In vitro collagen biomarkers in mechanically stimulated human tendon cells: a systematic review

References

• Thorpe CT, Birch HL, Clegg PD, Screen HRC. The role of the non-collagenous matrix in tendon function. Int J Exp Pathol. 2013;94(4):248–259. doi:10.1111/iep.12027.
   PubMed Web of Science ®Google Scholar
• Khan KM, Scott A. Mechanotherapy: how physical therapists’ prescription of exercise promotes tissue repair. Br J Sports Med. 2009;43(4):247–252. doi:10.1136/bjsm.2008.054239.
   PubMed Web of Science ®Google Scholar
• Wang JHC. Mechanobiology of tendon. J Biomech. 2006;39(9):1563–1582. doi:10.1016/j.jbiomech.2005.05.011.
   PubMed Web of Science ®Google Scholar
• Kjær M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm L, Doessing S, Kongsgaard M, Krogsgaard MR, Magnusson SP, et al. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports. 2009;19(4):500–510. doi:10.1111/j.1600-0838.2009.00986.x.
   PubMed Web of Science ®Google Scholar
• Kjær M, Magnusson P, Krogsgaard M, Møller JB, Olesen J, Heinemeier K, Hansen M, Haraldsson B, Koskinen S, Esmarck B, Langberg H. Extracellular matrix adaptation of tendon and skeletal muscle to exercise. J Anat. 2006;208(4):445–450. doi:10.1111/j.1469-7580.2006.00549.x.
   PubMed Web of Science ®Google Scholar
• Grant WP, Sullivan R, Sonenshine DE, Adam M, Slusser JH, Carson KA, Vinik AI. Electron microscopic investigation of the effects of diabetes mellitus on the achilles tendon. J Foot Ankle Surg. 1997;36(4):272–278. doi:10.1016/S1067-2516(97)80072-5.
   PubMedGoogle Scholar
• Behzad H, Sharma A, Mousavizadeh R, Lu A, Scott A. Mast cells exert pro-inflammatory effects of relevance to the pathophysiology of tendinopathy. Arthritis Res Ther. 2013;15(6):R184. doi:10.1186/ar4374.
   PubMed Web of Science ®Google Scholar
• Grewal N, Thornton GM, Behzad H, Sharma A, Lu A, Zhang P, Reid WD, Granville DJ, Scott A. Accumulation of oxidized LDL in the tendon tissues of C57BL/6 or apolipoprotein e knock-out mice that consume a high fat diet: potential impact on tendon health. Plos One. 2014;9(12):1–15. doi:10.1371/journal.pone.0114214.
   Web of Science ®Google Scholar
• Bohm S, Mersmann F, Arampatzis A. Human tendon adaptation in response to mechanical loading: a systematic review and meta-analysis of exercise intervention studies on healthy adults. Sport Med Open. 2015;1(1). doi:10.1186/s40798-015-0009-9.
   PubMedGoogle Scholar
• Mackey AL, Heinemeier KM, Koskinen SOA, Kjaer M. Dynamic adaptation of tendon and muscle connective tissue to mechanical loading. Connect Tissue Res. 2008;49(3–4):165–168. doi:10.1080/03008200802151672.
   PubMed Web of Science ®Google Scholar
• Magnusson SP, Langberg H, Kjaer M. The pathogenesis of tendinopathy: balancing the response to loading. Nat Rev Rheumatol. 2010;6(5):262–268. doi:10.1038/nrrheum.2010.43.
   PubMed Web of Science ®Google Scholar
• Cardoso TB, Pizzari T, Kinsella R, Hope D, Cook JL. Current trends in tendinopathy management. Best Pract Res Clin Rheumatol. 2019;33(1):122–140. doi:10.1016/j.berh.2019.02.001.
   PubMed Web of Science ®Google Scholar
• Scott A, Backman LJ, Speed C. Tendinopathy: update on pathophysiology. J Orthop Sport Phys. 2015;45(11):833–841. doi:10.2519/jospt.2015.5884.
   PubMed Web of Science ®Google Scholar
• Merry K, Napier C, Waugh CM, Scott A. Foundational principles and adaptation of the healthy and pathological achilles tendon in response to resistance exercise: a narrative review and clinical implications. J Clin Med. 2022;11(16):4722. doi:10.3390/jcm11164722.
   PubMed Web of Science ®Google Scholar
• Clegg PD, Strassburg S, Smith RK. Cell phenotypic variation in normal and damaged tendons. Int J Exp Pathol. 2007;88(4):227–235. doi:10.1111/j.1365-2613.2007.00549.x.
   PubMed Web of Science ®Google Scholar
• Wang JH, Goldschmidt-Clermont P, Wille J, Yin FC. Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J Biomech. 2001;34(12):1563–1572. doi:10.1016/S0021-9290(01)00150-6.
   PubMed Web of Science ®Google Scholar
• Thorpe CT, Godinho MSC, Riley GP, Birch HL, Clegg PD, Screen HRC. The interfascicular matrix enables fascicle sliding and recovery in tendon, and behaves more elastically in energy storing tendons. J Mech Behav Biomed Mater. 2015;52:85–94. doi:10.1016/j.jmbbm.2015.04.009.
   PubMed Web of Science ®Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372. doi:10.1136/bmj.n71.
   Google Scholar
• NTP-OHAT. Handbook for conducting a literature-based health assessment using OHAT approach for systematic review and evidence integration. National Toxicology Program - Office Of Health Assessment And Translation. Published online 2019: 1–96. https://ntp.niehs.nih.gov/whatwestudy/assessments/noncancer/handbook/index.html.
   Google Scholar
• Rooney A. Extending a risk-of-bias approach to address in vitro studies. National Toxicology Program Office Health Assessment Translation. 2015.
   Google Scholar
• Romeo S, Zeni O, Sannino A, Lagorio S, Biffoni M, Scarfì MR. Genotoxicity of radiofrequency electromagnetic fields: protocol for a systematic review of in vitro studies. Environ Int. 2021;148:106386. doi:10.1016/j.envint.2021.106386.
   PubMed Web of Science ®Google Scholar
• Chang W, Callan KT, Dragoo JL. The behavior of tendon progenitor cells from tendinopathic tendons: implications for treatment. Tissue Eng Part A. 2020;26(1–2):38–46. doi:10.1089/ten.tea.2019.0042.
   PubMed Web of Science ®Google Scholar
• Choi WJ, Park MS, Park KH, Courneya J-P, Cho JS, Schon LC, Lee JW. Comparative analysis of gene expression in normal and degenerative human tendon cells: effects of cyclic strain. Foot Ankle Int. 2014;35(10):1045–1056. doi:10.1177/1071100714540885.
   PubMed Web of Science ®Google Scholar
• Deniz P, Guler S, Çelik E, Hosseinian P, Aydin HM. Use of cyclic strain bioreactor for the upregulation of key tenocyte gene expression on Poly(glycerol-sebacate) (PGS) sheets. Mater Sci Eng: C. 2020;106( October 2019):110293. doi:10.1016/j.msec.2019.110293.
   PubMed Web of Science ®Google Scholar
• Evans CE, Trail IA. An in vitro comparison of human flexor and extensor tendon cells. J Hand Surg Am. 2001;26(4):307–313. doi:10.1054/jhsb.2001.0593.
   Web of Science ®Google Scholar
• Fong G, Backman LJ, Hart DA, Danielson P, McCormack B, Scott A. Substance P enhances collagen remodeling and MMP-3 expression by human tenocytes. J Orthop Res. 2013;31(1):91–98. doi:10.1002/jor.22191.
   PubMed Web of Science ®Google Scholar
• Herchenhan A, Dietrich-Zagonel F, Schjerling P, Kjær M, Eliasson P. Early growth response genes increases rapidly after mechanical overloading and unloading in tendon constructs. J Orthop Res. 2020;38(1):173–181. doi:10.1002/jor.24513.
   PubMed Web of Science ®Google Scholar
• Huisman E, Lu A, McCormack RG, Scott A. Enhanced collagen type i synthesis by human tenocytes subjected to periodic in vitro mechanical stimulation. BMC Musculoskelet Disord. 2014;15(1):1–8. doi:10.1186/1471-2474-15-386.
   PubMedGoogle Scholar
• Huisman E, Lu A, Jamil S. Influence of repetitive mechanical loading on MMP2 activity in tendon fibroblasts. J Orthop Res. 2016;34(11):1991–2000. doi:10.1002/jor.23207.
   PubMed Web of Science ®Google Scholar
• Jiang C, Shao L, Wang Q, Dong Y. Repetitive mechanical stretching modulates transforming growth factor-β induced collagen synthesis and apoptosis in human patellar tendon fibroblasts. Biochem Cell Biol. 2012;90(5):667–674. doi:10.1139/o2012-024.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Liu H, Li H, Wang F, Cheng K, Zhou G, Zhang W, Ye M, Cao Y, Liu W, Zou H. A proteomic analysis of engineered tendon formation under dynamic mechanical loading in vitro. Biomaterials. 2011;32(17):4085–4095. doi:10.1016/j.biomaterials.2011.02.033.
   PubMed Web of Science ®Google Scholar
• Jones E, Jones G, Legerlotz K, Riley G. Cyclical strain modulates metalloprotease and matrix gene expression in human tenocytes via activation of TGFbeta. Biochim Biophys Acta. 2013;1833(12):2596–2607. doi:10.1016/j.bbamcr.2013.06.019.
   PubMed Web of Science ®Google Scholar
• Lohberger B, Kaltenegger H, Stuendl N, Rinner B, Leithner A, Sadoghi P. Impact of cyclic mechanical stimulation on the expression of extracellular matrix proteins in human primary rotator cuff fibroblasts. Knee Surg Sports Traumatol Arthrosc. 2016;24(12):3884–3891. doi:10.1007/s00167-015-3790-6.
   PubMed Web of Science ®Google Scholar
• Mousavizadeh R, Khosravi S, Behzad H, McCormack RG, Duronio V, Scott A, Wang JH-C. Cyclic strain alters the expression and release of angiogenic factors by human tendon cells. Plos One. 2014;9(5):e97356. doi:10.1371/journal.pone.0097356.
   PubMed Web of Science ®Google Scholar
• Popov C, Burggraf M, Kreja L, Ignatius A, Schieker M, Docheva D. 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 Mol Biol. 2015;16(1):1–11. doi:10.1186/s12867-015-0036-6.
   PubMedGoogle Scholar
• Qi J, Chi L, Bynum D, Banes AJ. Gap junctions in IL-1β-mediated cell survival response to strain. J Appl Physiol. 2011;110(5):1425–1431. doi:10.1152/japplphysiol.00477.2010.
   PubMed Web of Science ®Google Scholar
• Skutek M, Van Griensven M, Zeichen J, Brauer N, Bosch U. Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol. 2001;86(1):48–52. doi:10.1007/s004210100502.
   PubMed Web of Science ®Google Scholar
• Tsuzaki M, Bynum D, Almekinders L, Yang X, Faber J, Banes AJ. ATP modulates load-inducible IL-1β, COX 2, and MMP-3 gene expression in human tendon cells. J Cell Biochem. 2003;89(3):556–562. doi:10.1002/jcb.10534.
   PubMed Web of Science ®Google Scholar
• Udeze CP, Jones ER, Riley GP, Morrissey D, Screen HRC. An in vitro investigation into the effects of 10 hz cyclic loading on tenocyte metabolism. Scand J Med Sci Sports. 2019;29(10):1511–1520. doi:10.1111/sms.13465.
   PubMed Web of Science ®Google Scholar
• Yang G, Im HJ, Wang JHC. Repetitive mechanical stretching modulates IL-1β induced COX-2, MMP-1 expression, and PGE2 production in human patellar tendon fibroblasts. Gene. 2005;363(1–2):166–172. doi:10.1016/j.gene.2005.08.006.
   PubMedGoogle Scholar
• Yang G, Crawford RC, Wang JHC. Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J Biomech. 2004;37(10):1543–1550. doi:10.1016/j.jbiomech.2004.01.005.
   PubMed Web of Science ®Google Scholar
• Tucker RP, Henningsson P, Franklin SL, Chen D, Ventikos Y, Bomphrey RJ, Thompson MS. See-saw rocking: an in vitro model for mechanotransduction research. J R Soc Interface. 2014;11(97):20140330. doi:10.1098/rsif.2014.0330.
   PubMed Web of Science ®Google Scholar
• Kjaer M, Langberg H, Miller BF. Metabolic activity and collagen turnover in human tendon in response to physical activity. J Musculoskelet Neuronal Interact. 2005;5(1):41–52.
   PubMedGoogle Scholar
• Miller BF, Olesen JL, Hansen M, Døssing S, Crameri RM, Welling RJ, Langberg H, Flyvbjerg A, Kjaer M, Babraj JA, Smith K, Rennie MJ. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol. 2005;567(3):1021–1033. doi:10.1113/jphysiol.2005.093690.
   PubMed Web of Science ®Google Scholar
• Langberg H, Skovgaard D, Petersen LJ, Bülow J, Kjær M. Type I collagen synthesis and degradation in peritendinous tissue after exercise determined by microdialysis in humans. J. Physiol. 1999;521(1):299–306. doi:10.1111/j.1469-7793.1999.00299.x.
   PubMed Web of Science ®Google Scholar
• Banos CC, Thomas AH, Kuo CK. Collagen fibrillogenesis in tendon development: Current models and regulation of fibril assembly. Birth Defects Res C Embryo Today. 2008;84(3):228–244. doi:10.1002/bdrc.20130.
   PubMedGoogle Scholar
• Thorpe CT, Screen HRC. Tendon structure and composition. Metabolic Influence Risk Tendon Disorder 2016 3–9. doi: 10.1007/978-3-319-33943-6.
   Google Scholar
• Magnusson SP, Heinemeier KM, Kjaer M. Collagen homeostasis and metabolism, 2016: 920. doi:10.1007/978-3-319-33943-6_2.
   Google Scholar
• Léjard V, Brideau G, Blais F, Salingcarnboriboon, R., Wagner, G., Roehrl, M.H., Noda, M., Duprez, D., Houillier, P. and Rossert, J. Scleraxis and NFATc regulate the expression of the pro-α1(I) collagen gene in tendon fibroblasts. J Biol Chem. 2007;282(24):17665–17675. doi:10.1074/jbc.M610113200.
   PubMed Web of Science ®Google Scholar
• Scott A, Danielson P, Abraham T, Fong G, Sampaio AV, Underhill TM. Mechanical force modulates scleraxis expression in bioartificial tendons. J Musculoskelet Neuronal Interact. 2011;11(2):124–132.
   PubMed Web of Science ®Google Scholar
• Klein MB, Yalamanchi N, Pham H, Longaker MT, Chang J. Flexor tendon healing in vitro: effects of TGF-β on tendon cell collagen production. J Hand Surg Am. 2002;27(4):615–620. doi:10.1053/jhsu.2002.34004.
   PubMed Web of Science ®Google Scholar
• Heinemeier K, Langberg H, Olesen J, Kjaer M. Role of TGF-β1 in relation to exercise-induced type I collagen synthesis in human tendinous tissue. J Appl Physiol. 2003;95(6):2390–2397. doi:10.1152/japplphysiol.00403.2003.
   PubMed Web of Science ®Google Scholar
• Lu J, Jiang L, Chen Y, Lyu K, Zhu B, Li Y, Liu X, Liu X, Long L, Wang X, Xu H, Wang D, Li S. The functions and mechanisms of basic fibroblast growth factor in tendon repair. Front Physiol. 2022;13(June):1–11. doi:10.3389/fphys.2022.852795.
   Google Scholar
• Kjær M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev. 2004;84(2):649–698. doi:10.1152/physrev.00031.2003.
   PubMed Web of Science ®Google Scholar
• Gulotta LV, Kovacevic D, Montgomery S, Ehteshami JR, Packer JD, Rodeo SA. Stem cells genetically modified with the developmental gene MT1-MMP improve regeneration of the supraspinatus tendon-to-bone insertion site. Am J Sports Med. 2010;38(7):1429–1437. doi:10.1177/0363546510361235.
   PubMed Web of Science ®Google Scholar
• Koskinen SOA, Heinemeier KM, Olesen JL, Langberg H, Kjaer M. Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon-related connective tissue. J Appl Physiol. 1985;96(3):861–864. doi:10.1152/japplphysiol.00489.2003.
   Google Scholar
• Langberg H, Skovgaard D, Karamouzis M, Bülow J, Kjær M. Metabolism and inflammatory mediators in the peritendinous space measured by microdialysis during intermittent isometric exercise in humans. J. Physiol. 1999;515(3):919–927. doi:10.1111/j.1469-7793.1999.919ab.x.
   PubMed Web of Science ®Google Scholar
• Gross MT. Chronic tendinitis: pathomechanics of injury, factors affecting the healing response, and treatment. J Orthop Sport Phys. 1992;16(6):248–261. doi:10.2519/jospt.1992.16.6.248.
   PubMed Web of Science ®Google Scholar
• Maffulli N, Ewen SWB, Waterston SW, Reaper J, Barrass V. Tenocytes from ruptured and tendinopathic achilles tendons produce greater quantities of type III collagen than tenocytes from normal achilles tendons: an in vitro model of human tendon healing. Am J Sports Med. 2000;28(4):499–505. doi:10.1177/03635465000280040901.
   PubMed Web of Science ®Google Scholar
• Singh D, Rai VK, Agrawal D. Regulation of collagen I and collagen III in tissue injury and regeneration. Cardiol Cardiovasc Med. 2023;7(01):5–16. doi:10.26502/fccm.92920302.
   PubMedGoogle Scholar
• Ireland D, Harrall R, Curry V, Holloway G, Hackney R, Hazleman B, Riley G. Multiple changes in gene expression in chronic human achilles tendinopathy. Matrix Biol. 2001;20(3):159–169. doi:10.1016/S0945-053X(01)00128-7.
   PubMed Web of Science ®Google Scholar
• Higgins J, Thomas J, Chandler J. Cochrane handbook for systematic reviews of interventions. 2nd ed. John Wiley & Sons; 2019.
   Google Scholar
• Fleischhacker V, Klatte-Schulz F, Minkwitz S, Schmock A, Rummler M, Seliger A, Willie BM, Wildemann B. In vivo and in vitro mechanical loading of mouse achilles tendons and tenocytes—a pilot study. Int J Mol Sci. 2020;21(4):1313. doi:10.3390/ijms21041313.
   PubMed Web of Science ®Google Scholar
• Zhang J, Wang JHC. The effects of mechanical loading on tendons–an in vivo and in vitro model study. Plos One 2013;8(8):1–12. doi:10.1371/journal.pone.0071740.
   Web of Science ®Google Scholar
• Lee AH, Elliott DM. Comparative multi-scale hierarchical structure of the tail, plantaris, and achilles tendons in the rat. J Anat. 2019;234(2):252–262. doi:10.1111/joa.12913.
   PubMed Web of Science ®Google Scholar
• Hast MW, Zuskov A, Soslowsky LJ. The role of animal models in tendon research. Bone Joint Res. 2014;3(6):193–202. doi:10.1302/2046-3758.36.2000281.
   PubMed Web of Science ®Google Scholar
• Schorpp M, Mattei MG, Herr I, Gack S, Schaper J, Angel P. Structural organization and chromosomal localization of the mouse collagenase type I gene. Biochem J. 1995;308(1):211–217. doi:10.1042/bj3080211.
   PubMedGoogle Scholar
• Giai via A, Frizziero A, Oliva F. Biological properties of mesenchymal stem cells from different sources. Muscles Ligaments Tendons J. 2012;2(3):154–162.
   PubMedGoogle Scholar
• Tan Q, Lui PPY, Rui YF, Wong YM. Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering. Tissue Eng Part A. 2012;18(7–8):840–851. doi:10.1089/ten.tea.2011.0362
   PubMed Web of Science ®Google Scholar