Intermingled cAMP, cGMP and calcium spatiotemporal dynamics in developing neuronal circuits

Frontiers in Cellular Neuroscience

Volumn 8, Issue November, 2014, Pages

  Averaimo, Stefania ^a,b,c   Nicol, Xavier ^a,b,c  

^a CNRS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

Author keywords

Axon guidance; Axon outgrowth; Calcium; cAMP; cGMP; Kinetics; Subcellular compartmentalization; Topographic maps

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; RYANODINE RECEPTOR; SEMAPHORIN 3A; VESICULAR GLUTAMATE TRANSPORTER;

ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONNECTOME; ENZYME ACTIVATION; ENZYME REGULATION; GABAERGIC TRANSMISSION; INTRACELLULAR SIGNALING; LONG TERM POTENTIATION; MUSCLE FIBER MEMBRANE POTENTIAL; NERVE FIBER GROWTH; NEUROMODULATION; NONHUMAN; POLARIZATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SPATIOTEMPORAL ANALYSIS; SYNAPTIC TRANSMISSION; TOPOGRAPHY;

EID: 84927546210     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00376     Document Type: Article

References (100)

1. Agarwal, S. R., MacDougall, D. A., Tyser, R., Pugh, S. D., Calaghan, S. C., and Harvey, R. D. (2011). Effects of cholesterol depletion on compartmentalized cAMP responses in adult cardiac myocytes. J. Mol. Cell. Cardiol. 50, 500-509. doi: 10.1016/j.yjmcc.2010.11.015.
2. Arimura, N., and Kaibuchi, K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194-205. doi: 10.1038/nrn2056.
3. Barnes, A. P., Solecki, D., and Polleux, F. (2008). New insights into the molecular mechanisms specifying neuronal polarity in vivo. Curr. Opin. Neurobiol. 18, 44-52. doi: 10.1016/j.conb.2008.05.003.
4. Blackman, B. E., Horner, K., Heidmann, J., Wang, D., Richter, W., Rich, T. C., et al. (2011). PDE4D and PDE4B function in distinct subcellular compartments in mouse embryonic fibroblasts. J. Biol. Chem. 286, 12590-12601. doi: 10.1074/jbc.m110.203604.
5. Bony, G., Szczurkowska, J., Tamagno, I., Shelly, M., Contestabile, A., and Cancedda, L. (2013). Non-hyperpolarizing GABAB receptor activation regulates neuronal migration and neurite growth and specification by cAMP/LKB1. Nat. Commun. 4:1800. doi: 10.1038/ncomms2820.
6. Borodinsky, L. N., Root, C. M., Cronin, J. A., Sann, S. B., Gu, X., and Spitzer, N. C. (2004). Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429, 523-530. doi: 10.1038/nature02518.
7. Borodinsky, L. N., and Spitzer, N. C. (2006). Second messenger pas de deux: the coordinated dance between calcium and cAMP. Sci. STKE 2006:pe22. doi: 10.1126/stke.3362006pe22.
8. Cai, D., Qiu, J., Cao, Z., McAtee, M., Bregman, B. S., and Filbin, M. T. (2001). Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J. Neurosci. 21, 4731-4739.
9. Castro, L. R. V., 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/jneurosci.5851-09.2010.
10. Col, J. A. D., Matsuo, T., Storm, D. R., and Rodriguez, I. (2007). Adenylyl cyclase-dependent axonal targeting in the olfactory system. Development 134, 2481-2489. doi: 10.1242/dev.006346.
11. Corredor, R. G., Trakhtenberg, E. F., Pita-Thomas, W., Jin, X., Hu, Y., and Goldberg, J. L. (2012). Soluble adenylyl cyclase activity is necessary for retinal ganglion cell survival and axon growth. J. Neurosci. 32, 7734-7744. doi: 10.1523/jneurosci.5288-11.2012.
12. Delint-Ramirez, I., Willoughby, D., Hammond, G. V. R., Ayling, L. J., and Cooper, D. M. F. (2011). Palmitoylation targets AKAP79 protein to lipid rafts and promotes its regulation of calcium-sensitive adenylyl cyclase type 8. J. Biol. Chem. 286, 32962-32975. doi: 10.1074/jbc.m111.243899.
13. Depry, C., Allen, M. D., and Zhang, J. (2011). Visualization of PKA activity in plasma membrane microdomains. Mol. Biosyst. 7, 52-58. doi: 10.1039/c0mb00079e.
14. Dhande, O. S., Bhatt, S., Anishchenko, A., Elstrott, J., Iwasato, T., Swindell, E. C., et al. (2012). Role of adenylate cyclase 1 in retinofugal map development. J. Comp. Neurol. 520, 1562-1583. doi: 10.1002/cne.23000.
15. Dhande, O. S., Hua, E. W., Guh, E., Yeh, J., Bhatt, S., Zhang, Y., et al. (2011). Development of single retinofugal axon arbors in normal and β2 knock-out mice. J. Neurosci. 31, 3384-3399. doi: 10.1523/JNEUROSCI.4899-10.2011.
16. Dunn, T. A., Storm, D. R., and Feller, M. B. (2009). Calcium-dependent increases in protein kinase-A activity in mouse retinal ganglion cells are mediated by multiple adenylate cyclases. PLoS One 4:e7877. doi: 10.1371/journal.pone.0007877.
17. Dunn, T. A., Wang, C.-T., Colicos, M. A., Zaccolo, M., DiPilato, L. M., Zhang, J., et al. (2006). Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. J. Neurosci. 26, 12807-12815. doi: 10.1523/jneurosci.3238-06.2006.
18. Dyachok, O., Isakov, Y., Sågetorp, J., and Tengholm, A. (2006). Oscillations of cyclic AMP in hormone-stimulated insulin-secreting beta-cells. Nature 439, 349-352. doi: 10.1038/nature04410.
19. Fagan, K. A., Graf, R. A., Tolman, S., Schaack, J., and Cooper, D. M. (2000). Regulation of a Ca2+-sensitive adenylyl cyclase in an excitable cell. Role of voltage-gated versus capacitative Ca2+ entry. J. Biol. Chem. 275, 40187-40194. doi: 10.1074/jbc.m006606200.
20. Feldheim, D. A., Kim, Y. I., Bergemann, A. D., Frisén, J., Barbacid, M., and Flanagan, J. G. (2000). Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25, 563-574. doi: 10.1016/s0896-6273(00)81060-0.
21. Feng, Q., Zhang, Y., Li, Y., Liu, Z., Zuo, J., and Fang, F. (2006). Two domains are critical for the nuclear localization of soluble adenylyl cyclase. Biochimie 88, 319-328. doi: 10.1016/j.biochi.2005.09.003.
22. Frisén, J., Yates, P. A., McLaughlin, T., Friedman, G. C., O'Leary, D. D., and Barbacid, M. (1998). Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system. Neuron 20, 235-243. doi: 10.1016/s0896-6273(00)80452-3.
23. Furman, M., Xu, H.-P., and Crair, M. C. (2013). Competition driven by retinal waves promotes morphological and functional synaptic development of neurons in the superior colliculus. J. Neurophysiol. 110, 1441-1454. doi: 10.1152/jn.01066.2012.
24. Gomez, T. M., Robles, E., Poo, M., and Spitzer, N. C. (2001). Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291, 1983-1987. doi: 10.1126/science.1056490.
25. Gomez, T. M., Snow, D. M., and Letourneau, P. C. (1995). Characterization of spontaneous calcium transients in nerve growth cones and their effect on growth cone migration. Neuron 14, 1233-1246. doi: 10.1016/0896-6273(95)90270-8.
26. Gomez, T. M., and Spitzer, N. C. (1999). In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397, 350-355. doi: 10.1038/16927.
27. Gorbunova, Y. V., and Spitzer, N. C. (2002). Dynamic interactions of cyclic AMP transients and spontaneous Ca2+ spikes. Nature 418, 93-96. doi: 10.1038/nature00835.
28. Guirland, C., Suzuki, S., Kojima, M., Lu, B., and Zheng, J. Q. (2004). Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 42, 51-62. doi: 10.1016/s0896-6273(04)00157-6.
29. Hong, K., Nishiyama, M., Henley, J., Tessier-Lavigne, M., and Poo, M. (2000). Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403, 93-98. doi: 10.1038/47507.
30. Hong, K. P., Spitzer, N. C., and Nicol, X. (2011). Improved molecular toolkit for cAMP studies in live cells. BMC Res. Notes 4:241. doi: 10.1186/1756-0500-4-241.
31. Höpker, V. H., Shewan, D., Tessier-Lavigne, M., Poo, M., and Holt, C. (1999). Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401, 69-73. doi: 10.1038/43441.
32. Horvat, S. J., Deshpande, D. A., Yan, H., Panettieri, R. A., Codina, J., DuBose, T. D. Jr., et al. (2012). A-kinase anchoring proteins regulate compartmentalized cAMP signaling in airway smooth muscle. FASEB J. 26, 3670-3679. doi: 10.1096/fj.11-201020.
33. Imai, T., Suzuki, M., and Sakano, H. (2006). Odorant receptor-derived cAMP signals direct axonal targeting. Science 314, 657-661. doi: 10.1126/science.1131794.
34. Iwasato, T., Inan, M., Kanki, H., Erzurumlu, R. S., Itohara, S., and Crair, M. C. (2008). Cortical adenylyl cyclase 1 is required for thalamocortical synapse maturation and aspects of layer IV barrel development. J. Neurosci. 28, 5931-5943. doi: 10.1523/JNEUROSCI.0815-08.2008.
35. Kleppisch, T. (2009). Phosphodiesterases in the central nervous system. Handb. Exp. Pharmacol. 191, 71-92. doi: 10.1007/978-3-540-68964-5_5.
36. Kobayashi, T., Nagase, F., Hotta, K., and Oka, K. (2013). Crosstalk between second messengers predicts the motility of the growth cone. Sci. Rep. 3:3118. doi: 10.1038/srep03118.
37. Landa, L. R. Jr., Harbeck, M., Kaihara, K., Chepurny, O., Kitiphongspattana, K., Graf, O., et al. (2005). Interplay of Ca2+ and cAMP signaling in the insulin-secreting MIN6 beta-cell line. J. Biol. Chem. 280, 31294-31302. doi: 10.1074/jbc.m505657200.
38. Li, L., Hutchins, B. I., and Kalil, K. (2009). Wnt5a induces simultaneous cortical axon outgrowth and repulsive axon guidance through distinct signaling mechanisms. J. Neurosci. 29, 5873-5883. doi: 10.1523/jneurosci.0183-09.2009.
39. Liu, S., Li, Y., Kim, S., Fu, Q., Parikh, D., Sridhar, B., et al. (2012). Phosphodiesterases coordinate cAMP propagation induced by two stimulatory G protein-coupled receptors in hearts. Proc. Natl. Acad. Sci. U S A 109, 6578-6583. doi: 10.1073/pnas.1117862109.
40. Lu, H.-C., Butts, D. A., Kaeser, P. S., She, W.-C., Janz, R., and Crair, M. C. (2006). Role of efficient neurotransmitter release in barrel map development. J. Neurosci. 26, 2692-2703. doi: 10.1523/jneurosci.3956-05.2006.
41. Luo, L., and Flanagan, J. G. (2007). Development of continuous and discrete neural maps. Neuron 56, 284-300. doi: 10.1016/j.neuron.2007.10.014.
42. Luo, L., and O'Leary, D. D. M. (2005). Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156. doi: 10.1146/annurev.neuro.28.061604.135632.
43. Maritan, M., Monaco, G., Zamparo, I., Zaccolo, M., Pozzan, T., and Lodovichi, C. (2009). Odorant receptors at the growth cone are coupled to localized cAMP and Ca2+ increases. Proc. Natl. Acad. Sci. U S A 106, 3537-3542. doi: 10.1073/pnas.0813224106.
44. McConnachie, G., Langeberg, L. K., and Scott, J. D. (2006). AKAP signaling complexes: getting to the heart of the matter. Trends Mol. Med. 12, 317-323. doi: 10.1016/j.molmed.2006.05.008.
45. Ming, G. L., Song, H. J., Berninger, B., Holt, C. E., Tessier-Lavigne, M., and Poo, M. M. (1997). cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225-1235. doi: 10.1016/s0896-6273(00)80414-6.
46. Moore, S. W., Lai Wing Sun, K., Xie, F., Barker, P. A., Conti, M., and Kennedy, T. E. (2008). Soluble adenylyl cyclase is not required for axon guidance to netrin-1. J. Neurosci. 28, 3920-3924. doi: 10.1523/jneurosci.0547-08.2008.
47. Muir-Robinson, G., Hwang, B. J., and Feller, M. B. (2002). Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J. Neurosci. 22, 5259-5264.
48. Munck, S., Bedner, P., Bottaro, T., and Harz, H. (2004). Spatiotemporal properties of cytoplasmic cyclic AMP gradients can alter the turning behaviour of neuronal growth cones. Eur. J. Neurosci. 19, 791-797. doi: 10.1111/j.0953-816x.2004.03118.x.
49. Murray, A. J., Tucker, S. J., and Shewan, D. A. (2009). cAMP-dependent axon guidance is distinctly regulated by Epac and protein kinase A. J. Neurosci. 29, 15434-15444. doi: 10.1523/jneurosci.3071-09.2009.
50. Nicol, X., Bennis, M., Ishikawa, Y., Chan, G. C.-K., Repérant, J., Storm, D. R., et al. (2006a). Role of the calcium modulated cyclases in the development of the retinal projections. Eur. J. Neurosci. 24, 3401-3414. doi: 10.1111/j.1460-9568.2006.05227.x.
51. Nicol, X., Hong, K. P., and Spitzer, N. C. (2011). Spatial and temporal second messenger codes for growth cone turning. Proc. Natl. Acad. Sci. U S A 108, 13776-13781. doi: 10.1073/pnas.1100247108.
52. Nicol, X., Muzerelle, A., Rio, J. P., Métin, C., and Gaspar, P. (2006b). Requirement of adenylate cyclase 1 for the ephrin-A5-dependent retraction of exuberant retinal axons. J. Neurosci. 26, 862-872. doi: 10.1523/jneurosci.3385-05.2006.
53. Nicol, X., Voyatzis, S., Muzerelle, A., Narboux-Nême, N., Südhof, T. C., Miles, R., et al. (2007). cAMP oscillations and retinal activity are permissive for ephrin signaling during the establishment of the retinotopic map. Nat. Neurosci. 10, 340-347. doi: 10.1038/nn1842.
54. Nikolaev, V. O., Bünemann, M., Hein, L., Hannawacker, A., and Lohse, M. J. (2004). Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279, 37215-37218. doi: 10.1074/jbc.C400302200.
55. Nishiyama, M., Hoshino, A., Tsai, L., Henley, J. R., Goshima, Y., Tessier-Lavigne, M., et al. (2003). Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 423, 990-995. doi: 10.1038/nature01751.
56. Omori, K., and Kotera, J. (2007). Overview of PDEs and their regulation. Circ. Res. 100, 309-327. doi: 10.1161/01.res.0000256354.95791.f1.
57. Ooashi, N., Futatsugi, A., Yoshihara, F., Mikoshiba, K., and Kamiguchi, H. (2005). Cell adhesion molecules regulate Ca2+-mediated steering of growth cones via cyclic AMP and ryanodine receptor type 3. J. Cell Biol. 170, 1159-1167. doi: 10.1083/jcb.200503157.
58. Penn, A. A., Riquelme, P. A., Feller, M. B., and Shatz, C. J. (1998). Competition in retinogeniculate patterning driven by spontaneous activity. Science 279, 2108-2112. doi: 10.1126/science.279.5359.2108.
59. Pham, T. A., Rubenstein, J. L., Silva, A. J., Storm, D. R., and Stryker, M. P. (2001). The CRE/CREB pathway is transiently expressed in thalamic circuit development and contributes to refinement of retinogeniculate axons. Neuron 31, 409-420. doi: 10.1016/s0896-6273(01)00381-6.
60. Pietrobon, M., Zamparo, I., Maritan, M., Franchi, S. A., Pozzan, T., and Lodovichi, C. (2011). Interplay among cGMP, cAMP and Ca2+ in living olfactory sensory neurons in vitro and in vivo. J. Neurosci. 31, 8395-8405. doi: 10.1523/jneurosci.6722-10.2011.
61. Piggott, L. A., Bauman, A. L., Scott, J. D., and Dessauer, C. W. (2008). The A-kinase anchoring protein Yotiao binds and regulates adenylyl cyclase in brain. Proc. Natl. Acad. Sci. U S A 105, 13835-13840. doi: 10.1073/pnas.0712100105.
62. Polito, M., Klarenbeek, J., Jalink, K., Paupardin-Tritsch, D., Vincent, P., and Castro, L. R. V. (2013). The NO/cGMP pathway inhibits transient cAMP signals through the activation of PDE2 in striatal neurons. Front. Cell. Neurosci. 7:211. doi: 10.3389/fncel.2013.00211.
63. Ponsioen, B., Zhao, J., Riedl, J., Zwartkruis, F., van der Krogt, G., Zaccolo, M., et al. (2004). Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 5, 1176-1180. doi: 10.1038/sj.embor.7400290.
64. Raslan, Z., and Naseem, K. M. (2014). Compartmentalisation of cAMP-dependent signalling in blood platelets: the role of lipid rafts and actin polymerisation. Platelets, 1-9. doi: 10.3109/09537104.2014.916792. [Epub ahead of print].
65. Ravary, A., Muzerelle, A., Hervé, D., Pascoli, V., Ba-Charvet, K. N., Girault, J.-A., et al. (2003). Adenylate cyclase 1 as a key actor in the refinement of retinal projection maps. J. Neurosci. 23, 2228-2238.
66. Robles, E., Huttenlocher, A., and Gomez, T. M. (2003). Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain. Neuron 38, 597-609. doi: 10.1016/s0896-6273(03)00260-5.
67. Roisen, F. J., Murphy, R. A., Pichichero, M. E., and Braden, W. G. (1972). Cyclic adenosine monophosphate stimulation of axonal elongation. Science 175, 73-74. doi: 10.1126/science.175.4017.73.
68. Root, C. M., Velázquez-Ulloa, N. A., Monsalve, G. C., Minakova, E., and Spitzer, N. C. (2008). Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J. Neurosci. 28, 4777-4784. doi: 10.1523/jneurosci.4873-07.2008.
69. Rossi, F. M., Pizzorusso, T., Porciatti, V., Marubio, L. M., Maffei, L., and Changeux, J.-P. (2001). Requirement of the nicotinic acetylcholine receptor β2 subunit for the anatomical and functional development of the visual system. Proc. Natl. Acad. Sci. U S A 98, 6453-6458. doi: 10.1073/pnas.101120998.
70. Ryu, M.-H., Moskvin, O. V., Siltberg-Liberles, J., and Gomelsky, M. (2010). Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J. Biol. Chem. 285, 41501-41508. doi: 10.1074/jbc.M110.177600.
71. Sample, V., DiPilato, L. M., Yang, J. H., Ni, Q., Saucerman, J. J., and Zhang, J. (2012). Regulation of nuclear PKA revealed by spatiotemporal manipulation of cyclic AMP. Nat. Chem. Biol. 8, 375-382. doi: 10.1038/nchembio.799.
72. Schröder-Lang, S., Schwärzel, M., Seifert, R., Strünker, T., Kateriya, S., Looser, J., et al. (2007). Fast manipulation of cellular cAMP level by light in vivo. Nat. Methods 4, 39-42. doi: 10.1038/nmeth975.
73. Serizawa, S., Miyamichi, K., Takeuchi, H., Yamagishi, Y., Suzuki, M., and Sakano, H. (2006). A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127, 1057-1069. doi: 10.1016/j.cell.2006.10.031.
74. Shelly, M., Cancedda, L., Heilshorn, S., Sumbre, G., and Poo, M.-M. (2007). LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129, 565-577. doi: 10.1016/j.cell.2007.04.012.
75. Shelly, M., Cancedda, L., Lim, B. K., Popescu, A. T., Cheng, P., Gao, H., et al. (2011). Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 71, 433-446. doi: 10.1016/j.neuron.2011.06.041.
76. Shelly, M., Lim, B. K., Cancedda, L., Heilshorn, S. C., Gao, H., and Poo, M. (2010). Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 327, 547-552. doi: 10.1126/science.1179735.
77. Shewan, D., Dwivedy, A., Anderson, R., and Holt, C. E. (2002). Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat. Neurosci. 5, 955-962. doi: 10.1038/nn919.
78. Song, H. J., Ming, G. L., and Poo, M. M. (1997). cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275-279. doi: 10.1038/40864.
79. Stellwagen, D., and Shatz, C. J. (2002). An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33, 357-367. doi: 10.1016/s0896-6273(02)00577-9.
80. Stellwagen, D., Shatz, C. J., and Feller, M. B. (1999). Dynamics of retinal waves are controlled by cyclic AMP. Neuron 24, 673-685. doi: 10.1016/s0896-6273(00)81121-6.
81. Stierl, M., Stumpf, P., Udwari, D., Gueta, R., Hagedorn, R., Losi, A., et al. (2011). Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J. Biol. Chem. 286, 1181-1188. doi: 10.1074/jbc.M110.185496.
82. Tang, F., Dent, E. W., and Kalil, K. (2003). Spontaneous calcium transients in developing cortical neurons regulate axon outgrowth. J. Neurosci. 23, 927-936.
83. Terrin, A., Di Benedetto, G., Pertegato, V., Cheung, Y.-F., Baillie, G., Lynch, M. J., et al. (2006). PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J. Cell Biol. 175, 441-451. doi: 10.1083/jcb.200605050.
84. Terrin, A., Monterisi, S., Stangherlin, A., Zoccarato, A., Koschinski, A., Surdo, N. C., et al. (2012). PKA and PDE4D3 anchoring to AKAP9 provides distinct regulation of cAMP signals at the centrosome. J. Cell Biol. 198, 607-621. doi: 10.1083/jcb.201201059.
85. Tojima, T., Itofusa, R., and Kamiguchi, H. (2009). The nitric oxide-cGMP pathway controls the directional polarity of growth cone guidance via modulating cytosolic Ca2+ signals. J. Neurosci. 29, 7886-7897. doi: 10.1523/jneurosci.0087-09.2009.
86. Valsecchi, F., Konrad, C., and Manfredi, G. (2014). Role of soluble adenylyl cyclase in mitochondria. Biochim. Biophys. Acta doi: 10.1016/j.bbadis.2014.05.035. [Epub ahead of print].
87. Vincent, P., Castro, L. R. V., Gervasi, N., Guiot, E., Brito, M., and Paupardin-Tritsch, D. (2012). PDE4 control on cAMP/PKA compartmentation revealed by biosensor imaging in neurons. Horm. Metab. Res. 44, 786-789. doi: 10.1055/s-0032-1311631.
88. Welker, E., Armstrong-James, M., Bronchti, G., Ourednik, W., Gheorghita-Baechler, F., Dubois, R., et al. (1996). Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless. Science 271, 1864-1867. doi: 10.1126/science.271.5257.1864.
89. Willoughby, D., and Cooper, D. M. F. (2006). Ca2+ stimulation of adenylyl cyclase generates dynamic oscillations in cyclic AMP. J. Cell Sci. 119, 828-836. doi: 10.1242/jcs.02812.
90. Willoughby, D., and Cooper, D. M. F. (2007). Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87, 965-1010. doi: 10.1152/physrev.00049.2006.
91. Willoughby, D., Everett, K. L., Halls, M. L., Pacheco, J., Skroblin, P., Vaca, L., et al. (2012). Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMP signaling. Sci. Signal. 5:ra29. doi: 10.1126/scisignal.2002299.
92. Willoughby, D., Masada, N., Wachten, S., Pagano, M., Halls, M. L., Everett, K. L., et al. (2010). AKAP79/150 interacts with AC8 and regulates Ca2+-dependent cAMP synthesis in pancreatic and neuronal systems. J. Biol. Chem. 285, 20328-20342. doi: 10.1074/jbc.m110.120725.
93. Wong, W., and Scott, J. D. (2004). AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5, 959-970. doi: 10.1038/nrm1527.
94. Wong, S. T., Trinh, K., Hacker, B., Chan, G. C., Lowe, G., Gaggar, A., et al. (2000). Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27, 487-497. doi: 10.1016/s0896-6273(00)00060-x.
95. Wu, K. Y., Zippin, J. H., Huron, D. R., Kamenetsky, M., Hengst, U., Buck, J., et al. (2006). Soluble adenylyl cyclase is required for netrin-1 signaling in nerve growth cones. Nat. Neurosci. 9, 1257-1264. doi: 10.1038/nn1767.
96. Zaccolo, M., and Movsesian, M. A. (2007). cAMP and cGMP signaling cross-talk: role of phosphodiesterases and implications for cardiac pathophysiology. Circ. Res. 100, 1569-1578. doi: 10.1161/circresaha.106.144501.
97. Zhang, J., Ackman, J. B., Xu, H.-P., and Crair, M. C. (2012). Visual map development depends on the temporal pattern of binocular activity in mice. Nat. Neurosci. 15, 298-307. doi: 10.1038/nn.3007.
98. Zhang, J., Ma, Y., Taylor, S. S., and Tsien, R. Y. (2001). Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl. Acad. Sci. U S A 98, 14997-15002. doi: 10.1073/pnas.211566798.
99. Zippin, J. H., Chen, Y., Nahirney, P., Kamenetsky, M., Wuttke, M. S., Fischman, D. A., et al. (2003). Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J. 17, 82-84. doi: 10.1096/fj.02-0598fje.
100. Zou, D.-J., Chesler, A. T., Le Pichon, C. E., Kuznetsov, A., Pei, X., Hwang, E. L., et al. (2007). Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J. Neurosci. 27, 6675-6683. doi: 10.1523/jneurosci.0699-07.2007.