Glycosaminoglycans, hyperglycemia, and disease

Antioxidants and Redox Signaling

Volumn 21, Issue 7, 2014, Pages 1032-1043

  Hiebert, Linda M ^a   Han, Juying ^b   Mandal, Anil Kumar ^c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b LERNER RESEARCH INSTITUTE   (United States)

^c Mandal Diabetes Research Foundation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSAMINOGLYCAN; GLYPICAN; HEPARAN SULFATE; HEPARANASE; PERLECAN; PROTEOHEPARAN SULFATE; REACTIVE OXYGEN METABOLITE; SYNDECAN;

CARDIOVASCULAR DISEASE; DIABETES MELLITUS; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; GLOMERULUS; HUMAN; HYPERGLYCEMIA; PRIORITY JOURNAL; REVIEW; ANIMAL; COMPLICATION; METABOLISM;

ANIMALS; DIABETES COMPLICATIONS; DIABETES MELLITUS; ENDOTHELIAL CELLS; GLYCOSAMINOGLYCANS; HEPARAN SULFATE PROTEOGLYCANS; HEPARITIN SULFATE; HUMANS; HYPERGLYCEMIA;

EID: 84905640296     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5695     Document Type: Review

References (120)

1. Aikawa T, Whipple CA, Lopez ME, Gunn J, Young A, Lander AD, and Korc M. Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells. J Clin Invest 118: 89-99, 2013.
2. Baker AB, Chatzizisis YS, Beigel R, Jonas M, Stone BV, Coskun AU, Maynard C, Rogers C, Koskinas KC, Feldman CL, Stone PH, and Edelman ER. Regulation of heparanase expression in coronary artery disease in diabetic, hyperlipidemic swine. Atherosclerosis 213: 436-442, 2010.
3. Bame KJ. Heparanases: endoglycosidases that degrade heparan sulfate proteoglycans. Glycobiology 11: 91R-98R, 2001.
4. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, and Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68: 729-777, 1999.
5. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, and Lose EJ. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 8: 365-393, 1992.
6. Bernfield M, and Sanderson RD. Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors. Philos Trans R London Ser B 327: 171-186, 1990.
7. Bierhaus A, Schiekofer S, Schwaninger M, Andrassy M, Humpert PM, Chen J, Hong M, Luther T, Henle T, Kloting I, Morcos M, Hofmann M, Tritschler H, Weigle B, Kasper M, Smith M, Perry G, Schmidt AM, Stern DM, Haring HU, Schleicher E, and Nawroth PP. Diabetesassociated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 50: 2792-2808, 2001.
8. Blich M, Golan A, Arvatz G, Sebbag A, Shafat I, Sabo E, Cohen-Kaplan V, Petcherski S, Avniel-Polak S, Eitan A, Hammerman H, Aronson D, Axelman E, Ilan N, Nussbaum G, and Vlodavsky I. Macrophage activation by heparanase is mediated by TLR-2 and TLR-4 and associates with plaque progression. Arterioscler Thromb Vasc Biol 33: e56-e65, 2013.
9. Brown DM, Klein DJ, Michael AF, and Oegema TR. 35Sglycosaminoglycans and 35S glycopeptide metabolism by diabetic glomeruli and aorta. Diabetes 31: 418-425, 1995.
10. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001.
11. Buse MG. Hexosamines, insulin resistance, and the complications of diabetes: current status. Am J Physiol Endocrinol Metab 290: E1-E8, 2006.
12. Campos-Xavier AB, Martinet D, Bateman J, Belluoccio D, Rowley L, Tan TY, Baxova A, Gustavson KH, Borochowitz ZU, Innes AM, Unger S, Beckmann JS, Mittaz L, Ballhausen D, Superti-Furga A, Savarirayan R, and Bonafe L. Mutations in the heparan-sulfate proteoglycan glypican 6 (GPC6) impair endochondral ossification and cause recessive omodysplasia. Am J Hum Genet 84: 760-770, 2009.
13. Castellot JJ Jr., Pukac LA, Caleb BL, Wright TC Jr., and Karnovsky MJ. Heparin selectively inhibits a protein kinase C-dependent mechanism of cell cycle progression in calf aortic smooth muscle cells. J Cell Biol 109: 3147-3155, 1989.
14. Casu B, Naggi A, and Torri G. Heparin-derived heparan sulfate mimics to modulate heparan sulfate-protein interaction in inflammation and cancer. Matrix Biol 29: 442-452, 2010.
15. Cizmeci-Smith G, Asundi V, Stahl RC, Teichman LJ, Chernousov M, Cowan K, and Carey DJ. Regulated expression of syndecan in vascular smooth muscle cells and cloning of rat syndecan core protein cDNA. J Biol Chem 267: 15729-15736, 1992.
16. David G, Van der SB, Marynen P, Cassiman JJ, and Van den BH. Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. J Cell Biol 118: 961-969, 1992.
17. Deckert T, Feldt-Rasmussen B, Borsch-Johnsen K, and Kofoed-Envoldsen A. Albuminuria reflects wide spread vascular damage: the Steno hypothesis. Diabetologia 32: 219-226, 1989.
18. Dilley RJ and Nataatmadja MI. Heparin inhibits mesenteric vascular hypertrophy in angiotensin II-infusion hypertension in rats. Cardiovasc Res 38: 247-255, 1998.
19. Dolan M, Horchar T, Rigatti B, and Hassell JR. Identification of sites in domain I of perlecan that regulate heparan sulfate synthesis. J Biol Chem 272: 4316-4322, 1997.
20. Donath MY and Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107, 2011.
21. Donath MY, Storling J, Maedler K, and Mandrup-Poulsen T. Inflammatory mediators and islet beta-cell failure: a link between type 1 and type 2 diabetes. J Mol Med (Berl) 81: 455-470, 2003.
22. Doolittle RF. New perspectives on evolution provided by protein sequences. In: New Perspectiveson Evolution, edited by Leonard W. New York: Wiley-Liss, 1991, pp. 165-173.
23. Endo K, Takino T, Miyamori H, Kinsen H, Yoshizaki T, Furukawa M, and Sato H. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J Biol Chem 278: 40764-40770, 2003.
24. Esko JD, Kimata K, and Lindahl U. Proteoglycans and Sulfated Glycosaminoglycans. In: Essentials of Glycobiology. 2nd edition, edited by Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, and Etzler ME. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2009, pp. 1-39.
25. Fairman RP, Sessler CN, Bierman M, and Glauser FL. Protamine sulfate causes pulmonary hypertension and edema in isolated rat lungs. J Appl Physiol 62: 1363-1367, 1987.
26. Filmus J, Capurro M, and Rast J. Glypicans. Genome Biol 9: 224, 2008.
27. Fitzgerald ML, Wang Z, Park PW, Murphy G, and Bernfield M. Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J Cell Biol 148: 811-824, 2000.
28. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, and Tarbell JM. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93: e136-e142, 2003.
29. Fox CS, Coady S, Sorlie PD, Levy D, Meigs JB, D'Agostino RB Sr., Wilson PW, and Savage PJ. Trends in cardiovascular complications of diabetes. JAMA 292: 2495-2499, 2004.
30. Gambaro G and Baggio B. Role of glycosaminoglycans in diabetic nephropathy. Acta Diabetol 29: 149-155, 1992.
31. Gambaro G, Kinalska I, Oksa A, Pont'usch P, Hertlova M, Olsovsky J, Manitius J, Fedele D, Czekalski S, Perusicova J, Skrl J, Taton J, Grezeszczak W, and Crepaldi G. Oral sulodexide reduces albuminuria in microalbuminuric and macroalbuminuric type 1 and type 2 diabetic patients: the Di.N.A.S. randomized trial. J Am Soc Nephrol 13: 1615-1625, 2002.
32. Gambaro G and Van Der Woude FJ. Glycosaminoglycans: use in treatment of diabetic nephropathy. J Am Soc Nephrol 11: 359-368, 2000.
33. Gambaro G, Venturini AP, Noonan DM, Fries W, Re G, Garbisa S, Milanesi C, Pesarini A, Borsatti A, Marchi E, and Baggio B. Treatment with a glycosaminoglycan formulation ameliorates experimental diabetic nephropathy. Kidney Int 43: 797-806, 1994.
34. Gil N, Goldberg R, Neuman T, Garsen M, Zcharia E, Rubinstein AM, van KT, Meirovitz A, Pisano C, Li JP, van d, V, Vlodavsky I, and Elkin M. Heparanase is essential for the development of diabetic nephropathy in mice. Diabetes 61: 208-216, 2012.
35. Goldin A, Beckman JA, Schmidt AM, and Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114: 597-605, 2006.
36. Groffen AJ, Ruegg MA, Dijkman H, van de Velden TJ, Buskens CA, van den BJ, Assmann KJ, Monnens LA, Veerkamp JH, and van den Heuvel LP. Agrin is a major heparan sulfate proteoglycan in the human glomerular basement membrane. J Histochem Cytochem 46: 19-27, 1998.
37. Haimov-Kochman R, Friedmann Y, Prus D, Goldman-Wohl DS, Greenfield C, Anteby EY, Aviv E, Vlodavsky I, and Yagel S. Localization of heparanase in normal and pathological human placenta. Mol Hum Reprod 8: 566-573, 2002.
38. Han J, Mandal AK, and Hiebert LM. Endothelial cell injury by high glucose and heparanase is prevented by insulin, heparin and basic fibroblast growth factor. Cardiovasc Diabetol 4: 12, 2005.
39. Han J, Woytowich AE, Mandal AK, and Hiebert LM. Heparanase upregulation in high glucose-treated endothelial cells is prevented by insulin and heparin. Exp Biol Med 232: 927-934, 2007.
40. Han J, Zhang F, Xie J, Linhardt RJ, and Hiebert LM. Changes in cultured endothelial cell glycosaminoglycans under hyperglycemic conditions and the effect of insulin and heparin. Cardiovasc Diabetol 8: 46, 2009.
41. Harvey SJ, Jarad G, Cunningham J, Rops AL, van d, V, Berden JH, Moeller MJ, Holzman LB, Burgess RW, and Miner JH. Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol 171: 139-152, 2007.
42. Hassan MS, Mileva MM, Dweck HS, and Rosenfeld L. Nitric oxide products degrade chondroitin sulfates. Nitric Oxide 2: 360-365, 1998.
43. Hiebert LM and Jaques LB. Heparin uptake on endothelium. Artery 2: 26-37, 1976.
44. Hiebert LM and Jaques LB. The observation of heparin on endothelium after injection. Thromb Res 8: 195-204, 1976.
45. Hiebert LM and Liu J. Heparin protects cultured endothelial cells from damage by toxic oxygen metabolites. Atherosclerosis 83: 47-51, 1990.
46. Hiebert LM and Liu J. Protective action of polyelectrolytes on endothelium. Semin Thromb Hemost 17(Supp 1): 42-46, 1991.
47. Hulett MD, Freeman C, Hamdorf BJ, Baker RT, Harris MJ, and Parish CR. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat Med 5: 803-809, 1999.
48. Ilan N, Elkin M, and Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol 38: 2018-2039, 2006.
49. Ilse Raats CJ, van den Born J, and Berden JHM. Glomerular heparan sulfate alterations: Mechanisms and relevance for proteinuria. Kidney Int 57: 385-400, 2000.
50. Jalkanen M, Rapraeger A, Saunders S, and Bernfield M. Cell surface proteoglycan of mouse mammary epithelial cells is shed by cleavage of its matrix-binding ectodomain from its membrane-associated domain. J Cell Biol 105: 3087-3096, 1987.
51. Jeansson M and Haraldsson B. Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Renal Physiol 290: F111-F116, 2006.
52. Jörneskog G, Brismar K, and Fagrell B. Low molecular weight heparin seems to improve local capillary circulation and healing of chronic foot ulcers in diabetic patients. Vasa 22: 137-141, 2006.
53. Kanwar YS, Veis A, Kimura JH, and Jakubowski ML. Characterization of heparan sulfate-proteoglycan of glomerular basement membranes. Proc Natl Acad Sci U S A 81: 762-766, 1984.
54. Kennett EC and Davies MJ. Degradation of matrix glycosaminoglycans by peroxynitrite/peroxynitrous acid: evidence for a hydroxyl-radical-like mechanism. Free Radic Biol Med 42: 1278-1289, 2007.
55. Kojima T, Shworak NW, and Rosenberg RD. Molecular cloning and expression of two distinct cDNA-encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line. J Biol Chem 267: 4870-4877, 1992.
56. Kokenyesi R and Bernfield M. Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1. J Biol Chem 269: 12304-12309, 1994.
57. Kosir MA, Foley-Loudon PA, Finkenauer R, and Tennenberg SD. Multiple heparanases are expressed in polymorphonuclear cells. J Surg Res 103: 100-108, 2002.
58. Kouretas PC, Hannan RL, Kapur NK, Hendrickson R, Redmond EM, Myers AK, Kim YD, Cahill PA, and Sitzmann JV. Non-anticoagulant heparin increases endothelial nitric oxide synthase activity: role of inhibitory guanine nucleotide proteins. J Mol Cell Cardiol 30: 2669-2682, 1998.
59. Kristova V, Liskova S, Sotnikova R, Vojtko R, and Kurtansky A. Sulodexide improves endothelial dysfunction in streptozotocin-induced diabetes in rats. Physiol Res 57: 491-494, 2008.
60. Lennon FE and Singleton PA. Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis 1: 200-213, 2011.
61. Levy-Adam F, Abboud-Jarrous G, Guerrini M, Beccati D, Vlodavsky I, and Ilan N. Identification and characterization of heparin/heparan sulfate binding domains of the endoglycosidase heparanase. J Biol Chem 280: 20457-20466, 2005.
62. Li Q, Park PW, Wilson CL, and Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111: 635-646, 2002.
63. Mandal AK, Lyden T, and Saklayen MG. Heparin lowers blood pressure:Biological and clinical perspectives. Kidney Int 47: 1017-1022, 1995.
64. Mandal AK, Ping T, Caldwell SJ, Bagnell R, and Hiebert LM. Electron microscopic analysis of glucose-induced endothelial damage in primary culture: possible mechanism and prevention. Histol Histopathol 21: 941-950, 2006.
65. Mandal AK, Puchalski JT, Lemley-Gillespie S, Taylor CA, and Kohno M. Effect of insulin and heparin on glucose-induced vascular damage in cell culture. Kidney Int 57: 2492-2501, 2000.
66. Maxhimer JB, Somenek M, Rao G, Pesce CE, Baldwin D Jr., Gattuso P, Schwartz MM, Lewis EJ, Prinz RA, and Xu X. Heparanase-1 gene expression and regulation by high glucose in renal epithelial cells: a potential role in the pathogenesis of proteinuria in diabetic patients. Diabetes 54: 2172-2178, 2005.
67. McKenzie E, Tyson K, Stamps A, Smith P, Turner P, Barry R, Hircock M, Patel S, Barry E, Stubberfield C, Terrett J, and Page M. Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member. Biochem Biophys Res Commun 276: 1170-1177, 2000.
68. Mertens G, Van Der Schueren B, Van Den Berghe H, and David G. Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content. J Cell Biol 132: 487-497, 1996.
69. Morita H, Yoshimura A, Inui K, Ideura T, Watanabe H, Wang L, Soininen R, and Tryggvason K. Heparan sulfate of perlecan is involved in glomerular filtration. J Am Soc Nephrol 16: 1703-1710, 2005.
70. Moseley R, Waddington RJ, and Embery G. Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes. Biochim Biophys Acta 1362: 221-231, 1997.
71. Myrup B, Hansen P, Jensen T, Kofoed-Envoldsen A, Feldt-Rasmussen B, Gram J, Kluft C, Jespersen J, and Deckert T. Effect of low-dose heparin on urinary albumin excretion in insulin-dependent diabetes mellitus. Lancet 345: 421-422, 1995.
72. Nader NB, Toma L, Pinhal MAS, Buonassisi V, Colburn P, and Dietrich CP. Effect of heparin and dextran sulfate on the synthesis and structure of heparan sulfate from cultured endothelial cells. Semin Thromb Hemost 17: 47-56, 1991.
73. Nagasawa K, Uchiyama H, Sato N, and Hatano A. Chemical change involved in the oxidative-reductive depolymerization of heparin. Carb Res 236: 165-180, 1992.
74. Noonan DM, Fulle A, Valente P, Cai S, Horigan E, Sasaki M, Yamada Y, and Hassell JR. The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J Biol Chem 266: 22939-22947, 1991.
75. Olsen BR. Life without perlecan has its problems. J Cell Biol 147: 909-912, 1999.
76. Pacher P, Obrosova IG, Mabley JG, and Szabo C. Role of nitrosative stress and peroxynitrite in the pathogenesis of diabetic complications. Emerging new therapeutical strategies. Curr Med Chem 12: 267-275, 2005.
77. Parish CR, Freeman C, and Hulett MD. Heparanase: a key enzyme involved in cell invasion. Biochim Biophys Acta 1471: M99-M108, 2001.
78. Parish CR, Freeman C, Ziolkowski AF, He YQ, Sutcliffe EL, Zafar A, Rao S, and Simeonovic CJ. Unexpected new roles for heparanase in Type 1 diabetes and immune gene regulation. Matrix Biol 32: 228-233, 2013.
79. Parsons BJ, Sibanda S, Heyes DJ, and Paterson AW. Reaction of superoxide radicals with glycosaminoglycan chloramides: a kinetic study. Free Radic Biol Med 61C: 111-118, 2013.
80. Parthasarathy N and Spiro RG. Isolation and characterization of the heparan sulfate proteoglycan of the bovine glomerular basement membrane. J Biol Chem 259: 12749-12755, 1984.
81. Pinhal MA, Walenga JM, Jeske W, Hoppensteadt D, Dietrich CP, Fareed J, and Nader HB. Antithrombotic agents stimulate the synthesis and modify the sulfation pattern of a heparan sulfate proteoglycan from endothelial cells. Thromb Res 74: 143-153, 1994.
82. Rao NV, Argyle B, Xu X, Reynolds PR, Walenga JM, Prechel M, Prestwich GD, MacArthur RB, Walters BB, Hoidal JR, and Kennedy TP. Low anticoagulant heparin targets multiple sites of inflammation, suppresses heparininduced thrombocytopenia, and inhibits interaction of RAGE with its ligands. Am J Physiol Cell Physiol 299: C97-C110, 2010.
83. Rapraeger AC and Ott VL. Molecular interactions of the syndecan core proteins. Curr Opin Cell Biol 10: 620-628, 1998.
84. Rask-Madsen C and King GL. Proatherosclerotic mechanisms involving protein kinace C in diabetes and insulin resistance. Arterioscler Thromb Vasc Biol 25: 487-496, 2004.
85. Rees MD, Hawkins CL, and Davies MJ. Hypochlorite and superoxide radicals can act synergistically to induce fragmentation of hyaluronan and chondroitin sulphates. Biochem J 381: 175-184, 2004.
86. Rees MD, Kennett EC, Whitelock JM, and Davies MJ. Oxidative damage to extracellular matrix and its role in human pathologies. Free Radic Biol Med 44: 1973-2001, 2008.
87. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, and oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 454: 345-359, 2007.
88. Rops AL, van den Hoven MJ, Veldman BA, Salemink S, Vervoort G, Elving LD, Aten J, Wetzels JF, van d, V, and Berden JH. Urinary heparanase activity in patients with Type 1 and Type 2 diabetes. Nephrol Dial Transplant 27: 2853-2861, 2012.
89. Sanderson RD and Iozzo RV. Targeting heparanase for cancer therapy at the tumor-matrix interface. Matrix Biol 31: 283-284, 2012.
90. Sato I, Zu J, Nishikawa S, and Kashimura N. Depolymerization of hyaluronic-acid by D-fructose 6-phosphate. Biosci Biotechnol Biochem 57: 2005-2009, 1993.
91. Satyajit M and Riezman H. Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5: 110-120, 2004.
92. Saunders S, Jalkanen M, O'Farrell S, and Bernfield M. Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol 108: 1547-1556, 1989.
93. Setter SM, Campbell RK, and Cahoon CJ. Biochemical pathways for microvascular complications of diabetes mellitus. Ann Pharmacother 37: 1858-1866, 2003.
94. Shafat I, Agbaria A, Boaz M, Schwartz D, Baruch R, Nakash R, Ilan N, Vlodavsky I, and Weinstein T. Elevated urine heparanase levels are associated with proteinuria and decreased renal allograft function. PLoS One 7: e44076, 2012.
95. Shafat I, Ilan N, Zoabi S, Vlodavsky I, and Nakhoul F. Heparanase levels are elevated in the urine and plasma of type 2 diabetes patients and associate with blood glucose levels. PLoS One 6: e17312, 2011.
96. Singh A, Ramnath RD, Foster RR, Wylie EC, Friden V, Dasgupta I, Haraldsson B, Welsh GI, Mathieson PW, and Satchell SC. Reactive oxygen species modulate the barrier function of the human glomerular endothelial glycocalyx. PLoS One 8: e55852, 2013.
97. Sotnikov I, Hershkoviz R, Grabovsky V, Ilan N, Cahalon L, Vlodavsky I, Alon R, and Lider O. Enzymatically quiescent heparanase augments T cell interactions with VCAM-1 and extracellular matrix components under versatile dynamic contexts. J Immunol 172: 5185-5193, 2004.
98. Subramanian SV, Fitzgerald ML, and Bernfield M. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J Biol Chem 272: 14713-14720, 1997.
99. Susic D, Mandal AK, Jovovic D, Stojanov M, Djordjevic-Denic G, and Kentera D. Antihypertensive action of heparin: role of the renin-angiotensin system and prostaglandins. J Clin Pharmacol 33: 342-347, 1993.
100. Tiefenbacher CP and Chilian WM. Basic fibroblast growth factor and heparin influence coronary arteriolar tone by causing endothelium-dependent dilation. Cardiovasc Res 34: 411-417, 1997.
101. Timpl R. Proteoglycans of basement membranes. Experientia 49: 417-428, 1993.
102. Tkachenko E, Rhodes JM, and Simons M. Syndecans: new kids on the signaling block. Circ Res 96: 488-500, 2005.
103. Traister A, Shi W, and Filmus J. Mammalian Notum induces the release of glypicans and other GPI-anchored proteins from the cell surface. Biochem J 410: 503-511, 2008.
104. Uchiyama H, Dobashi Y, Ohkouchi K, and Nagasawa K. Chemical change involved in the oxidative reductive depolymerization of hyaluronic acid. J Biol Chem 265: 7753-7759, 1990.
105. Van der Pijl JW, Lemkes HH, Frolich M, Van Der Woude FJ, van der Meer FJ, and Van Es LA. Effect of danaparoid sodium on proteinuria, von Willebrand factor, and hard exudates in patients with diabetes mellitus type 2. J Am Soc Nephrol 10: 1331-1336, 1999.
106. Van der Pijl JW, Van Der Woude FJ, Geelhoed-Duijvestijn PH, Frolich M, van der Meer FJ, Lemkes HH, and Van Es LA. Danaparoid sodium lowers proteinuria in diabetic nephropathy. J Am Soc Nephrol 8: 456-462, 1997.
107. Vilar RE, Ghael D, Li M, Bhagat DD, Arrigo LM, Cowman MK, Dweck HS, and Rosenfeld L. Nitric oxide degradation of heparin and heparan sulphate. Biochem J 324(Pt 2): 473-479, 1997.
108. Vlodavsky I, Blich M, Li JP, Sanderson RD, and Ilan N. Involvement of heparanase in atherosclerosis and other vessel wall pathologies. Matrix Biol 2013.
109. Vlodavsky I, Eldor A, Bar-Ner M, Friedman R, Cohen IR, and Klagsburn M. Heparan sulfate degradation in tumor cell invasion and angiogenesis. Adv Exp Med Biol 233: 201-210, 1988.
110. Vlodavsky I, Eldor A, Haimovitzfriedman A, Matzner Y, Ishaimichaeli R, Lider O, Naparstek Y, Cohen IR, and Fuks Z. Expression of heparanase by platelets and circulating cells of the immune system-Possible involvement in diapedesis and extravasation. Invasion Metastasis 12: 112-127, 1992.
111. Vlodavsky I, Friedmann Y, Elkin M, Aingorn H, Atzmon R, Ishai-Michaeli R, Bitan M, Pappo O, Peretz T, Michal I, Spector L, and Pecker I. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat Med 5: 793-802, 1999.
112. Wang F, Kim MS, Puthanveetil P, Kewalramani G, Deppe S, Ghosh S, Abrahani A, and Rodrigues B. Endothelial heparanase secretion after acute hypoinsulinemia is regulated by glucose and fatty acid. Am J Physiol Heart Circ Physiol 296: H1108-H1116, 2009.
113. Wang F, Wang Y, Kim MS, Puthanveetil P, Ghosh S, Luciani DS, Johnson JD, Abrahani A, and Rodrigues B. Glucose-induced endothelial heparanase secretion requires cortical and stress actin reorganization. Cardiovasc Res 87: 127-136, 2010.
114. Wasty F, Alavi MZ, and Moore S. Distribution of glycosaminoglycans in the intima of human aortas: changes in atherosclerosis and diabetes mellitus. Diabetologia 36: 316-322, 1993.
115. Whitelock JM, Melrose J, and Iozzo RV. Diverse cell signaling events modulated by perlecan. Biochemistry 47: 11174-11183, 2008.
116. Wild S, Roglic G, Green A, Sicree R, and King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27: 1047-1053, 2004.
117. Yamagishi S, Nakamura K, Matsui T, Takenaka K, Jinnouchi Y, and Imaizumi T. Cardiovascular disease in diabetes. Mini Rev Med Chem 6: 313-318, 2006.
118. Yan SF, Ramasamy R, and Schmidt AM. The RAGE axis: a fundamental mechanism signaling danger to the vulnerable vasculature. Circ Res 106: 842-853, 2010.
119. Young E. The anti-inflammatory effects of heparin and related compounds. Thromb Res 122: 743-752, 2008.
120. Zu J, Nishikawa S, and Kashimura N. Depolymerization of hyaluronic acid by low-molecular-weight Amadorirearrangement products and glycated polylysine. Biosci Biotechnol Biochem 61: 188-190, 1997.