Mechanical stimulation of human tendon stem/progenitor cells results in upregulation of matrix proteins, integrins and MMPs, and activation of p38 and ERK1/2 kinases

BMC Molecular Biology

Volumn 16, Issue 1, 2015, Pages

  Popov, Cvetan ^a   Burggraf, Martina ^a   Kreja, Ludwika ^b   Ignatius, Anita ^b   Schieker, Matthias ^a   Docheva, Denitsa ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Collagen binding integrins; Matrix metalloproteinases; Mechanical stimulation; Tendon stem progenitor cells; Tendon related genes

Indexed keywords

ALPHA1 INTEGRIN; ALPHA2 INTEGRIN; COLLAGENASE 3; FIBROMODULIN; GELATINASE B; INTEGRIN; INTEGRIN ALPHA11; LUMICAN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VERSICAN;

ADULT; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; INVESTIGATIVE PROCEDURES; MALE; MECHANICAL STIMULATION; NORMAL HUMAN; POLYMERASE CHAIN REACTION; QUANTITATIVE STUDY; STEM CELL; TENDON; TENDON STEM PROGENITOR CELL; UPREGULATION; WESTERN BLOTTING; ACHILLES TENDON; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; YOUNG ADULT;

ACHILLES TENDON; ADULT; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; MALE; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASES; MECHANOTRANSDUCTION, CELLULAR; STEM CELLS; STRESS, MECHANICAL; YOUNG ADULT;

EID: 84925334309     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/s12867-015-0036-6     Document Type: Article

References (53)

1. Bi Y, Ehirchiou D, Kilts TM, Inkson CA, Embree MC, Sonoyama W, et al. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med. 2007;13(10):1219-27.
2. Docheva D, Popov C, Alberton P, Aszodi A. Integrin signaling in skeletal development and function. Birth defects research Part C, Embryo today: reviews. 2014;102(1):13-36.
3. Mammoto A, Mammoto T, Ingber DE. Mechanosensitive mechanisms in transcriptional regulation. J Cell Sci. 2012;125(Pt 13):3061-73.
4. Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004;84(2):649-98.
5. Maeda E, Shelton JC, Bader DL, Lee DA. Differential regulation of gene expression in isolated tendon fascicles exposed to cyclic tensile strain in vitro. J Appl Physiol. 2009;106(2):506-12.
6. Wang JH. Mechanobiology of tendon. J Biomech. 2006;39(9):1563-82.
7. Docheva D, Popov C, Mutschler W, Schieker M. Human mesenchymal stem cells in contact with their environment: surface characteristics and the integrin system. J Cell Mol Med. 2007;11(1):21-38.
8. Popov C, Radic T, Haasters F, Prall WC, Aszodi A, Gullberg D, et al. Integrins alpha2beta1 and alpha11beta1 regulate the survival of mesenchymal stem cells on collagen I. Cell death & disease. 2011;2:e186.
9. Mackley JR, Ando J, Herzyk P, Winder SJ. Phenotypic responses to mechanical stress in fibroblasts from tendon, cornea and skin. Biochemical j. 2006;396(2):307-16.
10. Fong KD, Trindade MC, Wang Z, Nacamuli RP, Pham H, Fang TD, et al. Microarray analysis of mechanical shear effects on flexor tendon cells. Plast Reconstr Surg. 2005;116(5):1393-404. discussion 1405-1396.
11. Scott A, Cook JL, Hart DA, Walker DC, Duronio V, Khan KM. Tenocyte responses to mechanical loading in vivo: a role for local insulin-like growth factor 1 signaling in early tendinosis in rats. Arthritis Rheum. 2007;56(3):871-81.
12. Androjna C, Spragg RK, Derwin KA. Mechanical conditioning of cell-seeded small intestine submucosa: a potential tissue-engineering strategy for tendon repair. Tissue Eng. 2007;13(2):233-43.
13. Kohler J, Popov C, Klotz B, Alberton P, Prall WC, Haasters F, et al. Uncovering the cellular and molecular changes in tendon stem/progenitor cells attributed to tendon aging and degeneration. Aging cell. 2013;12(6):988-99.
14. Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O'Connor KC. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells. 2010;28(4):788-98.
15. Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis res ther. 2007;9(1):204.
16. Covas DT, Panepucci RA, Fontes AM, Silva Jr WA, Orellana MD, Freitas MC, et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol. 2008;36(5):642-54.
17. Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol. 2001;3(9):778-84.
18. Lin G, Liu G, Banie L, Wang G, Ning H, Lue TF, et al. Tissue distribution of mesenchymal stem cell marker Stro-1. Stem Cells Dev. 2011;20(10):1747-52.
19. Tempfer H, Wagner A, Gehwolf R, Lehner C, Tauber M, Resch H, et al. Perivascular cells of the supraspinatus tendon express both tendon- and stem cell-related markers. Histochem Cell Biol. 2009;131(6):733-41.
20. Brent AE, Schweitzer R, Tabin CJ. A somitic compartment of tendon progenitors. Cell. 2003;113(2):235-48.
21. Docheva D, Hunziker EB, Fassler R, Brandau O. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol. 2005;25(2):699-705.
22. Wang JH, Thampatty BP, Lin JS, Im HJ. Mechanoregulation of gene expression in fibroblasts. Gene. 2007;391(1-2):1-15.
23. Ying B, Fan H, Wen F, Xu D, Liu D, Yang D, et al. Mechanical strain-induced c-fos expression in pulmonary epithelial cell line A549. Biochem Biophys Res Commun. 2006;347(1):369-72.
24. Liedert A, Kassem M, Claes L, Ignatius A. Mechanosensitive promoter region in the human HB-GAM gene. Biochem Biophys Res Commun. 2009;387(2):289-93.
25. Yang G, Crawford RC, Wang JH. Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J Biomech. 2004;37(10):1543-50.
26. Howard PS, Kucich U, Taliwal R, Korostoff JM. Mechanical forces alter extracellular matrix synthesis by human periodontal ligament fibroblasts. J Periodontal Res. 1998;33(8):500-8.
27. Hsieh AH, Tsai CM, Ma QJ, Lin T, Banes AJ, Villarreal FJ, et al. Time-dependent increases in type-III collagen gene expression in medical collateral ligament fibroblasts under cyclic strains. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2000;18(2):220-7.
28. Yoon JH, Halper J. Tendon proteoglycans: biochemistry and function. Journal of musculoskeletal & neuronal interactions. 2005;5(1):22-34.
29. Wight TN. Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr Opin Cell Biol. 2002;14(5):617-23.
30. 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.
31. Desmoulin GT, Hewitt CR, Hunter CJ. Disc strain and resulting positive mRNA expression from application of a noninvasive treatment. Spine. 2011;36(14):E921-8.
32. 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(8):1942-53.
33. Burkholder TJ. Mechanotransduction in skeletal muscle. Frontiers in bioscience: a journal and virtual library. 2007;12:174-91.
34. Sakamoto K, Goodyear LJ. Invited review: intracellular signaling in contracting skeletal muscle. J Appl Physiol (1985). 2002;93(1):369-83.
35. Zhou Y, Millward-Sadler SJ, Lin H, Robinson H, Goldring M, Salter DM, et al. Evidence for JNK-dependent up-regulation of proteoglycan synthesis and for activation of JNK1 following cyclical mechanical stimulation in a human chondrocyte culture model. Osteoarthritis and cartilage / OARS, Osteoarthritis Research Society. 2007;15(8):884-93.
36. De Croos JN, Dhaliwal SS, Grynpas MD, Pilliar RM, Kandel RA. Cyclic compressive mechanical stimulation induces sequential catabolic and anabolic gene changes in chondrocytes resulting in increased extracellular matrix accumulation. Matrix biology: journal of the International Society for Matrix Biology. 2006;25(6):323-31.
37. Xu HG, Li ZR, Wang H, Liu P, Xiang SN, Wang CD, et al. Expression of ectonucleotide pyrophosphatase-1 in end-plate chondrocytes with transforming growth factor beta 1 siRNA interference by cyclic mechanical tension. Chin Med J. 2013;126(20):3886-90.
38. Toma CD, Ashkar S, Gray ML, Schaffer JL, Gerstenfeld LC. Signal transduction of mechanical stimuli is dependent on microfilament integrity: identification of osteopontin as a mechanically induced gene in osteoblasts. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 1997;12(10):1626-36.
39. Plotkin LI, Mathov I, Aguirre JI, Parfitt AM, Manolagas SC, Bellido T. Mechanical stimulation prevents osteocyte apoptosis: requirement of integrins, Src kinases, and ERKs. American journal of physiology Cell physiology. 2005;289(3):C633-43.
40. Kong D, Zheng T, Zhang M, Wang D, Du S, Li X, et al. Static mechanical stress induces apoptosis in rat endplate chondrocytes through MAPK and mitochondria-dependent caspase activation signaling pathways. PLoS One. 2013;8(7):e69403.
41. Matsui H, Fukuno N, Kanda Y, Kantoh Y, Chida T, Nagaura Y, et al. The expression of Fn14 via mechanical stress-activated JNK contributes to apoptosis induction in osteoblasts. The Journal of biological chemistry. 2014;289(10):6438-50.
42. Danciu TE, Adam RM, Naruse K, Freeman MR, Hauschka PV. Calcium regulates the PI3K-Akt pathway in stretched osteoblasts. FEBS Lett. 2003;536(1-3):193-7.
43. Munshi HG, Stack MS. Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Rev. 2006;25(1):45-56.
44. Yang G, Im HJ, Wang JH. Repetitive mechanical stretching modulates IL-1beta induced COX-2, MMP-1 expression, and PGE2 production in human patellar tendon fibroblasts. Gene. 2005;363:166-72.
45. Wang T, Lin Z, Day RE, Gardiner B, Landao-Bassonga E, Rubenson J, et al. Programmable mechanical stimulation influences tendon homeostasis in a bioreactor system. Biotechnol Bioeng. 2013;110(5):1495-507.
46. Fujisawa T, Hattori T, Takahashi K, Kuboki T, Yamashita A, Takigawa M. Cyclic mechanical stress induces extracellular matrix degradation in cultured chondrocytes via gene expression of matrix metalloproteinases and interleukin-1. J Biochem. 1999;125(5):966-75.
47. Sasaki K, Takagi M, Konttinen YT, Sasaki A, Tamaki Y, Ogino T, et al. Upregulation of matrix metalloproteinase (MMP)-1 and its activator MMP-3 of human osteoblast by uniaxial cyclic stimulation. J Biomed Mater Res B Appl Biomater. 2007;80(2):491-8.
48. Archambault J, Tsuzaki M, Herzog W, Banes AJ. Stretch and interleukin-1beta induce matrix metalloproteinases in rabbit tendon cells in vitro. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2002;20(1):36-9.
49. Sun HB, Yokota H. Reduction of cytokine-induced expression and activity of MMP-1 and MMP-13 by mechanical strain in MH7A rheumatoid synovial cells. Matrix biology: journal of the International Society for Matrix Biology. 2002;21(3):263-70.
50. Neidlinger-Wilke C, Wilke HJ, Claes L. Cyclic stretching of human osteoblasts affects proliferation and metabolism: a new experimental method and its application. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 1994;12(1):70-8.
51. Liu J, Zou L, Wang J, Zhao Z. Validation of beta-actin used as endogenous control for gene expression analysis in mechanobiology studies. Stem Cells. 2009;27(9):2371-2.
52. Kopf J, Petersen A, Duda GN, Knaus P. BMP2 and mechanical loading cooperatively regulate immediate early signalling events in the BMP pathway. BMC Biol. 2012;10:37.
53. Alberton P, Popov C, Pragert M, Kohler J, Shukunami C, Schieker M, et al. Conversion of human bone marrow-derived mesenchymal stem cells into tendon progenitor cells by ectopic expression of scleraxis. Stem Cells Dev. 2012;21(6):846-58.