Specific interaction of the envelope glycoproteins E1 and E2 with liver heparan sulfate involved in the tissue tropismatic infection by hepatitis C virus

Glycoconjugate Journal

Volumn 29, Issue 4, 2012, Pages 211-220

  Kobayashi, Fumi ^a   Yamada, Shuhei ^b,d   Taguwa, Shuhei ^c   Kataoka, Chikako ^c   Naito, Satomi ^b   Hama, Yoshiki ^a   Tani, Hideki ^c   Matsuura, Yoshiharu ^c   Sugahara, Kazuyuki ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d MEIJO UNIVERSITY   (Japan)

Author keywords

Chondroitin sulfate; Glycosaminoglycan; Heparan sulfate; Hepatitis C virus; Tissue tropism

Indexed keywords

GLYCOPROTEIN E1; GLYCOPROTEIN E2; GLYCOSAMINOGLYCAN; HEPARAN SULFATE;

ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; COW; ENZYME STRUCTURE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SULFATION; TISSUE DISTRIBUTION; VIRAL TROPISM; VIRUS INFECTIVITY;

ANIMALS; BINDING SITES; CATTLE; CELL LINE; HEPACIVIRUS; HEPARITIN SULFATE; LIVER; VIRAL ENVELOPE PROTEINS;

BOVINAE; CEPHALOPODA; HEPATITIS C VIRUS;

EID: 84862541499     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-012-9388-z     Document Type: Article

References (53)

1. Wasley, A., Alter, M.J.: Epidemiology of hepatitis C: geographic differences and temporal trends. Semin. Liver Dis. 20, 1-16 (2000)
2. Lauer, G.M., Walker, B.D.: Hepatitis C virus infection. N. Engl. J. Med. 345, 41-52 (2001)
3. Barth, H., Schafer, C., Adah, M.I., Zhang, F., Linhardt, R.J., Toyoda, H., Kinoshita-Toyoda, A., Toida, T., Van Kuppevelt, T.H., Depla, E., Von Weizsacker, F., Blum, H.E., Baumert, T.F.: Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 278, 41003-41012 (2003)
4. Koutsoudakis, G., Kaul, A., Steinmann, E., Kallis, S., Lohmann, V., Pietschmann, T., Bartenschlager, R.: Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J. Virol. 80, 5308-5320 (2006)
5. Agnello, V., Abel, G., Elfahal, M., Knight, G.B., Zhang, Q.X.: Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc. Natl. Acad. Sci. U. S. A. 96, 12766-12771 (1999)
6. Monazahian, M., Böhme, I., Bonk, S., Koch, A., Scholz, C., Grethe, S., Thomssen, R.: Low density lipoprotein receptor as a candidate receptor for hepatitis C virus. J. Med. Virol. 57, 223-229 (1999)
7. Pileri, P., Uematsu, Y., Campagnoli, S., Galli, G., Falugi, F., Petracca, R., Weiner, A.J., Houghton, M., Rosa, D., Grandi, G., Abrignani, S.: Binding of hepatitis C virus to CD81. Science 282, 938-941 (1998)
8. Bartosch, B., Vitelli, A., Granier, C., Goujon, C., Dubuisson, J., Pascale, S., Scarselli, E., Cortese, R., Nicosia, A., Cosset, F.L.: Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J. Biol. Chem. 278, 41624-41630 (2003)
9. Evans, M.J., von Hahn, T., Tscherne, D.M., Syder, A.J., Panis, M., Wölk, B., Hatziioannou, T., McKeating, J.A., Bieniasz, P.D., Rice, C.M.: Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446, 801-805 (2007)
10. Liu, S., Yang, W., Shen, L., Turner, J.R., Coyne, C.B., Wang, T.: Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J. Virol. 83, 2011-2014 (2009)
11. Moradpour, D., Penin, F., Rice, C.M.: Replication of hepatitis C virus. Nat. Rev. Microbiol. 5, 453-463 (2007)
12. Garson, J.A., Lubach, D., Passas, J., Whitby, K., Grant, P.R.: Suramin blocks hepatitis C binding to human hepatoma cells in vitro. J. Med. Virol. 57, 238-242 (1999)
13. Liu, B., Paranjpe, S., Bowen,W.C., Bell, A.W., Luo, J.H., Yu, Y.P., Mars, W.M., Michalopoulos, G.K.: Investigation of the role of glypican 3 in liver regeneration and hepatocyte proliferation. Am. J. Pathol. 175, 717-724 (2009)
14. Yagnik, A.T., Lahm, A., Meola, A., Roccasecca, R.M., Ercole, B.B., Nicosia, A., Tramontano, A.: A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40, 355-366 (2000)
15. Sugahara, K., Kitagawa, H.: Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10, 518-527 (2000)
16. Esko, J.D., Selleck, S.B.: Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471 (2001)
17. Yamada, S., Sugahara, K.: Potential therapeutic application of chondroitin sulfate/dermatan sulfate. Curr. Drug Discov. Tech. 5, 289-301 (2008)
18. Casu, B., Lindahl, U.: Structure and biological interactions of heparin and heparan sulfate. Adv. Carbohydr. Chem. Biochem. 57, 159-206 (2001)
19. Kreuger, J., Spillmann, D., Li, J.P., Lindahl, U.: Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell Biol. 174, 323-327 (2006)
20. Shukla, D., Spear, P.G.: Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Invest. 108, 503-510 (2001)
21. Spillmann, D.: Heparan sulfate: anchor for viral intruders? Biochimie 83, 811-817 (2001)
22. Rostand, K.S., Esko, J.D.: Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65, 1-8 (1997)
23. Giroglou, T., Florin, L., Schäfer, F., Streeck, R.E., Sapp, M.: Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75, 1565-1570 (2001)
24. Birkmann, A., Mahr, K., Ensser, A., Ya?ubo?lu, S., Titgemeyer, F., Fleckenstein, B., Neipel, F.: Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J. Virol. 75, 11583-11593 (2001)
25. Liu, J., Thorp, S.C.: Cell surface heparan sulfate and its roles in assisting viral infections. Med. Res. Rev. 22, 1-25 (2002)
26. Ishihara, M., Takano, R., Kanda, T., Hayashi, K., Hara, S., Kikuchi, H., Yoshida, K.: Importance of 6-O-sulfate groups of glucosamine residues in heparin for activation of FGF-1 and FGF-2. J. Biochem. 118, 1255-1260 (1995)
27. Ishihara, M., Kariya, Y., Kikuchi, H., Minamisawa, T., Yoshida, K.: Importance of 2-O-sulfate groups of uronate residues in heparin for activation of FGF-1 and FGF-2. J. Biochem. 121, 345-349 (1997)
28. Maccarana, M., Sakura, Y., Tawada, A., Yoshida, K., Lindahl, U.: Domain structure of heparan sulfates from bovine organs. J. Biol. Chem. 271, 17804-17810 (1996)
29. Yamane, Y., Tohno-oka, R., Yamada, S., Furuya, S., Shiokawa, K., Hirabayashi, Y., Sugino, H., Sugahara, K.: Molecular characterization of Xenopus embryo heparan sulfate. Differential structural requirements for the specific binding to basic fibroblast growth factor and follistatin. J. Biol. Chem. 273, 7375-7381 (1998)
30. Ueno, M., Yamada, S., Zako, M., Bernfield, M., Sugahara, K.: Structural characterization of heparan sulfate and chondroitin sulfate of syndecan-1 purified from normal murine mammary gland epithelial cells. Common phosphorylation of xylose and differential sulfation of galactose in the protein linkage region tetrasaccharide sequence. J. Biol. Chem. 276, 29134-29140 (2001)
31. Nandini, C.D., Itoh, N., Sugahara, K.: Novel 70-kDa chondroitin sulfate/dermatan sulfate hybrid chains with a unique heterogeneous sulfation pattern from shark skin, which exhibit neuritogenic activity and binding activities for growth factors and neurotrophic factors. J. Biol. Chem. 280, 4058-4069 (2005)
32. Kinoshita, A., Sugahara, K.: Microanalysis of glycosaminoglycanderived oligosaccharides labeled with the fluorophore 2- aminobenzamide by high-performance liquid chromatography: application to disaccharide composition analysis and exo-sequencing of oligosaccharides. Anal. Biochem. 269, 367-378 (1999)
33. Kawashima, H., Atarashi, K., Hirose, M., Hirose, J., Yamada, S., Sugahara, K., Miyasaka, M.: Oversulfated chondroitin/dermatan sulfates containing GlcAβ1/IdoAα1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J. Biol. Chem. 277, 12921-12930 (2002)
34. Saito, A., Munakata, H., Satoh, K.: Glyco-western blotting: biotinylated dermatan sulfate as a probe for the detection of dermatan sulfate binding proteins using western blotting. Connect. Tissue Res. 43, 1-7 (2002)
35. Tani, H., Komoda, Y., Matsuo, E., Suzuki, K., Hamamoto, I., Yamashita, T., Moriishi, K., Fujiyama, K., Kanto, T., Hayashi, N., Owsianka, A., Patel, A.H., Whitt, M.A., Matsuura, Y.: Replication-competent recombinant vesicular stomatitis virus encoding hepatitis C virus envelope proteins. J. Virol. 81, 8601-8612 (2007)
36. Vongchan, P., Warda, M., Toyoda, H., Toida, T., Marks, R.M., Linhardt, R.J.: Structural characterization of human liver heparin sulfate. Biochim. Biophys. Acta 1721, 1-8 (2005)
37. Volpi, N.: Disaccharide analysis and molecular mass determination to microgram level of single sulfated glycosaminoglycan species in mixtures following agarose-gel electrophoresis. Anal. Biochem. 273, 229-239 (1999)
38. Volpi, N.: Hyaluronic acid and chondroitin sulfate unsaturated disaccharides analysis by high-performance liquid chromatography and fluorimetric detection with dansylhydrazine. Anal. Biochem. 277, 19-24 (2000)
39. Matsuura, Y., Harada, S., Suzuki, R., Watanabe, Y., Inoue, Y., Saito, I., Miyamura, T.: Expression of processed envelope protein of hepatitis C virus in mammalian and insect cells. J. Virol. 66, 1425-1431 (1992)
40. Barth, H., Schnober, E.K., Zhang, F., Linhardt, R.J., Depla, E., Boson, B., Cosset, F.L., Patel, A.H., Blum, H.E., Baumert, T.F.: Viral and cellular determinants of the hepatitis C virus envelopeheparan sulfate interaction. J. Virol. 80, 10579-10590 (2006)
41. Li, F., Yamada, S., Basappa, Shetty, A.K., Sugiura, M., Sugahara, K.: Determination of iduronic acid and glucuronic acid in sulfated chondroitin/dermatan hybrid chains by 1H-nuclear magnetic resonance spectroscopy. Glycoconj. J. 25, 603-610 (2008)
42. Salmivirta, M., Lidholt, K., Lindahl, U.: Heparan sulfate: a piece of information. FASEB J. 10, 1270-1279 (1996)
43. Barth, H., Liang, T.J., Baumert, T.F.: Hepatitis C virus entry: molecular biology and clinical implications. Hepatology 44, 527-535 (2006)
44. Yanagiya, A., Ohka, S., Hashida, N., Okamura, M., Taya, C., Kamoshita, N., Iwasaki, K., Sasaki, Y., Yonekawa, H., Nomoto, A.: Tissue-specific replicating capacity of a chimeric poliovirus that carries the internal ribosome entry site of hepatitis C virus in a new mouse model transgenic for the human poliovirus receptor. J. Virol. 77 10479-10487 (2003)
45. Bergström, T., Trybala, E., Spillmann, D.: Heparan sulfate and viral tropism. Nat. Med. 3, 1177 (1997)
46. Dorner, M., Horwitz, J.A., Robbins, J.B., Barry, W.T., Feng, Q., Mu, K., Jones, C.T., Schoggins, J.W., Catanese, M.T., Burton, D.R., Law, M., Rice, C.M., Ploss, A.: A genetically humanized mouse model for hepatitis C virus infection. Nature 474, 208-211 (2011)
47. Lyon, M., Deakin, J.A., Gallagher, J.T.: Liver heparan sulfate structure. A novel molecular design. J. Biol. Chem. 269, 11208-11215 (1994)
48. Krey, T., d'Alayer, J., Kikuti, C.M., Saulnier, A., Damier-Piolle, L., Petitpas, I., Johansson, D.X., Tawar, R.G., Baron, B., Robert, B., England, P., Persson, M.A., Martin, A., Rey, F.A.: The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog. 6, e1000762 (2010)
49. Matsuura, Y., Tani, H., Suzuki, K., Kimura-Someya, T., Suzuki, R., Aizaki, H., Ishii, K., Moriishi, K., Robison, C.S., Whitt, M.A., Miyamura, T.: Characterization of pseudotype VSV possessing HCV envelope proteins. Virology 286, 263-275 (2001)
50. Gospodarowicz, D., Cheng, J.: Heparin protects basic and acidic FGF from inactivation. J. Cell. Physiol. 128, 475-484 (1986)
51. Powers, C.J., McLeskey, S.W., Wellstein, A.: Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Canc. 7, 165-197 (2000)
52. Fernig, D.G., Gallagher, J.T.: Fibroblast growth factors and their receptors: an information network controlling tissue growth, morphogenesis and repair. Progr. Growth Factor Res. 5, 353-377 (1994)
53. Mohammadi, M., Olsen, S.K., Goetz, R.: A protein canyon in the FGF-FGF receptor dimer selects from an à la carte menu of heparan sulfate motifs. Curr. Opin. Struct. Biol. 15, 506-516 (2005)