Protein kinase C theta (PKCθ) modulates the ClC-1 chloride channel activity and skeletal muscle phenotype: a biophysical and gene expression study in mouse models lacking the PKCθ

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 12, 2014, Pages 2215-2228

  Camerino, Giulia Maria ^a   Bouchè, Marina ^b   De Bellis, Michela ^a   Cannone, Maria ^a   Liantonio, Antonella ^a   Musaraj, Kejla ^a   Romano, Rossella ^a   Smeriglio, Piera ^b,d   Madaro, Luca ^b,c   Giustino, Arcangela ^a   De Luca, Annamaria ^a   Desaphy, Jean François ^a   Camerino, Diana Conte ^a   Pierno, Sabata ^a  

^a UNIVERSITY OF BARI   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Aging; ClC 1 chloride channel; Electrophysiology; Gene expression; Phenotype; PKC ; Skeletal muscle

Indexed keywords

CALCINEURIN; CHELERYTHRINE; CHLORIDE CHANNEL; CLC 1 CHLORIDE CHANNEL; FLUINDOSTATIN; HISTONE DEACETYLASE 5; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN RECEPTOR SUBSTRATE 1; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2D PROTEIN; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN TYPE 1; MYOSTATIN; PIRUVATE KINASE M2; PROTEIN; PROTEIN KINASE C ALPHA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C THETA; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; CHLORIDE; CLC-1 CHANNEL; ISOENZYME; PRKCQ PROTEIN, MOUSE; PROTEIN KINASE C;

AMPLITUDE OF THE ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CHLORIDE CONDUCTANCE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITABILITY; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE; GENE EXPRESSION; GENE INACTIVATION; GLUCOSE HOMEOSTASIS; LATENCY OF THE ACTION POTENTIAL; MEMBRANE CONDUCTANCE; MOUSE; MUSCLE ACTION POTENTIAL; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE TWITCH; NONHUMAN; PHENOTYPE; POTASSIUM CONDUCTANCE; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SLOW TWITCH MUSCLE; SOLEUS MUSCLE; TRIGGERING OF ONE ACTION POTENTIAL; WILD TYPE; ACTION POTENTIAL; ANIMAL; FAST MUSCLE FIBER; GENETICS; METABOLISM; PHYSIOLOGY; SLOW MUSCLE FIBER;

ACTION POTENTIALS; ANIMALS; CALCINEURIN; CHLORIDE CHANNELS; CHLORIDES; ISOENZYMES; MEF2 TRANSCRIPTION FACTORS; MICE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; PHENOTYPE; PROTEIN KINASE C;

EID: 84912021603     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1495-1     Document Type: Article

References (60)

1. Adrian RH, Bryant SH (1974) On the repetitive discharge in myotonic muscle fibres. J Physiol 240:505–515
2. Allen DL, Harrison BC, Maass A, Bell ML, Byrnes WC, Leinwand LA (2001) Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl Physiol 90(5):1900–1908
3. Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75:19–37
4. Berchtold MW, Brinkmeier H, Müntener M (2000) Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 80:1215–1265
5. Brinkmeier H, Jockusch H (1987) Activators of protein kinase C induce myotonia by lowering chloride conductance in muscle. Biochem Biophys Res Commun 148:1383–1389
6. Bryant SH, Conte-Camerino D (1991) Chloride channel regulation in the skeletal muscle of normal and myotonic goats. Pflugers Arch 417:605–610
7. Chang S, Bezprozvannaya S, Li S, Olson EN (2005) An expression screen reveals modulators of class II histone deacetylase phosphorylation. Proc Natl Acad Sci U S A 102:8120–8125
8. Conte-Camerino D, Tortorella V, Ferranini E, Bryant SH (1984) The toxic effects of clofibrate and its metabolite on mammalian skeletal muscle: an electrophysiological study. Arch Toxicol Suppl 7:482–484
9. D'Andrea M, Pisaniello A, Serra C, Senni MI, Castaldi L, Molinaro M, Bouché M (2006) Protein kinase C theta co-operates with calcineurin in the activation of slow muscle genes in cultured myogenic cells. J Cell Physiol 207:379–388
10. De Luca A, Conte Camerino D, Connold A, Vrbovà G (1990) Pharmacological block of chloride channels of developing rat skeletal muscle affects the differentiation of specific contractile properties. Pflugers Arch 416:17–21
11. De Luca A, Tricarico D, Pierno S, Conte Camerino D (1994) Aging and chloride channel regulation in rat fast-twitch muscle fibres. Pflugers Arch 427:80–85
12. Desaphy JF, Pierno S, Léoty C, George AL Jr, De Luca A, Camerino DC (2001) Skeletal muscle disuse induces fibre type-dependent enhancement of Na(+) channel expression. Brain 124:1100–1113
13. Desaphy JF, Pierno S, Liantonio A, De Luca A, Didonna MP, Frigeri A, Nicchia GP, Svelto M, Camerino C, Zallone A, Camerino DC (2005) Recovery of the soleus muscle after short- and long-term disuse induced by hindlimb unloading: effects on the electrical properties and myosin heavy chain profile. Neurobiol Dis 18:356–365
14. Elkina Y, von Haehling S, Anker SD, Springer J (2011) The role of myostatin in muscle wasting: an overview. J Cachex Sarcopenia Muscle 2:143–151
15. Fraysse B, Desaphy JF, Pierno S, De Luca A, Liantonio A, Mitolo CI, Camerino DC (2003) Decrease in resting calcium and calcium entry associated with slow-to-fast transition in unloaded rat soleus muscle. FASEB J 17:1916–1918
16. Gao Z, Cooper TA (2013) Reexpression of pyruvate kinase M2 in type 1 myofibers correlates with altered glucose metabolism in myotonic dystrophy. Proc Natl Acad Sci U S A 110:13570–13575
17. Gundersen K (2011) Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 86:564–600
18. Gupta V, Wellen KE, Mazurek S, Bamezai RN (2013) Pyruvate kinase M2: regulatory circuits and potential for therapeutic intervention. Curr Pharm Des Jun 25 [Epub ahead of print]
19. Hilgenberg L, Miles K (1995) Developmental regulation of a protein kinase C isoform localized in the neuromuscular junction. J Cell Sci 108:51–61
20. Hilgenberg L, Yearwood S, Milstein S, Miles K (1996) Neural influence on protein kinase C isoform expression in skeletal muscle. J Neurosci 16:4994–5003
21. Hsiao KM, Huang RY, Tang PH, Lin MJ (2010) Functional study of CLC-1 mutants expressed in Xenopus oocytes reveals that a C-terminal region Thr891-Ser892-Thr893 is responsible for the effects of protein kinase C activator. Cell Physiol Biochem 25:687–694
22. Jensen TE, Maarbjerg SJ, Rose AJ, Leitges M, Richter EA (2009) Knockout of the predominant conventional PKC isoform, PKCα, in mouse skeletal muscle does not affect contraction-stimulated glucose uptake. Am J Physiol Endocrinol Metab 297:E340–E348
23. 1101. J Biol Chem 279:45304–45307
24. 2+-release system. J Pharmacol Exp Ther 321:626–634
25. Lossin C, George AL Jr (2008) Myotonia congenita. Adv Genet 63:25–55
26. Lueck JD, Mankodi A, Swanson MS, Thornton CA, Dirksen RT (2007) Muscle chloride channel dysfunction in two mouse models of myotonic dystrophy. J Gen Physiol 129:79–94
27. Madaro L, Antonangeli F, Favia A, Esposito B, Biamonte F, Bouché M, Sica G, Ziparo E, Filippini A, D’Alessio A (2013) Knock down of caveolin-1 affects morphological and functional hallmarks of human endothelial cells. J Cell Biochem 114:1843–1851
28. Madaro L, Marrocco V, Carnio S, Sandri M, Bouché M (2013) Intracellular signaling in ER stress-induced autophagy in skeletal muscle cells. FASEB J 27(5):1990–2000
29. Madaro L, Marrocco V, Fiore P, Aulino P, Smeriglio P, Adamo S, Molinaro M, Bouché M (2011) PKCθ signaling is required for myoblast fusion by regulating the expression of caveolin-3 and β1D integrin upstream focal adhesion kinase. Mol Biol Cell 22:1409–1419
30. Madaro L, Pelle A, Nicoletti C, Crupi A, Marrocco V, Bossi G, Soddu S, Bouché M (2012) PKC theta ablation improves healing in a mouse model of muscular dystrophy. PLoS ONE 7(2):e31515
31. McCullagh KJ, Calabria E, Pallafacchina G, Ciciliot S, Serrano AL, Argentini C, Kalhovde JM, Lømo T, Schiaffino S (2004) NFAT is a nerve activity sensor in skeletal muscle and controls activity-dependent myosin switching. Proc Natl Acad Sci U S A 101:10590–10595
32. McGee SL (2007) Exercise and MEF2-HDAC interactions. Appl Physiol Nutr Metab 32:852–856
33. Meller N, Altman A, Isakov N (1998) New perspectives on PKCtheta, a member of the novel subfamily of protein kinase C. Stem Cells 16:178–192
34. Messina G, Biressi S, Monteverde S, Magli A, Cassano M, Perani L, Roncaglia E, Tagliafico E, Starnes L, Campbell CE, Grossi M, Goldhamer DJ, Gronostajski RM, Cossu G (2010) Nfix regulates fetal-specific transcription in developing skeletal muscle. Cell 140:554–566
35. Osada S, Mizuno K, Saido TC, Suzuki K, Kuroki T, Ohno S (1992) A new member of the protein kinase C family, nPKC theta, predominantly expressed in skeletal muscle. Mol Cell Biol 12:3930–3938
36. Pedersen TH, de Paoli F, Nielsen OB (2005) Increased excitability of acidified skeletal muscle: role of chloride conductance. J Gen Physiol 125:237–246
37. Pedersen TH, Macdonald WA, de Paoli FV, Gurung IS, Nielsen OB (2009) Comparison of regulated passive membrane conductance in action potential-firing fast- and slow-twitch muscle. J Gen Physiol 134:323–337
38. Pierno S, De Luca A, Camerino C, Huxtable RJ, Camerino DC (1998) Chronic administration of taurine to aged rats improves the electrical and contractile properties of skeletal muscle fibers. J Pharmacol Exp Ther 286(3):1183–1190
39. Pierno S, Desaphy JF, Liantonio A, De Bellis M, Bianco G, De Luca A, Frigeri A, Nicchia GP, Svelto M, Léoty C, George AL Jr, Camerino DC (2002) Change of chloride ion channel conductance is an early event of slow-to-fast fibre type transition during unloading-induced muscle disuse. Brain 125:1510–1521
40. Pierno S, Camerino GM, Cannone M, Liantonio A, De Bellis M, Digennaro C, Gramegna G, De Luca A, Germinario E, Danieli-Betto D, Betto R, Dobrowolny G, Rizzuto E, Musarò A, Desaphy JF, Camerino DC (2013) Paracrine effects of IGF-1 overexpression on the functional decline due to skeletal muscle disuse: molecular and functional evaluation in hindlimb unloaded MLC/mIgf-1 transgenic mice. PLoS ONE 8(6):e65167
41. Pierno S, Camerino GM, Cippone V, Rolland JF, Desaphy JF, De Luca A, Liantonio A, Bianco G, Kunic JD, George AL Jr, Conte Camerino D (2009) Statins and fenofibrate affect skeletal muscle chloride conductance in rats by differently impairing ClC-1 channel regulation and expression. Br J Pharmacol 156:1206–1215
42. Pierno S, De Luca A, Beck CL, George AL Jr, Conte Camerino D (1999) Aging-associated down-regulation of ClC-1 expression in skeletal muscle: phenotypic-independent relation to the decrease of chloride conductance. FEBS Lett 449:12–16
43. Pierno S, De Luca A, Desaphy JF, Fraysse B, Liantonio A, Didonna MP, Lograno M, Cocchi D, Smith RG, Camerino DC (2003) Growth hormone secretagogues modulate the electrical and contractile properties of rat skeletal muscle through a ghrelin-specific receptor. Br J Pharmacol 139:575–584
44. Pierno S, Desaphy JF, Liantonio A, De Luca A, Zarrilli A, Mastrofrancesco L, Procino G, Valenti G, Conte Camerino D (2007) Disuse of rat muscle in vivo reduces protein kinase C activity controlling the sarcolemma chloride conductance. J Physiol 584:983–995
45. Rosenbohm A, Rüdel R, Fahlke C (1999) Regulation of the human skeletal muscle chloride channel hClC-1 by protein kinase C. J Physiol 514:677–685
46. Ryder JW, Bassel-Duby R, Olson EN, Zierath JR (2003) Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J Biol Chem 278:44298–44304
47. Schiaffino S, Serrano A (2002) Calcineurin signaling and neural control of skeletal muscle fiber type and size. Trends Pharmacol Sci 23:569–575
48. Serra C, Federici M, Buongiorno A, Senni MI, Morelli S, Segratella E, Pascuccio M, Tiveron C, Mattei E, Tatangelo L, Lauro R, Molinaro M, Giaccari A, Bouché M (2003) Transgenic mice with dominant negative PKC-theta in skeletal muscle: a new model of insulin resistance and obesity. J Cell Physiol 196:89–97
49. Sneddon WB, Liu F, Gesek FA, Friedman PA (2000) Obligate mitogen-activated protein kinase activation in parathyroid hormone stimulation of calcium transport but not calcium signaling. Endocrinology 141:4185–4193
50. Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88:1341–1378
51. Steinmeyer K, Ortland C, Jentsch TJ (1991) Primary structure and functional expression of a developmentally regulated skeletal muscle chloride channel. Nature 354:301–304
52. Stuart CA, McCurry MP, Marino A, South MA, Howell ME, Layne AS, Ramsey MW, Stone MH (2013) Slow-twitch fiber proportion in skeletal muscle correlates with insulin responsiveness. J Clin Endocrinol Metab 98:2027–2036
53. Sun Z, Arendt CW, Ellmeier W, Schaeffer EM, Sunshine MJ, Gandhi L, Annes J, Petrzilka D, Kupfer A, Schwartzberg PL, Littman DR (2000) PKC-θ is required for TCR-induced NF-κB activation in mature but not immature T lymphocytes. Nature 404:402–407
54. Tokugawa S, Sakuma K, Fujiwara H, Hirata M, Oda R, Morisaki S, Yasuhara M, Kubo T (2009) The expression pattern of PKCθ in satellite cells of normal and regenerating muscle in the rat. Neuropathology 29:211–218
55. Tricarico D, Camerino DC (2011) Recent advances in the pathogenesis and drug action in periodic paralyses and related channelopathies. Front Pharmacol 2:8. doi:10.3389/fphar.2011.00008
56. Tricarico D, Conte Camerino D, Govoni S, Bryant SH (1991) Modulation of rat skeletal muscle chloride channels by activators and inhibitors of protein kinase C. Pflugers Arch 418:500–503
57. Webb BLJ, Hirst SJ, Giembycz MA (2000) Protein kinase C isoenzymes: a review of their structure, regulation and role in regulating airways smooth muscle tone and mitogenesis. Br J Pharmacol 130:1433–1452
58. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, DiMaio JM, Olson EN, Bassel-Duby R, Williams RS (2001) Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 20:6414–6423
59. Wu H, Olson EN (2002) Activation of the MEF2 transcription factor in skeletal muscles from myotonic mice. J Clin Invest 109:1327–1333
60. Zappelli F, Willems D, Osada S, Ohno S, Wetsel WC, Molinaro M, Cossu G, Bouché M (1996) The inhibition of differentiation caused by TGFβ in fetal myoblasts is dependent upon selective expression of PKCθ: a possible molecular basis for myoblast diversification during limb histogenesis. Dev Biol 180:156–164