Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions

Journal of Virology

Volumn 72, Issue 2, 1998, Pages 1438-1445

  Summerford, Candace ^a   Samulski, Richard Jude ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; HEPARAN; PROTEOHEPARAN SULFATE; VIRUS RECEPTOR;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ARTICLE; CELL SURFACE; CHO CELL; GENE THERAPY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS ADSORPTION; VIRUS INFECTION; VIRUS PURIFICATION;

EID: 0031906147     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.2.1438-1445.1998     Document Type: Article

References (66)

1. Amicon Division, W. R. Grace Co. 1993. Matrex cellufine sulfate. Amicon technical publication 845. Amicon Division. W. R. Grace Co., Beverly, Mass.
2. Atchison, R. W., B. C. Castro, and W. M. Hammond. 1965. Adeno-associated defective virus particles. Science 149:754-759.
3. Atha, D. H., A. W. Stephens, A. Rimon, and R. D. Rosenberg. 1984. Sequence variation in heparin octasaccharides with high affinity for antithrombin III. Biochemistry 23:5801-5812.
4. Bame, K., and J. D. Esko. 1989. Undersulfated heparan sulfate in a chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J. Biol. Chem. 264:8059-8069.
5. Bame, K. J., K. Lidholt, U. Lindahl, and J. D. Esko. 1991. Biosynthesis of heparan sulfate. J. Biol. Chem. 266:10287-10293.
6. 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 adenovirus 2 and 5. Science 275:1320-1323.
7. Bernfield, M., R. Kokenyesi, M. Kato, M. T. Hinkes, R. L. Gallo, and E. J. Lose. 1992. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8:365-393.
8. Berns, K. I. 1996. Parvoviridae: the viruses and their replication, p. 2173-2197. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, vol. 3. Lippincott-Raven, Philadelphia, Pa.
9. Berns, K. I., and J. A. Rose. 1970. Evidence for single stranded adenovirus-associated virus genome. Isolation and separation of complementary single strands. J. Virol. 5:693-699.
10. Bhat, S., S. L. Spitalink, F. Gonzalez-Scarano, and D. H. Silberg. 1991. Galactosyl ceramide or a derivative is an essential component of the neural receptor for human immunodeficiency virus type 1 envelope glycoprotein gp120. Proc. Natl. Acad. Sci. USA 88:7131-7134.
11. Brown, K. E., S. M. Anderson, and N. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-116.
12. Chen, Y., T. Maguire, R. E. Hileman, J. R. Fromm, J. D. Esko, R. J. Linhardt, and R. M. Marks. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3:866-871.
13. Compton, T., D. M. Nowlin, and N. R. Cooper. 1993. Initiation of human cytomegleovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834-841.
14. Diertrich, C. P., and C. M. F. Cassaro. 1977. Distribution of sulfated mucopolysaccharides in invertebrates. J. Biol. Chem. 252:2254-2261.
15. Esko, J. D., K. S. Rostand, and J. L. Weinke. 1988. Tumor formation dependent on proteoglycan biosynthesis. Science 241:1092-1095.
16. Esko, J. D., T. E. Stewart, and W. H. Taylor. 1985. Animal cell mutants defective in glycosaminoglycan synthesis. Proc. Natl. Acad. Sci. USA 82: 3197-3201.
17. Esko, J. D., J. L. Weinke, W. H. Taylor, G. Ekborg, L. Roden, G. Anantharamaiah, and A. Gawish. 1987. Inhibition of chondroitin and heparan sulfate biosynthesis in chinese hamster ovary cell mutants defective in galactosyl-transferase I. J. Biol. Chem. 262:12189-12195.
18. Ferrari, F. K., T. Samulski, T. Shenk, and R. J. Samulski. 1996. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 7:3277-3234.
19. Fisher, K. J., G. P. Gao, M. D. Weitzman, R. DeMatteo, J. F. Burda, and J. M. Wilson. 1996. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J. Virol. 70:520-532.
20. Flotte, T. 1997. Present at the Cystic Fibrosis Foundation Williamsburg Gene Therapy Conference, June.
21. Fuller, A. O., R. E. Santos, and P. G. Spear. 1989. Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration. J. Virol. 63:3435-3443.
22. Giraud, C., E. Winocour, and K. Berns. 1995. Recombinant junctions formed by site-specific integration of adeno-associated virus into an episome. J. Virol. 69:6917-6924.
23. Giraud, C., E. Winocour, and K. I. Berns. 1994. Site-specific integration by adeno-associated virus is directed by a cellular DNA sequence. Proc. Natl. Acad. Sci. USA 91:10039-10043.
24. Herrler, G. 1985. The receptor destroying enzyme of influenza C virus is neuraminate-O-acetylesterase. EMBO J. 4:1053-1056.
25. Hoggan, M. D., N. R. Blacklow, and W. P. Rowe. 1966. Studies of small DNA viruses found in various adenovirus preparations: physical, biological, and immunological characteristics. Proc. Natl. Acad. Sci. USA 55:1457-1471.
26. Huang, S., T. Kamata, Y. Takada, Z. M. Ruggeri, and G. R. Nemerow. 1996. Adenovirus interaction with distinct integrins mediates seperate events in cell entry and gene delivery to hematopoietic cells. J. Virol. 70:4502-4508.
27. Iozzo, R. V. 1987. Turnover of heparin sulfate proteoglycan in human colon carcinoma cells. J. Biol. Chem. 262:1888-1900.
28. Jackson, R. L., S. J. Busch, and A. D. Cardin. 1991. Glycosaminoglycans: molecular propeties, protein interactions, and role in physiological processes. Physiol. Rev. 71:481-539.
29. Jackson, T., F. M. Ellard, R. A. Ghazaleh, S. M. Brookes, W. E. Blakemore, A. H. Corteyn, D. I. Stuart, J. W. I. 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.
30. Kjellen, L., and U. Lindahl. 1991. Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60:443-475.
31. Kotin, R. M., M. Siniscalco, R. J. Samulski, X. Zhu, L. Hunter, C. A. Laughlin, S. McLaughlin, N. Muzyczka, M. Rocchi, and K. I. Berns. 1990. Site-specific integration by adeno-associated virus. Proc. Natl. Acad. Sci. USA 87:2211-2215.
32. 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.
33. Lindahl, U., G. Backstrom, L. Thunberg, and I. G. Leder. 1980. Evidence for a 3-O-sulfated D-glucosamine residue in the anti-thrombin-binding sequence of heparin. Proc. Natl. Acad. Sci. USA 77:6551-6555.
34. Linhardt, R. J. 1994. Analysis of glycosaminoglycans with polysaccharide lyases, p. 17.13.17-17.13.32. In K. Janssen (ed.), Current protocols in molecular biology, vol. 3. John Wiley & Sons, Inc., New York, N.Y.
35. Linhardt, R. J., C. L. Cooney, and P. M. Galliher. 1986. Polysaccharide lyases. Appl. Biochem. Biotechnol. 12:135-177.
36. Lycke, E., M. Johansson, B. Svennerholm, and U. Lindah. 1991. Binding of herpes simplex virus to cellular heparan sulfate, an initial step in the adsorption process. J. Gen. Virol. 72:1131-1137.
37. McCarty, D. M., and R. J. Samulski. 1997. Adeno-associated viral vectors, p. 62-78. In M. Strauss and J. Barranger (ed.), Concepts in gene therapy. Walter de Gruyter, Bellin, N.Y.
38. McCown, T. J., X. Xiao, J. Li, G. R. Breese, and R. J. Samulski. 1996. Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res. 713:99-107.
39. McKeon, C., and R. J. Samulski. 1996. NIDDK workshop on AAV vectors: gene transfer into quiescent cells. Hum. Gene Ther. 7:1615-1619.
40. Melnick, J. L., H. D. Mayor, K. O. Smith, and F. Rapp. 1965. Association of 20 millimicron particles with adenoviruses. J. Bacteriol. 90:271-274.
41. Mettenleiter, T. C., L. Zask, F. Zukermann, N. Sugg, H. Kern, and T. Ben-Porat. 1990. Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J. Virol. 64:278-286.
42. Mizukami, H., K. E. Brown, and N. Young. 1996. Adeno-associated virus type 2 binds to a 150-kilodalton cell membrane glycoprotein. Virology 217: 124-130.
43. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/ NGF receptor family. Cell 87:427-436.
44. Murphy-Ulrich, J. E., L. G. Westrick, J. D. Esko, and D. F. Mosher. 1988. Altered metabolism of thrombospondin hy chinese hamster ovary cells defective in glycosaminoglycan synthesis. J. Biol. Chem. 263:6400-6406.
45. Muzyczka, N. 1992. Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr. Top. Microbiol. Immunol. 158:97-129.
46. Ponnazhagan, S., X. Wang, M. J. Woody, F. Luo, L. Y. Kang, L. N. Madahavi, C. M. Munshi, Z. Z. Shang, and A. Srivasta. 1996. Differential expression in human cells from the p6 promoter of human parvovirus B19 following plasmid transfection and recombinant adeno-associated virus 2 (AAV) infection: human megacaryocytic leukaemia cells are non-permissive for AAV infection. J. Gen. Virol. 77:1111-1122.
47. Rogers, G. N., G. Herrler, J. C. Paulson, and H. D. Klenk. 1986. Influenza C viruses uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J. Biol. Chem. 261:5947-5941.
48. Roghani, M., and D. Moscatelli. 1992. Basic Fibroblast growth factor is internalized through both receptor-mediated and heparin sulfate mediated mechanisms. J. Biol. Chem. 267:22156-22162.
49. Rolling, F., and R. J. Samulski. Unpublished data.
50. Rostand, K. S., and J. D. Esko. 1997. Microbial adherence and invasion through proteoglycans. Infect. Immun. 65:1-8.
51. Ruoslahti, E. 1989. Proteoglycans in cell regulation. J. Biol. Chem. 264:13369-13372.
52. Samulski, R. J. 1995. Adeno-associated virus-based vectors for human gene theraphy, p. 232-271. In K. M. Hui (ed.), Gene therapy: from laboratory to the clinic. World Scientific Publishing Co., Singapore, Singapore.
53. Samulski, R. J. 1993. Adeno-associated virus: integration at a specific chromosomal locus. Curr. Opin. Genet. Dev. 3:74-80.
54. Samulski, R. J. 1997. Development of Adeno-assoeiated virus as a vector for invivo gene therapy, p. 197-203. In L. M. Houdebine (ed.), Transgenic animals: generation and use. Harwood Academic Publishers, Chur, Switzerland.
55. Samulski, R. J., L.-S. Chang, and T. Shenk. 1989. Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J. Virol. 63:3822-3828.
56. Samulski, R. J., X. Zhu, X. Xiao, J. D. Brook, D. E. Housman, N. Epstein, and L. A. Hunter. 1991. Targeted integration of adeno-assoaated virus (AAV) into human chromosome 19. EMBO J. 10:3941-3950.
57. Sattentau, Q. J., and R. A. Weiss. 1991. The CD4 antigen: pysiological ligand and HIV receptor. Cell. 52:631-633.
58. Saxena, U., M. G. Klein, and I. J. Goldberg. 1990. Metabolism of endothelial cell-bound lipoprotein lipase. J. Biol. Chem. 265:12880-12886.
59. Sheih, M., R. I. Montgomery, J. D. Esko, and P. Spear. 1992. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J. Cell Biol. 116:1273-1281.
60. Snyder, R. O., X. Xiao, and R. J. Samulski. 1996. Production of recombinant adeno-associated virus vectors, p. 12.1.1-12.2.23. In N. Dracopoli, J. Haines, B. Krof, D. Moir, C. Seidman, and J. Seichman (ed.), Current protocols in human genetics. John Wiley & Sons Ltd., New York, N.Y.
61. Summerford, C., and R. J. Samulski. Unpublished data.
62. Walsh, C., M. L. Johnson, J. L. Miller A. Nienhuis, and R. J. Samulski. 1994. Gene therapy for hemaglobinopathy. Mol. Cell. Biol. 14:289-299.
63. Wicham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrins αVβ3 and αVβ5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
64. WuDunn, D., and P. Spear. 1989. Initial interaction of herpes simplex virus with cells is binding to heparin sulfate. J. Virol. 63:52-58.
65. Xiao, X., J. Li, and R. J. Samulski. 1996. Efficient long term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J. Virol. 70:8098-8108.
66. Yanagishita, M., and V. C. Hascall. 1984. Metabolism of proteoglycans in rat ovarian granulosa cell culture. J. Biol. Chem. 259:10270-10283.