Pituitary adenylate cyclase-activating polypeptide plays a key role in nitroglycerol-induced trigeminovascular activation in mice

Neurobiology of Disease

Volumn 45, Issue 1, 2012, Pages 633-644

  Markovics, Adrienn ^a   Kormos, Viktoria ^a   Gaszner, Balazs ^a   Lashgarara, Arvin ^a   Szoke, Eva ^a   Sandor, Katalin ^a   Szabadfi, Krisztina ^b   Tuka, Bernadett ^c   Tajti, Janos ^c   Szolcsanyi, Janos ^a,f   Pinter, Erika ^a,f   Hashimoto, Hitoshi ^d,e   Kun, Jozsef ^a   Reglodi, Dora ^a   Helyes, Zsuzsanna ^a,f  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

^c UNIVERSITY OF SZEGED   (Hungary)

^d OSAKA UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f PharmInVivo Ltd   (Hungary)

Author keywords

C Fos immunohistochemistry; Laser Doppler blood perfusion scanning; Light aversive behavior; Light dark box; Meningeal microcirculation; PAC1 receptor immunohistochemistry

Indexed keywords

GLYCERYL TRINITRATE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; BLOOD FLOW; CARDIOVASCULAR SYSTEM; CONTROLLED STUDY; GENE DELETION; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; MICROCIRCULATION; MIGRAINE; MOUSE; MOUSE STRAIN; NERVOUS SYSTEM; NONHUMAN; PATHOPHYSIOLOGY; PHOTOPHOBIA; PRIORITY JOURNAL; SENSITIZATION; TRIGEMINAL NUCLEUS; TRIGEMINAL NUCLEUS CAUDALIS; TRIGEMINOVASCULAR SYSTEM; TRIGEMINUS GANGLION; VASODILATATION;

ANIMALS; BLOOD VESSELS; MICE; MICE, KNOCKOUT; NEURONS; NITROGLYCERIN; PHOTOPHOBIA; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; TRIGEMINAL NUCLEI; VASODILATION;

EID: 81955164095     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.10.010     Document Type: Article

References (86)

1. Allais A., Burel D., Isaac E.R., et al. Altered cerebellar development in mice lacking pituitary adenylate cyclase-activating polypeptide. Eur. J. Neurosci. 2007, 25:2604-2618.
2. Ausubel R.M., et al. Short Protocols in Molecular Biology, 2nd Edition, Eds., John Wiley and Sons.1992; pp. 14-24-14-30.
3. Baeres F.M., Møller M. Origin of PACAP-immunoreactive nerve fibers innervating the subarachnoidal blood vessels of the rat brain. J. Cereb. Blood Flow Metab. 2004, 24:628-635.
4. Banks W.A., Kastin A.J., Komaki G., et al. Passage of pituitary adenylate cyclase activating polypeptide1-27 and pituitary adenylate cyclase activating polypeptide1-38 across the blood-brain barrier. J. Pharmacol. Exp. Ther. 1993, 267:690-696.
5. Bergerot A., Holland P.R., Akerman S., et al. Animal models of migraine: looking at the component parts of a complex disorder. Eur. J. Neurosci. 2006, 24:1517-1534.
6. Boni L.J., Ploug K.B., Olesen J., et al. The in vivo effect of VIP, PACAP-38 and PACAP-27 and mRNA expression of their receptors in rat middle meningeal artery. Cephalalgia 2009, 29(8):837-847.
7. Bourgault S., Vaudry D., Dejda A., et al. Pituitary adenylate cyclase-activating polypeptide: focus on structure-activity relationships of a neuroprotective peptide. Curr. Med. Chem. 2009, 16(33):4462-4480.
8. Brabet P., Diriong S., Journot L., et al. Localization of the human pituitary adenylate cyclase-activating polypeptide receptor (PACAP1-R) gene to 7p15-p14 by fluorescence in situ hybridization. Genomics 1996, 38(1):100-102.
9. Bullitt E. Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J. Comp. Neurol. 1990, 296(4):517-530.
10. Buzzi M.G., Tassorelli C. Experimental models of migraine. Handb. Clin. Neurol. 2010, 97:109-123.
11. Chan K.Y., Vermeersch S., de Hoon J., et al. Potential mechanisms of prospective antimigraine drugs: a focus on vascular (side) effects. Pharmacol. Ther. 2011, 129(3):332-351.
12. Choi J.Y., Oh K., Kim B.J., et al. Usefulness of a photophobia questionnaire in patients with migraine. Cephalalgia 2009, 29(9):953-959.
13. Christiansen T., Bruun A., Knight Y.E., Goadsby P.J., Edvinsson L. Immunoreactivity of NOS, CGRP, PACAP, SP and VIP in the trigeminal nucleus caudalis and int he cervical spinal cord C1 and C2 of the cat. J. Headache Pain 2003, 4:156-163.
14. Delgado M., Munoz-Elias E.J., Martinez C., et al. VIP and PACAP38 modulate cytokine and nitric oxide production in peritoneal macrophages and macrophage cell lines. Ann. N. Y. Acad. Sci. 1999, 897:401-414.
15. Dickinson T., Fleetwood-Walker S.M., Mitchell R., et al. Evidence for roles of vasoactive intestinal polypeptide (VIP) and pituitary adenylate cyclase activating polypeptide (PACAP) receptors in modulating the responses of rat dorsal horn neurons to sensory inputs. Neuropeptides 1997, 31:175-185.
16. Edvinsson L., Owman C., Sjoberg N.O. Autonomic nerves, mast cells, and amine receptors in human brain vessels. A histochemical and pharmacological study. Brain Res. 1976, 115:377-393.
17. Edvinsson L., Elsås T., Suzuki N., et al. Origin and co-localization of nitric oxide synthase, CGRP, PACAP, and VIP in the cerebral circulation of the rat. Microsc. Res. Tech. 2001, 53(3):221-228.
18. Edvinsson L., Linde M. New drugs in migraine treatment and prophylaxis: telcagepant and topiramate. Lancet 2010, 376(9741):645-655.
19. Fahrenkrug J., Hannibal J. Pituitary adenylate cyclase activating polypeptide immunoreactivity in capsaicin-sensitive nerve fibres supplying the rat urinary tract. Neuroscience 1998, 83:1261-1272.
20. Gaszner B., Korosi A., Palkovits M., et al. Neuropeptide Y activates urocortin 1 neurons in the nonpreganglionic Edinger-Westphal nucleus. J. Comp. Neurol. 2007, 500(4):708-719.
21. Gaszner B., Jensen K.O., Farkas J., et al. Effects of maternal separation on dynamics of urocortin 1 and brain-derived neurotrophic factor in the rat non-preganglionic Edinger-Westphal nucleus. Int. J. Dev. Neurosci. 2009, 27(5):439-451.
22. Girard B.A., Lelievre V., Braas K.M., et al. Noncompensation in peptide/receptor gene expression and distinct behavioral phenotypes in VIP- and PACAP-deficient mice. J. Neurochem. 2006, 99:499-513.
23. Goadsby P.J. Headache. Neurotherapeutics 2010, 7:149-152.
24. Hashimoto H., Shintani N., Tanaka K., et al. Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13355-13360.
25. Hashimoto H., Shintani H., Baba A. New insights into the central PACAP-ergic system from the phenotypes of PACAP- and PACAP receptor-knockout mice. Ann. N. Y. Acad. Sci. 2006, 1070:75-89.
26. Hashimoto H., Hashimoto R., Shintani N., et al. Depression-like behavior in the forced swimming test in PACAP-deficient mice: amelioration by the atypical antipsychotic risperidone. J. Neurochem. 2009, 110:595-602.
27. Hatanaka M., Tanida M., Shintani N., et al. Lack of light-induced elevation of renal sympathetic nerve activity and plasma corticosterone levels in PACAP-deficient mice. Neurosci. Lett. 2008, 444:153-156.
28. Helyes Zs., Pozsgai G., Borzsei R., et al. Inhibitory effect of PACAP-38 on acute neurogenic and non-neurogenic inflammatory processes in the rat. Peptides 2007, 28:1847-1855.
29. Ho T.W., Ferrari M.D., Dodick D.W., et al. Efficacy and tolerability of MK-0974 (telcagepant), a new oral antagonist of calcitonin gene-related peptide receptor, compared with zolmitriptan for acute migraine: a randomised, placebo-controlled, parallel-treatment trial. Lancet 2008, 372(9656):2115-2123.
30. Ho T.W., Edvinsson L., Goadsby P.J. CGRP and its receptors provide new insights into migraine pathophysiology. Nat. Rev. Neurol. 2010, 6(10):573-582.
31. Jongsma H., Pettersson L.M., Zhang Y., et al. Markedly reduced chronic nociceptive response in mice lacking the PAC1 receptor. Neuroreport 2001, 12:2215-2219.
32. Kuris A., Xu C.B., Zhou M.F., et al. Enhanced expression of CGRP in rat trigeminal ganglion neurons during cell and organ culture. Brain Res. 2007, 1173:6-13.
33. Laburthe M., Couvineau A., Tan V. Class II G-protein-coupled receptors for VIP and PACAP: structure, models of activation and pharmacology. Peptides 2007, 28:1631-1639.
34. Láinez M.J. The effect of migraine prophylaxis on migraine-related resource use and productivity. CNS Drugs 2009, 23(9):727-738.
35. Lambert G.A., Donaldson C., Boers P.M., et al. Activation of trigeminovascular neurons by glyceryl trinitrate. Brain Res. 2000, 887(1):203-210.
36. Lenti L., Domoki F., Kis D., et al. Pituitary adenylate cyclase-activating polypeptide induces pial arteriolar vasodilation through cyclooxygenase dependent and independent mechanisms in newborn pigs. Brain Res. 2007, 1165:81-88.
37. Levy D., Burstein R., Kainz V., et al. Mast cell degranulation activates a pain pathway underlying migraine headache. Pain 2007, 130:166-176.
38. Levy D. Migraine pain, meningeal inflammation, and mast cells. Curr. Pain Headache Rep. 2009, 13:237-240.
39. Maassen VanDenBrink A., Reekers M., Bax W.A., et al. Coronary side-effect potential of current and prospective antimigraine drugs. Circulation 1998, 98(1):25-30.
40. Marquez P., Bebawy D., Lelievre V., et al. The role of endogenous PACAP in motor stimulation and conditioned place preference induced by morphine in mice. Psychopharmacology 2009, 204:457-463.
41. Messlinger K. Migraine: where and how does the pain originate?. Exp. Brain Res. 2009, 196(1):179-193.
42. Miyata A., Arimura A., Dahl R.R., et al. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem. Biophys. Res. Commun. 1989, 164:567-574.
43. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 1991, 14:421-451.
44. Moskowitz M.A., Nozaki K., Kraig R.P. Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J. Neurosci. 1993, 13(3):1167-1177.
45. Mulder H., Uddman R., Moller K., et al. Pituitary adenylate cyclase activating polypeptide expression in sensory neurons. Neuroscience 1994, 63:307-312.
46. Narita M., Dun S.L., Dun N.J., et al. Hyperalgesia induced by pituitary adenylate cyclase-activating polypeptide in the mouse spinal cord. Eur. J. Pharmacol. 1996, 311:121-126.
47. Neeb L., Reuter U. Nitric oxide in migraine. CNS Neurol. Disord. Drug Targets 2007, 6:258-264.
48. Nemeth J., Reglodi D., Pozsgai G., et al. Effect of pituitary adenylate cyclase activating polypeptide-38 on sensory neuropeptide release and neurogenic inflammation in rats and mice. Neuroscience 2006, 143:223-230.
49. Odum L., Petersen L.J., Skov P.S., et al. Pituitary adenylate cyclase activating polypeptide (PACAP) is localized in human dermal neurons and causes histamine release from skin mast cells. Inflamm. Res. 1998, 47(12):488-492.
50. Ohsawa M., Brailoiu G.C., Shiraki M., et al. Modulation of nociceptive transmission by pituitary adenylate cyclase activating polypeptide in the spinal cord of the mouse. Pain 2002, 100:27-34.
51. Olesen J., Thomsen L.L., Iversen H. Nitric oxide is a key molecule in migraine and other vascular headaches. Trends Pharmacol. Sci. 1994, 15(5):149-153.
52. Olesen J., Thomsen L., Lassen L.H., et al. The nitric oxide hypothesis of migraine and other vascular headaches. Cephalalgia 1995, 15(2):94-100.
53. Olesen J. Nitric oxide-related drug targets in headache. Neurotherapeutics 2010, 7(2):183-190.
54. Ottosson A., Edvinsson L. Release of histamine from dural mast cells by substance P and calcitonin gene-related peptide. Cephalalgia 1997, 17:166-174.
55. Pardutz A., Krizbai I., Multon S., et al. Systemic nitroglycerin increases nNOS levels in rat trigeminal nucleus caudalis. Neuroreport 2000, 11(14):3071-3075.
56. Paxinos G., Franklin K. The Mouse Brain in Stereotaxic Coordinatres 2003, Elsevier Academic Press, San Diego. 3rd edition.
57. Petersen K.A., Birk S., Doods H., et al. Inhibitory effect of BIBN4096BS on cephalic vasodilatation induced by CGRP or transcranial electrical stimulation in the rat. Br. J. Pharmacol. 2004, 143(6):697-704.
58. Recober A., Kaiser E.A., Kuburas A., et al. Induction of multiple photophobic behaviors in a transgenic mouse sensitized to CGRP. Neuropharmacology 2010, 58:156-165.
59. Rozniecki J.J., Dimiriadou V., Lambracht-Hall M., et al. Morphological and functional demonstration of rat dura mater mast cellneuron interactions in vitro and in vivo. Brain Res. 1999, 849:1-15.
60. Sakashita Y., Kurihara D., Uchida T., et al. Involvement of PACAP receptor in primary afferent fibre-evoked responses of ventral roots in the neonatal rat spinal cord. Br. J. Pharmacol. 2001, 132:1769-1776.
61. Sandor K., Bolcskei K., McDougall J., et al. Divergent peripheral effects of pituitary adenylate cyclase-activating polypeptide-38 on nociception in rats and mice. Pain 2009, 141:143-150.
62. Sandor K., Kormos V., Botz B., et al. Impaired nocifensive behaviors and mechanical hyperalgesia, but enhanced thermal allodynia in pituitary adenylate-cyclase activating polypeptide deficient mice. Neuropeptides 2010, 44(5):363-371.
63. Schürks M., Diener H.C. Migraine, allodynia, and implications for treatment. Eur. J. Neurol. 2008, 15(12):1279-1285.
64. Schytz H.W., Birk S., Wienecke T., et al. PACAP38 induces migraine-like attacks in patients with migraine without aura. Brain 2009, 132:16-25.
65. Schytz H.W. Investigation of carbachol and PACAP38 in a human model of migraine. Dan. Med. Bull. 2010, 57(12):B4223.
66. Schytz H.W., Olesen J., Ashina M. The PACAP receptor: a novel target for migraine treatment. Neurotherapeutics 2010, 7(2):191-196.
67. Schytz H.W., Schoonman G.G., Ashina M. What have we learnt from triggering migraine?. Curr. Opin. Neurol. 2010, 23(3):259-265.
68. Somogyvari-Vigh A., Reglodi D. Pituitary adenylate cyclase activating polypeptide: a potential neuroprotective peptide. Curr. Pharm. Des. 2004, 10:2861-2889.
69. Spengler D., Waeber C., Pantaloni C., et al. Differential signal transduction by five splice variants of the PACAP receptor. Nature 1993, 365:170-175.
70. Tajti J., Uddman R., Möller S., et al. Messenger molecules and receptor mRNA in the human trigeminal ganglion. J. Auton. Nerv. Syst. 1999, 76(2-3):176-183.
71. Tajti J., Uddman R., Edvinsson L. Neuropeptide localization in the "migraine generator" region of the human brainstem. Cephalalgia 2001, 21(2):96-101.
72. Tassorelli C., Joseph S.A. Systemic nitroglycerin induces Fos immunoreactivity in brainstem and forebrain structures of the rat. Brain Res. 1995, 682(1-2):167-181.
73. Tassorelli C., Joseph S.A., Nappi G. Neurochemical mechanisms of nitroglycerin-induced neuronal activation in rat brain: a pharmacological investigation. Neuropharmacology 1997, 36(10):1417-1424.
74. Tassorelli C., Joseph S.A., Buzzi M.G., et al. The effects on the central nervous system of nitroglycerin-putative mechanisms and mediators. Prog. Neurobiol. 1999, 57(6):607-624.
75. Theoharides T.C., Donelan J., Kandere-Grzybowska K., et al. The role of mast cells in migraine pathophysiology. Brain Res. Rev. 2005, 49(1):65-76.
76. Uddman R., Goadsby P.J., Jansen I., Edvinsson L. PACAP, a VIP-like peptide: immunohistochemical localization and effect upon cat pial arteries and cerebral blood flow. J. Cereb. Blood Flow Metab. 1993, 13(2):291-297.
77. Uddman R., Tajti J., Möller S., Sundler F., Edvinsson L. Neuronal messengers and peptide receptors in the human sphenopalatine and otic ganglia. Brain Res. 1999, 826(2):193-199.
78. Uddman R., Tajti J., Hou M., et al. Neuropeptide expression in the human trigeminal nucleus caudalis and in the cervical spinal cord C1 and C2. Cephalalgia 2002, 22(2):112-116.
79. van der Kuy P.H., Lohman J.J. The role of nitric oxide in vascular headache. Pharm. World Sci. 2003, 25(4):146-151.
80. Vaudry D., Falluel-Morel A., Bourgault S., et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20years after the discovery. Pharmacol. Rev. 2009, 61:283-357.
81. Villalón C.M., Centurión D., Valdivia L.F., et al. Migraine: pathophysiology, pharmacology, treatment and future trends. Curr. Vasc. Pharmacol. 2003, 1(1):71-84.
82. Warren J.B., Larkin S.W., Coughlan M., et al. Pituitary adenylate cyclase activating polypeptide is a potent vasodilator and oedema potentiator in rabbit skin in vivo. Br. J. Pharmacol. 1992, 106(2):331-334.
83. Xu X.J., Wiesenfeld-Hallin Z. Intrathecal pituitary adenylate cyclase activating polypeptide facilitates the spinal nociceptive flexor reflex in the rat. Neuroscience 1996, 72:801-804.
84. Yamada K., Matsuzaki S., Hattori T., et al. Increased stathmin1 expression in the dentate gyrus of mice causes abnormal axonal arborizations. PLoS One 2010, 5:e8596.
85. Zhang X.C., Strassman A.M., Burstein R., et al. Sensitization and activation of intracranial meningeal nociceptors by mast cell mediators. J. Pharmacol. Exp. Ther. 2007, 322:806-812.
86. Zhou C.J., Shioda S., Yada T., et al. PACAP and its receptors exert pleiotropic effects in the nervous system by activating multiple signaling pathways. Curr. Protein Pept. Sci. 2002, 3:423-439.