Biomaterials Research (생체재료학회지)

Korean Society for Biomaterials (한국생체재료학회)
권호 표지
DOI QR코드

DOI QR Code

Biomimetic substrate control of cellular mechanotransduction

  • Andalib, Mohammad Nahid (Department of Mechanical and Materials Engineering, University of Nebraska-Lincoln) ;
  • Dzenis, Yuris (Department of Mechanical and Materials Engineering, University of Nebraska-Lincoln) ;
  • Donahue, Henry J. (Department of Biomedical Engineering, Virginia Commonwealth University) ;
  • Lim, Jung Yul (Department of Mechanical and Materials Engineering, University of Nebraska-Lincoln)
  • Received : 2016.03.03
  • Accepted : 2016.04.12
  • Published : 2016.06.01
⟨ Previous Next ⟩

Abstract

Extracellular mechanophysical signals from both static substrate cue and dynamic mechanical loading have strong potential to regulate cell functions. Most of the studies have adopted either static or dynamic cue and shown that each cue can regulate cell adhesion, spreading, migration, proliferation, lineage commitment, and differentiation. However, there is limited information on the integrative control of cell functions by the static and dynamic mechanophysical signals. For example, a majority of dynamic loading studies have tested mechanical stimulation of cells utilizing cultures on flat surfaces without any surface modification. While these approaches have provided significant information on cell mechanotransduction, obtained outcomes may not correctly recapitulate complex cellular mechanosensing milieus in vivo. Several pioneering studies documented cellular response to mechanical stimulations upon cultures with biomimetic substrate modifications. In this min-review, we will highlight key findings on the integrative role of substrate cue (topographic, geometric, etc.) and mechanical stimulation (stretch, fluid shear) in modulating cell function and fate. The integrative approaches, though not fully established yet, will help properly understand cell mechanotransduction under biomimetic mechanophysical environments. This may further lead to advanced functional tissue engineering and regenerative medicine protocols.

Keywords

Acknowledgement

Supported by : NSF, NIH, ONR

References

  1. Delaine-Smith RM, Reilly GC. Mesenchymal stem cell responses to mechanical stimuli. Muscles Ligaments Tendons J. 2012;2:169-80.
  2. Maul TM, Chew DW, Nieponice A, Vorp DA. Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech Model Mechanobiol. 2011;10:939-53. https://doi.org/10.1007/s10237-010-0285-8
  3. Riehl BD, Lee JS, Ha L, Lim JY. Fluid-flow-induced mesenchymal stem cell migration: role of focal adhesion kinase and RhoA kinase sensors. J R Soc Interface. 2015;12:20141351. https://doi.org/10.1098/rsif.2014.1351
  4. Lee JS, Ha L, Park J-H, Lim JY. Mechanical stretch suppresses BMP4 induction of stem cell adipogenesis via upregulating ERK but not through downregulating Smad or p38. Biochem Biophys Res Commun. 2012;418:278-83. https://doi.org/10.1016/j.bbrc.2012.01.010
  5. Higgins S, Lee JS, Ha L, Lim JY. Inducing neurite outgrowth by mechanical cell stretch. Biores Open Access. 2013;2:212-6. https://doi.org/10.1089/biores.2013.0008
  6. Stoll H, Hamel FG, Lee JS, Ha L, Lim JY. Mechanical control of mesenchymal stem cell adipogenesis. Endocrinol Metab Syndr. 2015;4:152.
  7. McCain ML, Parker KK. Mechanotransduction: the role of mechanical stress, myocyte shape, and cytoskeletal architecture on cardiac function. Pflugers Arch Eur J Physiol. 2011;462:89-104. https://doi.org/10.1007/s00424-011-0951-4
  8. Adam C. Endogenous musculoskeletal tissue engineering-a focused perspective. Cell Tissue Res. 2012;347:489-99. https://doi.org/10.1007/s00441-011-1234-2
  9. Egginton S. Invited review: activity-induced angiogenesis. Pflugers Arch Eur J Physiol. 2009;457:963-77. https://doi.org/10.1007/s00424-008-0563-9
  10. Hsu S-L, Liang R, Woo SL. Functional tissue engineering of ligament healing. Sports Med Arthrosc Rehabil Ther Technol. 2010;2:12.
  11. Thompson WR, Rubin CT, Rubin J. Mechanical regulation of signaling pathways in bone. Gene. 2012;503:179-93. https://doi.org/10.1016/j.gene.2012.04.076
  12. Powell HM, McFarland KL, Butler DL, Supp DM, Boyce ST. Uniaxial strain regulates morphogenesis, gene expression, and tissue strength in engineered skin. Tissue Eng Part A. 2010;16:1083-92.
  13. Riha GM, Wang X, Wang H, Chai H, Mu H, Lin PH, et al. Cyclic strain induces vascular smooth muscle cell differentiation from murine embryonic mesenchymal progenitor cells. Surgery. 2007;141:394-402. https://doi.org/10.1016/j.surg.2006.07.043
  14. McMahon LA, Reid AJ, Campbell VA, Prendergast PJ. Regulatory effects of mechanical strain on the chondrogenic differentiation of MSCs in a collagen-GAG scaffold: experimental and computational analysis. Ann Biomed Eng. 2008;36:185-94. https://doi.org/10.1007/s10439-007-9416-5
  15. Bai K, Huang Y, Jia X, Fan Y, Wang W. Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations. J Biomech. 2010;43:1176-81. https://doi.org/10.1016/j.jbiomech.2009.11.030
  16. McFetridge PS, Abe K, Horrocks M, Chaudhuri JB. Vascular tissue engineering: bioreactor design considerations for extended culture of primary human vascular smooth muscle cells. ASAIO J. 2007;53:623-30. https://doi.org/10.1097/MAT.0b013e31812f3b7e
  17. Lim JY, Donahue HJ. Cell sensing and response to micro- and nanostructured surfaces produced by chemical and topographic patterning. Tissue Eng. 2007;13:1879-91. https://doi.org/10.1089/ten.2006.0154
  18. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. Micropatterned surfaces for control of cell shape, position, and function. Biotechnol Prog. 1998;14:356-63. https://doi.org/10.1021/bp980031m
  19. Shekaran A, Garcia AJ. Nanoscale engineering of extracellular matrixmimetic bioadhesive surfaces and implants for tissue engineering. Biochim Biophys Acta. 1810;2011:350-60.
  20. Andalib MN, Lee JS, Ha L, Dzenis Y, Lim JY. The role of RhoA kinase (ROCK) in cell alignment on nanofibers. Acta Biomater. 2013;9:7737-45. https://doi.org/10.1016/j.actbio.2013.04.013
  21. Lim JY, Siedlecki CA, Donahue HJ. Nanotopographic cell culture substrate: polymer-demixed nanotextured films under cell culture conditions. Biores Open Access. 2012;1:252-5. https://doi.org/10.1089/biores.2012.0255
  22. Do AV, Khorsand B, Geary SM, Salem AK. 3D printing of scaffolds for tissue regeneration applications. Adv Healthc Mater. 2015;4:1742-62. https://doi.org/10.1002/adhm.201500168
  23. Moretti M, Prina-Mello A, Reid AJ, Barron V, Prendergast PJ. Endothelial cell alignment on cyclically-stretched silicone surfaces. J Mater Sci Mater Med. 2004;15:1159-64. https://doi.org/10.1023/B:JMSM.0000046400.18607.72
  24. Neidlinger-Wilke C, Grood E, Claes L, Brand R. Fibroblast orientation to stretch begins within three hours. J Orthop Res. 2002;20:953-6. https://doi.org/10.1016/S0736-0266(02)00024-4
  25. Riehl BD, Park J-H, Kwon IK, Lim JY. Mechanical stretching for tissue engineering: two-dimensional and three-dimensional constructs. Tissue Eng Part B Rev. 2012;18:288-300. https://doi.org/10.1089/ten.teb.2011.0465
  26. Wang JH-C, Yang G, Li Z, Shen W. Fibroblast responses to cyclic mechanical stretching depend on cell orientation to the stretching direction. J Biomech. 2004;37:573-6. https://doi.org/10.1016/j.jbiomech.2003.09.011
  27. Wang JH, Grood ES. The strain magnitude and contact guidance determine orientation response of fibroblasts to cyclic substrate strains. Connect Tissue Res. 2000;41:29-36. https://doi.org/10.3109/03008200009005639
  28. Loesberg WA, Walboomers XF, van Loon JJWA, Jansen JA. The effect of combined cyclic mechanical stretching and microgrooved surface topography on the behavior of fibroblasts. J Biomed Mater Res A. 2005;75:723-32.
  29. Houtchens GR, Foster MD, Desai TA, Morgan EF, Wong JY. Combined effects of microtopography and cyclic strain on vascular smooth muscle cell orientation. J Biomech. 2008;41:762-9. https://doi.org/10.1016/j.jbiomech.2007.11.027
  30. Prodanov L, te Riet J, Lamers E, Domanski M, Luttge R, van Loon JJWA, et al. The interaction between nanoscale surface features and mechanical loading and its effect on osteoblast-like cells behavior. Biomaterials. 2010;31:7758-65. https://doi.org/10.1016/j.biomaterials.2010.06.050
  31. Ahmed WW, Wolfram T, Goldyn AM, Bruellhoff K, Rioja BA, Moller M, et al. Myoblast morphology and organization on biochemically micro-patterned hydrogel coatings under cyclic mechanical strain. Biomaterials. 2010;31:250-8. https://doi.org/10.1016/j.biomaterials.2009.09.047
  32. Park SA, Kim IA, Lee YJ, Shin JW, Kim C-R, Kim JK, et al. Biological responses of ligament fibroblasts and gene expression profiling on micropatterned silicone substrates subjected to mechanical stimuli. J Biosci Bioeng. 2006; 102:402-12. https://doi.org/10.1263/jbb.102.402
  33. Wang JH-C, Jia F, Yang G, Yang S, Campbell BH, Stone D, et al. Cyclic mechanical stretching of human tendon fibroblasts increases the production of prostaglandin E2 and levels of cyclooxygenase expression: a novel in vitro model study. Connect Tissue Res. 2003;44:128-33. https://doi.org/10.1080/03008200390223909
  34. Li Y, Chu JS, Kurpinski K, Li X, Bautista DM, Yang L, et al. Biophysical regulation of histone acetylation in mesenchymal stem cells. Biophys J. 2011;100:1902-9. https://doi.org/10.1016/j.bpj.2011.03.008
  35. Gopalan SM, Flaim C, Bhatia SN, Hoshijima M, Knoell R, Chien KR, Omens JHMA. Anisotropic stretch-induced hypertrophy in neonatal ventricular myocytes micropatterned on deformable elastomers. Biotechnol Bioeng. 2003;81:578-87. https://doi.org/10.1002/bit.10506
  36. Lee CH, Shin HJ, Cho IH, Kang Y-M, Kim IA, Park K-D, et al. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials. 2005;26:1261-70. https://doi.org/10.1016/j.biomaterials.2004.04.037
  37. Han WM, Heo S-J, Driscoll TP, Boggs ME, Duncan RL, Mauck RL, et al. Impact of cellular microenvironment and mechanical perturbation on calcium signalling in meniscus fibrochondrocytes. Eur Cell Mater. 2014;27:321-31. https://doi.org/10.22203/eCM.v027a23
  38. Subramony SD, Dargis BR, Castillo M, Azeloglu EU, Tracey MS, Su A, et al. The guidance of stem cell differentiation by substrate alignment and mechanical stimulation. Biomaterials. 2013;34:1942-53. https://doi.org/10.1016/j.biomaterials.2012.11.012
  39. Haq F, Keith C, Zhang G. Neurite development in PC12 cells on flexible micro-textured substrates under cyclic stretch. Biotechnol Prog. 2006;22: 133-40. https://doi.org/10.1021/bp0501625
  40. Saldana L, Crespo L, Bensiamar F, Arruebo M, Vilaboa N. Mechanical forces regulate stem cell response to surface topography. J Biomed Mater Res A. 2014;102:128-40. https://doi.org/10.1002/jbm.a.34674
  41. Morgan JT, Wood JA, Shah NM, Hughbanks ML, Russell P, Barakat AI, et al. Integration of basal topographic cues and apical shear stress in vascular endothelial cells. Biomaterials. 2012;33:4126-35. https://doi.org/10.1016/j.biomaterials.2012.02.047
  42. Uttayarat P, Chen M, Li M, Allen FD, Composto RJ, Lelkes PI. Microtopography and flow modulate the direction of endothelial cell migration. Am J Physiol Heart Circ Physiol. 2008;294:H1027-35. https://doi.org/10.1152/ajpheart.00816.2007
  43. Hsu S, Thakar R, Liepmann D, Li S. Effects of shear stress on endothelial cell haptotaxis on micropatterned surfaces. Biochem Biophys Res Commun. 2005;337:401-9. https://doi.org/10.1016/j.bbrc.2005.08.272
  44. Wallin P, Zanden C, Carlberg B, Hellstrom Erkenstam N, Liu J, Gold J. A method to integrate patterned electrospun fibers with microfluidic systems to generate complex microenvironments for cell culture applications. Biomicrofluidics. 2012;6:24131. https://doi.org/10.1063/1.4729747
  45. Zhong W, Zhang W, Wang S, Qin J. Regulation of fibrochondrogenesis of mesenchymal stem cells in an integrated microfluidic platform embedded with biomimetic nanofibrous scaffolds. PLoS One. 2013;8:e61283. https://doi.org/10.1371/journal.pone.0061283
  46. Kim IA, Park SA, Kim YJ, Kim S-H, Shin HJ, Lee YJ, et al. Effects of mechanical stimuli and microfiber-based substrate on neurite outgrowth and guidance. J Biosci Bioeng. 2006;101:120-6. https://doi.org/10.1263/jbb.101.120
  47. Whited BM, Rylander MN. The influence of electrospun scaffold topography on endothelial cell morphology, alignment, and adhesion in response to fluid flow. Biotechnol Bioeng. 2014;111:184-95. https://doi.org/10.1002/bit.24995
  48. Salvi JD, Lim JY, Donahue HJ. Increased mechanosensitivity of cells cultured on nanotopographies. J Biomech. 2010;43:3058-62. https://doi.org/10.1016/j.jbiomech.2010.07.015
  49. Lim JY, Dreiss AD, Zhou Z, Hansen JC, Siedlecki CA, Hengstebeck RW, et al. The regulation of integrin-mediated osteoblast focal adhesion and focal adhesion kinase expression by nanoscale topography. Biomaterials. 2007;28: 1787-97. https://doi.org/10.1016/j.biomaterials.2006.12.020
  50. Hansen JC, Lim JY, Xu L-C, Siedlecki CA, Mauger DT, Donahue HJ. Effect of surface nanoscale topography on elastic modulus of individual osteoblastic cells as determined by atomic force microscopy. J Biomech. 2007;40:2865-71. https://doi.org/10.1016/j.jbiomech.2007.03.018
  51. Lim JY, Loiselle AE, Lee JS, Zhang Y, Salvi JD, Donahue HJ. Optimizing the osteogenic potential of adult stem cells for skeletal regeneration. J Orthop Res. 2011;29:1627-33. https://doi.org/10.1002/jor.21441
  52. Sonam S, Sathe SR, Yim EK, Sheetz MP, Lim CT. Cell contractility arising from topography and shear flow determines human mesenchymal stem cell fate. Sci Rep. 2016;6:20415. https://doi.org/10.1038/srep20415

Cited by

  1. The cell-stretcher: A novel device for the mechanical stimulation of cell populations vol.87, pp.8, 2016, https://doi.org/10.1063/1.4959884
  2. Genetically Engineered Phage Induced Selective H9c2 Cardiomyocytes Patterning in PDMS Microgrooves vol.10, pp.8, 2016, https://doi.org/10.3390/ma10080973
  3. Study of myoblast differentiation using multi-dimensional scaffolds consisting of nano and micropatterns vol.21, pp.1, 2017, https://doi.org/10.1186/s40824-016-0087-x
  4. Selective cell response on natural polymer bio-interfaces textured by femtosecond laser vol.124, pp.2, 2016, https://doi.org/10.1007/s00339-018-1628-z
  5. The Effect of Physical Cues on the Stem Cell Differentiation vol.14, pp.3, 2016, https://doi.org/10.2174/1574888x14666181227120706
  6. Emerging Development of Microfluidics-Based Approaches to Improve Studies of Muscle Cell Migration vol.25, pp.1, 2016, https://doi.org/10.1089/ten.teb.2018.0181
  7. Driving Cells with Light‐Controlled Topographies vol.6, pp.14, 2016, https://doi.org/10.1002/advs.201801826
  8. Chitosan films for regenerative medicine: fabrication methods and mechanical characterization of nanostructured chitosan films vol.11, pp.5, 2016, https://doi.org/10.1007/s12551-019-00591-6
  9. Plant-Based Scaffolds Modify Cellular Response to Drug and Radiation Exposure Compared to Standard Cell Culture Models vol.8, pp.None, 2016, https://doi.org/10.3389/fbioe.2020.00932
  10. Stretching of fibroblast cells on micropatterned gelatin on silicone elastomer vol.8, pp.3, 2016, https://doi.org/10.1039/c9tb02203a
  11. Topographic Guidance in Melt-Electrowritten Tubular Scaffolds Enhances Engineered Kidney Tubule Performance vol.8, pp.None, 2016, https://doi.org/10.3389/fbioe.2020.617364