Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes

Journal of Biomedical Materials Research - Part A

Volumn 95, Issue 4, 2010, Pages 1261-1269

  Bajaj, Piyush ^a   Tang, Xin ^a,b   Saif, Taher A ^a,b   Bashir, Rashid ^a  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

beating force; cardiac myocytes; embryonic chicken; focal adhesions; substrate stiffness

Indexed keywords

BEATING FORCE; CARDIAC MYOCYTES; CARDIAC TISSUES; CYTOSKELETAL STRUCTURES; DIFFERENT SUBSTRATES; EMBRYONIC CHICKEN; FOCAL ADHESIONS; FORCE SENSOR; INDIVIDUAL CELLS; LAMININ; MICROELECTROMECHANICAL SYSTEMS; POLYACRYLAMIDES; SIGNIFICANT IMPACTS;

ADHESION; ANIMAL CELL CULTURE; ANIMALS; CELL CULTURE; CONFOCAL MICROSCOPY; FOCUSING; HEART; MICROELECTROMECHANICAL DEVICES; STIFFNESS; TISSUE CULTURE;

SUBSTRATES;

LAMININ; POLYACRYLAMIDE; TISSUE SCAFFOLD;

ANIMAL CELL; ARTICLE; CELL CULTURE; CHICK EMBRYO; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ELASTICITY; EMBRYO; FOCAL ADHESION; GEL; HEART CONTRACTION; HEART MUSCLE CELL; HEART RATE; MUSCLE FORCE; NONHUMAN; PHENOTYPE; TISSUE CULTURE; TISSUE ENGINEERING;

ACRYLIC RESINS; ACTINS; ANIMALS; CHICK EMBRYO; CYTOSKELETON; FLUORESCENCE; FOCAL ADHESIONS; MICRO-ELECTRICAL-MECHANICAL SYSTEMS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHENOTYPE; VINCULIN;

EID: 78449297031     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.32951     Document Type: Article

References (47)

1. Engler AJ, Sen S, Sweeney HL, Discher DE,. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126: 677-689.
2. Flanagan LA, Ju YE, Marg B, Osterfield M, Janmey PA,. Neurite branching on deformable substrates. Neuroreport 2002; 13: 2411-2415.
3. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA,. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 2007; 93: 4453-4461.
4. Lo CM, Wang H-B, Dembo M, Wang YL,. Cell movement is guided by the rigidity of the substrate. Biophys J 2000; 79: 144-152.
5. Engler AJ, Griffin MA, Sen S, BÃnnemann CG, Sweeney HL, Discher DE,. Myotubes differentiate optimally on substrates with tissue-like stiffness. J Cell Biol 2004; 166: 877-887.
6. Wang HB, Dembo M, Wang YL,. Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol 2000; 279: C1345-C1350.
7. Lammerding J, Kamm RD, Lee RT,. Mechanotransduction in cardiac myocytes. Anal N Y Acad Sci 2004; 1015: 53-70.
8. Discher DE, Janmey P, Wang YL,. Tissue cells feel and respond to the stiffness of their substrate. Science 2005; 310: 1139-1143.
9. Engler AJ, Rehfeldt F, Sen S, Discher DE,. Microtissue elasticity: Measurements by atomic force microscopy and its influence on cell differentiation. Methods Cell Biol 2007; 83: 521-545.
10. Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT, Jayasankar V, Morine KJ, Gardner TJ, Discher DE, Sweeney HL,. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 2006; 290: H2196-H2203.
11. Litwin S, Litwin C, Raya T, Warner A, Goldman S,. Contractility and stiffness of noninfarcted myocardium after coronary ligation in rats. Effects of chronic angiotensin converting enzyme inhibition. Circulation 1991; 83: 1028-1037.
12. Wang YL, Pelham RJ,. Preparation of a flexible porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol 1998; 298: 489-496.
13. Damljanovic V, Lagerholm BC, Jacobson K,. Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. BioTechniques 2005; 39: 847-851.
14. Cukierman E, Pankov R, Stevens DR, Yamada KM,. Taking cell-matrix adhesions to the third dimension. Science 2001; 294: 1708-1712.
15. Engler AJ, Bacakova L, Newman C, Hategan A, Griffin M, Discher D,. Substrate compliance versus ligand density in cell on gel responses. Biophys J 2004; 86: 617-628.
16. Gefen A, Margulies SS,. Are in vivo and in situ brain tissues mechanically similar?. J Biomech 2004; 37: 1339-1352.
17. Hertz HR,. Uber die Beruhrung fester elastischer Korper. J.f.d. Reine u. Angewandte Math 1882; 92: 156-171.
18. Radmacher M,. Measuring the elastic properties of biological samples with the AFM. IEEE Eng Med Biol Magn 1997; 16: 47-57.
19. Engler AJ, Richert L, Wong JY, Picart C, Discher DE,. Surface probe measurements of the elasticity of sectioned tissue, thin gels and polyelectrolyte multilayer films: Correlations between substrate stiffness and cell adhesion. Surf Sci 2004; 570: 142-154.
20. Hamburger V, Hamilton HL,. A series of normal stages in the development of the chick embryo. Dev Dyn 1992; 195: 231-272.
21. Abramoff MD, Magelhaes P, Ram SJ,. Image processing with ImageJ. Biophotonics Int 2004; 11: 36-42.
22. Marquez M, Fernandez-Tome MD, Favale N, Pescio L, Sterin-Speziale NB,. Bradykinin modulates focal adhesions and induces stress fiber remodeling in renal papillary collecting duct cells. Am J Physiol Renal Physiol 2008; 294: F603-F613.
23. Cavalcanti-Adam EA, Micoulet A, Blummel J, Auernheimer J, Kessler H, Spatz JP,. Lateral spacing of integrin ligands influences cell spreading and focal adhesion assembly. Eur J Cell Biol 2006; 85: 219-224.
24. Frey MT, Tsai IY, Russell TP, Hanks SK, Wang YL,. Cellular responses to substrate topography: Role of myosin II and focal adhesion kinase. Biophys J 2006; 90: 3774-3782.
25. Katz BZ, Zamir E, Bershadsky A, Kam Z, Yamada KM, Geiger B,. Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Mol Biol Cell 2000; 11: 1047-1060.
26. Guo WH, Frey MT, Burnham NA, Wang YL,. Substrate rigidity regulates the formation and maintenance of tissues. Biophys J 2006; 90: 2213-2220.
27. Lee SW, Otto JJ,. Vinculin and talin: Kinetics of entry and exit from the cytoskeletal pool. Cell Motil Cytoskeleton 1997; 36: 101-111.
28. Geiger B, Bershadsky A, Pankov R, Yamada KM,. Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2001; 2: 793-805.
29. Saunders RM, Holt MR, Jennings L, Sutton DH, Barsukov IL, Bobkov A, Liddington RC, Adamson EA, Dunn GA, Critchley DR,. Role of vinculin in regulating focal adhesion turnover. Eur J Cell Biol 2006; 85: 487-500.
30. Humphries JD, Wang P, Streuli C, Geiger B, Humphries MJ, Ballestrem C,. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J Cell Biol 2007; 179: 1043-1057.
31. Burridge K, Chrzanowska-Wodnicka M,. Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 1996; 12: 463-518.
32. Chrzanowska-Wodnicka M, Burridge K,. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 1996; 133: 1403-1415.
33. Pelham RJ, Wang YL,. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 1997; 94: 13661-13665.
34. Zaidel BR, Ballestrem C, Kam Z, Geiger B,. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 2003; 116: 4605-4613.
35. Saez A, Buguin A, Silberzan P, Ladoux B,. Is the mechanical activity of epithelial cells controlled by deformations or forces?. Biophys J 2005; 89: L52-L54.
36. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, Funaki M, Zahir N, Ming WY, Weaver V, Janmey PA,. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 2005; 60: 24-34.
37. Beningo KA, Dembo M, Kaverina I, Small JV, Wang YL,. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J Cell Biol 2001; 153: 881-887.
38. Yang S, Saif MT,. Micromachined force sensors for the study of cell mechanics. Rev Sci Instrum 2005; 76: 044301-044301-8.
39. Yang S, Saif MT,. Force response and actin remodeling (agglomeration) in fibroblasts due to lateral indentation. Acta Biomater 2007; 3: 77-87.
40. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, Geiger B,. Force and focal adhesion assembly: A close relationship studied using elastic micropatterned substrates. Nat Cell Biol 2001; 3: 466-472.
41. Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang HY, Speicher DW, Sanger JW, Sanger JM, Discher DE,. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: Scar-like rigidity inhibits beating. J Cell Sci 2008; 121: 3794-3802.
42. Kohl P, Camelliti P, Burton FL, Smith GL,. Electrical coupling of fibroblasts and myocytes: Relevance for cardiac propagation. J Electrocardiol 2005; 38: 45-50.
43. Harary I, Farley B,. In vitro studies on single beating rat heart cells: Growth and organization. Exp Cell Res 1963; 29: 451-465.
44. Jacot JG, McCulloch AD, Omens JH,. Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 2008; 95: 3479-3487.
45. Bhana B, Iyer RK, Chen WL, Zhao RG, Sider KL, Likhitpanichkul M, Simmons CA, Radisic M,. Influence of substrate stiffness on the phenotype of heart cells. Biotechnol Bioeng 2010: 1148-1160.
46. Dabiri GA, Turnacioglu KK, Sanger JM, Sanger JW,. Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci USA 1997; 94: 9493-9498.
47. Dlugosz AA, Antin PB, Nachmias VT, Holtzer H,. The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J Cell Biol 1984; 99: 2268-2278.