Role of membrane microdomains in compartmentation of cAMP signaling

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Agarwal, Shailesh R ^a   Yang, Pei Chi ^b   Rice, Monica ^a   Singer, Cherie A ^a   Nikolaev, Viacheslav O ^c   Lohse, Martin J ^d   Clancy, Colleen E ^b   Harvey, Robert D ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CHOLESTEROL; CYCLIC AMP; PHOSPHODIESTERASE; RECEPTOR;

ARTICLE; BIOSENSOR; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELL LINE; HUMAN; HUMAN CELL; LIPID RAFT; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; CELL LINE; CHEMISTRY; GENETIC PROCEDURES; METABOLISM;

BIOSENSING TECHNIQUES; CELL LINE; CHOLESTEROL; CYCLIC AMP; HUMANS; MEMBRANE MICRODOMAINS; SIGNAL TRANSDUCTION;

EID: 84899676539     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095835     Document Type: Article

References (66)

1. Brunton LL, Hayes JS, Mayer SE (1981) Functional compartmentation of cyclic AMP and protein kinase in heart. Adv Cyclic Nucleotide Res 14: 391-397.
2. Hayes JS, Brunton LL (1982) Functional compartments in cyclic nucleotide action. J Cyclic Nucleotide Res 8: 1-16. (Pubitemid 12047342)
3. Buxton IL, Brunton LL (1983) Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J Biol Chem 258: 10233-10239. (Pubitemid 14241179)
4. Hayes JS, Brunton LL, Mayer SE (1980) Selective activation of particulate cAMP-dependent protein kinase by isoproterenol and prostaglandin E1. J Biol Chem 255: 5113-5119. (Pubitemid 10015830)
5. Nikolaev VO, Lohse MJ (2006) Monitoring of cAMP synthesis and degradation in living cells. Physiology (Bethesda) 21: 86-92. (Pubitemid 43752504)
6. Berrera M, Dodoni G, Monterisi S, Pertegato V, Zamparo I, et al. (2008) A toolkit for real-time detection of cAMP: insights into compartmentalized signaling. Handb Exp Pharmacol: 285-298.
7. Karpen JW, Rich TC (2005) High-resolution measurements of cyclic adenosine monophosphate signals in 3D microdomains. Methods MolBiol 307: 15-26.
8. DiPilato LM, Zhang J (2009) The role of membrane microdomains in shaping beta2-adrenergic receptor-mediated cAMP dynamics. Mol Biosyst 5: 832-837.
9. Terrin A, Di Benedetto G, Pertegato V, Cheung YF, Baillie G, et al. (2006) PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J Cell Biol 175: 441-451. (Pubitemid 44708068)
10. Rich TC, Fagan KA, Tse TE, Schaack J, Cooper DM, et al. (2001) A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc Natl Acad Sci USA 98: 13049-13054. (Pubitemid 33051315)
11. Rich TC, Fagan KA, Nakata H, Schaack J, Cooper DM, et al. (2000) Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 116: 147-161. (Pubitemid 30637001)
12. Rich TC, Xin W, Mehats C, Hassell KA, Piggott L, et al. (2007) Cellular mechanisms underlying prostaglandin-induced transient cAMP signals near the plasma membrane of HEK-293 cells. Am J Physiol Cell Physiol 292: C319-C331. (Pubitemid 46115141)
13. Mika D, Leroy J, Vandecasteele G, Fischmeister R (2012) PDEs create local domains of cAMP signaling. J Mol Cell Cardiol 52: 323-329.
14. Oliveira RF, Terrin A, Di Benedetto G, Cannon RC, Koh W, et al. (2010) The role of type 4 phosphodiesterases in generating microdomains of cAMP: large scale stochastic simulations. PLoS One 5: e11725.
15. Zaccolo M, Pozzan T (2002) Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295: 1711-1715. (Pubitemid 34202906)
16. Ostrom RS, Insel PA (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 143: 235-245. (Pubitemid 39315143)
17. Cooper DM, Crossthwaite AJ (2006) Higher-order organization and regulation of adenylyl cyclases. Trends Pharmacol Sci 27: 426-431. (Pubitemid 44069584)
18. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
19. Epand RM (2008) Proteins and cholesterol-rich domains. Biochim Biophys Acta 1778: 1576-1582.
20. Pike LJ (2003) Lipid rafts: bringing order to chaos. J Lipid Res 44: 655-667.
21. Insel PA, Head BP, Patel HH, Roth DM, Bundey RA, et al. (2005) Compartmentation of G-protein-coupled receptors and their signalling components in lipid rafts and caveolae. Biochem Soc Trans 33: 1131-1134. (Pubitemid 41659132)
22. Agarwal SR, Macdougall DA, Tyser R, Pugh SD, Calaghan SC, et al. (2011) Effects of cholesterol depletion on compartmentalized cAMP responses in adult cardiac myocytes. J Mol Cell Cardiol 50: 500-509.
23. Ostrom RS, Gregorian C, Drenan RM, Xiang Y, Regan JW, et al. (2001) Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem 276: 42063-42069.
24. Ostrom RS, Liu X, Head BP, Gregorian C, Seasholtz TM, et al. (2002) Localization of adenylyl cyclase isoforms and G protein-coupled receptors in vascular smooth muscle cells: expression in caveolin-rich and noncaveolin domains. Mol Pharmacol 62: 983-992. (Pubitemid 35222489)
25. Liu X, Thangavel M, Sun SQ, Kaminsky J, Mahautmr P, et al. (2008) Adenylyl cyclase type 6 overexpression selectively enhances beta-adrenergic and prostacyclin receptor-mediated inhibition of cardiac fibroblast function because of colocalization in lipid rafts. Naunyn Schmiedebergs Arch Pharmacol 377: 359-369. (Pubitemid 351868523)
26. Bogard AS, Xu C, Ostrom RS (2011) Human Bronchial Smooth Muscle Cells Express Adenylyl Cyclase Isoforms 2, 4, and 6 in Distinct Membrane Microdomains. J Pharmacol Exp Ther 337: 209-217.
27. Pontier SM, Percherancier Y, Galandrin S, Breit A, Gales C, et al. (2008) Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J Biol Chem 283: 24659-24672.
28. Wachten S, Masada N, Ayling LJ, Ciruela A, Nikolaev VO, et al. (2010) Distinct pools of cAMP centre on different isoforms of adenylyl cyclase in pituitary-derived GH3B6 cells. J Cell Sci 123: 95-106.
29. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ (2004) Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279: 37215-37218. (Pubitemid 39195424)
30. Iancu RV, Ramamurthy G, Warrier S, Nikolaev VO, Lohse MJ, et al. (2008) Cytoplasmic cAMP concentrations in intact cardiac myocytes. Am J Physiol Cell Physiol 295: C414-C422. (Pubitemid 352755775)
31. Zacharias DA, Violin JD, Newton AC, Tsien RY (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296: 913-916. (Pubitemid 34464897)
32. Melkonian KA, Ostermeyer AG, Chen JZ, Roth MG, Brown DA (1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J Biol Chem 274: 3910-3917. (Pubitemid 29077242)
33. Depry C, Allen MD, Zhang J (2011) Visualization of PKA activity in plasma membrane microdomains. Mol Biosyst 7: 52-58.
34. Gao X, Lowry PR, Zhou X, Depry C, Wei Z, et al. (2011) PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains. Proc Natl Acad Sci U S A 108: 14509-14514.
35. Eggeling C, Ringemann C, Medda R, Schwarzmann G, Sandhoff K, et al. (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457: 1159-1162.
36. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11: 688-699.
37. Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, et al. (2003) Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 100: 13964-13969. (Pubitemid 37499174)
38. Ayling LJ, Briddon SJ, Halls ML, Hammond GR, Vaca L, et al. (2012) Adenylyl cyclase AC8 directly controls its micro-environment by recruiting the actin cytoskeleton in a cholesterol-rich milieu. J Cell Sci 125: 869-886.
39. Nishimura SY, Vrljic M, Klein LO, McConnell HM, Moerner WE (2006) Cholesterol depletion induces solid-like regions in the plasma membrane. Biophys J 90: 927-938.
40. Pucadyil TJ, Chattopadhyay A (2006) Role of cholesterol in the function and organization of G-protein coupled receptors. Progress in lipid research 45: 295-333. (Pubitemid 43818130)
41. Brameshuber M, Weghuber J, Ruprecht V, Gombos I, Horvath I, et al. (2010) Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane. J Biol Chem 285: 41765-41771.
42. Allen JA, Halverson-Tamboli RA, Rasenick MM (2007) Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8: 128-140. (Pubitemid 46146951)
43. Borner S, Schwede F, Schlipp A, Berisha F, Calebiro D, et al. (2011) FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat Protoc 6: 427-438.
44. Lynch MJ, Baillie GS, Mohamed A, Li X, Maisonneuve C, et al. (2005) 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 280: 33178-33189. (Pubitemid 41397113)
45. Matthiesen K, Nielsen J (2011) Cyclic AMP control measured in two compartments in HEK293 cells: phosphodiesterase K(M) is more important than phosphodiesterase localization. PLoS One 6: e24392.
46. Stoclet J-C, Keravis T, Komas N, Lugnier C (1995) Cyclic nucleotide phosphodiesterases as therapeutic targets in cardiovascular disease. Exp Opin Invest Drugs 4: 1081-1100.
47. Bolger GB, Erdogan S, Jones RE, Loughney K, Scotland G, et al. (1997) Characterization of five different proteins produced by alternatively spliced mRNAs from the human cAMP-specific phosphodiesterase PDE4D gene. Biochem J 328 (Pt 2): 539-548. (Pubitemid 27515598)
48. Inglese J, Luttrell LM, Iniguez-Lluhi JA, Touhara K, Koch WJ, et al. (1994) Functionally active targeting domain of the beta-adrenergic receptor kinase: an inhibitor of G beta gamma-mediated stimulation of type II adenylyl cyclase. Proc Natl Acad Sci USA 91: 3637-3641.
49. 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: 16513-16518. (Pubitemid 39557744)
50. Kenworthy AK, Nichols BJ, Remmert CL, Hendrix GM, Kumar M, et al. (2004) Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 165: 735-746. (Pubitemid 38765774)
51. Day CA, Kenworthy AK (2012) Mechanisms underlying the confined diffusion of cholera toxin B-subunit in intact cell membranes. PLoS One 7: e34923.
52. van Meer G (2005) Cellular lipidomics. EMBO J 24: 3159-3165.
53. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9: 112-124. (Pubitemid 351158912)
54. Vrljic M, Nishimura SY, Moerner WE, McConnell HM (2005) Cholesterol depletion suppresses the translational diffusion of class II major histocompatibility complex proteins in the plasma membrane. Biophys J 88: 334-347. (Pubitemid 40070680)
55. Lebreton S, Paladino S, Zurzolo C (2008) Selective roles for cholesterol and actin in compartmentalization of different proteins in the Golgi and plasma membrane of polarized cells. J Biol Chem 283: 29545-29553.
56. Harvey RD, Calaghan SC (2012) Caveolae create local signalling domains through their distinct protein content, lipid profile and morphology. J Mol Cell Cardiol 52: 366-375.
57. Rybin VO, Xu X, Lisanti MP, Steinberg SF (2000) 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 275: 41447-41457. (Pubitemid 32054981)
58. Thangavel M, Liu X, Sun SQ, Kaminsky J, Ostrom RS (2009) The C1 and C2 domains target human type 6 adenylyl cyclase to lipid rafts and caveolae. Cell Signal 21: 301-308.
59. Pinto C, Papa D, Hubner M, Mou TC, Lushington GH, et al. (2008) Activation and inhibition of adenylyl cyclase isoforms by forskolin analogs. J Pharmacol Exp Ther 325: 27-36. (Pubitemid 351439155)
60. Pieroni JP, Harry A, Chen J, Jacobowitz O, Magnusson RP, et al. (1995) Distinct characteristics of the basal activities of adenylyl cyclases 2 and 6. J Biol Chem 270: 21368-21373.
61. Insel PA, Ostrom RS (2003) Forskolin as a tool for examining adenylyl cyclase expression, regulation, and G protein signaling. Cell Mol Neurobiol 23: 305-314. (Pubitemid 36676277)
62. Warrier S, Belevych AE, Ruse M, Eckert RL, Zaccolo M, et al. (2005) Betaadrenergic and muscarinic receptor induced changes in cAMP activity in adult cardiac myocytes detected using a FRET based biosensor. Am J Physiol Cell Physiol 289: C455-C461. (Pubitemid 41008892)
63. Warrier S, Ramamurthy G, Eckert RL, Nikolaev VO, Lohse MJ, et al. (2007) cAMP microdomains and L-type Ca2+ channel regulation in guinea-pig ventricular myocytes. J Physiol (Lond) 580: 765-776. (Pubitemid 46909033)
64. Reits Ea, Neefjes JJ (2001) From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 3: E145-147.
65. Voit EO (2000) Computational Analysis of Biochemical Systems: A Practical Guide for Biochemists and Molecular Biologists. New York: Cambridge University Press.
66. Bender AT, Beavo JA (2006) Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58: 488-520. (Pubitemid 44394910)