Three-dimensional traction forces of Schwann cells on compliant substrates

Journal of the Royal Society Interface

Volumn 11, Issue 97, 2014, Pages

  López Fagundo, Cristina ^a,c,d   Bar Kochba, Eyal ^b   Livi, Liane L ^a,c   Hoffman Kim, Diane ^a,b,c   Franck, Christian ^b,c  

^a Physiology and Biotechnology ^*  (United States)

^b Brown University   (United States)

^c BROWN UNIVERSITY   (United States)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cell mechanics; Schwann cell; Traction force microscopy

Indexed keywords

CELL CULTURE; NEURONS; PROTEINS; SCAFFOLDS (BIOLOGY); STIFFNESS; TRACTION (FRICTION);

CELL MECHANICS; FUNCTIONAL INTEGRATION; MECHANICAL INTERACTIONS; PERIPHERAL NERVOUS SYSTEM; SCHWANN CELLS; THREE-DIMENSIONAL CHARACTERISTICS; TISSUE ENGINEERING SCAFFOLD; TRACTION FORCE MICROSCOPIES;

SUBSTRATES;

F ACTIN; ACTIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BIOPHYSICS; CELL INTERACTION; CELL STRUCTURE; CELL TYPE; FIBROBLAST; FORCE; MECHANICAL STRESS; MICROENVIRONMENT; NONHUMAN; RIGIDITY; SCHWANN CELL; TISSUE ENGINEERING; TRACTION THERAPY; YOUNG MODULUS; ANIMAL; BIOLOGICAL MODEL; CELL ADHESION; CELL CULTURE; CELL MOTION; COMPUTER SIMULATION; CYTOLOGY; CYTOSKELETON; FRICTION; MECHANOTRANSDUCTION; PHYSIOLOGY; RAT; SURFACE PROPERTY; TUMOR MICROENVIRONMENT;

ACTINS; ANIMALS; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; COMPUTER SIMULATION; CYTOSKELETON; ELASTIC MODULUS; FRICTION; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; RATS; SCHWANN CELLS; STRESS, MECHANICAL; SURFACE PROPERTIES;

EID: 84903643136     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.0247     Document Type: Article

References (43)

1. Horner PJ, Gage FH. 2000 Regenerating the damaged central nervous system. Nature 407, 963-970. (doi:10.1038/35039559)
2. Jessen KR, Mirsky R. 1999 Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci. 22, 402-410. (doi:10.1016/S0166-2236(98)01391-5)
3. Jessen KR, Mirsky R. 2005 The origin and development of glial cells in peripheral nerves. Nat. Rev. Neurosci. 6, 671-682. (doi:10.1038/nrn1746)
4. Bhatheja K, Field J. 2006 Schwann cells: origins and role in axonal maintenance and regeneration. Int. J. Biochem. Cell Biol. 38, 1995-1999. (doi:10. 1016/j.biocel.2006.05.007)
5. Hoke A. 2006 Mechanisms of disease: what factors limit the success of peripheral nerve regeneration in humans? Nat. Clin. Pract. Neurol. 2, 448-454. (doi:10.1038/ncpneuro0262)
6. Rodrigues MCO, Rodrigues AA, Glover LE, Voltarelli J, Borlongan CV. 2012 Peripheral nerve repair with cultured Schwann cells: getting closer to the clinics. Sci. World J. 2012, 413091. (doi:10.1100/2012/413091)
7. Kromer LF, Cornbrooks CJ. 1985 Transplants of Schwann cell cultures promote axonal regeneration in the adult mammalian brain. Proc. Natl Acad. Sci. USA 82, 6330-6334. (doi:10.1073/pnas.82. 18.6330)
8. Bunge MB. 1994 Transplantation of purified populations of Schwann cells into lesioned adult rat spinal cord. J. Neurol. 242, S36-S39. (doi:10.1007/ BF00939240)
9. Xu XM, Guénard V, Kleitman N, Bunge MB. 1995 Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351, 145-160. (doi:10.1002/cne.903510113)
10. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE. 2004 Myotubes differentiate optimally on substrates with tissue-like stiffness pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887. (doi:10.1083/jcb.200405004)
11. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006 Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. (doi:10.1016/j.cell.2006.06. 044)
12. Oakes PW, Patel DC, Morin NA, Zitterbart DP, Fabry B, Reichner JS, Tang JX. 2009 Neutrophil morphology and migration are affected by substrate elasticity. Blood 114, 1387-1395. (doi:10.1182/ blood-2008-11-191445)
13. Pelham RJ, Wang Y-L. 1997 Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13 661-13 665. (doi:10.1073/pnas.94.25.13661)
14. Wang H-B, Dembo M, Wang Y-L. 2000 Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am. J. Physiol. Cell Physiol. 279, C1345-C1350.
15. Gu Y, Ji Y, Zhao Y, Liu Y, Ding F, Gu X, Yang Y. 2012 The influence of substrate stiffness on the behavior and functions of Schwann cells in culture. Biomaterials 33, 6672-6681. (doi:10.1016/j. biomaterials.2012.06.006)
16. Hirakawa K, Hashizume K, Hayashi T. 1981 Viscoelastic property of human brain for the analysis of impact injury (author's transl). No To Shinkei 33, 1057-1065.
17. Miller K, Chinzei K, Orssengo G, Bednarz P. 2000 Mechanical properties of brain tissue in vivo: experiment and computer simulation. J. Biomech. 33, 1369-1376. (doi:10.1016/S0021-9290(00)00120-2)
18. Mitchel JA, Hoffman-Kim D. 2011 Cellular scale anisotropic topography guides Schwann cell motility. PLoS ONE 6, e24316. (doi:10.1371/journal. pone.0024316)
19. Wang Y, Teng H-L, Huang Z-H. 2012 Intrinsic migratory properties of cultured Schwann cells based on single-cell migration assay. PLoS ONE 7, e51824. (doi:10.1371/journal.pone.0051824)
20. Legant WR, Choi CK, Miller JS, Shao L, Gao L, Betzig E, Chen CS. 2013 Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions. Proc. Natl Acad. Sci. USA 110, 881-886. (doi:10.1073/pnas.1207997110)
21. Toyjanova J, Bar-Kochba E, Lopez-Fagundo C, Reichner JS, Hoffman-Kim D, Franck C. 2014 High resolution, large deformation 3D traction force microscopy. PLoS ONE 9, e90976. (doi:10.1371/ journal.pone.0090976)
22. Bar-Kochba E, Toyjanova J, Andrews E, Kim K-S, Franck C. In press. A fast iterative digital volume correlation algorithm for large deformations. Exp. Mech. (doi:10.1007/s11340-014-9874-2)
23. Farid H, Simoncelli EP. 2004 Differentiation of discrete multidimensional signals. IEEE Trans. Image Process. 13, 496-508. (doi:10.1109/TIP.2004.823819)
24. Butler JP, Tolić-Nørrelykke IM, Fabry B, Fredberg JJ. 2002 Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282, C595-C605. (doi:10.1152/ ajpcell. 00270.2001)
25. Hur SS, Zhao Y, Li Y-S, Botvinick E, Chien S. 2009 Live cells exert 3-dimensional traction forces on their substrata. Cell. Mol. Bioeng. 2, 425-436. (doi:10.1007/s12195-009-0082-6)
26. Koch TM, Munster S, Bonakdar N, Butler JP, Fabry B. 2012 3D traction forces in cancer cell invasion. PLoS ONE 7, e33476. (doi:10.1371/journal.pone. 0033476)
27. Maskarinec SA, Franck C, Tirrell DA, Ravichandran G. 2009 Quantifying cellular traction forces in three dimensions. Proc. Natl Acad. Sci. USA 106, 22 108-22 113. (doi:10.1073/pnas.0904565106)
28. Yang Z, Lin J-S, Chen J, Wang JH. 2006 Determining substrate displacement and cell traction fields-a new approach. J. Theor. Biol. 242, 607-616. (doi:10.1016/j.jtbi.2006.05.005)
29. Bower AF. 2011 Applied mechanics of solids. Boca Raton, FL: CRC Press.
30. D'Errico J. 2005 Surface fitting using gridfit. MATLAB central file exchange. See http://www.mathworks. com/matlabcentral/fileexchange/8998- surfacefitting-using-gridfit.
31. Dembo M, Wang Y-L. 1999 Stresses at the cell-tosubstrate interface during locomotion of fibroblasts. Biophys. J. 76, 2307-2316. (doi:10.1016/S0006- 3495(99)77386-8)
32. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. 1997 Geometric control of cell life and death. Science 276, 1425-1428. (doi:10.1126/ science.276.5317.1425)
33. Discher DE, Janmey P, Wang Y-L. 2005 Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143. (doi:10.1126/science. 1116995)
34. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA. 2007 Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93, 4453-4461. (doi:10.1529/biophysj.106.101386)
35. Yeung T et al. 2005 Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskelet. 60, 24-34. (doi:10. 1002/cm.20041)
36. Brown XQ, Ookawa K, Wong JY. 2005 Evaluation of polydimethylsiloxane scaffolds with physiologicallyrelevant elastic moduli: interplay of substrate mechanics and surface chemistry effects on vascular smooth muscle cell response. Biomaterials 26, 3123-3129. (doi:10.1016/j.biomaterials.2004. 08.009)
37. Gardel ML, Sabass B, Ji L, Danuser G, Schwarz US, Waterman CM. 2008 Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell. 183, 999-1005. (doi:10.1083/jcb.200810060)
38. Schwarz U, Balaban N, Riveline D, Addadi L, Bershadsky A, Safran S, Geiger B. 2003 Measurement of cellular forces at focal adhesions using elastic micro-patterned substrates. Mater. Sci. Eng. C 23, 387-394. (doi:10.1016/S0928- 4931(02) 00309-0)
39. Schwarz US, Gardel ML. 2012 United we stand-integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125, 3051-3060. (doi:10.1242/jcs. 093716)
40. Aratyn-Schaus Y, Gardel ML. 2008 Biophysics: clutch dynamics. Science 322, 1646-1647. (doi:10.1126/ science.1168102)
41. Aratyn-Schaus Y, Gardel ML. 2010 Transient frictional slip between integrin and the ECM in focal adhesions under myosin II tension. Curr. Biol. 20, 1145-1153. (doi:10.1016/j.cub.2010. 05.049)
42. Aratyn-Schaus Y, Oakes PW, Gardel ML. 2011 Dynamic and structural signatures of lamellar actomyosin force generation. Mol. Biol. Cell. 22, 1330-1339. (doi:10.1091/mbc.E10-11-0891)
43. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. 2003 Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl Acad. Sci. USA 100, 1484-1489. (doi:10.1073/pnas. 0235407100)