Uniaxial strain regulates morphogenesis, gene expression, and tissue strength in engineered skin

Tissue Engineering - Part A

Volumn 16, Issue 3, 2010, Pages 1083-1092

  Powell, Heather M ^a,b   McFarland, Kevin L ^a   Butler, David L ^c   Supp, Dorothy M ^a,d   Boyce, Steven T ^a,d  

^a SHRINERS HOSPITALS FOR CHILDREN   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Departments of Biomedical Engineering   (United States)

^d UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; CELL CULTURE; CELL PROLIFERATION; COLLAGEN; ENZYME ACTIVITY; GENE EXPRESSION; HISTOLOGY; MECHANICAL PROPERTIES; PHASE INTERFACES; TISSUE; TRANSPLANTATION (SURGICAL);

AIR LIQUID INTERFACES; COLLAGEN TYPE I; ELECTROSPUN COLLAGEN; ENGINEERED TISSUES; ENGRAFTMENT; EPIDERMAL CELLS; EXTRACELLULAR MATRIX PRODUCTION; EXTRACELLULAR MATRIX PROTEIN; GENES ENCODING; HUMAN DERMAL FIBROBLASTS; IN-VITRO; KERATINOCYTES; MECHANICAL STIMULATION; NORMAL SKIN; ORDERS OF MAGNITUDE; SURGICAL APPLICATIONS; TISSUE STRENGTH; UNI-AXIAL STRAINS; UP-REGULATION;

STRAIN;

BIOLOGICAL MARKER; COLLAGEN; SCLEROPROTEIN;

ANIMAL; ARTICLE; ARTIFICIAL SKIN; BIOMECHANICS; CATTLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KERATINOCYTE; MECHANICAL STRESS; METABOLISM; MORPHOGENESIS; SKIN; TISSUE ENGINEERING;

ANIMALS; BIOLOGICAL MARKERS; BIOMECHANICS; CATTLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; MORPHOGENESIS; SKIN; SKIN, ARTIFICIAL; STRESS, MECHANICAL; TISSUE ENGINEERING;

EID: 77649245014     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0542     Document Type: Article

References (49)

1. Compton, C, Butler, C.E., Yannas, I., Warland, G., and Orgill, D.P. Organized skin structure is regenerated in vivo from collagen-GAG matrices seeded with autologous kera-tinocytes. J Invest Dermatol 110, 908, 1998.
2. Boyce, S.T., Kagan, R.J., Yakuboff, K.P., Meyer, N.A., Rie-man, M.T., Greenhalgh, D.G., and Warden, G.D. Cultured skin substitutes reduce donor site harvesting for closure of excised, full-thickness burns. Ann Surg 235, 269, 2002.
3. Pham, C., Greenwood, J., Cleland, H., Woodruff, P., and Maddern, G. Bioengineered skin substitutes for the management of burns: a systematic review. Burns 33, 946, 2007.
4. MacNeil, S. Progress and opportunities for tissue-engineered skin. Nature 445, 874, 2007.
5. Boyce, S.T., Goretsky, M., Greenhalgh, D.G., Kagan, R.J., Rieman, M.T., and Warden, G.D. Comparative assessment of cultured skin substitutes and native skin autograft for treatment of full-thickness burns. Ann Surg 222, 743, 1995.
6. Boyce, S.T., Supp, A.P., Reed, M.A., and Kagan, R.J. Quantitative assessment of skin pliability after treatment of full-thickness burns with cultured skin substitutes and split-thickness autografts combined with Integra Artificial Skin® or cadaveric allograft. J Burn Care Rehabil 26, S168, 2005.
7. Agache, P.G., Monneur, C, Leveque, J.L., and DeRigal, J. Mechanical properties and Young's modulus of human skin in vivo. Arch Dermatol Res 269, 221, 1980.
8. LaFrance, H., Yahia, L., Germain, L., Guillot, M., and Auger, F.A. Study of the tensile properties of living skin equivalents. Biomed Mater Eng 5, 195, 1995.
9. Clark, J.A., Cheng, J.C.Y., and Leung, K.S. Mechanical properties of normal skin and hypertrophic scars. Burns 22, 443, 1996.
10. Khor, H., Ng, K., Schantz, J., Phan, T.-T., Lim, T., Teoh, S., and Hutmacher, D.W. Poly(E-caprolactone) films as a potential substrate for tissue engineering an epidermal equivalent. Mater Sci Eng C 20, 71, 2002.
11. Khatyr, F., Imberdis, C, Vescovo, P., Varchon, D., and La-garde, J.-M. Model of the viscoelastic behaviour of skin in vivo and study of anisotropy. Skin Res Technol 10, 96, 2004.
12. Powell, H.M., and Boyce, S.T. EDC cross-linking improves skin substitute strength and stability. Biomaterials 27, 5821, 2006.
13. Olde Damink, L.H.H., Dijkstra, P.J., Van Wachem, P.B., Van Luyn, M.J.A., Nieuwenhuis, P., and Feijen, J. In vitro degradation of dermal sheep collagen cross-linked using water-soluble carbodiimide. Biomaterials 17, 679, 1996.
14. Angele, P., Abke, J., Kujat, R., Faltermeier, H., Schumann, Z., Mehrl, R., and Mueller, R. Influence of different collagen species on physico-chemical properties of cross-linked collagen matrices. Biomaterials 25, 2831, 2004.
15. Zhong, S.P., Teo, W.E., Zhu, X., Beuertnan, R., Ramakrishna, S., and Yung, L.Y.L. Development of a novel collagen-GAG nanofibrous scaffold via electrospinning. Mater Sci Eng C 27, 262, 2007.
16. Cornwell, K.G., Lei, P., Andreadis, S.T., and Pins, G.D. Crosslinking of discrete self-assembled collagen threads: effects on mechanical strength and cell-matrix interactions. J Biomed Mater Res A 80A, 362, 2007.
17. Thompson, J.I., and Czernuszka, J.T. The effect of two types of cross-linking on some mechanical properties of collagen. Biomed Mater Eng 5, 37, 1995.
18. Ulubayram, K., Aksu, E., Gurhan, S.I.D., Serbetci, K., and Hasirci, N. Cytotoxicity evaluation of gelatin sponges prepared with different cross-linking agents. J Biomater Sci Polym Ed 13, 1203, 2002.
19. Powell, H.M., and Boyce, S.T. Engineered human skin fabricated using electrospun collagen-PCL blends: morphogenesis and mechanical properties. Tissue Eng Part A 15, 2177, 2009.
20. Stegemann, J.P., and Nerem, R.M. Phenotype modulation in vascular tissue engineering using biochemical and mechanical stimulation. Ann Biomed Eng 31, 391, 2003.
21. Freyria, A.M., Yang, Y., Chajra, H., Rousseau, C.F., Ronziere, M.C., Herbage, D., and El Haj, A.J. Optimization of dynamic culture conditions: effects on biosynthetic activities of chondrocytes grown in collagen sponges. Tissue Eng A11, 674, 2005.
22. Isenberg, B.C., Williams, C., and Tranquillo, R.T. Small-diameter artificial arteries engineered in vitro. Circ Res 98, 25, 2006.
23. De Croos, J.N.A., Dhaliwal, S.S., Grynpas, M.D., Pilliar, R.M., and Kandel, R.A. Cyclic compressive mechanical stimulation induces sequential catabolic and anabolic gene changes in chondrocytes resulting in increased extracellular matrix accumulation. Matrix Biol 26, 323, 2006.
24. Datta, N., Pham, Q.P., Sharma, U., Sikavitsas, V.I., Jansen, J.A., and Mikos, A.G. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci USA 103, 2488, 2006.
25. Nirmalanandhan, V.S., Rao, M., Shearn, J.T., Juncosa-Melvin, N., Gooch, C., and Butler, D.L. Effect of scaffold material, construct length and mechanical stimulation on the in vitro stiffness of the engineered tendon construct. J Bio-mech 41, 822, 2008.
26. Shin, H.J., Lee, C.H., Cho, I.H., Kim, Y., Lee, Y., Kim, I.A., Park, K.-D., Yui, N., and Shin, J.-W. Electrospun PLGA na-nofiber scaffolds for articular cartilage reconstruction: mechanical stability, degradation and cellular responses under mechanical stimulation in vitro. J Biomater Sci Polym Ed 17, 103, 2006.
27. Eastwood, M., Mudera, V.C., McGrouther, D.A., and Brown, R.A. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil Cytoskeleton 40, 13, 1999.
28. Yano, S., Komine, M., Fujimoto, M., Okochi, H., and Tamaki, K. Mechanical stretching in vitro regulates signal transduction pathways and cellular proliferation in human epidermal keratinocytes. J Invest Dermatol 122, 783, 2004.
29. Powell, H.M., and Boyce, S.T. Fiber density of electrospun gelatin scaffolds regulates morphogenesis of dermal-epidermal skin substitutes. J Biomed Mater Res A 84A, 1078, 2008.
30. Swope, V.B., Supp, A.P., and Boyce, S.T. Regulation of cutaneous pigmentation by titration of human melanocytes in cultured skin substitutes grafted to athymic mice. Wound Repair Regen 10, 378, 2006.
31. Gilbert, T.W., Sacks, M.S., Grashow, J.S., Woo, S.L.Y., Ba-dylak, S.F., and Chancellor, M.B. Fiber kinematics of small intestinal submucosa under biaxial and uniaxial stretch. J Biomech Eng 128, 890, 2006.
32. Liao, J., Yang, L., Grashow, J., and Sacks, M.S. Molecular orientation of collagen in intact planar connective tissues under biaxial stretch. Acta Biomater 1, 45, 2005.
33. Boulton, T.G., Yancopoulos, G.D., Gregory, J.S., Slaughter, C., Moomaw, C., Hsu, J., and Cobb, M.H. An insulin stimulated protein kinase similar to yeast kinases involved in cell cycle control. Science 249, 64, 1990.
34. Gomar, F.E., Bernd, A., Bereiter-Hahn, J., and Holzmann, H. A mew model of epidermal differentiation: induction by mechanical stimulation. Arch Dermatol Res 282, 22, 1990.
35. Takei, T., Rivas-Gotz, C., Delling, C.A., Koo, J.T., Mills, I., McCathy, T.L., Centrella, M., and Sumpio, B.E. Effect of strain on human keratinocytes in vitro. J Cell Physiol 173, 64, 1997.
36. Kippenberger, S., Bernd, A., Loitsch, S., Guschel, M., Muller, J., Bereiter-Hahn, J., and Kaufmann, R. Signaling of mechanical stretch in human keratinocytes via MAP kinases. J Invest Dermatol 114, 408, 2000.
37. Pietramaggiori, G., Liu, P., Scherer, S.S., Kaipainen, A., Prsa, M.J., Mayer, H., Newalder, J., Alperovich, M., Mentzer, S.J., Konerding, M.A., Huang, S., Ingber, D.E., and Orgill, D.P. Tensile forces stimulate vascular remodeling and epidermal cell proliferation in living skin. Ann Surg 246, 896, 2007.
38. Li, W.-J., Mauck, R.L., Cooper, J.A., Yuan, X., and Tuan, R.S. Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering. J Biomech 40, 1686, 2007.
39. Lambert, C.A., Soudant, E.P., Nusgens, B.V., and Lapiere, C.M. Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab Invest 66, 441, 1992.
40. Philips, J.A., Vacanti, C.A., and Bonassar, L.J. Fibroblasts regulate contractile force independent of MMP activity in 3D-collagen. Biochem Biophys Res Commun 312, 725, 2003.
41. Candi, E., Schmidtm, R., and Melino, G. The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol 6, 328, 2005.
42. Nemes, Z., and Steinert, P.M. Bricks and mortar of the epidermal barrier. Exp Mol Med 31, 5, 1999.
43. Ishida-Yamamoto, A., and Iizuka, H. Structural organization of cornified cell envelopes and alterations in inherited skin disorders. Exp Dermatol 7, 1, 1998.
44. Koch, P.J., de Viragh, P.A., Scharer, E., Bundman, D., Longley, M.A., Bickenbach, J., Kawachi, Y., Suga, Y., Zhou, Z., Huber, M., Hohl, D., Kartasova, T., Jarnik, M., Steven, A.C., and Roop, D.R. Lessons from loricrin-deficient mice: compensatory mechanisms maintaining skin barrier function in the absence of a major cornified envelope protein. J Cell Biol 151, 389, 2000.
45. Wu, Q.Q., and Chen, Q. Mechanoregulation of chondrocyte proliferation, maturation, and hypertrophy: ion-channel dependent transduction of matrix deformation signals. Exp Cell Res 256, 383, 2000.
46. Hu, H., and Sachs, M.F. Stretch-activated ion channels in the heart. J Mol Cell Cardiol 29, 1511, 2007.
47. Hohl, D., Mehrel, T., Lichti, U., Turner, M.L., Roop, D.R., and Steinert, P.M. Characterization of human loricrin. Structure and function of a new class of epidermal cell envelope proteins. J Biol Chem 266, 6626, 1991.
48. 2\+ inhibits murine keratinocyte differentiation in vitro. J Cell Physiol 163, 105, 1995.
49. De Filippo, R.E., and Atala, A. Stretch and growth: the molecular and physiologic influences of tissue expansion. Plast Reconstr Surg 109, 2450, 2002