Regulation of cAMP homeostasis by the efflux protein MRP4 in cardiac myocytes

FASEB Journal

Volumn 26, Issue 3, 2012, Pages 1009-1017

  Sassi, Yassine ^a,b   Abi Gerges, Aniella ^a   Fauconnier, Jeremy ^c   Mougenot, Nathalie ^d   Reiken, Steven ^e   Haghighi, Kobra ^f   Kranias, Evangelia G ^f   Marks, Andrew R ^e   Lacampagne, Alain ^c   Engelhardt, Stefan ^b   Hatem, Stephane N ^a   Lompre, Anne Marie ^a   Hulot, Jean Sébastien ^a,g  

^a INSERM   (France)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIV MONTPELLIER   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e New York Presbyterian Columbia University Medical Center   (United States)

^f UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^g MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cyclic nucleotides; MRP proteins; Phosphodiesterases

Indexed keywords

CYCLIC AMP; MULTIDRUG RESISTANCE PROTEIN 4; PHOSPHODIESTERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CONTROLLED STUDY; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE HYPERTROPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

1-METHYL-3-ISOBUTYLXANTHINE; ANIMALS; BLOTTING, WESTERN; CARDIOMEGALY; CELL MEMBRANE; CELLS, CULTURED; CYCLIC AMP; ECHOCARDIOGRAPHY; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HOMEOSTASIS; ISOENZYMES; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHODIESTERASE INHIBITORS; PHOSPHORIC DIESTER HYDROLASES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS;

MUS;

EID: 84857725831     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-194027     Document Type: Article

References (51)

1. Lohse, M. J., Engelhardt, S., and Eschenhagen, T. (2003) What is the role of beta-adrenergic signaling in heart failure? Circ. Res. 93, 896-906 (Pubitemid 37433227)
2. De Rooij, J., Zwartkruis, F. J., Verheijen, M. H., Cool, R. H., Nijman, S. M., Wittinghofer, A., and Bos, J. L. (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474-477 (Pubitemid 28553318)
3. Metrich, M., Berthouze, M., Morel, E., Crozatier, B., Gomez, A. M., and Lezoualc'h, F. (2010) Role of the cAMP-binding protein Epac in cardiovascular physiology and pathophysiology. Pflügers Arch. 459, 535-546
4. Metrich, M., Lucas, A., Gastineau, M., Samuel, J. L., Heymes, C., Morel, E., and Lezoualc'h, F. (2008) Epac mediates beta-adrenergic receptor-induced cardiomyocyte hypertrophy. Circ. Res. 102, 959-965 (Pubitemid 351591548)
5. Jurevicius, J., and Fischmeister, R. (1996) cAMP compartmentation is responsible for a local activation of cardiac Ca2+channels by beta-adrenergic agonists. Proc. Natl. Acad. Sci. U. S. A. 93, 295-299
6. Zaccolo, M., and Pozzan, T. (2002) Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295, 1711-1715 (Pubitemid 34202906)
7. Ostrom, R. S., Gregorian, C., Drenan, R. M., Xiang, Y., Regan, J. W., and Insel, P. A. (2001) Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J. Biol. Chem. 276, 42063-42069
8. Ostrom, R. S., Gregorian, C., and Insel, P. A. (2000) Cellular release of and response to ATP as key determinants of the set-point of signal transduction pathways. J. Biol. Chem. 275, 11735-11739 (Pubitemid 30237737)
9. Wong, W., and Scott, J. D. (2004) AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell. Biol. 5, 959-970 (Pubitemid 39611533)
10. Fischmeister, R., Castro, L. R., Abi-Gerges, A., Rochais, F., Jurevicius, J., Leroy, J., and Vandecasteele, G. (2006) Compartmentation of cyclic nucleotide signaling in the heart: the role of cyclic nucleotide phosphodiesterases. Circ. Res. 99, 816-828 (Pubitemid 44556380)
11. Borst, P., de Wolf, C., and van de Wetering, K. (2007) Multidrug resistance-associated proteins 3, 4, and 5. Pflügers Arch. 453, 661-673 (Pubitemid 46192537)
12. Russel, F. G., Koenderink, J. B., and Masereeuw, R. (2008) Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol. Sci. 29, 200-207
13. Ritter, C. A., Jedlitschky, G., Meyer zu Schwabedissen, H., Grube, M., Kock, K., and Kroemer, H. K. (2005) Cellular export of drugs and signaling molecules by the ATP-binding cassette transporters MRP4 (ABCC4) and MRP5 (ABCC5). Drug Metab. Rev. 37, 253-278 (Pubitemid 40250291)
14. Guo, Y., Kotova, E., Chen, Z. S., Lee, K., Hopper-Borge, E., Belinsky, M. G., and Kruh, G. D. (2003) MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2′,3′-dideoxycytidine and 9′-(2′-phosphonylmethoxyethyl) adenine. J. Biol. Chem. 278, 29509-29514 (Pubitemid 36962331)
15. Hamet, P., Pang, S. C., and Tremblay, J. (1989) Atrial natriuretic factor-induced egression of cyclic guanosine 3′:5′-monophosphate in cultured vascular smooth muscle and endothelial cells. J. Biol. Chem. 264, 12364-12369 (Pubitemid 19191126)
16. Kapoor, A. K., Bapat, S. K., and Saxena, V. C. (1977) Actions of glucagon on the perfused vessels of the isolated rabbit ear. Indian J. Physiol. Pharmacol. 21, 133-136 (Pubitemid 8219980)
17. Boixel, C., Gonzalez, W., Louedec, L., and Hatem, S. N. (2001) Mechanisms of L-type Ca(2+) current downregulation in rat atrial myocytes during heart failure. Circ. Res. 89, 607-613 (Pubitemid 32924215)
18. Sassi, Y., Lipskaia, L., Vandecasteele, G., Nikolaev, V. O., Hatem, S. N., Cohen Aubart, F., Russel, F. G., Mougenot, N., Vrignaud, C., Lechat, P., Lompre, A. M., and Hulot, J. S. (2008) Multidrug resistance-associated protein 4 regulates cAMP-dependent signaling pathways and controls human and rat SMC proliferation. J. Clin. Invest. 118, 2747-2757
19. Hara, Y., Sassi, Y., Guibert, C., Gambaryan, N., Dorfmuller, P., Eddahibi, S., Lompre, A. M., Humbert, M., and Hulot, J. S. (2011) Inhibition of MRP4 prevents and reverses pulmonary hypertension in mice. J. Clin. Invest. 121, 2888-2897
20. Leggas, M., Adachi, M., Scheffer, G. L., Sun, D., Wielinga, P., Du, G., Mercer, K. E., Zhuang, Y., Panetta, J. C., Johnston, B., Scheper, R. J., Stewart, C. F., and Schuetz, J. D. (2004) Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol. Cell. Biol. 24, 7612-7621 (Pubitemid 39121487)
21. De Wolf, C. J., Yamaguchi, H., van der Heijden, I., Wielinga, P. R., Hundscheid, S. L., Ono, N., Scheffer, G. L., de Haas, M., Schuetz, J. D., Wijnholds, J., and Borst, P. (2007) cGMP transport by vesicles from human and mouse erythrocytes. FEBS J. 274, 439-450 (Pubitemid 46046653)
22. Nikolaev, V. O., Bunemann, M., Schmitteckert, E., Lohse, M. J., and Engelhardt, S. (2006) Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching beta1-adrenergic but locally confined beta2-adrenergic receptor-mediated signaling. Circ. Res. 99, 1084-1091 (Pubitemid 44729932)
23. Van Aubel, R. A., Smeets, P. H., Peters, J. G., Bindels, R. J., and Russel, F. G. (2002) The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J. Am. Soc. Nephrol. 13, 595-603 (Pubitemid 34183923)
24. El-Haou, S., Balse, E., Neyroud, N., Dilanian, G., Gavillet, B., Abriel, H., Coulombe, A., Jeromin, A., and Hatem, S. N. (2009) Kv4 potassium channels form a tripartite complex with the anchoring protein SAP97 and CaMKII in cardiac myocytes. Circ. Res. 104, 758-769
25. Abi-Char, J., Maguy, A., Coulombe, A., Balse, E., Ratajczak, P., Samuel, J. L., Nattel, S., and Hatem, S. N. (2007) Membrane cholesterol modulates Kv1.5 potassium channel distribution and function in rat cardiomyocytes. J. Physiol. 582, 1205-1217 (Pubitemid 47104349)
26. Henaff, M., Antoine, S., Mercadier, J. J., Coulombe, A., and Hatem, S. N. (2002) The voltage-independent B-type Ca2+channel modulates apoptosis of cardiac myocytes. FASEB J. 16, 99-101
27. Fauconnier, J., Andersson, D. C., Zhang, S. J., Lanner, J. T., Wibom, R., Katz, A., Bruton, J. D., and Westerblad, H. (2007) Effects of palmitate on Ca(2+) handling in adult control and ob/ob cardiomyocytes: impact of mitochondrial reactive oxygen species. Diabetes 56, 1136-1142 (Pubitemid 46525069)
28. Bera, T. K., Lee, S., Salvatore, G., Lee, B., and Pastan, I. (2001) MRP8, a new member of ABC transporter superfamily, identified by EST database mining and gene prediction program, is highly expressed in breast cancer. Mol. Med. 7, 509-516
29. Dazert, P., Meissner, K., Vogelgesang, S., Heydrich, B., Eckel, L., Bohm, M., Warzok, R., Kerb, R., Brinkmann, U., Schaeffeler, E., Schwab, M., Cascorbi, I., Jedlitschky, G., and Kroemer, H. K. (2003) Expression and localization of the multidrug resistance protein 5 (MRP5/ABCC5), a cellular export pump for cyclic nucleotides, in human heart. Am. J. Pathol. 163, 1567-1577 (Pubitemid 37175103)
30. Houslay, M. D., Baillie, G. S., and Maurice, D. H. (2007) cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ. Res. 100, 950-966 (Pubitemid 46598920)
31. Conti, M., and Beavo, J. (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu. Rev. Biochem. 76, 481-511
32. Omori, K., and Kotera, J. (2007) Overview of PDEs and their regulation. Circ. Res. 100, 309-327
33. Yan, C., Miller, C. L., and Abe, J. (2007) Regulation of phosphodiesterase 3 and inducible cAMP early repressor in the heart. Circ. Res. 100, 489-501 (Pubitemid 46673258)
34. Abi-Gerges, A., Richter, W., Lefebvre, F., Mateo, P., Varin, A., Heymes, C., Samuel, J. L., Lugnier, C., Conti, M., Fischmeister, R., and Vandecasteele, G. (2009) Decreased expression and activity of cAMP phosphodiesterases in cardiac hypertrophy and its impact on beta-adrenergic cAMP signals. Circ. Res. 105, 784-792
35. Takahashi, K., Osanai, T., Nakano, T., Wakui, M., and Okumura K. (2002) Enhanced activities and gene expression of phosphodiesterase types 3 and 4 in pressure-induced congestive heart failure. Heart Vessels 16, 249-256 (Pubitemid 35244105)
36. Movsesian, M. A., Smith, C. J., Krall, J., Bristow, M. R., and Manganiello, V. C. (1991) Sarcoplasmic reticulum-associated cyclic adenosine 5′-monophosphate phosphodiesterase activity in normal and failing human hearts. J. Clin. Invest. 88, 15-19
37. Rodriguez, M. R., Diez, F., Ventimiglia, M. S., Morales, V., Copsel, S., Vatta, M. S., Davio, C. A., and Bianciotti, L. G. (2011) Atrial natriuretic factor stimulates efflux of cAMP in rat exocrine pancreas via multidrug resistance-associated proteins. Gastroenterology 140, 1292-1302
38. Cazorla, O., Lucas, A., Poirier, F., Lacampagne, A., and Lezoualc'h, F. (2009) The cAMP binding protein Epac regulates cardiac myofilament function. Proc. Natl. Acad. Sci. U. S. A. 106, 14144-14149
39. Balijepalli, R. C., Foell, J. D., Hall, D. D., Hell, J. W., and Kamp, T. J. (2006) Localization of cardiac L-type Ca(2+) channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation. Proc. Natl. Acad. Sci. U. S. A. 103, 7500-7505 (Pubitemid 43727862)
40. Russel, F. G., Masereeuw, R., and van Aubel, R. A. (2002) Molecular aspects of renal anionic drug transport. Annu. Rev. Physiol. 64, 563-594 (Pubitemid 34259241)
41. Li, C., Krishnamurthy, P. C., Penmatsa, H., Marrs, K. L., Wang, X. Q., Zaccolo, M., Jalink, K., Li, M., Nelson, D. J., Schuetz, J. D., and Naren, A. P. (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131, 940-951 (Pubitemid 350138082)
42. Akanuma, S., Hosoya, K., Ito, S., Tachikawa, M., Terasaki, T., and Ohtsuki, S. (2010) Involvement of multidrug resistance-associated protein 4 in efflux transport of prostaglandin E(2) across mouse blood-brain barrier and its inhibition by intravenous administration of cephalosporins. J. Pharmacol. Exp. Ther. 333, 912-919
43. Mendez, M., and LaPointe, M. C. (2005) PGE2-induced hypertrophy of cardiac myocytes involves EP4 receptor-dependent activation of p42/44 MAPK and EGFR transactivation. Am. J. Physiol. Heart Circ. Physiol. 288, H2111-H2117 (Pubitemid 40604094)
44. Engelhardt, S., Hein, L., Wiesmann, F., and Lohse, M. J. (1999) Progressive hypertrophy and heart failure in beta1-adrenergic receptor transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 96, 7059-7064 (Pubitemid 29275009)
45. Gaudin, C., Ishikawa, Y., Wight, D. C., Mahdavi, V., Nadal-Ginard, B., Wagner, T. E., Vatner, D. E., and Homcy, C. J. (1995) Overexpression of Gs alpha protein in the hearts of transgenic mice. J. Clin. Invest. 95, 1676-1683
46. Iwase, M., Bishop, S. P., Uechi, M., Vatner, D. E., Shannon, R. P., Kudej, R. K., Wight, D. C., Wagner, T. E., Ishikawa, Y., Homcy, C. J., and Vatner, S. F. (1996) Adverse effects of chronic endogenous sympathetic drive induced by cardiac GS alpha overexpression. Circ. Res. 78, 517-524
47. Feldman, D. S., Carnes, C. A., Abraham, W. T., and Bristow, M. R. (2005) Mechanisms of disease: beta-adrenergic receptors-alterations in signal transduction and pharmacogenomics in heart failure. Nat. Clin. Pract. Cardiovasc. Med. 2, 475-483 (Pubitemid 41223525)
48. Bristow, M. R. (1998) Why does the myocardium fail? Insights from basic science. Lancet 352(Suppl. 1), SI8-SI14
49. Cohn, J. N., Goldstein, S. O., Greenberg, B. H., Lorell, B. H., Bourge, R. C., Jaski, B. E., Gottlieb, S. O., McGrew, F., 3rd, DeMets, D. L., and White, B. G. (1998) A dose-dependent increase in mortality with vesnarinone among patients with severe heart failure. Vesnarinone trial investigators. N. Engl. J. Med. 339, 1810-1816 (Pubitemid 29005785)
50. Packer, M., Carver, J. R., Rodeheffer, R. J., Ivanhoe, R. J., DiBianco, R., Zeldis, S. M., Hendrix, G. H., Bommer, W. J., Elkayam, U., Kukin, M. L., Mallis, G. I., Solano, G. A., Shannon, J., Tandon, P. K., DeMets, D. L., and the PROMISE study research group. (1991) Effect of oral milrinone on mortality in severe chronic heart failure. The PROMISE Study Research Group. N. Engl. J. Med. 325, 1468-1475
51. Copsel, S., Garcia, C., Diez, F., Vermeulem, M., Baldi, A., Bianciotti, L. G., Russel, F. G., Shayo, C., and Davio, C. (2011) Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation. J. Biol. Chem. 286, 6979-6988