Regulation of nuclear PKA revealed by spatiotemporal manipulation of cyclic AMP

Nature Chemical Biology

Volumn 8, Issue 4, 2012, Pages 375-382

  Sample, Vedangi ^a   Dipilato, Lisa M ^a   Yang, Jason H ^b   Ni, Qiang ^a   Saucerman, Jeffrey J ^b   Zhang, Jin ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Virginia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; BICARBONATE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; PHOSPHODIESTERASE; PHOSPHOTRANSFERASE;

ARTICLE; BIOMANIPULATION; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CELL SHAPE; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME MODIFICATION; FLUORESCENCE; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPATIOTEMPORAL MANIPULATION;

EID: 84862806070     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.799     Document Type: Article

References (42)

1. Taskén, K. & Aandahl, E.M. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84, 137-167 (2004). (Pubitemid 38049878)
2. Steinberg, S.F. & Brunton, L.L. Compartmentation of G protein-coupled signaling pathways in cardiac myocytes. Annu. Rev. Pharmacol. Toxicol. 41, 751-773 (2001). (Pubitemid 32385905)
3. Houslay, M.D. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem. Sci. 35, 91-100 (2010).
4. Carnegie, G.K., Means, C.K. & Scott, J.D. A-kinase anchoring proteins: from protein complexes to physiology and disease. IUBMB Life 61, 394-406 (2009).
5. Altarejos, J.Y. & Montminy, M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 12, 141-151 (2011).
6. Kvissel, A.K. et al. Involvement of the catalytic subunit of protein kinase A and of HA95 in pre-mRNA splicing. Exp. Cell Res. 313, 2795-2809 (2007).
7. Martin, B.R., Deerinck, T.J., Ellisman, M.H., Taylor, S.S. & Tsien, R.Y. Isoform-specific PKA dynamics revealed by dye-triggered aggregation and DAKAP1alpha-mediated localization in living cells. Chem. Biol. 14, 1031-1042 (2007). (Pubitemid 47404903)
8. Harootunian, A.T. et al. Movement of the free catalytic subunit of cAMP-dependent protein kinase into and out of the nucleus can be explained by diffusion. Mol. Biol. Cell 4, 993-1002 (1993). (Pubitemid 23331539)
9. Mayr, B. & Montminy, M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609 (2001). (Pubitemid 33674011)
10. Meoli, E. et al. Protein kinase A effects of an expressed PRKAR1A mutation associated with aggressive tumors. Cancer Res. 68, 3133-3141 (2008).
11. Zippin, J.H. et al. Bicarbonate-responsive "soluble" adenylyl cyclase defines a nuclear cAMP microdomain. J. Cell Biol. 164, 527-534 (2004). (Pubitemid 38233314)
12. Jarnaess, E. et al. Splicing factor arginine/serine-rich 17A (SFRS17A) is an A-kinase anchoring protein that targets protein kinase A to splicing factor compartments. J. Biol. Chem. 284, 35154-35164 (2009).
13. Steegborn, C., Litvin, T.N., Levin, L.R., Buck, J. & Wu, H. Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat. Struct. Mol. Biol. 12, 32-37 (2005). (Pubitemid 40082914)
14. Chen, Y. et al. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289, 625-628 (2000). (Pubitemid 30622067)
15. Buck, J., Sinclair, M.L., Schapal, L., Cann, M.J. & Levin, L.R. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc. Natl. Acad. Sci. USA 96, 79-84 (1999). (Pubitemid 29036056)
16. DiPilato, L.M. & Zhang, J. The role of membrane microdomains in shaping β2-adrenergic receptor-mediated cAMP dynamics. Mol. Biosyst. 5, 832-837 (2009).
17. 2+-cAMP-PKA oscillatory circuit. Nat. Chem. Biol. 7, 34-40 (2011).
18. Terrin, A. et al. PGE1 stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J. Cell Biol. 175, 441-451 (2006). (Pubitemid 44708068)
19. DiPilato, L.M., Cheng, X. & Zhang, J. 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 (2004). (Pubitemid 39557744)
20. Allen, M.D. & Zhang, J. Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem. Biophys. Res. Commun. 348, 716-721 (2006). (Pubitemid 44188622)
21. Hagiwara, M. et al. Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol. Cell. Biol. 13, 4852-4859 (1993). (Pubitemid 23220391)
22. Burnham, K.P. & Anderson, D.R. Model Selection and Multi-Model Inference: Practical Information-Theoretic Approach Ch. 2, 49-97 (Springer, 2002).
23. Sugiura, N. Further analysis of data by Akaike's information criterion and finite corrections. Commun. Statist. 7, 13-26 (1978).
24. Shimojo, M., Paquette, A.J., Anderson, D.J. & Hersh, L.B. Protein kinase A regulates cholinergic gene expression in PC12 cells: REST4 silences the silencing activity of neuron-restrictive silencer factor/REST. Mol. Cell. Biol. 19, 6788-6795 (1999). (Pubitemid 29441862)
25. Lynch, M.J. et al. RNA silencing identifies PDE4D5 as the functionally relevant cAMP phosphodiesterase interacting with β arrestin to control the protein kinase A/AKAP79-mediated switching of the β2-adrenergic receptor to activation of ERK in HEK293B2 cells. J. Biol. Chem. 280, 33178-33189 (2005). (Pubitemid 41397113)
26. McCahill, A. et al. In resting COS1 cells a dominant negative approach shows that specific, anchored PDE4 cAMP phosphodiesterase isoforms gate the activation, by basal cyclic AMP production, of AKAP-tethered protein kinase A type II located in the centrosomal region. Cell. Signal. 17, 1158-1173 (2005). (Pubitemid 40933535)
27. de Rooij, J. et al. Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J. Biol. Chem. 275, 20829-20836 (2000). (Pubitemid 30457676)
28. Beavo, J.A., Bechtel, P.J. & Krebs, E.G. Activation of protein kinase by physiological concentrations of cyclic AMP. Proc. Natl. Acad. Sci. USA 71, 3580-3583 (1974).
29. Wong, W. & Scott, J.D. AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5, 959-970 (2004). (Pubitemid 39611533)
30. Dodge-Kafka, K.L. et al. The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437, 574-578 (2005). (Pubitemid 41613557)
31. Michel, J.J. & Scott, J.D. AKAP mediated signal transduction. Annu. Rev. Pharmacol. Toxicol. 42, 235-257 (2002). (Pubitemid 34160527)
32. Ellis-Davies, G.C. Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nat. Methods 4, 619-628 (2007). (Pubitemid 47202471)
33. Stierl, M. et al. Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J. Biol. Chem. 286, 1181-1188 (2011).
34. Schröder-Lang, S. et al. Fast manipulation of cellular cAMP level by light in vivo. Nat. Methods 4, 39-42 (2007). (Pubitemid 46029473)
35. Kholodenko, B.N., Hancock, J.F. & Kolch, W. Signalling ballet in space and time. Nat. Rev. Mol. Cell Biol. 11, 414-426 (2010).
36. Chuang, H.Y., Hofree, M. & Ideker, T. A decade of systems biology. Annu. Rev. Cell Dev. Biol. 26, 721-744 (2010).
37. Tay, S. et al. Single-cell NF-?B dynamics reveal digital activation and analogue information processing. Nature 466, 267-271 (2010).
38. Paliwal, S. et al. MAPK-mediated bimodal gene expression and adaptive gradient sensing in yeast. Nature 446, 46-51 (2007). (Pubitemid 46348042)
39. Rich, T.C. et al. Cellular mechanisms underlying prostaglandin-induced transient cAMP signals near the plasma membrane of HEK-293 cells. Am. J. Physiol. Cell Physiol. 292, C319-C331 (2007). (Pubitemid 46115141)
40. Xin, W., Tran, T.M., Richter, W., Clark, R.B. & Rich, T.C. Roles of GRK and PDE4 activities in the regulation of β2 adrenergic signaling. J. Gen. Physiol. 131, 349-364 (2008). (Pubitemid 351482774)
41. Saucerman, J.J. et al. Systems analysis of PKA-mediated phosphorylation gradients in live cardiac myocytes. Proc. Natl. Acad. Sci. USA 103, 12923-12928 (2006). (Pubitemid 44298662)
42. Greenberg, M.E. & Bender, T.P. Identification of newly transcribed RNA. Curr. Protoc. Mol. Biol. 4, 4.10 (2007).