Novel Epac fluorescent ligand reveals distinct Epac1 vs. Epac2 distribution and function in cardiomyocytes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 13, 2015, Pages 3991-3996

  Pereira, Laëtitia ^a   Rehmann, Holger ^b   Lao, Dieu Hung ^c   Erickson, Jeffrey R ^a,d   Bossuyt, Julie ^a   Chen, Ju ^c   Bers, Donald M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Cardiomyocytes; Epac1; Epac2; Fluorescence; Localization

Indexed keywords

CYCLIC AMP; EPAC1 PROTEIN; EPAC2 PROTEIN; HISTONE DEACETYLASE 5; UNCLASSIFIED DRUG; 8-(4-CHLOROPHENYLTHIO)-2'-O-METHYLADENOSINE-3',5'-MONOPHOSPHATE ACETOXYMETHYL ESTER; BETA ADRENERGIC RECEPTOR; CALCIUM; EPAC PROTEIN, MOUSE; EPAC-1 PROTEIN, RAT; EPAC-2 PROTEIN, RAT; FLUORESCENT DYE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HDAC5 PROTEIN, MOUSE; HISTONE DEACETYLASE; LIGAND; RAPGEF3 PROTEIN, HUMAN; RAPGEF4 PROTEIN, HUMAN; RAPGEF4 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CELL LYSATE; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUORESCENCE; GENETIC TRANSCRIPTION; HEART MUSCLE CELL; HEK293 CELL LINE; IMMUNOHISTOCHEMISTRY; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SARCOLEMMA; TRANSVERSE TUBULAR SYSTEM; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CARDIOMYOPATHY; CELL NUCLEUS; CHEMISTRY; FLUORESCENCE MICROSCOPY; HUMAN; KINETICS; METABOLISM; SIGNAL TRANSDUCTION; WISTAR RAT;

MUS;

ANIMALS; CALCIUM; CARDIOMYOPATHIES; CELL NUCLEUS; CYCLIC AMP; FLUORESCENT DYES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HISTONE DEACETYLASES; HUMANS; KINETICS; LIGANDS; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MYOCYTES, CARDIAC; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84961374070     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416163112     Document Type: Article

References (42)

1. Beavo JA, Brunton LL (2002) Cyclic nucleotide research-still expanding after half a century. Nat Rev Mol Cell Biol 3(9):710-718.
2. de Rooij J, et al. (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396(6710):474-477.
3. Kawasaki H, et al. (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282(5397):2275-2279.
4. Hothi SS, et al. (2008) Epac activation, altered calcium homeostasis and ventricular arrhythmogenesis in the murine heart. Pflugers Arch 457(2):253-270.
5. MétrichM, et al. (2010) Epac activation induces histone deacetylase nuclear export via a Ras-dependent signalling pathway. Cell Signal 22(10):1459-1468.
6. Métrich M, et al. (2008) Epac mediates beta-adrenergic receptor-induced cardiomyocyte hypertrophy. Circ Res 102(8):959-965.
7. Morel E, et al. (2005) cAMP-binding protein Epac induces cardiomyocyte hypertrophy. Circ Res 97(12):1296-1304.
8. 2+ release in the heart by activation of protein kinase Cepsilon and calcium-calmodulin kinase II. J Biol Chem 284(3):1514-1522.
9. 2+ mobilization in cardiac myocytes. J Biol Chem 282(8):5488-5495.
10. 2+/ calmodulin kinase signalling pathway in rat cardiac myocytes. J Physiol 583(Pt 2):685-694.
11. Pereira L, et al. (2012) Epac enhances excitation-transcription coupling in cardiac myocytes. J Mol Cell Cardiol 52(1):283-291.
12. Ruiz-Hurtado G, et al. (2012) Sustained Epac activation induces calmodulin dependent positive inotropic effect in adult cardiomyocytes. J Mol Cell Cardiol 53(5):617-625.
13. Ulucan C, et al. (2007) Developmental changes in gene expression of Epac and its upregulation in myocardial hypertrophy. Am J Physiol Heart Circ Physiol 293(3):H1662-H1672.
14. Pereira L, et al. (2013) Epac2 mediates cardiac β1-adrenergic-dependent sarcoplasmic reticulum Ca2+ leak and arrhythmia. Circulation 127(8):913-922.
15. Gloerich M, Bos JL (2010) Epac: Defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50:355-375.
16. Niimura M, et al. (2009) Critical role of the N-terminal cyclic AMP-binding domain of Epac2 in its subcellular localization and function. J Cell Physiol 219(3):652-658.
17. Borland G, et al. (2006) Microtubule-associated protein 1B-light chain 1 enhances activation of Rap1 by exchange protein activated by cyclic AMP but not intracellular targeting. Mol Pharmacol 69(1):374-384.
18. DiPilato LM, Cheng X, Zhang J (2004) Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proc Natl Acad Sci USA 101(47):16513-16518.
19. Hochbaum D, Hong K, Barila G, Ribeiro-Neto F, Altschuler DL (2008) Epac, in synergy with cAMP-dependent protein kinase (PKA), is required for cAMP-mediated mitogenesis. J Biol Chem 283(8):4464-4468.
20. Nikolaev VO, Bünemann M, Hein L, Hannawacker A, Lohse MJ (2004) Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279(36): 37215-37218.
21. Ponsioen B, et al. (2004) Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 5(12):1176-1180.
22. Qiao J, Mei FC, Popov VL, Vergara LA, Cheng X (2002) Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP. J Biol Chem 277(29): 26581-26586.
23. Ponsioen B, et al. (2009) Direct spatial control of Epac1 by cyclic AMP. Mol Cell Biol 29(10):2521-2531.
24. Dodge-Kafka KL, et al. (2005) The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437(7058):574-578.
25. Kapiloff MS, Jackson N, Airhart N (2001) mAKAP and the ryanodine receptor are part of a multi-component signaling complex on the cardiomyocyte nuclear envelope. J Cell Sci 114(Pt 17):3167-3176.
26. Enserink JM, et al. (2002) A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat Cell Biol 4(11):901-906.
27. Rehmann H, Schwede F, Døskeland SO, Wittinghofer A, Bos JL (2003) Ligandmediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. J Biol Chem 278(40):38548-38556.
28. Christensen AE, et al. (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(37):35394-35402.
29. Moll D, et al. (2008) Biochemical characterization and cellular imaging of a novel, membrane permeable fluorescent cAMP analog. BMC Biochem 9:18.
30. de Rooij J, et al. (2000) Mechanism of regulation of the Epac family of cAMPdependent RapGEFs. J Biol Chem 275(27):20829-20836.
31. Erickson JR, Patel R, Ferguson A, Bossuyt J, Bers DM (2011) Fluorescence resonance energy transfer-based sensor Camui provides new insight into mechanisms of calcium/ calmodulin-dependent protein kinase II activation in intact cardiomyocytes. Circ Res 109(7):729-738.
32. 2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 116(3):675-682.
33. 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(1):10-20.
34. Vliem MJ, et al. (2008) 8-pCPT-2′-O-Me-cAMP-AM: An improved Epac-selective cAMP analogue. ChemBioChem 9(13):2052-2054.
35. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2(12):905-909.
36. Cheng X, Ji Z, Tsalkova T, Mei F (2008) Epac and PKA: A tale of two intracellular cAMP receptors. Acta Biochim Biophys Sin (Shanghai) 40(7):651-662.
37. Laxman S, Riechers A, Sadilek M, Schwede F, Beavo JA (2006) Hydrolysis products of cAMP analogs cause transformation of Trypanosoma brucei from slender to stumpylike forms. Proc Natl Acad Sci USA 103(50):19194-19199.
38. 2+ from the sarcoplasmic reticulum of skinned cardiac cells. Nature 281(5727):146-148.
39. Fabiato A, Fabiato F (1979) Calcium and cardiac excitation-contraction coupling. Annu Rev Physiol 41:473-484.
40. Aflaki M, et al. (2014) Exchange protein directly activated by cAMP mediates slow delayed-rectifier current remodeling by sustained β-adrenergic activation in guinea pig hearts. Circ Res 114(6):993-1003.
41. Brette F, Blandin E, Simard C, Guinamard R, Sallé L (2013) Epac activator critically regulates action potential duration by decreasing potassium current in rat adult ventricle. J Mol Cell Cardiol 57:96-105.
42. 2+)/calmodulin kinase II after beta(1)-adrenergic receptor stimulation. J Cell Biol 189(3):573-587.