Microtopographical cues in 3D attenuate fibrotic phenotype and extracellular matrix deposition: Implications for tissue regeneration

Tissue Engineering - Part A

Volumn 16, Issue 8, 2010, Pages 2519-2527

  Ayala, Perla ^a   Lopez, Jose I ^b   Desai, Tejal A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; CELL PROLIFERATION; ETHYLENE; ETHYLENE GLYCOL; FIBROBLASTS; GELS; GENE EXPRESSION; GROWTH KINETICS; MECHANICAL PROPERTIES; MUSCLE; PHOTOLITHOGRAPHY; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; PROTEINS; THREE DIMENSIONAL;

3D CULTURE; ADHESION MOLECULES; CELL FUNCTIONS; CELL MORPHOLOGY; CYCLIND1; EXTRACELLULAR MATRIX DEPOSITION; EXTRACELLULAR MATRIX PROTEIN; EXTRACELLULAR MATRIX SYNTHESIS; FIBROBLAST PROLIFERATION; INTEGRINS; MATRIX; MICRO-MECHANICAL; MICRO-SCALES; MICRORODS; PHYSIOLOGICAL RANGE; POLY(ETHYLENE GLYCOL) DIMETHACRYLATE; SCAR TISSUES; SMOOTH MUSCLE ACTINS; SUBSTRATE GEOMETRY; THREE DIMENSIONS; THREE-DIMENSIONAL (3D); TISSUE REGENERATION; TUNABLE ELASTICITY; TWO-DIMENSION;

CELL CULTURE;

BIOMATERIAL;

ANIMAL; ARTICLE; CELL PROLIFERATION; CELL STRAIN 3T3; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; EXTRACELLULAR MATRIX; FIBROBLAST; MATERIALS TESTING; METHODOLOGY; MOUSE; PHENOTYPE; PHYSIOLOGY; REGENERATION; SURFACE PROPERTY; TISSUE ENGINEERING; YOUNG MODULUS;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; ELASTIC MODULUS; EXTRACELLULAR MATRIX; FIBROBLASTS; MATERIALS TESTING; MICE; NIH 3T3 CELLS; PHENOTYPE; REGENERATION; SURFACE PROPERTIES; TISSUE ENGINEERING;

EID: 77956075225     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0815     Document Type: Article

References (55)

1. Fazel, S., Cimini, M., Chen, L., Li, S., Angoulvant, D., Fedak, P., Verma, S., Weisel, R.D., Keating, A., and Li, R.K. Cardio-protective c-kit\+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 116, 1865, 2006.
2. Paul, D., Samuel, S.M., and Maulik, N. Mesenchymal stem cell: present challenges and prospective cellular cardio-myoplasty approaches for myocardial regeneration. Anti-oxid Redox Signal 11, 1841, 2009.
3. Kawamoto, A., Iwasaki, H., Kusano, K., Murayama, T., Oyamada, A., Silver, M., Hulbert, C., Gavin, M., Hanley, A., Ma, H., Kearney, M., Zak, V., Asahara, T., and Losordo, D.W. CD34-positive cells exhibit increased potency and safety for therapeutic neovascularization after myocardial infarction compared with total mononuclear cells. Circulation 114, 2163, 2006.
4. Boateng, S.Y., Hartman, T.J., Ahluwalia, N., Vidula, H., De-sai, T.A., and Russell, B. Inhibition of fibroblast proliferation in cardiac myocyte cultures by surface microtopography. Am J Physiol Cell Physiol 285, C171, 2003.
5. Brown, X.Q., Ookawa, K., and Wong, J.Y. Evaluation of polydimethylsiloxane scaffolds with physiologically-relevant elastic moduli: interplay of substrate mechanics and surface chemistry effects on vascular smooth muscle cell response. Biomaterials 26, 3123, 2005.
6. Chen, C.S., Mrksich, M., Huang, S., Whitesides, G.M., and Ingber, D.E. Geometric control of cell life and death. Science 276, 1425, 1997.
7. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677, 2006.
8. Kim, D.H., Kim, P., Song, I., Cha, J.M., Lee, S.H., Kim, B., and Suh, K.Y. Guided three-dimensional growth of functional cardiomyocytes on polyethylene glycol nanostructures. Langmuir 22, 5419, 2006.
9. Nelson, C.M., Jean, R.P., Tan, J.L., Liu, W.F., Sniadecki, N.J., Spector, A.A., and Chen, C.S. Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci\USA 102, 11594, 2005.
10. Norman, J.J., Collins, J.M., Sharma, S., Russell, B., and Desai, T.A. Microstructures in 3D biological gels affect cell proliferation. Tissue Eng Part A 14, 379, 2008.
11. Pelham, R.J., Jr., and Wang, Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci\USA 94, 13661, 1997.
12. Peyton, S.R., Raub, C.B., Keschrumrus, V.P., and Putnam, A.J. The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. Biomaterials 27, 4881, 2006.
13. Discher, D.E., Mooney, D.J., and Zandstra, P.W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673, 2009.
14. Reilly, G.C., and Engler, A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J Biomech 43, 55, 2009.
15. Butcher, D.T., Alliston, T., and Weaver, V.M. A tense situation: forcing tumour progression. Nat Rev Cancer 9, 108, 2009.
16. Gumbiner, B.M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345, 1996.
17. Nelson, C.M., and Bissell, M.J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22, 287, 2006.
18. Raines, E.W. The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int J Exp Pathol 81, 173, 2000.
19. Discher, D.E., Janmey, P., and Wang, Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139, 2005.
20. Gray, D.S., Tien, J., and Chen, C.S. Repositioning of cells by mechanotaxis on surfaces with micropatterned Young's modulus. J Biomed Mater Res A 66, 605, 2003.
21. Ghosh, K., Pan, Z., Guan, E., Ge, S., Liu, Y., Nakamura, T., Ren, X.D., Rafailovich, M., and Clark, R.A. Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials 28, 671, 2007.
22. Burlew, B.S., and Weber, K.T. Cardiac fibrosis as a cause of diastolic dysfunction. Herz 27, 92, 2002.
23. Levental, K.R., Yu, H., Kass, L., Lakins, J.N., Egeblad, M., Erler, J.T., Fong, S.F., Csiszar, K., Giaccia, A., Weninger, W., Yamauchi, M., Gasser, D.L., and Weaver, V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891, 2009.
24. Le Bousse-Kerdiles, M.C., Martyre, M.C., and Samson, M. Cellular and molecular mechanisms underlying bone marrow and liver fibrosis: a review. Eur Cytokine Netw 19, 69, 2008.
25. Aneja, A., Tang, W.H., Bansilal, S., Garcia, M.J., and Far-kouh, M.E. Diabetic cardiomyopathy: insights into patho-genesis, diagnostic challenges, and therapeutic options. Am J Med 121, 748, 2008.
26. De Wever, O., Demetter, P., Mareel, M., and Bracke, M. Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 123, 2229, 2008.
27. Iyengar, P., Espina, V., Williams, T.W., Lin, Y., Berry, D., Jelicks, L.A., Lee, H., Temple, K., Graves, R., Pollard, J., Chopra, N., Russell, R.G., Sasisekharan, R., Trock, B.J., Lippman, M., Calvert, V.S., Petricoin, E.F., 3rd, Liotta, L., Dadachova, E., Pestell, R.G., Lisanti, M.P., Bonaldo, P., and Scherer, P.E. Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J Clin Invest 115, 1163, 2005.
28. Paz, Z., and Shoenfeld, Y. Antifibrosis: to reverse the irreversible. Clin Rev Allergy Immunol 38, 276, 2009.
29. Sun, Y., Zhang, J.Q., Zhang, J., and Lamparter, S. Cardiac remodeling by fibrous tissue after infarction in rats. J Lab Clin Med 135, 316, 2000.
30. Sun, Y., and Weber, K.T. Infarct scar: a dynamic tissue. Cardiovasc Res 46, 250, 2000.
31. Bryant, J.E., Shamhart, P.E., Luther, D.J., Olson, E.R., Koshy, J.C., Costic, D.J., Mohile, M.V., Dockry, M., Doane, K.J., and Meszaros, J.G. Cardiac myofibroblast differentiation is attenuated by alpha(3) integrin blockade: potential role in post-MI remodeling. J Mol Cell Cardiol 46, 186, 2009.
32. Berry, M.F., Engler, A.J., Woo, Y.J., Pirolli, T.J., Bish, L.T., Jayasankar, V., Morine, K.J., Gardner, T.J., Discher, D.E., and Sweeney, H.L. Mesenchymal stem cell injection after myo-cardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 290, H2196, 2006.
33. Breitbach, M., Bostani, T., Roell, W., Xia, Y., Dewald, O., Nygren, J.M., Fries, J.W., Tiemann, K., Bohlen, H., Hescheler, J., Welz, A., Bloch, W., Jacobsen, S.E., and Fleischmann, B.K. Potential risks of bone marrow cell transplantation into in-farcted hearts. Blood 110, 1362, 2007.
34. Hinz, B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127, 526, 2007.
35. Thakar, R.G., Chown, M.G., Patel, A., Peng, L., Kumar, S., and Desai, T.A. Contractility-dependent modulation of cell proliferation and adhesion by microscale topographical cues. Small 4, 1416, 2008.
36. Collins, J.M., Ayala, P., Desai, T.A., and Russell, B. Three-Dimensional culture with stiff microstructures increases proliferation and slows osteogenic differentiation of human mesenchymal stem cells. Small 6, 355, 2009.
37. Bouffard, N.A., Cutroneo, K.R., Badger, G.J., White, S.L., Buttolph, T.R., Ehrlich, H.P., Stevens-Tuttle, D., and Lange-vin, H.M. Tissue stretch decreases soluble TGF-beta1 and type-1 procollagen in mouse subcutaneous connective tissue: evidence from ex vivo and in vivo models. J Cell Physiol 214, 389, 2008.
38. Langevin, H.M., Bouffard, N.A., Badger, G.J., Iatridis, J.C., and Howe, A.K. Dynamic fibroblast cytoskeletal response to subcutaneous tissue stretch ex vivo and in vivo. Am J Physiol Cell Physiol 288, C747, 2005.
39. Poobalarahi, F., Baicu, C.F., and Bradshaw, A.D. Cardiac myofibroblasts differentiated in 3D culture exhibit distinct changes in collagen I production, processing, and matrix deposition. Am J Physiol Heart Circ Physiol 291, H2924, 2006.
40. Wang, J., Seth, A., and McCulloch, C.A. Force regulates smooth muscle actin in cardiac fibroblasts. Am J Physiol Heart Circ Physiol 279, H2776, 2000.
41. Brown, R.D., Ambler, S.K., Mitchell, M.D., and Long, C.S. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol 45, 657, 2005.
42. Kleinman, H.K., McGarvey, M.L., Hassell, J.R., Star, V.L., Cannon, F.B., Laurie, G.W., and Martin, G.R. Basement membrane complexes with biological activity. Biochemistry 25, 312, 1986.
43. Kleinman, H.K., McGarvey, M.L., Liotta, L.A., Robey, P.G., Tryggvason, K., and Martin, G.R. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21, 6188, 1982.
44. Diramio, J.A., Kisaalita, W.S., Majetich, G.F., and Shimkus, J.M. Poly(ethylene glycol) methacrylate/dimethacrylate hydrogels for controlled release of hydrophobic drugs. Biotechnol Prog 21, 1281, 2005.
45. Pfister, P.M., Wendlandt, M., Neuenschwander, P., and Suter, U.W. Surface-textured PEG-based hydrogels with adjustable elasticity: synthesis and characterization. Biomaterials 28, 567, 2007.
46. Boontheekul, T., Hill, E.E., Kong, H.J., and Mooney, D.J. Regulating myoblast phenotype through controlled gel stiffness and degradation. Tissue Eng 13, 1431, 2007.
47. Costa-Pinto, A.R., Salgado, A.J., Correlo, V.M., Sol, P., Bhattacharya, M., Charbord, P., Reis, R.L., and Neves, N.M. Adhesion, proliferation, and osteogenic differentiation of a mouse mesenchymal stem cell line (BMC9) seeded on novel melt-based chitosan/polyester 3D porous scaffolds. Tissue Eng Part A 14, 1049, 2008.
48. Duong, H., Wu, B., and Tawil, B. Modulation of 3D fibrin matrix stiffness by intrinsic fibrinogen-thrombin compositions and by extrinsic cellular activity. Tissue Eng Part A 15, 1865, 2009.
49. Carver, W., Nagpal, M.L., Nachtigal, M., Borg, T.K., and Terracio, L. Collagen expression in mechanically stimulated cardiac fibroblasts. Circ Res 69, 116, 1991.
50. Caulfield, J.B., and Janicki, J.S. Structure and function of myocardial fibrillar collagen. Technol Health Care 5, 95, 1997.
51. Bashey, R.I., Martinez-Hernandez, A., and Jimenez, S.A. Isolation, characterization, and localization of cardiac collagen type VI. Associations with other extracellular matrix components. Circ Res 70, 1006, 1992.
52. Naugle, J.E., Olson, E.R., Zhang, X., Mase, S.E., Pilati, C.F., Maron, M.B., Folkesson, H.G., Horne, W.I., Doane, K.J., and Meszaros, J.G. Type VI collagen induces cardiac myofibroblast differentiation: implications for postinfarc-tion remodeling. Am J Physiol Heart Circ Physiol 290, H323, 2006.
53. Sherman-Baust, C.A., Weeraratna, A.T., Rangel, L.B., Pizer, E.S., Cho, K.R., Schwartz, D.R., Shock, T., and Morin, P.J. Remodeling of the extracellular matrix through over-expression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cell 3, 377, 2003.
54. Mollnau, H., Munkel, B., and Schaper, J. Collagen VI in the extracellular matrix of normal and failing human myocardium. Herz 20, 89, 1995.
55. Borok, Z. Role for alpha3 integrin in EMT and pulmonary fibrosis. J Clin Invest 119, 7, 2009.