Adenylyl cyclase AC8 directly controls its micro-environment by recruiting the actin cytoskeleton in a cholesterol-rich milieu

Journal of Cell Science

Volumn 125, Issue 4, 2012, Pages 869-886

  Ayling, Laura J ^a   Briddon, Stephen J ^b   Halls, Michelle L ^a   Hammond, Gerald R V ^a   Vaca, Luis ^c   Pacheco, Jonathan ^c   Hill, Stephen J ^b   Cooper, Dermot M F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Adenylyl cyclase; cAMP; Cholesterol; Cytoskeleton; FRAP; Rafts

Indexed keywords

ACTIN; ADENYLATE CYCLASE; ADENYLYL CYCLASE 8; CHOLESTEROL; CYCLIC AMP; STEROL; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL INTERACTION; CELL MEMBRANE; CHOLESTEROL TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ENZYME KINETICS; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; LIPID RAFT; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN DOMAIN;

ACTIN CYTOSKELETON; ADENYLATE CYCLASE; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CHOLESTEROL; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MEMBRANE MICRODOMAINS; PROTEIN BINDING; SIGNAL TRANSDUCTION; SPECTROMETRY, FLUORESCENCE;

EID: 84861215595     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.091090     Document Type: Article

References (84)

1. Bacskai, B. J., Hochner, B., Mahaut-Smith, M., Adams, S. R., Kaang, B. K., Kandel, E. R. and Tsien, R. Y. (1993). Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260, 222-226.
2. Bauman, A. L., Soughayer, J., Nguyen, B. T., Willoughby, D., Carnegie, G. K., Wong, W., Hoshi, N., Langeberg, L. K., Cooper, D. M. F., Dessauer, C. W. et al. (2006). Dynamic regulation of cAMP synthesis through anchored PKA-adenylyl cyclase V/VI complexes. Mol. Cell 23, 925-931.
3. 2+ mobilization in NCB-20 cells leading to direct inhibition of adenylylcyclase. A novel mechanism for inhibition of cAMP production. J. Biol. Chem. 266, 4995-5003.
4. Briddon, S. J., Middleton, R. J., Cordeaux, Y., Flavin, F. M., Weinstein, J. A., George, M. W., Kellam, B. and Hill, S. J. (2004). Quantitative analysis of the formation and diffusion of A1-adenosine receptor-antagonist complexes in single living cells. Proc. Natl. Acad. Sci. USA 101, 4673-4678.
5. Brown, D. A. and London, E. (1998). Functions of lipid rafts in biological membranes. Ann. Rev. Cell Dev. Biol. 14, 111-136.
6. Brown, D. A. and London, E. (2000). Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224.
7. Buxton, I. L. and Brunton, L. L. (1983). Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J. Biol. Chem. 258, 10233-10239.
8. Cha, B., Kenworthy, A., Murtazina, R. and Donowitz, M. (2004). The lateral mobility of NHE3 on the apical membrane of renal epithelial OK cells is limited by the PDZ domain proteins NHERF1/2, but is dependent on an intact actin cytoskeleton as determined by FRAP. J Cell Sci. 117, 3353-3365.
9. 2+ signals required for specific cell functions. PLoS Biol. 9, e1001025.
10. Chichili, G. R. and Rodgers, W. (2007). Clustering of membrane raft proteins by the actin cytoskeleton. J. Biol. Chem. 282, 36682-36691.
11. Chou, J. L., Huang, C. L., Lai, H. L., Hung, A. C., Chien, C. L., Kao, Y. Y. and Chern, Y. (2004). Regulation of type VI adenylyl cyclase by Snapin, a SNAP25- binding protein. J. Biol. Chem. 279, 46271-46279.
12. Contreras, F. X., Villar, A. V., Alonso, A., Kolesnick, R. N. and Goni, F. M. (2003). Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. J. Biol. Chem. 278, 37169-37174.
13. Cooper, D. M. F. and Crossthwaite, A. J. (2006). Higher-order organization and regulation of adenylyl cyclases. Trends Pharmacol. Sci. 27, 426-431.
14. Cristofanilli, M., Mizuno, F. and Akopian, A. (2007). Disruption of actin cytoskeleton causes internalization of Ca(v)1.3 (alpha 1D) L-type calcium channels in salamander retinal neurons. Mol. Vis. 13, 1496-1507.
15. Crossthwaite, A. J., Ciruela, A., Rayner, T. F. and Cooper, D. M. F. (2006). A direct interaction between the N terminus of adenylyl cyclase AC8 and the catalytic subunit of protein phosphatase 2A. Mol. Pharmacol. 69, 608-617.
16. Dell'Acqua, M. L., Smith, K. E., Gorski, J. A., Horne, E. A., Gibson, E. S. and Gomez, L. L. (2006). Regulation of neuronal PKA signalling through AKAP targeting dynamics. Eur. J. Cell Biol. 85, 627-633.
17. dos Remedios, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A. and Nosworthy, N. J. (2003). Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83, 433-473.
18. Edidin, M. (1992). Patches, posts and fences: proteins and plasma membrane domains. Trends Cell Biol. 2, 376-380.
19. Efendiev, R., Samelson, B. K., Nguyen, B. T., Phatarpekar, P. V., Baameur, F., Scott, J. D. and Dessauer, C. W. (2010). AKAP79 interacts with multiple adenylyl cyclase (AC) isoforms and scaffolds AC5 and -6 to alpha-amino-3-hydroxyl-5- methyl-4-isoxazole-propionate (AMPA) receptors. J. Biol. Chem. 285, 14450-14458.
20. Enserink, J. M., Christensen, A. E., de Rooij, J., van Triest, M., Schwede, F., Genieser, H. G., Døskeland, S. O., Blank, J. L. and Bos, J. L. (2002). A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 4, 901-906.
21. 2+ entry sites. J. Biol. Chem. 271, 12438-12444.
22. Gruenberg, J. (2001). The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2, 721-730.
23. Gu, C. and Cooper, D. M. F. (1999). Calmodulin-binding sites on adenylyl cyclase type VIII. J. Biol. Chem. 274, 8012-8021.
24. Haggie, P. M., Stanton, B. A. and Verkman, A. S. (2004). Increased diffusional mobility of CFTR at the plasma membrane after deletion of its C-terminal PDZ binding motif. J. Biol. Chem. 279, 5494-5500.
25. Halls, M. L. and Cooper, D. M. F. (2010). Sub-picomolar relaxin signaling by a pre- assembled RXFP1, AKAP-79, AC2, β-arrestin 2, PDE4D3 complex. EMBO J. 29, 2772-2787.
26. Hammond, G. R., Sim, Y., Lagnado, L. and Irvine, R. F. (2009). Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. J. Cell Biol. 184, 297-308.
27. Hancock, J. F. and Parton, R. G. (2005). Ras plasma membrane signalling platforms. Biochem. J. 389, 1-11.
28. Hansen, G. H., Niels-Christiansen, L. L., Thorsen, E., Immerdal, L. and Danielsen, E. M. (2000). Cholesterol depletion of enterocytes. Effect on the Golgi complex and apical membrane trafficking. J. Biol. Chem. 275, 5136-5142.
29. Haustein, E. and Schwille, P. (2004). Single-molecule spectroscopic methods. Curr. Opin. Struct. Biol. 14, 531-540.
30. Head, B. P., Patel, H. H., Roth, D. M., Murray, F., Swaney, J. S., Niesman, I. R., Farquhar, M. G. and Insel, P. A. (2006). Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J. Biol. Chem. 281, 26391-26399.
31. Howe, A. K. (2004). Regulation of actin-based cell migration by cAMP/PKA. Biochim. Biophys. Acta 1692, 159-174.
32. Iancu, R. V., Ramamurthy, G. and Harvey, R. D. (2008). Spatial and temporal aspects of cAMP signalling in cardiac myocytes. Clin. Exp. Pharmacol. Physiol. 35, 1343-1348.
33. Ilangumaran, S. and Hoessli, D. C. (1998). Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335, 433-440.
34. 2+ channels by beta-adrenergic agonists. Proc. Natl. Acad. Sci. USA 93, 295-299.
35. Kenworthy, A. K., Nichols, B. J., Remmert, C. L., Hendrix, G. M., Kumar, M., Zimmerberg, J. and Lippincott-Schwartz, J. (2004). Dynamics of putative raft- associated proteins at the cell surface. J. Cell Biol. 165, 735-746.
36. Kim, S. A., Heinze, K. G. and Schwille, P. (2007). Fluorescence correlation spectroscopy in living cells. Nat. Methods 4, 963-973.
37. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R. S., Kondo, J. and Fujiwara, T. (2005). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34, 351-378.
38. Langhorst, M. F., Solis, G. P., Hannbeck, S., Plattner, H. and Stuermer, C. A. (2007). Linking membrane microdomains to the cytoskeleton: regulation of the lateral mobility of reggie-1/flotillin-2 by interaction with actin. FEBS Lett. 581, 4697-4703.
39. Li, H. and Papadopoulos, V. (1998). Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139, 4991-4997.
40. Lingwood, D., Ries, J., Schwille, P. and Simons, K. (2008). Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. USA 105, 10005-10010.
41. Lynch, M. J., Baillie, G. S. and Houslay, M. D. (2007). cAMP-specific phosphodiesterase-4D5 (PDE4D5) provides a paradigm for understanding the unique non-redundant roles that PDE4 isoforms play in shaping compartmentalized cAMP cell signalling. Biochem. Soc. Trans. 35, 938-941.
42. Maciver, S. K. and Hussey, P. J. (2002). The ADF/cofilin family: actin-remodeling proteins. Genome Biol. 3, reviews 3007.
43. 2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol. Pharmacol. 75, 830-842.
44. Nadella, K. S., Saji, M., Jacob, N. K., Pavel, E., Ringel, M. D. and Kirschner, L. S. (2009). Regulation of actin function by protein kinase A-mediated phosphorylation of Limk1. EMBO Rep. 10, 599-605.
45. 2+-sensitive adenylyl cyclase/ aequorin chimera. J. Biol. Chem. 272, 18093-18097.
46. Nikolaev, V. O., Bunemann, M., Hein, L., Hannawacker, A. and Lohse, M. J. (2004). Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279, 37215-37218.
47. 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.
48. Nishimura, S. Y., Vrljic, M., Klein, L. O., McConnell, H. M. and Moerner, W. E. (2006). Cholesterol depletion induces solid-like regions in the plasma membrane. Biophys. J. 90, 927-938.
49. Oancea, E., Teruel, M. N., Quest, A. F. and Meyer, T. (1998). Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J. Cell Biol. 140, 485-498.
50. O'Connell, K. M., Rolig, A. S., Whitesell, J. D. and Tamkun, M. M. (2006). Kv2.1 potassium channels are retained within dynamic cell surface microdomains that are defined by a perimeter fence. J. Neurosci. 26, 9609-9618.
51. Pagano, M., Clynes, M. A., Masada, N., Ciruela, A., Ayling, L. J., Wachten, S. and Cooper, D. M. F. (2009). Insights into the residence in lipid rafts of adenylyl cyclase AC8 and its regulation by capacitative calcium entry. Am. J. Physiol. Cell Physiol. 296, C607-C619.
52. Paller, M. S. (1994). Lateral mobility of Na, K-ATPase and membrane lipids in renal cells. Importance of cytoskeletal integrity. J. Membr. Biol. 142, 127-135.
53. Pani, B., Ong, H. L., Liu, X., Rauser, K., Ambudkar, I. S. and Singh, B. B. (2008). Lipid rafts determine clustering of STIM1 in ER-plasma membrane junctions and regulation of SOCE. J. Biol. Chem. 20, 17333-17340.
54. Parekh, A. B. and Putney, J. W. (2005). Store-operated calcium channels. Physiol. Rev. 85, 757-810.
55. Park, W. S., Heo, W. D., Whalen, J. H., O'Rourke, N. A., Bryan, H. M., Meyer, T. and Teruel, M. N. (2008). Comprehensive identification of PIP3-regulated PH domains from C. elegans to H. sapiens by model prediction and live imaging. Mol. Cell 30, 381-392.
56. Popik, W. and Alce, T. M. (2004). CD4 receptor localized to non-raft membrane microdomains supports HIV-1 entry. Identification of a novel raft localization marker in CD4. J. Biol. Chem. 279, 704-712.
57. Pucadyil, T. J., Mukherjee, S. and Chattopadhyay, A. (2007). Organization and dynamics of NBD-labeled lipids in membranes analyzed by fluorescence recovery after photobleaching. J. Phys. Chem. B 111, 1975-1983.
58. Rich, T. C., Fagan, K. A., Nakata, H., Schaack, J., Cooper, D. M. F. and Karpen, J. W. (2000). Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J. Gen. Physiol. 116, 147-161.
59. Rodgers, W. and Zavzavadjian, J. (2001). Glycolipid-enriched membrane domains are assembled into membrane patches by associating with the actin cytoskeleton. Exp. Cell Res. 267, 173-183.
60. Rossin, A., Kral, R., Lounnas, N., Chakrabandhu, K., Mailfert, S., Marguet, D. and Hueber, A. O. (2010). Identification of a lysine-rich region of Fas as a raft nanodomain targeting signal necessary for Fas-mediated cell death. Exp. Cell Res. 316, 1513-1522.
61. Ruppelt, A., Mosenden, R., Gronholm, M., Aandahl, E. M., Tobin, D., Carlson, C. R., Abrahamsen, H., Herberg, F. W., Carpen, O. and Tasken, K. (2007). Inhibition of T cell activation by cyclic adenosine 5'-monophosphate requires lipid raft targeting of protein kinase A type I by the A-kinase anchoring protein ezrin. J. Immunol. 179, 5159-5168.
62. Sako, Y. and Kusumi, A. (1994). Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J. Cell Biol. 125, 1251-1264.
63. Salgado, A., Ordaz, B., Sampieri, A., Zepeda, A., Glazebrook, P., Kunze, D. and Vaca, L. (2008). Regulation of the cellular localization and function of human transient receptor potential channel 1 by other means of the TRPC family. Cell Calcium 43, 375-387.
64. Schroeder, F., Woodford, J. K., Kavecansky, J., Wood, W. G. and Joiner, C. (1995). Cholesterol domains in biological membranes. Mol. Membr. Biol. 12, 113-119.
65. Schubert, T. and Akopian, A. (2004). Actin filaments regulate voltage-gated ion channels in salamander retinal ganglion cells. Neuroscience 125, 583-590.
66. Schwille, P. (2001). Fluorescence correlation spectroscopy and its potential for intracellular applications. Cell Biochem. Biophys. 34, 383-408.
67. Shvartsman, D. E., Gutman, O., Tietz, A. and Henis, Y. I. (2006). Cyclodextrins but not compactin inhibit the lateral diffucion of membrane proteins independent of cholesterol. Traffic 7, 917-926.
68. 2+-stimulation of adenylyl cyclase type 8. J. Biol. Chem. 281, 17379-17389.
69. 2+ entry. J. Biol. Chem. 277, 6025-6031.
70. Stahlhut, M. and van Deurs, B. (2000). Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Mol. Biol. Cell 11, 325-337.
71. Staneva, G., Momchilova, A., Wolf, C., Quinn, P. J. and Koumanov, K. (2009). Membrane microdomains: role of ceramides in the maintenance of their structure and functions. Biochim. Biophys. Acta 1788, 666-675.
72. Suzuki, K., Ritchie, K., Kajikawa, E., Fujiwara, T. and Kusumi, A. (2005). Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys. J. 88, 3659-3680.
73. Tamkun, M. M., O'Connell, M. and Rolig, A. S. (2007). A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels. J. Cell Sci. 120, 2413-2423.
74. Tesmer, J. J., Sunahara, R. K., Johnson, R. A., Gosselin, G., Gilman, A. and Sprang, S. R. (1999). Two-metal-Ion catalysis in adenylyl cyclase. Science 285,756-760.
75. Tomishige, M., Sako, Y. and Kusumi, A. (1998). Regulation of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J. Cell Biol. 142,989-1000.
76. Umemura, M., Vrljic, M., Nishimura, S. Y., Fujiwara, T. K., Suzuki, K. G. and Kusumi, A. (2008). Both MHC class II and its GPI-anchored form undergo hop diffusion as observed by single-molecule tracking. Biophys. J. 95, 435-450.
77. Wachten, S., Masada, N., Ayling, L. J., Ciruela, A., Nikolaev, V. O., Lohse, M. J. and Cooper, D. M. F. (2010). Distinct pools of cAMP centre on different isoforms of adenylyl cyclase in pituitary-derived GH3B6 cells. J. Cell Sci. 123, 95-106.
78. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87, 965-1010.
79. 2+-regulated adenylyl cyclases from changes in intracellular pH. J. Biol. Chem. 280, 30864-30872.
80. Willoughby, D., Wong, W., Schaack, J., Scott, J. D. and Cooper, D. M. F. (2006). An anchored PKA and PDE4 complex regulates subplasmalemmal cAMP dynamics. EMBO J. 25, 2051-2061.
81. 2+ microdomains associated with different isoforms of adenylyl cyclase. J. Cell Sci. 123, 107-117.
82. 2+-dependent cAMP synthesis in pancreatic and neuronal systems. J. Biol. Chem. 285, 20328-20342.
83. Zaccolo, M. and Pozzan, T. (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295, 1711-1715.
84. Zidovetzki, R. and Levitan, I. (2007). Use of cyclodextrin to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta 1768, 1311-1324