Emerging Roles of Heparan Sulfate Proteoglycans in Viral Pathogenesis

Raghuram Koganti; Abdullah Memon; Deepak Shukla

doi:10.1055/s-0041-1725068

Seminars in Thrombosis and Hemostasis, Inhaltsverzeichnis

Semin Thromb Hemost 2021; 47(03): 283-294
DOI: 10.1055/s-0041-1725068

Review Article

Emerging Roles of Heparan Sulfate Proteoglycans in Viral Pathogenesis

Autor*innen

Raghuram Koganti

¹Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, Chicago, Illinois
Abdullah Memon

²College of Medicine, University of Illinois at Chicago, Chicago, Illinois
Deepak Shukla

³Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, Chicago, Illinois

⁴Department of Microbiology and Immunology, University of Illinois at Chicago, Chicago, Illinois

Abstract

Heparan sulfate is a glycosaminoglycan present in nearly all mammalian tissues. Heparan sulfate moieties are attached to the cell surface via heparan sulfate proteoglycans (HSPGs) which are composed of a protein core bound to multiple heparan sulfate chains. HSPGs contribute to the structural integrity of the extracellular matrix and participate in cell signaling by releasing bound cytokines and chemokines once cleaved by an enzyme, heparanase. HSPGs are often exploited by viruses during infection, particularly during attachment and egress. Loss or inhibition of HSPGs initially during infection can yield significant decreases in viral entry and infectivity. In this review, we provide an overview of HSPGs in the lifecycle of multiple viruses, including herpesviruses, human immunodeficiency virus, dengue virus, human papillomavirus, and coronaviruses.

Keywords

heparan sulfate - heparan sulfate proteoglycan - heparanase - herpesvirus - coronavirus

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Referenzen

References
1 Park PJ, Shukla D. Role of heparan sulfate in ocular diseases. Exp Eye Res 2013; 110: 1-9
2 Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest 2001; 108 (02) 169-173
3 Tiwari V, Maus E, Sigar IM, Ramsey KH, Shukla D. Role of heparan sulfate in sexually transmitted infections. Glycobiology 2012; 22 (11) 1402-1412
4 Tiwari V, Tarbutton MS, Shukla D. Diversity of heparan sulfate and HSV entry: basic understanding and treatment strategies. Molecules 2015; 20 (02) 2707-2727
5 Berninsone PM, Hirschberg CB. Nucleotide sugar transporters of the Golgi apparatus. Curr Opin Struct Biol 2000; 10 (05) 542-547
6 Hirschberg CB, Robbins PW, Abeijon C. Transporters of nucleotide sugars, ATP, and nucleotide sulfate in the endoplasmic reticulum and Golgi apparatus. Annu Rev Biochem 1998; 67: 49-69
7 Joice A, Raman K, Mencio C. et al. Enzymatic synthesis of heparan sulfate and heparin. Methods Mol Biol 2015; 1229: 11-19
8 Dulaney SB, Xu Y, Wang P. et al. Divergent synthesis of heparan sulfate oligosaccharides. J Org Chem 2015; 80 (24) 12265-12279
9 Liu J, Linhardt RJ. Chemoenzymatic synthesis of heparan sulfate and heparin. Nat Prod Rep 2014; 31 (12) 1676-1685
10 Sugahara K, Kitagawa H. Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr Opin Struct Biol 2000; 10 (05) 518-527
11 O'Donnell CD, Shukla D. The importance of heparan sulfate in herpesvirus infection. Virol Sin 2008; 23 (06) 383-393
12 Shworak NW, Liu J, Petros LM. et al. Multiple isoforms of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. Isolation, characterization, and expression of human cdnas and identification of distinct genomic loci. J Biol Chem 1999; 274 (08) 5170-5184
13 O'Donnell CD, Tiwari V, Oh MJ, Shukla D. A role for heparan sulfate 3-O-sulfotransferase isoform 2 in herpes simplex virus type 1 entry and spread. Virology 2006; 346 (02) 452-459
14 Xia G, Chen J, Tiwari V. et al. Heparan sulfate 3-O-sulfotransferase isoform 5 generates both an antithrombin-binding site and an entry receptor for herpes simplex virus, type 1. J Biol Chem 2002; 277 (40) 37912-37919
15 Xu D, Tiwari V, Xia G, Clement C, Shukla D, Liu J. Characterization of heparan sulphate 3-O-sulphotransferase isoform 6 and its role in assisting the entry of herpes simplex virus type 1. Biochem J 2005; 385 (Pt 2): 451-459
16 Yabe T, Shukla D, Spear PG, Rosenberg RD, Seeberger PH, Shworak NW. Portable sulphotransferase domain determines sequence specificity of heparan sulphate 3-O-sulphotransferases. Biochem J 2001; 359 (Pt 1): 235-241
17 Shukla D, Liu J, Blaiklock P. et al. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 1999; 99 (01) 13-22
18 Tumova S, Woods A, Couchman JR. Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int J Biochem Cell Biol 2000; 32 (03) 269-288
19 Bernfield M, Götte M, Park PW. et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999; 68: 729-777
20 Iozzo RV, Sanderson RD. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J Cell Mol Med 2011; 15 (05) 1013-1031
21 Bernfield M, Kokenyesi R, Kato M. et al. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 1992; 8: 365-393
22 Manon-Jensen T, Multhaupt HAB, Couchman JR. Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains. FEBS J 2013; 280 (10) 2320-2331
23 Nissinen L, Kähäri VM. Matrix metalloproteinases in inflammation. Biochim Biophys Acta 2014; 1840 (08) 2571-2580
24 Chen Q, Jin M, Yang F, Zhu J, Xiao Q, Zhang L. Matrix metalloproteinases: inflammatory regulators of cell behaviors in vascular formation and remodeling. Mediators Inflamm 2013; 2013 (03) 928315
25 Derksen PWB, Keehnen RMJ, Evers LM, van Oers MHJ, Spaargaren M, Pals ST. Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 2002; 99 (04) 1405-1410
26 Rapraeger AC. Synstatin: a selective inhibitor of the syndecan-1-coupled IGF1R-αvβ3 integrin complex in tumorigenesis and angiogenesis. FEBS J 2013; 280 (10) 2207-2215
27 Filmus J, Capurro M, Rast J. Glypicans. Genome Biol 2008; 9 (05) 224
28 Filmus J. Glypicans in growth control and cancer. Glycobiology 2001; 11 (03) 19R-23R
29 Capurro MI, Xu P, Shi W, Li F, Jia A, Filmus J. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev Cell 2008; 14 (05) 700-711
30 Song HH, Shi W, Xiang YY, Filmus J. The loss of glypican-3 induces alterations in Wnt signaling. J Biol Chem 2005; 280 (03) 2116-2125
31 Kjellén L, Lindahl U. Proteoglycans: structures and interactions. Annu Rev Biochem 1991; 60: 443-475
32 Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 2011; 3 (07) a004952
33 Iozzo RV. Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 1998; 67: 609-652
34 Halfter W, Dong S, Schurer B, Cole GJ. Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 1998; 273 (39) 25404-25412
35 Marneros AG, Olsen BR. The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol 2001; 20 (5–6): 337-345
36 Bix G, Iozzo RV. Novel interactions of perlecan: unraveling perlecan's role in angiogenesis. Microsc Res Tech 2008; 71 (05) 339-348
37 Molist A, Romarís M, Lindahl U, Villena J, Touab M, Bassols A. Changes in glycosaminoglycan structure and composition of the main heparan sulphate proteoglycan from human colon carcinoma cells (perlecan) during cell differentiation. Eur J Biochem 1998; 254 (02) 371-377
38 Jayson GC, Lyon M, Paraskeva C, Turnbull JE, Deakin JA, Gallagher JT. Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J Biol Chem 1998; 273 (01) 51-57
39 Feyzi E, Saldeen T, Larsson E, Lindahl U, Salmivirta M. Age-dependent modulation of heparan sulfate structure and function. J Biol Chem 1998; 273 (22) 13395-13398
40 Brickman YG, Ford MD, Gallagher JT, Nurcombe V, Bartlett PF, Turnbull JE. Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J Biol Chem 1998; 273 (08) 4350-4359
41 Whitley RJ. Herpesviruses. In: Baron S. ed. Medical Microbiology. 4th ed.. Galveston, TX: University of Texas Medical Branch at Galveston; 1996
42 Koganti R, Yadavalli T, Shukla D. Current and emerging therapies for ocular herpes simplex virus type-1 infections. Microorganisms 2019; 7 (10) 7
43 Salameh S, Sheth U, Shukla D. Early events in herpes simplex virus lifecycle with implications for an infection of lifetime. Open Virol J 2012; 6: 1-6
44 Koujah L, Suryawanshi RK, Shukla D. Pathological processes activated by herpes simplex virus-1 (HSV-1) infection in the cornea. Cell Mol Life Sci 2019; 76 (03) 405-419
45 Akhtar J, Shukla D. Viral entry mechanisms: cellular and viral mediators of herpes simplex virus entry. FEBS J 2009; 276 (24) 7228-7236
46 Karasneh GA, Shukla D. Herpes simplex virus infects most cell types in vitro: clues to its success. Virol J 2011; 8: 481
47 Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 1996; 87 (03) 427-436
48 Heldwein EE, Krummenacher C. Entry of herpesviruses into mammalian cells. Cell Mol Life Sci 2008; 65 (11) 1653-1668
49 Spear PG. Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol 2004; 6 (05) 401-410
50 Farooq AV, Valyi-Nagy T, Shukla D. Mediators and mechanisms of herpes simplex virus entry into ocular cells. Curr Eye Res 2010; 35 (06) 445-450
51 WuDunn D, Spear PG. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol 1989; 63 (01) 52-58
52 Trybala E, Liljeqvist JA, Svennerholm B, Bergström T. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J Virol 2000; 74 (19) 9106-9114
53 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 infectivity. J Virol 1991; 65 (03) 1090-1098
54 Oh M-J, Akhtar J, Desai P, Shukla D. A role for heparan sulfate in viral surfing. Biochem Biophys Res Commun 2010; 391 (01) 176-181
55 Clement C, Tiwari V, Scanlan PM, Valyi-Nagy T, Yue BYJT, Shukla D. A novel role for phagocytosis-like uptake in herpes simplex virus entry. J Cell Biol 2006; 174 (07) 1009-1021
56 Ladwein M, Rottner K. On the Rho'd: the regulation of membrane protrusions by Rho-GTPases. FEBS Lett 2008; 582 (14) 2066-2074
57 Akhtar J, Tiwari V, Oh M-J. et al. HVEM and nectin-1 are the major mediators of herpes simplex virus 1 (HSV-1) entry into human conjunctival epithelium. Invest Ophthalmol Vis Sci 2008; 49 (09) 4026-4035
58 Avitabile E, Forghieri C, Campadelli-Fiume G. Complexes between herpes simplex virus glycoproteins gD, gB, and gH detected in cells by complementation of split enhanced green fluorescent protein. J Virol 2007; 81 (20) 11532-11537
59 Carfí A, Willis SH, Whitbeck JC. et al. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell 2001; 8 (01) 169-179
60 Nicola AV, McEvoy AM, Straus SE. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol 2003; 77 (09) 5324-5332
61 Tiwari V, Clement C, Duncan MB, Chen J, Liu J, Shukla D. A role for 3-O-sulfated heparan sulfate in cell fusion induced by herpes simplex virus type 1. J Gen Virol 2004; 85 (Pt 4): 805-809
62 David AT, Baghian A, Foster TP, Chouljenko VN, Kousoulas KG. The herpes simplex virus type 1 (HSV-1) glycoprotein K(gK) is essential for viral corneal spread and neuroinvasiveness. Curr Eye Res 2008; 33 (05) 455-467
63 O'Donnell CD, Shukla D. A novel function of heparan sulfate in the regulation of cell-cell fusion. J Biol Chem 2009; 284 (43) 29654-29665
64 Bacsa S, Karasneh G, Dosa S, Liu J, Valyi-Nagy T, Shukla D. Syndecan-1 and syndecan-2 play key roles in herpes simplex virus type-1 infection. J Gen Virol 2011; 92 (Pt 4): 733-743
65 Nahmias AJ, Kibrick S. Inhibitory effect of heparin on herpes simplex virus. J Bacteriol 1964; 87 (05) 1060-1066
66 Tiwari V, Liu J, Valyi-Nagy T, Shukla D. Anti-heparan sulfate peptides that block herpes simplex virus infection in vivo. J Biol Chem 2011; 286 (28) 25406-25415
67 Hadigal SR, Agelidis AM, Karasneh GA. et al. Heparanase is a host enzyme required for herpes simplex virus-1 release from cells. Nat Commun 2015; 6: 6985
68 Thakkar N, Yadavalli T, Jaishankar D, Shukla D. Emerging roles of heparanase in viral pathogenesis. Pathogens 2017; 6 (03) 6
69 Sanderson RD, Elkin M, Rapraeger AC, Ilan N, Vlodavsky I. Heparanase regulation of cancer, autophagy and inflammation: new mechanisms and targets for therapy. FEBS J 2017; 284 (01) 42-55
70 Vlodavsky I, Singh P, Boyango I. et al. Heparanase: from basic research to therapeutic applications in cancer and inflammation. Drug Resist Updat 2016; 29: 54-75
71 Fux L, Ilan N, Sanderson RD, Vlodavsky I. Heparanase: busy at the cell surface. Trends Biochem Sci 2009; 34 (10) 511-519
72 Agelidis AM, Hadigal SR, Jaishankar D, Shukla D. Viral activation of heparanase drives pathogenesis of herpes simplex virus-1. Cell Rep 2017; 20 (02) 439-450
73 Thakkar N, Jaishankar D, Agelidis A. et al. Cultured corneas show dendritic spread and restrict herpes simplex virus infection that is not observed with cultured corneal cells. Sci Rep 2017; 7: 42559
74 Goldberg R, Meirovitz A, Hirshoren N. et al. Versatile role of heparanase in inflammation. Matrix Biol 2013; 32 (05) 234-240
75 Goldshmidt O, Zcharia E, Cohen M. et al. Heparanase mediates cell adhesion independent of its enzymatic activity. FASEB J 2003; 17 (09) 1015-1025
76 Rabelink TJ, van den Berg BM, Garsen M, Wang G, Elkin M, van der Vlag J. Heparanase: roles in cell survival, extracellular matrix remodelling and the development of kidney disease. Nat Rev Nephrol 2017; 13 (04) 201-212
77 Jin H, Zhou S. The functions of heparanase in human diseases. Mini Rev Med Chem 2017; 17 (06) 541-548
78 Hadigal S, Koganti R, Yadavalli T, Agelidis A, Suryawanshi R, Shukla D. Heparanase-regulated syndecan-1 shedding facilitates herpes simplex virus 1 egress. J Virol 2020; 94 (06) 94
79 Corey L, Holmes KK. Genital herpes simplex virus infections: current concepts in diagnosis, therapy, and prevention. Ann Intern Med 1983; 98 (06) 973-983
80 Jaishankar D, Shukla D. Genital herpes: insights into sexually transmitted infectious disease. Microb Cell 2016; 3 (09) 438-450
81 Cheshenko N, Herold BC. Glycoprotein B plays a predominant role in mediating herpes simplex virus type 2 attachment and is required for entry and cell-to-cell spread. J Gen Virol 2002; 83 (Pt 9): 2247-2255
82 Gerber SI, Belval BJ, Herold BC. Differences in the role of glycoprotein C of HSV-1 and HSV-2 in viral binding may contribute to serotype differences in cell tropism. Virology 1995; 214 (01) 29-39
83 Oyan AM, Dolter KE, Langeland N. et al. Resistance of herpes simplex virus type 2 to neomycin maps to the N-terminal portion of glycoprotein C. J Virol 1993; 67 (05) 2434-2441
84 Hutton RD, Ewert DL, French GR. Differentiation of types 1 and 2 herpes simplex virus by plaque inhibition with sulfated polyanions. Proc Soc Exp Biol Med 1973; 142 (01) 27-29
85 Langeland N, Holmsen H, Lillehaug JR, Haarr L. Evidence that neomycin inhibits binding of herpes simplex virus type 1 to the cellular receptor. J Virol 1987; 61 (11) 3388-3393
86 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 (06) 3461-3469
87 Hopkins J, Yadavalli T, Agelidis AM, Shukla D. Host enzymes heparanase and cathepsin L promote herpes simplex virus 2 release from cells. J Virol 2018; 92 (23) 92
88 Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010; 20 (04) 202-213
89 Gerna G, Baldanti F, Revello MG. Pathogenesis of human cytomegalovirus infection and cellular targets. Hum Immunol 2004; 65 (05) 381-386
90 Compton T, Nowlin DM, Cooper NR. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 1993; 193 (02) 834-841
91 Feire AL, Roy RM, Manley K, Compton T. The glycoprotein B disintegrin-like domain binds beta 1 integrin to mediate cytomegalovirus entry. J Virol 2010; 84 (19) 10026-10037
92 Dogra P, Martin EB, Williams A. et al. Novel heparan sulfate-binding peptides for blocking herpesvirus entry. PLoS One 2015; 10 (05) e0126239
93 Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 1995; 332 (18) 1186-1191
94 Veettil MV, Bandyopadhyay C, Dutta D, Chandran B. Interaction of KSHV with host cell surface receptors and cell entry. Viruses 2014; 6 (10) 4024-4046
95 Schäfer G, Blumenthal MJ, Katz AA. Interaction of human tumor viruses with host cell surface receptors and cell entry. Viruses 2015; 7 (05) 2592-2617
96 Wang FZ, Akula SM, Sharma-Walia N, Zeng L, Chandran B. Human herpesvirus 8 envelope glycoprotein B mediates cell adhesion via its RGD sequence. J Virol 2003; 77 (05) 3131-3147
97 Veettil MV, Sadagopan S, Sharma-Walia N. et al. Kaposi's sarcoma-associated herpesvirus forms a multimolecular complex of integrins (alphaVbeta5, alphaVbeta3, and alpha3beta1) and CD98-xCT during infection of human dermal microvascular endothelial cells, and CD98-xCT is essential for the postentry stage of infection. J Virol 2008; 82 (24) 12126-12144
98 Hensler HR, Tomaszewski MJ, Rappocciolo G, Rinaldo CR, Jenkins FJ. Human herpesvirus 8 glycoprotein B binds the entry receptor DC-SIGN. Virus Res 2014; 190: 97-103
99 Chakraborty S, Veettil MV, Bottero V, Chandran B. Kaposi's sarcoma-associated herpesvirus interacts with EphrinA2 receptor to amplify signaling essential for productive infection. Proc Natl Acad Sci U S A 2012; 109 (19) E1163-E1172
100 Akula SM, Wang FZ, Vieira J, Chandran B. Human herpesvirus 8 interaction with target cells involves heparan sulfate. Virology 2001; 282 (02) 245-255
101 Akula SM, Pramod NP, Wang FZ, Chandran B. Human herpesvirus 8 envelope-associated glycoprotein B interacts with heparan sulfate-like moieties. Virology 2001; 284 (02) 235-249
102 Jarousse N, Chandran B, Coscoy L. Lack of heparan sulfate expression in B-cell lines: implications for Kaposi's sarcoma-associated herpesvirus and murine gammaherpesvirus 68 infections. J Virol 2008; 82 (24) 12591-12597
103 Garrigues HJ, DeMaster LK, Rubinchikova YE, Rose TM. KSHV attachment and entry are dependent on αVβ3 integrin localized to specific cell surface microdomains and do not correlate with the presence of heparan sulfate. Virology 2014; 464–465: 118-133
104 Secchiero P, Sun D, De Vico AL. 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 (06) 4571-4580
105 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 (08) 3546-3550
106 Laing KJ, Ouwendijk WJD, Koelle DM, Verjans GMGM. Immunobiology of varicella-zoster virus infection. J Infect Dis 2018; 218 (suppl_2): S68-S74
107 Jacquet A, Haumont M, Chellun D. et al. The varicella zoster virus glycoprotein B (gB) plays a role in virus binding to cell surface heparan sulfate proteoglycans. Virus Res 1998; 53 (02) 197-207
108 Secchiero P, Berneman ZN, Sun D, Nicholas J, Reitz Jr MS. Identification of envelope glycoproteins H and B homologues of human herpesvirus 7. Intervirology 1997; 40 (01) 22-32
109 Barré-Sinoussi F, Chermann JC, Rey F. et al. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 1983; 220 (4599): 868-871
110 Wu Z, Chen Z, Phillips DM. Human genital epithelial cells capture cell-free human immunodeficiency virus type 1 and transmit the virus to CD4+ Cells: implications for mechanisms of sexual transmission. J Infect Dis 2003; 188 (10) 1473-1482
111 Saïdi H, Magri G, Nasreddine N, Réquena M, Bélec L. R5- and X4-HIV-1 use differentially the endometrial epithelial cells HEC-1A to ensure their own spread: implication for mechanisms of sexual transmission. Virology 2007; 358 (01) 55-68
112 Bobardt MD, Chatterji U, Selvarajah S. et al. Cell-free human immunodeficiency virus type 1 transcytosis through primary genital epithelial cells. J Virol 2007; 81 (01) 395-405
113 Connell BJ, Lortat-Jacob H. Human immunodeficiency virus and heparan sulfate: from attachment to entry inhibition. Front Immunol 2013; 4: 385
114 Nazli A, Kafka JK, Ferreira VH. et al. HIV-1 gp120 induces TLR2- and TLR4-mediated innate immune activation in human female genital epithelium. J Immunol 2013; 191 (08) 4246-4258
115 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 (04) 2233-2239
116 Rider CC, Coombe DR, Harrop HA. et al. Anti-HIV-1 activity of chemically modified heparins: correlation between binding to the V3 loop of gp120 and inhibition of cellular HIV-1 infection in vitro. Biochemistry 1994; 33 (22) 6974-6980
117 Crublet E, Andrieu JP, Vivès RR, Lortat-Jacob H. The HIV-1 envelope glycoprotein gp120 features four heparan sulfate binding domains, including the co-receptor binding site. J Biol Chem 2008; 283 (22) 15193-15200
118 Cannon PM, Matthews S, Clark N. et al. Structure-function studies of the human immunodeficiency virus type 1 matrix protein, p17. J Virol 1997; 71 (05) 3474-3483
119 Bugatti A, Giagulli C, Urbinati C. et al. Molecular interaction studies of HIV-1 matrix protein p17 and heparin: identification of the heparin-binding motif of p17 as a target for the development of multitarget antagonists. J Biol Chem 2013; 288 (02) 1150-1161
120 Bugatti A, Paiardi G, Urbinati C. et al. Heparin and heparan sulfate proteoglycans promote HIV-1 p17 matrix protein oligomerization: computational, biochemical and biological implications. Sci Rep 2019; 9 (01) 15768
121 de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology 2004; 324 (01) 17-27
122 Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 2009; 5 (02) e1000318
123 Schiller JT, Day PM, Kines RC. Current understanding of the mechanism of HPV infection. Gynecol Oncol 2010; 118 (1, Suppl): S12-S17
124 Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc Natl Acad Sci U S A 2009; 106 (48) 20458-20463
125 Selinka HC, Florin L, Patel HD. et al. Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus. J Virol 2007; 81 (20) 10970-10980
126 Culp TD, Budgeon LR, Marinkovich MP, Meneguzzi G, Christensen ND. Keratinocyte-secreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells. J Virol 2006; 80 (18) 8940-8950
127 Richards KF, Bienkowska-Haba M, Dasgupta J, Chen XS, Sapp M. Multiple heparan sulfate binding site engagements are required for the infectious entry of human papillomavirus type 16. J Virol 2013; 87 (21) 11426-11437
128 Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, Day PM. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J Virol 2009; 83 (05) 2067-2074
129 Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 2002; 10 (02) 100-103
130 Avirutnan P, Zhang L, Punyadee N. et al. Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog 2007; 3 (11) e183
131 Puerta-Guardo H, Glasner DR, Harris E. Dengue virus NS1 disrupts the endothelial glycocalyx, leading to hyperpermeability. PLoS Pathog 2016; 12 (07) e1005738
132 Choi Y, Chung H, Jung H, Couchman JR, Oh ES. Syndecans as cell surface receptors: unique structure equates with functional diversity. Matrix Biol 2011; 30 (02) 93-99
133 Abboud-Jarrous G, Atzmon R, Peretz T. et al. Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. J Biol Chem 2008; 283 (26) 18167-18176
134 El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 2012; 142 (06) 1264.e1-1273.e1
135 Jiang J, Cun W, Wu X, Shi Q, Tang H, Luo G. Hepatitis C virus attachment mediated by apolipoprotein E binding to cell surface heparan sulfate. J Virol 2012; 86 (13) 7256-7267
136 Barth H, Schafer C, Adah MI. et al. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 2003; 278 (42) 41003-41012
137 Xu Y, Martinez P, Séron K. et al. Characterization of hepatitis C virus interaction with heparan sulfate proteoglycans. J Virol 2015; 89 (07) 3846-3858
138 Zhang F, Sodroski C, Cha H, Li Q, Liang TJ. Infection of hepatocytes with HCV increases cell surface levels of heparan sulfate proteoglycans, uptake of cholesterol and lipoprotein, and virus entry by Up-regulating SMAD6 and SMAD7. Gastroenterology 2017; 152 (01) 257.e7-270.e7
139 Holberg CJ, Wright AL, Martinez FD, Ray CG, Taussig LM, Lebowitz MD. Risk factors for respiratory syncytial virus-associated lower respiratory illnesses in the first year of life. Am J Epidemiol 1991; 133 (11) 1135-1151
140 Levine S, Klaiber-Franco R, Paradiso PR. Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol 1987; 68 (Pt 9): 2521-2524
141 Richman AV, Pedreira FA, Tauraso NM. Attempts to demonstrate hemagglutination and hemadsorption by respiratory syncytial virus. Appl Microbiol 1971; 21 (06) 1099-1100
142 Hosoya M, Balzarini J, Shigeta S, De Clercq E. Differential inhibitory effects of sulfated polysaccharides and polymers on the replication of various myxoviruses and retroviruses, depending on the composition of the target amino acid sequences of the viral envelope glycoproteins. Antimicrob Agents Chemother 1991; 35 (12) 2515-2520
143 Walsh EE, Hruska J. Monoclonal antibodies to respiratory syncytial virus proteins: identification of the fusion protein. J Virol 1983; 47 (01) 171-177
144 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 (14) 6442-6447
145 CDC. . 2014–2016 Ebola outbreak in West Africa, History, Ebola (Ebola Virus Disease). Accessed November 3, 2020 at: https://www.cdc.gov/vhf/ebola/history/2014-2016-outbreak/index.html
146 O'Hearn A, Wang M, Cheng H. et al. Role of EXT1 and Glycosaminoglycans in the early stage of filovirus entry. J Virol 2015; 89 (10) 5441-5449
147 McCormick C, Leduc Y, Martindale D. et al. The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat Genet 1998; 19 (02) 158-161
148 Tamhankar M, Gerhardt DM, Bennett RS, Murphy N, Jahrling PB, Patterson JL. Heparan sulfate is an important mediator of Ebola virus infection in polarized epithelial cells. Virol J 2018; 15 (01) 135
149 Fehr AR, Perlman S. Coronaviruses: an overview of their replication and pathogenesis. Methods Mol Biol 2015; 1282: 1-23
150 Wassenaar TM, Zou Y. 2019_nCoV/SARS-CoV-2: rapid classification of betacoronaviruses and identification of traditional Chinese medicine as potential origin of zoonotic coronaviruses. Lett Appl Microbiol 2020; 70 (05) 342-348
151 Milewska A, Zarebski M, Nowak P, Stozek K, Potempa J, Pyrc K. Human coronavirus NL63 utilizes heparan sulfate proteoglycans for attachment to target cells. J Virol 2014; 88 (22) 13221-13230
152 Lang J, Yang N, Deng J. et al. Inhibition of SARS pseudovirus cell entry by lactoferrin binding to heparan sulfate proteoglycans. PLoS One 2011; 6 (08) e23710
153 Lu R, Zhao X, Li J. et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet 2020; 395 (10224): 565-574
154 Liu L, Chopra P, Li X, Wolfert M, Tompkins M, Boons G. SARS-CoV-2 spike protein binds heparan sulfate in ca length- and sequence-dependent manner. bioRxiv 2020. Doi: 10.1101/2020.05.10.087288