Apolipoprotein(a) inhibits hepatitis C virus entry through interaction with infectious particles

Hepatology

Volumn 65, Issue 6, 2017, Pages 1851-1864

  Oliveira, Catarina ^a   Fournier, Carole ^a   Descamps, Véronique ^a   Morel, Virginie ^a   Scipione, Corey A ^b   Romagnuolo, Rocco ^c   Koschinsky, Marlys L ^b   Boullier, Agnès ^d   Marcelo, Paulo ^a   Domon, Jean Marc ^a   Brochot, Etienne ^a   Duverlie, Gilles ^a,e   Francois, Catherine ^a   Castelain, Sandrine ^a   Helle, Francois ^a  

^a UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF WINDSOR   (Canada)

^d INSERM   (France)

^e AMIENS UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A; APOLIPOPROTEIN B; IODIXANOL; LOW DENSITY LIPOPROTEIN; RECOMBINANT PROTEIN; VERY LOW DENSITY LIPOPROTEIN; LIPOPROTEIN A; LYSINE; PROTEIN BINDING;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; COVALENT BOND; DISULFIDE BOND; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; KRINGLE DOMAIN; LIPID METABOLISM; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; RNA REPLICATION; SERUM; SIZE EXCLUSION CHROMATOGRAPHY; VIRUS ENTRY; VIRUS INHIBITION; VIRUS PARTICLE; BLOOD; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; HEPACIVIRUS; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; LIVER CELL; METABOLISM; PROCEDURES; SENSITIVITY AND SPECIFICITY; STRUCTURE ACTIVITY RELATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; IMMUNOPRECIPITATION; LIPOPROTEIN(A); LYSINE; PROTEIN BINDING; SENSITIVITY AND SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85018983581     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.29096     Document Type: Article

References (41)

1. Simmonds P. The origin of hepatitis C virus. Curr Top Microbiol Immunol 2013;369:1-15.
2. Lohmann V, Bartenschlager R. On the history of hepatitis C virus cell culture systems. J Med Chem 2014;57:1627-1642.
3. Steinmann E, Pietschmann T. Cell culture systems for hepatitis C virus. Curr Top Microbiol Immunol 2013;369:17-48.
4. Bartenschlager R, Penin F, Lohmann V, Andre P. Assembly of infectious hepatitis C virus particles. Trends Microbiol 2011;19:95-103.
5. Lindenbach BD. Virion assembly and release. Curr Top Microbiol Immunol 2013;369:199-218.
6. Douam F, Lavillette D, Cosset FL. The mechanism of HCV entry into host cells. Prog Mol Biol Transl Sci 2015;129:63-107.
7. Merz A, Long G, Hiet MS, Brugger B, Chlanda P, Andre P, et al. Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J Biol Chem 2011;286:3018-3032.
8. Schmidt K, Noureen A, Kronenberg F, Utermann G. Structure, function, and genetics of lipoprotein(a). J Lipid Res 2016;57:1339-1359.
9. Dube JB, Boffa MB, Hegele RA, Koschinsky ML. Lipoprotein(a): more interesting than ever after 50 years. Curr Opin Lipidol 2012;23:133-140.
10. Marcovina SM, Albers JJ. Lipoprotein (a) measurements for clinical application. J Lipid Res 2016;57:526-537.
11. Bergmark C, Dewan A, Orsoni A, Merki E, Miller ER, Shin MJ, et al. A novel function of lipoprotein [a] as a preferential carrier of oxidized phospholipids in human plasma. J Lipid Res 2008;49:2230-2239.
12. Helle F, Brochot E, Fournier C, Descamps V, Izquierdo L, Hoffmann TW, et al. Permissivity of primary human hepatocytes and different hepatoma cell lines to cell culture adapted hepatitis C virus. PLoS One 2013;8:e70809.
13. Romagnuolo R, Scipione CA, Boffa MB, Marcovina SM, Seidah NG, Koschinsky ML. Lipoprotein(a) catabolism is regulated by proprotein convertase subtilisin/kexin type 9 through the low density lipoprotein receptor. J Biol Chem 2015;290:11649-11662.
14. Helle F, Vieyres G, Elkrief L, Popescu CI, Wychowski C, Descamps V, et al. Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J Virol 2010;84:11905-11915.
15. Tao J, Kang KD, Hall SD, Laube AH, Liu J, Renfrow MB, et al. The serum very-low-density lipoprotein serves as a restriction factor against hepatitis C virus infection. J Virol 2015;89:6782-6791.
16. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996;68:850-858.
17. Brunner C, Lobentanz EM, Petho-Schramm A, Ernst A, Kang C, Dieplinger H, et al. The number of identical kringle IV repeats in apolipoprotein(a) affects its processing and secretion by HepG2 cells. J Biol Chem 1996;271:32403-32410.
18. Castelain S, Descamps V, Thibault V, Francois C, Bonte D, Morel V, et al. TaqMan amplification system with an internal positive control for HCV RNA quantitation. J Clin Virol 2004;31:227-234.
19. Koschinsky ML, Tomlinson JE, Zioncheck TF, Schwartz K, Eaton DL, Lawn RM. Apolipoprotein(a): expression and characterization of a recombinant form of the protein in mammalian cells. Biochemistry 1991;30:5044-5051.
20. Becker L, Cook PM, Koschinsky ML. Identification of sequences in apolipoprotein(a) that maintain its closed conformation: a novel role for apo(a) isoform size in determining the efficiency of covalent Lp(a) formation. Biochemistry 2004;43:9978-9988.
21. Chang KS, Jiang J, Cai Z, Luo G. Human apolipoprotein E is required for infectivity and production of hepatitis C virus in cell culture. J Virol 2007;81:13783-13793.
22. Owen DM, Huang H, Ye J, Gale M Jr. Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology 2009;394:99-108.
23. Hishiki T, Shimizu Y, Tobita R, Sugiyama K, Ogawa K, Funami K, et al. Infectivity of hepatitis C virus is influenced by association with apolipoprotein E isoforms. J Virol 2010;84:12048-12057.
24. Meunier JC, Engle RE, Faulk K, Zhao M, Bartosch B, Alter H, et al. Evidence for cross-genotype neutralization of hepatitis C virus pseudo-particles and enhancement of infectivity by apolipoprotein C1. Proc Natl Acad Sci USA 2005;102:4560-4565.
25. Dreux M, Boson B, Ricard-Blum S, Molle J, Lavillette D, Bartosch B, et al. The exchangeable apolipoprotein ApoC-I promotes membrane fusion of hepatitis C virus. J Biol Chem 2007;282:32357-32369.
26. Sun HY, Lin CC, Lee JC, Wang SW, Cheng PN, Wu IC, et al. Very low-density lipoprotein/lipo-viro particles reverse lipoprotein lipase-mediated inhibition of hepatitis C virus infection via apolipoprotein C-III. Gut 2013;62:1193-1203.
27. Sultanik P, Mallet V, Lagaye S, Casrouge A, Dorival C, Barthe Y, et al. Plasma apolipoprotein H limits HCV replication and associates with response to NS3 protease inhibitors-based therapy. Liver Int 2015;35:1833-1844.
28. Stefas I, Tigrett S, Dubois G, Kaiser M, Lucarz E, Gobby D, et al. Interactions between hepatitis C virus and the human apolipoprotein H acute phase protein: a tool for a sensitive detection of the virus. PLoS One 2015;10:e0140900.
29. Boyer A, Dumans A, Beaumont E, Etienne L, Roingeard P, Meunier JC. The association of hepatitis C virus glycoproteins with apolipoproteins E and B early in assembly is conserved in lipoviral particles. J Biol Chem 2014;289:18904-18913.
30. Saeed M, Andreo U, Chung HY, Espiritu C, Branch AD, Silva JM, et al. SEC14L2 enables pan-genotype HCV replication in cell culture. Nature 2015;524:471-475.
31. Harak C, Meyrath M, Romero-Brey I, Schenk C, Gondeau C, Schult P, et al. Tuning a cellular lipid kinase activity adapts hepatitis C virus to replication in cell culture. Nat Microbiol 2016;2:16247.
32. Steenbergen RH, Joyce MA, Thomas BS, Jones D, Law J, Russell R, et al. Human serum leads to differentiation of human hepatoma cells, restoration of very-low-density lipoprotein secretion, and a 1000-fold increase in HCV Japanese fulminant hepatitis type 1 titers. Hepatology 2013;58:1907-1917.
33. Catanese MT, Graziani R, von Hahn T, Moreau M, Huby T, Paonessa G, et al. High-avidity monoclonal antibodies against the human scavenger class B type I receptor efficiently block hepatitis C virus infection in the presence of high-density lipoprotein. J Virol 2007;81:8063-8071.
34. Lavillette D, Morice Y, Germanidis G, Donot P, Soulier A, Pagkalos E, et al. Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J Virol 2005;79:6023-6034.
35. Gondeau C, Briolotti P, Razafy F, Duret C, Rubbo PA, Helle F, et al. In vitro. infection of primary human hepatocytes by HCV-positive sera: insights on a highly relevant model. Gut 2014;63:1490-1500.
36. Tarr AW, Urbanowicz RA, Ball JK. The role of humoral innate immunity in hepatitis C virus infection. Viruses 2012;4:1-27.
37. Ball JK, Tarr AW, McKeating JA. The past, present and future of neutralizing antibodies for hepatitis C virus. Antiviral Res 2014;105:100-111.
38. Lavie M, Voisset C, Vu-Dac N, Zurawski V, Duverlie G, Wychowski C, et al. Serum amyloid A has antiviral activity against hepatitis C virus by inhibiting virus entry in a cell culture system. Hepatology 2006;44:1626-1634.
39. Andreo U, Maillard P, Kalinina O, Walic M, Meurs E, Martinot M, et al. Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell Microbiol 2007;9:2445-2456.
40. von Hahn T, Lindenbach BD, Boullier A, Quehenberger O, Paulson M, Rice CM, et al. Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology 2006;43:932-942.
41. Westhaus S, Bankwitz D, Ernst S, Rohrmann K, Wappler I, Agne C, et al. Characterization of the inhibition of hepatitis C virus entry by in vitro-generated and patient-derived oxidized low-density lipoprotein. Hepatology 2013;57:1716-1724.