Spatiotemporally regulated protein kinase a activity is a critical regulator of growth factor-stimulated extracellular signal-regulated kinase signaling in PC12 Cells

Molecular and Cellular Biology

Volumn 31, Issue 19, 2011, Pages 4063-4075

  Herbst, Katie J ^a   Allen, Michael D ^a,b   Zhang, Jin ^a  

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

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; EPIDERMAL GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; PHOSPHODIESTERASE III;

ARTICLE; BIOSENSOR; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; ENZYME INHIBITORS; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; NERVE GROWTH FACTOR; PC12 CELLS; RATS; SIGNAL TRANSDUCTION;

EID: 80053577384     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05459-11     Document Type: Article

References (38)

1. Baillie, G. S. 2009. Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J. 276:1790-1799. doi:10.1111/j.1742-4658.2009.06926.x.
2. Bender, A. T., and J. A. Beavo. 2006. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol. Rev. 58:488-520. doi: 10.1124/pr.58.3.5.
3. Depry, C., M. D. Allen, and J. Zhang. 2011. Visualization of PKA activity in plasma membrane microdomains. Mol. Biosyst. 7:52-58. doi:10.1039/ c0mb00079e.
4. Dumaz, N., and R. Marais. 2005. Integrating signals between cAMP and the RAS/RAF/MEK/ERK signalling pathways. Based on the anniversary prize of the Gesellschaft fur Biochemie und Molekularbiologie Lecture delivered on 5 July 2003 at the Special FEBS Meeting in Brussels. FEBS J. 272:3491-3504. doi:10.1111/j.1742-4658.2005.04763.x.
5. Grewal, S. S., R. D. York, and P. J. Stork. 1999. Extracellular-signal-regulated kinase signalling in neurons. Curr. Opin. Neurobiol. 9:544-553. doi: 10.1016/S0959-4388(99)00010-0.
6. Harding, A., T. Tian, E. Westbury, E. Frische, and J. F. Hancock. 2005. Subcellular localization determines MAP kinase signal output. Curr. Biol. 15:869-873. doi:10.1016/j.cub.2005.04.020.
7. Harvey, C. D., et al. 2008. A genetically encoded fluorescent sensor of ERK activity. Proc. Natl. Acad. Sci. U. S. A. 105:19264-19269. doi:10.1073/pnas.0804598105.
8. Herbst, K. J., Q. Ni, and J. Zhang. 2009. Dynamic visualization of signal transduction in living cells: from second messengers to kinases. IUBMB Life 61:spcone. doi:10.1002/iub.259.
9. Hilborn, M. D., S. G. Rane, and J. D. Pollock. 1997. EGF in combination with depolarization or cAMP produces morphological but not physiological differentiation in PC12 cells. J. Neurosci. Res. 47:16-26.
10. Kamenetsky, M., et al. 2006. Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 362:623-639. doi: 10.1016/j.jmb.2006.07.045.
11. Kholodenko, B. N. 2007. Untangling the signalling wires. Nat. Cell Biol. 9:247-249. doi:10.1038/ncb0307-247.
12. Klussmann, E., K. Maric, B. Wiesner, M. Beyermann, and W. Rosenthal. 1999. Protein kinase A anchoring proteins are required for vasopressinmediated translocation of aquaporin-2 into cell membranes of renal principal cells. J. Biol. Chem. 274:4934-4938.
13. Lissandron, V., and M. Zaccolo. 2006. Compartmentalized cAMP/PKA signalling regulates cardiac excitation-contraction coupling. J. Muscle Res. Cell Motil. 27:399-403. doi:10.1007/s10974-006-9077-2.
14. Mark, M. D., Y. Liu, S. T. Wong, T. R. Hinds, and D. R. Storm. 1995. Stimulation of neurite outgrowth in PC12 cells by EGF and KCl depolarization: a Ca(2+)-independent phenomenon. J. Cell Biol. 130:701-710.
15. Mark, M. D., and D. R. Storm. 1997. Coupling of epidermal growth factor (EGF) with the antiproliferative activity of cAMP induces neuronal differentiation. J. Biol. Chem. 272:17238-17244.
16. Mironov, S. L., et al. 2009. Imaging cytoplasmic cAMP in mouse brainstem neurons. BMC Neurosci. 10:29. doi:10.1186/1471-2202-10-29.
17. Mochizuki, N., et al. 2001. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411:1065-1068. doi:10.1038/35082594.
18. 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. doi:10.1074/jbc.C400302200.
19. Obara, Y., K. Labudda, T. J. Dillon, and P. J. Stork. 2004. PKA phosphorylation of Src mediates Rap1 activation in NGF and cAMP signaling in PC12 cells. J. Cell Sci. 117:6085-6094. doi:10.1242/jcs.01527.
20. Orton, R. J., O. E. Sturm, A. Gormand, W. Wolch, and D. R. Gilbert. 2008. Computational modelling reveals feedback redundancy within the epidermal growth factor receptor/extracellular-signal regulated kinase signalling pathway. IET Syst. Biol. 2:173-183. doi:10.1049/iet-syb:20070066.
21. Rubinfeld, H., and R. Seger. 2005. The ERK cascade: a prototype of MAPK signaling. Mol. Biotechnol. 31:151-174. doi:10.1385/MB:31.
22. Santos, S. D., P. J. Verveer, and P. I. Bastiaens. 2007. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol. 9:324-330. doi:10.1038/ncb1543.
23. Sasagawa, S., Y. Ozaki, K. Fujita, and S. Kuroda. 2005. Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat. Cell Biol. 7:365-373. doi:10.1038/ncb1233.
24. Shelly, M., et al. 2010. Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 327:547-552. doi:10.1126/science.1179735.
25. Smith, F. D., et al. 2010. AKAP-Lbc enhances cyclic AMP control of the ERK1/2 cascade. Nat. Cell Biol. 12:1242-1249. doi:10.1038/ncb2130.
26. Stessin, A. M., et al. 2006. Soluble adenylyl cyclase mediates nerve growth factor-induced activation of Rap1. J. Biol. Chem. 281:17253-17258. doi: 10.1074/jbc.M603500200.
27. Stork, P. J. 2005. Directing NGF's actions: it's a Rap. Nat. Cell Biol. 7:338-339. doi:10.1038/ncb0405-338.
28. Stork, P. J., and J. M. Schmitt. 2002. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol. 12:258-266.
29. Szaszak, M., F. Christian, W. Rosenthal, and E. Klussmann. 2008. Compartmentalized cAMP signalling in regulated exocytic processes in nonneuronal cells. Cell. Signal. 20:590-601. doi:10.1016/j.cellsig.2007.10.020.
30. Traverse, S., N. Gomez, H. Paterson, C. Marshall, and P. Cohen. 1992. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288(Pt. 2):351-355.
31. Traverse, S., et al. 1994. EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr. Biol. 4:694-701.
32. Vaudry, D., P. J. Stork, P. Lazarovici, and L. E. Eiden. 2002. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296:1648-1649. doi:10.1126/science.1071552.
33. Wang, Z., et al. 2006. Rap1-mediated activation of extracellular signalregulated kinases by cyclic AMP is dependent on the mode of Rap1 activation. Mol. Cell. Biol. 26:2130-2145. doi:10.1128/MCB.26.6.2130-2145.2006.
34. Xu, T. R., et al. 2010. Inferring signaling pathway topologies from multiple perturbation measurements of specific biochemical species. Sci. Signal. 3:ra20.
35. Yao, H., et al. 1995. Cyclic AMP can convert epidermal growth factor into a differentiating factor in neuronal cells. J. Biol. Chem. 270:20748-20753.
36. Yao, H., R. D. York, A. Misra-Press, D. W. Carr, and P. J. Stork. 1998. The cyclic AMP-dependent protein kinase (PKA) is required for the sustained activation of mitogen-activated kinases and gene expression by nerve growth factor. J. Biol. Chem. 273:8240-8247.
37. York, R. D., et al. 1998. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622-626. doi:10.1038/33451.
38. Zaccolo, M., et al. 2005. Imaging the cAMP-dependent signal transduction pathway. Biochem. Soc. Trans. 33:1323-1326. doi:10.1042/BST20051323.