PACAP receptor pharmacology and agonist bias: Analysis in primary neurons and glia from the trigeminal ganglia and transfected cells

British Journal of Pharmacology

Volumn 171, Issue 6, 2014, Pages 1521-1533

  Walker, C S ^a,b   Sundrum, T ^a   Hay, D L ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

bias signalling; G protein coupled receptor; glia; intracellular signalling; neuron; PAC1; PACAP; primary culture; trigeminal ganglia; VIP

Indexed keywords

CYCLIC AMP; HORMONE RECEPTOR STIMULATING AGENT; MITOGEN ACTIVATED PROTEIN KINASE; PACAP AGONIST; PITUITARY ADENYLATE CYCLASE-ACTIVATING PEPTIDE 27; PITUITARY ADENYLATE CYCLASE-ACTIVATING PEPTIDE 38; POLYPEPTIDE; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; GENETIC TRANSFECTION; GLIA CELL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TRIGEMINUS GANGLION;

BIAS SIGNALLING; G-PROTEIN COUPLED RECEPTOR; GLIA; INTRACELLULAR SIGNALLING; NEURON; PAC1; PACAP; PRIMARY CULTURE; TRIGEMINAL GANGLIA; VIP;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; MOLECULAR SEQUENCE DATA; NEUROGLIA; NEURONS; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; TRANSFECTION;

EID: 84895739766     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12541     Document Type: Article

References (76)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581.
2. Amin FM, Asghar MS, Hougaard A, Hansen AE, Larsen VA, de Koning PJ, et al. (2013). Magnetic resonance angiography of intracranial and extracranial arteries in patients with spontaneous migraine without aura: a cross-sectional study. Lancet Neurol 12: 454-461.
3. Bailey RJ, Hay DL, (2006). Pharmacology of the human CGRP1 receptor in Cos 7 cells. Peptides 27: 1367-1375.
4. Baun M, Pedersen MH, Olesen J, Jansen-Olesen I, (2012). Dural mast cell degranulation is a putative mechanism for headache induced by PACAP-38. Cephalalgia 32: 337-345.
5. Bellamy J, Bowen EJ, Russo AF, Durham PL, (2006). Nitric oxide regulation of calcitonin gene-related peptide gene expression in rat trigeminal ganglia neurons. Eur J Neurosci 23: 2057-2066.
6. Blechman J, Levkowitz G, (2013). Alternative splicing of the pituitary adenylate cyclase-activating polypeptide receptor PAC1: mechanisms of fine tuning of brain activity. Front Endocrinol 4: 55.
7. Bowen EJ, Schmidt TW, Firm CS, Russo AF, Durham PL, (2006). Tumor necrosis factor-alpha stimulation of calcitonin gene-related peptide expression and secretion from rat trigeminal ganglion neurons. J Neurochem 96: 65-77.
8. Broca C, Quoyer J, Costes S, Linck N, Varrault A, Deffayet PM, et al. (2009). beta-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.
9. Chaudhary P, Baumann TK, (2002). Expression of VPAC2 receptor and PAC1 receptor splice variants in the trigeminal ganglion of the adult rat. Brain Res Mol Brain Res 104: 137-142.
10. Chidiac P, Ross EM, (1999). Phospholipase C-beta1 directly accelerates GTP hydrolysis by Galphaq and acceleration is inhibited by Gbeta gamma subunits. J Biol Chem 274: 19639-19643.
11. Christopoulos A, Christopoulos G, Morfis M, Udawela M, Laburthe M, Couvineau A, et al. (2003). Novel receptor partners and function of receptor activity-modifying proteins. J Biol Chem 278: 3293-3297. (Pubitemid 36801242)
12. Couvineau A, Laburthe M, (2012). The family B1 GPCR: structural aspects and interaction with accessory proteins. Curr Drug Targets 13: 103-115.
13. Crouch MF, Osmond RI, (2008). New strategies in drug discovery for GPCRs: high throughput detection of cellular ERK phosphorylation. Comb Chem High Throughput Screen 11: 344-356. (Pubitemid 351830305)
14. Dautzenberg FM, Mevenkamp G, Wille S, Hauger RL, (1999). N-terminal splice variants of the type I PACAP receptor: isolation, characterization and ligand binding/selectivity determinants. J Neuroendocrinol 11: 941-949.
15. Davis-Taber R, Baker S, Lehto SG, Zhong C, Surowy CS, Faltynek CR, et al. (2008). Central pituitary adenylate cyclase 1 receptors modulate nociceptive behaviors in both inflammatory and neuropathic pain states. J Pain 9: 449-456.
16. DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK, (2007). Beta-arrestins and cell signaling. Annu Rev Physiol 69: 483-510.
17. Dressler H, Economides K, Favara S, Wu NN, Pang Z, Polites HG, (2013). The CRE luc bioluminescence transgenic mouse model for detecting ligand activation of GPCRs. J Biomol Screen 19: 232-241.
18. Durham PL, Russo AF, (1999). Regulation of calcitonin gene-related peptide secretion by a serotonergic antimigraine drug. J Neurosci 19: 3423-3429. (Pubitemid 29203122)
19. Edvinsson L, (2013). Role of VIP/PACAP in primary headaches. Cephalalgia 33: 1070-1072.
20. Eikermann-Haerter K, Moskowitz MA, (2008). Animal models of migraine headache and aura. Curr Opin Neurol 21: 294-300. (Pubitemid 351653979)
21. Firner M, Greffrath W, Treede RD, (2006). Phosphorylation of extracellular signal-related protein kinase is required for rapid facilitation of heat-induced currents in rat dorsal root ganglion neurons. Neurosci 143: 253-263. (Pubitemid 44667309)
22. Fu Y, Zhong H, Nanamori M, Mortensen RM, Huang X, Lan K, et al. (2004). RGS-insensitive G-protein mutations to study the role of endogenous RGS proteins. Methods Enzymol 389: 229-243. (Pubitemid 39119071)
23. Furness SG, Wootten D, Christopoulos A, Sexton PM, (2012). Consequences of splice variation on secretin family G protein-coupled receptor function. Br J Pharmacol 166: 98-109.
24. Gao YJ, Ji RR, (2009). c-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury. Open Pain J 2: 11-17.
25. Gerdin MJ, Eiden LE, (2007). Regulation of PC12 cell differentiation by cAMP signaling to ERK independent of PKA: do all the connections add up. Sci STKE 2007: pe15.
26. Gingell JJ, Qi T, Bailey RJ, Hay DL, (2010). A key role for tryptophan 84 in receptor activity-modifying protein 1 in the amylin 1 receptor. Peptides 31: 1400-1404.
27. Harmar AJ, Fahrenkrug J, Gozes I, Laburthe M, May V, Pisegna JR, et al. (2012). Pharmacology and functions of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide: IUPHAR review 1. Br J Pharmacol 166: 4-17.
28. Hashimoto H, Shintani N, Baba A, (2006). New insights into the central PACAPergic system from the phenotypes in PACAP- and PACAP receptor-knockout mice. Ann N Y Acad Sci 1070: 75-89. (Pubitemid 44126626)
29. Hay DL, Christopoulos G, Christopoulos A, Sexton PM, (2006). Determinants of 1-piperidinecarboxamide, N-[2-[[5-amino-l-[[4-(4-pyridinyl)-l-piperazinyl] carbonyl]pentyl]amino]-1-[(3,5-d ibromo-4-hydroxyphenyl)methyl]-2-oxoethyl]-4- (1,4-dihydro-2-oxo-3(2H)-quinazoliny l) (BIBN4096BS) affinity for calcitonin gene-related peptide and amylin receptors-the role of receptor activity modifying protein 1. Mol Pharmacol 70: 1984-1991. (Pubitemid 44771914)
30. Hou X, Vandermeers A, Gourlet P, Vandermeers-Piret MC, Robberecht P, (1994). Structural requirements for the occupancy of rat brain PACAP receptors and adenylate cyclase activation. Neuropharmacology 33: 1189-1195. (Pubitemid 24333934)
31. Jorgensen R, Kubale V, Vrecl M, Schwartz TW, Elling CE, (2007). Oxyntomodulin differentially affects glucagon-like peptide-1 receptor beta-arrestin recruitment and signaling through Galpha(s). J Pharmacol Exp Ther 322: 148-154. (Pubitemid 46956350)
32. Kaiser EA, Russo AF, (2013). CGRP and migraine: could PACAP play a role too. Neuropeptides 47: 451-461.
33. Katritch V, Cherezov V, Stevens RC, (2013). Structure-function of the G protein-coupled receptor superfamily. Annu Rev Pharmacol Toxicol 53: 531-556.
34. Kenakin T, Christopoulos A, (2013). Signalling bias in new drug discovery: detection, quantification and therapeutic impact. Nat Rev Drug Discov 12: 205-216.
35. Kienlen Campard P, Crochemore C, Rene F, Monnier D, Koch B, Loeffler JP, (1997). PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/PKA signaling pathway. DNA Cell Biol 16: 323-333.
36. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
37. Knutsson M, Edvinsson L, (2002). Distribution of mRNA for VIP and PACAP receptors in human cerebral arteries and cranial ganglia. Neuroreport 13: 507-509. (Pubitemid 34293200)
38. Komatsu T, Mizoguchi H, Sasaki M, Sakurada C, Tsuzuki M, Sakurada S, et al. (2011). Inhibition of ERK phosphorylation by substance P N-terminal fragment decreases capsaicin-induced nociceptive response. Neuropharmacology 61: 608-613.
39. Kumar S, Pioszak A, Zhang C, Swaminathan K, Xu HE, (2011). Crystal structure of the PAC1R extracellular domain unifies a consensus fold for hormone recognition by class B G-protein coupled receptors. PLoS ONE 6: e19682.
40. Kuris A, Xu CB, Zhou MF, Tajti J, Uddman R, Edvinsson L, (2007). Enhanced expression of CGRP in rat trigeminal ganglion neurons during cell and organ culture. Brain Res 1173: 6-13. (Pubitemid 47454602)
41. Laburthe M, Couvineau A, Tan V, (2007). Class II G protein-coupled receptors for VIP and PACAP: structure, models of activation and pharmacology. Peptides 28: 1631-1639. (Pubitemid 47371033)
42. Li J, Vause CV, Durham PL, (2008). Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res 1196: 22-32.
43. Llinas RR, Walton KD, Lang EJ, (2004). Chapter 7. Cerebellum. In:, Shepherd GM, (ed.). The Synaptic Organization of the Brain, 4th edn. Oxford University Press: New York, p. 271.
44. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
45. Markovics A, Kormos V, Gaszner B, Lashgarara A, Szoke E, Sandor K, et al. (2012). Pituitary adenylate cyclase-activating polypeptide plays a key role in nitroglycerol-induced trigeminovascular activation in mice. Neurobiol Dis 45: 633-644.
46. Maudsley S, Patel SA, Park SS, Luttrell LM, Martin B, (2012). Functional signaling biases in G protein-coupled receptors: game theory and receptor dynamics. Mini Rev Med Chem 12: 831-840.
47. Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, Jiang L, et al. (1989). Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 164: 567-574. (Pubitemid 19269770)
48. Moller K, Zhang YZ, Hakanson R, Luts A, Sjolund B, Uddman R, et al. (1993). Pituitary adenylate cyclase activating peptide is a sensory neuropeptide: immunocytochemical and immunochemical evidence. Neuroscience 57: 725-732. (Pubitemid 23350559)
49. Monaghan TK, Mackenzie CJ, Plevin R, Lutz EM, (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)
50. Morfis M, Tilakaratne N, Furness SG, Christopoulos G, Werry TD, Christopoulos A, et al. (2008). Receptor activity-modifying proteins differentially modulate the G protein-coupling efficiency of amylin receptors. Endocrinology 149: 5423-5431.
51. Nakajima E, Walkup RD, Fujii A, Shearer TR, Azuma M, (2013). Pituitary adenylate cyclase-activating peptide induces neurite outgrowth in cultured monkey trigeminal ganglion cells: involvement of receptor PAC1. Mol Vis 19: 174-183.
52. Olesen J, Ashina M, (2011). Emerging migraine treatments and drug targets. Trends Pharmacol Sci 32: 352-359.
53. Olianas MC, Ennas MG, Lampis G, Onali P, (1996). Presence of pituitary adenylate cyclase-activating polypeptide receptors in Y-79 human retinoblastoma cells. J Neurochem 67: 1293-1300. (Pubitemid 26277944)
54. Pisegna JR, Wank SA, (1996). 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. (Pubitemid 26244284)
55. Poulin B, Butcher A, McWilliams P, Bourgognon JM, Pawlak R, Kong KC, et al. (2010). The M3-muscarinic receptor regulates learning and memory in a receptor phosphorylation/arrestin-dependent manner. Proc Natl Acad Sci U S A 107: 9440-9445.
56. Qi T, Dong M, Watkins HA, Wootten D, Miller LJ, Hay DL, (2013). Receptor activity-modifying protein-dependent impairment of calcitonin receptor splice variant Δ(1-47)hCT((a)) function. Br J Pharmacol 168: 644-657.
57. Rahmann A, Wienecke T, Hansen JM, Fahrenkrug J, Olesen J, Ashina M, (2008). Vasoactive intestinal peptide causes marked cephalic vasodilation, but does not induce migraine. Cephalalgia 28: 226-236. (Pubitemid 351172031)
58. Rask-Andersen M, Almen MS, Schioth HB, (2011). Trends in the exploitation of novel drug targets. Nat Rev Drug Discov 10: 579-590.
59. Rat D, Schmitt U, Tippmann F, Dewachter I, Theunis C, Wieczerzak E, et al. (2011). Neuropeptide pituitary adenylate cyclase-activating polypeptide (PACAP) slows down Alzheimer's disease-like pathology in amyloid precursor protein-transgenic mice. FASEB J 25: 3208-3218.
60. Reglodi D, Borzsei R, Bagoly T, Boronkai A, Racz B, Tamas A, et al. (2008). Agonistic behavior of PACAP6-38 on sensory nerve terminals and cytotrophoblast cells. J Mol Neurosci 36: 270-278.
61. Ritter SL, Hall RA, (2009). Fine-tuning of GPCR activity by receptor-interacting proteins. Nat Rev Mol Cell Biol 10: 819-830.
62. Robberecht P, Gourlet P, De Neef P, Woussen-Colle MC, Vandermeers-Piret MC, Vandermeers A, et al. (1992a). Receptor occupancy and adenylate cyclase activation in AR 4-2J rat pancreatic acinar cell membranes by analogs of pituitary adenylate cyclase-activating peptides amino-terminally shortened or modified at position 1, 2, 3, 20, or 21. Mol Pharmacol 42: 347-355. (Pubitemid 23026170)
63. Robberecht P, Gourlet P, De Neef P, Woussen-Colle MC, Vandermeers-Piret MC, Vandermeers A, et al. (1992b). Structural requirements for the occupancy of pituitary adenylate-cyclase-activating-peptide (PACAP) receptors and adenylate cyclase activation in human neuroblastoma NB-OK-1 cell membranes. Discovery of PACAP(6-38) as a potent antagonist. Eur J Biochem 207: 239-246.
64. Schytz HW, Birk S, Wienecke T, Kruuse C, Olesen J, Ashina M, (2009). PACAP38 induces migraine-like attacks in patients with migraine without aura. Brain 132 (Pt 1): 16-25.
65. Schytz HW, Olesen J, Ashina M, (2010). The PACAP receptor: a novel target for migraine treatment. Neurother 7: 191-196.
66. Sherwood NM, Krueckl SL, McRory JE, (2000). The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr Rev 21: 619-670. (Pubitemid 32113287)
67. Spongier D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg PH, et al. (1993). Differential signal transduction by five splice variants of the PACAP receptor. Nature 365: 170-175. (Pubitemid 23282064)
68. Tajti J, Kuris A, Vecsei L, Xu CB, Edvinsson L, (2011). Organ culture of the trigeminal ganglion induces enhanced expression of calcitonin gene-related peptide via activation of extracellular signal-regulated protein kinase 1/2. Cephalalgia 31: 95-105.
69. Tfelt-Hansen PC, Olesen J, (2012). The 5-HT1F receptor agonist lasmiditan as a potential treatment of migraine attacks: a review of two placebo-controlled phase II trials. J Headache Pain 13: 271-275.
70. Tuka B, Helyes Z, Markovics A, Bagoly T, Szolcsanyi J, Szabo N, et al. (2013). Alterations in PACAP-38-like immunoreactivity in the plasma during ictal and interictal periods of migraine patients. Cephalalgia 33: 1085-1095.
71. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, et al. (2009). Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61: 283-357.
72. Villalba M, Bockaert J, Journot L, (1997). 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. (Pubitemid 27008852)
73. Wess J, Nakajima K, Jain S, (2013). Novel designer receptors to probe GPCR signaling and physiology. Trends Pharmacol Sci 34: 385-392.
74. van der Westhuizen ET, Werry TD, Sexton PM, Summers RJ, (2007). The relaxin family peptide receptor 3 activates extracellular signal-regulated kinase 1/2 through a protein kinase C-dependent mechanism. Mol Pharmacol 71: 1618-1629. (Pubitemid 47010915)
75. Wootten D, Lindmark H, Kadmiel M, Willcockson H, Caron KM, Barwell J, et al. (2013). Receptor activity modifying proteins (RAMPs) interact with the VPAC2 receptor and CRF1 receptors and modulate their function. Br J Pharmacol 168: 822-834.
76. Zhang Z, Winborn CS, Marquez de Prado B, Russo AF, (2007). Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J Neurosci 27: 2693-2703. (Pubitemid 46393588)