Proteoglycans Act as Cellular Hepatitis Delta Virus Attachment Receptors

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Lamas Longarela, Oscar ^a   Schmidt, Tobias T ^a   Schöneweis, Katrin ^a   Romeo, Raffaella ^b   Wedemeyer, Heiner ^c   Urban, Stephan ^a   Schulze, Andreas ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b UNIVERSITY OF MILAN   (Italy)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORATE; HEPARIN LYASE; HEPARINASE III; PROTEOGLYCAN; PROTEOHEPARAN SULFATE; PURINERGIC P2X RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOHYDRATE ANALYSIS; CELL SURFACE; CONTROLLED STUDY; DELTA AGENT HEPATITIS; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS DELTA VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RECEPTOR BINDING; VIRUS ATTACHMENT; VIRUS ENTRY;

CELL LINE; GLYCOSAMINOGLYCANS; HEPATITIS DELTA VIRUS; HUMANS; PROTEOGLYCANS; RECEPTORS, VIRUS; STATIC ELECTRICITY; SULFATES; VIRUS ATTACHMENT;

EID: 84874671326     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058340     Document Type: Article

References (47)

1. Hughes SA, Wedemeyer H, Harrison PM (2011) Hepatitis delta virus. Lancet 378: 73-85. S0140-6736(10)61931-9 [pii];10.1016/S0140-6736(10)61931-9 [doi].
2. Rizzetto M (2009) Hepatitis D: thirty years after. J Hepatol 50: 1043-1050. S0168-8278(09)00059-2 [pii];10.1016/j.jhep.2009.01.004 [doi].
3. Wedemeyer H (2011) Hepatitis D revival. Liver Int 31 Suppl 1: 140-144. 10.1111/j.1478-3231.2010.02408.x [doi].
4. Barrera A, Guerra B, Notvall L, Lanford RE, (2005) Mapping of the hepatitis B virus pre-S1 domain involved in receptor recognition. J Virol 79: 9786-9798.
5. Engelke M, Mills K, Seitz S, Simon P, Gripon P, et al. (2006) Characterization of a hepatitis B and hepatitis delta virus receptor binding site. Hepatology 43: 750-760.
6. Sureau C, (2006) The role of the HBV envelope proteins in the HDV replication cycle. Curr Top Microbiol Immunol 307: 113-131.
7. Blanchet M, Sureau C, (2007) Infectivity determinants of the hepatitis B virus pre-S domain are confined to the N-terminal 75 amino acid residues. J Virol 81: 5841-5849.
8. Le Seyec J, Chouteau P, Cannie I, Guguen-Guillouzo C, Gripon P, (1999) Infection process of the hepatitis B virus depends on the presence of a defined sequence in the pre-S1 domain. J Virol 73: 2052-2057.
9. Lutgehetmann M, Mancke LV, Volz T, Helbig M, Allweiss L, et al. (2012) Humanized chimeric uPA mouse model for the study of hepatitis B and D virus interactions and preclinical drug evaluation. Hepatology 55: 685-694. 10.1002/hep.24758 [doi].
10. Petersen J, Dandri M, Mier W, Lutgehetmann M, Volz T, et al. (2008) Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat Biotechnol 26: 335-341. nbt1389 [pii];10.1038/nbt1389 [doi].
11. Gripon P, Cannie I, Urban S, (2005) Efficient inhibition of hepatitis B virus infection by acylated peptides derived from the large viral surface protein. J Virol 79: 1613-1622.
12. Gripon P, Le Seyec J, Rumin S, Guguen-Guillouzo C, (1995) Myristylation of the hepatitis B virus large surface protein is essential for viral infectivity. Virology 213: 292-299.
13. Schulze A, Schieck A, Ni Y, Mier W, Urban S (2010) Fine mapping of pre-S sequence requirements for hepatitis B virus large envelope protein-mediated receptor interaction. J Virol 84: 1989-2000. JVI.01902-09 [pii];10.1128/JVI.01902-09 [doi].
14. Jaoude GA, Sureau C, (2005) Role of the antigenic loop of the hepatitis B virus envelope proteins in infectivity of hepatitis delta virus. J Virol 79: 10460-10466.
15. Salisse J, Sureau C (2009) A function essential to viral entry underlies the hepatitis B virus "a" determinant. J Virol 83: 9321-9328. JVI.00678-09 [pii];10.1128/JVI.00678-09 [doi].
16. Le DY, Blanchet M, Sureau C (2009) The pre-S1 and antigenic loop infectivity determinants of the hepatitis B virus envelope proteins are functionally independent. J Virol 83: 12443-12451. JVI.01594-09 [pii];10.1128/JVI.01594-09 [doi].
17. Glebe D, Urban S, (2007) Viral and cellular determinants involved in hepadnaviral entry. World J Gastroenterol 13: 22-38.
18. Yan H, Zhong G, Xu G, He W, Jing Z, et al. (2012) Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. elife 1: e00049. 10.7554/eLife.00049 [doi];00049 [pii].
19. Leistner CM, Gruen-Bernhard S, Glebe D (2008) Role of glycosaminoglycans for binding and infection of hepatitis B virus. Cell Microbiol 10: 122-133. CMI1023 [pii];10.1111/j.1462-5822.2007.01023.x [doi].
20. Schulze A, Gripon P, Urban S (2007) Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology 46: 1759-1768. 10.1002/hep.21896 [doi].
21. Honke K, Taniguchi N (2002) Sulfotransferases and sulfated oligosaccharides. Med Res Rev 22: 637-654. 10.1002/med.10020 [doi].
22. Lyon M, Deakin JA, Gallagher JT, (1994) Liver heparan sulfate structure. A novel molecular design. J Biol Chem 269: 11208-11215.
23. Vongchan P, Warda M, Toyoda H, Toida T, Marks RM, et al. (2005) Structural characterization of human liver heparan sulfate. Biochim Biophys Acta 1721: 1-8.
24. Stow JL, Kjellen L, Unger E, Hook M, Farquhar MG, (1985) Heparan sulfate proteoglycans are concentrated on the sinusoidal plasmalemmal domain and in intracellular organelles of hepatocytes. J Cell Biol 100: 975-980.
25. Taylor JM, Han Z (2010) Purinergic receptor functionality is necessary for infection of human hepatocytes by hepatitis delta virus and hepatitis B virus. PLoS One 5: e15784. 10.1371/journal.pone.0015784 [doi].
26. Bradley HJ, Liu X, Collins V, Owide J, Goli GR, et al. (2010) Identification of an intracellular microdomain of the P2X7 receptor that is crucial in basolateral membrane targeting in epithelial cells. FEBS Lett 584: 4740-4744. S0014-5793(10)00901-4 [pii];10.1016/j.febslet.2010.11.007 [doi].
27. Browne LE, Jiang LH, North RA (2010) New structure enlivens interest in P2X receptors. Trends Pharmacol Sci 31: 229-237. S0165-6147(10)00016-7 [pii];10.1016/j.tips.2010.02.004 [doi].
28. Wilson HL, Varcoe RW, Stokes L, Holland KL, Francis SE, et al. (2007) P2X receptor characterization and IL-1/IL-1Ra release from human endothelial cells. Br J Pharmacol 151: 115-127. 0707213 [pii];10.1038/sj.bjp.0707213 [doi].
29. Emmett DS, Feranchak A, Kilic G, Puljak L, Miller B, et al. (2008) Characterization of ionotrophic purinergic receptors in hepatocytes. Hepatology 47: 698-705. 10.1002/hep.22035 [doi].
30. Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, et al. (2002) Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci U S A 99: 15655-15660.
31. Ladner SK, Otto MJ, Barker CS, Zaifert K, Wang GH, et al. (1997) 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 41: 1715-1720.
32. Offensperger WB, Offensperger S, Walter E, Blum HE, Gerok W, (1993) Suramin prevents duck hepatitis B virus infection in vivo. Antimicrob Agents Chemother 37: 1539-1542.
33. Petcu DJ, Aldrich CE, Coates L, Taylor JM, Mason WS, (1988) Suramin inhibits in vitro infection by duck hepatitis B virus, Rous sarcoma virus, and hepatitis delta virus. Virology 167: 385-392.
34. Baeuerle PA, Huttner WB (1986) Chlorate-a potent inhibitor of protein sulfation in intact cells. Biochem Biophys Res Commun 141: 870-877. S0006-291X(86)80253-4 [pii].
35. Sureau C, Salisse J (2012) A conformational heparan sulfate-binding site essential to infectivity overlaps with the conserved hepatitis B virus a-determinant. Hepatology. 10.1002/hep.26125 [doi].
36. Voogd TE, Vansterkenburg EL, Wilting J, Janssen LH, (1993) Recent research on the biological activity of suramin. Pharmacol Rev 45: 177-203.
37. Fleck SL, Birdsall B, Babon J, Dluzewski AR, Martin SR, et al. (2003) Suramin and suramin analogues inhibit merozoite surface protein-1 secondary processing and erythrocyte invasion by the malaria parasite Plasmodium falciparum. J Biol Chem 278: 47670-47677. 10.1074/jbc.M306603200 [doi];M306603200 [pii].
38. McGeary RP, Bennett AJ, Tran QB, Cosgrove KL, Ross BP, (2008) Suramin: clinical uses and structure-activity relationships. Mini Rev Med Chem 8: 1384-1394.
39. Balzarini J, Mitsuya H, De CE, Broder S, (1986) Comparative inhibitory effects of suramin and other selected compounds on the infectivity and replication of human T-cell lymphotropic virus (HTLV-III)/lymphadenopathy-associated virus (LAV). Int J Cancer 37: 451-457.
40. Croon JJ, Wolff HL, (1982) The inhibition of yellow fever virus multiplication by suramin: a preliminary note. Acta Leiden 48: 5-8.
41. Aguilar JS, Rice M, Wagner EK, (1999) The polysulfonated compound suramin blocks adsorption and lateral difusion of herpes simplex virus type-1 in vero cells. Virology 258: 141-151.
42. De CE (1987) Suramin in the treatment of AIDS: mechanism of action. Antiviral Res 7: 1-10. 0166-3542(87)90034-9 [pii].
43. Garson JA, Lubach D, Passas J, Whitby K, Grant PR (1999) AID-JMV5>3.0.CO;2-G [pii].
44. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, et al. (2002) Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol 68: 206-215. 10.1002/jmv.10196 [doi].
45. Tsiquaye K, Zuckerman A, (1985) Suramin inhibits duck hepatitis B virus DNA polymerase activity. J Hepatol 1: 663-669.
46. Funk A, Hohenberg H, Mhamdi M, Will H, Sirma H, (2004) Spread of hepatitis B viruses in vitro requires extracellular progeny and may be codetermined by polarized egress. J Virol 78: 3977-3983.
47. Stokes L, Jiang LH, Alcaraz L, Bent J, Bowers K, et al. (2006) Characterization of a selective and potent antagonist of human P2X(7) receptors, AZ11645373. Br J Pharmacol 149: 880-887. 0706933 [pii];10.1038/sj.bjp.0706933 [doi].