Induced chronic hypoxia negates the pro-angiogenic effect of surface immobilized heparin in a polyurethane porous scaffold

Journal of Biomedical Materials Research - Part A

Volumn 98 A, Issue 4, 2011, Pages 621-628

  Schmidt, Christian ^a,b   Bezuidenhout, Deon ^a   Higham, Lawrence ^a   Zilla, Peter ^a   Davies, Neil H ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

angiogenesis; growth factor; polymeric scaffolds; protein delivery

Indexed keywords

ANGIOGENESIS; CELLULAR GROWTH; CHRONIC HYPOXIAS; ENDOGENOUS GROWTH; GROWTH FACTOR; POLYMERIC SCAFFOLD; POROUS SCAFFOLD; PROTEIN DELIVERY; SURFACE FUNCTIONALITIES; TISSUE REGENERATION; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULARIZATION;

FUNCTIONAL POLYMERS; PEPTIDES; TISSUE;

SCAFFOLDS (BIOLOGY);

HEPARIN; POLYURETHAN; TISSUE SCAFFOLD;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENDOTHELIUM; HYPOXIA; MALE; NONHUMAN; POROSITY; RAT; SURFACE PROPERTY;

ANIMALS; ANOXIA; BIOCOMPATIBLE MATERIALS; HEPARIN; IMPLANTS, EXPERIMENTAL; MALE; MATERIALS TESTING; NEOVASCULARIZATION, PHYSIOLOGIC; POLYURETHANES; POROSITY; RATS; RATS, WISTAR; SURFACE PROPERTIES; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80051474975     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.33150     Document Type: Article

References (47)

1. Williams DF,. To engineer is to create: The link between engineering and regeneration. Trends Biotechnol 2006; 24: 4-8. (Pubitemid 43017744)
2. Lee H, Cusick R, Browne F, Ho KT, Ma P, Utsunomiya H, Langer R, Vacanti J,. Local delivery of basic fibroblast growth factor increases both angiogenesis and engraftment of hepatocytes in tissue-engineered polymer devices. Transplantation 2002; 73: 1589-1593. (Pubitemid 34568670)
3. Patel Z, Mikos A,. Angiogenesis with biomaterial-based drug- and cell-delivery systems. J Biomater Sci Polym Ed 2004; 15: 701-726. (Pubitemid 38923490)
4. Bezuidenhout D, Davies N, Black M, Schmidt C, Oosthuysen A, Zilla P,. Covalent surface heparinization potentiates porous polyurethane scaffold vascularization. J Biomater Appl 2010; 24: 401-418.
5. Davies N, Dobner S, Bezuidenhout D, Schmidt C, Beck M, Zisch AH, Zilla P,. The dosage dependence of VEGF stimulation on scaffold neovascularisation. Biomaterials 2008; 29: 3531-3238.
6. Steffens G, Yao C, Prevel P, Markowicz M, Schenck P, Noah E, Pallua N,. Modulation of angiogenic potential of collagen matrices by covalent incorporation of heparin and loading with vascular endothelial growth factor. Tissue Eng 2004; 10: 1502-1509. (Pubitemid 39557853)
7. Nillesen ST, Geutjes PJ, Wismans R, Schalkwijk J, Daamen WF, van Kuppevelt TH,. Increased angiogenesis and blood vessel maturation in acellular collagen-heparin scaffolds containing both FGF2 and VEGF. Biomaterials 2007; 28: 1123-1131. (Pubitemid 44809425)
8. Knighton D, Hunt T, Scheuenstuhl H, Halliday B, Werb Z, Banda M,. Oxygen tension regulates the expression of angiogenesis factor by macrophages. Science 1983; 221: 1283-1285. (Pubitemid 13001278)
9. Chang N, Goodson WR, Gottrup F, Hunt T,. Direct measurement of wound and tissue oxygen tension in postoperative patients. Ann Surg 1983; 197: 470-478. (Pubitemid 13112792)
10. Kerger H, Groth G, Kalenka A, Vajkoczy P, Tsai AG, Intaglietta M,. pO(2) measurements by phosphorescence quenching: Characteristics and applications of an automated system. Microvasc Res 2003; 65: 32-38. (Pubitemid 36263288)
11. Shweiki D, Itin A, Soffer D, Keshet E,. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992; 359: 843-845.
12. Kuwabara K, Ogawa S, Matsumoto M, Koga S, Clauss M, Pinsky D, Lyn P, Leavy J, Witte L, Joseph-Silverstein J, Furie MB, Torcia G, Cozzolino F, Kamada T, Stern DM,. Hypoxia-mediated induction of acidic/basic fibroblast growth factor and platelet-derived growth factor in mononuclear phagocytes stimulates growth of hypoxic endothelial cells. Proc Natl Acad Sci U S A 1995; 92: 4606-4610.
13. Kourembanas S, Hannan R, Faller D,. Oxygen tension regulates the expression of the platelet-derived growth factor-B chain gene in human endothelial cells. J Clin Invest 1990; 86: 670-674. (Pubitemid 20271905)
14. Krikun G, Schatz F, Finlay T, Kadner S, Mesia A, Gerrets R, Lockwood C,. Expression of angiopoietin-2 by human endometrial endothelial cells: Regulation by hypoxia and inflammation. Biochem Biophys Res Commun 2000; 275: 159-163. (Pubitemid 30663645)
15. Mandriota S, Pepper M,. Regulation of angiopoietin-2 mRNA levels in bovine microvascular endothelial cells by cytokines and hypoxia. Circ Res 1998; 83: 852-859. (Pubitemid 28489082)
16. Marti H, Risau W,. Systemic hypoxia changes the organ-specific distribution of vascular endothelial growth factor and its receptors. Proc Natl Acad Sci U S A 1998; 95: 15809-15814. (Pubitemid 29018782)
17. Harik S, Hritz M, LaManna J,. Hypoxia-induced brain angiogenesis in the adult rat. J Physiol 1995; 485 (Pt 2): 525-530.
18. Boero J, Ascher J, Arregui A, Rovainen C, Woolsey T,. Increased brain capillaries in chronic hypoxia. J Appl Physiol 1999; 86: 1211-1219. (Pubitemid 29172154)
19. Smith K, Marshall J,. Physiological adjustments and arteriolar remodelling within skeletal muscle during acclimation to chronic hypoxia in the rat. J Physiol 1999; 521 (Pt 1): 261-272.
20. Howell K, Preston R, McLoughlin P, Chronic hypoxia causes angiogenesis in addition to remodelling in the adult rat pulmonary circulation. J Physiol 2003; 547 (Pt 1): 133-145. (Pubitemid 36285169)
21. Taipale J, Keski-Oja J,. Growth factors in the extracellular matrix. FASEB J 1997; 11: 51-59. (Pubitemid 27076324)
22. Tayalia P, Mooney DJ,. Controlled growth factor delivery for tissue engineering. Adv Mater 2009; 21: 3269-3285.
23. Nillesen ST, Geutjes PJ, Wismans R, Schalkwijk J, Daamen WF, van Kuppevelt TH,. Increased angiogenesis in acellular scaffolds by combined release of FGF2 and VEGF. J Control Release 2006; 116: e88-e90.
24. Ratcliffe A,. Tissue engineering of vascular grafts. Matrix Biol 2000; 19: 353-357. (Pubitemid 30665659)
25. Grad S, Kupcsik L, Gorna K, Gogolewski S, Alini M,. The use of biodegradable polyurethane scaffolds for cartilage tissue engineering: Potential and limitations. Biomaterials 2003; 24: 5163-5171. (Pubitemid 37279148)
26. Bezuidenhout D, Davies N, Zilla P,. Effect of well defined dodecahedral porosity on inflammation and angiogenesis. ASAIO J 2002; 48: 465-471.
27. Gamble M, Wilson I,. The hemantoxylins and eosin. In:, Bankroft JD, Gamble M, editors. Theory and Practice of Histological Techniques. London: Churchill Livingstone; 2002. p 125-139.
28. Beckstead J,. A simple technique for preservation of fixation-sensitive antigens in paraffin-embedded tissues. J Histochem Cytochem 1994; 42: 1127-1134. (Pubitemid 24226340)
29. LaManna J, Vendel L, Farrell R,. Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 1992; 72: 2238-2243.
30. Lakatta EG, Levy D,. Arterial and cardiac aging: Major shareholders in cardiovascular disease enterprises: Part I: Aging arteries: A "set up" for vascular disease. Circulation 2003; 107: 139-146. (Pubitemid 36070946)
31. Luscher TF, Creager MA, Beckman JA, Cosentino F,. Diabetes and vascular disease: Pathophysiology, clinical consequences, and medical therapy: Part II. Circulation 2003; 108: 1655-1661. (Pubitemid 37187795)
32. Niinikoski J,. Effect of oxygen supply on wound healing and formation of experimental granulation tissue. Acta Physiol Scand Suppl 1969; 334: 1-72.
33. Fujita M, Ishihara M, Simizu M, Obara K, Ishizuka T, Saito Y, Yura H, Morimoto Y, Takase B, Matsui T, Kikuchi M, Maehara T,. Vascularization in vivo caused by the controlled release of fibroblast growth factor-2 from an injectable chitosan/non-anticoagulant heparin hydrogel. Biomaterials 2004; 25: 699-706. (Pubitemid 37357283)
34. Ishihara M, Obara K, Ishizuka T, Fujita M, Sato M, Masuoka K, Saito Y, Yura H, Matsui T, Hattori H, Kikuchi M, Kurita A,. Controlled release of fibroblast growth factors and heparin from photocrosslinked chitosan hydrogels and subsequent effect on in vivo vascularization. J Biomed Mater Res 2003; 64A: 551-559. (Pubitemid 37522496)
35. Sakiyama-ES, Hubbell J,. Development of fibrin derivatives for controlled release of heparin-binding growth factors. J Control Release 2000; 65: 389-402. (Pubitemid 30122941)
36. Tanihara M, Suzuki Y, Yamamoto E, Noguchi A, Mizushima Y,. Sustained release of basic fibroblast growth factor and angiogenesis in a novel covalently crosslinked gel of heparin and alginate. J Biomed Mater Res 2001; 56: 216-221. (Pubitemid 32520696)
37. Doi K, Matsuda T,. Enhanced vascularization in a microporous polyurethane graft impregnated with basic fibroblast growth factor and heparin. J Biomed Mater Res 1997; 34: 361-370. (Pubitemid 27097806)
38. Soker S, Goldstaub D, Svahn C, Vlodavsky I, Levi B, Neufeld G,. Variations in the size and sulfation of heparin modulate the effect of heparin on the binding of VEGF165 to its receptors. Biochem Biophys Res Commun 1994; 203: 1339-1347.
39. Kan M, Wang F, Xu J, Crabb J, Hou J, McKeehan W,. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 1993; 259: 1918-1921. (Pubitemid 23124467)
40. Marikovsky M, Breuing K, Liu P, Eriksson E, Higashiyama S, Farber P, Abraham J, Klagsbrun M,. Appearance of heparin-binding EGF-like growth factor in wound fluid as a response to injury. Proc Natl Acad Sci U S A 1993; 90: 3889-3893. (Pubitemid 23134131)
41. McCaffrey T, Falcone D, Vicente D, Du B, Consigli S, Borth W,. Protection of transforming growth factor-beta 1 activity by heparin and fucoidan. J Cell Physiol 1994; 159: 51-59. (Pubitemid 24234576)
42. Simons M, Horowitz A,. Syndecan-4-mediated signalling. Cell Signal 2001; 13: 855-862. (Pubitemid 33139787)
43. Ashikari-Hada S, Habuchi H, Kariya Y, Kimata K,. Heparin regulates vascular endothelial growth factor165-dependent mitogenic activity, tube formation, and its receptor phosphorylation of human endothelial cells. Comparison of the effects of heparin and modified heparins. J Biol Chem 2005; 280: 31508-31515. (Pubitemid 41291893)
44. Folkman J, Shing Y,. Control of angiogenesis by heparin and other sulfated polysaccharides. Adv Exp Med Biol 1992; 313: 355-364.
45. Ruscher K, Isaev N, Trendelenburg G, Weih M, Iurato L, Meisel A, Dirnagl U,. Induction of hypoxia inducible factor 1 by oxygen glucose deprivation is attenuated by hypoxic preconditioning in rat cultured neurons. Neurosci Lett 1998; 254: 117-120. (Pubitemid 28454846)
46. Levy A,. A cellular paradigm for the failure to increase vascular endothelial growth factor in chronically hypoxic states. Coron Artery Dis 1999; 10: 427-430. (Pubitemid 29419560)
47. Liu Q, Berchner-Pfannschmidt U, Moller U, Brecht M, Wotzlaw C, Acker H, Jungermann K, Kietzmann T,. A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc Natl Acad Sci U S A 2004; 101: 4302-4307. (Pubitemid 38405924)