Role of heparan sulfate in ocular diseases

Experimental Eye Research

Volumn 110, Issue , 2013, Pages 1-9

  Park, Paul J ^a   Shukla, Deepak ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Age related macular degeneration; Bacterial keratitis; Choroidal neovascularization; Heparan sulfate; Herpetic keratitis; Proteoglycans

Indexed keywords

AGRIN; COLLAGEN TYPE 18; COMPLEMENT FACTOR H; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; GLYCOPROTEIN B; GLYCOPROTEIN D; HEPARAN SULFATE; PERLECAN; PROTEIN C; SULFOTRANSFERASE; SYNDECAN 1; SYNDECAN 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

BACTERIAL KERATITIS; CELL ADHESION; CELL GROWTH; CELL SURFACE; CHEMICAL MODIFICATION; COMPLEMENT ACTIVATION; CORNEA NEOVASCULARIZATION; EXTRACELLULAR MATRIX; EYE DISEASE; HUMAN; KERATITIS; MOLECULARLY TARGETED THERAPY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SUBRETINAL NEOVASCULARIZATION; SULFATION; VISUAL ACUITY; VISUAL IMPAIRMENT;

ANIMALS; CORNEAL NEOVASCULARIZATION; CORNEAL ULCER; EYE DISEASES; HEPARITIN SULFATE; HUMANS; KERATITIS, HERPETIC; MACULAR DEGENERATION;

EID: 84875360648     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.01.015     Document Type: Review

References (107)

1. Ali M.M., Karasneh G.A., Jarding M.J., Tiwari V., Shukla D. A 3-O-sulfated heparan sulfate binding peptide preferentially targets herpes simplex virus 2-infected cells. J. Virol. 2012, 86:6434-6443.
2. Anderson D.H., Radeke M.J., Gallo N.B., Chapin E.A., Johnson P.T., Curletti C.R., Hancox L.S., Hu J., Ebright J.N., Malek G., Hauser M.A., Rickman C.B., Bok D., Hageman G.S., Johnson L.V. The pivotal role of the complement system in aging and age-related macular degeneration: hypothesis re-visited. Prog. Retin. Eye Res. 2010, 29:95-112.
3. Aquino R.S., Lee E.S., Park P.W. Diverse functions of glycosaminoglycans in infectious diseases. Prog. Mol. Biol. Transl. Sci. 2010, 93:373-394.
4. 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, 92:733-743.
5. Baird A., Florkiewicz R.Z., Maher P.A., Kaner R.J., Hajjar D.P. Mediation of virion penetration into vascular cells by association of basic fibroblast growth factor with herpes simplex virus type 1. Nature 1990, 348:344-346.
6. Bartlett A.H., Hayashida K., Park P.W. Molecular and cellular mechanisms of syndecans in tissue injury and inflammation. Mol. Cells 2007, 24:153-166.
7. Bartlett A.H., Park P.W. Proteoglycans in host-pathogen interactions: molecular mechanisms and therapeutic implications. Expert Rev. Mol. Med. 2010, 12:e5.
8. Bernfield M., Götte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
9. Bourcier T., Thomas F., Borderie V., Chaumeil C., Laroche L. Bacterial keratitis: predisposing factors, clinical and microbiological review of 300 cases. Br. J. Ophthalmol. 2003, 87:834-838.
10. Brickman Y.G., Ford M.D., Gallagher J.T., Nurcombe V., Bartlett P.F., Turnbull J.E. Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 1998, 273:4350-4359.
11. Call T.W., Hollyfield J.G. Sulfated proteoglycans in Bruch's membrane of the human eye: localization and characterization using cupromeronic blue. Exp. Eye Res. 1990, 51:451-462.
12. Campochiaro P.A. Retinal and choroidal neovascularization. J. Cell. Physiol. 2000, 184:301-310.
13. Castellot J.J.J., Hoover R.L., Harper P.A., Karnovsky M.J. Heparin and glomerular epithelial cell-secreted heparin-like species inhibit mesangial-cell proliferation. Am. J. Pathol. 1985, 120:427-435.
14. Chen Y., Götte M., Liu J., Park P.W. Microbial subversion of heparan sulfate proteoglycans. Mol. Cells 2008, 26:415-426.
15. Chen Y., Maguire T., Hileman R.E., Fromm J.R., Esko J.D., Linhardt R.J., Marks R.M. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 1997, 3:866-871.
16. Clark S.J., Bishop P.N., Day A.J. Complement factor H and age-related macular degeneration: the role of glycosaminoglycan recognition in disease pathology. Biochem. Soc. Trans. 2010, 38:1342-1348.
17. Clark S.J., Higman V.A., Mulloy B., Perkins S.J., Lea S.M., Sim R.B., Day A.J. His-384 allotypic variant of factor H associated with age-related macular degeneration has different heparin binding properties from the non-disease-associated form. J. Biol. Chem. 2006, 281:24713-24720.
18. Clark S.J., Keenan T.D., Fielder H.L., Collinson L.J., Holley R.J., Merry C.L., van Kuppevelt T.H., Day A.J., Bishop P.N. Mapping the differential distribution of glycosaminoglycans in the adult human retina, choroid, and sclera. Invest. Ophthalmol. Vis. Sci. 2011, 52:6511-6521.
19. Clark S.J., Perveen R., Hakobyan S., Morgan B.P., Sim R.B., Bishop P.N., Day A.J. Impaired binding of the age-related macular degeneration-associated complement factor H 402H allotype to Bruch's membrane in human retina. J. Biol. Chem. 2010, 285:30192-30202.
20. Coleman H.R., Chan C.C., Ferris F.L., Chew E.Y. Age-related macular degeneration. Lancet 2008, 372:1835-1845.
21. Congdon N., O'Colmain B., Klaver C.C., Klein R., Muñoz B., Friedman D.S., Kempen J., Taylor H.R., Mitchell P., Eye Diseases Prevalence Research Group Causes and prevalence of visual impairment among adults in the United States. Arch. Ophthalmol. 2004, 122:477-485.
22. Crews J.E. The role of public health in addressing aging and sensory loss. Generations 2003, 27:83-90.
23. Despriet D.D., Klaver C.C., Witteman J.C., Bergen A.A., Kardys I., de Maat M.P., Boekhoorn S.S., Vingerling J.R., Hofman A., Oostra B.A., Uitterlinden A.G., Stijnen T., van Duijn C.M., de Jong P.T. Complement factor H polymorphism, complement activators, and risk of age-related macular degeneration. JAMA 2006, 296:301-309.
24. Dreyfuss J.L., Regatieri C.V., Jarrouge T.R., Cavalheiro R.P., Sampaio L.O., Nader H.B. Heparan sulfate proteoglycans: structure, protein interactions and cell signaling. An. Acad. Bras. Cienc 2009, 81:409-429.
25. Dreyfuss J.L., Regatieri C.V., Lima M.A., Paredes-Gamero E.J., Brito A.S., Chavante S.F., Belfort R., Farah M.E., Nader H.B. A heparin mimetic isolated from a marine shrimp suppresses neovascularization. J. Thromb. Haemost 2010, 8:1828-1837.
26. Dreyfuss J.L., Veiga S.S., Coulson-Thomas V.J., Santos I.A., Toma L., Coletta R.D., Nader H.B. Differences in the expression of glycosaminoglycans in human fibroblasts derived from gingival overgrowths is related to TGF-beta up-regulation. Growth Factor. 2010, 28:24-33.
27. Edwards A.O., Ritter R., Abel K.J., Manning A., Panhuysen C., Farrer L.A. Complement factor H polymorphism and age-related macular degeneration. Science 2005, 308:421-424.
28. Esko J.D., Lindahl U. Molecular diversity of heparan sulfate. J. Clin. Invest. 2001, 108:169-173.
29. Esko J.D., Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 2002, 71:435-471.
30. Feyzi E., Saldeen T., Larsson E., Lindahl U., Salmivirta M. Age-dependent modulation of heparan sulfate structure and function. J. Biol. Chem. 1998, 273:13395-13398.
31. Gass J.D. Drusen and disciform macular detachment and degeneration. Arch. Ophthalmol. 1973, 90:206-217.
32. Goureau O., Faure V., Courtois Y. Fibroblast growth factors decrease inducible nitric oxide synthase mRNA accumulation in bovine retinal pigmented epithelial cells. Eur. J. Biochem. 1995, 230:1046-1052.
33. Green M., Apel A., Stapleton F. Risk factors and causative organisms in microbial keratitis. Cornea 2008, 27:22-27.
34. Hageman G.S., Anderson D.H., Johnson L.V., Hancox L.S., Taiber A.J., Hardisty L.I., Hageman J.L., Stockman H.A., Borchardt J.D., Gehrs K.M., Smith R.J., Silvestri G., Russell S.R., Klaver C.C., Barbazetto I., Chang S., Yannuzzi L.A., Barile G.R., Merriam J.C., Smith R.T., Olsh A.K., Bergeron J., Zernant J., Merriam J.E., Gold B., Dean M., Allikmets R. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7227-7232.
35. Hageman G.S., Luthert P.J., Victor Chong N.H., Johnson L.V., Anderson D.H., Mullins R.F. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog. Retin. Eye Res. 2001, 20:705-732.
36. Haines J.L., Hauser M.A., Schmidt S., Scott W.K., Olson L.M., Gallins P., Spencer K.L., Kwan S.Y., Noureddine M., Gilbert J.R., Schnetz-Boutaud N., Agarwal A., Postel E.A., Pericak-Vance M.A. Complement factor H variant increases the risk of age-related macular degeneration. Science 2005, 308:419-421.
37. Hayashida A., Amano S., Park P.W. Syndecan-1 promotes Staphylococcus aureus corneal infection by counteracting neutrophil-mediated host defense. J. Biol. Chem. 2011, 286:3288-3297.
38. Hecker L.A., Edwards A.O., Ryu E., Tosakulwong N., Baratz K.H., Brown W.L., Charbel Issa P., Scholl H.P., Pollok-Kopp B., Schmid-Kubista K.E., Bailey K.R., Oppermann M. Genetic control of the alternative pathway of complement in humans and age-related macular degeneration. Hum. Mol. Genet. 2010, 19:209-215.
39. Hulett M.D., Freeman C., Hamdorf B.J., Baker R.T., Harris M.J., Parish C.R. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat. Med. 1999, 5:803-809.
40. Inomata T., Ebihara N., Funaki T., Matsuda A., Watanabe Y., Ning L., Xu Z., Murakami A., Arikawa-Hirasawa E. Perlecan-deficient mutation impairs corneal epithelial structure. Invest. Ophthalmol. Vis. Sci. 2012, 53:1277-1284.
41. Iozzo R.V. Heparan sulfate proteoglycans: intricate molecules with intriguing functions. J. Clin. Invest. 2001, 108:165-167.
42. Iozzo R.V., San Antonio J.D. Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J. Clin. Invest. 2001, 108:349-355.
43. Ivers R.Q., Norton R., Cumming R.G., Butler M., Campbell A.J. Visual impairment and risk of hip fracture. Am. J. Epidemiol. 2000, 152:633-639.
44. Jayson G.C., Lyon M., Paraskeva C., Turnbull J.E., Deakin J.A., Gallagher J.T. Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 1998, 273:51-57.
45. Jett B.D., Gilmore M.S. Host-parasite interactions in Staphylococcus aureus keratitis. DNA Cell. Biol. 2002, 21:397-404.
46. Jiang X., Couchman J.R. Perlecan and tumor angiogenesis. J. Histochem. Cytochem. 2003, 51:1393-1410.
47. Kaner R.J., Baird A., Mansukhani A., Basilico C., Summers B.D., Florkiewicz R.Z., Hajjar D.P. Fibroblast growth factor receptor is a portal of cellular entry for herpes simplex virus type 1. Science 1990, 248:1410-1413.
48. Kawaguchi H., Pilbeam C.C., Gronowicz G., Abreu C., Fletcher B.S., Herschman H.R., Raisz L.G., Hurley M.M. Transcriptional induction of prostaglandin G/H synthase-2 by basic fibroblast growth factor. J. Clin. Invest. 1995, 96:923-930.
49. Kelly U., Yu L., Kumar P., Ding J.D., Jiang H., Hageman G.S., Arshavsky V.Y., Frank M.M., Hauser M.A., Rickman C.B. Heparan sulfate, including that in Bruch's membrane, inhibits the complement alternative pathway: implications for age-related macular degeneration. J. Immunol. 2010, 185:5486-5494.
50. Kim B., Lee S., Kaistha S.D., Rouse B.T. Application of FGF-2 to modulate herpetic stromal keratitis. Curr. Eye Res. 2006, 31:1021-1028.
51. Klein R., Chou C.F., Klein B.E., Zhang X., Meuer S.M., Saaddine J.B. Prevalence of age-related macular degeneration in the US population. Arch. Ophthalmol. 2011, 129:75-80.
52. Klein R.J., Zeiss C., Chew E.Y., Tsai J.Y., Sackler R.S., Haynes C., Henning A.K., SanGiovanni J.P., Mane S.M., Mayne S.T., Bracken M.B., Ferris F.L., Ott J., Barnstable C., Hoh J. Complement factor H polymorphism in age-related macular degeneration. Science 2005, 308:385-389.
53. Liesegang T.J. Herpes simplex virus epidemiology and ocular importance. Cornea 2001, 20:1-13.
54. Limberg M.B. A review of bacterial keratitis and bacterial conjunctivitis. Am. J. Ophthalmol. 1991, 112:2S-9S.
55. Lindahl U., Kusche-Gullberg M., Kjellén L. Regulated diversity of heparan sulfate. J. Biol. Chem. 1998, 273:24979-24982.
56. Lindahl U., Lidholt K., Spillmann D., Kjellén L. More to " heparin" than anticoagulation. Thromb. Res. 1994, 75:1-32.
57. Loges S., Roncal C., Carmeliet P. Development of targeted angiogenic medicine. J. Thromb. Haemost 2009, 7:21-33.
58. Ly C.N., Pham J.N., Badenoch P.R., Bell S.M., Hawkins G., Rafferty D.L., McClellan K.A. Bacteria commonly isolated from keratitis specimens retain antibiotic susceptibility to fluoroquinolones and gentamicin plus cephalothin. Clin. Experiment. Ophthalmol. 2006, 34:44-50.
59. Marcum J.A., McKenney J.B., Galli S.J., Jackman R.W., Rosenberg R.D. Anticoagulantly active heparin-like molecules from mast cell-deficient mice. Am. J. Phys. 1986, 250:H879-H888.
60. Mataveli F.D., Han S.W., Nader H.B., Mendes A., Kanishiro R., Tucci P., Lopes A.C., Baptista-Silva J.C., Marolla A.P., de Carvalho L.P., Denapoli P.M., Pinhal M.A. Long-term effects for acute phase myocardial infarct VEGF165 gene transfer cardiac extracellular matrix remodeling. Growth Factor. 2009, 27:22-31.
61. Mirda D.P., Navarro D., Paz P., Lee P.L., Pereira L., Williams L.T. The fibroblast growth factor receptor is not required for herpes simplex virus type 1 infection. J. Virol. 1992, 66:448-457.
62. 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, 254:371-377.
63. Murphy P.R., Limoges M., Dodd F., Boudreau R.T., Too C.K. Fibroblast growth factor-2 stimulates endothelial nitric oxide synthase expression and inhibits apoptosis by a nitric oxide-dependent pathway in Nb2 lymphoma cells. Endocrinology 2001, 142:81-88.
64. Nadanaka S., Kitagawa H. Heparan sulphate biosynthesis and disease. J. Biochem. 2008, 144:7-14.
65. O'Donnell C.D., Kovacs M., Akhtar J., Valyi-Nagy T., Shukla D. Expanding the role of 3-O sulfated heparan sulfate in herpes simplex virus type-1 entry. Virology 2010, 397:389-398.
66. O'Donnell C.D., Tiwari V., Oh M.J., Shukla D. A role for heparan sulfate 3-O-sulfotransferase isoform 2 in herpes simplex virus type 1 entry and spread. Virology 2006, 346:452-459.
67. Oh M.J., Akhtar J., Desai P., Shukla D. A role for heparan sulfate in viral surfing. Biochem. Biophys. Res. Commun. 2010, 391:176-181.
68. Oppermann M., Manuelian T., Józsi M., Brandt E., Jokiranta T.S., Heinen S., Meri S., Skerka C., Götze O., Zipfel P.F. The C-terminus of complement regulator Factor H mediates target recognition: evidence for a compact conformation of the native protein. Clin. Exp. Immunol. 2006, 144:342-352.
69. Park P.W., Foster T.J., Nishi E., Duncan S.J., Klagsbrun M., Chen Y. Activation of syndecan-1 ectodomain shedding by Staphylococcus aureus alpha-toxin and beta-toxin. J. Biol. Chem. 2004, 279:251-258.
70. Perrimon N., Bernfield M. Specificities of heparan sulphate proteoglycans in developmental processes. Nature 2000, 404:725-728.
71. Rabenstein D.L. Heparin and heparan sulfate: structure and function. Nat. Prod. Rep. 2002, 19:312-331.
72. Rapraeger A., Jalkanen M., Endo E., Koda J., Bernfield M. The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J. Biol. Chem. 1985, 260:11046-11052.
73. Regatieri C.V., Dreyfuss J.L., Melo G.B., Lavinsky D., Farah M.E., Nader H.B. Dual role of intravitreous infliximab in experimental choroidal neovascularization: effect on the expression of sulfated glycosaminoglycans. Invest. Ophthalmol. Vis. Sci. 2009, 50:5487-5494.
74. Regatieri C.V., Dreyfuss J.L., Melo G.B., Lavinsky D., Hossaka S.K., Rodrigues E.B., Farah M.E., Maia M., Nader H.B. Quantitative evaluation of experimental choroidal neovascularization by confocal scanning laser ophthalmoscopy: fluorescein angiogram parallels heparan sulfate proteoglycan expression. Braz. J. Med. Biol. Res. 2010, 43:627-633.
75. Rein D.B., Wittenborn J.S., Zhang X., Honeycutt A.A., Lesesne S.B., Saaddine J., Vision Health Cost-Effectiveness Study Group Forecasting age-related macular degeneration through the year 2050: the potential impact of new treatments. Arch. Ophthalmol. 2009, 127:533-540.
76. Rein D.B., Zhang P., Wirth K.E., Lee P.P., Hoerger T.J., McCall N., Klein R., Tielsch J.M., Vijan S., Saaddine J. The economic burden of major adult visual disorders in the United States. Arch. Ophthalmol. 2006, 124:1754-1760.
77. Rodríguez de Córdoba S., Esparza-Gordillo J., Goicoechea de Jorge E., Lopez-Trascasa M., Sánchez-Corral P. The human complement factor H: functional roles, genetic variations and disease associations. Mol. Immunol. 2004, 41:355-367.
78. Saaddine J.B., Narayn K.M., Vinicor F. Vision loss: a public health problem?. Ophthalmology 2003, 110:253-254.
79. Safaiyan F., Lindahl U., Salmivirta M. Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells. Eur. J. Biochem. 1998, 252:576-582.
80. 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.
81. Sampaio L., Tersariol I., Lopes C., Boucas R., Nascimento F., Rocha H., Nader H. Heparins and heparans sulfates. Structure, distribution and protein interactions. Insights into Carbohydrate Structure and Biological Function 2006, 1-24. Transworld Research Network, Kerala. H. Verli (Ed.).
82. Sanderson R.D. Heparan sulfate proteoglycans in invasion and metastasis. Semin. Cell. Dev. Biol. 2001, 12:89-98.
83. Sasisekharan R., Ernst S., Venkataraman G. On the regulation of fibroblast growth factor activity by heparin-like glycosaminoglycans. Angiogenesis 1997, 1:45-54.
84. Schaefer F., Bruttin O., Zografos L., Guex-Crosier Y. Bacterial keratitis: a prospective clinical and microbiological study. Br. J. Ophthalmol. 2001, 85:842-847.
85. Shukla D., Liu J., Blaiklock P., Shworak N.W., Bai X., Esko J.D., Cohen G.H., Eisenberg R.J., Rosenberg R.D., Spear P.G. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 1999, 99:13-22.
86. Shworak N.W., Liu J., Petros L.M., Zhang L., Kobayashi M., Copeland N.G., Jenkins N.A., Rosenberg R.D. 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, 274:5170-5184.
87. Shworak N.W., Shirakawa M., Mulligan R.C., Rosenberg R.D. Characterization of ryudocan glycosaminoglycan acceptor sites. J. Biol. Chem. 1994, 269:21204-21214.
88. Soler R., Bruschini H., Martins J.R., Dreyfuss J.L., Camara N.O., Alves M.T., Leite K.R., Truzzi J.C., Nader H.B., Srougi M., Ortiz V. Urinary glycosaminoglycans as biomarker for urothelial injury: is it possible to discriminate damage from recovery?. Urology 2008, 72:937-942.
89. Su G., Blaine S.A., Qiao D., Friedl A. Shedding of syndecan-1 by stromal fibroblasts stimulates human breast cancer cell proliferation via FGF2 activation. J. Biol. Chem. 2007, 282:14906-14915.
90. Teeters V.W., Bird A.C. The development of neovascularization of senile disciform macular degeneration. Am. J. Ophthalmol. 1973, 76:1-18.
91. Tezel G., Edward D.P., Wax M.B. Serum autoantibodies to optic nerve head glycosaminoglycans in patients with glaucoma. Arch. Ophthalmol. 1999, 117:917-924.
92. Tiwari V., Clement C., Duncan M.B., 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, 85:805-809.
93. Tiwari V., Clement C., Xu D., Valyi-Nagy T., Yue B.Y., Liu J., Shukla D. Role for 3-O-sulfated heparan sulfate as the receptor for herpes simplex virus type 1 entry into primary human corneal fibroblasts. J. Virol. 2006, 80:8970-8980.
94. 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, 286:25406-25415.
95. Tiwari V., Maus E., Sigar I.M., Ramsey K.H., Shukla D. Role of heparan sulfate in sexually transmitted infections. Glycobiology 2012.
96. Tiwari V., O'Donnell C.D., Oh M.J., Valyi-Nagy T., Shukla D. A role for 3-O-sulfotransferase isoform-4 in assisting HSV-1 entry and spread. Biochem. Biophys. Res. Commun. 2005, 338:930-937.
97. Tkachenko E., Rhodes J.M., Simons M. Syndecans: new kids on the signaling block. Circ. Res. 2005, 96:488-500.
98. Turnbull J., Powell A., Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell. Biol. 2001, 11:75-82.
99. Vajpayee R.B., Dhakal B.P., Gupta S.K., Sachdev M.S., Satpathy G., Honavar S.G., Panda A. Evaluation of topical 0.03% flurbiprofen drops in the treatment of herpetic stromal keratitis. Aust. N. Z. J. Ophthalmol. 1996, 24:131-135.
100. Varki A., Freeze H.H. Glycans in acquired human diseases. Essentials of Glycobiology 2009, Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY). A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, M.E. Etzler (Eds.).
101. Vlodavsky I., Friedmann Y., Elkin M., Aingorn H., Atzmon R., Ishai-Michaeli R., Bitan M., Pappo O., Peretz T., Michal I., Spector L., Pecker I. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat. Med. 1999, 5:793-802.
102. Wadström T., Ljungh A. Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J. Med. Microbiol. 1999, 48:223-233.
103. Witmer A.N., van den Born J., Vrensen G.F., Schlingemann R.O. Vascular localization of heparan sulfate proteoglycans in retinas of patients with diabetes mellitus and in VEGF-induced retinopathy using domain-specifi{ligature}c antibodies. Curr. Eye Res. 2001, 22:190-197.
104. Xia G., Chen J., Tiwari V., Ju W., Li J.P., Malmstrom A., Shukla D., Liu J. 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, 277:37912-37919.
105. 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, 385:451-459.
106. Yabe T., Shukla D., Spear P., Rosenberg R.D., Seeberger P.H., Shworak N.W. Portable sulphotransferase domain determines sequence specificity of heparan sulphate 3-O-sulphotransferases. Biochem. J. 2001, 359:235-241.
107. Zhang H., Issekutz A.C. Growth factor regulation of neutrophil-endothelial cell interactions. J. Leukoc. Biol. 2001, 70:225-232.