Different effects of intermittent and continuous fluid shear stresses on osteogenic differentiation of human mesenchymal stem cells

Biomechanics and Modeling in Mechanobiology

Volumn 11, Issue 3-4, 2012, Pages 391-401

  Liu, Liyue ^a   Yu, Bin ^a   Chen, Jiarong ^a   Tang, Zihua ^a   Zong, Chen ^a   Shen, Dan ^b   Zheng, Qiang ^b   Tong, Xiangming ^b   Gao, Changyou ^b   Wang, Jinfu ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

FSS; HMSCs; Osteogenesis; Perfusion culture

Indexed keywords

ALKALINE PHOSPHATASE ACTIVITY; BONE TISSUE; BONE TISSUE ENGINEERING; DIFFERENT EFFECTS; EXPRESSION LEVELS; FLUID SHEAR STRESS; FSS; HMSCS; HUMAN MESENCHYMAL STEM CELLS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); IN-VIVO; MICROENVIRONMENTS; OSTEOGENESIS; OSTEOGENIC; OSTEOGENIC DIFFERENTIATION; PERFUSION CULTURES; SIGNALING MOLECULES;

BONE; GENE EXPRESSION; PHOSPHATASES; PHOSPHORYLATION; STEM CELLS; TISSUE; TISSUE ENGINEERING;

CELL CULTURE;

ALKALINE PHOSPHATASE;

ADULT; ARTICLE; BONE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; HUMAN; MECHANICAL STRESS; MESENCHYMAL STEM CELL; METABOLISM; METHODOLOGY; PERFUSION; PHOSPHORYLATION; SHEAR STRENGTH; SIGNAL TRANSDUCTION; TISSUE ENGINEERING;

ADULT; ALKALINE PHOSPHATASE; BONE AND BONES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; MAP KINASE SIGNALING SYSTEM; MESENCHYMAL STEM CELLS; OSTEOGENESIS; PERFUSION; PHOSPHORYLATION; SHEAR STRENGTH; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TISSUE ENGINEERING;

EID: 84861097397     PISSN: 16177959     EISSN: 16177940     Source Type: Journal    
DOI: 10.1007/s10237-011-0319-x     Document Type: Article

References (42)

1. Arnsdorf EJ, Tummala P, Kwon RY, Jacobs CR (2009) Mechanically induced osteogenic differentiation-the role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sci 122:546-553
2. Bancroft GN, Sikavitsas VI, van den Dolder J, Sheffield TL, Ambrose CG, Jansen JA, Mikos AG (2002) Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA 99:12600-12605
3. Boudreau NJ, Jones PL (1999) Extracellularmatrix and integrin signalling: the shape of things to come. Biochem J 339(Pt 3):481-488 (Pubitemid 29243508)
4. Brand RA, Stanford CM (1994) How connective tissues temporally process mechanical stimuli. Med Hypotheses 42:99-104 (Pubitemid 24087907)
5. Cheung PF, Wong CK, Ip WK, Lam CW (2008) FAK-mediated activation of ERK for eosinophil migration: a novel mechanism for infection-induced allergic inflammation. Int Immunol 20: 353-363 (Pubitemid 351321243)
6. Digirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ (1999) Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 107:275-281 (Pubitemid 29530211)
7. Dumas V, Ducharne B, Perrier A, Fournier C, Guignandon A, Thomas M, Peyroche S, Guyomar D, Vico L, Rattner A (2010) Extracellular matrix produced by osteoblasts cultured under lowmagnitude, high-frequency stimulation is favourable to osteogenic differentiation of mesenchymal stem cells. Calcif Tissue Int 87:351-364
8. Glossop JR, Cartmell SH (2009) Effect of fluid flow-induced shear stress on human mesenchymal stem cells: differential gene expression of IL1B and MAP3K8 in MAPK signaling. Gene Expr Patterns 9:381-388
9. Grellier M, Bareille R, Bourget C, Amedee J (2009) Responsiveness of human bone marrow stromal cells to shear stress. J Tissue Eng Regen Med 3:302-309
10. Guignandon A, Usson Y, Laroche N, Lafage-Proust MH, Sabido O, Alexandre C, Vico L (1997) Effects of intermittent or continuous gravitational stresses on cell-matrix adhesion: quantitative analysis of focal contacts in osteoblastic ROS 17/2.8 cells. Exp Cell Res 236:66-75 (Pubitemid 27452350)
11. Gurkan UA, Akkus O (2008) Themechanical environment of bone marrow: a review. Ann Biomed Eng 36:1978-1991
12. Haasper C, Jagodzinski M, Drescher M, Meller R, Wehmeier M, Krettek C, Hesse E (2008) Cyclic strain induces FosB and initiates osteogenic differentiation of mesenchymal cells. Exp Toxicol Pathol 59:355-363
13. Haudenschild AK, Hsieh AH, Kapila S, Lotz JC (2009) Pressure and distortion regulate human mesenchymal stem cell gene expression. Ann Biomed Eng 37:492-502
14. Hosseinkhani H, Inatsugu Y, Hiraoka Y, Inoue S, Tabata Y (2005) Perfusion culture enhances osteogenic differentiation of rat mesenchymal stem cells in collagen sponge reinforced with poly(glycolic Acid) fiber. Tissue Eng 11:1476-1488 (Pubitemid 41636433)
15. Huang CH, Chen MH, Young TH, Jeng JH, Chen YJ (2009) Interactive effects of mechanical stretching and extracellular matrix proteins on initiating osteogenic differentiation of human mesenchymal stem cells. J Cell Biochem 108:1263-1273
16. Inoue D, Kido S, Matsumoto T (2004) Transcriptional induction of FosB/DeltaFosB gene by mechanical stress in osteoblasts. J Biol Chem 279:49795-49803 (Pubitemid 39577785)
17. Irigoyen JP, Nagamine Y (1999) Cytoskeletal reorganization leads to induction of the urokinase-type plasminogen activator gene by activating FAK and Src and subsequently the Ras/Erk signaling pathway. Biochem Biophys Res Commun 262:666-670 (Pubitemid 29443716)
18. Kanno T, Takahashi T, Tsujisawa T, Ariyoshi W, Nishihara T (2007) Mechanical stress-mediated Runx2 activation is dependent on Ras/ERK1/2 MAPK signaling in osteoblasts. J Cell Biochem 101:1266-1277 (Pubitemid 47253725)
19. Kapur S, Baylink DJ, Lau KH (2003) Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32:241-251 (Pubitemid 36349527)
20. Kim SH, Choi YR, Park MS, Shin JW, Park KD, Kim SJ, Lee JW (2007) ERK 1/2 activation in enhanced osteogenesis of human mesenchymal stem cells in poly(lactic-glycolic acid) by cyclic hydrostatic pressure. J Biomed Mater Res A 80:826-836
21. Kreke MR, Sharp LA, Lee YW, Goldstein AS (2008) Effect of intermittent shear stress on mechanotransductive signaling and osteoblastic differentiation of bone marrow stromal cells. Tissue Eng Part A 14:529-537 (Pubitemid 351520460)
22. LaMothe JM, Zernicke RF (2004) Rest insertion combined with highfrequency loading enhances osteogenesis. J Appl Physiol 96: 1788-1793 (Pubitemid 38580004)
23. Lee DY, Yeh CR, Chang SF, Lee PL, Chien S, Cheng CK, Chiu JJ (2008) Integrin-mediated expression of bone formation-related genes in osteoblast-like cells in response to fluid shear stress: roles of extracellular matrix, Shc, and mitogen-activated protein kinase. J Bone Miner Res 23:1140-1149 (Pubitemid 351915736)
24. Liu L, Yuan W, Wang J (2010) Mechanisms for osteogenic differentiation of human mesenchymal stem cells induced by fluid shear stress. Biomech Model Mechanobiol 9:659-670
25. McAllister TN, Du T, Frangos JA (2000) Fluid shear stress stimulates prostaglandin and nitric oxide release in bone marrow-derived preosteoclast-like cells. Biochem Biophys Res Commun 270: 643-648 (Pubitemid 30446888)
26. Pavlin D, Dove SB, Zadro R, Gluhak-Heinrich J (2000) Mechanical loading stimulates differentiation of periodontal osteoblasts in a mouse osteoinduction model: effect on type I collagen and alkaline phosphatase genes. Calcif Tissue Int 67:163-172 (Pubitemid 30614643)
27. Rangaswami H, Marathe N, Zhuang S, Chen Y, Yeh JC, Frangos JA, Boss GR, Pilz RB (2009) Type II cGMP-dependent protein kinase mediates osteoblast mechanotransduction. J Biol Chem 284:14796-14808
28. Riddle RC, Taylor AF, Genetos DC, Donahue HJ (2006) MAP kinase and calcium signaling mediate fluid flow-induced human mesenchymal stem cell proliferation. Am J Physiol Cell Physiol 290:C776-C784
29. Sharp LA, Lee YW, Goldstein AS (2009) Effect of low-frequency pulsatile flow on expression of osteoblastic genes by bone marrow stromal cells. Ann Biomed Eng 37:445-453
30. Simmons CA, Matlis S, Thornton AJ, Chen S, Wang CY, Mooney DJ (2003) Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signalregulated kinase (ERK1/2) signaling pathway. J Biomech 36: 1087-1096 (Pubitemid 36794104)
31. Stephens JS, Cooper JA, Phelan FRJr, Dunkers JP (2007) Perfusion flow bioreactor for 3D in situ imaging: investigating cell/biomaterials interactions. Biotechnol Bioeng 97:952-961 (Pubitemid 47051063)
32. Stiehler M, Bunger C, Baatrup A, Lind M, Kassem M, Mygind T (2009) Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. J Biomed Mater Res A 89:96-107
33. Tanaka S, Matsuzaka K, Sato D, Inoue T (2007) Characteristics of newly formed bone during guided bone regeneration: analysis of cbfa-1, osteocalcin, and VEGF expression. J Oral Implantol 33:321-326
34. Wang W, Li B, Li Y, Jiang Y, Ouyang H, Gao C (2010) In vivo restoration of full-thickness cartilage defects by poly(lactide-coglycolide) sponges filled with fibrin gel, bone marrow mesenchymal stem cells and DNA complexes. Biomaterials 31:5953-5965
35. Weinbaum S, Cowin SC, Zeng Y (1994) A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27:339-360 (Pubitemid 24061729)
36. Winter LC, Walboomers XF, Bumgardner JD, Jansen JA (2003) Intermittent versus continuous stretching effects on osteoblast-like cells in vitro. J Biomed Mater Res A 67:1269-1275 (Pubitemid 37522740)
37. Xiao G, Jiang D, Thomas P, Benson MD, Guan K, Karsenty G, Franceschi RT (2000) MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J BiolChem 275:4453-4459 (Pubitemid 30094689)
38. Yang J, Cao C, Wang W, Tong X, Shi D, Wu F, Zheng Q, Guo C, Pan Z, Gao C, Wang J (2010) Proliferation and osteogenesis of immortalized bone marrow-derived mesenchymal stem cells in porous polylactic glycolic acid scaffolds under perfusion culture. J Biomed Mater Res A 92:817-829
39. Young SR, Gerard-O'Riley R, Kim JB, Pavalko FM (2009) Focal adhesion kinase is important for fluid shear stress-induced mechanotransduction in osteoblasts. J Bone Miner Res 24:411-424
40. Yourek G, McCormick SM, Mao JJ, Reilly GC (2010) Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen Med 5:713-724
41. Zhang L, Bewick M, Lafrenie RM (2002) Role of Raf-1 and FAK in cell density-dependent regulation of integrin-dependent activation of MAP kinase. Carcinogenesis 23:1251-1258 (Pubitemid 34814785)
42. Zhao H, Ma L, Gao C, Shen J (2009) A composite scaffold of PLGA microspheres/fibrin gel for cartilage tissue engineering: fabrication, physical properties, and cell responsiveness. J BiomedMater Res B Appl Biomater 88:240-249