Sulfated Homologues of Heparin Inhibit Hepatitis C Virus Entry into Mammalian Cells

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2007 Feb 9

PMID 17287282

Citations 38

Authors

Arnab Basu

Tatsuo Kanda

Aster Beyene

Kousuke Saito

Keith Meyer

Ranjit Ray

Affiliations

Soon will be listed here.

Abstract

The mechanism of entry of hepatitis C virus (HCV) through interactions between the envelope glycoproteins and specific cell surface receptors remains unclear at this time. We have previously shown with the vesicular stomatitis virus (VSV)/HCV pseudotype model that the hypervariable region 1 of the HCV E2 envelope glycoprotein helps in binding with glycosaminoglycans present on the cell surface. In this study, we have examined the binding of HCV envelope glycoproteins with chemically modified derivatives of heparin. Furthermore, we have determined the functional relevance of the interaction of heparin derivatives with HCV envelope glycoproteins for infectivity by using a human immunodeficiency virus (HIV)/HCV pseudotype, a VSV/HCV pseudotype, and cell culture-grown HCV genotype 1a. Taken together, our results suggest that the HCV envelope glycoproteins rely upon O-sulfated esters of a heparin homologue to facilitate entry into mammalian cells.

Citing Articles

Antiviral Polymers: A Review.

Akbari A, Bigham A, Rahimkhoei V, Sharifi S, Jabbari E Polymers (Basel). 2022; 14(9).

PMID: 35566804 PMC: 9101550. DOI: 10.3390/polym14091634.

Carbohydrate Ligands for COVID-19 Spike Proteins.

Lee Y, Chang W, Prakash E, Peng Y, Tu Z, Lin C Viruses. 2022; 14(2).

PMID: 35215921 PMC: 8880561. DOI: 10.3390/v14020330.

Hepatitis C Virus Glycan-Dependent Interactions and the Potential for Novel Preventative Strategies.

LeBlanc E, Kim Y, Capicciotti C, Colpitts C Pathogens. 2021; 10(6).

PMID: 34205894 PMC: 8230238. DOI: 10.3390/pathogens10060685.

Pharmacological Modulators of Autophagy as a Potential Strategy for the Treatment of COVID-19.

da Silva Pereira G, Leao A, Erustes A, Morais I, de Moraes Vrechi T, Zamarioli L Int J Mol Sci. 2021; 22(8).

PMID: 33920748 PMC: 8071111. DOI: 10.3390/ijms22084067.

Potential Use of Anti-Inflammatory Synthetic Heparan Sulfate to Attenuate Liver Damage.

Arnold K, Liao Y, Liu J Biomedicines. 2020; 8(11).

PMID: 33207634 PMC: 7697061. DOI: 10.3390/biomedicines8110503.

References

Yagnik A, Lahm A, Meola A, Roccasecca R, Ercole B, Nicosia A . A model for the hepatitis C virus envelope glycoprotein E2. Proteins. 2000; 40(3):355-66. DOI: 10.1002/1097-0134(20000815)40:3<355::aid-prot20>3.0.co;2-k. View

Drummer H, Poumbourios P . Hepatitis C virus glycoprotein E2 contains a membrane-proximal heptad repeat sequence that is essential for E1E2 glycoprotein heterodimerization and viral entry. J Biol Chem. 2004; 279(29):30066-72. DOI: 10.1074/jbc.M405098200. View

Lagging L, Meyer K, Owens R, Ray R . Functional role of hepatitis C virus chimeric glycoproteins in the infectivity of pseudotyped virus. J Virol. 1998; 72(5):3539-46. PMC: 109573. DOI: 10.1128/JVI.72.5.3539-3546.1998. View

Flint M, Maidens C, Loomis-Price L, Shotton C, Dubuisson J, Monk P . Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol. 1999; 73(8):6235-44. PMC: 112700. DOI: 10.1128/JVI.73.8.6235-6244.1999. View

Meyer K, Beyene A, Bowlin T, Basu A, Ray R . Coexpression of hepatitis C virus E1 and E2 chimeric envelope glycoproteins displays separable ligand sensitivity and increases pseudotype infectious titer. J Virol. 2004; 78(23):12838-47. PMC: 524985. DOI: 10.1128/JVI.78.23.12838-12847.2004. View

Zahn A, Allain J . Hepatitis C virus and hepatitis B virus bind to heparin: purification of largely IgG-free virions from infected plasma by heparin chromatography. J Gen Virol. 2005; 86(Pt 3):677-685. DOI: 10.1099/vir.0.80614-0. View

Andre P, Perlemuter G, Budkowska A, Brechot C, Lotteau V . Hepatitis C virus particles and lipoprotein metabolism. Semin Liver Dis. 2005; 25(1):93-104. DOI: 10.1055/s-2005-864785. View

Bartosch B, Verney G, Dreux M, Donot P, Morice Y, Penin F . An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J Virol. 2005; 79(13):8217-29. PMC: 1143705. DOI: 10.1128/JVI.79.13.8217-8229.2005. View

Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton D . Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A. 2005; 102(26):9294-9. PMC: 1166622. DOI: 10.1073/pnas.0503596102. View

10.

Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z . Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med. 2005; 11(7):791-6. PMC: 2918402. DOI: 10.1038/nm1268. View

11.

Lindenbach B, Evans M, Syder A, Wolk B, Tellinghuisen T, Liu C . Complete replication of hepatitis C virus in cell culture. Science. 2005; 309(5734):623-6. DOI: 10.1126/science.1114016. View

12.

Olenina L, Kuzmina T, Sobolev B, Kuraeva T, Kolesanova E, Archakov A . Identification of glycosaminoglycan-binding sites within hepatitis C virus envelope glycoprotein E2*. J Viral Hepat. 2005; 12(6):584-93. DOI: 10.1111/j.1365-2893.2005.00647.x. View

13.

Kanda T, Basu A, Steele R, Wakita T, Ryerse J, Ray R . Generation of infectious hepatitis C virus in immortalized human hepatocytes. J Virol. 2006; 80(9):4633-9. PMC: 1472020. DOI: 10.1128/JVI.80.9.4633-4639.2006. View

14.

Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, Pietschmann T . Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol. 2006; 80(11):5308-20. PMC: 1472176. DOI: 10.1128/JVI.02460-05. View

15.

Pfeiffer T, Pisch T, Devitt G, Holtkotte D, Bosch V . Effects of signal peptide exchange on HIV-1 glycoprotein expression and viral infectivity in mammalian cells. FEBS Lett. 2006; 580(15):3775-8. DOI: 10.1016/j.febslet.2006.05.070. View

16.

Barth H, Schnober E, Zhang F, Linhardt R, Depla E, Boson B . Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J Virol. 2006; 80(21):10579-90. PMC: 1641783. DOI: 10.1128/JVI.00941-06. View

17.

Kanda T, Steele R, Ray R, Ray R . Small interfering RNA targeted to hepatitis C virus 5' nontranslated region exerts potent antiviral effect. J Virol. 2006; 81(2):669-76. PMC: 1797438. DOI: 10.1128/JVI.01496-06. View

18.

Meyer K, Basu A, Ray R . Functional features of hepatitis C virus glycoproteins for pseudotype virus entry into mammalian cells. Virology. 2000; 276(1):214-26. DOI: 10.1006/viro.2000.0547. View

19.

Wunschmann S, Medh J, Klinzmann D, Schmidt W, Stapleton J . Characterization of hepatitis C virus (HCV) and HCV E2 interactions with CD81 and the low-density lipoprotein receptor. J Virol. 2000; 74(21):10055-62. PMC: 102044. DOI: 10.1128/jvi.74.21.10055-10062.2000. View

20.

Matsuura Y, Tani H, Suzuki K, Suzuki R, Aizaki H, Ishii K . Characterization of pseudotype VSV possessing HCV envelope proteins. Virology. 2001; 286(2):263-75. DOI: 10.1006/viro.2001.0971. View