Mechanical integrin stress and magnetic forces induce biological responses in mesenchymal stem cells which depend on environmental factors

Journal of Cellular Biochemistry

Volumn 111, Issue 6, 2010, Pages 1586-1597

  Kasten, Annika ^a   Müller, Petra ^a   Bulnheim, Ulrike ^a   Groll, Jürgen ^b   Bruellhoff, Kristina ^b   Beck, Ulrich ^a   Steinhoff, Gustav ^a   Möller, Martin ^b   Rychly, Joachim ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

biological response; integrin; mechanical loading; mesenchymal stem cells

Indexed keywords

ALKALINE PHOSPHATASE; ARGINYLGLYCYLASPARTIC ACID; BETA1 INTEGRIN; COLLAGEN TYPE 1; FIBRONECTIN; POLYSTYRENE; PROTEIN KINASE B; TRANSCRIPTION FACTOR SOX9; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BONE DEVELOPMENT; CELL ADHESION; CELL CULTURE; CELL STRESS; CHONDROGENESIS; CLINICAL ASSESSMENT; CONTROLLED STUDY; CULTURE MEDIUM; ENVIRONMENTAL FACTOR; ENZYME ACTIVATION; FEMALE; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; FLOW CYTOMETRY; FORCE; HUMAN; HUMAN CELL; MAGNETIC FIELD; MALE; MESENCHYMAL STEM CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE REGENERATION;

AGED; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CELL ADHESION; CELLS, CULTURED; CHROMONES; FEMALE; FLOW CYTOMETRY; HUMANS; INTEGRINS; MAGNETICS; MALE; MESENCHYMAL STEM CELLS; MICROSCOPY, ELECTRON, SCANNING; MIDDLE AGED; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, MECHANICAL;

EID: 78649794618     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22890     Document Type: Article

References (53)

1. Aaron RK, Ciombor DM,. 1993. Therapeutic effects of electromagnetic fields in the stimulation of connective tissue repair. J Cell Biochem 52: 42-46.
2. Barbier E, Dufy B, Veyret B,. 1996. Stimulation of Ca2+ influx in rat pituitary cells under exposure to a 50 Hz magnetic field. Bioelectromagnetics 17: 303-311.
3. Baureus Koch CL, Sommarin M, Persson BR, Salford LG, Eberhardt JL,. 2003. Interaction between weak low frequency magnetic fields and cell membranes. Bioelectromagnetics 24: 395-402.
4. Bianco P, Robey PG, Simmons PJ,. 2008. Mesenchymal stem cells: Revisiting history, concepts, and assays. Cell Stem Cell 2: 313-319.
5. Cantley LC,. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
6. Caplan AI,. 2009. Why are MSCs therapeutic? New data: New insight. J Pathol 217: 318-324.
7. Chiu KH, Ou KL, Lee SY, Lin CT, Chang WJ, Chen CC, Huang HM,. 2007. Static magnetic fields promote osteoblast-like cells differentiation via increasing the membrane rigidity. Ann Biomed Eng 35: 1932-1939.
8. Clark EA, Brugge JS,. 1995. Integrins and signal transduction pathways: The road taken. Science 268: 233-239.
9. da Silva Meirelles L, Caplan AI, Nardi NB,. 2008. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26: 2287-2299.
10. Delle Monache S, Alessandro R, Iorio R, Gualtieri G, Colonna R,. 2008. Extremely low frequency electromagnetic fields (ELF-EMFs) induce in vitro angiogenesis process in human endothelial cells. Bioelectromagnetics 29: 640-648.
11. Discher DE, Mooney DJ, Zandstra PW,. 2009. Growth factors, matrices, and forces combine and control stem cells. Science 324: 1673-1677.
12. Dumas V, Perrier A, Malaval L, Laroche N, Guignandon A, Vico L, Rattner A,. 2009. The effect of dual frequency cyclic compression on matrix deposition by osteoblast-like cells grown in 3D scaffolds and on modulation of VEGF variant expression. Biomaterials 30: 3279-3288.
13. Ellis SJ, Tanentzapf G,. 2010. Integrin-mediated adhesion and stem-cell-niche interactions. Cell Tissue Res 339: 121-130.
14. Engler AJ, Sen S, Sweeney HL, Discher DE,. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
15. Fuchs S, Ghanaati S, Orth C, Barbeck M, Kolbe M, Hofmann A, Eblenkamp M, Gomes M, Reis RL, Kirkpatrick CJ,. 2009a. Contribution of outgrowth endothelial cells from human peripheral blood on in vivo vascularization of bone tissue engineered constructs based on starch polycaprolactone scaffolds. Biomaterials 30: 526-534.
16. Fuchs S, Jiang X, Schmidt H, Dohle E, Ghanaati S, Orth C, Hofmann A, Motta A, Migliaresi C, Kirkpatrick CJ,. 2009b. Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells. Biomaterials 30: 1329-1338.
17. Gasteier P, Reska A, Schulte P, Salber J, Offenhausser A, Moeller M, Groll J,. 2007. Surface grafting of PEO-based star-shaped molecules for bioanalytical and biomedical applications. Macromol Biosci 7: 1010-1023.
18. Gotz H, Beginn U, Bartelink CF, Grunbauer HJM, Moller M,. 2002. Preparation of isophorone diisocyanate terminated star polyethers. Macromol Mater Eng 287: 223-230.
19. Groll J, Amirgoulova EV, Ameringer T, Heyes CD, Röcker C, Nienhaus GU, Möller M,. 2004. Biofunctionalized, ultrathin coatings of cross-linked star-shaped poly(ethylene oxide) allow reversible folding of immobilized proteins. J Am Chem Soc 126: 4234-4239.
20. Groll J, Fiedler J, Engelhard E, Ameringer T, Tugulu S, Klok HA, Brenner RE, Moeller M,. 2005. A novel star PEG-derived surface coating for specific cell adhesion. J Biomed Mater Res Part A 74A: 607-617.
21. Guilak F, Cohen DM, Estes BT, Gimble JM, Liedtke W, Chen CS,. 2009. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5: 17-26.
22. Hamidouche Z, Fromigue O, Ringe J, Haupl T, Vaudin P, Pages JC, Srouji S, Livne E, Marie PJ,. 2009. Priming integrin alpha5 promotes human mesenchymal stromal cell osteoblast differentiation and osteogenesis. Proc Natl Acad Sci USA 106: 18587-18591.
23. Hopper RA, VerHalen JP, Tepper O, Mehrara BJ, Detch R, Chang EI, Baharestani S, Simon BJ, Gurtner GC,. 2009. Osteoblasts stimulated with pulsed electromagnetic fields increase HUVEC proliferation via a VEGF-A independent mechanism. Bioelectromagnetics 30: 189-197.
24. 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.
25. Hynes RO,. 2002. Integrins: Bidirectional, allosteric signaling machines. Cell 110: 673-687.
26. Hynes RO,. 2009. The extracellular matrix: Not just pretty fibrils. Science 326: 1216-1219.
27. Jiang BH, Liu LZ,. 2008. PI3K/PTEN signaling in tumorigenesis and angiogenesis. Biochim Biophys Acta 1784: 150-158.
28. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE,. 2004. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94: 678-685.
29. 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.
30. Legate KR, Wickstrom SA, Fassler R,. 2009. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23: 397-418.
31. Lohmann CH, Schwartz Z, Liu Y, Guerkov H, Dean DD, Simon B, Boyan BD,. 2000. Pulsed electromagnetic field stimulation of MG63 osteoblast-like cells affects differentiation and local factor production. J Orthop Res 18: 637-646.
32. Manni V, Lisi A, Pozzi D, Rieti S, Serafino A, Giuliani L, Grimaldi S,. 2002. Effects of extremely low frequency (50Hz) magnetic field on morphological and biochemical properties of human keratinocytes. Bioelectromagnetics 23: 298-305.
33. Moser M, Legate KR, Zent R, Fassler R,. 2009. The tail of integrins, talin, and kindlins. Science 324: 895-899.
34. Muller P, Bulnheim U, Diener A, Luthen F, Teller M, Klinkenberg ED, Neumann HG, Nebe B, Liebold A, Steinhoff G, Rychly J,. 2008. Calcium phosphate surfaces promote osteogenic differentiation of mesenchymal stem cells. J Cell Mol Med 12: 281-291.
35. Pommerenke H, Schreiber E, Durr F, Nebe B, Hahnel C, Moller W, Rychly J,. 1996. Stimulation of integrin receptors using a magnetic drag force device induces an intracellular free calcium response. Eur J Cell Biol 70: 157-164.
36. Pommerenke H, Schmidt C, Durr F, Nebe B, Luthen F, Muller P, Rychly J,. 2002. The mode of mechanical integrin stressing controls intracellular signaling in osteoblasts. J Bone Miner Res 17: 603-611.
37. Rychly J, Pommerenke H, Durr F, Schreiber E, Nebe B,. 1998. Analysis of spatial distributions of cellular molecules during mechanical stressing of cell surface receptors using confocal microscopy. Cell Biol Int 22: 7-12.
38. Salasznyk RM, Williams WA, Boskey A, Batorsky A, Plopper GE,. 2004. Adhesion to vitronectin and collagen I promotes osteogenic differentiation of human mesenchymal stem cells. J Biomed Biotechnol 2004: 24-34.
39. Santini MT, Rainaldi G, Indovina PL,. 2009. Cellular effects of extremely low frequency (ELF) electromagnetic fields. Int J Radiat Biol 85: 294-313.
40. Scadden DT,. 2006. The stem-cell niche as an entity of action. Nature 441: 1075-1079.
41. Schmidt C, Pommerenke H, Durr F, Nebe B, Rychly J,. 1998. Mechanical stressing of integrin receptors induces enhanced tyrosine phosphorylation of cytoskeletally anchored proteins. J Biol Chem 273: 5081-5085.
42. Schwartz MA, DeSimone DW,. 2008. Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 20: 551-556.
43. Selvamurugan N, Kwok S, Vasilov A, Jefcoat SC, Partridge NC,. 2007. Effects of BMP-2 and pulsed electromagnetic field (PEMF) on rat primary osteoblastic cell proliferation and gene expression. J Orthop Res 25: 1213-1220.
44. Sen B, Xie Z, Case N, Ma M, Rubin C, Rubin J,. 2008. Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable beta-catenin signal. Endocrinology 149: 6065-6075.
45. Sorrell JM, Baber MA, Caplan AI,. 2009. Influence of adult mesenchymal stem cells on in vitro vascular formation. Tissue Eng Part A 15: 1751-1761.
46. Strauch B, Patel MK, Navarro JA, Berdichevsky M, Yu HL, Pilla AA,. 2007. Pulsed magnetic fields accelerate cutaneous wound healing in rats. Plast Reconstr Surg 120: 425-430.
47. Sumanasinghe RD, Bernacki SH, Loboa EG,. 2006. 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 12: 3459-3465.
48. Tepper OM, Callaghan MJ, Chang EI, Galiano RD, Bhatt KA, Baharestani S, Gan J, Simon B, Hopper RA, Levine JP, Gurtner GC,. 2004. Electromagnetic fields increase in vitro and in vivo angiogenesis through endothelial release of FGF-2. FASEB J 18: 1231-1233.
49. Thomas GP, el Haj AJ,. 1996. Bone marrow stromal cells are load responsive in vitro. Calcif Tissue Int 58: 101-108.
50. Vogel V, Sheetz MP,. 2009. Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr Opin Cell Biol 21: 38-46.
51. Winer JP, Janmey PA, McCormick ME, Funaki M,. 2009. Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A 15: 147-154.
52. Yin T, Li L,. 2006. The stem cell niches in bone. J Clin Invest 116: 1195-1201.
53. Zajac AL, Discher DE,. 2008. Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling. Curr Opin Cell Biol 20: 609-615.