Regulation of the nuclear export of the transcription factor NFATc1 by protein kinases after slow fibre type electrical stimulation of adult mouse skeletal muscle fibres

Journal of Physiology

Volumn 579, Issue 2, 2007, Pages 535-551

  Shen, Tiansheng ^a   Cseresnyés, Zoltán ^a   Liu, Yewei ^a   Randall, William R ^a   Schneider, Martin F ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE I; CASEIN KINASE IDELTA; CASEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3BETA; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; UNCLASSIFIED DRUG;

ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CONTROLLED STUDY; DISSOCIATION; ENZYME INHIBITION; MOUSE; NEUROMUSCULAR ELECTRICAL STIMULATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; SLOW MUSCLE FIBER; VIRUS EXPRESSION; CELL CULTURE; ELECTROSTIMULATION; FLEXOR DIGITORUM BREVIS MUSCLE; MODEL; MUSCLE CELL; MUSCLE EXCITATION; PROTEIN NUCLEAR EXPORT; PROTEIN TRANSPORT; SIMULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CASEIN KINASE I; CASEIN KINASE II; CELL NUCLEUS; CELLS, CULTURED; ELECTRIC STIMULATION; GLYCOGEN SYNTHASE KINASE 3; GREEN FLUORESCENT PROTEINS; MICE; MICE, INBRED STRAINS; MODELS, THEORETICAL; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; NFATC TRANSCRIPTION FACTORS; TIME FACTORS;

EID: 33847671261     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.120048     Document Type: Article

References (43)

1. Arron JR, Winslow MM, Polleri A, Chang C, Wu H, Gao X et al. (2006). NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature 441, 595-600.
2. Beals CR, Clipstone NA, Ho SN & Crabtree GR (1997 a). Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev 11, 824-834.
3. Beals CR, Sheridan CM, Turck CW, Gardner P & Crabtree GR (1997 b). Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275, 1930-1934.
4. Braz JC, Bueno OF, Liang Q, Wilkins BJ, Dai YS, Parsons S et al. (2003). Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J Clin Invest 111, 1475-1486.
5. Chijiwa T, Hagiwara M & Hiroyoshi H (1989). A newly synthesized selective casein kinase I inhibitor, N-(2-aminoethyl)-5-chloroisoquinoline-8-sulfonamide and affinity purification of casein kinase I from bovine testis. J Biol Chem 264, 4924-4927.
6. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R & Williams RS (1998). A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12, 2499-2509.
7. Dong C, Yang DD, Wysk M, Ahitmarsh RJ, Davis RJ & Flavell RA (1998). Defective T cell differentiation in the absence of JNK1. Science 282, 2092-2095.
8. Geiger PC, Wright DC, Han D & Holloszy JO (2005). Activation of p38 MAP kinase enhances sensitivity of muscle glucose transport to insulin. Am J Physiol Endocrinol Metab 288, E782-E788.
9. Graef IA, Mermelstein PG, Stankunas K, Neilson JR, Deisseroth K, Tsien RW & Crabtree GR (1999). L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 401, 703-708.
10. Gross SD & Anderson RA (1998). Casein kinase I: Spatial organization and positioning of a multifunctional protein kinase family. Cell Signal 10, 699-711.
11. Gwack Y, Sharma S, Nardone J, Tanasa B, Iuga A, Srikanth S, Okamura H, Bolton D, Feske S, Hogan1 PG & Rao A (2006). A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441, 646-650.
12. Haq S, Choukroun G, Kang ZB, Ranu H, Matsui T, Rosenzweig A et al. (2000). Glycogen synthase kinase-3β is a negative regulator of cardiomyocyte hypertrophy. J Cell Biol 151, 117-129.
13. Hennig R & Lomo T (1985). Firing patterns of motor units in normal rats. Nature 314, 164-166.
14. Hoey T, Sun YL, Williamson K & Xu X (1995). Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2, 461-472.
15. Jiang H, Li H & Dimario JX (2005). Control of slow myosin heavy chain 2 gene expression by glycogen synthase kinase activity in skeletal muscle fibers. Cell Tissue Res 323, 489-494.
16. Kehlenbach RH, Dickmanns A & Gerace L (1998). Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J Cell Biol 141, 863-874.
17. Klemm JD, Beals CR & Crabtree GR (1997). Rapid targeting of nuclear proteins to the cytoplasm. Curr Biol 7, 638-644.
18. Komarova SV, Pereverzev A, Shum JW, Sims SM & Dixon SJ (2005). Covergent signaling by acidosis and receptor activator of NF-kB ligand (RANKL) on the calcium/calcineurin/NFAT pathway in osteoclasts. Proc Natl Acad Sci U S A 102, 2643-2648.
19. Kumar A, Chaudhry I, Reid MB & Boriek AM (2002). Distinct signaling pathways are activated in response to mechanical stress applied axially and transversely to skeletal muscle fibers. J Biol Chem 277, 46493-46503.
20. Liang Q, Bueno OF, Wilkins BJ, Kuan CY, Xia Y & Molkentin JD (2003). c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. EMBO J 22, 5079-5089.
21. Liu Y, Carroll SL, Klein MG & Schneider MF (1997). Calcium transients and calcium homeostasis in adult mouse fast-twitch skeletal muscle fibers in culture. Am J Physiol Cell Physiol 272, C1919-C1927.
22. Liu Y, Cseresnyés Z, Randall WR & Schneider MF (2001). Activity-dependent nuclear translocation and intranuclear distribution of NFATc in adult skeletal muscle fibers. J Cell Biol 155, 27-39.
23. Liu Y, Randall WR & Schneider MF (2005). Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle. J Cell Biol 168, 887-897.
24. Molkentin JD (2004). Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovasc Res 63, 467-475.
25. Morisco C, Seta K, Hardt SE, Lee Y, Vatner SF & Sadoshima J (2001). Glycogen synthase kinase 3β regulates GATA4 in cardiac myocytes. J Biol Chem 276, 28586-28597.
26. Neal JW & Clipstone NA (2001). Glycogen synthase kinase-3 inhibits the DNA binding activity of NFATc. J Biol Chem 276, 3666-3673.
27. Neilson J, Stankunas K & Crabtree GR (2001). Monitoring the duration of antigen-receptor occupancy by calcineurin/glycogen-synthase-kinase-3 control of NF-AT nuclear shuttling. Curr Opin Immunol 13, 346-350.
28. Okamura H, Garcia-Rodriguez C, Martinson H, Qin J, Virshup DM & Rao A (2004). A conserved docking motif of CK1 binding controls the nuclear localization of NFAT1. Mol Cell Biol 24, 4184-4195.
29. Porter CM, Havens MA & Clipstone NA (2000). Indentification of amino acid residues and protein kinases involved in the regulation of NFATc subcellular localization. J Biol Chem 275, 3543-3551.
30. Rao A, Luo C & Hogan PG (1997). Transcription factors of the NFAT family: Regulation and function. Annu Rev Immunol 15, 707-747.
31. Rena G, Bain J, Elliott M & Cohen P (2004). D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Rep 5, 60-65.
32. Salazar C & Höfer T (2003). Allosteric regulation of the transcription factor NFAT1 by multiple phosphorylation sites: A mathematical analysis. J Mol Biol 327, 31-45.
33. Scarborough JB (1966). Numerical Mathematical Analysis, 6th edn. Johns Hopkins Press, Baltimore, MD.
34. Shaw JP, Utz PJ, Durand DB, Toole JJ, Emmel EA & Crabtree GR (1988). Identification of a putative regulator of early T cell activation genes. Science 241, 202-205.
35. Shen T, Liu Y, Cseresnyés Z, Hawkins A, Randall WR & Schneider MF (2006). Activity- and calcineurin-independent nuclear shuttling of NFATc1, but not NFATc3, in adult skeletal muscle fibers. Mol Biol Cell 17, 1570-1582.
36. Sheridan CM, Heist EK, Beals CR, Crabtree GR & Gardner P (2002). Protein kinase A negatively modulates the nuclear accumulation of NF-ATc1 by priming for subsequent phosphorylation by glycogen synthase kinase-3. J Biol Chem 277, 48664-48676.
37. + signaling and gene expression. J Physiol 554, 309-320.
38. 2+ oscillation. EMBO J 22, 3825-3832.
39. Welsh GI, Miyamotoi S, Price NT, Saferi B & Proud CG (1996). T-cell activation leads to rapid stimulation of translation initiation factor eIF2B and inactivation of glycogen synthase kinase-3. J Biol Chem 271, 11410-11413.
40. Woodgett JR (1994). Regulation and functions of the glycogen synthase kinase-3 subfamily. Semin Cancer Biol 5, 269-275.
41. Zhai W, Eynott PR, Oltmanns U, Leung SY & Chung KF (2004). Mitogen-activated protein kinase signaling pathways in IL-1β-dependent rat airway smooth muscle proliferation. Br J Pharmacol 143, 1042-1049.
42. Zhu J & McKeon F (1999). NF-AT activation requires suppression of Crm1-dependent export by calcineurin. Nature 398, 256-260.
43. Zhu J, Shibasaki F, Price R, Guillemot JC, Yano T, Dötsch V, Wagner G, Ferrara P & McKeon F (1998). Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell 93, 851-861.