Cyclic mechanical stretch regulates the AMPK/Egr1 pathway in tenocytes via Ca2+-mediated mechanosensing

References

• Wang JH. 2006. Mechanobiology of tendon. J Biomech. 39(9):1563–1582.
   PubMed Web of Science ®Google Scholar
• Lavagnino M, Wall ME, Little D, Banes AJ, Guilak F, Arnoczky SP. 2015. Tendon mechanobiology: current knowledge and future research opportunities. J Orthop Res. 33(6):813–822.
   PubMed Web of Science ®Google Scholar
• Nakajima T, Ikeya M. 2020. Development of pluripotent stem cell-based human tenocytes. Dev Growth Differ.63:38–46.
   PubMed Web of Science ®Google Scholar
• Nam HY, Pingguan-Murphy B, Amir Abbas A, Mahmood Merican A, Kamarul T. 2015. The proliferation and tenogenic differentiation potential of bone marrow-derived mesenchymal stromal cell are influenced by specific uniaxial cyclic tensile loading conditions. Biomech Model Mechanobiol. 14(3):649–663.
   PubMed Web of Science ®Google Scholar
• Morita Y, Watanabe S, Ju Y, Xu B. 2013. Determination of optimal cyclic uniaxial stretches for stem cell-to-tenocyte differentiation under a wide range of mechanical stretch conditions by evaluating gene expression and protein synthesis levels. Acta Bioeng Biomech. 15(3):71–79.
   PubMed Web of Science ®Google Scholar
• Liu Y, Xu J, Xu L, Wu T, Sun Y, Lee YW, Wang B, Chan HC, Jiang X, Zhang J et al. 2017. Cystic fibrosis transmembrane conductance regulator mediates tenogenic differentiation of tendon-derived stem cells and tendon repair: accelerating tendon injury healing by intervening in its downstream signalling. FASEB J. 31(9):3800–3815.
   PubMed Web of Science ®Google Scholar
• Zhang J, Pan T, Liu Y, Wang JH. 2010. Mouse treadmill running enhances tendons by expanding the pool of tendon stem cells (TSCs) and TSC-related cellular production of collagen. J Orthop Res. 28(9):1178–1183.
   PubMed Web of Science ®Google Scholar
• Wang T, Thien C, Wang C, Ni M, Gao J, Wang A, Jiang Q, Tuan RS, Zheng Q, Zheng MH. 2018. 3D uniaxial mechanical stimulation induces tenogenic differentiation of tendon-derived stem cells through a PI3K/AKT signalling pathway. FASEB J. 32(9):4804–4814.
   PubMed Web of Science ®Google Scholar
• Burner T, Gohr C, Mitton-Fitzgerald E, Rosenthal AK. 2012. Hyperglycemia reduces proteoglycan levels in tendons. Connect Tissue Res. 53(6):535–541.
   PubMed Web of Science ®Google Scholar
• Tsai WC, Liang FC, Cheng JW, Lin LP, Chang SC, Chen HH, and Pang JH. 2013. High glucose concentration up-regulates the expression of matrix metalloproteinase-9 and −13 in tendon cells. BMC Musculoskelet Disord. 14:255.
   PubMed Web of Science ®Google Scholar
• Wu YF, Wang HK, Chang HW, Sun J, Sun JS, and Chao YH. 2017. High glucose alters tendon homeostasis through downregulation of the AMPK/Egr1 pathway. Sci Rep. 7:44199.
   PubMed Web of Science ®Google Scholar
• Berridge MJ. 2001. The versatility and complexity of calcium signalling. Novartis Found Symp. 239(52–64): discussion 64-57. 150–159.
   Google Scholar
• Chin D, Means AR. 2000. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10(8):322–328.
   PubMed Web of Science ®Google Scholar
• Hook SS, Means AR. 2001. Ca(2+)/CaM-dependent kinases: from activation to function. Annu Rev Pharmacol Toxicol. 41:471–505.
   PubMed Web of Science ®Google Scholar
• Soderling TR. 1999. The Ca2+–calmodulin-dependent protein kinase cascade. Trends Biochem Sci. 24(6):232–236.
   PubMed Web of Science ®Google Scholar
• Anderson KA, Means RL, Huang QH, Kemp BE, Goldstein EG, Selbert MA, Edelman AM, Fremeau RT, Means AR. 1998. Components of a calmodulin-dependent protein kinase cascade. Molecular cloning, functional characterization and cellular localization of Ca2+/calmodulin-dependent protein kinase kinase beta. J Biol Chem. 273(48):31880–31889.
   PubMed Web of Science ®Google Scholar
• Vinet J, Carra S, Blom JM, Harvey M, Brunello N, Barden N, Tascedda F. 2003. Cloning of mouse Ca2+/calmodulin-dependent protein kinase kinase beta (CaMKKbeta) and characterization of CaMKKbeta and CaMKKalpha distribution in the adult mouse brain. Brain Res Mol Brain Res. 111(1–2):216–221.
   PubMedGoogle Scholar
• Green MF, Anderson KA, Means AR. 2011. Characterization of the CaMKKbeta-AMPK signalling complex. Cell Signal. 23(12):2005–2012.
   PubMed Web of Science ®Google Scholar
• Nakanishi A, Hatano N, Fujiwara Y, Bin Shari A, Takabatake S, Akano H, Kanayama N, Magari M, Nozaki N, Tokumitsu H. AMP-activated protein kinase-mediated feedback phosphorylation controls the Ca2+/calmodulin (CaM) dependence of Ca2+/CaM-dependent protein kinase kinase beta. J Biol Chem. 2017. doi:10.1074/jbc.M117.805085.
   Web of Science ®Google Scholar
• Anderson KA, Ribar TJ, Lin F, Noeldner PK, Green MF, Muehlbauer MJ, Witters LA, Kemp BE, Means AR. 2008. Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metab. 7(5):377–388.
   PubMed Web of Science ®Google Scholar
• Lejard V, Blais F, Guerquin MJ, Bonnet A, Bonnin MA, Havis E, Malbouyres M, Bidaud CB, Maro G, Gilardi-Hebenstreit P et al. 2011. Egr1 and egr2 involvement in vertebrate tendon differentiation. J Biol Chem. 286(7):5855–5867.
   PubMed Web of Science ®Google Scholar
• Guerquin MJ, Charvet B, Nourissat G, Havis E, Ronsin O, Bonnin MA, Ruggiu M, Olivera-Martinez I, Robert N, Lu Y et al. 2013. Transcription factor EGR1 directs tendon differentiation and promotes tendon repair. J Clin Invest. 123(8):3564–3576.
   PubMed Web of Science ®Google Scholar
• Gaut L, Robert N, Delalande A, Bonnin MA, Pichon C, Duprez D. 2016. Egr1 regulates transcription downstream of mechanical signals during tendon formation and healing. PLoS One. 11(11):e0166237.
   PubMed Web of Science ®Google Scholar
• Hammerman M, Blomgran P, Dansac A, Eliasson P, Aspenberg P. 2017. Different gene response to mechanical loading during early and late phases of rat achilles tendon healing. J Appl Physiol. 123(4):800–815.
   PubMed Web of Science ®Google Scholar
• Chiquet M, Gelman L, Lutz R, Maier S. 2009. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim Biophys Acta. 1793(5):911–920.
   PubMed Web of Science ®Google Scholar
• Havis E, Duprez D. 2020. Egr1 transcription factor is a multifaceted regulator of matrix production in tendons and other connective tissues. Int J Mol Sci. 21(5):1664.
   PubMed Web of Science ®Google Scholar
• Wang T, Chen P, Zheng M, Wang A, Lloyd D, Leys T, Zheng Q, Zheng MH. 2018. In vitro loading models for tendon mechanobiology. J Orthop Res. 36(2):566–575.
   PubMed Web of Science ®Google Scholar
• Wu YF, Huang YT, Wang HK, Yao CJ, Sun JS, and Chao YH. 2017. Hyperglycemia augments the adipogenic transdifferentiation potential of tenocytes and is alleviated by cyclic mechanical stretch. Int J Mol Sci. 19(1):90.
   PubMed Web of Science ®Google Scholar
• Lui PPY. 2017. Tendinopathy in diabetes mellitus patients-epidemiology, pathogenesis, and management. Scand J Med Sci Sports. 27(8):776–787.
   PubMed Web of Science ®Google Scholar
• Bosworth LA, Rathbone SR, Bradley RS, Cartmell SH. 2014. Dynamic loading of electrospun yarns guides mesenchymal stem cells towards a tendon lineage. J Mech Behav Biomed Mater. 39:175–183.
   PubMed Web of Science ®Google Scholar
• Sensini A, Cristofolini L, Zucchelli A, Focarete ML, Gualandi C, De M A, Kao AP, Roldo M, Blunn G, Tozzi G. 2020. Hierarchical electrospun tendon-ligament bioinspired scaffolds induce changes in fibroblasts morphology under static and dynamic conditions. J Microsc. 277(3):160–169.
   PubMed Web of Science ®Google Scholar
• Chen W, Deng Y, Zhang J, Tang K. 2015. Uniaxial repetitive mechanical overloading induces influx of extracellular calcium and cytoskeleton disruption in human tenocytes. Cell Tissue Res. 359(2):577–587.
   PubMed Web of Science ®Google Scholar
• Nam HY, Balaji Raghavendran HR, Pingguan-Murphy B, Abbas AA, Merican AM, Kamarul T. 2017. Fate of tenogenic differentiation potential of human bone marrow stromal cells by uniaxial stretching affected by stretch-activated calcium channel agonist gadolinium. PLoS One. 12(6):e0178117.
   PubMed Web of Science ®Google Scholar
• Kato T, Ishiguro N, Iwata H, Kojima T, Ito T, Naruse K. 1998. Up-regulation of COX2 expression by uni-axial cyclic stretch in human lung fibroblast cells. Biochem Biophys Res Commun. 244(3):615–619.
   PubMed Web of Science ®Google Scholar
• Inoh H, Ishiguro N, Sawazaki S, Amma H, Miyazu M, Iwata H, Sokabe M, Naruse K. 2002. Uni-axial cyclic stretch induces the activation of transcription factor nuclear factor kappab in human fibroblast cells. FASEB J. 16(3):405–407.
   PubMed Web of Science ®Google Scholar
• Tojkander S, Gateva G, Husain A, Krishnan R, Lappalainen P. 2015. Generation of contractile actomyosin bundles depends on mechanosensitive actin filament assembly and disassembly. Elife. 4:e06126.
   PubMed Web of Science ®Google Scholar
• Tojkander S, Ciuba K, Lappalainen P. 2018. CaMKK2 regulates mechanosensitive assembly of contractile actin stress fibers. Cell Rep. 24(1):11–19.
   PubMed Web of Science ®Google Scholar
• Racioppi L, Means AR. 2012. Calcium/calmodulin-dependent protein kinase kinase 2: roles in signalling and pathophysiology. J Biol Chem. 287(38):31658–31665.
   PubMed Web of Science ®Google Scholar
• Marcelo KL, Means AR, York B. 2016. The Ca(2+)/calmodulin/CaMKK2 axis: nature’s metabolic camshaft. Trends Endocrinol Metab. 27(10):706–718.
   PubMed Web of Science ®Google Scholar
• Chen YY, Lee MH, Hsu CC, Wei CL, Tsai YC. 2012. Methyl cinnamate inhibits adipocyte differentiation via activation of the CaMKK2-AMPK pathway in 3T3-L1 preadipocytes. J Agric Food Chem. 60(4):955–963.
   PubMed Web of Science ®Google Scholar
• Lin F, Ribar TJ, Means AR. 2011. The Ca2+/calmodulin-dependent protein kinase kinase, CaMKK2, inhibits preadipocyte differentiation. Endocrinology. 152(10):3668–3679.
   PubMed Web of Science ®Google Scholar
• Hamadi A, Bouali M, Dontenwill M, Stoeckel H, Takeda K, Ronde P. 2005. Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci. 118(Pt 19):4415–4425.
   PubMed Web of Science ®Google Scholar
• 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(8):1501–1509.
   PubMed Web of Science ®Google Scholar
• Vandenberghe M, Raphael M, Lehen’kyi V, Gordienko D, Hastie R, Oddos T, Rao A, Hogan PG, Skryma R, Prevarskaya N. 2013. ORAI1 calcium channel orchestrates skin homeostasis. Proc Natl Acad Sci U S A. 110(50):E4839–4848.
   PubMed Web of Science ®Google Scholar