The NO/cGMP pathway inhibits transient cAMP signals through the activation of PDE2 in striatal neurons

Frontiers in Cellular Neuroscience

Volumn 6, Issue NOV, 2013, Pages

  Polito, Marina ^a,b   Klarenbeek, Jeffrey ^c   Jalink, Kees ^c   Paupardin Tritsch, Daniele ^a,b   Vincent, Pierre ^a,b   Castro, Liliana R V ^a,b  

^a CNRS   (France)

^b Université Pierre et Marie Curie   (France)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Biosensor imaging; cyclic AMP; cyclic GMP; Dopamine; Nitric oxide; Phosphodiesterase; Striatum

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; FORSKOLIN; NITRIC OXIDE; SPLEEN EXONUCLEASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BIOSENSOR; BRAIN NERVE CELL; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC TRANSMISSION; ENZYME ACTIVATION; FLUORESCENCE ANALYSIS; GENETIC CODE; GLOBUS PALLIDUS; INTRACELLULAR SIGNALING; MALE; MOUSE; NEUROMODULATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN;

EID: 84888193790     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00211     Document Type: Article

References (54)

1. Ariano, M. A., Lewicki, J. A., Brandwein, H. J., and Murad, F. (1982). Immunohistochemical localization of guanylate cyclase within neurons of rat brain. Proc. Natl. Acad. Sci. U.S.A. 79, 1316-1320. doi: 10.1073/pnas.79.4.1316
2. Bateup, H. S., Svenningsson, P., Kuroiwa, M., Gong, S., Nishi, A., Heintz, N., et al. (2008). Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat. Neurosci. 11, 932-939. doi: 10.1038/nn.2153
3. Bertran-Gonzalez, J., Bosch, C., Maroteaux, M., Matamales, M., Herve, D., Valjent, E., et al. (2008). Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J. Neurosci. 28, 5671-5685. doi: 10.1523/JNEUROSCI.1039- 08.2008
4. Borner, S., Schwede, F., Schlipp, A., Berisha, F., Calebiro, D., Lohse, M. J., et al. (2011). FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat. Protoc. 6, 427-438. doi: 10.1038/nprot.2010.198
5. Calabresi, P., Centonze, D., Gubellini, P., Marfia, G. A., Pisani, A., Sancesario, G., et al. (2000). Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog. Neurobiol. 61, 231-265. doi: 10.1016/S0301-0082(99) 00030-1
6. Calabresi, P., Gubellini, P., Centonze, D., Sancesario, G., Morello, M., Giorgi, M., et al. (1999). A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J. Neurosci. 19, 2489-2499.
7. Calabresi, P., Picconi, B., Tozzi, A., and Di Filippo, M. (2007). Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci. 30, 211-219. doi: 10.1016/j.tins.2007.03.001
8. Castro, L. R., Brito, M., Guiot, E., Polito, M., Korn, C. W., Herve, D., et al. (2013). Striatal neurones have a specific ability to respond to phasic dopamine release. J. Physiol. 591, 3197-3214. doi: 10.1113/jphysiol.2013.252197
9. Castro, L. R., Gervasi, N., Guiot, E., Cavellini, L., Nikolaev, V. O., Paupardin- Tritsch, D., et al. (2010). Type 4 phosphodiesterase plays different integrating roles in different cellular domains in pyramidal cortical neurons. J. Neurosci. 30, 6143-6151. doi: 10.1523/JNEUR0SCI.5851-09.2010
10. Castro, L. R., Verde, I., Cooper, D. M., and Fischmeister, R. (2006). Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 113, 2221-2228. doi: 10.1161/CIRCULATI0NAHA.105.599241
11. Dao, K. K., Teigen, K., Kopperud, R., Hodneland, E., Schwede, F., Christensen, A. E., et al. (2006). Epac1 and cAMP-dependent protein kinase holoenzyme have similar cAMP affinity, but their cAMP domains have distinct structural features and cyclic nucleotide recognition. J. Biol. Chem. 281, 21500-21511. doi: 10.1074/jbc.M603116200
12. de Vente, J., Asan, E., Gambaryan, S., Markerink-van Ittersum, M., Axer, H., Gallatz, K., et al. (2001). Localization of cGMP-dependent protein kinase type II in rat brain. Neuroscience 108, 27-49. doi: 10.1016/S0306-4522(01) 00401-8
13. Ding, J. D., Burette, A., Nedvetsky, P. I., Schmidt, H. H., and Weinberg, R. J. (2004). Distribution of soluble guanylyl cyclase in the rat brain. J. Comp. Neurol. 472, 437-448. doi: 10.1002/cne.20054
14. Ehrengruber, M. U., Lundstrom, K., Schweitzer, C., Heuss, C., Schlesinger, S., and Gahwiler, B. H. (1999). Recombinant Semliki Forest virus and Sindbisvirus effi- cientlyinfect neurons in hippocampal slice cultures. Proc. Natl. Acad. Sci. U.S.A. 96, 7041-7046. doi: 10.1073/pnas.96.12.7041
15. El-Husseini, A. E., Bladen, C., and Vincent, S. R. (1995). Molecular characterization of a type II cyclic GMP-dependent protein kinase expressed in the rat brain. J. Neurochem. 64, 2814-2817. doi: 10.1046/j.1471-4159.1995. 64062814.x
16. El-Husseini, A. E., Williams, J., Reiner, P. B., Pelech, S., and Vincent, S. R. (1999). Localization of the cGMP-dependent protein kinases in relation to nitric oxide synthase in the brain. J. Chem. Neuroanat. 17, 45-55. doi: 10.1016/S0891- 0618(99)00023-X
17. Erneux, C., Couchie, D., Dumont, J. E., Baraniak, J., Stec, W. J., Abbad, E. G., et al. (1981). Specificity of cyclic GMP activation of a multi-substrate cyclic nucleotide phosphodiesterase from rat liver. Eur. J. Biochem. 115, 503-510. doi: 10.1111/j.1432-1033.1981.tb0b231.x
18. Galati, S., D'angelo, V., Scarnati, E., Stanzione, P., Martorana, A., Procopio, T., et al. (2008). In vivo electrophysiology of dopamine-denervated striatum: focus on the nitric oxide/cGMP signaling pathway. Synapse 62, 409-420. doi: 10.1002/syn.20510
19. Garris, P. A., and Wightman, R. M. (1994). Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J. Neurosci. 14, 442-450.
20. Garthwaite, G., Bartus, K., Malcolm, D., Goodwin, D., Kollb-Sielecka, M., Dooldeniya, C., et al. (2006). Signaling from blood vessels to CNS axons through nitric oxide. J. Neurosci. 26, 7730-7740. doi: 10.1523/JNEUR0SCI.1528- 06.2006
21. Garthwaite, J. (2008). Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 27, 2783-2802. doi: 10.1111/j.1460-9568.2008.06285.x
22. Gervasi, N., Hepp, R., Tricoire, L., Zhang, J., Lambolez, B., Paupardin-Tritsch, D., et al. (2007). Dynamics of protein kinase A signaling at the membrane, in the cytosol, and in the nucleus of neurons in mouse brain slices. J. Neurosci. 27, 2744-2750. doi: 10.1523/JNEUROSCI.5352-06.2007
23. Goedhart, J., von Stetten, D., Noirclerc-Savoye, M., Lelimousin, M., Joosen, L., Hink, M. A., et al. (2012). Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3, 751. doi: 10.1038/ncomms1738
24. Gonon, F. (1997). Prolonged and extrasynaptic excitatory action of dopamine mediated byD1 receptors in the rat striatum in vivo. J. Neurosci. 17, 5972-5978.
25. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
26. Hepp, R., Tricoire, L., Hu, E., Gervasi, N., Paupardin-Tritsch, D., Lambolez, B., et al. (2007). Phosphodiesterase type 2 and the homeostasis of cyclic GMP in living thalamic neurons. J. Neurochem. 102, 1875-1886. doi: 10.1111/j.1471- 4159.2007.04657.x
27. Herve, D., and Girault, J.-A. (2005). Chapter II Signal transduction of dopamine receptors, in Handbook of Chemical Neuroanatomy, Vol. 21, eds S. B. Dunnett, M. Bentivoglio, A. Bjorklund and T. Hokfelt, (Elsevier), 109-151. doi: 10.1016/S0924-8196(05)80006-5. Available online at: http://www.sciencedirect.com/science/article/pii/S0924819605800065
28. Honda, A., Adams, S. R., Sawyer, C. L., Lev-Ram, V., Tsien, R. Y., and Dostmann, W. R. G. (2001). Spatiotemporal dynamics of guanosine 3',5'-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc. Natl. Acad. Sci. U.S.A. 98,2437-2442. doi: 10.1073/pnas.051631298
29. Hopper, R. A., and Garthwaite, J. (2006). Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J. Neurosci. 26, 11513-11521. doi: 10.1523/JNEUROSCI.2259-06.2006
30. Kawaguchi, Y. (1997). Neostriatal cell subtypes and their functional roles. Neurosci Res. 27, 1-8. doi: 10.1016/S0168-0102(96)01134-0
31. Klarenbeek, J. B., Goedhart, J., Hink, M. A., Gadella, T. W., and Jalink, K. (2011). A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS ONE 6:e19170. doi: 10.1371/jour- nal.pone.0019170
32. Le Moine, C., and Bloch, B. (1995). D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol. 355, 418-426. doi: 10.1002/cne.903550308
33. Le Novere, N., Li, L., and Girault, J. A. (2008). DARPP-32: molecular integration of phosphorylation potential. Cell. Mol. Life Sci. 65, 2125-2127. doi: 10.1007/s00018-008-8150-y
34. Lin, D. T., Fretier, P., Jiang, C., and Vincent, S. R. (2010). Nitric oxide signaling via cGMP-stimulated phosphodiesterase in striatal neurons. Synapse 64, 460-466. doi: 10.1002/syn.20750
35. Martinez, S. E., Wu, A. Y., Glavas, N. A., Tang, X. B., Turley, S., Hol, W. G., et al. (2002). The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding. Proc. Natl. Acad. Sci. U.S.A. 99, 13260-13265. doi: 10.1073/pnas.192374899
36. Martins, T. J., Mumby, M. C., and Beavo, J. A. (1982). Purification and characterization of a cyclic GMP-stimulated cyclic nucleotide phosphodiesterase from bovine tissues. J. Biol. Chem. 257, 1973-1979.
37. Matsuoka, I., Giuili, G., Poyard, M., Stengel, D., Parma, J., Guellaen, G., et al. (1992). Localization of adenylyl and guanylyl cyclase in rat brain by in situ hybridization: comparison with calmodulin mRNA distribution. J. Neurosci. 12, 3350-3360.
38. Maurice, D. H. (2005). Cyclic nucleotide phosphodiesterase-mediated integration of cGMP and cAMP signaling in cells of the cardiovascular system. Front. Biosci. 10:1221-1228. doi: 10.2741/1614
39. Nikolaev, V. O., Gambaryan, S., Engelhardt, S., Walter, U., and Lohse, M. J. (2005). Real-time monitoring of the PDE2 activity of live cells: hormone-stimulated cAMP hydrolysis is faster than hormone-stimulated cAMP synthesis. J. Biol. Chem. 280, 1716-1719. doi: 10.1074/jbc.c400505200
40. Polli, J. W., and Kincaid, R. L. (1994). Expression of a calmodulin-dependent phosphodiesterase isoform (PDE1B1) correlates with brain regions having extensive dopaminergic innervation. J. Neurosci. 14, 1251-1261.
41. Repaske, D. R., Corbin, J. G., Conti, M., and Goy, M. F. (1993). A cyclic GMP- stimulated cyclic nucleotide phosphodiesterase gene is highly expressed in the limbic system of the rat brain. Neuroscience 56, 673-686. doi: 10.1016/0306- 4522(93)90364-L
42. Rushlow, W., Flumerfelt, B. A., and Naus, C. C. (1995). Colocalization of somatostatin, neuropeptide Y, and NADPH-diaphorase in the caudate-putamen of the rat. J. Comp. Neurol. 351,499-508. doi: 10.1002/cne.903510403
43. Schultz, W., and Dickinson, A. (2000). Neuronal coding of prediction errors. Annu.Rev. Neurosci. 23, 473-500. doi: 10.1146/annurev.neuro.23.1.473
44. Stangherlin, A., Gesellchen, F., Zoccarato, A., Terrin, A., Fields, L. A, Berrera, M., et al. (2011). cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ. Res. 108, 929-939. doi: 10.1161/CIRCRESAHA.110.230698
45. Van Staveren, W. C., Steinbusch, H. W., Markerink-Van Ittersum, M., Repaske, D. R., Goy, M. F., Kotera, J., et al. (2003). mRNA expression patterns of the cGMP- hydrolyzing phosphodiesterases types 2, 5, and 9 during development of the rat brain. J. Comp. Neurol. 467, 566-580. doi: 10.1002/cne.10955
46. Vincent, S. R. (2000). "Chapter II Histochemistry of nitric oxide synthase in the central nervous system," in Handbook of Chemical Neuroanatomy, Vol. 17, eds H. W. M. Steinbusch, J. De Vente, and S. R. Vincent (Elsevier), 19-49. doi: 10.1016/S0924-8196(00)80056-1
47. Vincent, S. R., and Kimura, H. (1992). Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46, 755-784. doi: 10.1016/0306- 4522(92)90184-4
48. Wei, J. Y., Roy, D. S., Leconte, L., and Barnstable, C. J. (1998). Molecular and pharmacological analysis of cyclic nucleotide-gated channel function in the central nervous system. Prog. Neurobiol. 56, 37-64. doi: 10.1016/S0301-0082(98) 00029-X
49. West, A. R., Galloway, M. P., and Grace, A. A. (2002). Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms. Synapse 44, 227-245. doi: 10.1002/syn.10076
50. West, A. R., and Grace, A. A. (2000). Striatal nitric oxide signaling regulates the neuronal activity of midbrain dopamine neurons in vivo. J. Neurophysiol. 83, 1796-1808.
51. West, A. R., and Grace, A. A. (2004). The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity states and electrophysiological properties of striatal medium spiny neurons recorded in vivo. J. Neurosci. 24, 1924-1935. doi: 10.1523/JNEUROSCI.4470-03.2004
52. West, A. R., and Tseng, K. Y. (2011). Nitric oxide-soluble guanylyl cyclase-cyclic GMP signaling in the striatum: new targets for the treatment of Parkinson's disease? Front. Syst. Neurosci. 5:55. doi: 10.3389/fnsys.2011.00055
53. Wykes, V., Bellamy, T. C., and Garthwaite, J. (2002). Kinetics of nitric oxide-cyclic GMP signalling in CNS cells and its possible regulation by cyclic GMP. J. Neurochem. 83, 37-47. doi: 10.1046/j.1471-4159.2002. 01106.x
54. Xie, Z., Adamowicz, W. O., Eldred, W. D., Jakowski, A. B., Kleiman, R. J., Morton, D. G., et al. (2006). Cellular and subcellular localization of PDE10A, a striatum-enriched phosphodiesterase. Neuroscience 139, 597-607. doi: 10.1016/j.neuroscience.2005.12.042