Opposing HDAC4 nuclear fluxes due to phosphorylation by β-adrenergic activated protein kinase A or by activity or Epac activated CaMKII in skeletal muscle fibres

Journal of Physiology

Volumn 591, Issue 14, 2013, Pages 3605-3623

  Liu, Yewei ^a   Schneider, Martin F ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BUCLADESINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; GREEN FLUORESCENT PROTEIN; HISTONE DEACETYLASE 4; ISOPRENALINE; PROPRANOLOL; SERINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SKELETAL MUSCLE;

ADRENERGIC BETA-AGONISTS; ANIMALS; ANIMALS, OUTBRED STRAINS; BUCLADESINE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL NUCLEUS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HISTONE DEACETYLASES; ISOPROTERENOL; MICE; MUSCLE FIBERS, SKELETAL; PHOSPHORYLATION;

EID: 84880762797     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.256263     Document Type: Article

References (42)

1. Andersson DC, Betzenhauser MJ, Reiken S, Umanskaya A, Shiomi T & Marks AR (2012). Stress-induced increase in skeletal muscle force requires protein kinase A phosphorylation of the ryanodine receptor. J Physiol 590, 6381-6387.
2. Bassel-Duby R & Olson EN (2006). Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem. 75, 19-37.
3. Baviera AM, Zanon NM, Navegantes LC & Kettelhut IC (2010). Involvement of cAMP/Epac/PI3K-dependent pathway in the antiproteolytic effect of epinephrine on rat skeletal muscle. Mol Cell Endocrinol 315, 104-112.
4. Chang CW, Lee L, Yu D, Dao K, Bossuyt J & Bers DM (2013). Acute β-adrenergic activation triggers nuclear import of histone deacetylase 5 and delays Gq-induced transcriptional activation. J Biol Chem 288, 192-204.
5. Christensen AE, Selheim F, de Rooij J, Dremier S, Schwede F, Dao KK, Martinez A, Maenhaut C, Bos JL, Genieser HG & Døskeland SO (2003). cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J Biol Chem 278, 35394-35402.
6. Dao KK, Teigen K, Kopperud R, Hodneland E, Schwede F, Christensen AE, Martinez A & Doskeland SO (2006). Epac1 and cAMP-dependent protein kinase holoenzyme have similar cAMP affinity, but their cAMP domains have distinct structural features and cyclic nucleotide recognition. J Biol Chem 281, 21500-21511.
7. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A & Bos JL (1998). Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474-477.
8. Du M, Perry RL, Nowacki NB, Gordon JW, Salma J, Zhao J, Aziz A, Chan J, Siu KW, McDermott JC (2008). Protein kinase A represses skeletal myogenesis by targeting myocyte enhancer factor 2D. Mol Cell Biol 28, 2952-2970.
9. Enserink JM, Christensen AE, de Rooij J, van Triest M, Schwede F, Genieser HG, Døskeland SO, Blank JL & Bos JL (2002). A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat Cell Biol 4, 901-906.
10. Galbo H, Richter EA, Hilsted J, Holst JJ, Christensen NJ & Henriksson J (1977). Hormonal regulation during prolonged exercise. Ann N Y Acad Sci 301, 72-80.
11. Gordon JW, Pagiatakis C, Salma J, Du M, Andreucci JJ, Zhao J, Hou G, Perry RL, Dan Q, Courtman D, Bendeck MP & McDermott JC (2009). Protein kinase A-regulated assembly of a MEF2·HDAC4 repressor complex controls c-Jun expression in vascular smooth muscle cells. J Biol Chem. 284, 19027-19042.
12. Goldfarb AH, Bruno JF & Buckenmeyer PJ (1989). Intensity and duration of exercise effects on skeletal muscle cAMP, phosphorylase, and glycogen. J Appl Physiol 66, 190-194.
13. Grozinger CM & Schreiber SL (2000). Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci USA 97, 7835-7840.
14. Gupta MP, Samant SA, Smith SH & Shroff SG (2008). HDAC4 and PCAF bind to cardiac sarcomeres and play a role in regulating myofilament contractile activity. J Biol Chem 283, 10135-10146.
15. Ha CH, Kim JY, Zhao J, Wang W, Jhun BS, Wong C & Jin ZG (2010). PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc Natl Acad Sci U S A 107, 15467-15472.
16. Hardy S, Kitamura M, Harris-Stansil T, Dai Y & Phipps ML (1997). Construction of Adenovirus vectors through Cre-lox recombination. J Virol 71, 1842-1849.
17. Helmstadter KG, Erickson JR, Dao K, Bossuyt J & Bers DM (2011). β-Adrenergic activation enhances histone deacetylase 4 nuclear localization via PKA and counters CAMKII-dependent effects in adult rabbit cardiac myocytes. Biophys J 100, 80a.
18. Holz GG, Chepurny OG & Schwede F (2008). Epac-selective cAMP analogs: new tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cell Signal 20, 10-20.
19. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, Housman DE & Graybiel AM (1998). A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275-2279.
20. Kim MS, Fielitz J, McAnally J, Shelton JM, Lemon DD, McKinsey TA, Richardson JA, Bassel-Duby R & Olson EN (2008). Protein kinase D1 stimulates MEF2 activity in skeletal muscle and enhances muscle performance. Mol Cell Biol 28, 3600-3609.
21. 2+ handling by phosphorylation status in mouse fast- and slowtwitch skeletal muscle fibres. Am J Physiol 273, C1915-1924.
22. 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.
23. Liu Y, Contreras M, Shen T, Randall WR & Schneider MF (2009). α-Adrenergic signalling activates protein kinase D and causes nuclear efflux of the transcriptional repressor HDAC5 in cultured adult mouse soleus skeletal muscle fibres. J Physiol 587, 1101-1115.
24. Liu Y, Hernández-Ochoa EO, Randall WR & Schneider MF (2012). NOX2-dependent ROS is required for HDAC5 nuclear efflux and contributes to HDAC4 nuclear efflux during intense repetitive activity of fast skeletal muscle fibres. Am J Physiol Cell Physiol 303, C334-347.
25. McGee SL & Hargreaves M (2011). Histone modifications and exercise adaptations. J Appl Physiol 110, 258-263.
26. McKinsey TA, Zhang CL & Olson EN (2001). Identification of a signal-responsive nuclear export sequence in class II histone deacetylases. Mol Cell. Biol 21, 6312-6321.
27. McKinsey TA, Zhang CL, Lu J & Olson EN (2000). Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408, 106-111.
28. Métrich M, Berthouze M, Morel E, Crozatier B, Gomez AM & Lezoualc'h F (2010a). Role of the cAMP-binding protein Epac in cardiovascular physiology and pathophysiology. Pflugers Arch 459, 535-546.
29. Métrich M, Laurent AC, Breckler M, Duquesnes N, Hmitou I, Courillau D, Blondeau JP, Crozatier B, Lezoualc'h F & Morel E (2010b). Epac activation induces histone deacetylase nuclear export via a Ras-dependent signalling pathway. Cell Signal 22, 1459-1468.
30. Montminy M (1997). Transcriptional regulation by cyclic AMP. Annu Rev Biochem 66, 807-822.
31. 2+ mobilization in cardiac myocytes. J Biol Chem 282, 5488-5495.
32. 2+ release in the heart by activation of protein kinase Ce{open} and calcium-calmodulin kinase II. J Biol Chem 284, 1514-1522.
33. Paroni G, Cernotta N, Dello Russo C, Gallinari P, Pallaoro M, Foti C, Talamo F, Orsatti L, Steinkühler C & Brancolini C (2008). PP2A regulates HDAC4 nuclear import. Mol Biol Cell 19, 655-667.
34. Parra M & Verdin E (2010). Regulatory signal transduction pathways for class IIa histone deacetylases. Curr Opin Pharmacol 10, 454-460.
35. 2+/calmodulin kinase signalling pathway in rat cardiac myocytes. J Physiol 583, 685-694.
36. Pereira L, Ruiz-Hurtado G, Morel E, Laurent AC, Métrich M, Domínguez-Rodríguez A, Lauton-Santos S, Lucas A, Benitah JP, Bers DM, Lezoualc'h F & Gómez AM (2012). Epac enhances excitation-transcription coupling in cardiac myocytes. J Mol Cell Cardiol 52, 283-291.
37. 2+ leak and arrhythmia. Circulation 127, 913-922.
38. Poppe H, Rybalkin SD, Rehmann H, Hinds TR, Tang XB, Christensen AE, Schwede F, Genieser HG, Bos JL, Doskeland SO, Beavo JA & Butt E (2008). Cyclic nucleotide analogs as probes of signalling pathways. Nat Methods 5, 277-278.
39. Schachter TN, Shen T, Liu Y & Schneider MF (2012). Kinetics of nuclear-cytoplasmic translocation of Foxo1 and Foxo3A in adult skeletal muscle fibres. Am J Physiol Cell Physiol 303, C977-C990.
40. Sullivan MJ, Green HJ & Cobb FR (1990). Skeletal muscle biochemistry and histology in ambulatory patients with long-term heart failure. Circulation 81, 518-527.
41. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN & McKinsey TA (2004). Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 24, 8374-8385.
42. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR & Molkentin JD (2004). Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94, 110-118.