Fibroblast morphology on dynamic softening of hydrogels

Annals of Biomedical Engineering

Volumn 40, Issue 5, 2012, Pages 1061-1072

  Previtera, Michelle L ^a   Trout, Kevin L ^b   Verma, Devendra ^a   Chippada, Uday ^c   Schloss, Rene S ^a   Langrana, Noshir A ^a,c  

^a RUTGERS UNIVERSITY   (United States)

^b School of Health Science   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Compliance; DNA gel; ECM; Stiffness; Strain; Stress; Wound healing

Indexed keywords

CELLULAR ENVIRONMENT; CELLULAR LEVELS; COMPLIANCE; CONTROLLED DELIVERY; DNA GELS; DYNAMIC CHARACTERISTICS; DYNAMIC DEFORMATION; IN-VIVO; LOCAL STRESS; ON DYNAMICS; POLYACRYLAMIDE HYDROGELS; WOUND HEALING;

BIOLOGICAL MATERIALS; CELL CULTURE; DNA; DRUG THERAPY; DYNAMICS; FIBROBLASTS; GELS; MILITARY ELECTRONIC COUNTERMEASURES; MORPHOLOGY; STIFFNESS; STIFFNESS MATRIX; STRAIN; STRESSES;

HYDROGELS;

DNA;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; CYTOLOGY; FIBROBLAST; HYDROGEL; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RAT; SYNTHESIS; WOUND HEALING;

ANIMALS; CELL LINE; DNA; FIBROBLASTS; HYDROGELS; MODELS, BIOLOGICAL; RATS; STRESS, PHYSIOLOGICAL; WOUND HEALING;

EID: 84862024784     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-011-0483-2     Document Type: Article

References (58)

1. Aarabi, S., K. A. Bhatt, Y. Shi, J. Paterno, E. I. Chang, S. A. Loh, J. W. Holmes, M. T. Longaker, H. Yee, and G. C. Gurtner. Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis. FASEB J. 21:3250, 2007.
2. Balaban, N. Q., U. S. Schwarz, D. Riveline, P. Goichberg, G. Tzur, I. Sabanay, D. Mahalu, S. Safran, A. Bershadsky, L. Addadi, and B. Geiger. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3:466-472, 2001. (Pubitemid 32422082)
3. Banerjee, I., K. Yekkala, T. K. Borg, and T. A. Baudino. Dynamic interactions between myocytes, fibroblasts, and extracellular matrix. Ann. N. Y. Acad. Sci. 1080:76-84, 2006. (Pubitemid 44955414)
4. Brown, X. Q., K. Ookawa, and J. Y. Wong. Evaluation of polydimethylsiloxane scaffolds with physiologically-relevant elastic moduli: interplay of substrate mechanics and surface chemistry effects on vascular smooth muscle cell response. Biomaterials 26:3123-3129, 2005. (Pubitemid 39647247)
5. Chippada, U. Non-Intrusive Characterization of Properties of Hydrogels. Rutgers University Electronic Theses and Dissertations, 2010.
6. Chippada, U., B. Yurke, and N. A. Langrana. Simultaneous determination of young's modulus, shear modulus, and Poisson's ratio of soft hydrogels. J. Mater. Res. 25:545-555, 2010.
7. Cukierman, E., R. Pankov, D. R. Stevens, and K. M. Yamada. Taking cell-matrix adhesions to the third dimension. Science. 294:1708-1712, 2001. (Pubitemid 33104840)
8. Dembo, M., and Y. L. Wang. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76:2307-2316, 1999. (Pubitemid 29266384)
9. Eastwood, M., D. A. McGrouther, and R. A. Brown. Fibroblast responses to mechanical forces. Proc. Inst. Mech. Eng. H: J. Eng. Med. 212:85-92, 1998. (Pubitemid 128769985)
10. Engler, A., L. Bacakova, C. Newman, A. Hategan, M. Griffin, and D. Discher. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86:617-628, 2004. (Pubitemid 38067491)
11. Flanagan, L. A., Y. E. Ju, B. Marg, M. Osterfield, and P. A. Janmey. Neurite branching on deformable substrates. Neuroreport. 13:2411, 2002.
12. Frank, C., D. McDonald, J. Wilson, D. Eyre, and N. Shrive. Rabbit medial collateral ligament scar weakness is associated with decreased collagen pyridinoline crosslink density. J. Orthop. Res. 13:157-165, 1995.
13. Friedland, J. C., M. H. Lee, and D. Boettiger. Mechanically activated integrin switch controls alpha(5)beta(1) function. Science. 323:642-644, 2009.
14. Gabbiani, G. The myofibroblast in wound healing and fibrocontractive diseases. J. Pathol. 200:500-503, 2003. (Pubitemid 36818250)
15. Galbraith, C. G., and M. P. Sheetz. A micromachined device provides a new bend on fibroblast traction forces. Proc. Natl Acad. Sci. USA 94:9114-9118, 1997. (Pubitemid 27357791)
16. Galbraith, C. G., and M. P. Sheetz. Forces on adhesive contacts affect cell function. Curr. Opin. Cell Biol. 10:566-571, 1998. (Pubitemid 28477013)
17. Galbraith, C. G., R. Skalak, and S. Chien. Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motil. Cytoskelet. 40:317-330, 1998. (Pubitemid 28364153)
18. Geiger, B., and A. Bershadsky. Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell 110:139-142, 2002. (Pubitemid 34876542)
19. Genes, N. G., J. A. Rowley, D. J. Mooney, and L. J. Bonassar. Effect of substrate mechanics on chondrocyte adhesion to modified alginate surfaces. Arch. Biochem. Biophys. 422:161-167, 2004. (Pubitemid 38169362)
20. Haston, W. S., J. M. Shields, and P. C. Wilkinson. The orientation of fibroblasts and neutrophils on elastic substrata. Exp. Cell Res. 146:117-126, 1983.
21. Huang, S., and D. E. Ingber. The structural and mechanical complexity of cell-growth control. Nat. Cell Biol. 1:E131-E138, 1999.
22. Hynes, R. O. The dynamic dialogue between cells and matrices: implications of fibronectin's elasticity. Proc. Natl Acad. Sci. USA 96:2588-2590, 1999. (Pubitemid 29148760)
23. Ingber, D. E. Mechanosensation through integrins: cells act locally but think globally. Proc. Natl Acad. Sci. USA 100:1472-1474, 2003. (Pubitemid 36254469)
24. Inoh, H., N. Ishiguro, S. Sawazaki, H. Amma, M. Miyazu, H. Iwata, M. Sokabe, and K. Naruse. Uni-axial cyclic stretch induces the activation of transcription factor nuclear factor kappab in human fibroblast cells. FASEB J. 16:405-407, 2002.
25. Jean, C., P. Gravelle, J. J. Fournie, and G. Laurent. Influence of stress on extracellular matrix and integrin biology. Oncogene. 30:2697-2706, 2011.
26. Jiang, X., P. C. Georges, B. Li, Y. Du, M. K. Kutzing, M. L. Previtera, N. A. Langrana, and B. L. Firestein. Cell growth in response to mechanical stiffness is affected by neuron-astroglia interactions. Open Neurosci. J. 1:7-14, 2007.
27. Jiang, F. X., B. Yurke, B. L. Firestein, and N. A. Langrana. Neurite outgrowth on a DNA crosslinked hydrogel with tunable stiffnesses. Ann. Biomed. Eng. 36:1565-1579, 2008.
28. Jiang, F. X., B. Yurke, R. S. Schloss, B. L. Firestein, and N. A. Langrana. Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel. Tissue Eng. A 16:1873-1889, 2010.
29. Jiang, F. X., B. Yurke, R. S. Schloss, B. L. Firestein, and N. A. Langrana. The relationship between fibroblast growth and the dynamic stiffnesses of a DNA crosslinked hydrogel. Biomaterials 31:1199-1212, 2010.
30. Kano, Y., K. Katoh, and K. Fujiwara. Lateral zone of cell- cell adhesion as the major fluid shear stress-related signal transduction site. Circ. Res. 86:425-433, 2000. (Pubitemid 30141761)
31. Kolodney, M. S., and R. B. Wysolmerski. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. J. Cell Biol. 117:73-82, 1992.
32. Kuo, S. C., and M. P. Sheetz. Forces of single kinesin molecules measured with optical tweezers. Science 260:232-234, 1993. (Pubitemid 23140892)
33. Lauffenburger, D. A., and A. F. Horwitz. Cell migration: a physically integrated molecular process. Cell 84:359-369, 1996. (Pubitemid 26058561)
34. Letourneau, P. C., M. L. Condic, and D. M. Snow. Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14:915, 1994.
35. Li, L., A. E. Davidovich, J. M. Schloss, U. Chippada, R. R. Schloss, N. A. Langrana, and M. L. Yarmush. Neural lineage differentiation of embryonic stem cells within alginate microbeads. Biomaterials 32:4489-4497, 2011.
36. Lin, D. C., B. Yurke, and N. A. Langrana. Mechanical properties of a reversible, DNA-crosslinked polyacrylamide hydrogel. J. Biomech. Eng. 126:104, 2004.
37. Lin, D. C., B. Yurke, and N. A. Langrana. Inducing reversible stiffness changes in DNA-crosslinked gels. J. Mater. Res. 20:1456-1464, 2005. (Pubitemid 41787028)
38. Lin, D. C., B. Yurke, and N. A. Langrana. Use of rigid spherical inclusions in young's moduli determination: application to DNA-crosslinked gels. J. Biomech. Eng. 127:571, 2005.
39. Lo, C. M., H. B. Wang, M. Dembo, and Y. L. Wang. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144-152, 2000. (Pubitemid 30436733)
40. MacKenna, D., S. R. Summerour, and F. J. Villarreal. Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis. Cardiovasc. Res. 46:257-263, 2000. (Pubitemid 30204597)
41. Neidlinger-Wilke, C., E. S. Grood, J.-C. Wang, R. A. Brand, and L. Claes. Cell alignment is induced by cyclic changes in cell length: studies of cells grown in cyclically stretched substrates. J. Orthop. Res. 19:286-293, 2001. (Pubitemid 32331705)
42. Pelham, R. J., Jr., and Y. Wang. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94:13661, 1997.
43. Polio, S. R., K. E. Rothenberg, D. Stamenović, and M. L. Smith. A micropatterning and image processing approach to simplify measurement of cellular traction force. Acta Biomater. 8:82-88, 2012.
44. Previtera, M. L., C. G. Langhammer, and B. L. Firestein. Effects of substrate stiffness and cell density on primary hippocampal cultures. J. Biosci. Bioeng. 110:459-470, 2010.
45. Previtera, M. L., C. G. Langhammer, N. A. Langrana, and B. L. Firestein. Dendrite arborization by substrate stiffness is mediated by glutamate receptor. Ann. Biomed. Eng. 38:3733-3743, 2010.
46. Raghow, R. The role of extracellular matrix in postinflammatory wound healing and fibrosis. FASEB J. 8:823, 1994.
47. Sheetz, M. P., D. P. Felsenfeld, and C. G. Galbraith. Cell migration: regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol. 8:51-54, 1998. (Pubitemid 28056811)
48. Singer, A. J., and R. A. F. Clark. Cutaneous wound healing. N. Engl. J. Med. 341:738, 1999.
49. Skutek, M., M. van Griensven, J. Zeichen, N. Brauer, and U. Bosch. Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur. J. Appl. Physiol. 86:48-52, 2001. (Pubitemid 33725691)
50. Solon, J., I. Levental, K. Sengupta, P. C. Georges, and P. A. Janmey. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93:4453-4461, 2007. (Pubitemid 350294491)
51. Sundararaghavan, H. G., G. A. Monteiro, B. L. Firestein, and D. I. Shreiber. Neurite growth in 3D collagen gels with gradients of mechanical properties. Biotechnol. Bioeng. 102:632-643, 2009
52. Thibeault, S. L., S. D. Gray, D. M. Bless, R. W. Chan, and C. N. Ford. Histologic and rheologic characterization of vocal fold scarring. J. Voice 16:96-104, 2002. (Pubitemid 36626574)
53. Tomasek, J. J., G. Gabbiani, B. Hinz, C. Chaponnier, and R. A. Brown. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3:349-363, 2002. (Pubitemid 34619269)
54. Wakatsuki, T., M. S. Kolodney, G. I. Zahalak, and E. L. Elson. Cell mechanics studied by a reconstituted model tissue. Biophys. J. 79:2353-2368, 2000.
55. Wang, N., J. P. Butler, and D. E. Ingber. Mechanotransduction across the cell-surface and through the cytoskeleton. Science. 260:1124-1127, 1993. (Pubitemid 23186787)
56. Wang, H. B., M. Dembo, S. K. Hanks, and Y. Wang. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl Acad. Sci. USA 98:11295, 2001.
57. Yeung, T., P. C. Georges, L. A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W. Ming, V. Weaver, and P. A. Janmey. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskelet. 60:24-34, 2005. (Pubitemid 40066224)
58. Zaman, M. H., L. M. Trapani, A. L. Sieminski, D. Mac- Kellar, H. Gong, R. D. Kamm, A. Wells, D. A. Lauffenburger, and P. Matsudaira. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell- matrix adhesion and proteolysis. Proc. Natl Acad. Sci. USA 103:10889, 2006.