Mitigation of diabetes-related complications in implanted collagen and elastin scaffolds using matrix-binding polyphenol

Biomaterials

Volumn 34, Issue 3, 2013, Pages 685-695

  Chow, James P ^a   Simionescu, Dan T ^a   Warner, Harleigh ^a   Wang, Bo ^b   Patnaik, Sourav S ^b   Liao, Jun ^b   Simionescu, Agneta ^a  

^a AMRL   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

AGE; Antioxidant; Heart valve; Matrix proteins; Vascular graft

Indexed keywords

AGE; ANTIOXIDANT; HEART VALVES; MATRIX PROTEINS; VASCULAR GRAFTS;

BIOMINERALIZATION; COLLAGEN; CROSSLINKING; GLUCOSE; GLYCOPROTEINS; GRAFTS; PATIENT TREATMENT;

SCAFFOLDS (BIOLOGY);

ADVANCED GLYCATION END PRODUCT; COLLAGEN; ELASTIN; GLUCOSE PENTAGALLATE; POLYPHENOL; TISSUE SCAFFOLD;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIFICATION; CONTROLLED STUDY; CROSS LINKING; DIABETES MELLITUS; ENZYMATIC DEGRADATION; HEART VALVE; IN VIVO STUDY; MALE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; TISSUE ENGINEERING;

ANIMALS; ANTIOXIDANTS; BIOCOMPATIBLE MATERIALS; BLOOD VESSEL PROSTHESIS; COLLAGEN; DIABETES MELLITUS, EXPERIMENTAL; ELASTIN; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; HYDROLYZABLE TANNINS; MALE; RATS; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

RATTUS;

EID: 84868503719     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.09.081     Document Type: Article

References (69)

1. http://www.cdc.gov/diabetes/pubs/pdf/ndfs_2011.pdf.
2. Goldberg R.B. Cardiovascular disease in patients who have diabetes. Cardiol Clin 2003, 21(3):399-413. vii.
3. Briand M., Lemieux I., Dumesnil J.G., Mathieu P., Cartier A., Despres J.P., et al. Metabolic syndrome negatively influences disease progression and prognosis in aortic stenosis. J Am Coll Cardiol 2006, 47(11):2229-2236.
4. Messika-Zeitoun D., Bielak L.F., Peyser P.A., Sheedy P.F., Turner S.T., Nkomo V.T., et al. Aortic valve calcification: determinants and progression in the population. Arterioscler Thromb Vasc Biol 2007, 27(3):642-648.
5. Peterson L.R., McKenzie C.R., Schaffer J.E. Diabetic cardiovascular disease: getting to the heart of the matter. J Cardiovasc Transl Res 2012, 5(4):436-445.
6. Winlove C.P., Parker K.H., Avery N.C., Bailey A.J. Interactions of elastin and aorta with sugars in vitro and their effects on biochemical and physical properties. Diabetologia 1996, 39(10):1131-1139.
7. Sakata N., Noma A., Yamamoto Y., Okamoto K., Meng J., Takebayashi S., et al. Modification of elastin by pentosidine is associated with the calcification of aortic media in patients with end-stage renal disease. Nephrol Dial Transplant 2003, 18(8):1601-1609.
8. Meli M., Granouillet R., Reynaud E., Chamson A., Frey J., Perier C. In vitro glycoxidation of insoluble fibrous type I collagen: solubilization and advanced glycation end products. J Protein Chem 2003, 22(6):527-531.
9. Sakuda S., Tamura S., Yamada A., Miyagawa J., Yamamoto K., Kiso S., et al. NF-kappaB activation in non-parenchymal liver cells after partial hepatectomy in rats: possible involvement in expression of heparin-binding epidermal growth factor-like growth factor. J Hepatol 2002, 36(4):527-533.
10. Nagai R., Murray D.B., Metz T.O., Baynes J.W. Chelation: a fundamental mechanism of action of AGE inhibitors, AGE breakers, and other inhibitors of diabetes complications. Diabetes 2012, 61(3):549-559.
11. Negre-Salvayre A., Salvayre R., Auge N., Pamplona R., Portero-Otin M. Hyperglycemia and glycation in diabetic complications. Antioxid Redox Signal 2009, 11(12):3071-3109.
12. Tayebjee M.H., Lip G.Y., MacFadyen R.J. What role do extracellular matrix changes contribute to the cardiovascular disease burden of diabetes mellitus?. Diabet Med 2005, 22(12):1628-1635.
13. Huebschmann A.G., Regensteiner J.G., Vlassara H., Reusch J.E. Diabetes and advanced glycoxidation end products. Diabetes Care 2006, 29(6):1420-1432.
14. Nguyen L.L. Percutaneous treatment of peripheral vascular disease: the role of diabetes and inflammation. J Vasc Surg 2007, 45(Suppl. A):A149-A157.
15. Nugent H.M., Edelman E.R. Tissue engineering therapy for cardiovascular disease. Circ Res 2003, 92(10):1068-1078.
16. Mensah G.A., Catravas J.D., Engelgau M.M., Hooper W.C., Madeddu P., Ryan U.S., et al. Vascular endothelium summary statement VI: research directions for the 21st century. Vascul Pharmacol 2007, 46(5):330-332.
17. Krawiec J.T., Vorp D.A. Adult stem cell-based tissue engineered blood vessels: a review. Biomaterials 2012, 33(12):3388-3400.
18. Peck M., Gebhart D., Dusserre N., McAllister T.N., L'Heureux N. The evolution of vascular tissue engineering and current state of the art. Cells Tissues Organs 2012, 195(1-2):144-158.
19. Isenberg B.C., Williams C., Tranquillo R.T. Small-diameter artificial arteries engineered in vitro. Circ Res 2006, 98(1):25-35.
20. Schoen F.J. Heart valve tissue engineering: quo vadis?. Curr Opin Biotechnol 2011, 22(5):698-705.
21. Tedder M.E., Simionescu A., Chen J., Liao J., Simionescu D.T. Assembly and testing of stem cell-seeded layered collagen constructs for heart valve tissue engineering. Tissue Eng Part A 2011, 17(1-2):25-36.
22. Iyer R.K., Chiu L.L., Reis L.A., Radisic M. Engineered cardiac tissues. Curr Opin Biotechnol 2011, 22(5):706-714.
23. Bursac N., Papadaki M., White J.A., Eisenberg S.R., Vunjak-Novakovic G., Freed L.E. Cultivation in rotating bioreactors promotes maintenance of cardiac myocyte electrophysiology and molecular properties. Tissue Eng 2003, 9(6):1243-1253.
24. Badylak S.F. The extracellular matrix as a biologic scaffold material. Biomaterials 2007, 28(25):3587-3593.
25. Chuang T.H., Stabler C., Simionescu A., Simionescu D.T. Polyphenol-stabilized tubular elastin scaffolds for tissue engineered vascular grafts. Tissue Eng Part A 2009, 15(10):2837-2851.
26. Sierad L.N., Simionescu A., Albers C., Chen J., Maivelett J., Tedder M.E., et al. Design and testing of a pulsatile conditioning system for dynamic endothelialization of polyphenol-stabilized tissue engineered heart valves. Cardiovasc Eng Technol 2010, 1(2):138-153.
27. Barnes C.A., Brison J., Michel R., Brown B.N., Castner D.G., Badylak S.F., et al. The surface molecular functionality of decellularized extracellular matrices. Biomaterials 2011, 32(1):137-143.
28. Jiao T., Clifton R.J., Converse G.L., Hopkins R.A. Measurements of the effects of decellularization on viscoelastic properties of tissues in ovine, baboon, and human heart valves. Tissue Eng Part A 2012, 18(3-4):423-431.
29. Dahan N., Zarbiv G., Sarig U., Karram T., Hoffman A., Machluf M. Porcine small diameter arterial extracellular matrix supports endothelium formation and media remodeling forming a promising vascular engineered biograft. Tissue Eng Part A 2012, 18(3-4):411-422.
30. Cummings I., George S., Kelm J., Schmidt D., Emmert M.Y., Weber B., et al. Tissue-engineered vascular graft remodeling in a growing lamb model: expression of matrix metalloproteinases. Eur J Cardiothorac Surg 2012, 41(1):167-172.
31. Henriksen E.J., Diamond-Stanic M.K., Marchionne E.M. Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic Biol Med 2011, 51(5):993-999.
32. Rees D.A., Alcolado J.C. Animal models of diabetes mellitus. Diabet Med 2005, 22(4):359-370.
33. Styskal J., Van Remmen H., Richardson A., Salmon A.B. Oxidative stress and diabetes: what can we learn about insulin resistance from antioxidant mutant mouse models?. Free Radic Biol Med 2012, 52(1):46-58.
34. Dobreva M.A., Frazier R.A., Mueller-Harvey I., Clifton L.A., Gea A., Green R.J. Binding of pentagalloyl glucose to two globular proteins occurs via multiple surface sites. Biomacromolecules 2011, 12(3):710-715.
35. Tedder M.E., Liao J., Weed B., Stabler C., Zhang H., Simionescu A., et al. Stabilized collagen scaffolds for heart valve tissue engineering. Tissue Eng Part A 2009, 15(6):1257-1268.
36. Isenburg J.C., Karamchandani N.V., Simionescu D.T., Vyavahare N.R. Structural requirements for stabilization of vascular elastin by polyphenolic tannins. Biomaterials 2006, 27(19):3645-3651.
37. Isenburg J.C., Simionescu D.T., Starcher B.C., Vyavahare N.R. Elastin stabilization for treatment of abdominal aortic aneurysms. Circulation 2007, 115(13):1729-1737.
38. Ren Y., Himmeldirk K., Chen X. Synthesis and structure-activity relationship study of antidiabetic penta-O-galloyl-D-glucopyranose and its analogues. J Med Chem 2006, 49(9):2829-2837.
39. Zhang J., Li L., Kim S.H., Hagerman A.E., Lu J. Anti-cancer, anti-diabetic and other pharmacologic and biological activities of penta-galloyl-glucose. Pharm Res 2009, 26(9):2066-2080.
40. Liao J., Joyce E.M., Sacks M.S. Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet. Biomaterials 2008, 29(8):1065-1074.
41. Kasyanov V., Isenburg J., Draughn R.A., Hazard S., Hodde J., Ozolanta I., et al. Tannic acid mimicking dendrimers as small intestine submucosa stabilizing nanomordants. Biomaterials 2006, 27(5):745-751.
42. Basalyga D.M., Simionescu D.T., Xiong W., Baxter B.T., Starcher B.C., Vyavahare N.R. Elastin degradation and calcification in an abdominal aorta injury model: role of matrix metalloproteinases. Circulation 2004, 110(22):3480-3487.
43. Badylak S.F., Freytes D.O., Gilbert T.W. Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 2009, 5(1):1-13.
44. Daley W.P., Peters S.B., Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci 2008, 121(Pt 3):255-264.
45. Reiser K.M. Nonenzymatic glycation of collagen in aging and diabetes. Proc Soc Exp Biol Med 1998, 218(1):23-37.
46. Chen X., Li Y. Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh Migr 2009, 3(4):337-341.
47. La Fleur M., Underwood J.L., Rappolee D.A., Werb Z. Basement membrane and repair of injury to peripheral nerve: defining a potential role for macrophages, matrix metalloproteinases, and tissue inhibitor of metalloproteinases-1. J Exp Med 1996, 184(6):2311-2326.
48. Albera C., Polak J.M., Janes S., Griffiths M.J., Alison M.R., Wright N.A., et al. Repopulation of human pulmonary epithelium by bone marrow cells: a potential means to promote repair. Tissue Eng 2005, 11(7-8):1115-1121.
49. Korossis S.A., Wilcox H.E., Watterson K.G., Kearney J.N., Ingham E., Fisher J. In-vitro assessment of the functional performance of the decellularized intact porcine aortic root. J Heart Valve Dis 2005, 14(3):408-421. discussion 422.
50. Martens F.M., van der Graaf Y., Dijk J.M., Olijhoek J.K., Visseren F.L. Carotid arterial stiffness is marginally higher in the metabolic syndrome and markedly higher in type 2 diabetes mellitus in patients with manifestations of arterial disease. Atherosclerosis 2008, 197(2):646-653.
51. Soldatos G., Jandeleit-Dahm K., Thomson H., Formosa M., D'Orsa K., Calkin A.C., et al. Large artery biomechanics and diastolic dysfunctionin patients with type 2 diabetes. Diabet Med 2011, 28(1):54-60.
52. Webb D.R., Khunti K., Silverman R., Gray L.J., Srinivasan B., Lacy P.S., et al. Impact of metabolic indices on central artery stiffness: independent association of insulin resistance and glucose with aortic pulse wave velocity. Diabetologia 2010, 53(6):1190-1198.
53. Karamitsos T.D., Karvounis H.I., Didangellos T.P., Papadopoulos C.E., Dalamanga E.G., Karamitsos D.T., et al. Usefulness of colour tissue doppler imaging in assessing aortic elastic properties in type 1 diabetic patients. Diabetic Med 2006, 23(11):1201-1206.
54. Rosenhek R., Baumgartner H. Aortic sclerosis, aortic stenosis and lipid-lowering therapy. Expert Rev Cardiovasc Ther 2008, 6(3):385-390.
55. Falcao-Pires I., Hamdani N., Borbely A., Gavina C., Schalkwijk C.G., van der Velden J., et al. Diabetes mellitus worsens diastolic left ventricular dysfunction in aortic stenosis through altered myocardial structure and cardiomyocyte stiffness. Circulation 2011, 124(10):1151-1159.
56. Xiao H., Cai G., Liu M. Fe2+-catalyzed non-enzymatic glycosylation alters collagen conformation during AGE-collagen formation in vitro. Arch Biochem Biophys 2007, 468(2):183-192.
57. Meli M., Granouillet O.R., Reynaud E., Chamson A., Frey J., Perier C. Changes in glycation of fibrous type I collagen during long-term in vitro incubation with glucose. J Protein Chem 2003, 22(6):521-525.
58. Alt N., Carson J.A., Alderson N.L., Wang Y., Nagai R., Henle T., et al. Chemical modification of muscle protein in diabetes. Arch Biochem Biophys 2004, 425(2):200-206.
59. Cervantes-Laurean D., Schramm D.D., Jacobson E.L., Halaweish I., Bruckner G.G., Boissonneault G.A. Inhibition of advanced glycation end product formation on collagen by rutin and its metabolites. J Nutr Biochem 2006, 17(8):531-540.
60. Charlton A.J., Baxter N.J., Khan M.L., Moir A.J., Haslam E., Davies A.P., et al. Polyphenol/peptide binding and precipitation. J Agric Food Chem 2002, 50(6):1593-1601.
61. Galkina E., Ley K. Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol 2006, 17(2):368-377.
62. Sage A.P., Tintut Y., Demer L.L. Regulatory mechanisms in vascular calcification. Nat Rev Cardiol 2010, 7(9):528-536.
63. Bostrom K.I., Rajamannan N.M., Towler D.A. The regulation of valvular and vascular sclerosis by osteogenic morphogens. Circ Res 2011, 109(5):564-577.
64. Edmonds M.E. Medial arterial calcification and diabetes mellitus. Z Kardiol 2000, 89(Suppl. 2):101-104.
65. Lehto S., Niskanen L., Suhonen M., Ronnemaa T., Laakso M. Medial artery calcification. A neglected harbinger of cardiovascular complications in non-insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 1996, 16(8):978-983.
66. Isenburg J.C., Simionescu D.T., Vyavahare N.R. Tannic acid treatment enhances biostability and reduces calcification of glutaraldehyde fixed aortic wall. Biomaterials 2005, 26(11):1237-1245.
67. Katz R., Wong N.D., Kronmal R., Takasu J., Shavelle D.M., Probstfield J.L., et al. Features of the metabolic syndrome and diabetes mellitus as predictors of aortic valve calcification in the multi-ethnic study of atherosclerosis. Circulation 2006, 113(17):2113-2119.
68. Gu X., Masters K.S. Regulation of valvular interstitial cell calcification by adhesive peptide sequences. J Biomed Mater Res A 2010, 93(4):1620-1630.
69. Simionescu A., Schulte J.B., Fercana G., Simionescu D.T. Inflammation in cardiovascular tissue engineering: the challenge to a promise: a minireview. Int J Inflam 2011, 2011958247.