture system supporting hepatitis C virus replication. Biochem Biophys Res Commun 227:822-826. http://dx.doi.org/10.1006/bbrc.1996.1591.
20. Mizutani T, Kato N, Saito S, Ikeda M, Sugiyama K, Shimotohno K. 1996. Characterization of hepatitis C virus replication in cloned cells obtained from a human T-cell leukemia virus type 1-infected cell line, MT-2 J Virol 70:7219-7223.
21. Sarhan MA, Pham TN, Chen AY, Michalak TI. 2012. Hepatitis C virus infection of human T lymphocytes is mediated by CD5. J Virol 86:3723-3735. http://dx.doi.org/10.1128/JVI.06956-11.
22. Sung VM, Shimodaira S, Doughty AL, Picchio GR, Can H, Yen TS, Lindsay KL, Levine AM, Lai MM. 2003. 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 77:2134-2146. http://dx.doi.org/10.1128/JVI.77.3.2134-2146.2003.
23. Schramm F, Soulier E, Royer C, Weitten T, Fafi-Kremer S, Brignon N, Meyer N, Ellero B, Woehl-Jaegle ML, Meyer C, Wolf P, Doffoel M, Baumert TF, Stoll-Keller F, Schvoerer E. 2008. Frequent compartmentalization of hepatitis C virus with leukocyte-related amino acids in the setting of liver transplantation. J Infect Dis 198:1656-1666. http://dx.doi.org/10.1086/592986.
24. Sarhan MA, Chen AY, Russell RS, Michalak TI. 2012. Patient-derived hepatitis C virus and JFH-1 clones differ in their ability to infect human hepatoma cells and lymphocytes. J Gen Virol 93:2399-2407. http://dx.doi.org/10.1099/vir.0.045393-0.
25. Marukian S, Jones CT, Andrus L, Evans MJ, Ritola KD, Charles ED, Rice CM, Dustin LB. 2008. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 48:1843-1850. http://dx.doi.org/10.1002/hep.22550.
26. Flint M, Thomas JM, Maidens CM, Shotton C, Levy S, Barclay WS, McKeating JA. 1999. Functional analysis of cell surface-expressed hepatitis C virus E2 glycoprotein. J Virol 73:6782-6790.
27. Flint M, Maidens C, Loomis-Price LD, Shotton C, Dubuisson J, Monk P, Higginbottom A, Levy S, McKeating JA. 1999. Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol 73:6235-6244.
28. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626. http://dx.doi.org/10.1126/science.1114016.
29. Douam F, Dao Thi VL, Maurin G, Fresquet J, Mompelat D, Zeisel MB, Baumert TF, Cosset FL, Lavillette D. 2014. Critical interaction between E1 and E2 glycoproteins determines binding and fusion properties of hepatitis C virus during cell entry. Hepatology 59:776-788. http://dx.doi.org/10.1002/hep.26733.
30. Bartosch B, Dubuisson J, Cosset FL. 2003. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 197:633-642. http://dx.doi.org/10.1084/jem.20021756.
31. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
32. Criscuolo A, Gribaldo S. 2010. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 10:210. http://dx.doi.org/10.1186/1471-2148-10-210.
33. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704. http://dx.doi.org/10.1080/10635150390235520.
34. Tarr AW, Owsianka AM, Szwejk A, Ball JK, Patel AH. 2007. Cloning, expression, and functional analysis of patient-derived hepatitis C virus glycoproteins. Methods Mol Biol 379:177-197. http://dx.doi.org/10.1007/978-1-59745-393-6_13.
35. Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, Wychowski C, Rouille Y. 2006. Hepatitis C virus entry depends on clathrinmediated endocytosis. J Virol 80:6964-6972. http://dx.doi.org/10.1128/JVI.00024-06.
36. Meuleman P, Hesselgesser J, Paulson M, Vanwolleghem T, Desollibere I, Reiser I, Leroux-Roels G. 2008. Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 48:1761-1768. http://dx.doi.org/10.1002/hep.22547.
37. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577-1581. http://dx.doi.org/10.1126/science.1113329.
38. Potel J, Rassam P, Montpellier C, Kaestner L, Werkmeister E, Tews BA, Couturier C, Popescu CI, Baumert TF, Rubinstein E, Dubuisson J, Milhiet PE, Cocquerel L. 2013. EWI-2wint promotes CD81 clustering that abrogates hepatitis C virus entry. Cell Microbiol 15:1234-1252. http://dx.doi.org/10.1111/cmi.12112.
39. Nguyen QT, Leruez-Ville M, Ferriere F, Cohen P, Roulot-Marullo D, Coste T, Deny P, Guillevin L. 1998. Hepatitis C virus genotypes implicated in mixed cryoglobulinemia. J Med Virol 54:20-25. http://dx.doi.org/10.1002/(SICI)1096-9071(199801)54:1<20::AID-JMV4>3.0.CO;2-R.
40. Viazov S, Widell A, Nordenfelt E. 2000. Mixed infection with two types of hepatitis C virus is probably a rare event. Infection 28:21-25. http://dx.doi.org/10.1007/s150100050005.
41. Antonishyn NA, Ast VM, McDonald RR, Chaudhary RK, Lin L, Andonov AP, Horsman GB. 2005. Rapid genotyping of hepatitis C virus by primer-specific extension analysis. J Clin Microbiol 43:5158-5163. http://dx.doi.org/10.1128/JCM.43.10.5158-5163.2005.
42. Di Liberto G, Feray C. 2005. The anhepatic phase of liver transplantation as a model for measuring the extra-hepatic replication of hepatitis C virus. J Hepatol 42:441-443. http://dx.doi.org/10.1016/j.jhep.2005.02.001.
43. Gray RR, Strickland SL, Veras NM, Goodenow MM, Pybus OG, Lemon SM, Fried MW, Nelson DR, Salemi M. 2012. Unexpected maintenance of hepatitis C viral diversity following liver transplantation. J Virol 86: 8432-8439. http://dx.doi.org/10.1128/JVI.00749-12.