Cyclic nucleotide phosphodiesterase 3 signaling complexes

Hormone and Metabolic Research

Volumn 44, Issue 10, 2012, Pages 776-785

  Ahmad, F ^a   Degerman, E ^b   Manganiello, V C ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b LUND UNIVERSITY   (Sweden)

Author keywords

phosphodiesterase; protein kinase A; signalosomes

Indexed keywords

ADENYLATE CYCLASE; BETA 1 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; BREFELDIN A; CAVEOLIN 1; CHOLESTEROL; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INSULIN; JANUS KINASE 2; LEPTIN RECEPTOR; MILRINONE; MULTIPROTEIN COMPLEX; PERILIPIN; PHOSPHODIESTERASE 3A; PHOSPHODIESTERASE 3B; PHOSPHODIESTERASE III; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE IV INHIBITOR; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SMALL INTERFERING RNA; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; WORTMANNIN;

ADIPOCYTE; ADRENERGIC STIMULATION; CARDIOMYOPATHY; CAVEOLA; CELL ADHESION; CELL COMPARTMENTALIZATION; CELL CYCLE G0 PHASE; CELL FRACTIONATION; CELL METABOLISM; CELL STRAIN 3T3; CELLULAR DISTRIBUTION; ENZYME LOCALIZATION; ENZYMIC BIOSENSOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; G1 PHASE CELL CYCLE CHECKPOINT; GEL FILTRATION CHROMATOGRAPHY; HEART; HEART LEFT VENTRICLE OVERLOAD; HEART MUSCLE CELL; HOMEOSTASIS; HUMAN; HYDROLYSIS; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INSULIN RELEASE; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; LIVER CELL; NONHUMAN; OOCYTE; OOCYTE MATURATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; THROMBOCYTE ACTIVATION; VASCULAR SMOOTH MUSCLE; XENOPUS;

ADIPOCYTES; ANIMALS; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; HUMANS; INSULIN; LIGANDS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84866121851     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0032-1312646     Document Type: Review

References (101)

1. Conti M, Beavo J. Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem: 2007; 76 481 511
2. Miki T, Taira M, Hockman S, Shimada F, Lieman J, Napolitano M, Ward D, Taira M, Makino H, Manganiello V C. Characterization of the cDNA and gene encoding human PDE3B, the cGIP1 isoform of the human cyclic GMP-inhibited cyclic nucleotide phosphodiesterase family. Genomics: 1996; 36 476 485
3. Lobbert R W, Winterpacht A, Seipel B, Zabel B U. Molecular cloning and chromosomal assignment of the human homologue of the rat cGMP-inhibited phosphodiesterase 1 (PDE3A) - a gene involved in fat metabolism located at 11p 15.1. Genomics: 1996; 37 211 218
4. Kasuya J, Goko H, Fujita-Yamaguchi Y. Multiple transcripts for the human cardiac form of the cGMP-inhibited cAMP phosphodiesterase. J Biol Chem: 1995; 270 14305 14312
5. Hambleton R, Krall J, Tikishvili E, Honeggar M, Ahmad F, Manganiello V C, Movsesian M A. Isoforms of cyclic nucleotide phosphodiesterase PDE3 and their contribution to cAMP hydrolytic activity in subcellular fractions of human myocardium. J Biol Chem: 2005; 280 39168 39174
6. Lakics V, Karran E H, Boess F G. Quantitative comparison of phosphodiesterase mRNA distribution in human brain and peripheral tissues. Neuropharmacology: 2010; 59 367 374
7. Omori K, Kotera J. Overview of PDEs and their regulation. Circ Res: 2007; 100 309 327
8. Bender A T, Beavo J A. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev: 2006; 58 488 520
9. Thompson P E, Manganiello V, Degerman E. Re-discovering PDE3 inhibitors - new opportunities for a long neglected target. Curr Top Med Chem: 2007; 7 421 436
10. Manganiello V C, Ahmad F, Choi Y, Tang Y, Trzebiatowska E, Walz H, Berger K, Shen W, Liu H, Hockman S, Park S, Holst L S, Degerman E. Regulation of cyclic nucleotide phosphodiesterase 3 (PDE3). In: Tagawa T, Murata T, Shimizu K. (eds.). Phosphodiesterase and Intracellular Signaling. Mie University Press: 2007; 101 125
11. Degerman E, Belfrage P, Manganiello V C. Structure, localization, and regulation of cGMP-inhibited phosphodiesterase (PDE3). J Biol Chem: 1997; 272 6823 6826
12. Leroy M J, Degerman E, Taira M, Murata T, Wang L H, Movsesian M A, Meacci E, Manganiello V C. Characterization of two recombinant PDE3 (cGMP-inhibited cyclic nucleotide phosphodiesterase) isoforms, RcGIP1 and HcGIP2, expressed in NIH 3006 murine fibroblasts and Sf9 insect cells. Biochemistry: 1996; 35 10194 10202
13. Nilsson R, Ahmad F, Sward K, Andersson U, Weston M, Manganiello V, Degerman E. Plasma membrane cyclic nucleotide phosphodiesterase 3B (PDE3B) is associated with caveolae in primary adipocytes. Cell Signal: 2006; 18 1713 1721
14. Ahmad F, Lindh R, Tang Y, Weston M, Degerman E, Manganiello V C. Insulin-induced formation of macromolecular complexes involved in activation of cyclic nucleotide phosphodiesterase 3B (PDE3B) and its interaction with PKB. Biochem J: 2007; 404 257 268
15. Kenan Y, Murata T, Shakur Y, Degerman E, Manganiello V C. Functions of the N-terminal region of cyclic nucleotide phosphodiesterase 3 (PDE 3) isoforms. J Biol Chem: 2000; 275 12331 12338
16. Shakur Y, Takeda K, Kenan Y, Yu Z X, Rena G, Brandt D, Houslay M D, Degerman E, Ferrans V J, Manganiello V C. Membrane localization of cyclic nucleotide phosphodiesterase 3 (PDE3). Two N-terminal domains are required for the efficient targeting to, and association of, PDE3 with endoplasmic reticulum. J Biol Chem: 2000; 275 38749 38761
17. Kono T, Robinson F W, Sarver J A. Insulin-sensitive phosphodiesterase. Its localization, hormonal stimulation, and oxidative stabilization. J Biol Chem: 1975; 250 7826 7835
18. Varnerin J P, Chung C C, Patel S B, Scapin G, Parmee E R, Morin N R, MacNeil D J, Cully D F, Van der Ploeg L H, Tota M R. Expression, refolding, and purification of recombinant human phosphodiesterase 3B: definition of the N-terminus of the catalytic core. Protein Expr Purif: 2004; 35 225 236
19. Scapin G, Patel S B, Chung C, Varnerin J P, Edmondson S D, Mastracchio A, Parmee E R, Singh S B, Becker J W, Van der Ploeg L H, Tota M R. Crystal structure of human phosphodiesterase 3B: atomic basis for substrate and inhibitor specificity. Biochemistry: 2004; 43 6091 6100
20. Taira M, Hockman S C, Calvo J C, Taira M, Belfrage P, Manganiello V C. Molecular cloning of the rat adipocyte hormone-sensitive cyclic GMP-inhibited cyclic nucleotide phosphodiesterase. J Biol Chem: 1993; 268 18573 18579
21. Francis S H, Colbran J L, McAllister-Lucas L M, Corbin J D. Zinc interactions and conserved motifs of the cGMP-binding cGMP-specific phosphodiesterase suggest that it is a zinc hydrolase. J Biol Chem: 1994; 269 22477 22480
22. Zhang W, Ke H, Colman R W. Identification of interaction sites of cyclic nucleotide phosphodiesterase type 3A with milrinone and cilostazol using molecular modeling and site-directed mutagenesis. Mol Pharmacol: 2002; 62 514 520
23. Zhang W, Ke H, Tretiakova A P, Jameson B, Colman R W. Identification of overlapping but distinct cAMP and cGMP interaction sites with cyclic nucleotide phosphodiesterase 3A by site-directed mutagenesis and molecular modeling based on crystalline PDE4B. Protein Sci: 2001; 10 1481 1489
24. Ke H. Implications of PDE4 structure on inhibitor selectivity across PDE families. Int J Impot Res: 2004; 16 01 S24 S27
25. Choi Y H, Ekholm D, Krall J, Ahmad F, Degerman E, Manganiello V C, Movsesian M A. Identification of a novel isoform of the cyclic-nucleotide phosphodiesterase PDE3A expressed in vascular smooth-muscle myocytes. Biochem J: 2001; 353 41 50
26. Zmuda-Trzebiatowska E, Oknianska A, Manganiello V, Degerman E. Role of PDE3B in insulin-induced glucose uptake, GLUT-4 translocation and lipogenesis in primary rat adipocytes. Cell Signal: 2006; 18 382 390
27. Elks M L, Manganiello V C. Antilipolytic action of insulin: role of cAMP phosphodiesterase activation. Endocrinology: 1985; 116 2119 2121
28. Zaccolo M. cAMP signal transduction in the heart: understanding spatial control for the development of novel therapeutic strategies. Br J Pharmacol: 2009; 158 50 60
29. Leroy J, Abi-Gerges A, Nikolaev V O, Richter W, Lechene P, Mazet J L, Conti M, Fischmeister R, Vandecasteele G. Spatiotemporal dynamics of beta-adrenergic cAMP signals and L-type Ca2+ channel regulation in adult rat ventricular myocytes: role of phosphodiesterases. Circ Res: 2008; 102 1091 1100
30. Houslay M D. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci: 2010; 35 91 100
31. Raymond D R, Wilson L S, Carter R L, Maurice D H. Numerous distinct PKA-, or EPAC-based, signalling complexes allow selective phosphodiesterase 3 and phosphodiesterase 4 coordination of cell adhesion. Cell Signal: 2007; 19 2507 2518
32. Scott J D, Santana L F. A-kinase anchoring proteins: getting to the heart of the matter. Circulation: 2010; 121 1264 1271
33. Stangherlin A, Stangherlin A, Zaccolo M. Local Termination of cAMP signals: the Role of AKAP-Anchored Phosphodiesterases. J Cardiovasc Pharmacol: 2011; 58 345 353
34. Kritzer M D, Li J, Dodge-Kafka K, Kapiloff M S. AKAPs: The architectural underpinnings of local cAMP signaling. J Mol Cell Cardiol: 2011; 52 351 358
35. Nikolaev V O, Bunemann M, Schmitteckert E, Lohse M J, Engelhardt S. Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching beta1-adrenergic but locally confined beta2-adrenergic receptor-mediated signaling. Circ Res: 2006; 99 1084 1091
36. Leroy J, Richter W, Mika D, Castro L R, Abi-Gerges A, Xie M, Scheitrum C, Lefebvre F, Schittl J, Mateo P, Westenbroek R, Catterall W A, Charpentier F, Conti M, Fischmeister R, Vandecasteele G. Phosphodiesterase 4B in the cardiac L-type Ca(2) channel complex regulates Ca(2) current and protects against ventricular arrhythmias in mice. J Clin Invest: 2011; 121 2651 2661
37. Houslay M D, Baillie G S, Maurice D H. cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ Res: 2007; 100 950 966
38. Barki-Harrington L, Perrino C, Rockman H A. Network integration of the adrenergic system in cardiac hypertrophy. Cardiovasc Res: 2004; 63 391 402
39. Sin Y Y, Edwards H V, Li X, Day J P, Christian F, Dunlop A J, Adams D R, Zaccolo M, Houslay M D, Baillie G S. Disruption of the cyclic AMP phosphodiesterase-4 (PDE4)-HSP20 complex attenuates the beta-agonist induced hypertrophic response in cardiac myocytes. J Mol Cell Cardiol: 2011; 50 872 883
40. Fan G C, Yuan Q, Song G, Wang Y, Chen G, Qian J, Zhou X, Lee Y J, Ashraf M, Kranias E G. Small heat-shock protein Hsp20 attenuates beta-agonist-mediated cardiac remodeling through apoptosis signal-regulating kinase 1. Circ Res: 2006; 99 1233 1242
41. Bauman A L, Michel J J, Henson E, Dodge-Kafka K L, Kapiloff M S. The mAKAP signalosome and cardiac myocyte hypertrophy. IUBMB Life: 2007; 59 163 169
42. Dodge K L, Khouangsathiene S, Kapiloff M S, Mouton R, Hill E V, Houslay M D, Langeberg L K, Scott J D. mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. Embo J: 2001; 20 1921 1930
43. Dodge-Kafka K L, Bauman A, Mayer N, Henson E, Heredia L, Ahn J, McAvoy T, Nairn A C, Kapiloff M S. cAMP-stimulated protein phosphatase 2A activity associated with muscle A kinase-anchoring protein (mAKAP) signaling complexes inhibits the phosphorylation and activity of the cAMP-specific phosphodiesterase PDE4D3. J Biol Chem: 2010; 285 11078 11086
44. Dodge-Kafka K L, Soughayer J, Pare G C, Carlisle Michel J J, Langeberg L K, Kapiloff M S, Scott J D. The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature: 2005; 437 7058 574 578
45. Lehnart S E, Wehrens X H, Reiken S, Warrier S, Belevych A E, Harvey R D, Richter W, Jin S L, Conti M, Marks A R. Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias. Cell: 2005; 123 25 35
46. Lehnart S E, Marks A R. Phosphodiesterase 4D and heart failure: a cautionary tale. Expert Opin Ther Targets: 2006; 10 677 688
47. Begum N, Hockman S, Manganiello V C. Phosphodiesterase 3A (PDE3A) deletion suppresses proliferation of cultured murine vascular smooth muscle cells (VSMCS) via inhibition of mitogen activated protein kinase (MAPK) signaling and alterations in critical cell cycle regulatory proteins. J Biol Chem: 2011; 286 26238 26249
48. Vinogradova T M, Sirenko S, Lyashkov A E, Younes A, Li Y, Zhu W, Yang D, Ruknudin A M, Spurgeon H, Lakatta E G. Constitutive phosphodiesterase activity restricts spontaneous beating rate of cardiac pacemaker cells by suppressing local Ca2+ releases. Circ Res: 2008; 102 761 769
49. Tsai E J, Kass D A. Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol Ther: 2009; 122 216 238
50. Sun B, Li H, Shakur Y, Hensley J, Hockman S, Kambayashi J, Manganiello V C, Liu Y. Role of phosphodiesterase type 3A and 3B in regulating platelet and cardiac function using subtype-selective knockout mice. Cell Signal: 2007; 19 1765 1771
51. Lygren B, Carlson C R, Santamaria K, Lissandron V, McSorley T, Litzenberg J, Lorenz D, Wiesner B, Rosenthal W, Zaccolo M, Tasken K, Klussmann E. AKAP complex regulates Ca2+ re-uptake into heart sarcoplasmic reticulum. EMBO Rep: 2007; 8 1061 1067
52. Kerfant B G, Gidrewicz D, Sun H, Oudit G Y, Penninger J M, Backx P H. Cardiac sarcoplasmic reticulum calcium release and load are enhanced by subcellular cAMP elevations in PI3Kgamma-deficient mice. Circ Res: 2005; 96 1079 1086
53. Patrucco E, Notte A, Barberis L, Selvetella G, Maffei A, Brancaccio M, Marengo S, Russo G, Azzolino O, Rybalkin S D, Silengo L, Altruda F, Wetzker R, Wymann M P, Lembo G, Hirsch E. PI3Kgamma modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell: 2004; 118 375 387
54. Voigt P, Dorner M B, Schaefer M. Characterization of p87PIKAP, a novel regulatory subunit of phosphoinositide 3-kinase gamma that is highly expressed in heart and interacts with PDE3B. J Biol Chem: 2006; 281 9977 9986
55. Perino A, Ghigo A, Ferrero E, Morello F, Santulli G, Baillie G S, Damilano F, Dunlop A J, Pawson C, Walser R, Levi R, Altruda F, Silengo L, Langeberg L K, Neubauer G, Heymans S, Lembo G, Wymann M P, Wetzker R, Houslay M D, Iaccarino G, Scott J D, Hirsch E. Integrating cardiac PIP3 and cAMP signaling through a PKA anchoring function of p110gamma. Mol Cell: 2011; 42 84 95
56. Wilson L S, Baillie G S, Pritchard L M, Umana B, Terrin A, Zaccolo M, Houslay M D, Maurice D H. A phosphodiesterase 3B-based signaling complex integrates exchange protein activated by cAMP 1 and phosphatidylinositol 3-kinase signals in human arterial endothelial cells. J Biol Chem: 2011; 286 16285 16296
57. Kerfant B G, Zhao D, Lorenzen-Schmidt I, Wilson L S, Cai S, Chen S R, Maurice D H, Backx P H. 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
58. Penmatsa H, Zhang W, Yarlagadda S, Li C, Conoley V G, Yue J, Bahouth S W, Buddington R K, Zhang G, Nelson D J, Sonecha M D, Manganiello V, Wine J J, Naren A P. Compartmentalized cyclic adenosine 3,5-monophosphate at the plasma membrane clusters PDE3A and cystic fibrosis transmembrane conductance regulator into microdomains. Mol Biol Cell: 2010; 21 1097 1110
59. Puxeddu E, Uhart M, Li C C, Ahmad F, Pacheco-Rodriguez G, Manganiello V C, Moss J, Vaughan M. Interaction of phosphodiesterase 3A with brefeldin A-inhibited guanine nucleotide-exchange proteins BIG1 and BIG2 and effect on ARF1 activity. Proc Natl Acad Sci USA: 2009; 106 6158 6163
60. Shen W, Ahmad F, Hockman S, Ma J, Omi H, Raghavachari N, Manganiello V. Female infertility in PDE3A(-/-) mice: polo-like kinase 1 (Plk1) may be a target of protein kinase A (PKA) and involved in meiotic arrest of oocytes from PDE3A(-/-) mice. Cell Cycle: 2010; 9 4720 4734
61. Elbatarny H S, Maurice D H. Leptin-mediated activation of human platelets: involvement of a leptin receptor and phosphodiesterase 3A-containing cellular signaling complex. Am J Physiol Endocrinol Metab: 2005; 289 E695 E702
62. Rondinone C M, Carvalho E, Rahn T, Manganiello V C, Degerman E, Smith U P. Phosphorylation of PDE3B by phosphatidylinositol 3-kinase associated with the insulin receptor. J Biol Chem: 2000; 275 10093 10098
63. Onuma H, Osawa H, Yamada K, Ogura T, Tanabe F, Granner D K, Makino H. Identification of the insulin-regulated interaction of phosphodiesterase 3B with 14-3-3 beta protein. Diabetes: 2002; 51 3362 3367
64. Pozuelo R M, Campbell D G, Morrice N A, Mackintosh C. Phosphodiesterase 3A binds to 14-3-3 proteins in response to PMA-induced phosphorylation of Ser428. Biochem J: 2005; 392 Pt 1 163 172
65. Hunter R W, Mackintosh C, Hers I. Protein kinase C-mediated phosphorylation and activation of PDE3A regulate cAMP levels in human platelets. J Biol Chem: 2009; 284 12339 12348
66. Palmer D, Jimmo S L, Raymond D R, Wilson L S, Carter R L, Maurice D H. Protein kinase A phosphorylation of human phosphodiesterase 3B promotes 14-3-3 protein binding and inhibits phosphatase-catalyzed inactivation. J Biol Chem: 2007; 282 9411 9419
67. Kitamura T, Kitamura Y, Kuroda S, Hino Y, Ando M, Kotani K, Konishi H, Matsuzaki H, Kikkawa U, Ogawa W, Kasuga M. Insulin-induced phosphorylation and activation of cyclic nucleotide phosphodiesterase 3B by the serine-threonine kinase Akt. Mol Cell Biol: 1999; 19 6286 6296
68. Onuma H, Osawa H, Ogura T, Tanabe F, Nishida W, Makino H. A newly identified 50 kDa protein, which is associated with phosphodiesterase 3B, is phosphorylated by insulin in rat adipocytes. Biochem Biophys Res Commun: 2005; 337 976 982
69. rd edn Philadelphia Lippincott Raven: 2004; 373 383
70. Wijkander J, Landstrom T R, Manganiello V, Belfrage P, Degerman E. Insulin-induced phosphorylation and activation of phosphodiesterase 3B in rat adipocytes: possible role for protein kinase B but not mitogen-activated protein kinase or p70 S6 kinase. Endocrinology: 1998; 139 219 227
71. Ahmad F, Gao G, Wang L M, Landstrom T R, Degerman E, Pierce J H, Manganiello V C. IL-3 and IL-4 activate cyclic nucleotide phosphodiesterases 3 (PDE3) and 4 (PDE4) by different mechanisms in FDCP2 myeloid cells. J Immunol: 1999; 162 4864 4875
72. Ahmad F, Cong L N, Stenson H L, Wang L M, Rahn L T, Pierce J H, Quon M J, Degerman E, Manganiello V C. Cyclic nucleotide phosphodiesterase 3B is a downstream target of protein kinase B and may be involved in regulation of effects of protein kinase B on thymidine incorporation in FDCP2 cells. J Immunol: 2000; 164 4678 4688
73. Ahmad F, Lindh R, Tang Y, Ruishalme I, Ost A, Sahachartsiri B, Stralfors P, Degerman E, Manganiello V C. Differential regulation of adipocyte PDE3B in distinct membrane compartments by insulin and the beta3-adrenergic receptor agonist CL316243: effects of caveolin-1 knockdown on formation/maintenance of macromolecular signalling complexes. Biochem J: 2009; 424 399 410
74. Zhao A Z, Zhao H, Teague J, Fujimoto W, Beavo J A. Attenuation of insulin secretion by insulin-like growth factor 1 is mediated through activation of phosphodiesterase 3B. Proc Natl Acad Sci USA: 1997; 94 3223 3228
75. Zhao A Z, Bornfeldt K E, Beavo J A. Leptin inhibits insulin secretion by activation of phosphodiesterase 3B. J Clin Invest: 1998; 102 869 873
76. Zhao A Z, Shinohara M M, Huang D, Shimizu M, Eldar-Finkelman H, Krebs E G, Beavo J A, Bornfeldt K E. Leptin induces insulin-like signaling that antagonizes cAMP elevation by glucagon in hepatocytes. J Biol Chem: 2000; 275 11348 11354
77. Sadler S E. Type III phosphodiesterase plays a necessary role in the growth-promoting actions of insulin, insulin-like growth factor-I, and Ha p21ras in Xenopus laevis oocytes. Mol Endocrinol: 1991; 5 1939 1946
78. Andersen C B, Sakaue H, Nedachi T, Kovacina K S, Clayberger C, Conti M, Roth R A. Protein kinase B/Akt is essential for the insulin- but not progesterone-stimulated resumption of meiosis in Xenopus oocytes. Biochem J: 2003; 369 Pt 2 227 238
79. Rahn T, Ridderstrale M, Tornqvist H, Manganiello V, Fredrikson G, Belfrage P, Degerman E. Essential role of phosphatidylinositol 3-kinase in insulin-induced activation and phosphorylation of the cGMP-inhibited cAMP phosphodiesterase in rat adipocytes. Studies using the selective inhibitor wortmannin. FEBS Lett: 1994; 350 314 318
80. Okada T, Kawano Y, Sakakibara T, Hazeki O, Ui M. Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J Biol Chem: 1994; 269 3568 3573
81. Lindh R, Ahmad F, Resjo S, James P, Yang J S, Fales H M, Manganiello V, Degerman E. Multisite phosphorylation of adipocyte and hepatocyte phosphodiesterase 3B. Biochim Biophys Acta: 2007; 1773 584 592
82. Mercier I, Jasmin J F, Pavlides S, Minetti C, Flomenberg N, Pestell R G, Frank P G, Sotgia F, Lisanti M P. Clinical and translational implications of the caveolin gene family: lessons from mouse models and human genetic disorders. Lab Invest: 2009; 89 614 623
83. Parton R G. Caveolae and caveolins. Curr Opin Cell Biol: 1996; 8 542 548
84. Rothberg K G, Heuser J E, Donzell W C, Ying Y S, Glenney J R, Anderson R G. Caveolin, a protein component of caveolae membrane coats. Cell: 1992; 68 673 682
85. Garver W S, Heidenreich R A, Erickson R P, Thomas M A, Wilson J M. Localization of the murine Niemann-Pick C1 protein to two distinct intracellular compartments. J Lipid Res: 2000; 41 673 687
86. Predescu S A, Predescu D N, Palade G E. Endothelial transcytotic machinery involves supramolecular protein-lipid complexes. Mol Biol Cell: 2001; 12 1019 1033
87. Pelkmans L, Burli T, Zerial M, Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell: 2004; 118 767 780
88. Head B P, Insel P A. Do caveolins regulate cells by actions outside of caveolae? Trends Cell Biol: 2007; 17 51 57
89. Harris J, Werling D, Koss M, Monaghan P, Taylor G, Howard C J. Expression of caveolin by bovine lymphocytes and antigen-presenting cells. Immunology: 2002; 105 190 195
90. Swaney J S, Patel H H, Yokoyama U, Head B P, Roth D M, Insel P A. Focal adhesions in (myo)fibroblasts scaffold adenylyl cyclase with phosphorylated caveolin. J Biol Chem: 2006; 281 17173 17179
91. del Pozo M A, Balasubramanian N, Alderson N B, Kiosses W B, Grande-Garcia A, Anderson R G, Schwartz M A. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol: 2005; 7 901 908
92. Cohen A W, Park D S, Woodman S E, Williams T M, Chandra M, Shirani J, Pereira de S A, Kitsis R N, Russell R G, Weiss L M, Tang B, Jelicks L A, Factor S M, Shtutin V, Tanowitz H B, Lisanti M P. Caveolin-1 null mice develop cardiac hypertrophy with hyperactivation of p42/44 MAP kinase in cardiac fibroblasts. Am J Physiol Cell Physiol: 2003; 284 C457 C474
93. Torres V A, Tapia J C, Rodriguez D A, Parraga M, Lisboa P, Montoya M, Leyton L, Quest A F. Caveolin-1 controls cell proliferation and cell death by suppressing expression of the inhibitor of apoptosis protein survivin. J Cell Sci: 2006; 119 Pt 9 1812 1823
94. Razani B, Combs T P, Wang X B, Frank P G, Park D S, Russell R G, Li M, Tang B, Jelicks L A, Scherer P E, Lisanti M P. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem: 2002; 277 8635 8647
95. Fernandez M A, Albor C, Ingelmo-Torres M, Nixon S J, Ferguson C, Kurzchalia T, Tebar F, Enrich C, Parton R G, Pol A. Caveolin-1 is essential for liver regeneration. Science: 2006; 313 5793 1628 1632
96. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft F C, Schedl A, Haller H, Kurzchalia T V. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science: 2001; 293 5539 2449 2452
97. Trushina E, Du C J, Parisi J, McMurray C T. Neurological abnormalities in caveolin-1 knock out mice. Behav Brain Res: 2006; 172 24 32
98. Augustus A S, Buchanan J, Addya S, Rengo G, Pestell R G, Fortina P, Koch W J, Bensadoun A, Abel E D, Lisanti M P. Substrate uptake and metabolism are preserved in hypertrophic caveolin-3 knockout hearts. Am J Physiol Heart Circ Physiol: 2008; 295 H657 H666
99. Head B P, Patel H H, Roth D M, Lai N C, Niesman I R, Farquhar M G, Insel P A. 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
100. 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
101. Cohen A W, Razani B, Schubert W, Williams T M, Wang X B, Iyengar P, Brasaemle D L, Scherer P E, Lisanti M P. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes: 2004; 53 1261 1270