Signaling through the neuropeptide GPCR PAC1 induces neuritogenesis via a single linear cAMP- and ERK-dependent pathway using a novel cAMP sensor

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3199-3211

  Emery, Andrew C ^a   Eiden, Lee E ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Adenylate cyclase; Neurite; Neuroscreen 1; PC12; Signal transduction

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 8 (4 CHLOROPHENYLTHIO) CYCLIC AMP; 8 BROMO CYCLIC AMP; ADENYLATE CYCLASE; BUCLADESINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP DERIVATIVE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NEUROPEPTIDE; RAP1 PROTEIN;

ANIMAL CELL; ARTICLE; BIOSENSOR; CELL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE ACTIVATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REPORTER GENE; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; ANIMALS; CELL LINE, TUMOR; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FORSKOLIN; MICE; NEURITES; PC12 CELLS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; SIGNAL TRANSDUCTION;

EID: 84864750962     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-203042     Document Type: Article

References (56)

1. Greengard, P. (2001) The neurobiology of slow synaptic transmission. Science 294, 1024-1030
2. Kandel, E. R. (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038
3. Bers, D. M. (2007) Going to cAMP just got more complicated. J. Physiol. 583, 415-416
4. Hamelink, C., Lee, H.-W., Grimaldi, M., and Eiden, L. E. (2002) Coincident elevation of cyclic AMP and calcium influx by PACAP-27 synergistically regulates VIP gene transcription through a novel PKA-independent signaling pathway. J. Neurosci. 22, 5310-5320 (Pubitemid 35386452)
5. Ravni, A., Vaudry, D., Gerdin, M. J., Eiden, M. V., Falluel-Morel, A., Gonzalez, B., Vaudry, H., and Eiden, L. E. (2008) A cAMP-dependent, PKA-independent signaling pathway mediating neuritogenesis through Egr1 in PC12 cells. Mol. Pharmacol. 73, 1688-1708 (Pubitemid 351724358)
6. Holighaus, Y., Weihe, E., and Eiden, L. E. (2012) STC1 induction by PACAP is mediated through cAMP and ERK1/2 but not PKA in cultured cortical neurons. J. Mol. Neurosci. 46, 75-87
7. Kim, H. S., Yumkham, S., Kim, S. H., Yea, K., Shin, Y. C., Ryu, S. H., and Suh, P. G. (2006) Secretin induces neurite outgrowth of PC12 through cAMP-mitogen-activated protein kinase pathway. Exp. Mol. Med. 38, 85-93 (Pubitemid 43352437)
8. Cibelli, G., Corsi, P., Diana, G., Vitiello, F., and Thiel, G. (2001) Corticotropin-releasing factor triggers neurite outgrowth of a catecholaminergic immortalized neuron via cAMP and MAP kinase signalling pathways. Eur. J. Neurosci. 13, 1339-1348 (Pubitemid 32328488)
9. Monaghan, T. K., Mackenzie, C. J., Plevin, R., and Lutz, E. M. (2008) PACAP-38 induces neuronal differentiation of human SH-SY5Y neuroblastoma cells via cAMP-mediated activation of ERK and p38 MAP kinases. J. Neurochem. 104, 74-88 (Pubitemid 350265065)
10. Gerdin, M. J., and Eiden, L. E. (2007) Regulation of PC12 cell differentiation by cAMP signaling to ERK independent of PKA: do all the connections add up? Sci. STKE 2007, pe15
11. Obara, Y., Labudda, K., Dillon, T. J., and Stork, P. J. (2004) PKA phosphorylation of Src mediates Rap1 activation in NGF and cAMP signaling in PC12 cells. J. Cell Sci. 117, 6085-6094 (Pubitemid 40123973)
12. York, R. D., Yao, H., Dillon, T., Ellig, C. L., Eckert, S. P., McCleskey, E. W., and Stork, P. J. S. (1998) Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392, 622-626 (Pubitemid 28207722)
13. Vaudry, D., Chen, Y., Ravni, A., Hamelink, C., Elkahloun, A. G., and Eiden, L. E. (2002) Analysis of the PC12 cell transcriptome after differentiation with pituitary adenylate cyclase-activating polypeptide (PACAP). J. Neurochem. 83, 1272-1284 (Pubitemid 35477467)
14. Lazarovici, P., Jiang, H., and Fink, D., Jr. (1998) The 38-amino-acid form of pituitary adenylate cyclase-activating polypeptide induces neurite outgrowth in PC12 cells that is dependent on protein kinase C and extracellular signal-regulated kinase but not on protein kinase A, nerve growth factor receptor tyrosine kinase, p21ras G protein, and pp60c-src cytoplasmic tyrosine kinase. Mol. Pharmacol. 54, 547-558 (Pubitemid 28442948)
15. Ginty, D. D., Glowacka, D., DeFranco, C., and Wagner, J. A. (1991) Nerve growth factor-induced neuronal differentiation after dominant repression of both type I and type II cAMP-dependent protein kinase activities. J. Biol. Chem. 266, 15325-15333 (Pubitemid 21907651)
16. Stork, P. J., and Schmitt, J. M. (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol. 12, 258-266 (Pubitemid 34634174)
17. Enserink, J. M., Christensen, A. E., de Rooij, J., van Triest, M., Schwede, F., Genieser, H. G., Doskeland, S. O., Blank, J. L., and Bos, J. L. (2002) A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 4, 901-906 (Pubitemid 35331366)
18. Wang, Z., Dillon, T. J., Pokala, V., Mishra, S., Labudda, K., Hunter, B., and Stork, P. J. (2006) Rap1-mediated activation of extracellular signal-regulated kinases by cyclic AMP is dependent on the mode of Rap1 activation. Mol. Cell. Biol. 26, 2130-2145 (Pubitemid 43346916)
19. Gutkind, J. S. (2000) Regulation of mitogen-activated protein kinase signaling networks by G protein-coupled receptors. Sci. STKE 2000, re1
20. Radio, N. M., Breier, J. M., Shafer, T. J., and Mundy, W. R. (2008) Assessment of chemical effects on neurite outgrowth in PC12 cells using high content screening. Toxicol. Sci. 105, 106-118
21. Deutsch, P. J., and Sun, Y. (1992) The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J. Biol. Chem. 267, 5108-5113
22. Grumolato, L., Louiset, E., Alexandre, D., Ait-Ali, D., Turquier, V., Fournier, A., Fasolo, A., Vaudry, H., and Anouar, Y. (2003) PACAP and NGF regulate common and distinct traits of the sympathoadrenal lineage: effects on electrical properties, gene markers and transcription factors in differentiating PC12 cells. Eur. J. Neurosci. 17, 71-82 (Pubitemid 36098877)
23. Samal, B. B., and Eiden, L. E. (2008) pathFinder: a static network analysis tool for pharmacological analysis of signal transduction pathways. Sci. Signal. 1, pt4
24. Ueda, Y., Hirai, S., Osada, S., Suzuki, A., Mizuno, K., and Ohno, S. (1996) Protein kinase C activates the MEK-ERK pathway in a manner independent of Ras and dependent on Raf. J. Biol. Chem. 271, 23512-23519 (Pubitemid 26314803)
25. Dumaz, N., and Marais, R. (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 (Pubitemid 41021163)
26. Lioudyno, M., Skoglosa, Y., Takei, N., and Lindholm, D. (1998) Pituitary adenylate cyclase-activating polypeptide (PACAP) protects dorsal root ganglion neurons from death and induces calcitonin gene-related peptide (CGRP) immunoreactivity in vitro. J. Neurosci. Res. 51, 243-256 (Pubitemid 28073032)
27. Guirland, C., Buck, K. B., Gibney, J. A., DiCicco-Bloom, E., and Zheng, J. Q. (2003) Direct cAMP signaling through G-protein-coupled receptors mediates growth cone attraction induced by pituitary adenylate cyclase-activating polypeptide. J. Neurosci. 23, 2274-2283 (Pubitemid 36368915)
28. Armstrong, B. D., Abad, C., Chhith, S., Cheung-Lau, G., Hajji, O. E., Nobuta, H., and Waschek, J. A. (2008) Impaired nerve regeneration and enhanced neuroinflammatory response in mice lacking pituitary adenylyl cyclase activating peptide. Neuroscience 151, 63-73
29. Waschek, J. A., Dicicco-Bloom, E., Nicot, A., and Lelievre, V. (2006) Hedgehog signaling: new targets for GPCRs coupled to cAMP and protein kinase A. Ann. N. Y. Acad. Sci. 1070, 120-128 (Pubitemid 44126629)
30. Tan, Y. V., Abad, C., Lopez, R., Dong, H., Liu, S., Lee, A., Gomariz, R. P., Leceta, J., and Waschek, J. A. (2009) Pituitary adenylyl cyclase-activating polypeptide is an intrinsic regulator of Treg abundance and protects against experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U. S. A. 106, 2012-2017
31. Voice, J. K., Grinninger, C., Kong, Y., Bangale, Y., Paul, S., and Goetzl, E. J. (2003) Roles of vasoactive intestinal peptide (VIP) in the expression of different immune phenotypes by wild-type mice and T cell-targeted type II VIP receptor transgenic mice. J. Immunol. 170, 308-314 (Pubitemid 36026154)
32. Abad, C., Martinez, C., Leceta, J., Gomariz, R. P., and Delgado, M. (2001) Pituitary adenylate cyclase-activating polypeptide inhibits collagen-induced arthritis: an experimental immunomodulatory therapy. J. Immunol. 167, 3182-3189 (Pubitemid 32852557)
33. Gressens, P., Hill, J. M., Gozes, I., Fridkin, M., and Brenneman, D. E. (1993) Growth factor function of vasoactive intestinal peptide in whole cultured mouse embryos. Nature 362, 155-158 (Pubitemid 23085254)
34. Vaudry, D., Gonzalez, B. J., Basille, M., Fournier, A., and Vaudry, H. (1999) Neurotrophic activity of pituitary adenylate cyclase-activating polypeptide on rat cerebellar cortex during development. Proc. Natl. Acad. Sci. U. S. A. 96, 9415-9420 (Pubitemid 29374769)
35. DiCicco-Bloom, E., Deutsch, P. J., Maltzman, J., Zhang, J., Pintar, J. E., Zheng, J., Friedman, W. F., Zhou, X., and Zaremba, T. (2000) Autocrine expression and ontogenetic functions of the PACAP ligand/receptor system during sympathetic development. Dev. Biol. 219, 197-213 (Pubitemid 30152599)
36. Otto, C., Kovalchuk, Y., Wolfer, D. P., Gass, P., Martin, M., Zuschratter, W., Gröne, H. J., Kellendonk, C., Tronche, F., Maldonado, R., Lipp, H.-P., Konnerth, A., and Schütz, G. (2001) Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J. Neurosci. 21, 5520-5527 (Pubitemid 32692150)
37. q, protein kinase C, and activation of Src. J. Neurosci. 25, 11374-11384
38. Ohtaki, H., Nakamachi, T., Dohi, K., and Shioda, S. (2008) Role of PACAP in ischemic neural death. J. Mol. Neurosci. 36, 16-25
39. Chen, Y., Samal, B., Hamelink, C. R., Xiang, C. C., Chen, Y., Chen, M., Vaudry, D., Brownstein, M. J., Hallenbeck, J. M., and Eiden, L. E. (2006) Neuroprotection by endogenous and exogenous PACAP following stroke. Regul. Pept. 137, 4-19 (Pubitemid 44751193)
40. Ohtaki, H., Nakamachi, T., Dohi, K., Aizawa, Y., Takaki, A., Hodoyama, K., Yofu, S., Hashimoto, H., Shintani, N., Baba, A., Kopf, M., Iwakura, Y., Matsuda, K., Arimura, A., and Shioda, S. (2006) Pituitary adenylate cyclase-activating polypeptide (PACAP) decreases ischemic neuronal cell death in association with IL-6. Proc. Natl. Acad. Sci. U. S. A. 103, 7488-7493 (Pubitemid 43727860)
41. Grumolato, L., Elkahloun, A. G., Ghzili, H., Alexandre, D., Coulouarn, C., Yon, L., Salier, J. P., Eiden, L. E., Fournier, A., Vaudry, H., and Anouar, Y. (2003) Microarray and suppression subtractive hybridization analyses of gene expression in pheochromocytoma cells reveal pleiotropic effects of pituitary adenylate cyclase-activating polypeptide on cell proliferation, survival, and adhesion. Endocrinology 144, 2368-2379 (Pubitemid 36637089)
42. Hammack, S. E., Cheung, J., Rhodes, K. M., Schutz, K. C., Falls, W. A., Braas, K. M., and May, V. (2009) Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 34, 833-843
43. Stroth, N., Liu, Y., Aguilera, G., and Eiden, L. E. (2011) Pituitary adenylate cyclase-activating polypeptide (PACAP) controls stimulus- transcription coupling in the hypothalamic-pituitary-adrenal axis to mediate sustained hormone secretion during stress. J. Neuroendocrinol. 23, 944-955
44. Hashimoto, H., Shintani, N., Tanaka, K., Mori, W., Hirose, M., Matsuda, T., Sakaue, M., Miyazaki, J.-I., Niwa, H., Tashiro, F., Yamamoto, K., Koga, K., Tomimoto, S., Kunugi, A., Suetake, S., and Baba, A. (2001) Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc. Natl. Acad. Sci. U. S. A. 98, 13355-13360 (Pubitemid 33051367)
45. Chen, D., Buchanan, G. F., Ding, J. M., Hannibal, J., and Gillette, M. U. (1999) Pituitary adenylyl cyclase-activating peptide: a pivotal modulator of glutamatergic regulation of the suprachiasmatic circadian clock. Proc. Natl. Acad. Sci. U. S. A. 96, 13468-13473
46. Lelievre, V., Seksenyan, A., Nobuta, H., Yong, W. H., Chhith, S., Niewiadomski, P., Cohen, J. R., Dong, H., Flores, A., Liau, L. M., Kornblum, H. I., Scott, M. P., and Waschek, J. A. (2008) Disruption of the PACAP gene promotes medulloblastoma in ptc1 mutant mice. Dev. Biol. 313, 359-370 (Pubitemid 350298324)
47. Vaudry, D., Gonzalez, B. J., Basille, M., Anouar, Y., Fournier, A., and Vaudry, H. (1998) Pituitary adenylate cyclase-activating polypeptide stimulates both c-Fos gene expression and cell survival in rat cerebellar granule neurons through activation of the protein kinase A pathway. Neuroscience 84, 801-812 (Pubitemid 28137896)
48. Vaudry, D., Falluel-Morel, A., Basille, M., Pamantung, T. F., Fontaine, M., Fournier, A., Vaudry, H., and Gonzalez, B. J. (2003) Pituitary adenylate cyclase-activating polypeptide prevents C2-ceramide-induced apoptosis of cerebellar granule cells. J. Neurosci. Res. 72, 303-316 (Pubitemid 36504699)
49. +channels in cerebellar neurons. Proc. Natl. Acad. Sci. U. S. A. 104, 2519-2524
50. Roscioni, S. S., Kistemaker, L. E., Menzen, M. H., Elzinga, C. R., Gosens, R., Halayko, A. J., Meurs, H., and Schmidt, M. (2009) PKA and Epac cooperate to augment bradykinin-induced interleukin-8 release from human airway smooth muscle cells. Respir. Res. 10, 88
51. Nijholt, I. M., Dolga, A. M., Ostroveanu, A., Luiten, P. G., Schmidt, M., and Eisel, U. L. (2008) Neuronal AKAP150 coordinates PKA and Epac-mediated PKB/Akt phosphorylation. Cell. Signal. 20, 1715-1724
52. Pham, N., Cheglakov, I., Koch, C. A., de Hoog, C. L., Moran, M. F., and Rotin, D. (2000) The guanine nucleotide exchange factor CNrasGEF activates ras in response to cAMP and cGMP. Curr. Biol. 10, 555-558 (Pubitemid 30308317)
53. Sun, H., Charles, C. H., Lau, L. F., and Tonks, N. K. (1993) MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75, 487-493 (Pubitemid 23335074)
54. Burgun, C., Esteve, L., Humblot, N., Aunis, D., and Zwiller, J. (2000) Cyclic AMP-elevating agents induce the expression of MAP kinase phosphatase-1 in PC12 cells. FEBS Lett. 484, 189-193
55. Engh, R. A., Girod, A., Kinzel, V., Huber, R., and Bossemeyer, D. (1996) Crystal structures of catalytic subunit of cAMP-dependent protein kinase in complex with isoquinolinesulfonyl protein kinase inhibitors H7, H8, and H89. Structural implications for selectivity. J. Biol. Chem. 271, 26157-26164 (Pubitemid 26347460)
56. Cheadle, C., Nesterova, M., Watkins, T., Barnes, K. C., Hall, J. C., Rosen, A., Becker, K. G., and Cho-Chung, Y. S. (2008) Regulatory subunits of PKA define an axis of cellular proliferation/ differentiation in ovarian cancer cells. BMC Med. Genomics 1, 43