Glycoconjugate glycans as viral receptors

Annals of Medicine

Volumn 37, Issue 3, 2005, Pages 154-172

  Olofsson, Sigvard ^a   Bergström, Tomas ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Glycoprotein; Glycosphingolipid; Heparan sulphate; Pathogenesis; Proteoglycans; Receptor; Virus

Indexed keywords

BLOOD GROUP ANTIGEN; GLYCAN DERIVATIVE; GLYCOCONJUGATE; GLYCOLIPID; GLYCOPROTEIN; GLYCOSAMINOGLYCAN POLYSULFATE; PROTEOGLYCAN; SIALIC ACID DERIVATIVE; VIRUS RECEPTOR;

BINDING AFFINITY; GENE DELETION; GENE MUTATION; HUMAN; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; RESPIRATORY SYSTEM; REVIEW; TISSUE DISTRIBUTION; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS RESISTANCE;

CARBOHYDRATE SEQUENCE; CELL MEMBRANE; GLYCOCONJUGATES; GLYCOSAMINOGLYCANS; HUMANS; MOLECULAR STRUCTURE; N-ACETYLNEURAMINIC ACID; OLIGOSACCHARIDES; RECEPTORS, CELL SURFACE; RECEPTORS, VIRUS;

EID: 20344381822     PISSN: 07853890     EISSN: None     Source Type: Journal    
DOI: 10.1080/07853890510007340     Document Type: Review

References (158)

1. Ravn V, Dabelsteen E. Tissue distribution of histo-blood group antigens. APMIS. 2000;108:1-28.
2. Moore JP, Trkola A, Dragic T. Co-receptors for HIV-1 entry. Curr Opin Immunol. 1997;9:551-62.
3. Bomsel M, David V. Mucosal gatekeepers: Selecting HIV viruses for early infection. Nat Med. 2002;8:114-6.
4. Martin J, Wharton SA, Lin YP, Takemoto DK, Skehel JJ, Wiley DC, et al. Studies of the binding properties of influenza hemagglutinin receptor- site mutants. Virology. 1998;241:101-11.
5. Trybala E, Olofsson S, Mårdberg K, Svennerholm B, Umemoto K, Glorioso JC, et al. Structural and functional features of the polycationic peptide required for inhibition of herpes simplex virus type 1 invasion of cells. Virus Res. 2004;62:125-34.
6. Hansson GC, Karlsson KA, Larson G, Strömberg N, Thurin J, Orvell C, et al. A novel approach to the study of glycolipid receptors for viruses. Binding of Sendai virus to thin-layer chromatograms. FEBS Lett. 1984;170:15-8.
7. Holmgren J, Svennerholm L, Elwing H, Fredman P, Strannegård Ö. Sendai virus receptor: proposed recognition structure based on binding to plastic-adsorbed gangliosides. Proc Natl Acad Sci U S A. 1980;77:1947-50.
8. Karlsson KA, Ångstrom J, Bergström J, Lanne B. Microbial interaction with animal cell surface carbohydrates. APMIS Suppl. 1992;27:71-83.
9. Miller-Podraza H, Johansson L, Johansson P, Larsson T, Matrosovich M, Karlsson KA. A strain of human influenza A virus binds to extended but not short gangliosides as assayed by thin-layer chromatography overlay. Glycobiology. 2000;10:975-82.
10. Gilbert J, Dahl J, Riney C, You J, Cui C, Holmes R, et al. Ganglioside GD1a restores infectibility to mouse cells lacking functional receptors for polyomavirus. J Virol. 2005;79:615-8.
11. McCormick C, Leduc Y, Martindale D, Mattison K, Esford LE, Dyer AP, et al. The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat Genet. 1998;19:158-61.
12. Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, et al. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell. 1999;99:13-22.
13. Suzuki T, Portner A, Scroggs RA, Uchikawa M, Koyama N, Matsuo K, et al. Receptor specificities of human respiro-viruses. J Virol. 2001;75:4604-13.
14. Hoorn B, Tyrrell DA. Organ cultures in virology. Prog Med Virol. 1969;11:408-50.
15. Skehel JJ, Wiley DC. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem. 2000;69:531-69.
16. Arnberg N, Pring-Akerblom P, Wadell G. Adenovirus type 37 uses sialic acid as a cellular receptor on Chang C cells. J Virol. 2002;76:8834-41.
17. Arnberg N, Kidd AH, Edlund K, Olfat F, Wadell G. Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus alpha(v) integrins. J Virol. 2000;74:7691-3.
18. Arnberg N, Edlund K, Kidd AH, Wadell G. Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol. 2000;74:42-8.
19. Terraciano AJ, Wang N, Schuman JS, Haffner G, Panjwani N, Zhao Z, et al. Sialyl Lewis X, Lewis X, and N-acetyllactosamine expression on normal and glaucomatous eyes. Curr Eye Res. 1999;18:73-8.
20. Arnberg N, Kidd AH, Edlund K, Nilsson J, Pring-Akerblom P, Wadell G. Adenovirus type 37 binds to cell surface sialic acid through a charge-dependent interaction. Virology. 2002;302:33-43.
21. Burmeister WP, Guilligay D, Cusack S, Wadell G, Arnberg N. Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J Virol. 2004;78:7727-36.
22. Alexander DA, Dimock K. Sialic acid functions in enterovirus 70 binding and infection. J Virol. 2002;76:11265-72.
23. Nokbeh MR, Hazra S, Alexander DA, Khan A, McAllister M, Suuronen EJ, et al. Enterovirus 70 binds to different glycoconjugates containing 2,3-linked sialic acid on different cell lines. J Virol. 2005;79. In press.
24. Haddad A, Nokhbeh MR, Alexander DA, Dawe SJ, Grise C, Gulzar N, et al. Binding to decay-accelerating factor is not required for infection of human leukocyte cell lines by enterovirus 70. J Virol. 2004;78:2674-81.
25. Uncapher CR, DeWitt CM, Colonno RJ. The major and minor group receptor families contain all but one human rhinovirus serotype. Virology. 1991;180:814-7.
26. Blomqvist S, Savolainen C, Raman L, Roivainen M, Hovi T. Human rhinovirus 87 and enterovirus 68 represent a unique serotype with rhinovirus and enterovirus features. J Clin Microbiol. 2002;40:4218-23.
27. Zambon MC. Epidemiology and pathogenesis of influenza. J Antimicrob Chemother. 1999;44Suppl B: 3-9.
28. Hirst G. The agglutination of red cells by allantoic fluid of chick embryos infected with influenza virus. Science. 1941;94:22-3.
29. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56:152-79.
30. Wright P, Webster RG. Ortomyxoviruses. In: Knipe D, Howley P, editors. Fields Virology, Fourth Edition. Vol. 1. Philadelphia: Lippincott Williams & Wilkins; 2001. p. 1487-531.
31. Lipatov AS, Govorkova EA, Webby RJ, Ozaki H, Peiris M, Guan Y, et al. Influenza: emergence and control. J Virol. 2004;78:8951-9.
32. Nicholson KG, Wood JM, Zambon M. Influenza. Lancet. 2003;362:1733-45.
33. Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology. 1983;127:361-73.
34. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004;101:4620-4.
35. Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, et al. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet. 2004;363:587-93.
36. Webby RJ, Webster RG. Are we ready for pandemic influenza? Science. 2003;302:1519-22.
37. Webby R, Hoffmann E, Webster R. Molecular constraints to interspecies transmission of viral pathogens. Nat Med. 2004;10(Suppl): S77-81.
38. Olofsson S, Kumlin U, Dimock K, Arnberg N. Avian influenza and sialic acid receptors: More than meets the eye. Lancet Infect Dis. 2005;5:184-8.
39. Rosenthal PB, Zhang X, Formanowski F, Fitz W, Wong CH, Meier-Ewert H, et al. Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature. 1998;396:92-6.
40. Kunkel F, Herrler G. Structural and functional analysis of the surface protein of human coronavirus OC43. Virology. 1993;195:195-202.
41. Markwell MA, Svennerholm L, Paulson JC. Specific gangliosides function as host cell receptors for Sendai virus. Proc Natl Acad Sci U S A. 1981;78:5406-10.
42. Ah-Tye C, Schwartz S, Huberman K, Carlin E, Moscona A. Virus-receptor interactions of human parainfluenza viruses types 1, 2 and 3. Microb Pathog. 1999;27:329-36.
43. Padgett BL, Walker DL. Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. J Infect Dis. 1973; 127:467-70.
44. Di Taranto C, Pietropaolo V, Orsi GB, Jin L, Sinibaldi L, Degener AM. Detection of BK polyomavirus genotypes in healthy and HIV-positive children. Eur J Epidemiol. 1997;13:653-7.
45. Liu CK, Wei G, Atwood WJ. Infection of glial cells by the human polyomavirus JC is mediated by an N-linked glycoprotein containing terminal alpha(2-6)-linked sialic acids. J Virol. 1998;72:4643-9.
46. Sinibaldi L, Goldoni P, Pietropaolo V, Longhi C, Orsi N. Involvement of gangliosides in the interaction between BK virus and Vero cells. Arch Virol. 1990;113:291-6.
47. Eash S, Querbes W, Atwood WJ. Infection of vero cells by BK virus is dependent on caveolae. J Virol. 2004; 78:11583-90.
48. Fujinaga Y, Wolf AA, Rodighiero C, Wheeler H, Tsai B, Allen L, et al. Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm. Mol Biol Cell. 2003;14:4783-93.
49. Lai CM, Lai YK, Rakoczy PE. Adenovirus and adeno-associated virus vectors. DNA Cell Biol. 2002;21:895-913.
50. Davidson BL, Stein CS, Heth JA, Martins I, Kotin RM, Derksen TA, et al. Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc Natl Acad Sci U S A. 2000;97:3428-32.
51. Walters RW, Yi SM, Keshavjee S, Brown KE, Welsh MJ, Chiorini JA, et al. Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J Biol Chem. 2001;276:20610-6.
52. Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA. Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J Virol. 2001;75:6884-93.
53. Matrosovich M, Klenk HD. Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor binding. Rev Med Virol. 2003;13:85-97.
54. Colman PM, Ward CW. Structure and diversity of influenza virus neuraminidase. Curr Top Microbiol Immunol. 1985;114:177-255.
55. Uhnoo I, Linde A, Pauksens K, Lindberg A, Eriksson M, R. N. Treatment and prevention of influenza: Swedish recommendations. Scand J Infect Dis. 2003;35:3-11.
56. Kim CU, Chen XBMD. Neuraminidase inhibitors as antiinfluenza virus agents. Antimicrob Agents Chemother. 1999;10:141-54.
57. Strasser P, Unger U, Strobl B, Vilas U, Vlasak R. Recombinant viral sialate-O-acetylesterases. Glycoconj J. 2004;20:551-61.
58. Mason DY, Andre P, Bensussan A, Buckley C, Civin C, Clark E, et al. CD antigens 2001. Tissue Antigens. 2001;58:425-30.
59. Smits SL, Gerwig GJ, van Vliet AL, Lissenberg A, Briza P, Kamerling JP, et al. Nidovirus sialate-O-acetylesterases: Evolution and substrate specificity of corona- and toroviral receptor-destroying enzymes. J Biol Chem. 2005;280: 6933-41.
60. Hutson AM, Atmar RL, Estes MK. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 2004;12:279-87.
61. Marionneau S, Ruvoen N, Le Moullac-Vaidye B, Clement M, Cailleau-Thomas A, Ruiz-Palacois G, et al. Norwalk virus binds to histo-blood group, antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology. 2002;122:1967-77.
62. Hutson AM, Atmar RL, Graham DY, Estes MK. Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis. 2002;185:1335-7.
63. Harrington PR, Lindesmith L, Yount B, Moe CL, Baric RS. Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J Virol. 2002;76:12335-43.
64. Huang P, Farkas T, Marionneau S, Zhong W, Ruvoen-Clouet N, Morrow AL, et al. Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J Infect Dis. 2003;188:19-31.
65. Tan M, Huang P, Meiler J, Zhong W, Farkas T, Jiang X. Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. J Virol. 2003;77:12562-71.
66. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, et al. Human susceptibility and resistance to Norwalk virus infection. Nat Med. 2003;9:548-53.
67. Heegaard ED, Brown KE. Human parvovirus B19. Clin Microbiol Rev. 2002;15:485-505.
68. Brown KE, Hibbs JR, Gallinella G, Anderson SM, Lehman ED, McCarthy, et al. Resistance to parvovirus B19 infection due to lack of virus receptor (erythrocyte P antigen). N Engl J Med. 1994;330:1192-6.
69. Brown KE, Anderson SM, Young NS. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science. 1993;262:114-7.
70. von dem Borne AE, Bos MJ, Joustra-Maas N, Tromp JF, van't Veer MB, van Wijngaarden-du Bois R, et al. A murine monoclonal IgM antibody specific for blood group P antigen (globoside). Br J Haematol. 1986;63:35-46.
71. Jordan JA, DeLoia JA. Globoside expression within the human placenta. Placenta. 1999;20:103-8.
72. Kaufmann B, Simpson AA, Rossmann MG. The structure of human parvovirus B19. Proc Natl Acad Sci U S A. 2004;101:11628-33.
73. Weigel-Kelley KA, Yoder MC, Srivastava A. Alpha5beta1 integrin as a cellular coreceptor for human parvovirus B19: requirement of functional activation of beta1 integrin for viral entry. Blood. 2003;102:3927-33.
74. Marcus DM, Kundu SK, Suzuki A. The P blood group system: recent progress in immunochemistry and genetics. Semin Hematol. 1981;18:63-71.
75. Marcus DM. Blood group immunochemistry and genetics. Introduction. Semin Hematol. 1981;18:1-3.
76. Brown KE, Liu Z, Gallinella G, Wong S, Mills IP, O'Sullivan MG. Simian parvovirus infection: a potential zoonosis. J Infect Dis. 2004;190:1900-7.
77. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, Ravkov EV, et al. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science. 1998;282:2079-81.
78. Martin PT. Dystroglycan glycosylation and its role in matrix binding in skeletal muscle. Glycobiology. 2003;13:55R-66.
79. Kunz S, Sevilla N, McGavern DB, Campbell KP, Oldstone MBA. Molecular analysis of the interaction of LCMV with its cellular receptor {alpha}-dystroglycan. J Cell Biol. 2001;155:301-10.
80. Lindahl U, Kusche-Gullberg M, Kjellen L. Regulated diversity of heparan sulfate. J Biol Chem. 1998; 273:24979-82.
81. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest. 2001;108:169-73.
82. Duncan G, McCormick C, Tufaro F. The link between heparan sulfate and hereditary bone disease: finding a function for the EXT family of putative tumor suppressor proteins. J Clin Invest. 2001;108:511-6.
83. McCormick C, Duncan G, Tufaro F. Herpes simplex virus: discovering the link between heparan sulphate and hereditary bone tumours. Rev Med Virol. 2000;10:373-84.
84. Liu J, Shriver Z, Pope RM, Thorp SC, Duncan MB, Copeland RJ, et al. Characterization of a heparan sulfate octasaccharide that binds to herpes simplex virus type 1 glycoprotein D. J Biol Chem. 2002;277:33456-67.
85. Kinoshita A, Yamada S, Haslam SM, Morris HR, Dell A, Sugahara K. Isolation and structural determination of novel sulfated hexasaccharides from squid cartilage chondroitin sulfate E that exhibits neuroregulatory activities. Biochemistry. 2001;40:12654-65.
86. Birkmann A, Mahr K, Ensser A, Yaguboglu S, Titgemeyer F, Fleckenstein B, et al. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J Virol. 2001;75:11583-93.
87. Akula SM, Pramod NP, Wang FZ, Chandran B. Human herpesvirus 8 envelope-associated glycoprotein B interacts with heparan sulfate-like moieties. Virology. 2001;284: 235-49.
88. Compton T, Nowlin DM, Cooper NR. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology. 1993;193:834-41.
89. Gehrz RC, Nelson CM, Kari BE. A combination of human cytomegalovirus (HCMV)-specific murine monoclonal antibodies exhibits synergistic antiviral activity in vitro. Antiviral Res. 1992;17:115-31.
90. Zhu Z, Gershon MD, Ambron R, Gabel C, Gershon AA. Infection of cells by varicella zoster virus: inhibition of viral entry by mannose 6-phosphate and heparin. Proc Natl Acad Sci U S A. 1995;92:3546-50.
91. Secchiero P, Sun D, De Vico AL, Crowley RW, Reitz MS, Zauli G, et al. Role of the extracellular domain of human herpesvirus 7 glycoprotein B in virus binding to cell surface heparan sulfate proteoglycans. J Virol. 1997;71:4571-80.
92. Herold BC, WuDunn D, Soltys N, Spear PG. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectiviry. J Virol. 1991;65:1090-8.
93. Trybala E, Liljeqvist JA, Svennerholm B, Bergstrom T. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J Virol. 2000;74:9106-14.
94. Lycke E, Johansson M, Svennerholm B, Lindahl U. Binding of herpes simplex virus to cellular heparan sulphate, an initial step in the adsorption process. J Gen Virol. 1991;72:1131-7.
95. Herold BC, Gerber SI, Polonsky T, Belval BJ, Shaklee PN, Holme K. Identification of structural features of heparin required for inhibition of herpes simplex virus type 1 binding. Virology. 1995;206:1108-16.
96. Feyzi E, Trybala E, Bergstrom T, Lindahl U, Spillmann D. Structural requirement of heparan sulfate for interaction with herpes simplex virus type 1 virions and isolated glycoprotein C. J Biol Chem. 1997;272:24850-7.
97. Herold BC, Gerber SI, Belval BJ, Siston AM, Shulman N. Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. J Virol. 1996;70:3461-9.
98. Trybala E, Bergstrom T, Svennerholm B, Jeansson S, Glorioso JC, Olofsson S. Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate. J Gen Virol. 1994;75:743-52.
99. Mardberg K, Trybala E, Glorioso JC, Bergstrom T. Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. J Gen Virol. 2001;82:1941-50.
100. Terhune SS, Coleman KT, Sekulovich R, Burke RL, Spear PG. Limited variability of glycoprotein gene sequences and neutralizing targets in herpes simplex virus type 2 isolates and stability on passage in cell culture. J Infect Dis. 1998;178:8-15.
101. Trybala E, Roth A, Johansson M, Liljeqvist JA, Rekabdar E, Larm O, et al. Glycosaminoglycan-binding ability is a feature of wild-type strains of herpes simplex virus type 1. Virology. 2002;302:413-9.
102. Liu J, Shriver Z, Blaiklock P, Yoshida K, Sasisekharan R, Rosenberg RD. Heparan sulfate D-glucosaminyl 3-O-sulfotransferase-3A sulfates N-unsubstituted glucosamine residues. J Biol Chem. 1999;274:38155-62.
103. Yoon M, Spear PG. Random mutagenesis of the gene encoding a viral ligand for multiple cell entry receptors to obtain viral mutants altered for receptor usage. Proc Natl Acad Sci U S A. 2004;101:17252-7.
104. Spear PG. Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol. 2004;6:401-10.
105. Dementiev A, Petitou M, Herbert JM, Gettins PG. The ternary complex of antithrombin-anhydrothrombin-heparin reveals the basis of inhibitor specificity. Nat Struct Mol Biol. 2004;11:863-7.
106. Krusat T, Strecken HJ. Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. Arch Virol. 1997;142:1247-54.
107. Hallak LK, Collins PL, Knudson W, Peeples ME. Iduronic acid-containing glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology. 2000;271:264-75.
108. Shields B, Mills J, Ghildyal R, Gooley P, Meanger J. Multiple heparin binding domains of respiratory syncytial virus G mediate binding to mammalian cells. Arch Virol. 2003;148:1987-2003.
109. Feldman SA, Hendry RM, Beeler JA. Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J Virol. 1999;73:6610-7.
110. Feldman SA, Audet S, Beeler JA. The fusion glycoprotein of human respiratory syncytial virus facilitates virus attachment and infectivity via an interaction with cellular heparan sulfate. J Virol. 2000;74:6442-7.
111. Hallak LK, Spillmann D, Collins PL, Peeples ME. Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J Virol. 2000;74:10508-13.
112. Wyde PR, Moylett EH, Chetry SN, Jewell A, Bowlin TL, Piedra PA. Comparison of the inhibition of human meta-pneumovirus and respiratory syncytial virus by NMSO3 in tissue culture assays. Antiviral Res. 2004;63:51-9.
113. Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD, Linhardt RJ, et al. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med. 1997;3:866-71.
114. Su CM, Liao CL, Lee YL, Lin YL. Highly sulfated forms of heparin sulfate are involved in Japanese encephalitis virus infection. Virology. 2001;286:206-15.
115. Mandl CW, Kroschewski H, Allison SL, Kofler R, Holzmann H, Meixner T, et al. Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo. J Virol. 2001;75:5627-37.
116. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, Ruigrok RW, et al. Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology. 2002;292:162-8.
117. Lin YL, Lei HY, Lin YS, Yeh TM, Chen SH, Liu HS. Heparin inhibits dengue-2 virus infection of five human liver cell lines. Antiviral Res. 2002;56:93-6.
118. Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, et al. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem. 2003;278:41003-12.
119. Vongchan P, Warda M, Toyoda H, Toida T, Marks RM, Linhardt RJ. Structural characterization of human liver heparan sulfate. Biochim Biophys Acta. 2005;1721:1-8.
120. Ying C, Van Pelt JF, Van Lommel A, Van Ranst M, Leyssen P, De Clercq E, et al. Sulphated and sulphonated polymers inhibit the initial interaction of hepatitis B virus with hepatocytes. Antivir Chem Chemother. 2002; 13:157-64.
121. Patel M, Yanagishita M, Roderiquez G, Bou-Habib DC, Oravecz T, Hascall VC, et al. Cell-surface heparan sulfate proteoglycan mediates HIV-1 infection of T-cell lines. AIDS Res Hum Retroviruses. 1993;9:167-74.
122. Roderiquez G, Oravecz T, Yanagishita M, Bou-Habib DC, Mostowski H, Norcross MA. Mediation of human immunodeficiency virus type 1 binding by interaction of cell surface heparan sulfate proteoglycans with the V3 region of envelope gp120-gp41. J Virol. 1995;69:2233-9.
123. Ibrahim J, Griffin P, Coombe DR, Rider CC, James W. Cell-surface heparan sulfate facilitates human immunodeficiency virus Type 1 entry into some cell lines but not primary lymphocytes. Virus Res. 1999;60:159-69.
124. Saphire AC, Bobardt MD, Zhang Z, David G, Gallay PA. Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J Virol. 2001;75:9187-200.
125. Argyris EG, Acheampong E, Nunnari G, Mukhtar M, Williams KJ, Pomerantz RJ. Human immunodeficiency virus type 1 enters primary human brain microvascular endothelial cells by a mechanism involving cell surface proteoglycans independent of lipid rafts. J Virol. 2003;77:12140-51.
126. Bobardt MD, Salmon P, Wang L, Esko JD, Gabuzda D, Fiala M, et al. Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J Virol. 2004;78:6567-84.
127. Damonte EB, Matulewicz MC, Cerezo AS. Sulfated seaweed polysaccharides as antiviral agents. Curr Med Chem. 2004;11:2399-419.
128. Vaheri A, Cantell K. The Effect of Heparin on Herpes Simplex Virus. Virology. 1963;21:661-2.
129. Neyts J, De Clercq E. Effect of polyanionic compounds on intracutaneous and intravaginal herpesvirus infection in mice: impact on the search for vaginal microbicides with anti-HIV activity. J Acquir Immune Defic Syndr Hum Retrovirol. 1995;10:8-12.
130. Piret J, Lamontagne J, Bestman-Smith J, Roy S, Gourde P, Desormeaux A, et al. In vitro and in vivo evaluations of sodium lauryl sulfate and dextran sulfate as microbicides against herpes simplex and human immunodeficiency viruses. J Clin Microbiol. 2000;38:110-9.
131. Witvrouw M, De Clercq E. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen Pharmacol. 1997;29:497-511.
132. Joyce JG, Tung JS, Przysiecki CT, Cook JC, Lehman ED, Sands JA, et al. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem. 1999;274:5810-22.
133. Ito M, Baba M, Sato A, Pauwels R, De Clercq E, Shigeta S. Inhibitory effect of dextran sulfate and heparin on the replication of human immunodeficiency virus (HIV) in vitro. Antiviral Res. 1987;7:361-7.
134. Carlucci MJ, Ciancia M, Matulewicz MC, Cerezo AS, Damonte EB. Antiherpetic activity and mode of action of natural carrageenans of diverse structural types. Antiviral Res. 1999;43:93-102.
135. Carlucci MJ, Scolaro LA, Noseda MD, Cerezo AS, Damonte EB. Protective effect of a natural carrageenan on genital herpes simplex virus infection in mice. Antiviral Res. 2004;64:137-41.
136. Aguilar JS, Rice M, Wagner EK. The polysulfonated compound suramin blocks adsorption and lateral difusion of herpes simplex virus type-1 in vero cells. Virology. 1999;258:141-51.
137. Nyberg K, Ekblad M, Bergstrom T, Freeman C, Parish CR, Ferro V, et al. The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. Antiviral Res. 2004;63:15-24.
138. Pastey MK, Gower TL, Spearman PW, Crowe JE Jr. Graham BS. A RhoA-derived peptide inhibits syncytium formation induced by respiratory syncytial virus and parainfluenza virus type 3. Nat Med. 2000;6:35-40.
139. Budge PJ, Li Y, Beeler JA, Graham BS. RhoA-derived peptide dimers share mechanistic properties with other polyanionic inhibitors of respiratory syncytial virus (RSV), including disruption of viral attachment and dependence on RSV G. J Virol. 2004;78:5015-22.
140. Fry EE, Lea SM, Jackson T, Newman JW, Ellard FM, Blakemore WE, et al. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 1999;18:543-54.
141. Dechecchi MC, Tamanini A, Bonizzato A, Cabrini G. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology. 2000; 268:382-90.
142. Lee E, Hall RA, Lobigs M. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J Virol. 2004;78:8271-80.
143. Kari B, Gehrz R. Structure, composition and heparin binding properties of a human cytomegalovirus glycoprotein complex designated gC-II. J Gen Virol. 1993;74:255-64.
144. Cooling LL, Koerner TA, Naides SJ. Multiple glycosphingolipids determine the tissue tropism of parvovirus B19. J Infect Dis. 1995;172:1198-205.
145. Suzuki Y, Nagao Y, Kato H, Suzuki T, Matsumoto M, Murayama J. The hemagglutinins of the human influenza viruses A and B recognize different receptor microdomains. Biochim Biophys Acta. 1987;903:417-24.
146. Shafti-Keramat S, Handisurya A, Kriehuber E, Meneguzzi G, Slupetzky K, Kirnbauer R. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J Virol. 2003;77:13125-35.
147. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M. Human papillomavirus infection requires cell surface heparan sulfate. J Virol. 2001;75:1565-70.
148. Opie SR, Warrington KHJr. Agbandje-McKenna M, Zolotukhin S, Muzyczka N. Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding. J Virol. 2003;77:6995-7006.
149. Hsiao JC, Chung CS, Chang W. Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J Virol. 1999;73:8750-61.
150. Chung CS, Hsiao JC, Chang YS, Chang W. A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J Virol. 1998;72:1577-85.
151. Paul RW, Choi AH, Lee PW. The alpha-anomeric form of sialic acid is the minimal receptor determinant recognized by reovirus. Virology. 1989;172:382-5.
152. Gentsch JR, Pacitti AF. Differential interaction of reovirus type 3 with sialylated receptor components on animal cells. Virology. 1987;161:245-8.
153. Pacitti AF, Gentsch JR. Inhibition of reovirus type 3 binding to host cells by sialylated glycoproteins is mediated through the viral attachment protein. J Virol. 1987;61:1407-15.
154. Svensson L. Group C rotavirus requires sialic acid for erythrocyte and cell receptor binding. J Virol. 1992; 66:5582-5.
155. Ciarlet M, Ludert JE, Iturriza-Gomara M, Liprandi F, Gray JJ, Desselberger U, et al. Initial interaction of rotavirus strains with N-acetylneuraminic (sialic) acid residues on the cell surface correlates with VP4 genotype, not species of origin. J Virol. 2002;76:4087-95.
156. Ciarlet M, Crawford SE, Cheng E, Blutt SE, Rice DA, Bergelson JM, et al. VLA-2 (alpha2beta1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J Virol. 2002;76:1109-23.
157. Bobardt MD, Armand-Ugon M, Clotet I, Zhang Z, David G, Este JA. et al. Effect of polyanion-resistance on HIV-1 infection. Virology. 2004;325:389-98.
158. Monzavi-Karbassi B, Luo P, Cunto-Amesty G, Jousheghany F, Pashov A, Weissman D, et al. Fucosylated lactosamines participate in adhesion of HIV-1 envelope glycoprotein to dendritic cells. Arch Virol. 2004;149:75-91.