A targeted functional RNA interference screen uncovers glypican 5 as an entry factor for hepatitis B and D viruses

Hepatology

Volumn 63, Issue 1, 2016, Pages 35-48

  Verrier, Eloi R ^a,b   Colpitts, Che C ^a,b   Bach, Charlotte ^a,b   Heydmann, Laura ^a,b   Weiss, Amélie ^c   Renaud, Mickaël ^c   Durand, Sarah C ^a,b   Habersetzer, François ^d   Durantel, David ^e   Abou Jaoudé, Georges ^f   López Ledesma, Maria M ^g   Felmlee, Daniel J ^a,b   Soumillon, Magali ^h   Croonenborghs, Tom ^i,j   Pochet, Nathalie ⁱ   Nassal, Michael ^k   Schuster, Catherine ^a,b   Brino, Laurent ^c   Sureau, Camille ^f   Zeisel, Mirjam B ^a,b   Baumert, Thomas F ^a,b,d   more..

^a Hopitaux Universitaires de Strasbourg   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d HÔPITAL CIVIL   (France)

^e UNIVERSITÉ DE LYON   (France)

^f INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

^g UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^h BROAD INSTITUTE OF MIT AND HARVARD   (United States)

ⁱ HARVARD MEDICAL SCHOOL   (United States)

^j UNIVERSITY OF LEUVEN   (Belgium)

^k UNIVERSITY OF FREIBURG   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLYPICAN; GLYPICAN 5; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE SILENCING; HEPATITIS B VIRUS; HEPATITIS DELTA VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; VIRION; VIRUS CELL INTERACTION; VIRUS ENTRY; CELL CULTURE; PATHOGENICITY; PHYSIOLOGY;

CELLS, CULTURED; GLYPICANS; HEPATITIS B VIRUS; HEPATITIS DELTA VIRUS; HUMANS; RNA, UNTRANSLATED; VIRUS INTERNALIZATION;

EID: 84952638184     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28013     Document Type: Article

References (50)

1. Glebe D, Bremer CM. The molecular virology of hepatitis B virus. Semin Liver Dis 2013;33:103-112.
2. Trepo C, Chan HL, Lok A. Hepatitis B virus infection. Lancet 2014;384:2053-2063.
3. Fattovich G, Giustina G, Christensen E, Pantalena M, Zagni I, Realdi G, et al. Influence of hepatitis delta virus infection on morbidity and mortality in compensated cirrhosis type B. The European Concerted Action on Viral Hepatitis (Eurohep). Gut 2000;46:420-426.
4. Taylor JM. Virology of hepatitis D virus. Semin Liver Dis 2012;32:195-200.
5. Gish R, Jia JD, Locarnini S, Zoulim F. Selection of chronic hepatitis B therapy with high barrier to resistance. Lancet Infect Dis 2012;12:341-353.
6. Wedemeyer H, Yurdaydin C, Dalekos GN, Erhardt A, Cakaloglu Y, Degertekin H, et al. Peginterferon plus adefovir versus either drug alone for hepatitis delta. N Engl J Med 2011;364:322-331.
7. Ciancio A, Rizzetto M. Chronic hepatitis D at a standstill: where do we go from here? Nat Rev Gastroenterol Hepatol 2014;11:68-71.
8. Yan H, Zhong G, Xu G, He W, Jing Z, Gao Z, et al. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife 2012;1:e00049.
9. Ni Y, Lempp FA, Mehrle S, Nkongolo S, Kaufman C, Falth M, et al. Hepatitis B and D viruses exploit sodium taurocholate co-transporting polypeptide for species-specific entry into hepatocytes. Gastroenterology 2014;146:1070-1083.
10. Watashi K, Urban S, Li W, Wakita T. NTCP and beyond: opening the door to unveil hepatitis B virus entry. Int J Mol Sci 2014;15:2892-2905.
11. Bishop JR, Schuksz M, Esko JD. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 2007;446:1030-1037.
12. Chen Y, Gotte M, Liu J, Park PW. Microbial subversion of heparan sulfate proteoglycans. Mol Cells 2008;26:415-426.
13. Schulze A, Gripon P, Urban S. Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology 2007;46:1759-1768.
14. Lamas Longarela O, Schmidt TT, Schoneweis K, Romeo R, Wedemeyer H, Urban S, et al. Proteoglycans act as cellular hepatitis delta virus attachment receptors. PLoS One 2013;8:e58340.
15. Sureau C, Salisse J. A conformational heparan sulfate binding site essential to infectivity overlaps with the conserved hepatitis B virus a-determinant. Hepatology 2013;57:985-994.
16. Baumert TF, Meredith L, Ni Y, Felmlee DJ, McKeating JA, Urban S. Entry of hepatitis B and C viruses-recent progress and future impact. Curr Opin Virol 2014;4C:58-65.
17. Urban S, Bartenschlager R, Kubitz R, Zoulim F. Strategies to inhibit entry of HBV and HDV into hepatocytes. Gastroenterology 2014;147:48-64.
18. Watashi K, Sluder A, Daito T, Matsunaga S, Ryo A, Nagamori S, et al. Cyclosporin A and its analogs inhibit hepatitis B virus entry into cultured hepatocytes through targeting a membrane transporter, sodium taurocholate cotransporting polypeptide (NTCP). Hepatology 2014;59:1726-1737.
19. Volz T, Allweiss L, Barek MB, Warlich M, Lohse AW, Pollok JM, et al. The entry inhibitor Myrcludex-B efficiently blocks intrahepatic virus spreading in humanized mice previously infected with hepatitis B virus. J Hepatol 2013;58:861-867.
20. Bogomolov P, Voronkova N, Allweiss L, Dandri M, Schwab M, Lempp FA, et al. A proof-of-concept phase 2a clinical trial with HBV/HDV entry inhibitor Myrcludex B. Hepatology 2014;60:1279a-1280a.
21. Blanchet M, Sureau C, Labonte P. Use of FDA approved therapeutics with hNTCP metabolic inhibitory properties to impair the HDV lifecycle. Antiviral Res 2014;106:111-115.
22. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 2011;17:589-595.
23. Ladner SK, Otto MJ, Barker CS, Zaifert K, Wang GH, Guo JT, et al. Inducible expression of human hepatitis B virus (HBV) in stably transfected hepatoblastoma cells: a novel system for screening potential inhibitors of HBV replication. Antimicrob Agents Chemother 1997;41:1715-1720.
24. Sureau C. The use of hepatocytes to investigate HDV infection: the HDV/HepaRG model. Methods Mol Biol 2010;640:463-473.
25. Blanchet M, Sureau C. Infectivity determinants of the hepatitis B virus pre-S domain are confined to the N-terminal 75 amino acid residues. J Virol 2007;81:5841-5849.
26. Habersetzer F, Moenne-Loccoz R, Meyer N, Schvoerer E, Simo-Noumbissie P, Dritsas S, et al. Loss of hepatitis B surface antigen in a real-life clinical cohort of patients with chronic hepatitis B virus infection. Liver Int 2015;35:130-139.
27. Laras A, Koskinas J, Dimou E, Kostamena A, Hadziyannis SJ. Intrahepatic levels and replicative activity of covalently closed circular hepatitis B virus DNA in chronically infected patients. Hepatology 2006;44:694-702.
28. Barrera A, Guerra B, Notvall L, Lanford RE. Mapping of the hepatitis B virus pre-S1 domain involved in receptor recognition. J Virol 2005;79:9786-9798.
29. Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, Cannie I, et al. Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci USA 2002;99:15655-15660.
30. Baumert TF, Yang C, Schurmann P, Kock J, Ziegler C, Grullich C, et al. Hepatitis B virus mutations associated with fulminant hepatitis induce apoptosis in primary Tupaia hepatocytes. Hepatology 2005;41:247-256.
31. Ren S, Nassal M. Hepatitis B virus (HBV) virion and covalently closed circular DNA formation in primary tupaia hepatocytes and human hepatoma cell lines upon HBV genome transduction with replication-defective adenovirus vectors. J Virol 2001;75:1104-1116.
32. Iwamoto M, Watashi K, Tsukuda S, Aly HH, Fukasawa M, Fujimoto A, et al. Evaluation and identification of hepatitis B virus entry inhibitors using HepG2 cells overexpressing a membrane transporter NTCP. Biochem Biophys Res Commun 2014;443:808-813.
33. Nkongolo S, Ni Y, Lempp FA, Kaufman C, Lindner T, Esser-Nobis K, et al. Cyclosporin A inhibits hepatitis B and hepatitis D virus entry by cyclophilin-independent interference with the NTCP receptor. J Hepatol 2014;60:723-731.
34. Lefevre M, Felmlee DJ, Parnot M, Baumert TF, Schuster C. Syndecan 4 is involved in mediating HCV entry through interaction with lipoviral particle-associated apolipoprotein E. PLoS One 2014;9:e95550.
35. Gripon P, Diot C, Guguen-Guillouzo C. Reproducible high level infection of cultured adult human hepatocytes by hepatitis B virus: effect of polyethylene glycol on adsorption and penetration. Virology 1993;192:534-540.
36. Pal R, Mamidi MK, Das AK, Bhonde R. Diverse effects of dimethyl sulfoxide (DMSO) on the differentiation potential of human embryonic stem cells. Arch Toxicol 2012;86:651-661.
37. Filmus J, Capurro M, Rast J. Glypicans. Genome Biol 2008;9:224.
38. Song HH, Filmus J. The role of glypicans in mammalian development. Biochim Biophys Acta 2002;1573:241-246.
39. Okamoto K, Tokunaga K, Doi K, Fujita T, Suzuki H, Katoh T, et al. Common variation in GPC5 is associated with acquired nephrotic syndrome. Nat Genet 2011;43:459-463.
40. Gordon AT, Brinkschmidt C, Anderson J, Coleman N, Dockhorn-Dworniczak B, Pritchard-Jones K, et al. A novel and consistent amplicon at 13q31 associated with alveolar rhabdomyosarcoma. Genes Chromosomes Cancer 2000;28:220-226.
41. Li Y, Sheu CC, Ye Y, de Andrade M, Wang L, Chang SC, et al. Genetic variants and risk of lung cancer in never smokers: a genome-wide association study. Lancet Oncol 2010;11:321-330.
42. Bergefall K, Trybala E, Johansson M, Uyama T, Naito S, Yamada S, et al. Chondroitin sulfate characterized by the E-disaccharide unit is a potent inhibitor of herpes simplex virus infectivity and provides the virus binding sites on gro2C cells. J Biol Chem 2005;280:32193-32199.
43. Misinzo G, Delputte PL, Meerts P, Lefebvre DJ, Nauwynck HJ. Porcine circovirus 2 uses heparan sulfate and chondroitin sulfate B glycosaminoglycans as receptors for its attachment to host cells. J Virol 2006;80:3487-3494.
44. Shi Q, Jiang J, Luo G. Syndecan-1 serves as the major receptor for attachment of hepatitis C virus to the surfaces of hepatocytes. J Virol 2013;87:6866-6875.
45. Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, et al. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 2003;278:41003-41012.
46. Oehler N, Volz T, Bhadra OD, Kah J, Allweiss L, Giersch K, et al. Binding of hepatitis B virus to its cellular receptor alters the expression profile of genes of bile acid metabolism. Hepatology 2014;60:1483-1493.
47. Mailly L, Xiao F, Lupberger J, Wilson GK, Aubert P, Duong FHT, et al. Clearance of persistent hepatitis C virus infection using a monoclonal antibody specific for thight junction protein claudin-1. Nat Biotechnol 2015;33:549-554.
48. Ho M, Kim H. Glypican-3: a new target for cancer immunotherapy. Eur J Cancer 2011;47:333-338.
49. Li F, Shi W, Capurro M, Filmus J. Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J Cell Biol 2011;192:691-704.
50. Williamson D, Selfe J, Gordon T, Lu YJ, Pritchard-Jones K, Murai K, et al. Role for amplification and expression of glypican-5 in rhabdomyosarcoma. Cancer Res 2007;67:57-65.