PGE1 stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: Role of compartmentalized phosphodiesterases

Journal of Cell Biology

Volumn 175, Issue 3, 2006, Pages 441-451

  Terrin, Anna ^a   Di Benedetto, Giulietta ^a   Pertegato, Vanessa ^a   Cheung, York Fong ^b   Baillie, George ^b   Lynch, Martin J ^b   Elvassore, Nicola ^c   Prinz, Anke ^d   Herberg, Friedrich W ^d   Houslay, Miles D ^b   Zaccolo, Manuela ^a  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF PADOVA   (Italy)

^d UNIVERSITY OF KASSEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; PHOSPHODIESTERASE; PHOSPHODIESTERASE IV; PROSTAGLANDIN E1;

ARTICLE; CELL MEMBRANE; CELL STIMULATION; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC MANIPULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

3',5'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASE; ALPROSTADIL; BIOSENSING TECHNIQUES; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSOL; DIFFUSION; ENZYME ACTIVATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICROSCOPY, CONFOCAL; PROTEIN SORTING SIGNALS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SECOND MESSENGER SYSTEMS; TIME FACTORS; TRANSFECTION;

EID: 33750720277     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200605050     Document Type: Article

References (50)

1. Abrahamsen, H., G. Baillie, J. Ngai, T. Vang, K. Nika, A. Ruppelt, T. Mustelin, M. Zaccolo, M. Houslay, and K. Tasken. 2004. TCR- and CD28-mediated recruitment of phosphodiesterase 4 to lipid rafts potentiates TCR signaling. J. Immunol. 173:4847-4858.
2. Bacskai, B.J., B. Hochner, M. Mahaut-Smith, S.R. Adams, B.K. Kaang, E.R. Kandel, and R.Y. Tsien. 1993. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science. 260:222-226.
3. Baillie, G.S., A. Sood, I. McPhee, I. Gall, S.J. Perry, R.J. Lefkowitz, and M.D. Houslay. 2003. beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc. Natl. Acad. Sci. USA. 100:940-945.
4. Baillie, G.S., J.D. Scott, and M.D. Houslay. 2005. Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett. 579:3264-3270.
5. Barnes, A.P., G. Livera, P. Huang, C. Sun, W.K. O'Neal, M. Conti, M.J. Stutts, and S.L. Milgram. 2005. Phosphodiesterase 4D forms a cAMP diffusion barrier at the apical membrane of the airway epithelium. J. Biol. Chem. 280:7997-8003.
6. Beavo, J.A., and L.L. Brunton. 2002. Cyclic nucleotide research-still expanding after half a century. Nat. Rev. Mol. Cell Biol. 3:710-718.
7. Biel, M., X. Zong, A. Ludwig, A. Sautter, and F. Hofmann. 1999. Structure and function of cyclic nucleotide-gated channels. Rev. Physiol. Biochem. Pharmacol. 135:151-171.
8. Bos, J.L. 2003. Epac: a new cAMP target and new avenues in cAMP research. Nat. Rev. Mol. Cell Biol. 4:733-738.
9. Brunton, L.L. 2003. PDE4: arrested at the border. Sci. STKE. doi:10.1126/stke.2003.204.pe44.
10. Buxton, I.L., and L.L. Brunton. 1983. Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J. Biol. Chem. 258:10233-10239.
11. Cook, P.F., M.E. Neville Jr., K.E. Vrana, F.T. Hartl, and R. Roskoski Jr. 1982. Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit. Biochemistry. 21:5794-5799.
12. Cooper, D.M. 2003. Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 375:517-529.
13. Cooper, D.M. 2005. Compartmentalization of adenylate cyclase and cAMP signalling. Biochem. Soc. Trans. 33:1319-1322.
14. Davare, M.A., V. Avdonin, D.D. Hall, E.M. Peden, A. Burette, R.J. Weinberg, M.C. Horne, T. Hoshi, and J.W. Hell. 2001. A beta2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2. Science. 293:98-101.
15. DiPilato, L.M., X. Cheng, and J. Zhang. 2004. Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signalling within discrete subcellular compartments. Proc. Natl. Acad. Sci. USA. 101:16513-16518.
16. Dodge, K.L., S. Khouangsathiene, M.S. Kapiloff, R. Mouton, E.V. Hill, M.D. Houslay, L.K. Langeberg, and J.D. Scott. 2001. mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J. 20:1921-1930.
17. Dodge-Kafka, K.L., J. Soughayer, G.C. Pare, J.J. Carlisle Michel, L.K. Langeberg, M.S. Kapiloff, and J.D. Scott. 2005. The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature. 437:574-578.
18. Francis, S.H., I.V. Turko, and J.D. Corbin. 2001. Cyclic nucleotide phosphodiesterases: relating structure and function. Prog. Nucleic Acid Res. Mol. Biol. 65:1-52.
19. Herberg, F.W., S.M. Bell, and S.S. Taylor. 1993. Expression of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli: multiple isozymes reflect different phosphorylation states. Protein Eng. 6:771-777.
20. Houslay, M.D., and G. Milligan. 1997. Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem. Sci. 22:217-224.
21. Houslay, M.D., and D.R. Adams. 2003. PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem. J. 370:1-18.
22. Jurevicius, J., and R. Fischmeister. 1996. cAMP compartmentation is responsible for a local activation of cardiac Ca2+ channels by beta-adrenergic agonists. Proc. Natl. Acad. Sci. USA. 93:295-299.
23. Jurevicius, J., V.A. Skeberdis, and R. Fischmeister. 2003. Role of cyclic nucleotide phosphodiesterase isoforms in cAMP compartmentation following beta2-adrenergic stimulation of ICa,L in frog ventricular myocytes. J. Physiol. 551:239-252.
24. Lissandron, V., A. Terrin, M. Collini, L. D'Alfonso, G. Chirico, S. Pantano, and M. Zaccolo. 2005. Improvement of a FRET-based indicator for cAMP by linker design and stabilization of donor-acceptor interaction. J. Mol. Biol. 354:546-555.
25. Lugnier, C. 2006. Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol. Ther. 109:366-398.
26. Lynch, M.J., G.S. Baillie, A. Mohamed, X. Li, C. Maisonneuve, E. Klussmann, G. van Heeke, and M.D. Houslay. 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.
27. MacKenzie, S.J., and M.D. Houslay. 2000. 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. 347:571-578.
28. MacKenzie, S.J., G.S. Baillie, I. McPhee, C. MacKenzie, R. Seamons, T. McSorley, J. Millen, M.B. Beard, G. van Heeke, and M.D. Houslay. 2002. Long PDE4 cAMP specific phosphodiesterases are activated by protein kinase A-mediated phosphorylation of a single serine residue in Upstream Conserved Region 1 (UCR1). Br. J. Pharmacol. 136:421-433.
29. Manganiello, V.C., and E. Degerman. 1999. Cyclic nucleotide phosphodiesterases (PDEs): diverse regulators of cyclic nucleotide signals and inviting molecular targets for novel therapeutic agents. Thromb. Haemost. 82:407-411.
30. Mongillo, M., T. McSorley, S. Evellin, A. Sood, V. Lissandron, A. Terrin, E. Huston, A. Hannawacker, M.J. Lohse, T. Pozzan, et al. 2004. Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases. Circ. Res. 95:67-75.
31. Mongillo, M., C.G. Tocchetti, A. Terrin, V. Lissandron, Y.F. Cheung, W.R. Dostmann, T. Pozzan, D.A. Kass, N. Paolocci, M.D. Houslay, and M. Zaccolo. 2006. Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ. Res. 98:226-234.
32. Nikolaev, V.O., M. Bunemann, L. Hein, A. Hannawacker, and M.J. Lohse. 2004. Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279:37215-37218.
33. Perry, S.J., G.S. Baillie, T.A. Kohout, I. McPhee, M.M. Magiera, K.L. Ang, W.E. Miller, A.J. McLean, M. Conti, M.D. Houslay, and R.J. Lefkowitz. 2002. Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science. 298:834-836.
34. Ponsioen, B., J. Zhao, J. Riedl, F. Zwartkruis, G. van der Krogt, M. Zaccolo, W.H. Moolenaar, J.L. Bos, and K. Jalink. 2004. Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 5:1176-1180.
35. Resh, M.D. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta. 1451:1-16.
36. Rich, T.C., K.A. Fagan, H. Nakata, J. Schaack, D.M. Cooper, and J.W. Karpen. 2000. Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J. Gen. Physiol. 116:147-161.
37. Rich, T.C., K.A. Fagan, T.E. Tse, J. Schaack, D.M. Cooper, and J.W. Karpen. 2001. A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc. Natl. Acad. Sci. USA. 98:13049-13054.
38. Rochais, F., G. Vandecasteele, F. Lefebvre, C. Lugnier, H. Lum, J.L. Mazet, D.M. Cooper, and R. Fischmeister. 2004. Negative feedback exerted by cAMP-dependent protein kinase and cAMP phosphodiesterase on subsarcolemmal cAMP signals in intact cardiac myocytes: an in vivo study using adenovirus-mediated expression of CNG channels. J. Biol. Chem. 279:52095-52105.
39. Romoser, V., R. Ball, and A.V. Smrcka. 1996. Phospholipase C beta2 association with phospholipid interfaces assessed by fluorescence resonance energy transfer. G protein betagamma subunit-mediated translocation is not required for enzyme activation. J. Biol. Chem. 271:25071-25078.
40. Slice, L.W., and S.S. Taylor. 1989. Expression of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli. J. Biol. Chem. 264:20940-20946.
41. Smith, K.J., G. Scotland, J. Beattie, I.P. Trayer, and M.D. Houslay. 1996. Determination of the structure of the N-terminal splice region of the cyclic AMP-specific phosphodiesterase RD1 (RNPDE4A1) by 1H NMR and identification of the membrane association domain using chimeric constructs. J. Biol. Chem. 271:16703-16711.
42. Soderling, S.H., and J.A. Beavo. 2000. Regulation of cAMP and cGMP signaling: new phosphodiesterases and new functions. Curr. Opin. Cell Biol. 12:174-179.
43. Tasken, K., and E.M. Aandahl. 2004. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84:137-167.
44. Willoughby, D., W. Wong, J. Schaack, J.D. Scott, and D.M. Cooper. 2006. An anchored PKA and PDE4 complex regulates subplasmalemmal cAMP dynamics. EMBO J. 25:2051-2061.
45. Witczak, O., B.S. Skalhegg, G. Keryer, M. Bornens, K. Tasken, T. Jahnsen, and S. Orstavik. 1999. Cloning and characterization of a cDNA encoding an A-kinase anchoring protein located in the centrosome, AKAP450. EMBO J. 18:1858-1868.
46. Wong, W., and J.D. Scott. 2004. AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5:959-970.
47. Zaccolo, M., and T. Pozzan. 2002. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science. 295:1711-1715.
48. Zaccolo, M., F. De Giorgi, C.Y. Cho, L. Feng, T. Knapp, P.A. Negulescu, S.S. Taylor, R.Y. Tsien, and T. Pozzan. 2000. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat. Cell Biol. 2:25-29.
49. Zaccolo, M., P. Magalhaes, and T. Pozzan. 2002. Compartmentalisation of cAMP and Ca(2+) signals. Curr. Opin. Cell Biol. 14:160-166.
50. Zippin, J.H., Y. Chen, P. Nahirney, M. Kamenetsky, M.S. Wuttke, D.A. Fischman, L.R. Levin, and J. Buck. 2003. Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J. 17:82-84.