A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C

Journal of Cell Biology

Volumn 161, Issue 5, 2003, Pages 899-909

  Violin, Jonathan D ^a   Zhang, Jin ^a   Tsien, Roger Y ^a   Newton, Alexandra C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NONE   (United States)

Author keywords

Calcium; Fluorescence resonance energy transfer; Oscillation; Phosphatase; PKC

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CALCIUM ION; DIACYLGLYCEROL; HISTAMINE; INOSITOL TRISPHOSPHATE; PHOSPHATASE; PHOSPHOLIPASE C; PHOSPHOTRANSFERASE; PROTEIN KINASE C; TRIPHOSPHOINOSITIDE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL STRAIN; CORRELATION ANALYSIS; DIAGNOSTIC IMAGING; ENERGY TRANSFER; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC CODE; HELA CELL; MAMMAL; MEMBRANE STRUCTURE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPORTER GENE; SECOND MESSENGER; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL CLOCKS; CALCIUM SIGNALING; CELL MEMBRANE; DIGLYCERIDES; DOGS; EUKARYOTIC CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GENES, REPORTER; HELA CELLS; HISTAMINE; HUMANS; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPASE C; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN TRANSPORT; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA;

EID: 0037780971     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200302125     Document Type: Article

References (52)

1. Brown, G.C., and B.N. Kholodenko. 1999. Spatial gradients of cellular phosphoproteins. FEBS Lett. 457:452-454.
2. Codazzi, F., M.N. Teruel, and T. Meyer. 2001. Control of astrocyte Ca(2+) oscillations and waves by oscillating translocation and activation of protein kinase C. Curr. Biol. 11:1089-1097.
3. Coghlan, V.M., B.A. Perrino, M. Howard, L.K. Langeberg, J.B. Hicks, W.M. Gallatin, and J.D. Scott. 1995. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science. 267:108-111.
4. De Koninck, P., and H. Schulman. 1998. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science. 279:227-230.
5. Dolmetsch, R.E., K. Xu, and R.S. Lewis. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature. 392:933-936.
6. Durocher, D., I.A. Taylor, D. Sarbassova, L.F. Haire, S.L. Westcott, S.P. Jackson, S.J. Smerdon, and M.B. Yaffe. 2000. The molecular basis of FHA domain: phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol. Cell 6:1169-1182.
7. Gijon, M.A., D.M. Spencer, A.L. Kaiser, and C.C. Leslie. 1999. Role of phosphotylation sites and the C2 domain in regulation of cytosolic phospholipase A2. J. Cell Biol. 145:1219-1232.
8. Gray, A., J. Van Der Kaay, and C.P. Downes. 1999. The pleckstrin homology domains of protein kinase B and GRP1 (general receptor for phosphoinositides-1) are sensitive and selective probes for the cellular detection of phosphatidylinositol 3,4-bisphosphate and/or phosphatidylinositol 3,4,5-trisphosphate in vivo. Biochem. J. 344(Pt 3):929-936.
9. Griesbeck, O., G.S. Baird, R.E. Campbell, D.A. Zacharias, and R.Y. Tsien. 2001. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276:29188-29194.
10. Harootunian, A.T., J.P. Kao, S. Paranjape, and R.Y. Tsien. 1991. Generation of calcium oscillations in fibroblasts by positive feedback between calcium and IP3. Science. 251:75-78.
11. Hirose, K., S. Kadowaki, M. Tanabe, H. Takeshima, and M. Iino. 1999. Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns. Science. 284:1527-1530.
12. Jaken, S., and P.J. Parker. 2000. Protein kinase C binding partners. Bioessays. 22: 245-254.
13. Johnson, J.E., J. Giorgione, and A.C. Newton. 2000. The C1 and C2 domains of protein kinase C are independent membrane targeting modules, with specificity for phosphatidylserine conferred by the C1 domain. Biochemistry. 39: 11360-11369.
14. Kajimoto, T., S. Ohmori, Y. Shirai, N. Sakai, and N. Saito. 2001. Subtype-specific translocation of the delta subtype of protein kinase C and its activation by tyrosine phosphotylation induced by ceramide in HeLa cells. Mol. Cell Biol. 21:1769-1783.
15. Kozak, M. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125-8148.
16. Kraft, A.S., and W.B. Anderson. 1983. Phorbol esters increase the amount of Ca2+, phospholipid-dependent protein kinase associated with plasma membrane. Nature. 301:621-623.
17. Kraft, A.S., W.B. Anderson, H.L. Cooper, and J.J. Sando. 1982. Decrease in cytosolic calcium/phospholipid-dependent protein kinase activity following phorbol ester treatment of EL4 thymoma cells. J. Biol. Chem. 257:13193-13196.
18. Li, W., J. Llopis, M. Whitney, G. Zlokarnik, and R.Y. Tsien. 1998. Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature. 392:936-941.
19. Llopis, J., J.M. McCaffety, A. Miyawaki, M.G. Farquhar, and R.Y. Tsien. 1998. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. USA. 95:6803-6808.
20. Mellor, H., and P.J. Parker. 1998. The extended protein kinase C superfamily. Biochem. J. 332(Pt 2):281-292.
21. Miyawaki, A., and R.Y. Tsien. 2000. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 327:472-500.
22. Mochly-Rosen, D. 1995. Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science. 268:247-251.
23. Nagai, T., A. Sawano, E.S. Park, and A. Miyawaki. 2001. Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc. Natl. Acad. Sci. USA. 98:3197-3202.
24. Nalefski, E.A., and A.C. Newton. 2001. Membrane binding kinetics of protein kinase C beraII mediated by the C2 domain. Biochemistry. 40:13216-13229.
25. Nash, M.S., K.W. Young, R.A. Challiss, and S.R. Nahorski. 2001. Intracellular signalling. Receptor-specific messenger oscillations. Nature. 413:381-382.
26. Newton, A.C. 2001. Protein kinase C: structural and spatial regulation by phosphotyladon, cofactors, and macromolecular interactions. Chem. Rev. 101: 2353-2364.
27. Newton, A.C. 2002a. Analyzing protein kinase C activation. Methods Enzymol. 345:499-506.
28. Newton, A.C. 2002b. Regulation of the ABC kinases by phosphotylation: protein kinase C as a paradigm. Biochem J. 370(Pt 2):361-371.
29. Newton, A.C., and L.M. Keranen. 1994. Phosphaddyl-L-serine is necessaty for protein kinase C's high-affinity interaction with diacylglycerol-containing membranes. Biochemistry. 33:6651-6658.
30. Nishikawa, K., A. Toker, F.J. Johannes, Z. Songyang, and L.C. Candey. 1997. Determination of the specific substrate sequence motifs of protein kinase C isozymes. J. Biol. Chem. 272:952-960.
31. Nishizuka, Y. 1984. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 308:693-698.
32. Nishizuka, Y. 1995. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9:484-496.
33. Oancea, E., and T. Meyer. 1998. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell. 95:307-318.
34. Oancea, E., M.N. Teruel, A.F. Quest, and T. Meyer. 1998. Green fluorescent protein (GFP)-tagged cysreine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J. Cell Biol. 140: 485-498.
35. Orr, J.W., and A.C. Newton. 1992. Interaction of protein kinase C with phosphatidylserine. 1. Cooperativity in lipid binding. Biochemistry. 31:4661-4667.
36. Sakai, N., K. Sasaki, N. Ikegaki, Y. Shirai, Y. Ono, and N. Saito. 1997. Direct visualization of the translocadon of the gamma-subspecies of protein kinase C in living cells using fusion proteins with green fluorescent protein. J. Cell Biol. 139:1465-1476.
37. Sato, M., T. Ozawa, K. Inukai, T. Asano, and Y. Umezawa. 2002. Fluorescent indicators for imaging protein phosphotyladon in single living cells. Nat. Biotechnol. 20:287-294.
38. Sauve, R., A. Diarra, M. Chahine, C. Simoneau, N. Morier, and G. Roy. 1991. Ca2+ oscillations induced by histamine H1 receptor stimulation in HeLa cells: Fura-2 and patch clamp analysis. Cell Calcium. 12:165-176.
39. Shirai, Y., K. Kashiwagi, K. Yagi, N. Sakai, and N. Saito. 1998a. Distinct effects of fatty acids on translocation of gamma- and epsilon-subspecles of protein kinase C. J. Cell Biol. 143:511-521.
40. Shirai, Y., N. Sakai, and N. Saito. 1998b. Subspecies-specific targeting mechanism of protein kinase C. Jpn. J. Pharmacol. 78:411-417.
41. Songyang, Z., S. Blechner, N. Hoagland, M.F. Hoekstra, H. Piwnica-Worms, and L.C. Candey. 1994. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4:973-982.
42. Tanimura, A., A. Nezu, T. Morita, N. Hashimoto, and Y. Tojyo. 2002. Interplay between calcium, diacylglycerol, and phosphotyladon in the spatial and temporal regulation of PKCalpha-GFP. J. Biol. Chem. 277:29054-29062.
43. Thomas, A.P., G.S. Bird, G. Hajnoczky, L.D. Robb-Gaspers, and J.W. Putney, Jr. 1996. Spatial and temporal aspects of cellular calcium signaling. FASEB J. 10:1505-1517.
44. Ting, A.Y., K.H. Kain, R.L. Klemke, and R.Y. Tsien. 2001. Genetically encoded fluorescent reporters of protein tyroslne kinase activities in living cells. Proc. Natl. Acad. Sci. USA. 98:15003-15008.
45. Tsien, R.Y. 1989. Fluorescent indicators of ion concentrations. Methods Cell Biol. 30:127-156.
46. van der Wal, J., R. Habets, P. Varnai, T. Balla, and K. Jalink. 2001. Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. J. Biol. Chem. 276:15337-15344.
47. Wang, J., A. Gambhir, G. Hangyas-Mihalyne, D. Murray, U. Golebiewska, and S. McLaughlin. 2002. Lateral sequestration of phosphaddylinosirol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase subsrrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 277:34401-34412.
48. Wesrphal, R.S., K.A. Anderson, A.R. Means, and B.E. Wadzinski. 1998. A signaling complex of Ca2+-calmodulin-dependent protein kinase IV and protein phospharase 2A. Science. 280:1258-1261.
49. Yaffe, M.B., K. Ritringer, S. Volinia, P.R. Caron, A. Airken, H. Leffers, S.J. Gamblin, S.J. Smerdon, and L.C. Candey. 1997. The structural basis for 14-3-3: phosphopeptide binding specificity. Cell. 91:961-971.
50. Yaffe, M.B., G.G. Leparc, J. Lal, T. Obata, S. Volinia, and L.C. Cantley. 2001. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19:348-353.
51. Zacharias, D.A., J.D. Violin, A.C. Newton, and R.Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296:913-916.
52. Zhang, J., Y. Ma, S.S. Taylor, and R.Y. Tsien. 2001. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl. Acad. Sci. USA. 98:14997-15002.