Caveolae compartmentalise β2-adrenoceptor signals by curtailing cAMP production and maintaining phosphatase activity in the sarcoplasmic reticulum of the adult ventricular myocyte

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 2, 2012, Pages 388-400

  MacDougall, David A ^a   Agarwal, Shailesh R ^b   Stopford, Elizabeth A ^a   Chu, Hongjin ^a   Collins, Jennifer A ^a   Longster, Anna L ^a   Colyer, John ^a   Harvey, Robert D ^b   Calaghan, Sarah ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

2 adrenoceptor; Caveolae; Compartmentation; Cyclic AMP; Phosphatase

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CHOLESTEROL; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHATASE; PHOSPHOLAMBAN; SERINE;

ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CAVEOLA; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEART MUSCLE CONTRACTILITY; INOTROPISM; MUSCLE FIBER CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION;

ANIMALS; BETA-CYCLODEXTRINS; CALCIUM; CAVEOLAE; CELLS, CULTURED; CHROMONES; CYCLIC AMP; HEART VENTRICLES; MALE; MORPHOLINES; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA-2; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84855988494     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.06.014     Document Type: Article

References (75)

1. Laflamme M.A., Becker P.L. Do beta 2-adrenergic receptors modulate Ca2+ in adult rat ventricular myocytes?. Am J Physiol 1998, 274:H1308-H1314.
2. Xiao R.P., Lakatta E.G. Beta 1-adrenoceptor stimulation and beta 2-adrenoceptor stimulation differ in their effects on contraction, cytosolic Ca2+, and Ca2+ current in single rat ventricular cells. Circ Res 1993, 73:286-300.
3. Nikolaev V.O., Bunemann M., Schmitteckert E., Lohse M.J., Engelhardt S. Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching {beta}1-adrenergic but locally confined {beta}2-adrenergic receptor-mediated signaling. Circ Res 2006, 99:1084-1091.
4. Soto D., De A.V., Zhang J., Xiang Y. Dynamic protein kinase a activities induced by beta-adrenoceptors dictate signaling propagation for substrate phosphorylation and myocyte contraction. Circ Res 2009, 104:770-779.
5. Kuschel M., Zhou Y.Y., Spurgeon H.A., Bartel S., Karczewski P., Zhang S.J., et al. beta2-adrenergic cAMP signaling is uncoupled from phosphorylation of cytoplasmic proteins in canine heart. Circulation 1999, 99:2458-2465.
6. Hulme J.T., Westenbroek R.E., Scheuer T., Catterall W.A. Phosphorylation of serine 1928 in the distal C-terminal domain of cardiac CaV1.2 channels during beta1-adrenergic regulation. Proc Natl Acad Sci USA 2006, 103:16574-16579.
7. Sulakhe P.V., Vo X.T. Regulation of phospholamban and troponin-I phosphorylation in the intact rat cardiomyocytes by adrenergic and cholinergic stimuli: roles of cyclic nucleotides, calcium, protein kinases and phosphatases and depolarization. Mol Cell Biochem 1995, 149-150:103-126.
8. Marx S.O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N., et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 2000, 101:365-376.
9. Calaghan S., Kozera L., White E. Compartmentalisation of cAMP-dependent signalling by caveolae in the adult cardiac myocyte. J Mol Cell Cardiol 2008, 45:88-92.
10. Xiao R.P., Cheng H., Zhou Y.Y., Kuschel M., Lakatta E.G. Recent advances in cardiac beta(2)-adrenergic signal transduction. Circ Res 1999, 85:1092-1100.
11. Kuschel M., Zhou Y.Y., Cheng H., Zhang S.J., Chen Y., Lakatta E.G., et al. G(i) protein-mediated functional compartmentalization of cardiac beta(2)-adrenergic signaling. J Biol Chem 1999, 274:22048-22052.
12. Jo S.H., Leblais V., Wang P.H., Crow M.T., Xiao R.P. Phosphatidylinositol 3-kinase functionally compartmentalizes the concurrent G(s) signaling during beta2-adrenergic stimulation. Circ Res 2002, 91:46-53.
13. Chen-Izu Y., Xiao R.P., Izu L.T., Cheng H., Kuschel M., Spurgeon H., et al. G(i)-dependent localization of beta(2)-adrenergic receptor signaling to L-type Ca(2+) channels. Biophys J 2000, 79:2547-2556.
14. Rochais F., Abi-Gerges A., Horner K., Lefebvre F., Cooper D.M., Conti M., et al. A specific pattern of phosphodiesterases controls the cAMP signals generated by different Gs-coupled receptors in adult rat ventricular myocytes. Circ Res 2006, 98:1081-1088.
15. Razani B., Woodman S.E., Lisanti M.P. Caveolae: from cell biology to animal physiology. Pharmacol Rev 2002, 54:431-467.
16. Hansen C.G., Nichols B.J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 2010, 20:177-186.
17. Insel P.A., Head B.P., Ostrom R.S., Patel H.H., Swaney J.S., Tang C.M., et al. Caveolae and lipid rafts: G protein-coupled receptor signaling microdomains in cardiac myocytes. Ann N Y Acad Sci 2005, 1047:166-172.
18. Sargiacomo M., Scherer P.E., Tang Z., Kubler E., Song K.S., Sanders M.C., et al. Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci USA 1995, 92:9407-9411.
19. Couet J., Li S., Okamoto T., Ikezu T., Lisanti M.P. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 1997, 272:6525-6533.
20. Rybin V.O., Pak E., Alcott S., Steinberg S.F. Developmental changes in beta2-adrenergic receptor signaling in ventricular myocytes: the role of Gi proteins and caveolae microdomains. Mol Pharmacol 2003, 63:1338-1348.
21. Head B.P., Patel H.H., Roth D.M., Lai N.C., Niesman I.R., Farquhar M.G., et al. G-protein-coupled receptor signaling components localize in both sarcolemmal and intracellular caveolin-3-associated microdomains in adult cardiac myocytes. J Biol Chem 2005, 280:31036-31044.
22. Balijepalli R.C., Foell J.D., Hall D.D., Hell J.W., Kamp T.J. 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 USA 2006, 103:7500-7505.
23. Agarwal S.R., Macdougall D.A., Tyser R., Pugh S.D., Calaghan S.C., Harvey R.D. Effects of cholesterol depletion on compartmentalized cAMP responses in adult cardiac myocytes. J Mol Cell Cardiol 2011, 50:500-509.
24. Toya Y., Schwencke C., Couet J., Lisanti M.P., Ishikawa Y. Inhibition of adenylyl cyclase by caveolin peptides. Endocrinology 1998, 139:2025-2031.
25. Razani B., Rubin C.S., Lisanti M.P. Regulation of cAMP-mediated signal transduction via interaction of caveolins with the catalytic subunit of protein kinase A. J Biol Chem 1999, 274:26353-26360.
26. Li S., Okamoto T., Chun M., Sargiacomo M., Casanova J.E., Hansen S.H., et al. Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 1995, 270:15693-15701.
27. Calaghan S., White E. Caveolae modulate excitation-contraction coupling and beta2-adrenergic signalling in adult rat ventricular myocytes. Cardiovasc Res 2006, 69:816-824.
28. Calaghan S.C., White E., Colyer J. Co-ordinated changes in cAMP, phosphorylated phospholamban, Ca2+ and contraction following beta-adrenergic stimulation of rat heart. Pflugers Arch 1998, 436:948-956.
29. Warrier S., Belevych A.E., Ruse M., Eckert R.L., Zaccolo M., Pozzan T., et al. Beta-adrenergic- and muscarinic receptor-induced changes in cAMP activity in adult cardiac myocytes detected with FRET-based biosensor. Am J Physiol Cell Physiol 2005, 289:C455-C461.
30. Warrier S., Ramamurthy G., Eckert R.L., Nikolaev V.O., Lohse M.J., Harvey R.D. cAMP microdomains and L-type Ca2+ channel regulation in guinea-pig ventricular myocytes. J Physiol 2007, 580:765-776.
31. Kozera L., White E., Calaghan S. Caveolae act as membrane reserves which limit mechanosensitive I(Cl, swell) channel activation during swelling in the rat ventricular myocyte. PLoS One 2009, 4:e8312.
32. Jackson W.A., Colyer J. Translation of Ser16 and Thr17 phosphorylation of phospholamban into Ca 2+-pump stimulation. Biochem J 1996, 316(Pt. 1):201-207.
33. MacKenzie S.J., Houslay M.D. Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-response-element-binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem J 2000, 347:571-578.
34. Lynch M.J., Baillie G.S., Mohamed A., Li X., Maisonneuve C., Klussmann E., et al. RNA silencing identifies PDE4D5 as the functionally relevant cAMP phosphodiesterase interacting with beta arrestin to control the protein kinase A/AKAP79-mediated switching of the beta2-adrenergic receptor to activation of ERK in HEK293B2 cells. J Biol Chem 2005, 280:33178-33189.
35. Rybin V.O., Xu X., Lisanti M.P., Steinberg S.F. Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. A mechanism to functionally regulate the cAMP signaling pathway. J Biol Chem 2000, 275:41447-41457.
36. Xiang Y., Rybin V.O., Steinberg S.F., Kobilka B. Caveolar localization dictates physiologic signaling of beta 2-adrenoceptors in neonatal cardiac myocytes. J Biol Chem 2002, 277:34280-34286.
37. Ostrom R.S., Gregorian C., Drenan R.M., Xiang Y., Regan J.W., Insel P.A. Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem 2001, 276:42063-42069.
38. Baker J.G. The selectivity of beta-adrenoceptor agonists at human beta1-, beta2- and beta3-adrenoceptors. Br J Pharmacol 2010, 160:1048-1061.
39. Nichols C.B., Rossow C.F., Navedo M.F., Westenbroek R.E., Catterall W.A., Santana L.F., et al. Sympathetic stimulation of adult cardiomyocytes requires association of AKAP5 with a subpopulation of L-type calcium channels. Circ Res 2010, 107:747-756.
40. Mauban J.R., O'Donnell M., Warrier S., Manni S., Bond M. AKAP-scaffolding proteins and regulation of cardiac physiology. Physiology (Bethesda) 2009, 24:78-87.
41. Iancu R.V., Ramamurthy G., Warrier S., Nikolaev V.O., Lohse M.J., Jones S.W., et al. Cytoplasmic cAMP concentrations in intact cardiac myocytes. Am J Physiol Cell Physiol 2008, 295:C414-C422.
42. Kranias E.G. Regulation of Ca2+ transport by cyclic 3',5'-AMP-dependent and calcium-calmodulin-dependent phosphorylation of cardiac sarcoplasmic reticulum. Biochim Biophys Acta 1985, 844:193-199.
43. Rodriguez P., Bhogal M.S., Colyer J. Stoichiometric phosphorylation of cardiac ryanodine receptor on serine 2809 by calmodulin-dependent kinase II and protein kinase A. J Biol Chem 2003, 278:38593-38600.
44. Xiao B., Jiang M.T., Zhao M., Yang D., Sutherland C., Lai F.A., et al. Characterization of a novel PKA phosphorylation site, serine-2030, reveals no PKA hyperphosphorylation of the cardiac ryanodine receptor in canine heart failure. Circ Res 2005, 96:847-855.
45. Zhang R., Zhao J., Potter J.D. Phosphorylation of both serine residues in cardiac troponin I is required to decrease the Ca2+ affinity of cardiac troponin C. J Biol Chem 1995, 270:30773-30780.
46. Carter S., Colyer J., Sitsapesan R. Maximum phosphorylation of the cardiac ryanodine receptor at serine-2809 by protein kinase a produces unique modifications to channel gating and conductance not observed at lower levels of phosphorylation. Circ Res 2006, 98:1506-1513.
47. Feron O., Dessy C., Opel D.J., Arstall M.A., Kelly R.A., Michel T. Modulation of the endothelial nitric-oxide synthase-caveolin interaction in cardiac myocytes. Implications for the autonomic regulation of heart rate. J Biol Chem 1998, 273:30249-30254.
48. Patel H.H., Hamuro L.L., Chun B.J., Kawaraguchi Y., Quick A., Rebolledo B., et al. Disruption of protein kinase A localization using a trans-activator of transcription (TAT)-conjugated A-kinase anchoring peptide reduces cardiac function. J Biol Chem 2010, 285:27632-27640.
49. Kerfant B.G., Zhao D., Lorenzen-Schmidt I., Wilson L.S., Cai S., Chen S.R., et al. PI3Kgamma is required for PDE4, not PDE3, activity in subcellular microdomains containing the sarcoplasmic reticular calcium ATPase in cardiomyocytes. Circ Res 2007, 101:400-408.
50. Fischmeister R., Castro L.R., Abi-Gerges A., Rochais F., Jurevicius J., Leroy J., et al. Compartmentation of cyclic nucleotide signaling in the heart: the role of cyclic nucleotide phosphodiesterases. Circ Res 2006, 99:816-828.
51. Berger K., Lindh R., Wierup N., Zmuda-Trzebiatowska E., Lindqvist A., Manganiello V.C., et al. Phosphodiesterase 3B is localized in caveolae and smooth ER in mouse hepatocytes and is important in the regulation of glucose and lipid metabolism. PLoS One 2009, 4:e4671.
52. Daaka Y., Luttrell L.M., Lefkowitz R.J. Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 1997, 390:88-91.
53. Xiao R.P., Avdonin P., Zhou Y.Y., Cheng H., Akhter S.A., Eschenhagen T., et al. Coupling of beta2-adrenoceptor to Gi proteins and its physiological relevance in murine cardiac myocytes. Circ Res 1999, 84:43-52.
54. Claing A., Laporte S.A., Caron M.G., Lefkowitz R.J. Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and beta-arrestin proteins. Prog Neurobiol 2002, 66:61-79.
55. Zamah A.M., Delahunty M., Luttrell L.M., Lefkowitz R.J. Protein kinase A-mediated phosphorylation of the beta 2-adrenergic receptor regulates its coupling to Gs and Gi. Demonstration in a reconstituted system. J Biol Chem 2002, 277:31249-31256.
56. Seibold A., Williams B., Huang Z.F., Friedman J., Moore R.H., Knoll B.J., et al. Localization of the sites mediating desensitization of the beta(2)-adrenergic receptor by the GRK pathway. Mol Pharmacol 2000, 58:1162-1173.
57. Wang Y., De A.V., Gao X., Ramani B., Jung Y.S., Xiang Y. Norepinephrine- and epinephrine-induced distinct beta2-adrenoceptor signaling is dictated by GRK2 phosphorylation in cardiomyocytes. J Biol Chem 2008, 283:1799-1807.
58. Baillie G.S., Sood A., McPhee I., Gall I., Perry S.J., Lefkowitz R.J., et al. beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci USA 2003, 100:940-945.
59. Perry S.J., Baillie G.S., Kohout T.A., McPhee I., Magiera M.M., Ang K.L., et al. Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science 2002, 298:834-836.
60. Heubach J.F., Graf E.M., Molenaar P., Jager A., Schroder F., Herzig S., et al. Murine ventricular L-type Ca(2+) current is enhanced by zinterol via beta(1)-adrenoceptors, and is reduced in TG4 mice overexpressing the human beta(2)-adrenoceptor. Br J Pharmacol 2001, 133:73-82.
61. Ostrom R.S., Insel P.A. The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 2004, 143:235-245.
62. Woo A.Y., Wang T.B., Zeng X., Zhu W., Abernethy D.R., Wainer I.W., et al. Stereochemistry of an agonist determines coupling preference of beta2-adrenoceptor to different G proteins in cardiomyocytes. Mol Pharmacol 2009, 75:158-165.
63. Needham D., Nunn R.S. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys J 1990, 58:997-1009.
64. Violin J.D., DiPilato L.M., Yildirim N., Elston T.C., Zhang J., Lefkowitz R.J. beta2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J Biol Chem 2008, 283:2949-2961.
65. Jones S.W., Baker D.J., Greenhaff P.L. G protein-coupled receptor kinases 2 and 5 are differentially expressed in rat skeletal muscle and remain unchanged following beta2-agonist administration. Exp Physiol 2003, 88:277-284.
66. Aoyama H., Ikeda Y., Miyazaki Y., Yoshimura K., Nishino S., Yamamoto T., et al. Isoform-specific roles of protein phosphatase 1 catalytic subunits in sarcoplasmic reticulum-mediated Ca2+ cycling. Cardiovasc Res 2010.
67. McCluskey A., Sakoff J.A. Small molecule inhibitors of serine/threonine protein phosphatases. Mini Rev Med Chem 2001, 1:43-55.
68. Gupta R.C., Neumann J., Watanabe A.M., Lesch M., Sabbah H.N. Evidence for presence and hormonal regulation of protein phosphatase inhibitor-1 in ventricular cardiomyocyte. Am J Physiol 1996, 270:H1159-H1164.
69. He J.Q., Balijepalli R.C., Haworth R.A., Kamp T.J. Crosstalk of beta-adrenergic receptor subtypes through Gi blunts beta-adrenergic stimulation of L-type Ca2+ channels in canine heart failure. Circ Res 2005, 97:566-573.
70. Chesley A., Lundberg M.S., Asai T., Xiao R.P., Ohtani S., Lakatta E.G., et al. The beta(2)-adrenergic receptor delivers an antiapoptotic signal to cardiac myocytes through G(i)-dependent coupling to phosphatidylinositol 3'-kinase. Circ Res 2000, 87:1172-1179.
71. Bristow M.R., Ginsburg R., Umans V., Fowler M., Minobe W., Rasmussen R., et al. Beta 1- and beta 2-adrenergic-receptor subpopulations in nonfailing and failing human ventricular myocardium: coupling of both receptor subtypes to muscle contraction and selective beta 1-receptor down-regulation in heart failure. Circ Res 1986, 59:297-309.
72. Xiao R.P., Zhang S.J., Chakir K., Avdonin P., Zhu W., Bond R.A., et al. Enhanced G(i) signaling selectively negates beta2-adrenergic receptor (AR)-but not beta1-AR-mediated positive inotropic effect in myocytes from failing rat hearts. Circulation 2003, 108:1633-1639.
73. Ratajczak P., Damy T., Heymes C., Oliviero P., Marotte F., Robidel E., et al. Caveolin-1 and -3 dissociations from caveolae to cytosol in the heart during aging and after myocardial infarction in rat. Cardiovasc Res 2003, 57:358-369.
74. Hare J.M., Lofthouse R.A., Juang G.J., Colman L., Ricker K.M., Kim B., et al. Contribution of caveolin protein abundance to augmented nitric oxide signaling in conscious dogs with pacing-induced heart failure. Circ Res 2000, 86:1085-1092.
75. Salikova S.P., Stadnikov A.A., Semagin A.P. Morphological aspects of heart remodeling in chronic heart failure. Morfologiia 2002, 122:60-62.