PACAP-induced ERK activation in HEK cells expressing PAC1 receptors involves both receptor internalization and PKC signaling

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 11, 2014, Pages

  May, Victor ^a   Buttolph, Thomas R ^a   Girard, Beatrice M ^a   Clason, Todd A ^a   Parsons, Rodney L ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

ERK phosphorylation; Pituitary adenylate cyclase activating polypeptide PAC1 receptor; Protein kinase C; Signaling endosome

Indexed keywords

CYCLIC AMP; DIACYLGLYCEROL; G PROTEIN COUPLED RECEPTOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE; PAC1 RECEPTOR; PHOSPHOLIPASE C; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL;

ERK PHOSPHORYLATION; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE PAC1 RECEPTOR; PROTEIN KINASE C; SIGNALING ENDOSOME;

CELL NUCLEUS; CYTOPLASM; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTEIN KINASE C; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; SIGNAL TRANSDUCTION;

EID: 84901768188     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00001.2014     Document Type: Article

References (50)

1. Ahn S, Senoy SK, Wei H, Lefkowitz RJ. Differential kinetic and spatial patterns of β-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J Biol Chem 279: 35518-35525, 2004.
2. Barrie AP, Clohessy AM, Buensuceso CS, Rogers MV, Allen JM. Pituitary adenylyl cyclase-activating peptide stimulates extracellular signal-regulated kinase 1 or 2 (ERK1/2) activity in a Ras-independent, mitogen-activated protein kinase/ERK kinase 1 or 2-dependent manner in PC12 cells. J Biol Chem 272: 19666-19671, 1997.
3. Bouschet T, Perez V, Fernandez C, Bockaert J, Eychene A, Journot L. Stimulation of the ERK pathway by GTP-loaded Rap1 requires the concomitant activation of Ras, protein kinase C, and protein kinase A in neuronal cells. J Biol Chem 278: 4778-4785, 2003.
4. Braas KM, May V. Pituitary adenylate cyclase-activating polypeptides directly stimulate sympathetic neuron NPY release through PAC1 receptor isoform activation of specific intracellular signaling pathways. J Biol Chem 274: 27702-27710, 1999.
5. Broca C, Quoyer J, Costes S, Linck N, Varrault A, Deffayet PM, Bockaert J, Dalle S, Bertrand G. β-Arrestin 1 is required for PAC1 receptor-mediated potentiation of long-lasting ERK1/2 activation by glucose in pancreatic beta-cells. J Biol Chem 284: 4332-4342, 2009.
6. Calebiro D, Nikolaev VO, Lohse MJ. Imaging of persistent cAMP signaling by internalized G protein-coupled receptors. J Mol Endocrinol 45: 1-8, 2010.
7. Calebiro D, Nikolaev VO, Persani L, Lohse MJ. Signaling by internalized G-protein-coupled receptors. Trends Pharmacol Sci 31: 221-228, 2010.
8. Calebiro D, Nikolaev VO, Gagliani MC, de Filippis T, Dees C, Tacchetti C, Persani L, Lohse MJ. Persistent cAMP signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7: e1000172, 2009.
9. Chemin J, Mezghrani A, Bidaud I, Dupasquier S, Marger F, Barrère C, Nargeot J, Lory P. Temperature-dependent modulation of CaV3 T-type calcium channels by protein kinases C and A in mammalian cells. J Biol Chem 282: 32710-32718, 2007.
10. DeFea KA, Zalevsky J, Thoma MS, Déry O, Mullins RD, Bunnett NW. β-Arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J Cell Biol 148: 1267-1281, 2000.
11. Deutsch PJ, Sun Y. 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, 1992.
12. Dumaz N, Marais R. Integrating signals between cAMP and the RAS/ RAF/MEK/ERK signalling pathways. FEBS J 272: 3491-3504, 2005.
13. Emery AC, Eiden LE. Signaling through the neuropeptide GPCR PAC1 induces neuritogenesis via a single linear cAMP-and ERK-dependent pathway using a novel cAMP sensor. FASEB J 26: 3199-3211, 2012.
14. Ferrandon S, Feinstein TN, Castro M, Wang B, Bouley R, Potts JT, Gardella TJ, Vilardaga JP. Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 5: 734-742, 2009.
15. Girard BM, Keller ET, Schutz KC, May V, Braas KM. Pituitary adenylate cyclase activating polypeptide and PAC1 receptor signaling increase Homer 1a expression in central and peripheral neurons. Regul Pept 123: 107-116, 2004.
16. Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls WA, Braas KM, May V. 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, 2009.
17. Harmar AJ, Fahrenkrug J, Gozes I, Laburthe M, May V, Pisegna JR, Vaudry D, Vaudry H, Waschek JA, Said SI. Pharmacology and functions of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Br J Pharmacol 166: 4-17, 2012.
18. Hoffman JF, Linderman JJ, Omann GM. Receptor up-regulation, internalization, and interconverting receptor states. Critical components of a quantitative description of N-formyl peptide-receptor dynamics in the neutrophil. J Biol Chem 271: 18394-18404, 1996.
19. Irannejad R, Tomshine JC, Tomshine JR, Chevalier M, Mahoney JP, Steyaert J, Rasmussen SG, Sunahara RK, El-Samad H, Huang B, von Zastrow M. Conformational biosensors reveal GPCR signalling from endosomes. Nature 495: 534-538, 2013.
20. Jalink K, Moolenaar WH. G protein-coupled receptors: the inside story. Bioessays 32: 13-16, 2010.
21. Lehmann ML, Mustafa T, Eiden AM, Herkenham M, Eiden LE. PACAP-deficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress. Psychoneuroendocrinology 38: 702-715, 2013.
22. Liu F, He K, Yang X, Xu N, Liang Z, Xu M, Zhao X, Han Q, Zhang Y. α1A-Adrenergic receptor induces activation of extracellular signalregulated kinase 1/2 through endocytic pathway. PLos One 6: e21520, 2011.
23. Luttrell LM, Gesty-Palmer D. Beyond desensitization: physiological relevance of arrestin-dependent signaling. Pharmacol Rev 62: 305-330, 2010.
24. Luttrell LM, Ferguson SS, Daaka Y, Miller WE, Maudsley S, Della Rocca GJ, Lin F, Kawakatsu H, Owada K, Luttrell DK, Caron MG, Lefkowitz RJ. β-Arrestin-dependent formation of β2-adrenergic receptor-Src protein kinase complexes. Science 283: 655-661, 1999.
25. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850, 2006.
26. Magalhaes AC, Dunn H, Ferguson SS. Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins. Br J Pharmacol 165: 1717-1736, 2012.
27. May V, Schiller MR, Eipper BA, Mains RE. Kalirin Dbl-homology guanine nucleotide exchange factor 1 domain initiates new axon outgrowths via RhoG-mediated mechanisms. J Neurosci 22: 6980-6990, 2002.
28. May V, Lutz E, MacKenzie C, Schutz KC, Dozark K, Braas KM. Pituitary adenylate cyclase-activating polypeptide (PACAP)/PACAP1HOP1 receptor activation coordinates multiple neurotrophic signaling pathways: Akt activation through phosphatidylinositol 3-kinase-γ and vesicle endocytosis for neuronal survival. J Biol Chem 285: 9749-9761, 2010.
29. McCann CM, Tapia JC, Kim H, Coggan JS, Lichtman JW. Rapid and modifiable neurotransmitter receptor dynamics at a neuronal synapse in vivo. Nat Neurosci 11: 807-815, 2008.
30. McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533, 2011.
31. Merriam LA, Baran CN, Girard BM, Hardwick JC, May V, Parsons RL. Pituitary adenylate cyclase 1 receptor internalization and endosomal signaling mediate the pituitary adenylate cyclase activating polypeptideinduced increase in guinea pig cardiac neuron excitability. J Neurosci 33: 4614-4622, 2013.
32. Milligan G. G protein-coupled receptor dimerization: function and ligand pharmacology. Mol Pharmacol 66: 1-7, 2004.
33. Mullershausen F, Zecri F, Cetin C, Billich A, Guerini D, Seuwen K. Persistent signaling induced by FTY720-phosphate is mediated by internalized S1P1 receptors. Nat Chem Biol 5: 428-434, 2009.
34. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG. Association of β-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 274: 32248-32257, 1999.
35. Oakley RH, Laporte SA, Holt JA, Caron MG, Barak LS. Differential affinities of visual arrestin, β-arrestin1, and β-arrestin2 for G proteincoupled receptors delineate two major classes of receptors. J Biol Chem 275: 17201-17210, 2000.
36. Otto C, Kovalchuk Y, Wolfer DP, Gass P, Martin M, Zuschratter W, Gröne HJ, Kellendonk C, Tronche F, Maldonado R, Lipp HP, Konnerth A, Schütz G. 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, 2001.
37. Perez-Aso M, Segura V, Montó F, Barettino D, Noguera MA, Milligan G, D'Ocon P. The three α1-adrenoceptor subtypes show different spatiotemporal mechanisms of internalization and ERK1/2 phosphorylation. Biochim Biophys Acta 1833: 2322-2333, 2013.
38. Pisegna JR, Wank SA. Cloning and characterization of the signal transduction of four splice variants of the human pituitary adenylate cyclase activating polypeptide receptor. Evidence for dual coupling to adenylate cyclase and phospholipase C. J Biol Chem 271: 17267-17274, 1996.
39. Popp RL, Reneau JC, Brotherton BJ. Activation of protein kinase C enhances NMDA-induced currents in primary cultured cerebellar granule cells: effect of temperature and NMDA NR2 subunit composition. Eur J Pharmacol 599: 1-10, 2008.
40. Roskoski RJ. ERK1/2 kinases: structure MAP, function, regulation. Pharmacol Res 66: 105-143, 2012.
41. Rozengurt E. Mitogenic signaling pathways induced by G proteincoupled receptors. J Cell Physiol 213: 589-602, 2007.
42. Scita G, Di Fiore PP. The endocytic matrix. Nature 463: 464-473, 2010.
43. Shenoy SK, Lefkowitz RJ. Multifaceted roles of β-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem J 375: 503-515, 2003.
44. Spengler D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg PH, Journot L. Differential signal transduction by five splice variants of the PACAP receptor. Nature 365: 170-175, 1993.
45. Stork PJ, Schmitt JM. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12: 258-266, 2002.
46. Tohgo A, Choy EW, Gesty-Palmer D, Pierce KL, Laporte S, Oakley RH, Caron MG, Lefkowitz RJ, Luttrell LM. The stability of the G protein-coupled receptor-β-arrestin interaction determines the mechanism and functional consequence of ERK activation. J Biol Chem 278: 6258-6267, 2003.
47. Vaudry D, Gonzalez BJ, Basille M, Fournier A, Vaudry H. Neurotrophic activity of pituitary adenylate cyclase-activating polypeptide on rat cerebellar cortex during development. Proc Natl Acad Sci USA 96: 9415-9420, 1999.
48. Villalba M, Bockaert J, Journot L. Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J Neurosci 17: 83-90, 1997.
49. von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, MacGregor KA, Tomilin N, Pechstein A, Chau N, Chircop M, Sakoff J, von Kries JP, Saenger W, Kräusslich HG, Shupliakov O, Robinson PJ, McCluskey A, Haucke V. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146: 471-484, 2011.
50. Werthmann RC, Volpe S, Lohse MJ, Calebiro D. Persistent cAMP signaling by internalized TSH receptors occurs in thyroid but not in HEK293 cells. FASEB J 26: 2043-2048, 2012.