Micropatterned cell sheets with defined cell and extracellular matrix orientation exhibit anisotropic mechanical properties

Journal of Biomechanics

Volumn 45, Issue 5, 2012, Pages 756-761

  Isenberg, Brett C ^a   Backman, Daniel E ^a   Kinahan, Michelle E ^a   Jesudason, Rajiv ^a   Suki, Bela ^a   Stone, Phillip J ^b   Davis, Elaine C ^c   Wong, Joyce Y ^a  

^a Boston University   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Blood vessels; Cell sheet; Mechanical anisotropy; Micropatterning; Smooth muscle cells; Tissue engineering

Indexed keywords

ANISOTROPIC MECHANICAL PROPERTIES; ARTERIAL REPLACEMENT GRAFT; ASCORBIC ACIDS; BIOCHEMICAL COMPOSITION; BOVINE AORTIC; CELL LAYERS; CELL ORGANIZATION; CELL SHEET; COLLAGEN FIBER; COMPLEX TISSUES; EXTRACELLULAR MATRICES; FUNCTIONAL CHANGES; FUNCTIONAL PROPERTIES; LARGE ARRAYS; MACRO SCALE; MATERIAL BEHAVIOR; MECHANICAL ANISOTROPY; MICRO PATTERN; MICRO-SCALES; MICROPATTERNED; MICROPATTERNING; POLYDIMETHYLSILOXANE PDMS; SMOOTH MUSCLE CELLS; STRUCTURAL ORGANIZATION; TISSUE GROWTH; VESSEL WALLS;

ALIGNMENT; ANISOTROPY; BLOOD VESSELS; CELLS; CYTOLOGY; KETONES; MECHANICAL TESTING; ORGANIC ACIDS; SILICONES; STIFFNESS; STRENGTH OF MATERIALS; TISSUE; TISSUE ENGINEERING; WALLS (STRUCTURAL PARTITIONS);

BIOMECHANICS;

ASCORBIC ACID; DIMETICONE;

ANIMAL CELL; ANIMAL TISSUE; ANISOTROPY; AORTA MEDIA; ARTICLE; ARTIFICIAL MEMBRANE; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR MATRIX; MECHANICAL STRESS; MICROPATTERNED CELL SHEET; MOLECULAR MECHANICS; MUSCLE STIFFNESS; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; TENSILE STRENGTH; TISSUE CULTURE; TISSUE ENGINEERING; TISSUE GROWTH; TISSUE STRUCTURE;

ANIMALS; ANISOTROPY; ARTERIES; ASCORBIC ACID; BIOMECHANICS; CATTLE; CELL CULTURE TECHNIQUES; CELLS, CULTURED; DIMETHYLPOLYSILOXANES; EXTRACELLULAR MATRIX; HEMODYNAMICS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; TISSUE ENGINEERING;

EID: 84857649282     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2011.11.015     Document Type: Article

References (48)

1. Ai H., Lvov Y.M., Mills D.K., Jennings M., Alexander J.S., Jones S.A. Coating and selective deposition of nanofilm on silicone rubber for cell adhesion and growth. Cell Biochemistry and Biophysics 2003, 38:103-114.
2. Auger F.A., Remy-Zolghadri M., Grenier G., Germain L. The self-assembly approach for organ reconstruction by tissue engineering. e-biomed: The Journal of Regenerative Medicine 2000, 1:75-86.
3. Badie N., Bursac N. Novel micropatterned cardiac cell cultures with realistic ventricular microstructure. Biophysical Journal 2009, 96:3873-3885.
4. Black L.D., Allen P.G., Morris S.M., Stone P.J., Suki B. Mechanical and failure properties of extracellular matrix sheets as a function of structural protein composition. Biophysical Journal 2008, 94:1916-1929.
5. Canham P.B., Talman E.A., Finlay H.M., Dixon J.G. Medial collagen organization in human arteries of the heart and brain by polarized light microscopy. Connective Tissue Research 1991, 26:121-134.
6. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Micropatterned surfaces for control of cell shape, position, and function. Biotechnology Progress 1998, 14:356-363.
7. Cowin S.C. How is a tissue built?. Journal of Biomechanical Engineering 2000, 122:553-569.
8. Curtis A., Wilkinson C. Topographical control of cells. Biomaterials 1997, 18:1573-1583.
9. Dahl S.L.M., Kypson A.P., Lawson J.H., Blum J.L., Strader J.T., Li Y., Manson R.J., Tente W.E., Dibernardo L., Hensley M.T., et al. Readily available tissue-engineered vascular grafts. Science Translational Medicine 2011, 3. 68ra9.
10. Dahl S.L.M., Vaughn M.E., Niklason L.E. An ultrastructural analysis of collagen in tissue engineered arteries. Annals of Biomedical Engineering 2007, 35:1749-1755.
11. Davis E.C. Smooth muscle cell to elastic lamina connections in developing mouse aorta. Role in aortic medial organization. Laboratory Investigation, a Journal of Technical Methods and Pathology 1993, 68:89-99.
12. Desai T.A. Micro- and nanoscale structures for tissue engineering constructs. Medical Engineering and Physics 2000, 22:595-606.
13. Elloumi Hannachi I., Itoga K., Kumashiro Y., Kobayashi J., Yamato M., Okano T. Fabrication of transferable micropatterned-co-cultured cell sheets with microcontact printing. Biomaterials 2009, 30:5427-5432.
14. Fujita H., Shimizu K., Nagamori E. Application of a cell sheet-polymer film complex with temperature sensitivity for increased mechanical strength and cell alignment capability. Biotechnology and Bioengineering 2009, 103:370-377.
15. Fung Y.-C. Biomechanics: Mechanical Properties of Living Tissues 1993, Spinger-Verlag, New York.
16. Gauvin R., Parenteau-Bareil R., Larouche D., Marcoux H., Bisson F., Bonnet A., Auger F.A., Bolduc S., Germain L. Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding. Acta Biomaterialia 2011, 7:3294-3301.
17. Glagov S. Relation of structure to function in arterial walls. Artery 1979, 5:295-304.
18. Glawe J.D., Hill J.B., Mills D.K., McShane M.J. Influence of channel width on alignment of smooth muscle cells by high-aspect-ratio microfabricated elastomeric cell culture scaffolds. Journal of Biomedical Materials Research Part A 2005, 75:106-114.
19. Grenier G., Rémy-Zolghadri M., Larouche D., Gauvin R., Baker K., Bergeron F., Dupuis D., Langelier E., Rancourt D., Auger F.A., et al. Tissue reorganization in response to mechanical load increases functionality. Tissue Engineering 2005, 11:90-100.
20. Griffith L.G., Swartz M.A. Capturing complex 3D tissue physiology in vitro. Nature Reviews. Molecular Cell Biology 2006, 7:211-224.
21. Isenberg B.C., Tsuda Y., Williams C., Shimizu T., Yamato M., Okano T., Wong J.Y. A thermoresponsive, microtextured substrate for cell sheet engineering with defined structural organization. Biomaterials 2008, 29:2565-2572.
22. Isenberg B.C., Williams C., Tranquillo R.T. Small-diameter artificial arteries engineered in vitro. Circulation Research 2006, 98:25-35.
23. Jesudason R., Sato S., Parameswaran H., Araujo A.D., Majumdar A., Allen P.G., Bartolák-Suki E., Suki B. Mechanical forces regulate elastase activity and binding site availability in lung elastin. Biophysical Journal 2010, 99:3076-3083.
24. Kakisis J.D., Liapis C.D., Breuer C., Sumpio B.E. Artificial blood vessel: the holy grail of peripheral vascular surgery. Journal of Vascular Surgery 2005, 41:349-354.
25. Kane R.S., Takayama S., Ostuni E., Ingber D.E., Whitesides G.M. Patterning proteins and cells using soft lithography. Biomaterials 1999, 20:2363-2376.
26. Konig G., McAllister T.N., Dusserre N., Garrido S.A., Iyican C., Marini A., Fiorillo A., Avila H., Wystrychowski W., Zagalski K., et al. Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. Biomaterials 2009, 30:1542-1550.
27. Kononov S., Brewer K., Sakai H., Cavalcante F.S., Sabayanagam C.R., Ingenito E.P., Suki B. Roles of mechanical forces and collagen failure in the development of elastase-induced emphysema. American Journal of Respiratory and Critical Care Medicine 2001, 164:1920-1926.
28. Kubo H., Shimizu T., Yamato M., Fujimoto T., Okano T. Creation of myocardial tubes using cardiomyocyte sheets and an in vitro cell sheet-wrapping device. Biomaterials 2007, 28:3508-3516.
29. Lansing A.I., Rosenthal T.B., Alex M., Dempsey E.W. The structure and chemical characterization of elastic fibers as revealed by elastase and by electron microscopy. The Anatomical Record 1952, 114:555-575.
30. Lee J., Cuddihy M.J., Kotov N.A. Three-dimensional cell culture matrices: state of the art. Tissue Engineering Part B, Reviews 2008, 14:61-86.
31. L'Heureux N., Dusserre N., Konig G., Victor B., Keire P., Wight T.N., Chronos N.A.F., Kyles A.E., Gregory C.R., Hoyt G., et al. Human tissue-engineered blood vessels for adult arterial revascularization. Nature Medicine 2006, 12:361-365.
32. McAllister T.N., Maruszewski M., Garrido S.A., Wystrychowski W., Dusserre N., Marini A., Zagalski K., Fiorillo A., Avila H., Manglano X., et al. Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet 2009, 373:1440-1446.
33. Morris S.M., Stone P.J. Immunocytochemical study of the degradation of elastic fibers in a living extracellular matrix. The Journal of Histochemistry and Cytochemistry: Official Journal of the Histochemistry Society 1995, 43:1145-1153.
34. Nelson C.M., Tien J. Microstructured extracellular matrices in tissue engineering and development. Current Opinion in Biotechnology 2006, 17:518-523.
35. Pietak A., McGregor A., Gauthier S., Oleschuk R., Waldman S.D. Are micropatterned substrates for directed cell organization an effective method to create ordered 3D tissue constructs?. Journal of Tissue Engineering and Regenerative Medicine 2008, 2:450-453.
36. Rhodin J. Architecture of the vessel wall. In Handbook of Physiology 1980, Waverly Press, Inc, Baltimore, pp. 1-31.
37. Ritter M.C., Jesudason R., Majumdar A., Stamenovic D., Buczek-Thomas J.A., Stone P.J., Nugent M.A., Suki B. A zipper network model of the failure mechanics of extracellular matrices. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:1081-1086.
38. Sarkar S., Dadhania M., Rourke P., Desai T.A., Wong J.Y. Vascular tissue engineering: microtextured scaffold templates to control organization of vascular smooth muscle cells and extracellular matrix. Acta Biomaterialia 2005, 1:93-100.
39. Shen C.J., Fu J., Chen C.S. Patterning cell and tissue function. Cellular and Molecular Bioengineering 2008, 1:15-23.
40. Stone P.J., Lucey E.C., Snider G.L., Franzblau C. Distribution of elastin in hamsters and the turnover rates of different elastin pools. Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine (New York, N.Y.) 1997, 215:94-101.
41. Stone P.J., McMahon M.P., Morris S.M., Calore J.D., Franzblau C. Elastin in a neonatal rat smooth muscle cell culture has greatly decreased susceptibility to proteolysis by human neutrophil elastase. An in vitro model of elastolytic injury. In Vitro Cellular and Developmental Biology: Journal of the Tissue Culture Association 1987, 23:663-676.
42. Tsuda Y., Shimizu T., Yamato M., Kikuchi A., Sasagawa T., Sekiya S., Kobayashi J., Chen G., Okano T. Cellular control of tissue architectures using a three-dimensional tissue fabrication technique. Biomaterials 2007, 28:4939-4946.
43. Vernon R.B., Gooden M.D., Lara S.L., Wight T.N. Microgrooved fibrillar collagen membranes as scaffolds for cell support and alignment. Biomaterials 2005, 26:3131-3140.
44. Wagenseil J.E., Mecham R.P. Vascular extracellular matrix and arterial mechanics. Physiological Reviews 2009, 89:957-989.
45. Williams C., Tsuda Y., Isenberg B.C., Yamato M., Shimizu T., Okano T., Wong J.Y. Aligned cell sheets grown on thermo-responsive substrates with microcontact printed protein patterns. Advanced Materials 2009, 21:2161-2164.
46. Williams C., Xie A.W., Yamato M., Okano T., Wong J.Y. Stacking of aligned cell sheets for layer-by-layer control of complex tissue structure. Biomaterials 2011, 32:5625-5632.
47. Yang J., Yamato M., Shimizu T., Sekine H., Ohashi K., Kanzaki M., Ohki T., Nishida K., Okano T. Reconstruction of functional tissues with cell sheet engineering. Biomaterials 2007, 28:5033-5043.
48. Zorlutuna P., Elsheikh A., Hasirci V. Nanopatterning of collagen scaffolds improve the mechanical properties of tissue engineered vascular grafts. Bio macromolecules 2009, 10:814-821.