Undifferentiated human mesenchymal stem cells (hMSCs) are highly sensitive to mechanical strain: transcriptionally controlled early osteo-chondrogenic response in vitro

Osteoarthritis and Cartilage

Volumn 15, Issue 11, 2007, Pages 1293-1300

  Friedl, G ^a   Schmidt, H ^a   Rehak, I ^a   Kostner, G ^a   Schauenstein, K ^a   Windhager, R ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Bone marrow stromal cells; c Fos; Chondrogenesis; Donor to donor variance; Endochondral ossification; Integrin receptors; Mechanical strain; Osteogenesis

Indexed keywords

ALKALINE PHOSPHATASE; BETA 2 MICROGLOBULIN; BETA5 INTEGRIN; CD51 ANTIGEN; CLATHRIN HEAVY CHAIN; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA1; DECORIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; KI 67 ANTIGEN; LUMICAN; OSTEONECTIN; OSTEOPONTIN; PROTEIN C FOS; SIALOPROTEIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ARTICLE; BONE DEVELOPMENT; BONE MATRIX; CELL DIFFERENTIATION; CELL STIMULATION; CHONDROGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; FEMALE; GENE EXPRESSION; GENE SEQUENCE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MARKER GENE; MECHANICAL STRESS; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TENSILE STRENGTH; TRANSCRIPTION REGULATION;

ADULT; AGED; AGED, 80 AND OVER; ALKALINE PHOSPHATASE; BIOLOGICAL MARKERS; BONE MARROW CELLS; CELLS, CULTURED; CHONDROGENESIS; FEMALE; HUMANS; MALE; MESENCHYMAL STEM CELLS; MIDDLE AGED; OSTEOGENESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, MECHANICAL; STROMAL CELLS; TRANSCRIPTION FACTORS;

EID: 35648934652     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2007.04.002     Document Type: Article

References (51)

1. Quarto R., Mastrogiacomo M., Cancedda R., Kutepov S.M., Mukhachev V., Lavroukov A., et al. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344 5 (2001) 385-386
2. Wakitani S., Imoto K., Yamamoto T., Saito M., Murata N., and Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 10 3 (2002) 199-206
3. Awad H.A., Boivin G.P., Dressler M.R., Smith F.N., Young R.G., and Butler D.L. Repair of patellar tendon injuries using a cell-collagen composite. J Orthop Res 21 3 (2003) 420-431
4. Yamaguchi A., Komori T., and Suda T. Regulation of osteoblast differentiation mediated by bone morphogenetic proteins, hedgehogs, and Cbfa1. Endocr Rev 21 4 (2000) 393-411
5. Shapiro F., Koide S., and Glimcher M.J. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 75 4 (1993) 532-553
6. Jee W.S., and Frost H.M. Skeletal adaptations during growth. Triangle 31 2/3 (1992) 77-88
7. Duncan R.L., and Turner C.H. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int 57 5 (1995) 344-358
8. Kapur S., Baylink D.J., and Lau K.H. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32 3 (2003) 241-251
9. Mikuni-Takagaki Y., Suzuki Y., Kawase T., and Saito S. Distinct responses of different populations of bone cells to mechanical stress. Endocrinology 137 5 (1996) 2028-2035
10. Jansen J.H., Weyts F.A., Westbroek I., Jahr H., Chiba H., Pols H.A., et al. Stretch-induced phosphorylation of ERK1/2 depends on differentiation stage of osteoblasts. J Cell Biochem 93 3 (2004) 542-551
11. Millward-Sadler S.J., and Salter D.M. Integrin-dependent signal cascades in chondrocyte mechanotransduction. Ann Biomed Eng 32 3 (2004) 435-446
12. Mauck R.L., Soltz M.A., Wang C.C., Wong D.D., Chao P.H., Valhmu W.B., et al. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122 3 (2000) 252-260
13. Mauck R.L., Nicoll S.B., Seyhan S.L., Ateshian G.A., and Hung C.T. Synergistic action of growth factors and dynamic loading for articular cartilage tissue engineering. Tissue Eng 9 4 (2003) 597-611
14. O'Driscoll S.W., and Salter R.B. The repair of major osteochondral defects in joint surfaces by neochondrogenesis with autogenous osteoperiosteal grafts stimulated by continuous passive motion. An experimental investigation in the rabbit. Clin Orthop Relat Res 208 (1986) 131-140
15. Setton L.A., Mow V.C., Muller F.J., Pita J.C., and Howell D.S. Mechanical behavior and biochemical composition of canine knee cartilage following periods of joint disuse and disuse with remobilization. Osteoarthritis Cartilage 5 1 (1997) 1-16
16. Peake M.A., Cooling L.M., Magnay J.L., Thomas P.B., and el Haj A.J. Selected contribution: regulatory pathways involved in mechanical induction of c-fos gene expression in bone cells. J Appl Physiol 89 6 (2000) 2498-2507
17. Stein G.S., Lian J.B., Stein J.L., van Wijnen A.J., and Montecino M. Transcriptional control of osteoblast growth and differentiation. Physiol Rev 76 2 (1996) 593-629
18. Turner C.H., Tu Y., and Onyia J.E. Mechanical loading of bone in vivo caused bone formation through early induction of c-fos, but not c-jun or c-myc. (Abstract). Ann Biomed Eng 24 (1996) S74
19. Lewinson D., Rachmiel A., Rihani-Bisharat S., Kraiem Z., Schenzer P., Korem S., et al. Stimulation of Fos- and Jun-related genes during distraction osteogenesis. J Histochem Cytochem 51 9 (2003) 1161-1168
20. Cavalcanti-Adam E.A., Adams C.S., et al. RGD peptides immobilized on a mechanically deformable surface promote osteoblast differentiation. J Bone Miner Res 17 12 (2003) 2130-2140
21. Hu D.D., Lin E.C., Kovach N.L., Hoyer J.R., and Smith J.W. A biochemical characterization of the binding of osteopontin to integrins alpha v beta 1 and alpha v beta 5. J Biol Chem 270 44 (1995) 26232-26238
22. Kurtis M.S., Schmidt T.A., Bugbee W.D., Loeser R.F., and Sah R.L. Integrin-mediated adhesion of human articular chondrocytes to cartilage. Arthritis Rheum 48 1 (2003) 110-118
23. Gronthos S., Simmons P.J., Graves S.E., and Robey P.G. Integrin-mediated interactions between human bone marrow stromal precursor cells and the extracellular matrix. Bone 28 2 (2001) 174-181
24. Tuan R.S., Boland G., and Tuli R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 5 1 (2003) 32-45
25. Estes B.T., Gimble J.M., and Guilak F. Mechanical signals as regulators of stem cell fate. Curr Top Dev Biol 60 (2004) 91-126
26. Neidlinger-Wilke C., Grood E.S., Wang H.H.-C., Brand R.A., and Claes L. Cell alignment is induced by cyclic changes in cell length: studies of cells grown in cyclically stretched substrates. J Orthop Res 19 2 (2001) 286-293
27. Bottlang M., Simnacher M., Schmitt H., Brand R.A., and Claes L. A cell strain system for small homogeneous strain applications. Biomed Tech (Berl) 42 11 (1997) 305-309
28. Murray D.W., and Rushton N. The effect of strain on bone cell prostaglandin E2 release: a new experimental method. Calcif Tissue Int 47 1 (1990) 35-39
29. Schluter C., Duchrow M., Wohlenberg C., Becker M.H., Key G., Flad H.D., et al. The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123 3 (1993) 513-522
30. Mackay A.M., Beck S.C., Murphy J.M., Barry F.P., Chichester C.O., and Pittenger M.F. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4 4 (1998) 415-428
31. Kulterer B., Friedl G., Jandrositz A., Sanchez-Cabo F., Prokesch A., Paar C., et al. Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics 8 1 (2007) 70
32. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 4 (2001) 402-408
33. Sottile V., Halleux C., Bassilana F., Keller H., and Seuwen K. Stem cell characteristics of human trabecular bone-derived cells. Bone 30 5 (2002) 699-704
34. el Haj A.J., Minter S.L., Rawlinson S.C., Suswillo R., and Lanyon L.E. Cellular responses to mechanical loading in vitro. J Bone Miner Res 5 9 (1990) 923-932
35. Bi W., Deng J.M., Zhang Z., Behringer R.R., and de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet 22 1 (1999) 85-89
36. Lian J.B., Javed A., Zaidi S.K., Lengner C., Montecino M., van Wijnen A.J., et al. Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors. Crit Rev Eukaryot Gene Expr 14 1-2 (2004) 1-41
37. Barry F., Boynton R.E., Liu B., and Murphy J.M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp Cell Res 268 2 (2001) 189-200
38. Kuznetsov S.A., Krebsbach P.H., Satomura K., Kerr J., Riminucci M., Benayahu D., et al. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 12 9 (1997) 1335-1347
39. Aubin J.E., and Triffitt J.T. Mesenchymal stem cells and the osteoblast lineage. Principles of Bone Biology. 2nd edn vol. 1 (2002) pp. 59-81
40. Phinney D.G., Kopen G., Righter W., Webster S., Tremain N., and Prockop D.J. Donor variation in the growth properties and osteogenic potential of human marrow stromal cells. J Cell Biochem 75 3 (1999) 424-436
41. Marom R., Shur I., Solomon R., and Benayahu D. Characterization of adhesion and differentiation markers of osteogenic marrow stromal cells. J Cell Physiol 202 1 (2005) 41-48
42. Madras N., Gibbs A.L., Zhou Y., Zandstra P.W., and Aubin J.E. Modeling stem cell development by retrospective analysis of gene expression profiles in single progenitor-derived colonies. Stem Cells 20 3 (2002) 230-240
43. Candeliere G.A., Rao Y., Floh A., Sandler S.D., and Aubin J.E. cDNA fingerprinting of osteoprogenitor cells to isolate differentiation stage-specific genes. Nucleic Acids Res 27 4 (1999) 1079-1083
44. Tremain N., Korkko J., Ibberson D., Kopen G.C., DiGirolamo C., and Phinney D.G. MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells 19 5 (2001) 408-418
45. Peake M.A., and el Haj A.J. Preliminary characterisation of mechanoresponsive regions of the c-fos promoter in bone cells. FEBS Lett 537 1-3 (2003) 117-120
46. Papachristou D.J., Pirttiniemi P., Kantomaa T., Papavassiliou A.G., and Basdra E.K. JNK/ERK-AP-1/Runx2 induction "paves the way" to cartilage load-ignited chondroblastic differentiation. Histochem Cell Biol 124 3-4 (2005) 215-223
47. Saamanen A.M., Salminen H.J., Rantakokko A.J., Heinegard D., and Vuorio E.I. Murine fibromodulin: cDNA and genomic structure, and age-related expression and distribution in the knee joint. Biochem J 355 Pt 3 (2001) 577-585
48. Huang C.Y., Reuben P.M., and Cheung H.S. 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 23 8 (2005) 1113-1121
49. Benya P.D., and Shaffer J.D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30 1 (1982) 215-224
50. Mauney J.R., Jaquiery C., Volloch V., Heberer M., Martin I., and Kaplan D.L. In vitro and in vivo evaluation of differentially demineralized cancellous bone scaffolds combined with human bone marrow stromal cells for tissue engineering. Biomaterials 26 16 (2005) 3173-3185
51. Leskela H.V., Olkku A., Lehtonen S., Mahonen A., Koivunen J., Turpeinen M., et al. Estrogen receptor alpha genotype confers interindividual variability of response to estrogen and testosterone in mesenchymal-stem-cell-derived osteoblasts. Bone 39 5 (2006) 1026-1034