Optimizing an intermittent stretch paradigm using ERK1/2 phosphorylation results in increased collagen synthesis in engineered ligaments

Tissue Engineering - Part A

Volumn 18, Issue 3-4, 2012, Pages 277-284

  Paxton, Jennifer Z ^a   Hagerty, Paul ^b   Andrick, Jonathan J ^c   Baar, Keith ^a,b,c  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; OPTIMIZATION; TISSUE;

COLLAGEN CONTENT; COLLAGEN SYNTHESIS; CYCLIC STRETCH; DYNAMIC MECHANICAL; MECHANICAL STRETCH;

PHOSPHORYLATION;

COLLAGEN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL; ARTICLE; BIOREACTOR; BIOSYNTHESIS; CHICKEN; CYTOLOGY; ENZYME ACTIVATION; ENZYMOLOGY; FIBROBLAST; LIGAMENT; MECHANICAL STRESS; METABOLISM; METHODOLOGY; PHOSPHORYLATION; RAT; TENDON; TISSUE ENGINEERING;

ANIMALS; BIOREACTORS; CHICKENS; COLLAGEN; ENZYME ACTIVATION; FIBROBLASTS; LIGAMENTS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; RATS; STRESS, MECHANICAL; TENDONS; TISSUE ENGINEERING;

EID: 84856241478     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2011.0336     Document Type: Article

References (40)

1. Maffulli, N., Waterston, S.W., Squair, J., Reaper, J., and Douglas, A.S. Changing incidence of Achilles tendon rupture in Scotland: a 15-year study. Clin J Sport Med 9, 157, 1999.
2. Loitz, B.J., Zernicke, R.F., Vailas, A.C., Kody, M.H., and Meals, R.A. Effects of short-term immobilization versus continuous passive motion on the biomechanical and biochemical properties of the rabbit tendon. Clin Orthop 244, 265, 1989.
3. Vailas, A.C., Deluna, D.M., Lewis, L.L., Curwin, S.L., Roy, R.R., and Alford, E.K. Adaptation of bone and tendon to prolonged hindlimb suspension in rats. J Appl Physiol 65, 373, 1988.
4. Arruda, E.M., Calve, S., Dennis, R.G., Mundy, K., and Baar, K. Regional variation of tibialis anterior tendon mechanics is lost following denervation. J Appl Physiol 101, 1113, 2006.
5. Heinemeier, K., Langberg, H., Olesen, J.L., and Kjaer, M. Role of TGF-beta1 in relation to exercise-induced type I collagen synthesis in human tendinous tissue. J Appl Physiol 95, 2390, 2003.
6. Kjaer, M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84, 649, 2004.
7. Kjaer, M., Langberg, H., Heinemeier, K., Bayer, M.L., Hansen, M., Holm, L., et al. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports 19, 500, 2009.
8. Mackey,A.L., Heinemeier, K.M., Koskinen, S.O., and Kjaer,M. Dynamic adaptation of tendon andmuscle connective tissue to mechanical loading. Connective Tissue Res 49, 165, 2008.
9. Heinemeier, K.M., Olesen, J.L., Haddad, F., Langberg, H., Kjaer, M., Baldwin, K.M., et al. Expression of collagen and related growth factors in rat tendon and skeletal muscle in response to specific contraction types. J Physiol 582, 1303, 2007.
10. Wang, J.G., Miyazu, M., Matsushita, E., Sokabe, M., and Naruse, K. Uniaxial cyclic stretch induces focal adhesion kinase (FAK) tyrosine phosphorylation followed by mitogen-activated protein kinase (MAPK) activation. Biochem Biophys Res Commun 288, 356, 2001.
11. Banes, A.J., Tsuzaki, M., Hu, P., Brigman, B., Brown, T., Almekinders, L., et al. PDGF-BB, IGF-I and mechanical load stimulate DNA synthesis in avian tendon fibroblasts in vitro. J Biomech 28, 1505, 1995.
12. Arnoczky, S.P., Tian, T., Lavagnino, M., Gardner, K., Schuler, P., and Morse, P. Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude, and cytosolic calcium. J Orthop Res 20, 947, 2002.
13. MacKenna, D.A., Dolfi, F., Vuori, K., and Ruoslahti, E. Extracellular signal-regulated kinase and c-Jun NH2-terminal kinase activation by mechanical stretch is integrin-dependent and matrix-specific in rat cardiac fibroblasts. J Clin Invest 101, 301, 1998.
14. Papakrivopoulou, J., Lindahl, G.E., Bishop, J.E., and Laurent, G.J. Differential roles of extracellular signal-regulated kinase 1/2 and p38MAPK in mechanical load-induced procollagen alpha1(I) gene expression in cardiac fibroblasts. Cardiovasc Res 61, 736, 2004.
15. Cukierman, E., Pankov, R., Stevens, D.R., and Yamada, K.M. Taking cell-matrix adhesions to the third dimension. Science 294, 1708, 2001.
16. Bayer, M.L., Yeung, C.Y., Kadler, K.E., Qvortrup, K., Baar, K., Svensson, R.B., et al. The initiation of embryoniclike collagen fibrillogenesis by adult human tendon fibroblasts when cultured under tension. Biomaterials 31, 4889, 2010.
17. Kapacee, Z., Richardson, S.H., Lu, Y., Starborg, T., Holmes, D.F., Baar, K., et al. Tension is required for fibripositor formation. Matrix Biol 27, 371, 2008.
18. Paxton, J.Z., Donnelly, K., Keatch, R.P., Baar, K., and Grover, L.M. Factors affecting the longevity and strength in an in vitro model of the bone-ligament interface. Ann Biomed Eng 38, 2155, 2010.
19. Paxton, J.Z., Grover, L.M., and Baar, K. Engineering an in vitro model of a functional ligament from bone to bone. Tissue Eng Part A 16, 3515, 2010.
20. Paxton, J.Z., Donnelly, K., Keatch, R.P., and Baar, K. Engineering the bone-ligament interface using polyethylene glycol diacrylate incorporated with hydroxyapatite. Tissue Eng Part A 15, 1201, 2009.
21. Birla, R.K., Huang, Y.C., and Dennis, R.G. Development of a novel bioreactor for the mechanical loading of tissueengineered heart muscle. Tissue Eng 13, 2239, 2007.
22. Woessner, J.F., Jr. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93, 440, 1961.
23. Neuman, R.E., and Logan, M.A. The determination of hydroxyproline. J Biol Chem 184, 299, 1950.
24. Yasuda, K., Erickson, A.R., Beynnon, B.D., Johnson, R.J., and Pope, M.H. Dynamic elongation behavior in the medial collateral and anterior cruciate ligaments during lateral impact loading. J Orthop Res 11, 190, 1993.
25. Miyaki, S., Ushida, T., Nemoto, K., Shimojo, H., Itabashi, A., Ochiai, N., et al. Mechanical stretch in anterior cruciate ligament derived cells regulates type I collagen and decorin expression through extracellular signal-regulated kinase 1/2 pathway. Mater Sci Eng C 17, 91, 2001.
26. Zhu, J., Zhang, X., Wang, C., and Peng, X. Periprosthetic strain magnitude-dependent upregulation of type I collagen synthesis in human osteoblasts through an ERK1/2 pathway. Int Orthop 33, 1455, 2009.
27. Nishimura, K., Blume, P., Ohgi, S., and Sumpio, B.E. Effect of different frequencies of tensile strain on human dermal fibroblast proliferation and survival. Wound Repair Regen 15, 646, 2007.
28. Rubin, J., Murphy, T.C., Fan, X., Goldschmidt, M., and Taylor, W.R. Activation of extracellular signal-regulated kinase is involved in mechanical strain inhibition of RANKL expression in bone stromal cells. J Bone Miner Res 17, 1452, 2002.
29. 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, 542, 2004.
30. Nishimura, K., Blume, P., Ohgi, S., and Sumpio, B.E. The effect of different frequencies of stretch on human dermal keratinocyte proliferation and survival. J Surg Res 155, 125, 2009.
31. Martineau, L.C., and Gardiner, P.F. Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 91, 693, 2001.
32. Fleming, B.C., Beynnon, B.D., Renstrom, P.A., Johnson, R.J., Nichols, C.E., Peura, G.D., et al. The strain behavior of the anterior cruciate ligament during stair climbing: an in vivo study. Arthroscopy 15, 185, 1999.
33. Beynnon, B.D., and Fleming, B.C. Anterior cruciate ligament strain in-vivo: a review of previous work. J Biomech 31, 519, 1998.
34. Lim, H.C., Bae, J.H., Wang, J.H., Bae, T.S., Kim, C.W., Hwang, J.H., et al. The biomechanical performance of bone block and soft-tissue posterior cruciate ligament graft fixation with interference screw and cross-pin techniques. Arthroscopy 25, 250, 2009.
35. Wang, I.E.,Mitroo, S., Chen, F.H., Lu,H.H., andDoty, S.B.Agedependent changes in matrix composition and organization at the ligament-to-bone insertion. J Orthop Res 24, 1745, 2006.
36. Juncosa-Melvin, N., Matlin, K.S., Holdcraft, R.W., Nirmalanandhan, V.S., and Butler, D.L. Mechanical stimulation increases collagen type I and collagen type III gene expression of stem cell-collagen sponge constructs for patellar tendon repair. Tissue Eng 13, 1219, 2007.
37. Balestrini, J.L., and Billiar, K.L. Magnitude and duration of stretch modulate fibroblast remodeling. J Biomech Eng 131, 051005, 2009.
38. Saber, S., Zhang, A.Y., Ki, S.H., Lindsey, D.P., Smith, R.L., Riboh, J., et al. Flexor tendon tissue engineering: bioreactor cyclic strain increases construct strength. Tissue Eng Part A 16, 2085, 2010.
39. Sengupta, S., Peterson, T.R., and Sabatini, D.M. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40, 310, 2010.
40. Hamilton, D.L., Philp, A., MacKenzie, M.G., and Baar, K. A limited role for PI(3,4,5)P3 regulation in controlling skeletal muscle mass in response to resistance exercise. PLoS One 5, e11624, 2010.