Effect of Mechanical Stimulations on the Fate of Stem Cells – A Review

Authors
M. Halvaei 1
A. Solouk 1
N. Abolfathi 1
N. Haghighipour 2
M. Eskandari 1
M. A. Shokrgozar 2
1 Department of Tissue Engineering, Faculty of Biomedical Engineering, Amirkabir University of Technology, Tehran, Iran
2 National Cell Bank of Iran, Pasteur Institute of Iran, Tehran, Iran
Abstract
The provision of an adequate quantity of cells with proper function and purity is one of the main challenges of tissue engineering studies. Stem cells, with their self-renewal and differentiation capacity, are considered one of the main cell sources in the field of tissue engineering. Previously, the use of chemical factors seemed to be the only possible way for stem cell differentiation. However, scientists have recently realized that physiological processes of the human body are composed of chemical, mechanical and electrical signals. Mechanical stimulation is one of the current methods that produce cells with proper morphology and alignment in the scaffold. Specific differentiation, a higher rate of cell growth, proliferation and differentiation, and lower experiment costs can be achieved using mechanical stimulation. Different parameters such as the chemical environment, physical environment that surrounds the cell (including geometry, stiffness and topology of scaffold surface), amplitude, frequency, and duration of mechanical stimulation can affect the stem cell fate. In this study we have investigated the impact of all types of mechanical stimulations under different loading regimes on the fate of stem cells with respect to the target tissue. The result has been reflected in the design of a proper bioreactor.

Keywords

[1]     Lanza R, Langer R, Vacanti J. Principles of tissue engineering. 3rd Edition, Amsterdam; Boston: Elsevier Academic Press, 2007; p: 135-50, 550-65.
[2]     Freed LE, Guilak F, Guo XE, Gray ML, Tranquillo R, Holmes JW, Radisic M, Sefton MV, Kaplan D, Vunjak-Novakovic G. Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. Tissue Eng 2006; 12(12): 3285-305.
[3]     Goldstein LSB, Schneider M. Stem cells for dummies. Hoboken, NJ: Wiley Publishing, Inc, 2010; p: 19-25, 99-119.
[4]     Li S, L'Heureux N, Elisseeff J. Stem cell and tissue engineering. Singapore: World Scientific, 2011; p: 1-10.
[5]     Kim JH,Cho CS, Choung YH, Lim KT, Son HM, Seonwoo H, Baik SJ, Jeon SH, Park JY, Choung PH, Chung JH. Mechanical stimulation of mesenchymal stem cells for tissue engineering. TERM 2009; 6(1): 199-206.
[6]     Wang JH, Thampatty BP. Mechanobiology of adult and stem cells. Int Rev Cell Mol Biol 2008; 271: 301-46.
[7]     Li D, Zhou J, Chowdhury F, Cheng J, Wang N, Wang F. Role of mechanical factors in fate decisions of stem cells. Regen Med 2011; 6(2): 229-40.
[8]     Clause KC, Liu LJ, Tobita K. Directed stem cell differentiation: the role of physical forces. Cell Commun Adhes 2010; 17(2): 48-54.
[9]     Ikada Y. Tissue engineering: fundamentals and applications. Amsterdam; Boston: Academic Press/ Elsevier, 2006; p: 51-65.
[10]  Li Z, Yao SJ, Alini M, Stoddart MJ. Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites is modulated by frequency and amplitude of dynamic compression and shear stress. Tissue Eng Part A 2010; 16(2): 575-84.
[11]  Schätti O, Grad S, Goldhahn J, Salzmann G, Li Z, Alini M, Stoddart MJ. A combination of shear and dynamic compression leads to mechanically induced chondrogenesis of human mesenchymal stem cells. Eur Cell Mater 2011; 22: 214-25.
[12]  Kasper C, Griensven M, Portner R, Al-Rubeai M. Bioreator systems for tissue engineering. Berlin: Springer, 2009; p: 95-125.
[13]  Carter DR. Mechanical loading histories and cortical bone remodeling. Calcif Tissue Int 1984; 36 Suppl 1: S19-24.
[14]  Skedros JG, Brand RA. Biographical sketch: Georg Hermann von Meyer (1815-1892). Clin Orthop Relat Res 2011; 469(11): 3072-6.
[15]  Phillips ATM. Structural optimisation: bio-mechanics of the femur. Eng Comput Mech 2012; 165: 147-54.
[16]  Ethier CR, Simmons CA. Introductory biomechanics: from cells to organisms (Cambridge Text in Biomedical Engineering). CambridgeUniversity Press; 2007; 35-90.
[17]  Brown TD. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech 2000; 33(1): 3-14.
[18]  Brown TD. Techniques for cell and tissue culture mechanostimulation: historical and contemporary design considerations. Iowa Orthop J 1995; 15: 112-7.
[19]  Orr AW, Helmke BP, Blackman BR, Schwartz MA. Mechanisms of mechanotransduction. Dev Cell 2006; 10(1): 11-20.
[20]  Wang N, Tytell JD, Ingber DE. Mechano-transduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10(1): 75-82.
[21]  Stolberg S, McCloskey KE. Can shear stress direct stem cell fate? Biotechnol Prog 2009; 25(1): 10-9.
[22]  Huang H, Kamm RD, Lee RT. Cell mechanics and mechanotransduction: pathways, probes, and physiology. Am J Physiol Cell Physiol 2004; 287(1): C1-11.
[23]  Matthews BD, Overby DR, Mannix R, Ingber DE. Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 2006; 119(Pt 3): 508-18.
[24]  Zhang ZY, Teoh SH, Chong WS, Foo TT, Chng YC, Choolani M, Chan J. A biaxial rotating bioreactor for the culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 2009; 30(14): 2694-704.
[25]  Nieponice A, Maul TM, Cumer JM, Soletti L, Vorp DA. Mechanical stimulation induces morphological and phenotypic changes in bone marrow-derived progenitor cells within a three-dimensional fibrin matrix. J Biomed Mater Res A 2007; 81(3): 523-30.
[26]  Sim WY, Park SW, Park SH, Min BH, Park SR, Yang SS. A pneumatic micro cell chip for the differentiation of human mesenchymal stem cells under mechanical stimulation. Lab Chip 2007; 7(12): 1775-82.
[27]  Zhang ZY, Teoh SH, Teo EY, Khoon Chong MS, Shin CW, Tien FT, Choolani MA, Chan JK. A comparison of bioreactors for culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 2010; 31(33): 8684-95.
[28]  Waldman SD, Couto DC, Grynpas MD, Pilliar RM, Kandel RA. A single application of cyclic loading can accelerate matrix deposition and enhance the properties of tissue-engineered cartilage. Osteoarthritis Cartilage 2006; 14(4): 323-30.
[29]  Singh H, Teoh SH, Low HT, Hutmacher DW. Flow modelling within a scaffold under the influence of uni-axial and bi-axial bioreactor rotation. J Biotechnol 2005; 119(2): 181-96.
[30]  Lim CT, Zhou EH, Quek ST. Mechanical models for living cells--a review. J Biomech 2006; 39(2): 195-216.
[31]  Kim TK, Jeong OC. Fabrication of a pneumatically driven single-cell trap. Microelectron Eng 2011; 88(8): 1768-71.
[32]  Kim TK, Jeong OC. Effect of mechanical stimuli on live cells in a pneumatically driven cell trap. Microelectron Eng 2012; 97: 324-8.
[33]  Lee DA, Knight MM, Campbell JJ, Bader DL. Stem cell mechanobiology. J Cell Biochem 2011; 112(1): 1-9.
[34]  Finger AR, Sargent CY, Dulaney KO, Bernacki SH, Loboa EG. Differential effects on messenger ribonucleic acid expression by bone marrow-derived human mesenchymal stem cells seeded in agarose constructs due to ramped and steady applications of cyclic hydrostatic pressure. Tissue Eng 2007; 13(6): 1151-8.
[35]  Chen YJ, Huang CH, Lee IC, Lee YT, Chen MH, Young TH. Effects of cyclic mechanical stretching on the mRNA expression of tendon/ligament-related and osteoblast-specific genes in human mesenchymal stem cells. Connect Tissue Res 2008; 49(1): 7-14.
[36]  Huang CY, Reuben PM, Cheung HS. Temporal expression patterns and corresponding protein inductions of early responsive genes in rabbit bone marrow-derived mesenchymal stem cells under cyclic compressive loading. Stem Cells 2005; 23(8): 1113-21.
[37]  Cohen DM, Chen CS. Mechanical control of stem cell differentiation. StemBook [Internet]. Cambridge (MA): Harvard Stem Cell Institute; 2008; Available at: http://www.ncbi.nlm.nih.gov/ pubmed/20614621.
[38]  Maul TM, Chew DW, Nieponice A, Vorp DA. Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech Model Mechanobiol 2011; 10(6): 939-53.
[39]  Wu HW, Lin CC, Hwang SM, Chang YJ, Lee GB. A microfluidic device for chemical and mechanical stimulation of mesenchymal stem cells. Microfluid Nanofluid 2011; 11(5): 545-56.
[40]  Lee HL, Boccazzi P, Ram RJ, Sinskey AJ. Microbioreactor arrays with integrated mixers and fluid injectors for high-throughput experimentation with pH and dissolved oxygen control. Lab Chip 2006; 6(9): 1229-35.
[41]  Chen HC, Hu YC. Bioreactors for tissue engineering. Biotechnol Lett 2006; 28(18): 1415-23.
[42]  Meinel L, Karageorgiou V, Hofmann S, Fajardo R, Snyder B, Li C, Zichner L, Langer R, Vunjak-Novakovic G, Kaplan DL. Engineering bone-like tissue in vitro using human bone marrow stem cells and silk scaffolds. J Biomed Mater Res A 2004; 71(1): 25-34.
[43]  Goldstein AS, Juarez TM, Helmke CD, Gustin MC, Mikos AG. Effect of convection on osteoblastic cell growth and function in biodegradable polymer foam scaffolds. Biomaterials 2001; 22(11): 1279-88.
[44]  Koike M, Shimokawa H, Kanno Z, Ohya K, Soma K. Effects of mechanical strain on proliferation and differentiation of bone marrow stromal cell line ST2. J Bone Miner Metab 2005; 23(3): 219-25.
[45]  Jagodzinski M, Drescher M, Zeichen J, Hankemeier S, Krettek C, Bosch U, van Griensven M. Effects of cyclic longitudinal mechanical strain and dexamethasone on osteogenic differentiation of human bone marrow stromal cells. Eur Cell Mater 2004; 7: 35-41.
[46]  Qi MC, Hu J, Zou SJ, Chen HQ, Zhou HX, Han LC. Mechanical strain induces osteogenic differentiation: Cbfa1 and Ets-1 expression in stretched rat mesenchymal stem cells. Int J Oral Maxillofac Surg 2008; 37(5): 453-8.
[47]  Sumanasinghe RD, Bernacki SH, Loboa EG. Osteogenic differentiation of human mesenchymal stem cells in collagen matrices: effect of uniaxial cyclic tensile strain on bone morphogenetic protein (BMP-2) mRNA expression. Tissue Eng 2006; 12(12): 3459-65.
[48]  Safshekan F, Tafazzoli-Shadpour M, Shokrgozar MA, Haghighipour N, Mahdian R, Hemmati A. Intermittent hydrostatic pressure enhances growth factor-induced chondroinduction of human adipose-derived mesenchymal stem cells. Artif Organs 2012; 36(12): 1065-71.
[49]  Wimmer MA, Grad S, Kaup T, Hänni M, Schneider E, Gogolewski S, Alini M. Tribology approach to the engineering and study of articular cartilage. Tissue Eng 2004; 10(9-10): 1436-45.
[50]  Mukherjee N, Saris DB, Schultz FM, Berglund LJ, An KN, O' Driscoll SW. The enhancement of periosteal chondrogenesis in organ culture by dynamic fluid pressure. J Orthop Res 2001; 19(4): 524-30.
[51]  Lee HJ, Choi BH, Min BH, Son YS, Park SR. Low-intensity ultrasound stimulation enhances chondrogenic differentiation in alginate culture of mesenchymal stem cells. Artif Organs 2006; 30(9): 707-15.
[52]  Cui JH, Park K, Park SR, Min BH. Effects of low-intensity ultrasound on chondrogenic differentiation of mesenchymal stem cells embedded in polyglycolic acid: an in vivo study. Tissue Eng 2006; 12(1): 75-82.
[53]  Schumann D, Kujat R, Zellner J, Angele MK, Nerlich M, Mayr E, Angele P. Treatment of human mesenchymal stem cells with pulsed low intensity ultrasound enhances the chondrogenic phenotype in vitro. Biorheology 2006; 43(3-4): 431-43.
[54]  Angele P, Schumann D, Angele M, Kinner B, Englert C, Hente R, Füchtmeier B, Nerlich M, Neumann C, Kujat R. Cyclic, mechanical compression enhances chondrogenesis of mesenchymal progenitor cells in tissue engineering scaffolds. Biorheology 2004; 41(3-4): 335-46.
[55]  Huang CY, Hagar KL, Frost LE, Sun Y, Cheung HS. Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 2004; 22(3): 313-23.
[56]  Mouw JK, Connelly JT, Wilson CG, Michael KE, Levenston ME. Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells. Stem Cells 2007; 25(3): 655-63.
[57]  Miyanishi K, Trindade MC, Lindsey DP, Beaupré GS, Carter DR, Goodman SB, Schurman DJ, Smith RL. Effects of hydrostatic pressure and transforming growth factor-beta 3 on adult human mesenchymal stem cell chondrogenesis in vitro. Tissue Eng 2006; 12(6): 1419-28.
[58]  Miyanishi K, Trindade MC, Lindsey DP, Beaupré GS, Carter DR, Goodman SB, Schurman DJ, Smith RL. Dose- and time-dependent effects of cyclic hydrostatic pressure on transforming growth factor-beta3-induced chondrogenesis by adult human mesenchymal stem cells in vitro. Tissue Eng 2006; 12(8): 2253-62.
[59]  Pelaez D, Huang CY, Cheung HS. Cyclic compression maintains viability and induces chondrogenesis of human mesenchymal stem cells in fibrin gel scaffolds. Stem Cells Dev 2009; 18(1): 93-102.
[60]  Wagner DR, Lindsey DP, Li KW, Tummala P, Chandran SE, Smith RL, Longaker MT, Carter DR, Beaupre GS. Hydrostatic pressure enhances chondrogenic differentiation of human bone marrow stromal cells in osteochondrogenic medium. Ann Biomed Eng 2008; 36(5): 813-20.
[61]  Altman GH, Horan RL, Martin I, Farhadi J, Stark PR, Volloch V, Richmond JC, Vunjak-Novakovic G, Kaplan DL. Cell differentiation by mechanical stress. FASEB J 2002; 16(2): 270-2.
[62]  Juncosa-Melvin N, Matlin KS, Holdcraft RW, Nirmalanandhan VS, Butler DL. Mechanical stimulation increases collagen type I and collagen type III gene expression of stem cell-collagen sponge constructs for patellar tendon repair. Tissue Eng 2007; 13(6): 1219-26.
[63]  Juncosa-Melvin N, Shearn JT, Boivin GP, Gooch C, Galloway MT, West JR, Nirmalanandhan VS, Bradica G, Butler DL. Effects of mechanical stimulation on the biomechanics and histology of stem cell-collagen sponge constructs for rabbit patellar tendon repair. Tissue Eng 2006; 12(8): 2291-300.
[64]  Kanda K, Matsuda T. Mechanical stress-induced orientation and ultrastructural change of smooth muscle cells cultured in three-dimensional collagen lattices. Cell Transplant 1994; 3(6): 481-92.
[65]  Grenier G, Rémy-Zolghadri M, Larouche D, Gauvin R, Baker K, Bergeron F, Dupuis D, Langelier E, Rancourt D, Auger FA, Germain L. Tissue reorganization in response to mechanical load increases functionality. Tissue Eng 2005; 11(1-2): 90-100.
[66]  Park JS, Chu JS, Cheng C, Chen F, Chen D, Li S. Differential effects of equiaxial and uniaxial strain on mesenchymal stem cells. Biotechnol Bioeng 2004; 88(3): 359-68.
[67]  Riha GM, Wang X, Wang H, Chai H, Mu H, Lin PH, Lumsden AB, Yao Q, Chen C. Cyclic strain induces vascular smooth muscle cell differentiation from murine embryonic mesenchymal progenitor cells. Surgery 2007; 141(3): 394-402.
[68]  Shimizu N, Yamamoto K, Obi S, Kumagaya S, Masumura T, Shimano Y, Naruse K, Yamashita JK, Igarashi T, Ando J. Cyclic strain induces mouse embryonic stem cell differentiation into vascular smooth muscle cells by activating PDGF receptor beta. J Appl Physiol (1985) 2008; 104(3): 766-72.
[69]  Kurpinski K, Chu J, Hashi C, Li S. Anisotropic mechanosensing by mesenchymal stem cells. Proc Natl Acad Sci U S A 2006; 103(44): 16095-100.
[70]  Haghighipour N, Heidarian S, Shokrgozar MA, Amirizadeh N. Differential effects of cyclic uniaxial stretch on human mesenchymal stem cell into skeletal muscle cell. Cell Biol Int 2012; 36(7): 669-75.
[71]  Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 2005; 25(9): 1817-23.
[72]  Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J. Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol 2005; 288(4): H1915-24.
[73]  Shojaei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N. Effects of mechanical and chemical stimuli on differentiation of human adipose-derived stem cells into endothelial cells. Int J Artif Organs 2013; 36(9): 663-73.
[74]  Maul TM, Hamilton DW, Nieponice A, Soletti L, Vorp DA. A new experimental system for the extended application of cyclic hydrostatic pressure to cell culture. J Biomech Eng 2007; 129(1): 110-6.
[75]  Van Dyke WS, Sun X, Richard AB, Nauman EA, Akkus O. Novel mechanical bioreactor for concomitant fluid shear stress and substrate strain. J Biomech 2012; 45(7): 1323-7.
[76]  Xu F, Wu J, Wang S, Durmus NG, Gurkan UA, Demirci U. Microengineering methods for cell-based microarrays and high-throughput drug-screening applications. Biofabrication 2011; 3(3): 034101.
[77]  Chung BG, Kang L, Khademhosseini A. Micro- and nanoscale technologies for tissue engineering and drug discovery applications. Expert Opin Drug Discov 2007; 2(12): 1653-68.
[78]  Ross TD, Coon BG, Yun S, Baeyens N, Tanaka K, Ouyang M, Schwartz MA. Integrins in mechanotransduction. Curr Opin Cell Biol 2013; 25(5): 613-8.
[79]  Haghighipour N, Tafazzoli-Shadpour M, Shokrgozar MA, Amini S. Effects of cyclic stretch waveform on endothelial cell morphology using fractal analysis. Artif Organs 2010; 34(6): 481-90.
Pathobiology Reserach
Volume 16, Issue 3
December 2013
Pages 1-23