The role of hyaluronic acid in atherosclerosis and intimal hyperplasia

Journal of Surgical Research

Volumn 173, Issue 2, 2012, Pages

  Sadowitz, Benjamin ^a,b   Seymour, Keri ^a,b   Gahtan, Vivian ^a,b   Maier, Kristopher G ^a,b  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b VA Healthcare Network Upstate New York   (United States)

Author keywords

atherosclerosis; CD44; endothelial cells; extracellular matrix; hyaluronic acid; leukocytes; platelets; restenosis; RHAMM; vascular smooth muscle cells

Indexed keywords

CD44V ANTIGEN; HYALURONIC ACID;

ARTERY INJURY; ARTERY INTIMA PROLIFERATION; ATHEROGENESIS; ATHEROSCLEROSIS; DIABETES MELLITUS; ENDOTHELIUM CELL; ENDOVASCULAR SURGERY; EXTRACELLULAR MATRIX; HUMAN; HYPERGLYCEMIA; INFLAMMATION; LEUKOCYTE ADHERENCE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SURGICAL TECHNIQUE; THROMBOCYTE; VASCULAR SMOOTH MUSCLE; WOUND CONTRACTION;

ANIMALS; ANTIGENS, CD44; ATHEROSCLEROSIS; CORONARY RESTENOSIS; HYALURONIC ACID; HYPERPLASIA; TUNICA INTIMA;

EID: 84858289995     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2011.09.025     Document Type: Review

References (92)

1. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999;340:115.
2. Bot P, Hoefer I, Piek J, et al. Hyaluronic acid: Targeting immune modulatory components of the extracellular matrix in atherosclerosis. Curr Med Chem 2008;15:786.
3. Tabata T, Mine S, Okada Y, et al. Low molecular weight hyaluronan increases the uptaking of oxidized LDL into monocytes. Endocr J 2007;54:685.
4. Riessen R, Wight T, Pastore C, et al. Distribution of hyaluronan during extracellular matrix remodeling in human restenotic arteries and balloon-injured rat carotid arteries. Circulation 1996; 93:1141.
5. Toole B, Wight T, Tammi M. Hyaluronan-cell interactions in cancer and vascular disease. J Biol Chem 2001;277:4593.
6. Shirali A, Goldstein D. Activation of the innate immune system by the endogenous ligand hyaluronan. Curr Opin Organ Transplant 2008;13:20.
7. Lee J, Spicer A. Hyaluronan: A multifunctional, megaDalton, stealth molecule. Curr Opin Cell Biol 2000;12:581.
8. Itano N, Sawai T, Yoshida M, et al. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J Biol Chem 1999;274:25085.
9. Levesque H, Girard N, Maingonnat C, et al. Localization and solubilization of hyaluronan and of the hyaluronan-binding protein hyaluronectin in human normal and arteriosclerotic arterial walls. Atherosclerosis 1994;105:51.
10. Day A, Sheehan J. Hyaluronan: Polysaccharide chaos to protein organization. Curr Opin Struct Biol 2001;11:617.
11. Stern R, Asari A, Sugahara K. Hyaluronan fragments: An information-rich system. Eur J Cell Biol 2006;85:699.
12. Coleman P, Scott D, Mason R, et al. Characterization of the effect of high molecular weight hyaluronan on trans-synovial flow in rabbit knees. J Physiol (Lond) 1999;514:265.
13. Lepperdinger G, Mullegger J, Krell G. Hyal2-less active, but more versatile? Matrix Biol 2001;20:509.
14. Slevin M, Krupinski J, Gaffney J, et al. Hyaluronan-mediated angiogenesis in vascular disease: Uncovering RHAMM and CD44 receptor signaling pathways. Matrix Biol 2007;26:58.
15. Jackson D. Immunological functions of hyaluronan and its receptors in the lymphatics. Immunol Rev 2009;2230:216.
16. Allison D, Wight T, Ripp N, et al. Endogenous overexpression of hyaluronan synthases within dynamically cultured collagen gels: Implications for vascular and valvular disease. Biomaterials 2008;29:2969.
17. DeAngelis P. Hyaluronan synthases: Fascinating glycosyltransferases from vertebrates, bacterial pathogens, and algal viruses. Cell Mol Life Sci 1999;56:670.
18. Zhou B, Weigel J, Fauss L, et al. Identification of the hyaluronan receptor for endocytosis (HARE). J Biol Chem 2000;275: 37733.
19. Harada H, Takahashi M. CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and -2. J Biol Chem 2007;282:5597.
20. Ponta H, Sherman L, Herrlich P. CD44: From adhesion molecules to signaling regulators. Nat Rev Mol Cell Biol 2003;4:33.
21. Lesley J, Hascall V, Tammi M, et al. Hyaluronan binding by cell surface CD44. J Biol Chem 2000;275:26967.
22. Culty M, Nguyen H, Underhill, C. The hyaluronan receptor (CD44) participates in the uptake and degradation of hyaluronan. J Cell Biol 1992;116:1055.
23. Banerji S, Ni J, Wang S, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999;144:789.
24. DeGuine V, Menasche M, Ferrari P, et al. Free radical depolymerization of hyaluronan by millard reaction products: Role in liquefaction of aging vitreous. Int J Biol Macromol 1998;22:17.
25. Soltes L, Stankovska M, Kogan G, et al. Contribution of oxidative-reductive reactions to high-molecular-weight hyaluronan catabolism. Chem Biodiversity 2005;2:1242.
26. Frost G, Csoka T, Wong T, et al. Purification, cloning, and expression of human plasma hyaluronidase. Biochem Biophys Res Commun 1997;236:10.
27. Rai S, Duh F, Vigdorovich V, et al. Candidate tumor suppressor HYAL2 is a glycosylphosphatidylinositol (GPI)-anchored cell-surface receptor for Jaagsiekte sheep retrovirus, the envelope protein of which mediates oncogenic transformation. Proc Natl Acad Sci USA 2001;98:4443.
28. Turley E, Noble P, Bourguignon L. Signaling properties of hyaluronan receptors. J Biol Chem 2002;277:4589.
29. Jiang D, Liang J, Noble P. Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol 2007;23:435.
30. Jackson D. Biology of the lymphatic marker LYVE-1 and applications in research into lymphatic trafficking and lymphangiogenesis. Acta Pathol Microbiol Immunol Scand 2004;112:526.
31. Mohamadzadeh M, DeGrendele H, Arizpe H, et al. Proinflammatory stimuli regulate endothelial hyaluronan expression and CD44/HA-dependent primary adhesion. J Clin Invest 1998; 101:97.
32. Lesley J, Schulte R, Hyman R. Binding of hyaluronic acid to lymphoid cell lines is inhibited by monoclonal antibodies against Pgp-1. Exp Cell Res 1990;187:224.
33. Levesque M, Haynes B. In vitro culture of human peripheral blood monocytes induces hyaluronan binding and up-regulates monocyte variant CD44 isoform expression. J Immunol 1996; 156:1557.
34. Levesque M, Haynes B. Cytokine induction of the ability of human monocyte CD44 to bind hyaluronan is mediated primarily by TNF-α and is inhibited by IL-4 and IL-13. J Immunol 1997; 159:6184.
35. Lesley J, Howes N, Perschl A, et al. Hyaluronan binding function of CD44 is transiently activated on T cells during and in vivo immune response. J Exp Med 1994;180:383.
36. Sun CX, Robb VA, Gutmann DH. Protein 4.1 tumor suppressors: Getting a FERM grip on growth regulation. J Cell Sci 2002; 115:3991.
37. Kalomiris EL, Bourguignon LY. Mouse T lymphoma cells contain a transmembrane glycoprotein (GP85) that binds ankyrin. J Cell Biol 1988;106:319.
38. Hawkins CL, Davies MJ. Degradation of hyaluronic acid, polyand monosaccharides, and model compounds by hypochlorite: Evidence for radical intermediates and fragmentation. Free Radic Biol Med 1998;24:1396.
39. Maier KG, Sadowitz B, Cullen S, et al. Thrombospondin-1-induced vascular smooth muscle cell migration is dependent on the hyaluronic acid receptor CD44. Am J Surg 2009;198:664.
40. Entwistle J, Hall C, Turley E. HA receptors: Regulators of signaling to the cytoskeleton. J Cell Biochem 1996;61:569.
41. Hall C, Wang C, Lange L, et al. Hyaluronan and the hyaluronan receptor RHAMM promote focal adhesion turnover and transient tyrosine kinase activity. J Cell Biol 1994;126:575.
42. Goueffic Y, Guilluy C, Guerin P, et al. Hyaluronan induces vascular smooth muscle cell migration through RHAMM-mediated PI3K-dependent Rac activation. Cardiovasc Res 2006;72:339.
43. Lokeshwar V, Selzer M. Differences in hyaluronic acid-mediated functions and signaling in arterial, microvessel, and vein-derived human endothelial cells. J Biol Chem 2000;275:27641.
44. Zhou R, Wu X, Skalli O. The hyaluronan receptor RHAMM/ IHABP in astrocytoma cells: Expression of a tumor-specific variant and association with microtubules. J Neurooncol 2002;59:15.
45. Maxwell CA, Keats JJ, Crainie M, et al. RHAMM is a centrosomal protein that interacts with dynein and maintains spindle pole stability. Mol Biol Cell 2003;14:2262.
46. Evanko SP, Parks WT, Wight TN. Intracellular hyaluronan in arterial smooth muscle cells: Association with microtubules, RHAMM, and the mitotic spindle. J Histochem Cytochem 2004; 52:1525.
47. Prevo R, Banerji S, Ferguson D, et al. Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J Biol Chem 2001;276:19420.
48. Johnson L, Prevo R, Clasper S, et al. Inflammation-induced uptake and degradation of the lymphatic endothelial hyaluronan receptor LYVE-1. J Biol Chem 2007;282:33671.
49. Harris EN, Kyosseva SV, Weigel JA, et al. Expression, processing, and glycosaminoglycan binding activity of the recombinant human 315-kDa hyaluronic acid receptor for endocytosis (HARE). J Biol Chem 2007;282:2785.
50. Laurent TC, Fraser JR. Hyaluronan. FASEB J 1992;6:2397.
51. Harris EN, Weigel PH. The ligand-binding profile of HARE: Hyaluronan and chondroitin sulfates A, C, and D bind to overlapping sites distinct from the sites for heparin, acetylated low-density lipoprotein, dermatan sulfate, and CS-E. Glycobiology 2008;18:638.
52. Harris EN, Weigel JA, Weigel PH. The human hyaluronan receptor for endocytosis (HARE/Stabilin-2) is a systemic clearance receptor for heparin. J Biol Chem 2008;283:17341.
53. Falkowski M, Schledzewski K, Hansen B, et al. Expression of stabilin-2, a novel fasciclin-like hyaluronan receptor protein, in murine sinusoidal endothelia, avascular tissues, and at solid/liquid interfaces. Histochem Cell Biol 2003;120:361.
54. Siegel-Axel D, Daub K, Seizer P, et al. Platelet lipoprotein interplay: Trigger of foam cell formation and driver of atherosclerosis. Cardiovasc Res 2008;78:8.
55. Rajagopalan S, Mckay I, Ford I, et al. Platelet activation increases with the severity of peripheral arterial disease: Implications for clinical management. J Vasc Surg 2007;46:485.
56. de la Motte C, Nigro J, Vasanji A, et al. Platelet-derived hyaluronidase 2 cleaves hyaluronan into fragments that trigger monocyte-mediated production of proinflammatory cytokines. Am J Pathol 2009;174:2254.
57. Ikeda U, Ikeda M, Oohara T, et al. Interleukin 6 stimulates growth of vascular smooth muscle cells in a PDGF-dependent manner. Am J Physiol 1991;260:H1713.
58. Taylor K, Trowbridge J, Rudisill J, et al. Hyaluronan fragments stimulate endothelial recognition of injury through TRL4. J Biol Chem 2004;279:17079.
59. Gillitzer R, Goebeler M. Chemokines in cutaneous wound healing. J Leukoc Biol 2001;69:513.
60. Jialal I, Devaraj S, Venugopal S. C-reactive protein: Risk marker or mediator in atherothrombosis? Hypertension 2004;44:6.
61. Papakonstantinou E, Roth M, Block L, et al. The differential distribution of hyaluronic acid in the layers of human atheromatic aortas is associated with vascular smooth muscle cell proliferation and migration. Atherosclerosis 1998;138:79.
62. Evanko S, Angello J, Wight T. Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1999;19:1004.
63. Wilkinson T, Bressler S, Evanko S, et al. Overexpression of hyaluronan synthases alters vascular smooth muscle cell phenotype and promotes monocyte adhesion. J Cell Physiol 2006; 206:378.
64. de la Motte C, Hascall V, Calabro A, et al. Mononuclear leukocytes preferentially BInd via CD44 to hyaluronan on human intestinal mucosal smooth muscle cells after virus infection or treatment with poly(IC). J Biol Chem 1999;274:30747.
65. de la Motte C, Hascall V, Drazba J, et al. Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid: Polycytidylic Acid. Am J Pathol 2003;163:121.
66. DeGrendele H, Estess P, Picker L, et al. CD44 and its ligand hyaluronate mediate rolling under physiologic flow: A novel lymphocyte-endothelial cell primary adhesion pathway. J Exp Med 1996;183:1119.
67. Chajara A, Raoudi M, Delpech D, et al. Inhibition of arterial cells proliferation in vivo in injured arteries by hyaluronan fragments. Atherosclerosis 2003;171:15.
68. Sumpio B, Riley J, Dardik A. Cells in focus: Endothelial cell. Int J Biochem Cell Biol 2002;34:1508.
69. Jonasson L, Holm J, Skalli O, et al. Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis 1986;6:131.
70. Nandi A, Estess P, Siegelman M. Bimolecular complex between rolling and firm adhesion receptors required for cell arrest: CD44 association with VLA-4 in T cell extravasation. Immunity 2004;20:455.
71. Bonder C, Clark S, Norman M, et al. Use of CD44 by CD4+ Th1 and Th2 lymphocytes to roll and adhere. Blood 2006; 107:4798.
72. Sainio A, Jokela T, Tammi MI, et al. Hyperglycemic conditions modulate connective tissue reorganization by human vascular smooth muscle cells through stimulation of hyaluronan synthesis. Glycobiology 2010;20:1117.
73. Maier KG, Han X, Sadowitz B, et al. Thrombospondin-1: A proatherosclerotic protein augmented by hyperglycemia. J Vasc Surg 2010;51:1238.
74. Liu M, Roubin G, King S. Restenosis after coronary angioplasty. Potential biologic determinants and role of intimal hyperplasia. Circulation 1989;79:1374.
75. Mondy J, Williams J, Adams M, et al. Structural determinants of lumen narrowing after angioplasty in atherosclerotic nonhuman primates. J Vasc Surg 1997;26:875.
76. Post M, Borst C, Kuntz R. The relative importance of arterial remodeling compared with intimal hyperplasia in lumen renarrowing after balloon angioplasty. A study in the normal rabbit and the hypercholesterolemic Yucatan micropig. Circulation 1994;89:2816.
77. Geary R, Nikkari S, Wagner W, et al. Wound healing: A paradigm for lumen narrowing after arterial reconstruction. J Vasc Surg 1998;27:96.
78. Geary R, Williams J, Golden D, et al. Time course of cellular proliferation, intimal hyperplasia, and remodeling following angioplasty in monkeys with established atherosclerosis. Arterioscler Thromb Vasc Biol 1996;16:34.
79. Mintz G, Popma J, Pichard A, et al. Arterial remodeling after coronary angioplasty. Circulation 1996;94:35.
80. Martin P. Wound healing - aiming for perfect skin regeneration. Science 1997;276:75.
81. Travis JA, Hughes MG, Wong JM, et al. Hyaluronan enhances contraction of collagen by smooth muscle cells and adventitial fibroblasts: Role of CD44 and implications for constrictive remodeling. Circ Res 2001;88:77.
82. De Vries HJ, Zeegelaar JE, Middelkoop E, et al. Reduced wound contraction and scar formation in punch biopsy wounds. Native collagen dermal substitutes. A clinical study. Br J Dermatol 1995;132:690.
83. Savani R, Wang C, Yang B, et al. Migration of bovine aortic smooth muscle cells after wounding injury: The role of hyaluronan and RHAMM. J Clin Invest 1995;95:1158.
84. Jain M, He Q, Lee W, et al. Role of CD44 in the reaction of vascular smooth muscle cells to arterial wall injury. J Clin Invest 1996;97:596.
85. Chajara A, Levesque H, Courel M, et al. Hyaluronan and hyaluronectin production in injured rat thoracic aorta. Atherosclerosis 1996;125:193.
86. Riessen R, Isner JM, Blessing E, et al. Regional differences in the distribution of the proteoglycans biglycan and decorin in the extracellular matrix of atherosclerotic and restenotic human coronary arteries. Am J Pathol 1994;144:962.
87. Lexis CP, Rahel BM, Meeder JG, et al. The role of glucose lowering agents on restenosis after percutaneous coronaryintervention in patients with diabetes mellitus. Cardiovasc Diabetol 2009;8:41.
88. Chajara A, Raoudi M, Delpech B, et al. Effects of diabetes and insulin treatment of diabetic rats on hyaluronan and hyaluronectin production in injured aorta. J Vasc Res 1999;36:209.
89. Chajara A, Raoudi M, Delpech B, et al. Increased hyauronan and hyaluronidase production and hyaluronan degradation in injured aorta of insulin-resistant rats. Arterioscler Thromb Vasc Biol 2000;20:1480.
90. Savani R, Turley E. The role of hyaluronan and its receptors in restenosis after balloon angioplasty: Development of a potential therapy. Int J Tissue React 1995;17:141.
91. Chajara A, Delpech B, Courel M, et al. Effect of aging on neointima formation and hyaluronan, hyaluronidase, and hyaluronectin production in injured rat aorta. Atherosclerosis 1998; 138:53.
92. Goodison S, Urquidi V, Tarin D. CD44 cell adhesion molecules. Mol Pathol 1999;52:189.