Heparan sulfates and coxsackievirus-adenovirus receptor: Each one mediates coxsackievirus B3 PD infection

Journal of Virology

Volumn 77, Issue 18, 2003, Pages 10071-10077

  Zautner, A E ^a   Korner U ^a   Henke, A ^a   Badorff, C ^b   Schmidtke, M ^a,c  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; DECAY ACCELERATING FACTOR; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN LYASE; PENTOSAN POLYSULFATE; SCATTER FACTOR; VIRUS RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL POLARITY; COXSACKIE VIRUS; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SEROTYPE; VIRUS EXPRESSION; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION; WOUND HEALING;

AMINO ACID SUBSTITUTION; ANIMALS; CAPSID PROTEINS; CHO CELLS; COXSACKIEVIRUS INFECTIONS; CRICETINAE; ENTEROVIRUS B, HUMAN; HEPARIN; HEPARIN LYASE; HEPARITIN SULFATE; HEPATOCYTE GROWTH FACTOR; RECEPTORS, VIRUS; TRANSFECTION;

EID: 0141681882     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.18.10071-10077.2003     Document Type: Article

References (43)

1. Bai, X., and J. D. Esko. 1996. An animal cell mutant defective in heparan sulfate hexuronic acid 2-O-sulfation. J. Biol. Chem. 271:17711-17717.
2. Bame, K. J., and J. D. Esko. 1989. Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J. Biol. Chem. 264:8059-8065.
3. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
4. Bergelson, J. M., A. Krithivas, L. Celi, G. Droguett, M. S. Horwitz, T. Wickham, R. L. Crowell, and R. W. Finberg. 1998. The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. J. Virol. 72:415-419.
5. Bergelson, J. M., J. G. Mohanty, R. L. Crowell, N. F. St John, D. M. Lublin, and R. W. Finberg. 1995. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J. Virol. 69:1903-1906.
6. Bernfield, M., M. Gotte, P. W. Park, O. Reizes, M. L. Fitzgerald, J. Lincecum, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:729-777.
7. Cohen, C. J., J. T. Shieh, R. J. Pickles, T. Okegawa, J. T. Hsieh, and J. M. Bergelson. 2001. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl. Acad. Sci. USA 98:15191-15196.
8. Dechecchi, M. C., A. Tamanini, A. Bonizzato, and G. Cabrini. 2000. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology 268:382-390.
9. Esko, J. D., T. E. Stewart, and W. H. Taylor. 1985. Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA 82:3197-3201.
10. Giroglou, T., L. Florin, F. Schafer, R. E. Streeck, and M. Sapp. 2001. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75:1565-1570.
11. Goodfellow, I. G., A. B. Sioofy, R. M. Powell, and D. J. Evans. 2001. Echoviruses bind heparan sulfate at the cell surface. J. Virol. 75:4918-4921.
12. Hallak, L. K., P. L. Collins, W. Knudson, and M. E. Peeples. 2000. Iduronic acid-containing glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology 271:264-275.
13. Herold, B. C., S. I. Gerber, B. J. Belval, A. M. Siston, and N. Shulman. 1996. Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. J. Virol. 70:3461-3469.
14. Herold, B. C., S. I. Gerber, T. Polonsky, B. J. Belval, P. N. Shaklee, and K. Holme. 1995. Identification of structural features of heparin required for inhibition of herpes simplex virus type 1 binding. Virology 206:1108-1116.
15. Ito, M., M. Kodama, M. Masuko, M. Yamaura, K. Fuse, Y. Uesugi, S. Hirono, Y. Okura, K. Kato, Y. Hotta, T. Honda, R. Kuwano, and Y. Aizawa. 2000. Expression of coxsackievirus and adenovirus receptor in hearts of rats with experimental autoimmune myocarditis. Circ. Res. 86:275-280.
16. Jackson, T., F. M. Ellard, R. A. Ghazaleh, S. M. Brookes, W. E. Blakemore, A. H. Corteyn, D. I. Stuart, J. W. Newman, and A. M. King. 1996. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J. Virol. 70:5282-5287.
17. Lidholt, K., J. L. Weinke, C. S. Kiser, F. N. Lugemwa, K. J. Bame, S. Cheifetz, J. Massague, U. Lindahl, and J. D. Esko. 1992. A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc. Natl. Acad. Sci. USA 89:2267-2271.
18. Lindberg, A. M., R. L. Crowell, R. Zell, R. Kandolf, and U. Pettersson. 1992. Mapping of the RD phenotype of the Nancy strain of coxsackievirus B3. Virus Res. 24:187-196.
19. Martino, T. A., M. Petric, H. Weingartl, J. M. Bergelson, M. A. Opavsky, C. D. Richardson, J. F. Modlin, R. W. Finberg, K. C. Kain, N. Willis, C. J. Gauntt, and P. P. Liu. 2000. The coxsackie-adenovirus receptor (CAR) is used by reference strains and clinical isolates representing all six serotypes of coxsackievirus group B and by swine vesicular disease virus. Virology 271:99-108.
20. Mena, L. C. Fischer, J. R. Gebhard, C. M. Perry, S. Harkins, and J. L. Whitton. 2000. Coxsackievirus infection of the pancreas: evaluation of receptor expression, pathogenesis, and immunopathology. Virology 271:276-288.
21. Mondor, I., M. Moulard, S. Ugolini, P. J. Klasse, J. Hoxie, A. Amara, T. Delaunay, R. Wyatt, J. Sodroski, and Q. J. Sattentau. 1998. Interactions among HIV gp120, CD4, and CXCR4: dependence on CD4 expression level, gp120 viral origin, conservation of the gp120 COOH- and NH2-termini and V1/V2 and V3 loops, and sensitivity to neutralizing antibodies. Virology 248:394-405.
22. Muckelbauer, J. K., M. Kremer, I. Minor, G. Diana, F. J. Dutko, J. Groarke, D. C. Pevear, and M. G. Rossmann. 1995. The structure of coxsackievirus B3 at 3.5 A resolution. Structure 3:653-667.
23. Nalbantoglu, J., G. Pari, G. Karpati, and P. C. Holland. 1999. Expression of the primary coxsackie and adenovirus receptor is downregulated during skeletal muscle maturation and limits the efficacy of adenovirus-mediated gene delivery to muscle cells. Hum. Gene Ther. 10:1009-1019.
24. Noutsias, M., H. Fechner, H. de Jonge, X. Wang, D. Dekkers, A. B. Houtsmuller, M. Pauschinger, J. Bergelson, R. Warraich, M. Yacoub, R. Hetzer, J. Lamers, H. P. Schultheiss, and W. Poller. 2001. Human coxsackie-adenovirus receptor is colocalized with integrins alpha(v)beta(3) and alpha(v) beta(5) on the cardiomyocyte sarcolemma and upregulated in dilated cardiomyopathy: implications for cardiotropic viral infections. Circulation 104:275-280.
25. Reddi, H. V., and H. L. Lipton. 2002. Heparan sulfate mediates infection of high-neurovirulence Theiler's viruses. J. Virol. 76:8400-8407.
26. Reed, J., and H. Muench. 1938. A simple method of estimation of fifty per cent end points. Am. J. Hyg. 493-497.
27. Rossmann, M. G. 1989. The canyon hypothesis. Hiding the host cell receptor attachment site on a viral surface from immune surveillance. J. Biol. Chem. 264:14587-14590.
28. Schmidtke, M., A. Karger, A. Meerbach, R. Egerer, A. Stelzner, and V. Makarov. 2003. Binding of a N,N′-bisheteryl derivative of dispirotripiperazine to heparan sulfate residues on the cell surface specifically prevents infection of viruses from different families. Virology 311:134-143.
29. Schmidtke, M., O. Riabova, H. M. Dahse, A. Stelzner, and V. Makarov. 2002. Synthesis, cytotoxicity and antiviral activity of N,N′ -bis-5-nitropyrimidyl derivatives of dispirotripiperazine. Antivir. Res. 55:117-127.
30. Schmidtke, M., U. Schnittler, B. Jahn, H. Dahse, and A. Stelzner. 2001. A rapid assay for evaluation of antiviral activity against coxsackie virus B3, influenza virus A, and herpes simplex virus type 1. J. Virol. Methods 95:133-143.
31. Schmidtke, M., H. C. Selinka, A. Heim, B. Jahn, M. Tonew, R. Kandolf, A. Stelzner, and R. Zell. 2000. Attachment of coxsackievirus B3 variants to various cell lines: mapping of phenotypic differences to capsid protein VP1. Virology 275:77-88.
32. Selinka, H., T. Giroglou, and M. Sapp. 2002. Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299:279-287.
33. Shafren, D. R., R. C. Bates, M. V. Agrez, R. L. Herd, G. F. Burns, and R. D. Barry. 1995. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J. Virol. 69:3873-3877.
34. Shieh, J. T., and J. M. Bergelson. 2002. Interaction with decay-accelerating factor facilitates coxsackievirus B infection of polarized epithelial cells. J. Virol. 76:9474-9480.
35. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
36. Shukla, D., and P. G. Spear. 2001. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Investig. 108:503-510.
37. Spiller, O. B., I. G. Goodfellow, D. J. Evans, J. W. Almond, and B. P. Morgan. 2000. Echoviruses and coxsackie B viruses that use human decay-accelerating factor (DAF) as a receptor do not bind the rodent analogue of DAF. J. Infect. Dis. 181:340-343.
38. Tomko, R. P., C. B. Johansson, M. Totrov, R. Abagyan, J. Frisen, and L. Philipson. 2000. Expression of the adenovirus receptor and its interaction with the fiber knob. Exp. Cell Res. 255:47-55.
39. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94:3352-3356.
40. Tonew, M., M. Hartmann, M. Schmidtke, and A. Stelzner. 1995. Replication and persistence of coxsackieviruses B3 in human fibroblasts. Zentbl. Bakteriol. 282:92-101.
41. Tonew, M., B. Wagner, M. Wagner, M. Schmidtke, and A. Stelzner. 1996. Permissiveness of human embryonal fibroblasts for coxsackieviruses B3. Investigations on virus genetic markers in vitro and localization of virus receptor distribution by immunogold replica technique. Zentbl. Bakteriol. 284:443-456.
42. Turnbull, J., A. Powell, and S. Guimond. 2001. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 11:75-82.
43. Walters, R. W., T. Grunst, J. M. Bergelson, R. W. Finberg, M. J. Welsh, and J. Zabner. 1999. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J. Biol. Chem. 274:10219-10226.