Integrin - Dependent Mechanotransduction in Mechanically Stimulated Human Annulus Fibrosus Cells: Evidence for an Alternative Mechanotransduction Pathway Operating with Degeneration

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Gilbert, Hamish T J ^a   Nagra, Navraj S ^a   Freemont, Anthony J ^a   Millward Sadler, Sarah J ^a   Hoyland, Judith A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECANASE 1; ARGINYLGLYCYLASPARTIC ACID; COLLAGEN TYPE 1; FOCAL ADHESION KINASE; INTEGRIN;

ADULT; ANNULUS FIBROSUS; ANNULUS FIBROSUS CELL; ARTICLE; CELL VIABILITY; CONNECTIVE TISSUE CELL; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; INTERVERTEBRAL DISK DEGENERATION; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CELL SURVIVAL; CELLS, CULTURED; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; MECHANOTRANSDUCTION, CELLULAR; OLIGOPEPTIDES; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84883499674     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072994     Document Type: Article

References (50)

1. Shirazi-Adl SA, Shrivastava SC, Ahmed AM, (1984) Stress analysis of the lumbar disc-body unit in compression. A three-dimensional nonlinear finite element study. Spine (Phila Pa 1976) 9: 120-134.
2. Adams MA, McNally DS, Dolan P, (1996) 'Stress' distributions inside intervertebral discs. The effects of age and degeneration. J Bone Joint Surg Br 78: 965-972.
3. Ishihara H, McNally DS, Urban JP, Hall AC, (1996) Effects of hydrostatic pressure on matrix synthesis in different regions of the intervertebral disk. J Appl Physiol 80: 839-846.
4. Hutton WC, Elmer WA, Bryce LM, Kozlowska EE, Boden SD, et al. (2001) Do the intervertebral disc cells respond to different levels of hydrostatic pressure? Clin Biomech (Bristol, Avon) 16: 728-734.
5. MacLean JJ, Lee CR, Grad S, Ito K, Alini M, et al. (2003) Effects of immobilization and dynamic compression on intervertebral disc cell gene expression in vivo. Spine (Phila Pa 1976) 28: 973-981.
6. MacLean JJ, Lee CR, Alini M, Iatridis JC, (2005) The effects of short-term load duration on anabolic and catabolic gene expression in the rat tail intervertebral disc. J Orthop Res 23: 1120-1127.
7. Kasra M, Merryman WD, Loveless KN, Goel VK, Martin JD, et al. (2006) Frequency response of pig intervertebral disc cells subjected to dynamic hydrostatic pressure. J Orthop Res 24: 1967-1973.
8. Neidlinger-Wilke C, Wurtz K, Urban JP, Borm W, Arand M, et al. (2006) Regulation of gene expression in intervertebral disc cells by low and high hydrostatic pressure. Eur Spine J 15Suppl 3: S372-378.
9. Wang DL, Jiang SD, Dai LY, (2007) Biologic response of the intervertebral disc to static and dynamic compression in vitro. Spine (Phila Pa 1976) 32: 2521-2528.
10. Korecki CL, Kuo CK, Tuan RS, Iatridis JC, (2009) Intervertebral disc cell response to dynamic compression is age and frequency dependent. J Orthop Res 27: 800-806.
11. Wuertz K, Godburn K, Maclean JJ, Barbir A, Stinnett Donnelly J, et al. (2009) In vivo remodeling of intervertebral discs in response to short- and long-term dynamic compression. J Orthop Res.
12. Gilbert HT, Hoyland JA, Millward-Sadler SJ, (2010) The response of human anulus fibrosus cells to cyclic tensile strain is frequency-dependent and altered with disc degeneration. Arthritis Rheum 62: 3385-3394.
13. Hutton WC, Elmer WA, Boden SD, Hyon S, Toribatake Y, et al. (1999) The effect of hydrostatic pressure on intervertebral disc metabolism. Spine (Phila Pa 1976) 24: 1507-1515.
14. Matsumoto T, Kawakami M, Kuribayashi K, Takenaka T, Tamaki T, (1999) Cyclic mechanical stretch stress increases the growth rate and collagen synthesis of nucleus pulposus cells in vitro. Spine (Phila Pa 1976) 24: 315-319.
15. Kasra M, Goel V, Martin J, Wang ST, Choi W, et al. (2003) Effect of dynamic hydrostatic pressure on rabbit intervertebral disc cells. J Orthop Res 21: 597-603.
16. Maclean JJ, Lee CR, Alini M, Iatridis JC, (2004) Anabolic and catabolic mRNA levels of the intervertebral disc vary with the magnitude and frequency of in vivo dynamic compression. J Orthop Res 22: 1193-1200.
17. Wenger KH, Woods JA, Holecek A, Eckstein EC, Robertson JT, et al. (2005) Matrix remodeling expression in anulus cells subjected to increased compressive load. Spine (Phila Pa 1976) 30: 1122-1126.
18. Lotz JC, Chin JR, (2000) Intervertebral disc cell death is dependent on the magnitude and duration of spinal loading. Spine 25: 1477-1483.
19. Court C, Colliou OK, Chin JR, Liebenberg E, Bradford DS, et al. (2001) The effect of static in vivo bending on the murine intervertebral disc. Spine J 1: 239-245.
20. Le Maitre CL, Frain J, Fotheringham AP, Freemont AJ, Hoyland JA, (2008) Human cells derived from degenerate intervertebral discs respond differently to those derived from non-degenerate intervertebral discs following application of dynamic hydrostatic pressure. Biorheology 45: 563-575.
21. Li S, Jia X, Duance VC, Blain EJ, (2011) The effects of cyclic tensile strain on the organisation and expression of cytoskeletal elements in bovine intervertebral disc cells: an in vitro study. Eur Cell Mater 21: 508-522.
22. Gilbert HT, Hoyland JA, Freemont AJ, Millward-Sadler SJ, (2011) The involvement of interleukin-1 and interleukin-4 in the response of human annulus fibrosus cells to cyclic tensile strain: an altered mechanotransduction pathway with degeneration. Arthritis Res Ther 13: R8.
23. Hynes RO, (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
24. Gupta V, Grande-Allen KJ, (2006) Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. Cardiovasc Res 72: 375-383.
25. Salter DM, Robb JE, Wright MO, (1997) Electrophysiological responses of human bone cells to mechanical stimulation: evidence for specific integrin function in mechanotransduction. J Bone Miner Res 12: 1133-1141.
26. Wright MO, Nishida K, Bavington C, Godolphin JL, Dunne E, et al. (1997) Hyperpolarisation of cultured human chondrocytes following cyclical pressure-induced strain: evidence of a role for alpha 5 beta 1 integrin as a chondrocyte mechanoreceptor. J Orthop Res 15: 742-747.
27. Millward-Sadler SJ, Wright MO, Lee H, Nishida K, Caldwell H, et al. (1999) Integrin-regulated secretion of interleukin 4: A novel pathway of mechanotransduction in human articular chondrocytes. J Cell Biol 145: 183-189.
28. Holledge MM, Millward-Sadler SJ, Nuki G, Salter DM, (2008) Mechanical regulation of proteoglycan synthesis in normal and osteoarthritic human articular chondrocytes-roles for alpha5 and alphaVbeta5 integrins. Biorheology 45: 275-288.
29. Kock LM, Schulz RM, van Donkelaar CC, Thummler CB, Bader A, et al. (2009) RGD-dependent integrins are mechanotransducers in dynamically compressed tissue-engineered cartilage constructs. J Biomech 42: 2177-2182.
30. Le Maitre CL, Frain J, Millward-Sadler J, Fotheringham AP, Freemont AJ, et al. (2009) Altered integrin mechanotransduction in human nucleus pulposus cells derived from degenerated discs. Arthritis Rheum 60: 460-469.
31. Liu S, Calderwood DA, Ginsberg MH, (2000) Integrin cytoplasmic domain-binding proteins. J Cell Sci 113 (Pt 20): 3563-3571.
32. Yano Y, Geibel J, Sumpio BE, (1996) Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. Am J Physiol 271: C635-649.
33. Ali MH, Mungai PT, Schumacker PT, (2006) Stretch-induced phosphorylation of focal adhesion kinase in endothelial cells: role of mitochondrial oxidants. Am J Physiol Lung Cell Mol Physiol 291: L38-45.
34. 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.
35. Lee HS, Millward-Sadler SJ, Wright MO, Nuki G, Salter DM, (2000) Integrin and mechanosensitive ion channel-dependent tyrosine phosphorylation of focal adhesion proteins and beta-catenin in human articular chondrocytes after mechanical stimulation. J Bone Miner Res 15: 1501-1509.
36. Xia M, Zhu Y, (2008) Expression of integrin subunits in the herniated intervertebral disc. Connect Tissue Res 49: 464-469.
37. Loeser RF, (2000) Chondrocyte integrin expression and function. Biorheology 37: 109-116.
38. Nettles DL, Richardson WJ, Setton LA, (2004) Integrin expression in cells of the intervertebral disc. J Anat 204: 515-520.
39. Millward-Sadler SJ, Wright MO, Davies LW, Nuki G, Salter DM, (2000) Mechanotransduction via integrins and interleukin-4 results in altered aggrecan and matrix metalloproteinase 3 gene expression in normal, but not osteoarthritic, human articular chondrocytes. Arthritis Rheum 43: 2091-2099.
40. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
41. Chowdhury TT, Appleby RN, Salter DM, Bader DA, Lee DA, (2006) Integrin-mediated mechanotransduction in IL-1 beta stimulated chondrocytes. Biomech Model Mechanobiol 5: 192-201.
42. MacLean JJ, Roughley PJ, Monsey RD, Alini M, Iatridis JC, (2008) In vivo intervertebral disc remodeling: kinetics of mRNA expression in response to a single loading event. J Orthop Res 26: 579-588.
43. Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, et al. (1994) Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79: 1157-1164.
44. Frisch SM, Francis H, (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124: 619-626.
45. McGill G, Shimamura A, Bates RC, Savage RE, Fisher DE, (1997) Loss of matrix adhesion triggers rapid transformation-selective apoptosis in fibroblasts. J Cell Biol 138: 901-911.
46. Terahara K, Takahashi KG, Mori K, (2003) Apoptosis by RGD-containing peptides observed in hemocytes of the Pacific oyster, Crassostrea gigas. Dev Comp Immunol 27: 521-528.
47. Millward-Sadler SJ, Wright MO, Lee H, Caldwell H, Nuki G, et al. (2000) Altered electrophysiological responses to mechanical stimulation and abnormal signalling through alpha5beta1 integrin in chondrocytes from osteoarthritic cartilage. Osteoarthritis Cartilage 8: 272-278.
48. Bellin R, Capila I, Lincecum J, Park PW, Reizes O, et al. (2002) Unlocking the secrets of syndecans: transgenic organisms as a potential key. Glycoconj J 19: 295-304.
49. Sachs F, (2010) Stretch-activated ion channels: what are they? Physiology (Bethesda) 25: 50-56.
50. Knudson CB, Knudson W (2004) Hyaluronan and CD44: modulators of chondrocyte metabolism. Clin Orthop Relat Res: S152-162.