Peripheral and central alterations of pituitary adenylate cyclase activating polypeptide-like immunoreactivity in the rat in response to activation of the trigeminovascular system

Peptides

Volumn 33, Issue 2, 2012, Pages 307-316

  Tuka, Bernadett ^a,b   Helyes, Zsuzsanna ^c,e   Markovics, Adrienn ^c   Bagoly, Teréz ^c   Németh, József ^d   Márk, László ^c   Brubel, Réka ^c   Regldi, Dóra ^c   Párdutz, Árpád ^a   Szolcsányi, János ^c,e   Vécsei, László ^a,b   Tajti, János ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

^c UNIVERSITY OF PÉCS   (Hungary)

^d UNIVERSITY OF DEBRECEN   (Hungary)

^e PharmInVivo Ltd   (Hungary)

Author keywords

Blood plasma; Electrical and chemical stimulation; Mass spectrometry; Nitroglycerol; Trigeminal ganglion; Trigeminal nucleus caudalis

Indexed keywords

GLYCERYL TRINITRATE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE 27;

ANIMAL EXPERIMENT; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; ELECTROSTIMULATION; FEMALE; MALE; MASS SPECTROMETRY; MIGRAINE; NERVE STIMULATION; NONHUMAN; PLASMA; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; SPINAL CORD; TISSUE HOMOGENATE; TRIGEMINAL NUCLEUS; TRIGEMINUS GANGLION;

ANIMALS; ELECTRIC STIMULATION; IMMUNOHISTOCHEMISTRY; NITROGLYCERIN; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TRIGEMINAL CAUDAL NUCLEUS; TRIGEMINAL GANGLION; VASODILATOR AGENTS; VASOMOTOR SYSTEM;

RATTUS;

EID: 84858800138     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2011.12.019     Document Type: Article

References (103)

1. T. Abe, N. Ohshita, S. Sugiyo, M. Moritani, M. Kobayashi, and M. Takemura Elimination of neurokinin-1 receptor neurons in caudal nucleus reverses the effects of systemic bicuculline on c-Fos expression in rat trigeminal sensory nucleus: I. High intensity electrical stimulation of the trigeminal ganglion Neuroscience 133 2005 739 747 (Pubitemid 40798326)
2. A. Arimura PACAP: the road to discovery Peptides 28 2007 1617 1619 (Pubitemid 47361429)
3. F.M. Baeres, and M. Moller Origin of PACAP-immunoreactive nerve fibers innervating the subarachnoidal blood vessels of the rat brain J Cereb Blood Flow Metab 24 2004 628 635 (Pubitemid 38725367)
4. M. Barberi, B. Muciaccia, M.B. Morelli, M. Stefanini, S. Cecconi, and R. Canipari Expression localisation and functional activity of pituitary adenylate cyclase-activating polypeptide, vasoactive intestinal polypeptide and their receptors in mouse ovary Reproduction 134 2007 281 292 (Pubitemid 47278801)
5. S. Behrends, E. Knyihar-Csillik, J. Kempfert, H. Scholz, B. Csillik, and L. Vecsei Glyceryl trinitrate treatment up-regulates soluble guanylyl cyclase in rat dura mater Neuroreport 12 2001 3993 3996 (Pubitemid 33152440)
6. A. Bergerot, P.R. Holland, S. Akerman, T. Bartsch, A.H. Ahn, and A. Maassen Van DenBrink Animal models of migraine: looking at the component parts of a complex disorder Eur J Neurosci 24 2006 1517 1534 (Pubitemid 44429881)
7. R. Borzsei, L. Mark, A. Tamas, T. Bagoly, C. Bay, and K. Csanaky Presence of pituitary adenylate cyclase activating polypeptide-38 in human plasma and milk Eur J Endocrinol 160 2009 561 565
8. S. Bourgault, D. Vaudry, B. Botia, A. Couvineau, M. Laburthe, and H. Vaudry Novel stable PACAP analogs with potent activity towards the PAC1 receptor Peptides 29 2008 919 932
9. M.G. Buzzi, W.B. Carter, T. Shimizu, H. Heath 3rd, and M.A. Moskowitz Dihydroergotamine and sumatriptan attenuate levels of CGRP in plasma in rat superior sagittal sinus during electrical stimulation of the trigeminal ganglion Neuropharmacology 30 1991 1193 1200
10. M.G. Buzzi, and C. Tassorelli Experimental models of migraine Handb Clin Neurol 97 2010 109 123
11. K.Y. Chan, M. Baun, R. de Vries, A.J. van den Bogaerdt, C.M. Dirven, and A.H. Danser Pharmacological characterization of VIP and PACAP receptors in the human meningeal and coronary artery Cephalalgia 31 2011 181 189
12. T. Dickinson, R. Mitchell, P. Robberecht, and S.M. Fleetwood-Walker The role of VIP/PACAP receptor subtypes in spinal somatosensory processing in rats with an experimental peripheral mononeuropathy Neuropharmacology 38 1999 167 180 (Pubitemid 29073536)
13. K. Elekes, K. Sandor, A. Moricz, L. Kereskai, A. Kemeny, and E. Szoke Pituitary adenylate cyclase-activating polypeptide plays an anti-inflammatory role in endotoxin-induced airway inflammation: in vivo study with gene-deleted mice Peptides 2011
14. J. Fahrenkrug, and J. Hannibal Localisation of the neuropeptide PACAP and its receptors in the rat parathyroid and thyroid glands Gen Comp Endocrinol 171 2011 105 113
15. M. Fanciullacci, M. Alessandri, R. Sicuteri, and S. Marabini Responsiveness of the trigeminovascular system to nitroglycerine in cluster headache patients Brain 120 Pt 2 1997 283 288 (Pubitemid 27107661)
16. A. Ferencz, G. Weber, Z. Helyes, H. Hashimoto, A. Baba, and D. Reglodi Presence of endogenous PACAP-38 ameliorated intestinal cold preservation tissue injury J Mol Neurosci 42 2010 428 434
17. P.J. Goadsby, L. Edvinsson, and R. Ekman Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system Ann Neurol 23 1988 193 196 (Pubitemid 18081459)
18. R. Greco, A.S. Mangione, G. Sandrini, M. Maccarrone, G. Nappi, and C. Tassorelli Effects of anandamide in migraine: data from an animal model J Headache Pain 12 2011 177 183
19. S. Gupta, D.K. Bhatt, L.J. Boni, and J. Olesen Improvement of the closed cranial window model in rats by intracarotid infusion of signalling molecules implicated in migraine Cephalalgia 30 2010 27 36
20. J. Hannibal Pituitary adenylate cyclase-activating peptide in the rat central nervous system: an immunohistochemical and in situ hybridization study J Comp Neurol 453 2002 389 417 (Pubitemid 35231190)
21. J. Hannibal, and J. Fahrenkrug Pituitary adenylate cyclase-activating polypeptide in intrinsic and extrinsic nerves of the rat pancreas Cell Tissue Res 299 2000 59 70 (Pubitemid 30028723)
22. H. Hashimoto, N. Shintani, M. Tanida, A. Hayata, R. Hashimoto, and A. Baba PACAP is implicated in the stress axes Curr Pharm Des 17 2011 985 989
23. Z. Helyes, G. Pozsgai, R. Borzsei, J. Nemeth, T. Bagoly, and L. Mark Inhibitory effect of PACAP-38 on acute neurogenic and non-neurogenic inflammatory processes in the rat Peptides 28 2007 1847 1855 (Pubitemid 47361436)
24. M. Hou, R. Uddman, J. Tajti, and L. Edvinsson Nociceptin immunoreactivity and receptor mRNA in the human trigeminal ganglion Brain Res 964 2003 179 186 (Pubitemid 36165142)
25. Y. Ishizuka, K. Kashimoto, T. Mochizuki, K. Sato, K. Ohshima, and N. Yanaihara Cardiovascular and respiratory actions of pituitary adenylate cyclase-activating polypeptides Regul Pept 40 1992 29 39
26. H.K. Iversen, J. Olesen, and P. Tfelt-Hansen Intravenous nitroglycerin as an experimental model of vascular headache. Basic characteristics Pain 38 1989 17 24 (Pubitemid 19184833)
27. B. Jakab, D. Reglodi, R. Jozsa, T. Hollosy, A. Tamas, and A. Lubics Distribution of PACAP-38 in the central nervous system of various species determined by a novel radioimmunoassay J Biochem Biophys Methods 61 2004 189 198 (Pubitemid 39561698)
28. H. Jongsma, L.M. Pettersson, Y. Zhang, M.K. Reimer, M. Kanje, and A. Waldenstrom Markedly reduced chronic nociceptive response in mice lacking the PAC1 receptor Neuroreport 12 2001 2215 2219 (Pubitemid 32646275)
29. C. Kimura, S. Ohkubo, K. Ogi, M. Hosoya, Y. Itoh, and H. Onda A novel peptide which stimulates adenylate cyclase: molecular cloning and characterization of the ovine and human cDNAs Biochem Biophys Res Commun 166 1990 81 89 (Pubitemid 20040155)
30. E. Knyihar-Csillik, Z. Chadaide, E. Okuno, B. Krisztin-Peva, J. Toldi, and C. Varga Kynurenine aminotransferase in the supratentorial dura mater of the rat: effect of stimulation of the trigeminal ganglion Exp Neurol 186 2004 242 247 (Pubitemid 38333197)
31. E. Knyihar-Csillik, J. Tajti, A.E. Csillik, Z. Chadaide, A. Mihaly, and L. Vecsei Effects of eletriptan on the peptidergic innervation of the cerebral dura mater and trigeminal ganglion, and on the expression of c-fos and c-jun in the trigeminal complex of the rat in an experimental migraine model Eur J Neurosci 12 2000 3991 4002
32. E. Knyihar-Csillik, J. Tajti, S. Mohtasham, G. Sari, and L. Vecsei Electrical stimulation of the Gasserian ganglion induces structural alterations of calcitonin gene-related peptide-immunoreactive perivascular sensory nerve terminals in the rat cerebral dura mater: a possible model of migraine headache Neurosci Lett 184 1995 189 192
33. E. Knyihar-Csillik, J. Tajti, M. Samsam, G. Sary, P. Buzas, and L. Vecsei Depletion of calcitonin gene-related peptide from the caudal trigeminal nucleus of the rat after electrical stimulation of the Gasserian ganglion Exp Brain Res 118 1998 111 114 (Pubitemid 28052683)
34. E. Knyihar-Csillik, J. Toldi, B. Krisztin-Peva, Z. Chadaide, H. Nemeth, and R. Fenyo Prevention of electrical stimulation-induced increase of c-fos immunoreaction in the caudal trigeminal nucleus by kynurenine combined with probenecid Neurosci Lett 418 2007 122 126 (Pubitemid 46635993)
35. K. Koves, A. Arimura, A. Somogyvari-Vigh, S. Vigh, and J. Miller Immunohistochemical demonstration of a novel hypothalamic peptide, pituitary adenylate cyclase-activating polypeptide, in the ovine hypothalamus Endocrinology 127 1990 264 271 (Pubitemid 20228129)
36. K. Koves, O. Kantor, J.G. Scammell, and A. Arimura PACAP colocalizes with luteinizing and follicle-stimulating hormone immunoreactivities in the anterior lobe of the pituitary gland Peptides 19 1998 1069 1072 (Pubitemid 28383805)
37. M. Laburthe, A. Couvineau, and V. Tan Class II G protein-coupled receptors for VIP and PACAP: structure, models of activation and pharmacology Peptides 28 2007 1631 1639 (Pubitemid 47371033)
38. A. Lacombe, V. Lelievre, C.E. Roselli, W. Salameh, Y.H. Lue, and G. Lawson Delayed testicular aging in pituitary adenylate cyclase-activating peptide (PACAP) null mice Proc Natl Acad Sci USA 103 2006 3793 3798 (Pubitemid 43376634)
39. G.A. Lambert, C. Donaldson, P.M. Boers, and A.S. Zagami Activation of trigeminovascular neurons by glyceryl trinitrate Brain Res 887 2000 203 210 (Pubitemid 32008041)
40. L. Lenti, F. Domoki, D. Kis, O. Hegyi, G.K. Toth, and D.W. Busija Pituitary adenylate cyclase-activating polypeptide induces pial arteriolar vasodilation through cyclooxygenase-dependent and independent mechanisms in newborn pigs Brain Res 1165 2007 81 88 (Pubitemid 47224936)
41. V. Limmroth, Z. Katsarava, B. Liedert, H. Guehring, K. Schmitz, and H.C. Diener An in vivo rat model to study calcitonin gene related peptide release following activation of the trigeminal vascular system Pain 92 2001 101 106 (Pubitemid 32367941)
42. T. Mabuchi, N. Shintani, S. Matsumura, E. Okuda-Ashitaka, H. Hashimoto, and T. Muratani Pituitary adenylate cyclase-activating polypeptide is required for the development of spinal sensitization and induction of neuropathic pain J Neurosci 24 2004 7283 7291 (Pubitemid 39100698)
43. A. Malick, and R. Burstein Peripheral and central sensitization during migraine Funct Neurol 15 Suppl. 3 2000 28 35 (Pubitemid 32051372)
44. A. Markovics, V. Kormos, B. Gaszner, A. Lashgarara, E. Szoke, and K. Sandor Pituitary adenylate cyclase-activating polypeptide plays a key role in nitroglycerol-induced trigeminovascular activation in mice Neurobiol Dis 45 2012 633 644
45. S. Markowitz, K. Saito, and M.A. Moskowitz Neurogenically mediated leakage of plasma protein occurs from blood vessels in dura mater but not brain J Neurosci 7 1987 4129 4136 (Pubitemid 18012423)
46. Y. Masuo, T. Ohtaki, Y. Masuda, M. Tsuda, and M. Fujino Binding sites for pituitary adenylate cyclase activating polypeptide (PACAP): comparison with vasoactive intestinal polypeptide (VIP) binding site localization in rat brain sections Brain Res 575 1992 113 123
47. A. May, and P.J. Goadsby The trigeminovascular system in humans: pathophysiologic implications for primary headache syndromes of the neural influences on the cerebral circulation J Cereb Blood Flow Metab 19 1999 115 127 (Pubitemid 29284258)
48. N. Mirabella, C. Squillacioti, G. Germano, E. Varricchio, and G. Paino Pituitary adenylate cyclase activating peptide (PACAP) immunoreactivity in the ureter of the duck Cell Tissue Res 305 2001 341 349 (Pubitemid 34212127)
49. A. Miyata, A. Arimura, R.R. Dahl, N. Minamino, A. Uehara, and L. Jiang Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells Biochem Biophys Res Commun 164 1989 567 574 (Pubitemid 19269770)
50. T.W. Moody, T. Ito, N. Osefo, and R.T. Jensen VIP and PACAP: recent insights into their functions/roles in physiology and disease from molecular and genetic studies Curr Opin Endocrinol Diabetes Obes 18 2011 61 67
51. H. Mulder, H. Jongsma, Y. Zhang, S. Gebre-Medhin, F. Sundler, and N. Danielsen Pituitary adenylate cyclase-activating polypeptide and islet amyloid polypeptide in primary sensory neurons: functional implications from plasticity in expression on nerve injury and inflammation Mol Neurobiol 19 1999 229 253 (Pubitemid 29418893)
52. H. Murabayashi, H. Kuramoto, H. Kawano, M. Sasaki, N. Kitamura, and K. Miyakawa Immunohistochemical features of substance P-immunoreactive chromaffin cells and nerve fibers in the rat adrenal gland Arch Histol Cytol 70 2007 183 196 (Pubitemid 350224154)
53. M. Narita, S.L. Dun, N.J. Dun, and L.F. Tseng Hyperalgesia induced by pituitary adenylate cyclase-activating polypeptide in the mouse spinal cord Eur J Pharmacol 311 1996 121 126 (Pubitemid 26330366)
54. J. Nemeth, D. Reglodi, G. Pozsgai, A. Szabo, K. Elekes, and E. Pinter Effect of pituitary adenylate cyclase activating polypeptide-38 on sensory neuropeptide release and neurogenic inflammation in rats and mice Neuroscience 143 2006 223 230 (Pubitemid 44755233)
55. H.S. Nielsen, J. Hannibal, and J. Fahrenkrug Embryonic expression of pituitary adenylate cyclase-activating polypeptide in sensory and autonomic ganglia and in spinal cord of the rat J Comp Neurol 394 1998 403 415 (Pubitemid 28183566)
56. M. Ohsawa, G.C. Brailoiu, M. Shiraki, N.J. Dun, K. Paul, and L.F. Tseng Modulation of nociceptive transmission by pituitary adenylate cyclase activating polypeptide in the spinal cord of the mouse Pain 100 2002 27 34 (Pubitemid 35305121)
57. M. Ohtsuka, H. Fukumitsu, and S. Furukawa PACAP decides neuronal laminar fate via PKA signaling in the developing cerebral cortex Biochem Biophys Res Commun 369 2008 1144 1149
58. J. Olesen Nitric oxide-related drug targets in headache Neurotherapeutics 7 2010 183 190
59. J. Olesen, H.K. Iversen, and L.L. Thomsen Nitric oxide supersensitivity: a possible molecular mechanism of migraine pain Neuroreport 4 1993 1027 1030 (Pubitemid 23242637)
60. A. Pardutz, Z. Hoyk, H. Varga, L. Vecsei, and J. Schoenen Oestrogen-modulated increase of calmodulin-dependent protein kinase II (CamKII) in rat spinal trigeminal nucleus after systemic nitroglycerin Cephalalgia 27 2007 46 53 (Pubitemid 46020801)
61. A. Pardutz, I. Krizbai, S. Multon, L. Vecsei, and J. Schoenen Systemic nitroglycerin increases nNOS levels in rat trigeminal nucleus caudalis Neuroreport 11 2000 3071 3075
62. A. Pardutz, S. Multon, B. Malgrange, A. Parducz, L. Vecsei, and J. Schoenen Effect of systemic nitroglycerin on CGRP and 5-HT afferents to rat caudal spinal trigeminal nucleus and its modulation by estrogen Eur J Neurosci 15 2002 1803 1809 (Pubitemid 35471905)
63. A. Pardutz, E. Szatmari, L. Vecsei, and J. Schoenen Nitroglycerin-induced nNOS increase in rat trigeminal nucleus caudalis is inhibited by systemic administration of lysine acetylsalicylate but not of sumatriptan Cephalalgia 24 2004 439 445 (Pubitemid 38748025)
64. L.M. Pettersson, L.B. Dahlin, and N. Danielsen Changes in expression of PACAP in rat sensory neurons in response to sciatic nerve compression Eur J Neurosci 20 2004 1838 1848 (Pubitemid 39471577)
65. L.M. Pettersson, T. Heine, V.M. Verge, F. Sundler, and N. Danielsen PACAP mRNA is expressed in rat spinal cord neurons J Comp Neurol 471 2004 85 96 (Pubitemid 38282967)
66. B. Racz, D. Reglodi, G. Horvath, A. Szigeti, B. Balatonyi, and E. Roth Protective effect of PACAP against doxorubicin-induced cell death in cardiomyocyte culture J Mol Neurosci 42 2010 419 427
67. A. Rahmann, T. Wienecke, J.M. Hansen, J. Fahrenkrug, J. Olesen, and M. Ashina Vasoactive intestinal peptide causes marked cephalic vasodilation, but does not induce migraine Cephalalgia 28 2008 226 236 (Pubitemid 351172031)
68. P. Raval, S. Bingham, N. Aiyar, J.D. Elliott, A.J. Hunter, and E.H. Ohlstein Trigeminal nerve ganglion stimulation-induced neurovascular reflexes in the anaesthetized cat: role of endothelin(B) receptors in carotid vasodilatation Br J Pharmacol 126 1999 485 493 (Pubitemid 29057600)
69. D. Reglodi, P. Kiss, G. Horvath, A. Lubics, E. Laszlo, and A. Tamas Effects of pituitary adenylate cyclase activating polypeptide in the urinary system, with special emphasis on its protective effects in the kidney Neuropeptides 2011
70. D. Reglodi, P. Kiss, A. Lubics, and A. Tamas Review on the protective effects of PACAP in models of neurodegenerative diseases in vitro and in vivo Curr Pharm Des 17 2011 962 972
71. M. Samsam, R. Covenas, R. Ahangari, J. Yajeya, J.A. Narvaez, and G. Tramu Alterations in neurokinin A-, substance P- and calcitonin gene-related peptide immunoreactivities in the caudal trigeminal nucleus of the rat following electrical stimulation of the trigeminal ganglion Neurosci Lett 261 1999 179 182 (Pubitemid 29104974)
72. M. Samsam, R. Covenas, R. Ahangari, J. Yajeya, J.A. Narvaez, and G. Tramu Simultaneous depletion of neurokinin A, substance P and calcitonin gene-related peptide from the caudal trigeminal nucleus of the rat during electrical stimulation of the trigeminal ganglion Pain 84 2000 389 395 (Pubitemid 30074242)
73. M. Samsam, R. Covenas, B. Csillik, R. Ahangari, J. Yajeya, and R. Riquelme Depletion of substance P, neurokinin A and calcitonin gene-related peptide from the contralateral and ipsilateral caudal trigeminal nucleus following unilateral electrical stimulation of the trigeminal ganglion: a possible neurophysiological and neuroanatomical link to generalized head pain J Chem Neuroanat 21 2001 161 169 (Pubitemid 32324239)
74. K. Sandor, K. Bolcskei, J.J. McDougall, N. Schuelert, D. Reglodi, and K. Elekes Divergent peripheral effects of pituitary adenylate cyclase-activating polypeptide-38 on nociception in rats and mice Pain 141 2009 143 150
75. K. Sandor, V. Kormos, B. Botz, A. Imreh, K. Bolcskei, and B. Gaszner Impaired nocifensive behaviours and mechanical hyperalgesia, but enhanced thermal allodynia in pituitary adenylate cyclase-activating polypeptide deficient mice Neuropeptides 44 2010 363 371
76. H.W. Schytz, S. Birk, T. Wienecke, C. Kruuse, J. Olesen, and M. Ashina PACAP38 induces migraine-like attacks in patients with migraine without aura Brain 132 2009 16 25
77. H.W. Schytz, J. Olesen, and M. Ashina The PACAP receptor: a novel target for migraine treatment Neurotherapeutics 7 2010 191 196
78. T. Seaborn, O. Masmoudi-Kouli, A. Fournier, H. Vaudry, and D. Vaudry Protective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) against apoptosis Curr Pharm Des 17 2011 204 214
79. N.M. Sherwood, S.L. Krueckl, and J.E. McRory The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily Endocr Rev 21 2000 619 670 (Pubitemid 32113287)
80. F. Sicuteri, E. Del Bene, M. Poggioni, and A. Bonazzi Unmasking latent dysnociception in healthy subjects Headache 27 1987 180 185 (Pubitemid 18001961)
81. H.H. Strange-Vognsen, J. Arnbjerg, and J. Hannibal Immunocytochemical demonstration of pituitary adenylate cyclase activating polypeptide (PACAP) in the porcine epiphyseal cartilage canals Neuropeptides 31 1997 137 141 (Pubitemid 27240054)
82. J. Tajti, A. Pardutz, E. Vamos, B. Tuka, A. Kuris, and Z. Bohar Migraine is a neuronal disease J Neural Transm 118 2011 511 524
83. J. Tajti, R. Uddman, S. Moller, F. Sundler, and L. Edvinsson Messenger molecules and receptor mRNA in the human trigeminal ganglion J Auton Nerv Syst 76 1999 176 183 (Pubitemid 29322040)
84. M. Takemura, T. Shimada, and Y.G.A.B.A. Shigenaga B receptor-mediated effects on expression of c-Fos in rat trigeminal nucleus following high- and low-intensity afferent stimulation Neuroscience 103 2001 1051 1058 (Pubitemid 32289315)
85. C. Tassorelli, R. Greco, A. Morocutti, A. Costa, and G. Nappi Nitric oxide-induced neuronal activation in the central nervous system as an animal model of migraine: mechanisms and mediators Funct Neurol 16 2001 69 76 (Pubitemid 34295896)
86. C. Tassorelli, and S.A. Joseph Systemic nitroglycerin induces Fos immunoreactivity in brainstem and forebrain structures of the rat Brain Res 682 1995 167 181
87. C. Tassorelli, S.A. Joseph, and G. Nappi Neurochemical mechanisms of nitroglycerin-induced neuronal activation in rat brain: a pharmacological investigation Neuropharmacology 36 1997 1417 1424 (Pubitemid 27502199)
88. R. Uddman, J. Tajti, M. Hou, F. Sundler, and L. Edvinsson Neuropeptide expression in the human trigeminal nucleus caudalis and in the cervical spinal cord C1 and C2 Cephalalgia 22 2002 112 116 (Pubitemid 34494131)
89. S. Uemura, S. Pompolo, J.B. Furness, and K.J. Hardy Nitric oxide synthase in neurons of the human gall-bladder and its colocalization with neuropeptides J Gastroenterol Hepatol 12 1997 257 265 (Pubitemid 27158001)
90. L. Uyttebroek, I.T. Shepherd, F. Harrisson, G. Hubens, R. Blust, and J.P. Timmermans Neurochemical coding of enteric neurons in adult and embryonic zebrafish (Danio rerio) J Comp Neurol 518 2010 4419 4438
91. D. Vaudry, A. Falluel-Morel, S. Bourgault, M. Basille, D. Burel, and O. Wurtz Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery Pharmacol Rev 61 2009 283 357
92. L. Vecsei, E. Widerlov, R. Ekman, K. Kovacs, I. Jelencsik, and G. Bozsik Suboccipital cerebrospinal fluid and plasma concentrations of somatostatin, neuropeptide Y and beta-endorphin in patients with common migraine Neuropeptides 22 1992 111 116
93. M.A. Vizzard Up-regulation of pituitary adenylate cyclase-activating polypeptide in urinary bladder pathways after chronic cystitis J Comp Neurol 420 2000 335 348 (Pubitemid 30183763)
94. J.B. Warren, J.R. Cockcroft, S.W. Larkin, R. Kajekar, A. Macrae, and M.A. Ghatei Pituitary adenylate cyclase activating polypeptide is a potent vasodilator in humans J Cardiovasc Pharmacol 20 1992 83 87
95. J. Watanabe, T. Nakamachi, R. Matsuno, D. Hayashi, M. Nakamura, and S. Kikuyama Localization, characterization and function of pituitary adenylate cyclase-activating polypeptide during brain development Peptides 28 2007 1713 1719 (Pubitemid 47364750)
96. F. Willoch, U. Gamringer, R. Medele, U. Steude, and T.R. Tolle Analgesia by electrostimulation of the trigeminal ganglion in patients with trigeminopathic pain: a PET activation study Pain 103 2003 119 130 (Pubitemid 36579092)
97. T. Yamamoto, and I. Tatsuno Antinociceptive effect of intrathecally administered pituitary adenylate cyclase activating polypeptide (PACAP) on the rat formalin test Neurosci Lett 184 1995 32 35
98. Y. Zhang, N. Danielsen, F. Sundler, and H. Mulder Pituitary adenylate cyclase-activating peptide is upregulated in sensory neurons by inflammation Neuroreport 9 1998 2833 2836 (Pubitemid 28435172)
99. Y. Zhang, A.B. Malmberg, B. Sjolund, and T.L. Yaksh The effect of pituitary adenylate cyclase activating peptide (PACAP) on the nociceptive formalin test Neurosci Lett 207 1996 187 190 (Pubitemid 26117606)
100. Y. Zhang, A.B. Malmberg, T.L. Yaksh, B. Sjolund, F. Sundler, and R. Hakanson Capsaicin-evoked release of pituitary adenylate cyclase activating peptide (PACAP) and calcitonin gene-related peptide (CGRP) from rat spinal cord in vivo Regul Pept 69 1997 83 87 (Pubitemid 27240368)
101. X. Zhu, Y. Han, W. Xiong, W. Liu, S. Lu, and J. Li Effects of heating coagulation of middle meningeal artery on plasma CGRP level and c-fos expression in migraine rat triggered by nitroglycerin Neurol Sci 32 2011 589 594
102. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110 (Pubitemid 13058546)
103. K. Zvarova, J.D. Dunleavy, and M.A. Vizzard Changes in pituitary adenylate cyclase activating polypeptide expression in urinary bladder pathways after spinal cord injury Exp Neurol 192 2005 46 59 (Pubitemid 40208537)