Bicarbonate-responsive "soluble" adenylyl cyclase defines a nuclear cAMP microdomain

Journal of Cell Biology

Volumn 164, Issue 4, 2004, Pages 527-534

  Zippin, Jonathan H ^a   Farrell, Jeanne ^a   Huron, David ^a   Kamenetsky, Margarita ^a   Hess, Kenneth C ^a   Fischman, Donald A ^b   Levin, Lonny R ^a,b   Buck, Jochen ^a  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Compartmentalization; CREB; Gene expression; PKA; Signal transduction

Indexed keywords

ADENYLATE CYCLASE; BICARBONATE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL STRAIN COS7; CONTROLLED STUDY; ENZYME ACTIVATION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SECOND MESSENGER; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADENYLATE CYCLASE; ANIMALS; BICARBONATES; CELL LINE; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; IMMUNOHISTOCHEMISTRY; PHOSPHORYLATION; RATS; SECOND MESSENGER SYSTEMS;

ANIMALIA; MAMMALIA;

EID: 1242285150     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200311119     Document Type: Article

References (38)

1. Alto, N., J.J. Carlisle Michel, K.L. Dodge, L.K. Langeberg, and J.D. Scott. 2002. Intracellular targeting of protein kinases and phosphatases. Diabetes. 51(3): S385-S388.
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. Bailey, C.H., D. Bartsch, and E.R. Kandel. 1996. Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. USA. 93:13445-13452.
4. Bevensee, M.O., S.L. Alper, P.S. Aronson, and W.F. Boron. 2000. Control of intracellular pH. In The Kidney. Vol. I. D.W. Seldin and G. Giebisch, editors. Lippincott Williams & Wilkins, Philadelphia, PA. 391-442.
5. Buck, J., M.L. Sinclair, L. Schapal, M.J. Cann, and L.R. Levin. 1999. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc. Natl. Acad. Sci. USA. 96:79-84.
6. Byus, C.V., and W.H. Fletcher. 1982. Direct cytochemical localization of catalytic subunits dissociated from cAMP-dependent protein kinase in Reuber H-35 hepatoma cells. II. Temporal and spatial kinetics. J. Cell Biol. 93:727-734.
7. Chen, Y., M.J. Cann, T.N. Litvin, V. Iourgenko, M.L. Sinclair, L.R. Levin, and J. Buck. 2000. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science. 289:625-628.
8. Constantinescu, A., I. Diamond, and A.S. Gordon. 1999. Ethanol-induced translocation of cAMP-dependent protein kinase to the nucleus. Mechanism and functional consequences. J. Biol. Chem. 274:26985-26991.
9. Daniel, P.B., W.H. Walker, and J.F. Habener. 1998. Cyclic AMP signaling and gene regulation. Annu. Rev. Nutr. 18:353-383.
10. 2+ channel Cav1.2. Science. 293:98-101.
11. De Cesare, D., and P. Sassone-Corsi. 2000. Transcriptional regulation by cyclic AMP-responsive factors. Prog. Nucleic Acid Res. Mol. Biol. 64:343-369.
12. Griffioen, G., P. Anghileri, E. Imre, M.D. Baroni, and H. Ruis. 2000. Nutritional control of nucleocytoplasmic localization of cAMP-dependent protein kinase catalytic and regulatory subunits in Saccharomyces cerevisiae. J. Biol. Chem. 275:1449-1456.
13. Hagiwara, M., A. Alberts, P. Brindle, J. Meinkoth, J. Feramisco, T. Deng, M. Karin, S. Shenolikar, and M. Montminy. 1992. Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell. 70:105-113.
14. Hagiwara, M., P. Brindle, A. Harootunian, R. Armstrong, J. Rivier, W. Vale, R. Tsien, and M.R. Montminy. 1993. 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.
15. Hanoune, J., and N. Defer. 2001. Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 41:145-174.
16. Jaiswal, B.S., and M. Conti. 2003. Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc. Natl. Acad. Sci. USA. 100:10676-10681.
17. Jungmann, R.A., M.R. Kuettel, S.P. Squinto, and J. Kwast-Welfeld. 1988. Using immunocolloidal gold electron microscopy to investigate cAMP-dependent protein kinase cellular compartmentalization. Methods Enzymol. 159:225-235.
18. Kuettel, M.R., S.P. Squinto, J. Kwast-Welfeld, G. Schwoch, J.S. Schweppe, and R.A. Jungmann. 1985. Localization of nuclear subunits of cyclic AMP-dependent protein kinase by the immunocolloidal gold method. J. Cell Biol. 101:965-975.
19. Litvin, T.N., M. Kamenetsky, A. Zarifyan, J. Buck, and L.R. Levin. 2003. Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J. Biol. Chem. 278:15922-15926.
20. Michel, J.J., and J.D. Scott. 2002. AKAP mediated signal transduction. Annu. Rev. Pharmacol. Toxicol. 42:235-257.
21. Murray, S.A., C.V. Byus, and W.H. Fletcher. 1985. Intracellular kinetics of free catalytic units dissociated from adenosine 3′,5′ -monophosphate-dependent protein kinase in adrenocortical tumor cells (Y-1). Endocrinology. 116:364-374.
22. Pastor-Soler, N., V. Beaulieu, T.N. Litvin, N. Da Silva, Y. Chen, D. Brown, J. Buck, L.R. Levin, and S. Breton. 2003. Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J. Biol. Chem. 278:49523-49529.
23. Qiao, J., F.C. Mei, V.L. Popov, L.A. Vergara, and X. Cheng. 2002. Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP. J. Biol. Chem. 277:26581-26586.
24. Riabowol, K.T., J.S. Fink, M.Z. Gilman, D.A. Walsh, R.H. Goodman, and J.R. Feramisco. 1988a. The catalytic subunit of cAMP-dependent protein kinase induces expression of genes containing cAMP-responsive enhancer elements. Nature. 336:83-86.
25. Riabowol, K.T., M.Z. Gilman, and J.R. Feramisco. 1988b. Microinjection of the catalytic subunit of cAMP-dependent protein kinase induces expression of the c-fos gene. Cold Spring Harb. Symp. Quant. Biol. 53:85-90.
26. 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.
27. 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.
28. Sinclair, M.L., X.Y. Wang, M. Mattia, M. Conti, J. Buck, D.J. Wolgemuth, and L.R. Levin. 2000. Specific expression of soluble adenylyl cyclase in male germ cells. Mol. Reprod. Dev. 56:6-11.
29. Singh, L.P., J. Andy, V. Anyamale, K. Greene, M. Alexander, and E.D. Crook. 2001. Hexosamine-induced fibronectin protein synthesis in mesangial cells is associated with increases in cAMP responsive element binding (CREB) phosphorylation and nuclear CREB: the involvement of protein kinases A and C. Diabetes. 50:2355-2362.
30. Spector, D.L., R.D. Goldman, and L.A. Leinwand, editors. 1998. Culture and Biochemical Analysis of Cells. Vol. 1 of Cells: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Trumper, A., K. Trumper, and D. Horsch. 2002. Mechanisms of mitogenic and anti-apoptotic signaling by glucose-dependent insulinotropic polypeptide in beta(INS-1)-cells. J. Endocrinol. 174:233-246.
32. Wuttke, M.S., J. Buck, and L.R. Levin. 2001. Bicarbonate-regulated soluble adenylyl cyclase. JOP. 2:154-158.
33. Yan, S.Z., and W.J. Tang. 2002. Construction of soluble adenylyl cyclase from human membrane-bound type 7 adenylyl cyclase. Methods Enzymol. 345:231-241.
34. Yang, J., J.A. Drazba, D.G. Ferguson, and M. Bond. 1998. A-kinase anchoring protein 100 (AKAP100) is localized in multiple subcellular compartments in the adult rat heart. J. Cell Biol. 142:511-522.
35. Zaccolo, M., and T. Pozzan. 2002. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science. 295:1711-1715.
36. Zhang, Q., D.W. Carr, K.M. Lerea, J.D. Scott, and S.A. Newman. 1996. Nuclear localization of type II cAMP-dependent protein kinase during limb cartilage differentiation is associated with a novel developmentally regulated A-kinase anchoring protein. Dev. Biol. 176:51-61.
37. Zippin, J.H., L.R. Levin, and J. Buck. 2001. CO(2)/HCO(3)(-)-responsive soluble adenylyl cyclase as a putative metabolic sensor. Trends Endocrinol. Metab. 12:366-370.
38. 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.