From scrawny to brawny: The quest for neomusculogenesis; smart surfaces and scaffolds for muscle tissue engineering

Expert Review of Medical Devices

Volumn 4, Issue 5, 2007, Pages 709-728

  Rowlands, Andrew S ^a   Hudson, James E ^a   Cooper White, Justin J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cardiomyocyte; Cell stimulation; Cell surface interaction; Muscle; Myoblast; Scaffolds; Tissue engineering

Indexed keywords

ACTIN; ALGINIC ACID; ANTIINFLAMMATORY AGENT; BIOMATERIAL; BONE MORPHOGENETIC PROTEIN 2; CHITOSAN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGENASE; CORTICOSTEROID; DYSTROPHIN; ELASTIN; FIBRONECTIN; GELATIN; GLYPICAN; HYALURONIC ACID; LAMININ 1; MACROGOL; MATRIGEL; MEROSIN; METHOTREXATE; MYOSIN; POLYCAPROLACTONE; POLYGLACTIN; POLYGLYCOLIC ACID; POLYLACTIDE; PROTEOGLYCAN; SARCOGLYCAN; UNINDEXED DRUG;

ACTIN FILAMENT; ANTINEOPLASTIC ACTIVITY; ARTIFICIAL HEART; CANCER; CANCER INHIBITION; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; HEART INFARCTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; MUSCLE BLOOD VESSEL; MUSCLE CONTRACTILITY; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE LENGTH; MUSCLE REGENERATION; MUSCLE STRENGTH; MUSCLE TRANSPLANTATION; MUSCLE TRANSPOSITION; MYOPATHY; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; QUALITY OF LIFE; REVIEW; SKULL DEFECT; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; TISSUE ENGINEERING;

ANIMALS; BIOMECHANICS; ELECTROPHYSIOLOGY; HUMANS; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLES; POLYMERS; RATS; SURFACE PROPERTIES; TISSUE ENGINEERING;

EID: 34848882149     PISSN: 17434440     EISSN: 17452422     Source Type: Journal    
DOI: 10.1586/17434440.4.5.709     Document Type: Review

References (225)

1. Echeverri K, Tanaka EM. Mechanisms of muscle dedifferentiation during regeneration. Semin. Cell Dev. Biol. 13(5), 353-360 (2002).
2. Baek C-H, Ko Y-J. Characteristics of tissue-engineered cartilage on macroporous biodegradable PLGA scaffold. Laryngoscope 116(10), 1829-1834 (2006).
3. Cao Y, Mitchell G, Messina A et al. The influence of architecture on degradation and tissue ingrowth into three-dimensional poly(lactic-co-glycolic acid) scaffolds in vitro and in vivo. Biomaterials 27(14), 2854-2864 (2006).
4. Douglas T, Heinemann S, Mietrach C et al. Interactions of collagen types I and II with chondroitin sulfates A-C and their effect on osteoblast adhesion. Biomacromolecules 8(4), 1085-1092 (2007).
5. Tjia JS, Aneskievich BJ, Moghe PV. Substrate-adsorbed collagen and cell secreted fibronectin concertedly induce cell migration on poly(lactide-glycolide) substrates. Biomaterials 20(23-24), 2223-2233 (1999).
6. Bhati RS, Mukherjee DP, McCarthy KJ et al. The growth of chondrocytes into a fibronectin-coated biodegradable scaffold. J. Biomed. Mater. Res. 56(1), 74-82 (2001).
7. Yu X, Bellamkonda RV. Tissue-engineered scaffolds are effective alternatives to autografts for bridging peripheral nerve gaps. Tissue Eng. 9(3), 421-430 (2003).
8. Hubbell JA. Bioactive biomaterials. Curr. Opin. Biotechnol. 10(2), 123-129 (1999).
9. Ralston E, Lu Z, Biscocho N et al. Blood vessels and desmin control the positioning of nuclei in skeletal muscle fibers. J. Cell. Physiol. 209(3), 874-882 (2006).
10. Osses N, Brandan E. ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. Am. J. Physiol. Cell. Physiol. 282(2), C383-C394 (2002).
11. Sewry CA, Muntoi F. Inherited disorders of the extracellular matrix. Curr. Opin. Neurol. 12(5), 519-526 (1999).
12. Campbell KP, Kahl SD. Association of dystrophin and an integral membrane glycoprotein. Nature 338(6212), 259-262 (1989).
13. Prior TW, Bartolo C, Pearl DK et al. Spectrum of small mutations in the dystrophin coding region. Am. J. Hum. Genet. 57(1), 22-33 (1995).
14. Chan Y-M, Bonnemann CG, Lidov HGW, Kunkel LM. Molecular organization of sarcoglycan complex in mouse myotubes in culture. J. Cell Biol. 143(7), 2033-2044 (1998).
15. 12 cells: biophysical, biochemical, and immunocytochemical properties. Am. J. Physiol. Cell Physiol. 266(6). C1795-C1802 (1994).
16. Leite-Moreira AF. Current perspectives in diastolic dysfunction and diastolic heart failure. Heart 92(5), 712-718 (2006).
17. Beltrami AP, Barlucchi L, Torella D et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114(6), 763-776 (2003).
18. Smith RR, Barile L, Cho HC et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7), 896-908 (2007).
19. Zimmermann WH, Fink C, Kralisch D et al. Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol. Bioeng. 68(1), 106-114 (2000).
20. Claycomb WC, Nicholas A. Lanson J et al. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc. Natl Acad. Sci. USA 95, 2979-2984 (1998).
21. Kielty CM. Elastic fibres in health and disease. Expert Rev. Mol. Med. 8, 1-23 (2006).
22. Stegemann JP, Hong H, Nerem RM. Mechanical, biochemical, and extracellular matrix effects on vascular smooth muscle cell phenotype. J. Appl. Physiol. 98, 2321-2327 (2005).
23. Dekkers BGJ, Schaafsma D, Nelemans SA, Zaagsma J, Meurs H. Extracellular matrix proteins differentially regulate airway smooth muscle phenotype and function. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L1405-L1413 (2007).
24. Hayward IP, Bridle KR, Campbell GR, Underwood PA, Campbell JH. Effect of extracellular matrix proteins on vascular smooth muscle cell phenotype. Cell Biol. Int. 19(10), 839-846 (1995).
25. Moiseeva EP, Adhesion receptors of vascular smooth muscle cells and their functions. Cardiovasc. Res. 52(3), 372-386 (2001).
26. Firulli AB, Han D, Kelly-Roloff L et al. A comparative molecular analysis of four rat smooth muscle cell lines. In Vitro Cell. Dev. Biol. Anim. 34(3), 217-226 (1998).
27. Martini FH. Fundamentals of Anatomy and Physiology. Benjamin Cummings, CA, USA 683-777 (2004).
28. Harris DE, Warshaw DM. Length vs. active force relationship in single isolated smooth muscle cells. Am. J. Physiol. Cell Physiol. 260(5). C1104-C1112 (1991).
29. Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA. Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J. Biomech. 34(12), 1545-1553 (2001).
30. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 126(4), 677-689 (2006).
31. Gordon AM, Huxley AF, Julian FJ. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184(1). 170-192 (1966).
32. Dobrin PB. Mechanical properties of arterises. Physiol. Rev. 58(2), 397-460 (1978).
33. Fish D, Orenstein J, Bloom S. Passive stiffness of isolated cardiac and skeletal myocytes in the hamster. Circ. Res. 54(3). 267-276 (1984).
34. Dillon PF, Murphy RA. High force development and crossbridge attachment in smooth muscle from swine carotid arteries. Circ. Res. 50(6). 799-804 (1982).
35. Zimmermann WH, Didie M, Doker S et al. Heart muscle engineering: an update on cardiac muscle replacement therapy, Cardiovasc. Res. 71(3), 419-429 (2006).
36. Chamley-Campbell J, Campbell GR, Ross R. The smooth muscle cell in culture. Physiol. Rev. 59(1), 1-61 (1979).
37. Olivetti G, Melissari M, Marchetti G, Anversa P. Quantitative structural changes of the rat thoracic aorta in early spontaneous hypertension. Tissue compositiom and hypertrophy and hyperplasia of smooth muscle cells. Circ. Res. 51(1), 19-26 (1982).
38. Cieslar J, Huang M-T, Dobson GP. Tissue spaces in rat heart, liver, and skeletal muscle in vivo Am. J. Physiol Regul. Integr. Comp. Physiol. 275(5), R1530-R1536 (1998).
39. Bers DM. Excitation - Contraction Coupling and Cardiac Contractile Force (2nd Edition). Kluwer Academic Publishers, Dordrecht, The Netherlands (2001).
40. Heistad DD, Marcus ML, Law EG et al. Regulation of blood flow to the aortic media in dogs. J. Clin. Invest. 62(1), 133-140 (1978).
41. Delp MD, Laughlin MH. Regulation of skeletal muscle perfusion during exercise. Acta Physiol. Scand. 162(3), 411-419 (1998).
42. Bulbring E. Measurements of oxygen consumption in smooth muscle. J. Physiol. 122(1), 111-134 (1953).
43. 2 consumption rate in vascular smooth muscle. Am. J. Physiol. 228(3), 915-922 (1975).
44. Andersen P, Saitin B. Maximal perfusion of skeletal muscle in man. J. Physiol. 366(1), 233-249 (1985).
45. Allen B, Rosenkranz E, Buckberg G et al. High oxygen requirements of dyskinetic cardiac muscle. J. Thorac. Cardiovasc. Surg. 92(3), 543-552 (1986).
46. Galili O, Herrmann J, Woodrum J et al. Adventitial vasa vasorum heterogeneity among different vascular beds. J. Vasc. Surg. 40(3), 529-535 (2004).
47. Hudlicka O, Brown M, Egginton S. Angiogenesis in skeletal and cardiac muscle. Physiol. Rev. 72(2), 369-417 (1992).
48. Hara Y, Kubota M, Szurszewski JH. Electrophysiology of smooth muscle of the small intestine of some mammals. J. Physiol. 372(1), 501-520 (1986).
49. Eschenhagen T, Fink C, Remmers U et al. Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J. 11(8), 683-694 (1997).
50. Itabashi Y, Miyoshi S, Yuasa S et al. Analysis of the electrophysiological properties and arrhythmias in directly contacted skeletal and cardiac muscle cell sheets. Cardiovasc. Res. 67(3), 561-570 (2005).
51. Ratner RD. Reducing capsular thickness and enhancing angiogenesis around implant drug release systems. J. Control. Release 78(1-3), 211-218 (2002).
52. Kidane A, Lantz GC, Jo S, Park K. Surface modification with PEO-containing triblock copolymer for improved biocompatibility: in vitro and ex vivo studies. J. Biomater. Sci. 10(10), 1089-1105 (1999).
53. Kingshott P, McArthur S, Thissen H, Castner DG, Griesser HJ. Ultrasensitive probing of the protein resistance of PEG surfaces by secondary ion mass spectrometry. Biomaterials 23(24), 4775-4785 (2002).
54. Park JH, Bae YH. Hydrogels based on poly(ethylene oxide) and poly(tetramethylene oxide) or poly (dimethyl siloxane). III. In vivo biocompatibility and biostability. J. Biomed. Mater. Res. A 64A(2), 309-319 (2003).
55. Park K, Shim HS, Dewanjee MK, Eigler NL. In vitro and in vivo studies of PEO-grafted blood-contacting cardiovascular prostheses. [i J. Biomater. Sci. 11(11), 1121-1134 (2000).
56. Pasche S, Voros J, Griesser HJ, Spencer ND, Textor M. Effects of ionic strength and surface charge on protein adsorption at PEGylated surfaces. J. Phys. Chem. B 109(37), 17545-17552 (2005).
57. Croll TI, O'Connor AJ, Stevens GW, Cooper-White JJ. A blank slate? Layer-by-layer deposition of hyaluronic acid and chitosan onto various surfaces. Biomacromolecules 7(5), 1610-1622 (2006).
58. Mendelsohn JD, Yang SY, Hiller J, Hochbaum AI, Rubner MF. Rational design of cytophilic and cytophobic polyelectrolyte multilayer thin films. Biomacromolecules 4(1), 96-106 (2003).
59. Crou TI, Cao Y, Cooper-White JJ. Tailoring scaffolds for tissue regeneration. Presented at: Tissue Engineering and Regenerative Medicine International Society Annual Meeting. Rotterdam, The Netherlands, 8-11 October 2006.
60. Berg MC, Yang SY, Hammond PT, Rubner MF. Controlling mammalian cell interactions on patterned polyelectrolyte multilayer surfaces. Langmuir 20(4), 1362-1368 (2004).
61. Engler AJ, Griffin MA, Sen S et al. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166(6), 877-887 (2004).
62. Glawe JD, Hill JB, Mills DK, McShane MJ. Influence of channel width on alignment of smooth muscle cells by high-aspect-ratio microfabricated elastomeric cell culture scaffolds. J. Biomed. Mater. Res. A 75A(1), 106-114 (2005).
63. Sarkar S, Manisha D, Rourke P, Desai TA, Wong JY. Vascular tissue engineering: microtextured scaffold templates to control organization of vascular smooth muscle cells and extracellular matrix. Acta Biomater. 1, 93-100 (2005).
64. Charest JL, Garcia AJ, King WP. Myoblast alignment and differentiation on cell culture substrates with microscale topography and model chemistries. Biomaterials 28(13), 2202-2210 (2007).
65. Evans DJR, Britland S, Wigmore PM. Differential response of fetal and neonatal myoblasts to topographical guidance cues in vitro. Dev. Genes Evol. 209. 438-442 (1999).
66. Lam MT, Sim S, Zhu X, Takayama S. The effect of continuous wavy micropatterns on silicone substrates on the alignment of skeletal muscle myoblasts and myotubes. Biomaterials 27(24), 4340-4347 (2006).
67. Molnar P, Wang W, Natarajan A, Rumsey JW. Hickman JJ. Photolithographic patterning of C2C12 myotubes using vitronectin as growth substrate in serum-free medium. Biotechnol. Prog. 23(1), 265-268 (2007).
68. Papenburg BJ, Vogelaar L, Bolhuis-Versteeg LAM et al. One-step fabrication of porous micropatterned scaffolds to control cell behavior. Biomaterials 28(11), 1998-2009 (2007).
69. Patz TM, Doraiswamy A, Narayan RJ, Modi R, Chrisey DB. Two-dimensional differential adherence and alignment of C2C12 myoblasts. Mat. Sci. Eng. B 123(3), 242-247 (2005).
70. Khademhosseini A, Eng G, Yeh J et al. Microfluidic patterning for fabrication of contractile cardiac organoids. Biomed. Microdevices 9(2), 149-157 (2007).
71. McDevitt TC, Angello JC; Whitney ML et al. In vitro generation of differentiated cardiac myofibers on micropatterned laminin surfaces. J. Biomed Mater. Res. 60(3), 472-479 (2002).
72. Kim J, Park J, Cha JM. et al. The dependence of contractile force for cardiomyocytes on a different engineered surface. IEEE 299-302 (2005).
73. Clark P, Dunn GA, Knibbs A, Peckham M. Alignment of myoblasts on ultrafine gratings inhibits fusion in vitro. Int. J. Biochem. Cell Biol. 34(7), 816-825 (2002).
74. Thakara RG, Ho F, Huang NF, Liepmann D, Li S. Regulation of vascular smooth muscle cells by micropatterning. Biochem. Biophys. Res. Commun. 307(4), 883-890 (2003).
75. Lee KY, Alsberg E, Hsiong S et al. Nanoscale adhesion ligand organization regulates osteoblast proliferation and differentiation. Nano. Lett. 4(8), 1501-1506 (2004).
76. Chen S-L, Fang W-W, Ye F et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 94(1), 92-95 (2004).
77. Kennedy SB, Washburn NR Jr, Simon GC, Amis EJ. Combinatorial screen of the effect of surface energy on fibronectin-mediated osteoblast adhesion, spreading and proliferation. Biomaterials 27(20), 3817-3824 (2006).
78. Vogler EA. Structure and reactivity of water at biomaterial surfaces. Adv. Colloid. Interface Sci. 74, 69-117 (1998).
79. Popescu DC, Lems R, Rossi NAA et al. The patterning and alignment of muscle cells using the selective adhesion of poly (oligoethylene glycol methyl ether methacrylate)-based ABA block copolymers. Adv. Mat. 17(19), 2324-2329 (2005).
80. Khor HL, Kuan Y, Kukula H et al. Response of cells on surface-induced nanopatterns: fibroblasts and mesenchymal progenitor cells. Biomacromolecules 8(5), 1530-1540 (2007).
81. VandeVondele S, Vörös J, Hubbell JA. RGD-grafted poly-L-lysine-graft-(polyethylene glycol) copolymers block non-specific protein adsorption while promoting cell adhesion. Biotechnol. Bioeng. 82(7), 784-790 (2003).
82. Engler A, Bacakova L, Newman C et al. Substrate compliace versus ligand density in cell on gel responses. Biophys. J. 86(1), 617-628 (2004).
83. Wang H-B, Dembo M, Wangn Y-L. Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am. J. Physiol. Cell. Physiol. 279, C1345-C1350 (2000).
84. Yeung T, Georges PC, Flanagan LA et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34 (2005).
85. Lo C-M, Wang H-B, Dembo M, Wang Y-L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152 (2000).
86. Wong JY, Leach JB, Brown XQ. Balance of chemistry, topography, and mechanics at the cell-biomaterial interface: issues and challenges for assessing the role of substrate mechanics on cell response. Surf. Sci. 570, 119-133 (2004).
87. Shapira-Schweitzer K, Seliktar D. Matrix stiffness affects spontaneous contraction of cardiomyocytes cultured within a PEGylated fibrinogen biomaterial. Acta Biomater. 3(1), 33-41 (2007).
88. Wang N, Tolic-Norrelykke IM, Chen J et al. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Phhysiol. Cell. Physiol. 282(3), C606-C616 (2002).
89. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification - supplemental data. Cell 126(4), 677-689 (2006).
90. Discher DE, Janmey P, Wang Y-L. Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751), 1139-1143 (2005).
91. Li R-K, Jia Z-Q, Weisel RD et al. Survival and function of bioengineered cardiac grafts. Circulation 100(90002), II63-II69 (1999).
92. Li R-K, Yau TM, Weisel RD et al. Construction of a bioengineered cardiac graft. J. Thorac. Cardiovasc. Surg. 119(2), 368-375 (2000).
93. Isenberg BC, Williams C, Tranquillo RT. Small-diameter artificial arteries engineered in vitro. Circ. Res. 98(1), 25-35 (2006).
94. van Luyn MJA, Tio RA, Gallego Y et al. Cardiac tissue engineering: characteristics of in unison contracting two- and three-dimensional neonatal rat ventricle cell (co)-cultures. Biomaterials 23(24), 4793-4801 (2002).
95. Schwarzkopf R, Shachar M, Dvir T et al. Autospecies and post-myocardial infarction sera enhance the viability, proliferation, and maturation of 3D cardiac cell culture. Tissue Eng. 12(12), 3467-3475 (2006).
96. Venugopal J, Zhang YZ, Ramakrishna S. Fabrication of modified and functionalized polycaprolactone nanofibre scaffolds for vascular tissue engineering. Nanotechnology 16(10), 2138-2142 (2005).
97. Piao H, Kwon J-S, Piao S et al. Effects of cardiac patches engineered with bone marrow-derived mononuclear cells and PGCL scaffolds in a rat myocardial infarction model. Biomaterials 28(4), 641-649 (2007).
98. Radisic M, Cannizzaro C, Vunjak-Novakovic G. Scaffolds and fluid flow in cardiac tissue engineering. FDMP 2(1), 1-15 (2006).
99. Neumann T, Hauschka SD, Sanders JE. Tissue engineering of skeletal muscle using polymer fiber arrays. Tissue Eng. 9(5), 995-1003 (2003).
100. Riboldi SA, Sampaolesi M, Neuenschwander P, Cossu G, Mantero S. Electrospun degradable polyesterurethane membranes: potential scaffolds for skeletal muscle tissue engineering. Biomaterials 26(22), 4606-4615 (2005).
101. Levenberg S, Rouwkema J, Macdonald M et al. Engineering vascularized skeletal muscle tissue. Nat. Biotech. 23(7), 879-884 (2005).
102. Boldrin L, Elvassore N, Materba A et al. Satellite cells delivered by micro-patterned scaffolds: a new strategy for cell transplantation in muscle diseases. Tissue Eng. 13, 253-262 (2007).
103. Bursac N, Papadaki M, Cohen RJ et al. Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am. J. Physiol. Heart Circ. Physiol. 277(2), H433-H444 (1999).
104. Carrier RL, Papadaki M, Rupnick M et al. Cardiac tissue engineering: cell seeding, - cultivation parameters, and tissue construct characterization. Biotechnol. Bioeng. 64(5), 580-589 (1999).
105. Krupnick AS, Kreisel D. Engels FH et al. A novel small animal model of left ventricular tissue engineering. J. Heart Lung Transplant. 21(2), 233-243 (2002).
106. Zong X, Bien H, Chung C-Y et al. Electrospun fine-textured scaffolds for heart tissue constructs. Biomaterials 26(26). 5330-5338 (2005).
107. Ishii O, Shin M, Sueda T, Vacanti JP. In vitro tissue engineering of a cardiac graft using a degradable scaffold with an extracellular matrix-like topography. J. Thorac. Cardiovasc. Surg. 130(5), 1358-1363 (2005).
108. Zimmermann W-H, Melnychenko I, Wasmeier G et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat. Med. 12(4), 452-458 (2006).
109. Eschenhagen T, Didié M, Münzel F et al. 3D engineered heart tissue for replacement therapy. Basic Res. Cardiol. 97 (Suppl. 1), I146-I152 (2002).
110. Eschenhagen T, Zimmermann WH. Engineering myocardial tissue. Cirr. Res. 97, 1220-1231 (2005).
111. Fink C, Ergun S, Kralisch D et al. Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J. 14(5), 669-679 (2000).
112. Naito H, Melnychenko I, Didie M et al. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114 (1 Suppl.), 172-178 (2006).
113. Zimmermann WH, Schneiderbanger K, Schubert P et al. Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 90(2), 223-230 (2002).
114. Zimmermann WH, Didie M, Wasmeier GH et al. Cardiac grafting of engineered heart tissue in syngenic rats. Circulation 106(90121), I151-I157 (2002).
115. Zimmermann WH, Eschenhagen T. Cardiac tissue engineering for replacement therapy. Heart Fail. Rev. 8(3), 259-269 (2003).
116. Hecker L, Baar K, Dennis RG, Bitar KN. Development of a three-dimensional physiological model of the internal anal sphincter bioengineered in vitro from isolated smooth muscle cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289(2), G188-G196 (2005).
117. Nakase Y, Hagiwara A, Nakamura T et al. Tissue engineering on small intestinal tissue using collagen sponge scaffolds seeded with smooth muscle cells. Tizue Eng. 12(2), 403-412 (2006).
118. Boccafoschi F, Habermehl J, Vesentini S, Mantovani D. Biological performances of collagen-based scaffolds for vascular tissue engineering. Biomaterials 26(35), 7410-7417 (2005).
119. Grassl ED, Oegema TR, Tranquillo RT. A fibrin-based arterial media equivalent. J. Biomed. Mater. Res. A 66A(3), 550-561 (2003).
120. Isenberg BC, Tranquillo RT. Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann. Biomed. Eng. 31(8), 937-949 (2003).
121. Berglund JD, Nerem RM, Sambanis A. Incorporation of intact elastin scaffolds in tissue-engineered collagen-based vascular grafts. Tissue Eng. 10(9), 1526-1535 (2004).
122. Almany L, Seliktar D. Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures. Biomaterials 26(15), 2467-2477 (2005).
123. Halstenberg S, Panitch A, Rizzi S, Hall H, Hubbell JA. Biologically engineered protein-graft-poly(ethylene glycol) hydrogels: a cell adhesive and plasmin-degradable biosynthetic material for tissue repair. Biomacromolecules 3(4), 710-723 (2002).
124. Lutolf MP, Weber FE, Schmoekel HG et al. Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nature 21(5), 513-518 (2003).
125. Mann BK, Gobin AS, Tsai AT, Schmedlen RH, West JL. Smooth muscle cell growth in photopolymerized hydrogels with cell adhesive and proteolytically degradable domains: synthetic ECM analogs for tissue engineering. Biomaterials 22(22), 3045-3051 (2001).
126. Seliktar D, Zisch AH, Lutolf MP, Wrana JL, Hubbell JA. MMP-2 sensitive, VEGF-bearing bioactive hydrogels for promotion of vascular healing. J. Biomed. Mater. Res. A 68A(4), 704-716 (2004).
127. Dennis RG, Kosnik PE. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell. Dev. Biol. Anim. 36(5), 327-335 (2000).
128. Borschel GH, Dow DE, Dennis RG, Brown DL. Tissue-engineered axially vascularized contractile skeletal muscle. Plast. Reconstr. Surg. 117(7), 2235-2242. (2006).
129. Saxena V, Malhotra BD. Prospects of conducting polymers in molecular electronics. Curr. Appl. Phys. 3, 293-305 (2003).
130. Cassell OCS, Hofer SOP, Morrison WA, Knight KR. Vascularisation of tissue-engineered grafts - the regulation of angiogenesis in reconstructive and in disease states. Br. J. Plast. Surg. 55, 603-610 (2002).
131. Elcin AE, Elcin YM. Localized angiogenesis induced by human vascular endothelial growth factor-activated PLGA sponge. Tissue Eng. 12(4), 959-968 (2006).
132. Perets A, Baruch Y, Weisbuch F et al. Enhancing the vascularization of three-dimensional porous alginate scaffolds by incorporating controlled release basic fibroblast growth factor microspheres. J. Biomed. Mater. Res. A 65A(4), 489-497 (2003).
133. Iyer RK, Radisic M, Cannizzaro C, Vunjak-Novakovic G. Synthetic oxygen carriers in cardiac tissue-engineering. Artif. Cells Blood Substit. Immobil. Biotechnol. 35(1), 135-148 (2007).
134. Neumann T, Nicholson BS, Sander JE. Tissue engineering of perfused microvessels. Microvasc. Res. 66(1), 59-67 (2003).
135. Kanematsu A, Yamamoto S, Ozeki M et al. Collagenous matrices as release carriers of exogenous growth factors. Biomaterials 25(18), 4513-4520 (2004).
136. Laham RJ, Sellke FW, Edelman ER et al. Local perivascular delivery of basic fibroblast growth factor in patients undergoing coronary bypass surgery: results of a Phase I randomized, double-blind, placebo-controlled trial. Circulation 100(18), 1865-1871 (1999).
137. Peattie RA, Nayate AP, Firpo MA et al. Stimulation of in vivo angiogenesis by cytokine-loaded hyaluronic acid hydrogel implants. [i Biomaterials 25(14), 2789-2798 (2004).
138. Seeherman H, Wozney JM. Delivery of bone morphogenetic proteins for orthopaedic tissue regeneration. Cytokine Growth Factor Rev. 16(3), 329-345 (2005).
139. Silverman LD, Lukashova L, Herman OT, Lane JM, Boskey AL. Release of gentamicin from a tricalcium phosphate bone implant. J. Orthop. Res. 25(1), 23-29 (2007).
140. Jang J-H, Houchin TL, Shea LD. Gene delivery from polymer scaffolds for tissue engineering. Expert. Rev. Med. Devices 1(1), 127-138 (2004).
141. Kushibiki T, Tomoshige R, Fukunaka Y, Kakemi M, Tabata Y. In vivo release and gene expression of plasmid DNA by hydrogels of gelatin with different cationization extents. J. Control. Release 90, 207-216 (2003).
142. Lin J, Zhang S, Chen T, Lin S, Jin H. Micelle formation and drug release behaviour of polypeptide graft copolymer and its mixture with polypeptide block copolymer. Int. J. Pharm. 336(1), 49-57 (2007).
143. Richard P, Bossard F, Desigaux L et al. Amphiphilic block copolymers promote gene delivery in vivo to pathological skeletal muscles. Hum. Gene Ther. 16(11), 1318-1324 (2005).
144. Abidian MR, Kim DH, Martin DC. Conducting-polymer nanotubes for controlled drug release. Adv. Mat. 18(4), 405-409 (2006).
145. Wadhwa R, Lagenaur CF, Cui XT. Electrochemically controlled release of dexamethasone from conducting polymer polypyrrole coated electrode. J. Control. Release 110(3), 531-541 (2006).
146. Jeong B, Bae YH, Kim SW Drug release from biodegradable injectable thermosensitive hydrogel of PEG-PLGA-PEG triblock copolymers. J. Control. Release 63(1-2), 155-163 (2000).
147. Dong W, Zhang T, McDonald M et al. Biocompatible nanofiber scaffolds on metal for controlled release and cell colonization. Nanomedicine 2(4), 248-252 (2006).
148. Kim H-J, Matsuda H, Zhou H, Honma I. Ultrasound-triggered smart drug release from a poly (dimethylsiloxane)- mesoporous silica composite. Adv. Mat. 18(23), 3083-3088 (2006).
149. George PM, LaVan DA, Burdick JA et al. Electrically controlled drug delivery. from biotin-doped conductive polypyrrole. Adv. Mat. 18(5), 577-581 (2006).
150. Richardson RT, Thompson B, Moulton S et al. The effect of polypyrrole with incorporated neurotrophin-3 on the promotion of neurite outgrowth from auditory neurons. Biomaterials 28(3), 513-523 (2007).
151. Thompson BC, Moulton SE, Ding J et al. Optimising the incorporation and release of a neurotrophic factor using conducting polypyrrole. J. Control. Release 116(3), 285-294 (2006).
152. Han X, Chunlei W, Lawrence K, Jim Z, Marc M. Sensor-integrated polymer actuators for closed-loop drug delivery system. Presented at: Smart Structures and NDE for Health Monitoring and Diagnostics. San Diego, CA, USA, 26 February-2 March 2006.
153. Gizdavic-Nikolaidis M, Travas-Sejdic J, Bowmaker GA et al. The antioxidant activity of conducting polymers in biomedical applications. Curr. Appl. Phys. 4(2-4), 347-350 (2004).
154. Kilmartin PA, Gizdavic-Nikolaidis M, Zujovic Z et al. Free radical scavenging and antioxidant properties of conducting polymers examined using EPR and NMR spectroscopies. Synthetic Metals 153 (1-3), 153-156 (2005).
155. Aiagno M, Mastrocola R, Catalano MG et al. Oxidative stress impairs skeletal muscle repair in diabetic rats. Diabetes 53(4), 1082-1088 (2004).
156. Murthy N, Campbell J, Fausto N, Hoffman AS, Stayton PS. Bioinspired pH-responsive polymers for the intracellular delivery of biomolecular drugs. Bioconjugate Chem. 14 (2), 412-419 (2003).
157. Lee KY, Peters MC, Anderson KW, Mooney DJ. Controlled growth factor release from synthetic extracellular matrices. Nature 408 (6815), 998-1000 (2000).
158. Chau Y, Tan FE, Langer R. Synthesis and characterization of dextran-peptide methotrexate conjugates for tumor targeting via mediation by matrix metalloproteinase II and matrix metalloproteinase IX. Bioconjugate Chem. 15(4), 931-941 (2004).
159. Chau Y, Padera RF, Dang NM, Langer R. Antitumor efficacy of a novel polymerpeptide-drug conjugate in human tumor xenograft models. Int. J Cancer 118(6), 1519-1526 (2006).
160. Law B, Weissleder R, Tung CH. Peptidebased biomaterials for protease-enhanced drug delivery. Biomacromolecules 7 (4), 1261-1265 (2006).
161. Ai-Tahami K, Singh J. Smart polymer based delivery systems for peptides and proteins. Recent Patents Drug Delivery & Formation 1, 65-71 (2007).
162. Kim B-S, Nikolovski J, Bonadio, J, Mooney DJ. Cyclic mechanical strain regulates the development of engineered smooth muscle tissue. Nat. Biotech. 17(10), 979-983 (1999).
163. Kim B, Mooney DJ. Scaffolds for engineering smooth muscle under cyclic mechanical strain conditions. J. Biomech. Eng. 122, 210-215 (2000).
164. Li W, Chen Q, Mills I, Sumpio BE. 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(2), 202-209 (2003).
165. McKnight NL, Frangos IA. Strain rate mechanotransduction in aligned human vascular smooth muscle cells. Ann. Biomed, Eng. 31, 239-249 (2003).
166. Reusch P, Wagdy H, Reusch R, Wilson E, Ives HE. Mechanical strain increases smooth muscle and decreases nonmuscle myosin expression in rat vascular smooth muscle cells. Circ. Res. 79, 1046-1053 (1996).
167. Jeong SI, Kwon JH, Lim JI et al. Mechano-active tissue engineering of vascular smooth muscle using pulsatile perfusion bioreactors, elasticPLCL scaffolds. Biomaterials26(12), 1405-1411 (2005).
168. Standley PR, Camaratta A, Nolan BP, Purgason CT, Stanley MA. Cyclic stretch induces vascular smooth muscle cell alignment via NO signalling. Am. J. Physiol. Heart Circ. Physiol. 283. 1907-1914 (2002).
169. O'Callaghan CJ, Williams B. Mechanical strain-induced extracellular matrix production by human vascular smooth muscle cells: role of TGF-β1. Hypertension 36(3), 319-324 (2000).
170. Owens GK. Role of mechanical strain in regulation of differentiation of vascular smooth muscle cells. Circ. Res. 79, 1054-1055 (1996).
171. Gupta V, Grande-Allen KJ. Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. Cardiovasc. Res. 72(3), 375-383 (2006).
172. Cevallos M, Riha GM, Wang X et al. Cyclic strain induces expression of specific smooth muscle cell markers in human endothelial cells. Differentiation 74 (9- 10), 552-561 (2006).
173. Le Ricousse-Roussanne S, Larghero J. Zini J-M et al. Ex vivo generation of mature and functional human smooth muscle cells differentiated from skeletal myoblasts. Exp. Cell Res. 313(7), 1337-1346 (2007).
174. Cai D, Marty-Roix R, Hsu H-P, Spector M. Lapine and canine bone marrow stromal cells contain smooth muscle actin and contract a collagenglycosaminoglycan matrix. Tissue Eng. 7(6), 829-841 (2001).
175. Hamilton DW, Maul TM, Vorp, DA. The influence of cyclic strain on the differentiation of rat bone marrow derived mesenchymal stem cells to vascular smooth muscle. Presented at: Second Joint EMBS/BMES Conference. Houston, TX, USA, 23-26 October 2002.
176. Kobayashi N, Yasu T, Ueba H et al. Mechanical stress promotes the expression of smooth muscle-like properties in marrow stromal cells. 32(12), 1238-1245 (2004).
177. Kurpinski K, Park J, Thakar RG, Song L. Regulation of vascular smooth muscle cells and mesenchymal stem cells by mechanical strain. Mol. Cell. Biomech. 3 (1), 21-34 (2006).
178. Ball SG, Shuttleworth AC, Kielty CM. Direct cell contact influences bone marrow mesenchymal stem cell fate. Int. J Biochem. Cell Biol. 36(4), 714-727 (2004).
179. Powell CA, Smiley BL, Mills J, Vandenburgh HH. Mechanical stimulation Improves tissue-engineered human skeletal muscle. Am. J. Physiol. Cell. Physiol. 283(5), C1557-CI565 (2002).
180. Vandenburgh HH, Hatfaludy S, Karlisch P, Shansky J. Skeletal muscle growth is stimulated by intermittent stretch-relaxation in tissue culture. Am. J. Physiol. Cell. Physiol. 256 (3), C674-C682 (1989).
181. Collinsworth AM, Torgan CE, Nagda SN et al. Orientation and length of mammalian skeletal myocytes in response to a unidirectional stretch. Cell. Tissue Res. 302(2), 243-251 (2000).
182. Sakata T, Tatsumi R, Yamada M et al. Preliminary experiments on mechanical stretch-induced activation of skeletal muscle satellite cells in vivo. Anim. Sci. J. 77(5), 518-525 (2006).
183. Tatsumi R, Sheehan SM, Iwasaki H, Hattori A, Allen RE. Mechanical stretch induces activation of skeletal muscle satellite cells in vitro. Exp. Cell Res. 267(1), 107-114 (2001).
184. Kofidis T, Akhyari P, Boublik J et al. In vitro engineering of heart muscle: artificial myocardial tissue. J Thorac. Cardiovasc. Surg. 124(1), 63-69 (2002).
185. Akimoto T, Pohert SC, Li P et al. Exercise stimulates Pgc- lα trascription in skeletal muscle through activation of the p38
186. Zhan M, Jin B, Chen S-E, Reecy JM, Li Y-P. TACE release of TNF-α mediates mechanotransduction-induced activation of p38 MAPK and myogenesis. J. Cell Sci. 120(4), 692-701 (2007).
187. Goldschmidt ME, McLeod KJ, Taylor WR. Integrin-mediated mechanotransduction in vascular smooth muscle cells frequency and force response characteristics. Circ. Res. 88, 674-680 (2001).
188. Li J, Johnson SE. ERK2 is required for efficient terminal differentiation of skeletal myoblasts. Biochem. Biophys. Res. Commun. 345(4), 1425-1433 (2006).
189. Barker AT, Jaffe LF, Vanable JW Jr. The glabrous epidermis of cavies contains a powerful battery. Am. J Physiol. Regul. Integr. Camp. Physiol. 242(3), R358-R366 (1982).
190. Li X Kolega J. Effects of direct current electric fields on cell migration and catin filament distribution in bonvine vascular endothetial cells. J. Vasc. Res. 39, 391-404 (2002).
191. Onuma EK, Hui SW Electric field-directed cell shape changes, displacement, and cytoskeletal reorganization are calcium dependent. J. Cell Biol. 106(6), 2067-2075 (1988).
192. Patel N, Poo M. Orientation of neurite growth by extracellular electric fields. J Neurosci. 2(4), 483-396 (1982).
193. Radisic M, Park H, Langer R, Freed LE, Vunjak-Novakovic G. Co-culture of cardiac fibroblasts and myocytes enhances functional assembly of engineered myocardium. Presented at: 7th Internatinal Congress of the Cell Transplant Society. Boston, MA, USA, 17-20 November 2004.
194. Borgens RB. Electrically mediated regeneration and guidance of adult mammalian spinal axons into polymeric channels. Neuroscience91(1), 251-264 (1999).
195. Kotwal A, Schmidt CE. Electrical stimulation alters protein adsorption and nerve cell interactions with electrically conducting biomaterials. Biomaterials 22, 1055-1064 (2001).
196. Schmidt CE, Shastri VR, Vacanti JP, Langer R. Stimulation of neurite outgrowth using an electrically conducting polymer. Proc. Natl Acad. Sci. USA 94, 8948-8953 (1997).
197. Pedrotty DM, Koh J, Davis BH et al. Engineering skeletal myoblasts: roles of three-dimensional culture and electrical stimulation. Am. J Physiol. Heart Cirn. Physiol. 288(4), H1620-H1626 (2005).
198. Supronowicz PR, Ajayan PM, Ullmann KR et al. Novel current-conducting composite substrates for exposing osteoblasts to alternating current stimulation. J. Biomed, Mater. Res. 59(3), 499-506 (2001).
199. Ullmann KR, Plawsky J, Kumar K, Bizlos R. Osteoblast responses to electrical stimulation. Presented at: 1999 Bioengineering Conference. Big Sky, MT, USA, 6-20 June 1999.
200. Wang Q, Zhong S, Ouyang J et al. Osteogenesis of electrically stimulated bone cells mediated in part by calcium ions. Clin. Orthrop. Relat. Res. 348, 259-268 (1998).
201. Hagiwara T, Bell W. Effect of electrical stimulation on mandibular distraction osteogenesis. J. Craniomaxillofac. Surg. 28, 12-19 (2000).
202. Yamada M, Tanemura K, Okada S et al. Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells 25(3), 562-570 (2007).
203. Helgason T, Gargiulo P, Johannesdottir F et al. Monitoring muscle growth and tissue changes induced by electrical stimulation of denervated degenerated muscles with CT and stereolithographic 3D modeling. Artif Organs 29 (6), 440-443 (2005).
204. Mayr W, Hofer C, Bijak M et al. Functional electrical stimulation (FES) of denervated muscles: existing and prospective technological solutions. Basic Appl. Myol. 12, 287-290 (2002).
205. Zhao M, Bai H, Wang E, Forrester JV, McCaig CD. Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signalling through VEGF receptors. J Cell Sci. 117, 397-405 (2004).
206. Kanno S, Oda N, Abe M et al. Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation 99, 2682-2687 (1999).
207. Kawahara Y, Yamaoka K, Iwata M et al. Novel electrical stimulation sets the cultured myoblast contractile function to on Pathobiology 73, 288-294 (2006)
208. Stern-Straeter J Bach AD, Stangenberg L et al. Impact of electrical stimulatin on three-dimensional myoblast cultures - a real-time RT-PCR study. J.Cell. Mol. 9(4). 883-892 (2005).
209. Radisic M, Park H, Shing H et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl Acad. Sci. 101(52), 18129-18134 (2004).
210. Kim B, Koncar V, Devaux E. Electrical properties of conductive polymers: PET - nanocomposite fibres. AutexRJ4 (1), 9-13 (2004).
211. Rivers TJ, Terr WH, Schmidt CE. Synthesis of a novel, biodegradable electrically conducting polymer for biomedical applications. Adv. Funct. Mater. 12(1), 33-37 (2002).
212. Bidez PR, Li S, MacDiarmid AG et al. Polyaniline, an electroactive polymer, supports adhesion and proliferation of cardiac myoblasts. J. Biomater Sci. Polymer Ed. 17(1-2), 199-212 (2006).
213. Shi G, Rouabhia M,'Wang Z, Dao L, Zhang Z. A novel electrically conductive and biodegradable composite made of polypyrrole nanoparticles and polylactide. Biomaterials 25, 2477-2488 (2004).
214. Rowlands AS, Moulton S, Wallace G, Campbell J, Cooper-White JJ. Conducting scaffolds for muscle tissue engineering. Presented at: Tissue Engineering and Regeneative Medicine International Society Annual Meeting. Rotterdam, The Netherlands, 8-11 October 2006.
215. Zelikin AN, Lynn DM, Farhadi j et al. Erodible conducting polymers for potential biomedical applications. Angew. Chem. Int Ed. 41(1), 141-144 (2002).
216. Salomonsson M, Gustafsson F, Andreasen D, Jensen BL, Holstein-Rathlou NH. Local electric stimulation causes conducted calcium response in rat interlobular arteries. Am. J Physiol. Renal Physiol. 283(3), F473-17480 (2002).
217. Hinkle L, McCaig CD, Robinson KR. The direction of growth of differentiating, neurons and myoblast from frog embryos in an applied electric field. J. Physiol. 314, 121-135 (1981).
218. Todorovic Z, Stojanovic R, Divac ZN et al. Type of electrical stimulation influences diaphragm response to adrenoceptor and calcium channel modulators: the role of extracellular and intracellular calcium events. J. Pharacol. Sci. 102, 347-353 (2006).
219. Khatib L, Golan DE, Chio M. Physiologic electrical stimulation prosrokes intracellular calcium increase mediated by phosholipase C activation in human osteoblasts. FASEB J. 18, 1903-1905 (2004).
220. 2+. signals through a Gβγ/phosphatidylinositol 3-kinase γ pathway in skeletal myotubes. J. Biol Chem. 281(17), 12143-12154 (2006).
221. 12 Co-culture on a fibroblast substratum enables sustained survival of contractile, highly differentiated myotubes with peripheral nuclei and adult fast myosin expression. Cell. Motil. Cytoskeleton 58(3), 200-211 (2004).
222. Dennis RG, Kosnik PE 2nd, Gilbert ME, Faulkner JA. Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines. Am. J. Physiol. Cell. Physiol. 280(2), C288-C295 (2001).
223. Wang T, Xu Z, Jiang W, Ma A. Cell-to-cell contact induces mesenchymal stem cell to differentiate into cardiomyocyte and smooth muscle cell. Int. J Cardiol. 109 (1), 74-81 (2006).
224. Caspi O, Lennan A, Basevitch Y et al. Tissue engineering of vascularised cardiac muscle from human embryonic stem cells. Circ. Res. 100, 263-272 (2007).
225. Kizana E, Ginn SL, Smyth CM et al. Fibroblasts modulate cardiomyocyte excitability: implications for cardiac gene therapy. Gene Ther. 13(22), 1611-1615 (2006).