Necking and failure of constrained 3D microtissues induced by cellular tension

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 52, 2013, Pages 20923-20928

  Wang, Hailong ^a   Svoronos, Alexander A ^b   Boudou, Thomas ^a   Sakar, Mahmut Selman ^c   Schell, Jacquelyn Youssef ^b   Morgan, Jeffrey R ^b   Chen, Christopher S ^a   Shenoy, Vivek B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BROWN UNIVERSITY   (United States)

^c ETH ZURICH   (Switzerland)

Author keywords

Tissue mechanics; Tissue remodeling

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE;

ARTICLE; CARDIAC MICROTISSUE; EXTRACELLULAR MATRIX; FIBROBLAST; FINITE ELEMENT ANALYSIS; HEART; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; MECHANICAL STRESS; MECHANOTRANSDUCTION; MICROELECTROMECHANICAL SYSTEM; PRIORITY JOURNAL; RIGIDITY; TISSUE ENGINEERING; TISSUE STRUCTURE;

EID: 84891362168     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1313662110     Document Type: Article

References (41)

1. Hotulainen P, Lappalainen P (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173(3): 383-394.
2. Pollard TD, Wu JQ (2010) Understanding cytokinesis: Lessons from fission yeast. Nat Rev Mol Cell Biol 11(2): 149-155.
3. Dean DM, Rago AP, Morgan JR (2009) Fibroblast elongation and dendritic extensions in constrained versus unconstrained microtissues. Cell Motil Cytoskeleton 66(3): 129-141.
4. Dean DM, Napolitano AP, Youssef J, Morgan JR (2007) Rods, tori, and honeycombs: The directed self-assembly of microtissues with prescribed microscale geometries. FASEB J 21(14): 4005-4012.
5. Legant WR, et al. (2009) Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. Proc Natl Acad Sci USA 106(25): 10097-10102.
6. Boudou T, et al. (2012) A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. Tissue Eng Part A 18(9-10): 910-919.
7. Thomas S, et al. (2011) Src and caveolin-1 reciprocally regulate metastasis via a common downstream signaling pathway in bladder cancer. Cancer Res 71(3): 832-841.
8. Castella LF, Buscemi L, Godbout C, Meister JJ, Hinz B (2010) A new lock-step mechanism of matrix remodelling based on subcellular contractile events. J Cell Sci 123(Pt 10): 1751-1760.
9. Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751): 1139-1143.
10. Saez A, Buguin A, Silberzan P, Ladoux B (2005) Is the mechanical activity of epithelial cells controlled by deformations or forces? Biophys J 89(6):L52-L54.
11. Ghibaudo M, et al. (2008) Traction forces and rigidity sensing regulate cell functions. Soft Matter 4(9): 1836-1843.
12. Mitrossilis D, et al. (2009) Single-cell response to stiffness exhibits muscle-like behavior. Proc Natl Acad Sci USA 106(43): 18243-18248.
13. Steinberg MS (1962) Mechanism of tissue reconstruction by dissociated cells. II. Timecourse of events. Science 137(3532): 762-763.
14. Foty RA, Steinberg MS (2005) The differential adhesion hypothesis: A direct evaluation. Dev Biol 278(1): 255-263.
15. Hansen A, et al. (2010) Development of a drug screening platform based on engineered heart tissue. Circ Res 107(1): 35-44.
16. Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci 126(843): 136-195.
17. Burridge K, Chrzanowska-Wodnicka M (1996) Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 12: 463-518.
18. Mochitate K, Pawelek P, Grinnell F (1991) Stress relaxation of contracted collagen gels: Disruption of actin filament bundles, release of cell surface fibronectin, and down-regulation of DNA and protein synthesis. Exp Cell Res 193(1): 198-207.
19. Grinnell F (1994) Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol 124(4): 401-404.
20. Thomopoulos S, Fomovsky GM, Holmes JW (2005) The development of structural and mechanical anisotropy in fibroblast populated collagen gels. J Biomech Eng 127(5): 742-750.
21. Deshpande VS, McMeeking RM, Evans AG (2006) A bio-chemo-mechanical model for cell contractility. Proc Natl Acad Sci USA 103(38): 14015-14020.
22. Hutchinson JW, Neale KW (1977) Influence of strain-rate sensitivity on necking under uniaxial tension. Acta Metall 25(8): 839-846.
23. ABAQUS Manual (2010) (Dassault Systemes, Providence, RI), Version 6.10.
24. Bushell GR, et al. (1999) Imaging and force-distance analysis of human fibroblasts in vitro by atomic force microscopy. Cytometry 36(3): 254-264.
25. Berry MF, et al. (2006) Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 290(6):H2196-H2203.
26. Chen QZ, et al. (2008) Characterisation of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Biomaterials 29(1): 47-57.
27. Zhao RG, Boudou T, Wang WG, Chen CS, Reich DH (2013) Decoupling cell and matrix mechanics in engineered microtissues using magnetically actuated microcantilevers. Adv Mater 25(12): 1699-1705.
28. Lai VK, Lake SP, Frey CR, Tranquillo RT, Barocas VH (2012) Mechanical behavior of collagen-fibrin co-gels reflects transition from series to parallel interactions with increasing collagen content. J Biomech Eng 134(1):011004.
29. Considère A (1885) Ann Ponts Chaussees 9: 574-775.
30. Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA (2005) Nonlinear elasticity in biological gels. Nature 435(7039): 191-194.
31. Schwarz US, Erdmann T, Bischofs IB (2006) Focal adhesions as mechanosensors: The two-spring model. Biosystems 83(2-3): 225-232.
32. Besser A, Schwarz US (2007) Coupling biochemistry and mechanics in cell adhesion: A model for inhomogeneous stress fiber contraction. N J Phys 9(11):425.
33. Zemel A, Rehfeldt F, Brown AEX, Discher DE, Safran SA (2010) Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 6(6): 468-473.
34. Guthardt Torres P, Bischofs IB, Schwarz US (2012) Contractile network models for adherent cells. Phys Rev E Stat Nonlin Soft Matter Phys 85(1):011913.
35. Köpf MH, Pismen LM (2013) A continuum model of epithelial spreading. Soft Matter 9(14): 3727-3734.
36. Mertz AF, et al. (2013) Cadherin-based intercellular adhesions organize epithelial cellmatrix traction forces. Proc Natl Acad Sci USA 110(3): 842-847.
37. Banerjee S, Marchetti MC (2011) Instabilities and oscillations in isotropic active gels. Soft Matter 7(2): 463-473.
38. Bendix PM, et al. (2008) A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys J 94(8): 3126-3136.
39. Youssef J, Chen P, Shenoy VB, Morgan JR (2012) Mechanotransduction is enhanced by the synergistic action of heterotypic cell interactions and TGF-β1. FASEB J 26(6): 2522-2530.
40. Taber LA (2000) Pattern formation in a nonlinear membrane model for epithelial morphogenesis. Acta Biotheor 48(1): 47-63.
41. Taber LA, Zahalak GI (2001) Theoretical model for myocardial trabeculation. Dev Dyn 220(3): 226-237.