NFAT activation by membrane potential follows a calcium pathway distinct from other activity-related transcription factors in skeletal muscle cells

American Journal of Physiology - Cell Physiology

Volumn 294, Issue 3, 2008, Pages

  Valdés, Juan Antonio ^a   Gaggero, Eduardo ^a   Hidalgo, Jorge ^a   Leal, Nancy ^a   Jaimovich, Enrique ^a   Carrasco, M Angélica ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

Calcineurin; Inositol 1,4,5 trisphosphate receptor; Nuclear factor of activated T cells transcription; Nuclear factor of activated T cells translocation; Ryanodine receptor

Indexed keywords

CALCINEURIN; CALCIUM ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATASE; RYANODINE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; EXCITATION CONTRACTION COUPLING; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; STIMULUS RESPONSE; TRANSCRIPTION REGULATION; VOLTAGE CLAMP;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANIMALS, NEWBORN; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; CELL LINE; CYCLOSPORINE; ELECTRIC STIMULATION; ENZYME INHIBITORS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MEMBRANE POTENTIALS; MICE; MUSCLE FIBERS; MUSCLE, SKELETAL; NFATC TRANSCRIPTION FACTORS; PHOSPHORYLATION; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 41549143871     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00195.2007     Document Type: Article

References (38)

1. Abbott KL, Friday BB, Thaloor D, Murphy TJ, Pavlath GK. Activation and cellular localization of the cyclosporine A-sensitive transcription factor NFAT in skeletal muscle cells. Mol Biol Cell 9: 2905-2916, 1998.
2. Araya R, Liberona J, Cárdenas J, Riveros N, Estrada M, Powell J, Carrasco MA, Jaimovich E. Dihydropyridine receptors as voltage sensors for a depolarization-evoked, IP3R-mediated, slow calcium signal in skeletal muscle cells. J Gen Physiol 121: 3-16, 2003.
3. 2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk. EMBO J 18: 522-533, 1999.
4. Cárdenas C, Müller M, Jaimovich E, Pérez F, Buchuk D, Quest AFG, Carrasco MA. Depolarization of skeletal muscle cells induces phosphorylation of cAMP response element binding protein via calcium and protein kinase Cα. J Biol Chem 279: 39122-39131, 2004.
5. Carrasco MA, Riveros N, Ríos J, Müller M, Torres F, Pineda J, Lantadilla S, Jaimovich E. Depolarization induced slow transients activates early genes in skeletal muscle cells. Am J Physiol Cell Physiol 284: C1438-C1447, 2003.
6. Chawla S, Bading H. CREB/CBP and SRE-interacting transcriptional regulators are fast on-off switches: duration of calcium transients specifies the magnitude of transcriptional responses. J Neurochem 79: 849-858, 2001.
7. 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 12: 2499-2509, 1998.
8. 2+ response amplitude and duration. Nature 386: 855-858, 1997.
9. Dolmetsch RE, Xu K, Lewis R. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936, 1998.
10. Eltit J, Hidalgo J, Liberona JL, Jaimovich E. Slow calcium signals after tetanic electrical stimulation in skeletal myotubes. Biophys J 86: 3042-3051, 2004.
11. Estrada M, Cárdenas C, Liberona JL, Carrasco MA, Mignery GA, Allen PD, Jaimovich E. Calcium transients in 1B5 myotubes lacking ryanodine receptors are related to inositol trisphosphate receptors. J Biol Chem 276: 22868-22874, 2001.
12. 2+ signaling networks in regulating gene expression by action potentials. Cell Calcium 37: 433-442, 2005.
13. Genazzani AA, Carafoli E, Guerini D. Calcineurin controls inositol 1,4,5-trisphosphate type 1 receptor expression in neurons. Proc Natl Acad Sci USA 96: 5797-5801, 1999.
14. Graef IA, Mermelstein PG, Stankunas K, Neilson JR, Deisseroth K, Tsien RW, Crabtree GR. L-type calcium channels and GSK-3 regulate the activity of NFATc4 in hippocampal neurons. Nature 401: 703-708, 1999.
15. Groth RD, Mermelstein PG. Brain-derived neurotrophic factor activation of NFAT (nuclear factor of activated T-cells)-dependent transcription: a role for the transcription factor NFATc4 in neurotrophin-mediated gene expression. J Neurosci 23: 8125-8134, 2003.
16. Hogan PG, Chen L, Nardone J, Rao A. Transcriptional regulation by calcium, calcineurin and NFAT. Genes Dev 17: 2205-2232, 2003.
17. Horsley V, Pavlath GK. NFAT: ubiquitous regulator of cell differentiation and adaptation. J Cell Biol 156: 771-774, 2002.
18. 2+ signals in cultured skeletal muscle. Am J Physiol Cell Physiol 278: C998-C1010, 2000.
19. Jiang H, Jordan T, Li J, Li H, DiMario JX. Innervation-dependent and fiber type-specific transcriptional regulation of the slow myosin heavy chain 2 promoter in avian skeletal muscle fibers. Dev Dyn 231: 292-302, 2004.
20. Jordan T, Jiang H, Li H, DiMario JX. Inhibition of ryanodine receptor 1 in fast skeletal muscle fibers induces a fast-to-slow muscle fiber type transition. J Cell Sci 117: 6175-6183, 2004.
21. Jordan T, Jiang H, Li H, DiMario JX. Regulation of skeletal muscle fiber type and slow myosin heavy chain 2 gene expression by inositol trisphosphate receptor 1. J Cell Sci 118: 2295-2302, 2005.
22. 2+ transients stimulate transcription of IL-6 gene in skeletal muscle cells. Am J Physiol Cell Physiol 290: C1428-C1436, 2006.
23. Juretic N, Urzúa U, Munroe DJ, Jaimovich E, Riveros N. Differential gene expression in skeletal muscle cells after membrane depolarization. J Cell Physiol 3: 819-830, 2007.
24. Kramer D, Fresu L, Ashby DS, Freeman TC, Genazzani AA. Calcineurin controls the expression of numerous genes in cerebellar granule cells. Mol Cell Neurosci 23: 325-330, 2003.
25. Kubis HP, Scheibe RJ, Meissner JD, Hornung G, Gros G. Fast-to-slow transformation and nuclear import/export kinetics of the transcription factor NFATc1 during electrostimulation of rabbit muscle cells in culture. J Physiol 541: 835-847. 2002.
26. 2+ transients activate calcineurin/NFATc1 and initiate fast-to-slow transformation in primary skeletal muscle culture. Am J Physiol Cell Physiol 285: C56-C63, 2003.
27. 2+ release in rat skeletal myotubes. Cell Calcium. In press.
28. Liu Y, Cseresnyés Z, Randall WR, Schneider MF. Activity-dependent nuclear translocation and intranuclear distribution of NFATc in adult skeletal muscle fibers. J Cell Biol 155: 27-39, 2001.
29. McCullagh KJ, Calabria E, Pallafacchina G, Ciciliot S, Serrano A, Argentini C, Kalhovde JM, Lomo T, Schiaffino S. NFAT is a nerve activity sensor in skeletal muscle and controls activity-dependent myosin switching. Proc Natl Acad Sci USA 29: 10590-10595, 2004.
30. Musaro A, McCullagh KJ, Naya FJ, Olson EN, Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400: 581-585, 1999.
31. 2+ signaling pathway in skeletal muscle. J Cell Sci 114: 3673-3683, 2001.
32. Rosenberg P, Hawkins A, Stiber J, Shelton JM, Hutcheson K, Bassel-Duby R, Shin DM, Yan Z, Williams RS. TRPC3 channels confer cellular memory of recent neuromuscular activity. Proc Natl Acad Sci USA 25: 9387-9392, 2004.
33. 2+-dependent calcineurin signalling pathway. Nature 400: 576-581, 1999.
34. Shen T, Liu Y, Cseresnyés Z, Hawkins A, Randall WR, Schneider MF. Activity- and calcineurin-independent nuclear shuttling of NFATc1, but not NFATc3, in adult skeletal muscle fibers. Mol Biol Cell 17: 1570-1582, 2006.
35. Stiber JA, Tabatabaei N, Hawkins AF, Hawke T, Worley PF, Williams RF, Rosenberg P. Homer modulates NFAT-dependent signaling during muscle differentiation. Dev Biol 287: 213-224, 2005.
36. 2+ signals in decoding Ca2+ oscillation. EMBO J 22: 3825-3832, 2003.
37. Tothova J, Blaauw B, Pallafacchina G, Rudolf R, Argentini C, Reggiani C, Schiaffino S. NFATc1 nucleocytoplasmic shuttling is controlled by nerve activity in skeletal muscle. J Cell Sci 119: 1604-1611, 2006.
38. 3 receptors-mediated calcium signals. Am J Physiol Cell Physiol 292: C1960-C1970, 2007.