CaMKII content affects contractile, but not mitochondrial, characteristics in regenerating skeletal muscle
Tóm tắt
The multi-meric calcium/calmodulin-dependent protein kinase II (CaMKII) is the main CaMK in skeletal muscle and its expression increases with endurance training. CaMK family members are implicated in contraction-induced regulation of calcium handling, fast myosin type IIA expression and mitochondrial biogenesis. The objective of this study was to investigate the role of an increased CaMKII content for the expression of the contractile and mitochondrial phenotype in vivo. Towards this end we attempted to co-express alpha- and beta-CaMKII isoforms in skeletal muscle and characterised the effect on the contractile and mitochondrial phenotype. Fast-twitch muscle m. gastrocnemius (GM) and slow-twitch muscle m. soleus (SOL) of the right leg of 3-month old rats were transfected via electro-transfer of injected expression plasmids for native α/β CaMKII. Effects were identified from the comparison to control-transfected muscles of the contralateral leg and non-transfected muscles. α/β CaMKII content in muscle fibres was 4-5-fold increased 7 days after transfection. The transfection rate was more pronounced in SOL than GM muscle (i.e. 12.6 vs. 3.5%). The overexpressed α/β CaMKII was functional as shown through increased threonine 287 phosphorylation of β-CaMKII after isometric exercise and down-regulated transcripts COXI, COXIV, SDHB after high-intensity exercise in situ. α/β CaMKII overexpression under normal cage activity accelerated excitation-contraction coupling and relaxation in SOL muscle in association with increased SERCA2, ANXV and fast myosin type IIA/X content but did not affect mitochondrial protein content. These effects were observed on a background of regenerating muscle fibres. Elevated CaMKII content promotes a slow-to-fast type fibre shift in regenerating muscle but is not sufficient to stimulate mitochondrial biogenesis in the absence of an endurance stimulus.
Tài liệu tham khảo
Berchtold MW, Brinkmeier H, Muntener M: Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 2000, 80: 1215-1265.
Chin ER: Role of Ca2+/calmodulin-dependent kinases in skeletal muscle plasticity. J Appl Physiol 2005, 99: 414-423. 10.1152/japplphysiol.00015.2005
Fluck M, Hoppeler H: Molecular basis of skeletal muscle plasticity–from gene to form and function. Rev Physiol Biochem Pharmacol 2003, 146: 159-216. 10.1007/s10254-002-0004-7
Darveau CA, Suarez RK, Andrews RD, Hochachka PW: Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 2002, 417: 166-170. 10.1038/417166a
Díaz-Herrera P, Torres A, Morcuende JA, García-Castellano JM, Calbet JA, Sarrat R: Effect of endurance running on cardiac and skeletal muscle in rats. Histol Histopathol 2001, 16: 29-35.
Wada M, Inashima S, Yamada T, Matsunaga S: Endurance training-induced changes in alkali light chain patterns in type IIB fibers of the rat. J Appl Physiol 2003, 4: 923-9.
Kubis HP, Haller EA, Wetzel P, Gros G: Adult fast myosin pattern and Ca2 + -induced slow myosin pattern in primary skeletal muscle culture. Proc Natl Acad Sci U S A 1997, 94: 4205-4210. 10.1073/pnas.94.8.4205
Sreter FA, Lopez JR, Alamo L, Mabuchi K, Gergely J: Changes in intracellular ionized Ca concentration associated with muscle fiber type transformation. Am J Physiol 1987, 253: C296-C300.
Wright DC, Geiger PC, Han DH, Jones TE, Holloszy JO: Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 2007, 282: 18793-18799. 10.1074/jbc.M611252200
Tavi P, Westerblad H: The role of in vivo Ca(2)(+) signals acting on Ca(2)(+)-calmodulin-dependent proteins for skeletal muscle plasticity. J Physiol 2011, 589: 5021-5031. 10.1113/jphysiol.2011.212860
Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS: A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 1998, 12: 2499-2509. 10.1101/gad.12.16.2499
Parsons SA, Millay DP, Wilkins BJ, Bueno OF, Tsika GL, Neilson JR, Liberatore CM, Yutzey KE, Crabtree GR, Tsika RW, Molkentin JD: Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy. J Biol Chem 2004, 279: 26192-26200. 10.1074/jbc.M313800200
Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lomo T, Schiaffino S: Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc Natl Acad Sci U S A 2001, 98: 13108-13113. 10.1073/pnas.231148598
Garcia-Roves PM, Huss J, Holloszy JO: Role of calcineurin in exercise-induced mitochondrial biogenesis. Am J Physiol Endocrinol Metabol 2006, 290: E1172-E1179. 10.1152/ajpendo.00633.2005
Jiang LQ, Garcia-Roves PM, De Castro BT, Zierath JR: Constitutively active calcineurin in skeletal muscle increases endurance performance and mitochondrial respiratory capacity. Am J Physiol Endocrinol Metabol 2010, 298: E8-E16. 10.1152/ajpendo.00403.2009
Long YC, Glund S, Garcia-Roves PM, ZIERATH JR: Calcineurin regulates skeletal muscle metabolism via coordinated changes in gene expression. J Biol Chem 2007, 282: 1607-1614. 10.1074/jbc.M609208200
Ojuka EO, Jones TE, Han DH, Chen M, Holloszy JO: Raising Ca2+ in L6 myotubes mimics effects of exercise on mitochondrial biogenesis in muscle. FASEB J 2003, 17: 675-681. 10.1096/fj.02-0951com
Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS: Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 2002, 296: 349-352. 10.1126/science.1071163
Allen DL, Leinwand LA: Intracellular calcium and myosin isoform transitions. Calcineurin and calcium-calmodulin kinase pathways regulate preferential activation of the IIa myosin heavy chain promoter. J Biol Chem 2002, 277: 45323-45330. 10.1074/jbc.M208302200
Mu X, Brown LD, Liu Y, Schneider MF: Roles of the calcineurin and CaMK signaling pathways in fast-to-slow fiber type transformation of cultured adult mouse skeletal muscle fibers. Physiol Genomics 2007, 30: 300-312. 10.1152/physiolgenomics.00286.2006
Hawkins C, Xu A, Narayanan N: Sarcoplasmic reticulum calcium pump in cardiac and slow twitch skeletal muscle but not fast twitch skeletal muscle undergoes phosphorylation by endogenous and exogenous Ca2+/calmodulin-dependent protein kinase. Characterization of optimal conditions for calcium pump phosphorylation. J Biol Chem 1994, 269: 31198-31206.
Tavi P, Allen DG, Niemela P, Vuolteenaho O, Weckstrom M, Westerblad H: Calmodulin kinase modulates Ca2+ release in mouse skeletal muscle. J Physiol 2003, 551: 5-12. 10.1113/jphysiol.2003.042002
Akimoto T, Ribar TJ, Williams RS, Yan Z: Skeletal muscle adaptation in response to voluntary running in Ca2+/calmodulin-dependent protein kinase IV-deficient mice. Am J Physiol Cell Physiol 2004, 287: C1311-C1319. 10.1152/ajpcell.00248.2004
Witczak CA, Jessen N, Warro DM, Toyoda T, Fujii N, Anderson ME, Hirshman MF, Goodyear LJ: CaMKII regulates contraction- but not insulin-induced glucose uptake in mouse skeletal muscle. Am J Physiol Endocrinol Metabol 2010, 298: E1150-E1160. 10.1152/ajpendo.00659.2009
Anderson ME, Brown JH, Bers DM: CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol 2011, 51: 468-473. 10.1016/j.yjmcc.2011.01.012
De Koninck P, Schulman H: Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 1998, 279: 227-230. 10.1126/science.279.5348.227
Rose AJ, Alsted TJ, Kobbero JB, Richter EA: Regulation and function of Ca2 + -calmodulin-dependent protein kinase II of fast-twitch rat skeletal muscle. J Physiol 2007, 580: 993-1005. 10.1113/jphysiol.2006.127464
Rose AJ, Kiens B, Richter EA: Ca2 + -calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise. J Physiol 2006, 574: 889-903. 10.1113/jphysiol.2006.111757
Eilers W, Gevers W, Van Overbeek D, De Haan A, Jaspers RT, Hilbers PA, Van Riel N, Fluck M: Muscle-Type Specific Autophosphorylation of CaMKII Isoforms after Paced Contractions. BioMed Res Internat 2014, 943806. doi:10.1155/2014/943806. Epub 2014 Jun 26.
Jain SS, Paglialunga S, Vigna C, Ludzki A, Herbst EA, Lally JS, Schrauwen P, Hoeks J, Tupling AR, Bonen A, Holloway GP: High-fat diet-induced mitochondrial biogenesis is regulated by mitochondrial derived reactive oxygen species activation of CaMKII. Diabetes 2014,63(6):1907-1913. 10.2337/db13-0816
Benziane B, Burton TJ, Scanlan B, Galuska D, Canny BJ, Chibalin AV, Zierath JR, Stepto NK: Divergent cell signaling after short-term intensified endurance training in human skeletal muscle. Am J Physiol Endocrinol Metab 2008, 295: E1427-E1438. 10.1152/ajpendo.90428.2008
Rose AJ, Frosig C, Kiens B, Wojtaszewski JF, Richter EA: Effect of endurance exercise training on Ca2+ calmodulin-dependent protein kinase II expression and signalling in skeletal muscle of humans. J Physiol 2007, 583: 785-795. 10.1113/jphysiol.2007.138529
Baylor SM, Hollingworth S: Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 2003, 551: 125-138. 10.1113/jphysiol.2003.041608
Hennig R, Lomo T: Firing patterns of motor units in normal rats. Nature 1985, 314: 164-166. 10.1038/314164a0
Gaertner TR, Kolodziej SJ, Wang D, Kobayashi R, Koomen JM, Stoops JK, Waxham MN: Comparative analyses of the three-dimensional structures and enzymatic properties of alpha, beta, gamma and delta isoforms of Ca2 + -calmodulin-dependent protein kinase II. J Biol Chem 2004, 279: 12484-12494. 10.1074/jbc.M313597200
Woodgett JR, Cohen P, Yamauchi T, Fujisawa H: Comparison of calmodulin-dependent glycogen synthase kinase from skeletal muscle and calmodulin-dependent protein kinase-II from brain. FEBS Lett 1984, 170: 49-54. 10.1016/0014-5793(84)81366-6
Gorassini M, Eken T, Bennett DJ, Kiehn O, Hultborn H: Activity of hindlimb motor units during locomotion in the conscious rat. J Neurophysiol 2000, 83: 2002-2011.
Durieux AC, Bonnefoy R, Manissolle C, Freyssenet D: High-efficiency gene electrotransfer into skeletal muscle: description and physiological applicability of a new pulse generator. Biochem Biophys Res Commun 2002, 296: 443-450. 10.1016/S0006-291X(02)00901-4
Durieux AC, D'antona G, Desplanches D, Freyssenet D, Klossner S, Bottinelli R, Fluck M: Focal adhesion kinase is a load-dependent governor of the slow contractile and oxidative muscle phenotype. J Physiol 2009, 587: 3703-3717. 10.1113/jphysiol.2009.171355
Rizzuto G, Cappelletti M, Maione D, Savino R, Lazzaro D, Costa P, Mathiesen I, Cortese R, Ciliberto G, Laufer R, La Monica N, Fattori E: Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proc Natl Acad Sci U S A 1999, 96: 6417-6422. 10.1073/pnas.96.11.6417
Bayer K, Harbers K, Schulman H: alphaKAP is an anchoring protein for a novel CaM kinase II isoform in skeletal muscle. EMBO J 1998, 17: 5598-5605. 10.1093/emboj/17.19.5598
Duguez S, Feasson L, Denis C, Freyssenet D: Mitochondrial biogenesis during skeletal muscle regeneration. Am J Physiol Endocrinol Metabol 2002, 282: E802-E809.
Shu B, Shen Y, Wang AM, Fang XQ, Li X, Deng HY, Yu ZQ: Histological, enzymohistochemical and biomechanical observation of skeletal muscle injury in rabbits. Chin J Traumatol 2007, 10: 150-153.
Esposito A, Germinario E, Zanin M, Palade PT, Betto R, Danieli-Betto D: Isoform switching in myofibrillar and excitation-contraction coupling proteins contributes to diminished contractile function in regenerating rat soleus muscle. J Appl Physiol 2007, 102: 1640-1648. 10.1152/japplphysiol.01397.2006
Fluck M, Schmutz S, Wittwer M, Hoppeler H, Desplanches D: Transcriptional reprogramming during reloading of atrophied rat soleus muscle. Am J Physiology Regul Integ Comp Physiol 2005, 289: R4-R14. 10.1152/ajpregu.00833.2004
Wang J, Best PM: Inactivation of the sarcoplasmic reticulum calcium channel by protein kinase. Nature 1992, 359: 739-741. 10.1038/359739a0
Dulhunty AF, Laver D, Curtis SM, Pace S, Haarmann C, Gallant EM: Characteristics of irreversible ATP activation suggest that native skeletal ryanodine receptors can be phosphorylated via an endogenous CaMKII. Biophysical J 2001, 81: 3240-3252. 10.1016/S0006-3495(01)75959-0
Xu A, Narayanan N: Ca2+/calmodulin-dependent phosphorylation of the Ca2 + -ATPase, uncoupled from phospholamban, stimulates Ca2 + -pumping in native cardiac sarcoplasmic reticulum. Biochem Biophys Res Commun 1999, 258: 66-72. 10.1006/bbrc.1999.0579
Arcuri C, Giambanco I, Bianchi R, Donato R: Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience 2002, 109: 371-388. 10.1016/S0306-4522(01)00330-X
Zador E, Mendler L, Ver Heyen M, Dux L, Wuytack F: Changes in mRNA levels of the sarcoplasmic/endoplasmic-reticulum Ca(2+)-ATPase isoforms in the rat soleus muscle regenerating from notexin-induced necrosis. Biochem J 1996,320(Pt 1):107-113.
Ramirez MT, Zhao XL, Schulman H, Brown JH: The nuclear deltaB isoform of Ca2+/calmodulin-dependent protein kinase II regulates atrial natriuretic factor gene expression in ventricular myocytes. J Biol Chem 1997, 272: 31203-31208. 10.1074/jbc.272.49.31203
Ronkainen JJ, Hanninen SL, Korhonen T, Koivumaki JT, Skoumal R, Rautio S, Ronkainen VP, Tavi P: Ca2 + -calmodulin-dependent protein kinase II represses cardiac transcription of the L-type calcium channel alpha(1C)-subunit gene (Cacna1c) by DREAM translocation. J Physiol 2011, 589: 2669-2686. 10.1113/jphysiol.2010.201400
Srinivasan M, Edman CF, Schulman H: Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus. J Cell Biol 1994, 126: 839-852. 10.1083/jcb.126.4.839
Sun P, Enslen H, Myung PS, Maurer RA: Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev 1994, 8: 2527-2539. 10.1101/gad.8.21.2527
Sun P, Lou L, Maurer RA: Regulation of activating transcription factor-1 and the cAMP response element-binding protein by Ca2+/calmodulin-dependent protein kinases type I, II, and IV. J Biol Chem 1996, 271: 3066-3073. 10.1074/jbc.271.6.3066
Murgia M, Elbenhardt Jensen T, Cusinato M, Garcia M, Richter EA, Schiaffino S: Multiple signalling pathways redundantly control GLUT4 gene transcription in skeletal muscle. J Physiol 2009,587(Pt 17):4319-4327. 10.1113/jphysiol.2009.174888
Klossner S, Dapp C, Schmutz S, Vogt M, Hoppeler H, Fluck M: Muscle transcriptome adaptations with mild eccentric ergometer exercise. Pflugers Arch 2007, 455: 555-562. 10.1007/s00424-007-0303-6
Schmutz S, Dapp C, Wittwer M, Vogt M, Hoppeler H, Fluck M: Endurance training modulates the muscular transcriptome response to acute exercise. Pflugers Arch 2006, 451: 678-687. 10.1007/s00424-005-1497-0
Marsh DR, Carson JA, Stewart LN, Booth FW: Activation of the skeletal alpha-actin promoter during muscle regeneration. J Muscle Res Cell Motil 1998, 19: 897-907. 10.1023/A:1005485400448
Haan A, Huijing PA, Vliet MR: Rat medial gastrocnemius muscles produce maximal power at a length lower than the isometric optimum length. Pflugers Archiv Europ J Physiol 2003, 445: 728-733.
De Haan A, De Ruiter CJ, Lind A, Sargeant AJ: Age-related changes in force and efficiency in rat skeletal muscle. Acta Physiol Scand 1993, 147: 347-355. 10.1111/j.1748-1716.1993.tb09511.x
Fluck M, Waxham MN, Hamilton MT, Booth FW: Skeletal muscle Ca(2+)-independent kinase activity increases during either hypertrophy or running. J Appl Physiol 2000, 88: 352-358.
Desplanches D, Amami M, Dupré-Aucouturier S, Valdivieso P, Schmutz S, Mueller M, Hoppeler H, Kreis R, Flück M: Hypoxia refines plasticity of mitochondrial respiration to repeated muscle work. Eur J Appl Physiol 2014,114(2):405-417. 10.1007/s00421-013-2783-8
Van Wessel T, De Haan A, van der Laarse WJ, Jaspers RT: The muscle fiber type-fiber size paradox: hypertrophy or oxidative metabolism? Eur J Appl Physiol 2010, 110: 665-694. 10.1007/s00421-010-1545-0
