ELF-MF transiently increases skeletal myoblast migration: Possible role of calpain system

References

• Allen RG, Tresini M. 2000. Oxidative stress and gene regulation. Free Radical Biology & Medicine 28:463–499.
   PubMed Web of Science ®Google Scholar
• Arnaudeau S, Holzer N, König S, Bader CR, Bernheim L. 2006. Calcium sources used by post-natal human myoblasts during initial differentiation. Journal of Cellular Physiology 208:435–445.
   PubMedGoogle Scholar
• Arthur JS, Mykles DL. 2000. Calpain zymography with casein or fluorescein isothiocyanate casein. Methods in Molecular Biology 144:109–116.
   PubMedGoogle Scholar
• Averna M, De Tullio R, Passalacqua M, Salamino F, Pontremoli S, Melloni E. 2001. Changes in intracellular calpastatin localization are mediated by reversible phosphorylation. Biochemical Journal 354:25–30.
   PubMed Web of Science ®Google Scholar
• Averna M, De Tullio R, Capini P, Salamino F, Pontremoli S, Melloni E. 2003. Changes in calpastatin localization and expression during calpain activation: A new mechanism for the regulation of intracellular Ca2+-dependent proteolysis. Cellular and Molecular Life Sciences 60:2669–2678.
   PubMedGoogle Scholar
• Averna M, Stifanese R, De Tullio R, Passalacqua M, Defranchi E, Salamino F, Melloni E, Pontremoli S. 2007. Regulation of calpain activity in rat brain with altered Ca2 + homeostasis. The Journal of Biological Chemistry 282:2656–2665.
   PubMedGoogle Scholar
• Balcerzak D, Poussard S, Brustis JJ, Elamrani N, Soriano M, Cottin P, Ducastaing A. 1995. An antisense oligodeoxyribonucleotide to m-calpain mRNA inhibits myoblast fusion. Journal of Cell Science 108:2077–2082.
   PubMedGoogle Scholar
• Balcerzak D, Cottin P, Poussard S, Cucuron A, Brustis JJ, Ducastaing A. 1998. Calpastatin-modulation of m-calpain activity is required for myoblast fusion. European Journal of Cell Biology 75:247–253.
   PubMedGoogle Scholar
• Barnoy S, Supino-Rosin L, Kosower NS. 2000. Regulation of calpain and calpastatin in differentiating myoblasts: mRNA levels, protein synthesis and stability. Biochemical Journal 351:413–420.
   PubMedGoogle Scholar
• Bersani F, Marinelli F, Ognibene A, Matteucci A, Cecchi S, Santi S, Squarzoni S, Maraldi NM. 1997. Intramembrane protein distribution in cell cultures is affected by 50 Hz pulsed magnetic fields. Bioelectromagnetics 18:463–469.
   PubMed Web of Science ®Google Scholar
• Bhatt A, Kaverina I, Otey C, Huttenlocher A. 2002. Regulation of focal complex composition and disassembly by tha calcium dependent protease calpain. Journal of Cell Science 115:3415–3425.
   PubMed Web of Science ®Google Scholar
• Blank M, Goodman R. 2004a. Comment: A biological guide for electromagnetic safety: The stress response. Bioelectromagnetics 25:642–646.
   PubMed Web of Science ®Google Scholar
• Blank M, Goodman R. 2004b. Initial interactions in electromagnetic field-induced biosynthesis. Journal of Cellular Physiology 199: 359–363.
   PubMed Web of Science ®Google Scholar
• Blank M, Goodman R. 2008. A mechanism for stimulation of biosynthesis by electromagnetic fields: Charge transfer in DNA and base pair separation. Journal of Cellular Physiology 214:20–26.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–254.
   PubMed Web of Science ®Google Scholar
• Calle Y, Carragher NO, Thrasher AJ, Jones GE. 2006. Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. Journal of Cell Science 119:2375–2385.
   PubMedGoogle Scholar
• Dargelos E, Brulé C, Combaret L, Hadj-Sassi A, Dulong S, Poussard S, Cottin P. 2007. Involvement of the calcium-dependent proteolytic system in skeletal muscle aging. Experimental Gerontology 42:1088–1098.
   PubMedGoogle Scholar
• Dargelos E, Brulé C, Stuelsatz P, Mouly V, Veschambre P, Cottin P, Poussard S. 2010. Up-regulation of calcium-dependent proteolysis in human myoblasts under acute oxidative stress. Experimental Cell Research 316:115–125.
   PubMedGoogle Scholar
• De Mattei M, Varani K, Masieri FF, Pellati A, Ongaro A, Fini M, Cadossi R, Vincenzi F, Borea PA, Caruso A. 2009. Adenosine analogs and electromagnetic fields inhibit prostaglandin E2 release in bovine synovial fibroblasts. Osteoarthritis Cartilage 17:252–262.
   PubMed Web of Science ®Google Scholar
• De Tullio RD, Passalacqua M, Averna M, Salamino F, Melloni E, Pontremoli S. 1999. Changes in intracellular localization of calpastatin during calpain activation. Biochemical Journal 343:467–472.
   PubMedGoogle Scholar
• Dedieu S, Mazères G, Cottin P, Brustis J-J. 2002. Involvement of myogenic factors during fusion in cell line C2C12. The International Journal of Developmental Biology 46:235–241.
   PubMed Web of Science ®Google Scholar
• Dedieu S, Dourdin N, Dargelos E, Poussard S, Veschambre P, Cottin P, Brustis JJ. 2003a. Calpain and myogenesis: Development of a convenient cell culture model. Biology of the Cell 94:65–76.
   Google Scholar
• Dedieu S, Mazères G, Dourdin N, Cottin P, Brustis J-J. 2003b. Transactivation of capn2 by myogenic regulatory factors during myogenesis. Journal of Molecular Biology 326:453–465.
   PubMedGoogle Scholar
• Dedieu S, Mazères G, Poussard S, Brustis JJ, Cottin P. 2003c. Myoblast migration is prevented by a calpain-dependent accumulation of MARCKS. Biology of the Cell 95:615–623.
   PubMedGoogle Scholar
• Dedieu S, Poussard S, Mazères G, Grise F, Dargelos E, Cottin P, Ducastain A. 2004. Myoblast migration is regulated by calpain through its involvement in cell attachment and cytoskeletal organisation. Experimental Cell Research 292:187–200.
   PubMed Web of Science ®Google Scholar
• Delle Monache S, Alessandro R, Iorio R, Gualtieri G, Colonna R. 2008. Extremely low frequency electromagnetic fields (ELF-EMFs) induce in vitro angiogenesis process in human endothelial cells. Bioelectromagnetics 29:640–648.
   PubMed Web of Science ®Google Scholar
• Di Loreto S, Falone S, Caracciolo V, Sebastiani P, D’Alessandro A, Mirabilio A, Zimmitti V, Amicarelli F. 2009. Fifty hertz extremely low-frequency magnetic field exposure elicits redox and trophic response in rat-cortical neurons. Journal of Cellular Physiology 219:334–343.
   PubMed Web of Science ®Google Scholar
• Disatnik MH, Boutet SC, Pacio W, Chan AY, Ross LB, Lee CH, Rando TA. 2004. The bi-directional translocation of MARCKS between membrane and cytosol regulates integrin-mediated muscle cell spreading. Journal of Cell Science 117:4469–4479.
   PubMedGoogle Scholar
• Dourdin N, Bhatt AK, Dutt P, Greer PA, Arthur JS, Elce JS, Huttenlocher A. 2001. Reduced cell migration and disruption of the actin cytoskeleton in calpain-deficient embryonic fibroblasts. Journal of Biological Chemistry 276:48382–4838.
   PubMed Web of Science ®Google Scholar
• Dulong S, Goudenege S, Vuillier-Devillers K, Manenti S, Poussard S, Cottin P. 2004. Myristoylated alanine-rich C kinase substrate (MARCKS) is involved in myoblast fusion through its regulation by protein kinase Calpha and calpain proteolytic cleavage. Biochemical Journal 382:1015–1023.
   PubMed Web of Science ®Google Scholar
• Emori Y, Saigo K. 1994. Calpain localization changes in coordination with actin-related cytoskeletal changes during early embryonic development of Drosophila. Journal of Biological Chemistry 269: 25137–25142.
   PubMedGoogle Scholar
• Formigli L, Meacci E, Sassoli C, Chellini F, Giannini R, Quercioli F, Tiribilli B, Squecco R, Bruni P, Francini F, Zecchi-Orlandini S. 2005. Sphingosine 1-phosphate induces cytoskeletal reorganization in C2C12 myoblasts: Physiological relevance for stress fibres in the modulation of ion current through stretch-activated channels. Journal of Cell Science 118:1161–1171.
   PubMed Web of Science ®Google Scholar
• Formigli L, Meacci E, Sassoli C, Squecco R, Nosi D, Chellini F, Naro F, Francini F, Zecchi-Orlandini S. 2007. Cytoskeleton/stretch-activated ion channel interaction regulates myogenic differentiation of skeletal myoblasts. Journal of Cellular Physiology 211:296–306.
   PubMed Web of Science ®Google Scholar
• Formigli L, Sassoli C, Squecco R, Bini F, Martinesi M, Chellini F, Luciani G, Sbrana F, Zecchi-Orlandini S, Francini F, Meacci E. 2009. Regulation of transient receptor potential canonical channel 1 (TRPC1) by sphingosine 1-phosphate in C2C12 myoblasts and its relevance for a role of mechanotransduction in skeletal muscle differentiation. Journal of Cell Science 122:1322–1333.
   PubMed Web of Science ®Google Scholar
• Franco S, Perrin B, Huttenlocher A. 2004. Isoform specific function of calpain 2 in regulating membrane protusion. Experimental Cell Research 299:179–187.
   PubMed Web of Science ®Google Scholar
• Gartzke J, Lange K. 2002. Cellular target of weak magnetic fields: Ionic conduction along actin filaments of microvilli. American Journal of Physiology – Cell Physiology 283(5):C1333–1346.
   Google Scholar
• Glading A, Chang P, Lauffenburger DA, Wells A. 2000. Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. The Journal of Biological Chemistry 275:2390–2398.
   PubMed Web of Science ®Google Scholar
• Glading A, Lauffenburger DA, Wells A. 2002. Cutting to the chase: Calpain proteases in cell motility. Trends in Cell Biology 12:46–54.
   PubMed Web of Science ®Google Scholar
• Glading A, Bodnar RJ, Reynolds IJ, Shiraha H, Satish L, Potter DA, Blair HC, Wells A. 2004. Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal- regulated kinase-mediated phosphorylation. Molecular and Cellular Biology 24:2499–2512.
   PubMed Web of Science ®Google Scholar
• Goetsch KP, Niesler CU. 2011. Optimization of the scratch assay for in vitro skeletal muscle wound healing analysis. Analytical Biochemistry 411:158–160.
   PubMedGoogle Scholar
• Goll DE, Thompson VF, Li H, Wei W, Cong J. 2003. The calpain system. Physiological Reviews 83:731–801.
   PubMed Web of Science ®Google Scholar
• Grassi C, D’Ascenzo M, Torsello A, Martinotti G, Wolf F, Cittadini A, Azzena GB. 2004. Effects of 50 Hz electromagnetic fields on voltage-gated Ca2 + channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium 35: 307–315.
   PubMed Web of Science ®Google Scholar
• Huang L, Dong L, Chen Y, Qi H, Xiao D. 2006. Effects of sinusoidal magnetic field observed on cell proliferation, ion concentration and osmolarity in two human cancer cell lines. Electromagnetic Biology and Medicine 25:113–126.
   PubMed Web of Science ®Google Scholar
• Huttenlocher A, Palecek SP, Lu Q, Zhang W, Mellgren RL, Lauffenburger DA, Ginsberg MH, Horwitz AF. 1997. Regulation of cell migration by the calcium-dependent protease calpain. The Journal of Biological Chemistry 272:32719–32722.
   PubMedGoogle Scholar
• Jia C, Zhou Z, Liu R, Chen S, Xia R. 2007. EGF receptor clustering is induced by a 0.4 mT power frequency magnetic field and blocked by the EGF receptor tyrosine kinase inhibitor PD153035. Bioelectromagnetics 28:197–207.
   PubMed Web of Science ®Google Scholar
• Ke XQ, Sun WJ, Lu DQ, Fu YT, Chiang H. 2008. 50-Hz magnetic field induces EGF-receptor clustering and activates RAS. International Journal of Radiation Biology 84:413–420.
   PubMed Web of Science ®Google Scholar
• Kefaloyianni E, Gaitanaki C, Beis I. 2006. ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-kappaB transactivation during oxidative stress in skeletal myoblasts. Cellular Signalling 18:2238–2251.
   PubMed Web of Science ®Google Scholar
• Kirschvink JL. 1992. Uniform magnetic fields and double-wrapped coil systems: Improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13:401–411.
   PubMed Web of Science ®Google Scholar
• Lambrechts A, Van Troys M, Ampe C. 2004. The actin cytoskeleton in normal and pathological cell motility. The International Journal of Biochemistry & Cell Biology 36:1890–1909.
   PubMed Web of Science ®Google Scholar
• Le Grand F, Rudnicki M. 2007. Satellite and stem cells in muscle growth and repair. Development 134:3953–3957.
   PubMedGoogle Scholar
• Leloup L, Mazères G, Daury L, Cottin P, Brustis JJ. 2006. Involvement of calpains in growth factor mediated migration. The International Journal of Biochemistry & Cell Biology 38:2049–2063.
   PubMed Web of Science ®Google Scholar
• Leloup L, Daury L, Mazères G, Cottin P, Brustis JJ. 2007. Involvement of the ERK/MAP kinase signalling pathway in milli-calpain activation and myogenic cell migration. The International Journal of Biochemistry & Cell Biology 39:1177–1189.
   PubMedGoogle Scholar
• Li H, Thompson VF, Goll DE. 2004. Effects of autolysis on properties of mu- and m-calpain. Biochimica et Biophysica Acta 3;1691(2–3): 91–103.
   Google Scholar
• Lisi A, Pozzi D, Pasquali E, Rieti S, Girasole M, Cricenti A, Generosi R, Serafino AL, Congiu-Castellano A, Ravagnan G, Giuliani L, Grimaldi S. 2000. Three dimensional (3D) analysis of the morphological changes induced by 50 Hz magnetic field exposure on human lymphoblastoid cells (Raji). Bioelectromagnetics 21:46–51.
   PubMed Web of Science ®Google Scholar
• Lisi A, Ledda M, Rosola E, Pozzi D, D’Emilia E, Giuliani L, Folletti A, Modesti A, Morris SJ, Grimaldi S. 2006. Extremely low frequency electromagnetic field exposure promotes differentiation of pituitary corticotrope-derived AtT20 D16V cells. Bioelectromagnetics 27:641–651.
   PubMed Web of Science ®Google Scholar
• Louis M, Zanou N, Van Schoor M, Gailly P. 2008. TRPC1 regulates skeletal myoblast migration and differentiation. Journal of Cell Science 121:3951–3959.
   PubMed Web of Science ®Google Scholar
• Manni V, Lisi A, Pozzi D, Rieti S, Serafino A, Giuliani L, Grimaldi S. 2002. Effects of extremely low frequency (50 Hz) magnetic field on morphological and biochemical properties of human keratinocytes. Bioelectromagnetics 23:298–305.
   PubMed Web of Science ®Google Scholar
• Massot O, Grimaldi B, Bailly JM, Kochanek M, Deschamps F, Lambrozo J, Fillion G. 2000. Magnetic field desensitizes 5-HT(1B) receptor in brain: Pharmacological and functional studies Brain Research 858:143–150.
   Google Scholar
• Mazères G, Leloup L, Daury L, Cottin P, Brustis J-J. 2006. Myoblast attachment and spreading are regulated by different patters by ubiquitous calpains. Cell Motility and the Cytoskeleton 63:193–207.
   PubMedGoogle Scholar
• Morabito C, Rovetta F, Bizzarri M, Mazzoleni G, Fanò G, Mariggiò MA. 2010. Modulation of redox status and calcium handling by extremely low frequency electromagnetic field in C2C12 cells: A real-time, single-cell approach. Free Radical Biology & Medicine 48:579–589.
   PubMed Web of Science ®Google Scholar
• Nikolova T, Czyz J, Rolletschek A, Blyszczuk P, Fuchs J, Jovtchev G, Schuderer J, Kuster N, Wobus AN. 2005. Electromagnetic fields affect transcript levels of apoptosis-related genes in embryonic stem cell-derived neural progenitor cells. FASEB Journal 19:1686–1688.
   PubMed Web of Science ®Google Scholar
• Piacentini R, Ripoli C, Mezzogori D, Azzena GB, Grassi C. 2008. Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via up-regulation of Ca(v)1-channel activity. Journal of Cellular Physiology 215:129–139.
   PubMed Web of Science ®Google Scholar
• Porter GA Jr, Makuck RF, Rivkees RA. 2002. Reduction in intracellular calcium levels inhibits myoblast differentiation. Journal of Biological Chemistry 277:28942–28947.
   PubMed Web of Science ®Google Scholar
• Potter DA, Tirnauer JS, Janssen R, Croall DE, Hughes CN, Fiacco KA, Mier JW, Maki M, Herman IM. 1998. Calpain regulates actin remodeling during cell spreading. The Journal of Cell Biology 141:647–662.
   PubMed Web of Science ®Google Scholar
• Poussard S, Dulong S, Aragon B, Jacques Brustis J, Veschambre P, Ducastaing A, Cottin P. 2001 Evidence for a MARCKS-PKCalpha complex in skeletal muscle. The International Journal of Biochemistry & Cell Biology 33:711–721.
   PubMedGoogle Scholar
• Przybylski RJ, Szigeti V, Davidheiser S, Kirby AC. 1994. Calcium regulation of skeletal myogenesis. II. Extracellular and cell surface effects. Cell Calcium 15:132–142.
   PubMedGoogle Scholar
• Raynaud F, Bonnal C, Fernandez E, Bremaud L, Cerutti M, Lebart MC, Roustan C, Ouali A, Benyamin Y. 2003. The calpain 1-α-actinin interaction. Resting complex between the calcium-dependant protease and its target in cytoskeleton. 2 European Journal of Biochemistry 70:4662–4670.
   Google Scholar
• Roumes H, Leloup L, Dargelos E, Brustis JJ, Daury L, Cottin P. 2010. Calpains: Markers of tumor aggressiveness?Experimental Cell Research 316:1587–1599.
   PubMedGoogle Scholar
• Santoro N, Lisi A, Pozzi D, Pasquali E, Serafino A, Grimaldi S. 1997. Effect of extremely low frequency (ELF) magnetic field exposure on morphological and biophysical properties of human lymphoid cell line (Raji). Biochimica et Biophysica Acta 1357:281–290.
   PubMed Web of Science ®Google Scholar
• Sbrana F, Sassoli C, Meacci E, Nosi D, Squecco R, Paternostro F, Tiribilli B, Zecchi-Orlandini S, Francini F, Formigli L. 2008. Role for stress fiber contraction in surface tension development and stretch-activated channel regulation in C2C12 myoblasts. American Journal of Physiology – Cell Physiology 295:C160–172.
   PubMedGoogle Scholar
• Schwartz Z, Simon BJ, Duran MA, Barabino G, Chaudhri R, Boyan BD. 2008. Pulsed electromagnetic fields enhance BMP-2 dependent osteoblastic differentiation of human mesenchymal stem cells. Journal of Orthopaedic Research 26:1250–1255.
   PubMed Web of Science ®Google Scholar
• Shiraha H, Glading A, Chou J, Jia Z, Wells A. 2002. Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain. Molecular and Cellular Biology 22:2716–2727.
   PubMed Web of Science ®Google Scholar
• Simkó M. 2007. Cell type redox status is responsible for diverse electromagnetic field effects. Current Medicinal Chemistry 14: 1141–1152.
   PubMed Web of Science ®Google Scholar
• Tapp H, Al-Naggar IM, Yarmola EG, Harrison A, Shaw G, Edison AS, Bubb MR. 2005. MARCKS is a natively unfolded protein with an inaccessible actin-binding site: Evidence for long-range intramolecular interactions. Journal of Biological Chemistry 280: 9946–9956.
   PubMedGoogle Scholar
• Temm-Grove CJ, Wert D, Thompson VF, Allen RE, Goll DE. 1999. Microinjection of calpastatin inhibits fusion in myoblasts. Experimental Cell Research 247:293–303.
   PubMedGoogle Scholar
• Varani K, Gessi S, Merighi S, Iannotta V, Cattabriga E, Spisani S, Cadossi R, Borea PA. 2002. Effect of low frequency electromagnetic fields on A2A adenosine receptors in human neutrophils. British Journal of Pharmacology 136:57–66.
   PubMed Web of Science ®Google Scholar
• Vianale G, Reale M, Amerio P, Stefanachi M, Di Luzio S, Muraro R. 2008. Extremely low frequency electromagnetic field enhances human keratinocyte cell growth and decreases proinflammatory chemokine production. British Journal of Dermatology 158:1189–1196.
   PubMed Web of Science ®Google Scholar
• Wendt A, Thompson VF, Goll DE. 2004. Interaction of calpastatin with calpain: A review. Biological Chemistry 385:465–472.
   PubMed Web of Science ®Google Scholar
• Wolf FI, Torsello A, Tedesco B, Fasanella S, Boninsegna A, D’Ascenzo M, Grassi C, Azzena GB, Cittadini A. 2005. 50-Hz extremely low frequency electromagnetic fields enhance cell proliferation and DNA damage: Possible involvement of redox mechanism. Biochimica et Biophysica Acta 1743:120–129.
   PubMed Web of Science ®Google Scholar
• Wu H, Ren K, Zhao W, Baojian GE, Peng S. 2005. Effect of electromagnetic fields on proliferation and differentiation of cultured mouse bone marrow mesenchymal stem cells. Journal of Huazhong University of Science and Technology[Medical Science] 25:185–187.
   PubMedGoogle Scholar
• Zanou N, Iwata Y, Schakman O, Lebacq J, Wakabayashi S, Gailly P. 2009. Essential role of TRPV2 ion channel in the sensitivity of dystrophic muscle to eccentric contractions. FEBS Letters 583:3600–3604.
   PubMedGoogle Scholar
• Zhou J, Yao G, Zhang J, Chang Z. 2002. CREB DNA binding activation by a 50-Hz magnetic field in HL60 cells is dependent on extra- and intracellular Ca(2+) but not PKA, PKC, ERK, or p38 MAPK. Biochemical and Biophysical Research Communications 296:1013–1018.
   PubMed Web of Science ®Google Scholar
• Zwirska-Korczala K, Jochem J, Adamczyk-Sowa M, Sowa P, Polaniak R, Birkner E, Latocha M, Pilc K, Suchanek R. 2005. Effect of extremely low frequency of electromagnetic fields on cell proliferation, antioxidative enzyme activities and lipid peroxidation in 3T3-L1 preadipocytes – an in vitro study. Journal of Physiology and Pharmacology 6:101–108.
   Google Scholar