Composite fibrin scaffolds increase mechanical strength and preserve contractility of tissue engineered blood vessels

Pharmaceutical Research

Volumn 25, Issue 5, 2008, Pages 1212-1221

  Yao, Lan ^a   Liu, Jinyu ^a   Andreadis, Stelios T ^a,b  

^a the State University of New York   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cardiovascular tissue engineering; Composite materials; Contractility; Fibrin; Smooth muscle

Indexed keywords

FIBRIN; FIBRINOGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BLOOD VESSEL; BLOOD VESSEL REACTIVITY; CELL FREE SYSTEM; CELL FUNCTION; CONTROLLED STUDY; HYDROGEL; LAMB; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; STRENGTH; TENSILE STRENGTH; TISSUE ENGINEERING;

ACTINS; ANIMALS; ANIMALS, NEWBORN; BIOMECHANICS; BLOOD VESSEL PROSTHESIS; CROSS-LINKING REAGENTS; CYTOSKELETON; FIBRIN; FIBRINOGEN; HYDROGELS; IMMUNOHISTOCHEMISTRY; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; SHEEP; TENSILE STRENGTH; TISSUE SCAFFOLDS;

EID: 42049123678     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-007-9499-6     Document Type: Article

References (60)

1. M. Gaudino, C. Cellini, C. Pragliola, C. Trani, F. Burzotta, G. Schiavoni, G. Nasso, and G. Possati. Arterial versus venous bypass grafts in patients with in-stent restenosis. Circulation 112:I265-269 (2005).
2. J. K. Drury, T. R. Ashton, J. D. Cunningham, R. Maini, and J. G. Pollock. Experimental and clinical experience with a gelatin impregnated Dacron prosthesis. Ann. Chir. Vasc 1:542-547 (1987).
3. M. Pasic, W. Muller-Glauser, B. Odermatt, M. Lachat, B. Seifert, and M. Turina. Seeding with omental cells prevents late neointimal hyperplasia in small-diameter Dacron grafts. Circulation 92:2605-2616 (1995).
4. M. Deutsch, J. Meinhart, T. Fischlein, P. Preiss, and P. Zilla. Clinical autologous in vitro endothelialization of infrainguinal ePTFE grafts in 100 patients: a 9-year experience. Surgery 126:847-855 (1999).
5. T. Huynh, G. Abraham, J. Murray, K. Brockbank, P. O. Hagen, and S. Sullivan. Remodeling of an acellular collagen graft into a physiologically responsive neovessel. Nat. Biotechnol 17:1083-1086 (1999).
6. A. Bader, G. Steinhoff, K. Strobl, T. Schilling, G. Brandes, H. Mertsching, D. Tsikas, J. Froelich, and A. Haverich. Engineering of human vascular aortic tissue based on a xenogeneic starter matrix. Transplantation 70:7-14 (2000).
7. S. Kaushal, G. E. Amiel, K. J. Guleserian, O. M. Shapira, T. Perry, F. W. Sutherland, E. Rabkin, A. M. Moran, F. J. Schoen, A. Atala, S. Soker, J. Bischoff, and J. E. Mayer, Jr. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo.[comment]. Nat. Med 7:1035-1040 (2001).
8. N. L'Heureux, S. Paquet, R. Labbe, L. Germain, and F. A. Auger. A completely biological tissue-engineered human blood vessel. [comment]. FASEB J 12:47-56 (1998).
9. N. L'Heureux, J. C. Stoclet, F. A. Auger, G. J. Lagaud, L. Germain, and R. Andriantsitohaina. A human tissue-engineered vascular media: a new model for pharmacological studies of contractile responses. FASEB J 15:515-524 (2001).
10. L. E. Niklason, J. Gao, W. M. Abbott, K. K. Hirschi, S. Houser, R. Marini, and R. Langer. Functional arteries grown in vitro. Science 284:489-493 (1999).
11. L. E. Niklason, W. Abbott, J. Gao, B. Klagges, K. K. Hirschi, K. Ulubayram, N. Conroy, R. Jones, A. Vasanawala, S. Sanzgiri, and R. Langer. Morphologic and mechanical characteristics of engineered bovine arteries. J. Vasc. Surg 33:628-638 (2001).
12. S. P. Higgins, A. K. Solan, and L. E. Niklason. Effects of polyglycolic acid on porcine smooth muscle cell growth and differentiation. J. Biomed. Mater. Res 67A:295-302 (2003).
13. V. H. Barocas, T. S. Girton, and R. T. Tranquillo. Engineered alignment in media equivalents: magnetic prealignment and mandrel compaction. J. Biomech. Eng 120:660-666 (1998).
14. D. Seliktar, R. A. Black, R. P. Vito, and R. M. Nerem. Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann. Biomed. Eng 28:351-362 (2000).
15. D. Seliktar, R. M. Nerem, and Z. S. Galis. The role of matrix metalloproteinase-2 in the remodeling of cell-seeded vascular constructs subjected to cyclic strain. Ann Biomed Eng 29:923-934 (2001).
16. D. Seliktar, R. M. Nerem, and Z. S. Galis. Mechanical strain-stimulated remodeling of tissue-engineered blood vessel constructs. Tissue Eng 9:657-666 (2003).
17. J. P. Stegemann, and R. M. Nerem. Altered response of vascular smooth muscle cells to exogenous biochemical stimulation in two- and three-dimensional culture. Exp. Cell Res 283:146-155 (2003).
18. M. Thie, W. Schlumberger, R. Semich, J. Rauterberg, and H. Robenek. Aortic smooth muscle cells in collagen lattice culture: effects on ultrastructure, proliferation and collagen synthesis. Eur. J. Cell Biol 55:295-304 (1991).
19. R. A. Clark, L. D. Nielsen, M. P. Welch, and J. M. McPherson. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J. Cell Sci 108:1251-1261 (1995).
20. T. L. Tuan, A. Song, S. Chang, S. Younai, and M. E. Nimni. In vitro fibroplasia: matrix contraction, cell growth, and collagen production of fibroblasts cultured in fibrin gels. Exp. Cell Res 223:127-134 (1996).
21. E. D. Grassl, T. R. Oegema, and R. T. Tranquillo. A fibrin-based arterial media equivalent. J. Biomed. Mater. Res 66A:550-561 (2003).
22. J. L. Longand, and R. T. Tranquillo. Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol 22:339-350 (2003).
23. D. D. Swartz, J. A. Russell, and S. T. Andreadis. Engineering of fibrin-based functional and implantable small-diameter blood vessels. Am. J. Physiol. Heart Circ. Physiol 288:H1451-H1460 (2005)Epub 2004 Oct 1414.
24. B. C. Isenbergand, and R. T. Tranquillo. Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann. Biomed. Eng 31:937-949 (2003).
25. T. S. Girton, T. R. Oegema, and R. T. Tranquillo. Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering. J. Biomed. Mater. Res 46:87-92 (1999).
26. T. S. Girton, T. R. Oegema, E. D. Grassl, B. C. Isenberg, and R. T. Tranquillo. Mechanisms of stiffening and strengthening in media-equivalents fabricated using glycation. J. Biomech. Eng 122:216-223 (2000).
27. K. Ishibashiand, and T. Matsuda. Reconstruction of a hybrid vascular graft hierarchically layered with three cell types. Asaio. J 40:M284-290 (1994).
28. T. Matsudaand, and H. Miwa. A hybrid vascular model biomimicking the hierarchic structure of arterial wall: neointimal stability and neoarterial regeneration process under arterial circulation. J. Thorac. Cardiovasc. Surg 110:988-997 (1995).
29. J. D. Berglund, M. M. Mohseni, R. M. Nerem, and A. Sambanis. A biological hybrid model for collagen-based tissue engineered vascular constructs. Biomaterials 24:1241-1254 (2003).
30. D. J. Geer, D. D. Swartz, and S. T. Andreadis. In vivo model of wound healing based on transplanted tissue-engineered skin. Tissue Eng 10:1006-1017 (2004).
31. L. Yao, D. D. Swartz, S. F. Gugino, J. A. Russell, and S. T. Andreadis. Fibrin-based tissue-engineered blood vessels: differential effects of biomaterial and culture parameters on mechanical strength and vascular reactivity. Tissue Eng 11:991-1003 (2005).
32. D. J. Geer, D. D. Swartz, and S. T. Andreadis. Biomimetic delivery of keratinocyte growth factor upon cellular demand for accelerated wound healing in vitro and in vivo. Am. J. Pathol 167:1575-1586 (2005).
33. C. B. Herbert, C. Nagaswami, G. D. Bittner, J. A. Hubbell, and J. W. Weisel. Effects of fibrin micromorphology on neurite growth from dorsal root ganglia cultured in three-dimensional fibrin gels. J. Biomed. Mater. Res 40:551-559 (1998).
34. J. D. Smith, N. Davies, A. I. Willis, B. E. Sumpio, and P. Zilla. Cyclic stretch induces the expression of vascular endothelial growth factor in vascular smooth muscle cells. Endothelium 8:41-48 (2001).
35. W. Li, Q. Chen, I. Mills, and B. E. Sumpio. Involvement of S6 kinase and p38 mitogen activated protein kinase pathways in strain-induced alignment and proliferation of bovine aortic smooth muscle cells. J. Cell Physiol 195:202-209 (2003).
36. Q. Chen, W. Li, Z. Quan, and B. E. Sumpio. Modulation of vascular smooth muscle cell alignment by cyclic strain is dependent on reactive oxygen species and P38 mitogen-activated protein kinase. J. Vasc. Surg 37:660-668 (2003).
37. B. S. Kim, J. Nikolovski, J. Bonadio, and D. J. Mooney. Cyclic mechanical strain regulates the development of engineered smooth muscle tissue. Nat. Biotechnol 17:979-983 (1999).
38. J. Nikolovski, B. S. Kim, and D. J. Mooney. Cyclic strain inhibits switching of smooth muscle cells to an osteoblast-like phenotype. FASEB J 17:455-457 (2003)Epub 2003 Jan 2002.
39. B. S. Kim, J. Nikolovski, J. Bonadio, E. Smiley, and D. J. Mooney. Engineered smooth muscle tissues: regulating cell phenotype with the scaffold. Exp. Cell Res 251:318-328 (1999).
40. T. Shin'oka, Y. Imai, and Y. Ikada. Transplantation of a tissue-engineered pulmonary artery. N. England J. Med 344:532-533 (2001).
41. M. Watanabe, T. Shin'oka, S. Tohyama, N. Hibino, T. Konuma, G. Matsumura, Y. Kosaka, T. Ishida, Y. Imai, M. Yamakawa, Y. Ikada, and S. Morita. Tissue-engineered vascular autograft: inferior vena cava replacement in a dog model. Tissue Eng 7:429-439 (2001).
42. S. H. Lee, B. S. Kim, S. H. Kim, S. W. Choi, S. I. Jeong, I. K. Kwon, S. W. Kang, J. Nikolovski, D. J. Mooney, Y. K. Han, and Y. H. Kim. Elastic biodegradable poly(glycolide-co-caprolactone) scaffold for tissue engineering. J. Biomed. Mater. Res. A 66:29-37 (2003).
43. S. P. Hoerstrup, A. Kadner, C. Breymann, C. F. Maurus, C. I. Guenter, R. Sodian, J. F. Visjager, G. Zund, and M. I. Turina. Living, autologous pulmonary artery conduits tissue engineered from human umbilical cord cells. Ann. Thorac. Surg 74:46-52 (2002)discussion 52.
44. M. C. Wake, P. K. Gupta, and A. G. Mikos. Fabrication of pliable biodegradable polymer foams to engineer soft tissues. Cell Transplant 5:465-473 (1996).
45. M. E. Nimni, D. Cheung, B. Strates, M. Kodama, and K. Sheikh. Chemically modified collagen: a natural biomaterial for tissue replacement. J. Biomed. Mater. Res 21:741-771 (1987).
46. L.H. Olde Damink, P.J. Dijkstra, M.J. van Luyn, P.B. van Wachem, P. Nieuwenhuis, and J. Feijen. Cross-linking of dermal sheep collagen using a water-soluble carbodiimide. Biomaterials 17:765-773 (1996).
47. P. B. van Wachem, M. J. van Luyn, L. H. Olde Damink, P. J. Dijkstra, J. Feijen, and P. Nieuwenhuis. Biocompatibility and tissue regenerating capacity of crosslinked dermal sheep collagen. J. Biomed. Mater. Res 28:353-363 (1994).
48. M. J. van Luyn, P. B. van Wachem, L. O. Damink, P. J. Dijkstra, J. Feijen, and P. Nieuwenhuis. Relations between in vitro cytotoxicity and crosslinked dermal sheep collagens. J. Biomed. Mater Res 26:1091-1110 (1992).
49. H. F. Dvorak, V. S. Harvey, P. Estrella, L. F. Brown, J. McDonagh, and A. M. Dvorak. Fibrin containing gels induce angiogenesis. Implications for tumor stroma generation and wound healing. Lab. Invest 57:673-686 (1987).
50. A. Takei, Y. Tashiro, Y. Nakashima, and K. Sueishi. Effects of fibrin on the angiogenesis in vitro of bovine endothelial cells in collagen gel. In Vitro Cell Dev. Biol. Anim 31:467-472 (1995).
51. P. Hudlett, A. Neuville, A. Miternique, C. Griffon, D. Weltin, and D. Stephan. Angiogenesis and arteriogenesis are increased in fibrin gel chambers implanted in prehypertensive spontaneously hypertensive rats. J. Hypertens 23:1559-1564 (2005).
52. L. Martineauand, and C. J. Doillon. Angiogenic response of endothelial cells seeded dispersed versus on beads in fibrin gels. Angiogenesis 10:269-277 (2007).
53. J. C. Schense, J. Bloch, P. Aebischer, and J. A. Hubbell. Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension. Nat. Biotechnol 18:415-419 (2000).
54. S. E. Sakiyama-Elbertand, and J. Hubbell. Development of fibrin derivatives for controlled release of heparin- binding growth factors. J. Control Release 65:389-402 (2000).
55. A. H. Zisch, U. Schenk, J. C. Schense, S. E. Sakiyama-Elbert, and J. A. Hubbell. Covalently conjugated VEGF-fibrin matrices for endothelialization. J. Control Release 72:101-113 (2001).
56. A. H. Zisch, M. P. Lutolf, M. Ehrbar, G. P. Raeber, S. C. Rizzi, N. Davies, H. Schmokel, D. Bezuidenhout, V. Djonov, P. Zilla, and J. A. Hubbell. Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth. FASEB J 17:2260-2262 (2003).
57. S. E. Sakiyama-Elbertand, and J. A. Hubbell. Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix. J. Control Release 69:149-158 (2000).
58. S. L. Brown, C. H. Lundgren, T. Nordt, and S. Fujii. Stimulation of migration of human aortic smooth muscle cells by vitronectin: implications for atherosclerosis. Cardiovasc. Res 28:1815-1820 (1994).
59. J. I. Jones, T. Prevette, A. Gockerman, and D. R. Clemmons. Ligand occupancy of the alpha-V-beta3 integrin is necessary for smooth muscle cells to migrate in response to insulin-like growth factor. Proc. Natl. Acad. Sci. USA 93:2482-2487 (1996).
60. J. J. Rossand, and R. T. Tranquillo. ECM gene expression correlates with in vitro tissue growth and development in fibrin gel remodeled by neonatal smooth muscle cells. Matrix Biol 22:477-490 (2003).