A naturalistic glyceryl trinitrate infusion migraine model in the rat

Cephalalgia

Volumn 32, Issue 1, 2012, Pages 73-84

  Ramachandran, Roshni ^a   Bhatt, Deepak Kumar ^a   Ploug, Kenneth Beri ^a   Olesen, Jes ^a   Jansen Olesen, Inger ^a   Hay Schmidt, Anders ^b   Gupta, Saurabh ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

awake rat model; c fos; Glyceryl trinitrate; migraine; nociception; sumatriptan

Indexed keywords

GLYCERYL TRINITRATE; MESSENGER RNA; PROTEIN FOS; SUMATRIPTAN;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; DRUG INFUSION; IMMUNOHISTOCHEMISTRY; MIGRAINE; NOCICEPTION; NONHUMAN; ONCOGENE C FOS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RODENT; TOXICOLOGY; TRIGEMINAL NUCLEUS; UPREGULATION; WAKEFULNESS;

ANESTHESIA; ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MALE; MIGRAINE DISORDERS; NITROGLYCERIN; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TRIGEMINAL CAUDAL NUCLEUS; VASODILATOR AGENTS; WAKEFULNESS;

EID: 84863011940     PISSN: 03331024     EISSN: 14682982     Source Type: Journal    
DOI: 10.1177/0333102411430855     Document Type: Article

References (45)

1. Afridi SK, Kaube H, Goadsby PJ. Glyceryl trinitrate triggers premonitory symptoms in migraineurs. Pain. 2004 ; 110: 675-680 (Pubitemid 39036799)
2. Iversen HK, Olesen J, Tfelt-Hansen P. Intravenous nitroglycerin as an experimental model of vascular headache. Basic characteristics. Pain. 1989 ; 38: 17-24 (Pubitemid 19184833)
3. Schoonman GG, Sandor PS, Agosti RM, Siccoli M, Bartsch P, Ferrari MD, et al. Normobaric hypoxia and nitroglycerin as trigger factors for migraine. Cephalalgia. 2006 ; 26: 816-819 (Pubitemid 43882990)
4. Thomsen LL, Brennum J, Iversen HK, Olesen J. Effect of a nitric oxide donor (glyceryl trinitrate) on nociceptive thresholds in man. Cephalalgia. 1996 ; 16: 169-174 (Pubitemid 26163559)
5. Thomsen LL, Olesen J. Nitric oxide in primary headaches. Curr Opin Neurol. 2001 ; 14: 315-321 (Pubitemid 32510595)
6. Tassorelli C, Greco R, Morazzoni P, Riva A, Sandrini G, Nappi G. Parthenolide is the component of tanacetum parthenium that inhibits nitroglycerin-induced Fos activation: studies in an animal model of migraine. Cephalalgia. 2005 ; 25: 612-621 (Pubitemid 41026027)
7. Varga H, Pardutz A, Vamos E, Bohar Z, Bago F, Tajti J, et al. Selective inhibition of cyclooxygenase-2 attenuates nitroglycerin-induced calmodulin-dependent protein kinase II alpha in rat trigeminal nucleus caudalis. Neurosci Lett. 2009 ; 451: 170-173
8. Tassorelli C, Joseph SA. Systemic nitroglycerin induces Fos immunoreactivity in brainstem and forebrain structures of the rat. Brain Res. 1995 ; 682: 167-181
9. Martin RS, Martin GR. Investigations into migraine pathogenesis: time course for effects of m-CPP, BW723C86 or glyceryl trinitrate on appearance of Fos-like immunoreactivity in rat trigeminal nucleus caudalis (TNC). Cephalalgia. 2001 ; 21: 46-52 (Pubitemid 32304300)
10. Offenhauser N, Zinck T, Hoffmann J, Schiemann K, Schuh-Hofer S, Rohde W, et al. CGRP release and c-fos expression within trigeminal nucleus caudalis of the rat following glyceryltrinitrate infusion. Cephalalgia. 2005 ; 25: 225-236 (Pubitemid 40321716)
11. Stenberg C, Ovlisen K, Svendsen O, Lauritzen B. Effect of local anaesthesia on neuronal c-fos expression in the spinal dorsal horn and hypothalamic paraventricular nucleus after surgery in rats. Basic Clin Pharmacol Toxicol. 2005 ; 96: 381-386 (Pubitemid 40676592)
12. Sommers MG, Nguyen NK, Veening JG, Vissers KC, Ritskes-Hoitinga M, van Egmond J. Suppression of noxious-induced c-fos expression in the rat lumbar spinal cord by isoflurane alone or combined with fentanyl. Anesth Analg. 2008 ; 106: 1303-1308 (Pubitemid 351450564)
13. Meng ID, Bereiter DA. Differential distribution of Fos-like immunoreactivity in the spinal trigeminal nucleus after noxious and innocuous thermal and chemical stimulation of rat cornea. Neuroscience. 1996 ; 72: 243-254 (Pubitemid 26092388)
14. Sugiyo S, Uehashi D, Satoh F, Abe T, Yonehara N, Kobayashi M, et al. Effects of systemic bicuculline or morphine on formalin-evoked pain-related behaviour and c-Fos expression in trigeminal nuclei after formalin injection into the lip or tongue in rats. Exp Brain Res. 2009 ; 196: 229-237
15. Nozaki K, Boccalini P, Moskowitz MA. Expression of c-fos-like immunoreactivity in brainstem after meningeal irritation by blood in the subarachnoid space. Neuroscience. 1992 ; 49: 669-680
16. Olesen J, Burstein R, Ashina M, Tfelt-Hansen P. Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol. 2009 ; 8: 679-690
17. Ramachandran R, Ploug KB, Hay-Schmidt A, Olesen J, Jansen-Olesen I, Gupta S. Nitric oxide synthase (NOS) in the trigeminal vascular system and other brain structures related to pain in rats. Neurosci Lett. 2010 ; 484: 192-196
18. Sixt ML, Messlinger K, Fischer MJ. Calcitonin gene-related peptide receptor antagonist olcegepant acts in the spinal trigeminal nucleus. Brain. 2009 ; 132: 3134-3141
19. Bunag R, Mullenix P. Augmentation of drug-induced blood pressure increases in rats by amorbarbital. Br J Pharmacol. 1972 ; 46: 511-513
20. Le Noble JL, Struyker-Boudier HA, Smits JF. Differential effects of general anesthetics on regional vasoconstrictor responses in the rat. Arch Int Pharmacodyn Ther. 1987 ; 289: 82-92 (Pubitemid 18039899)
21. Koulchitsky S, Fischer MJ, Messlinger K. Calcitonin gene-related peptide receptor inhibition reduces neuronal activity induced by prolonged increase in nitric oxide in the rat spinal trigeminal nucleus. Cephalalgia. 2009 ; 29: 408-417
22. Koulchitsky S, Fischer MJ, De CR, Schlechtweg PM, Messlinger K. Biphasic response to nitric oxide of spinal trigeminal neurons with meningeal input in rat-possible implications for the pathophysiology of headaches. J Neurophysiol. 2004 ; 92: 1320-1328 (Pubitemid 39100634)
23. Ashina M, Bendtsen L, Jensen R, Olesen J. Nitric oxide-induced headache in patients with chronic tension-type headache. Brain. 2000 ; 123: 1830-1837 (Pubitemid 30664285)
24. Gardiner SM, March JE, Kemp PA, Bennett T. Complex regional haemodynamic effects of anandamide in conscious rats. Br J Pharmacol. 2002 ; 135: 1889-1896 (Pubitemid 34478300)
25. US Department of Health and Human Services, Food and Drug Administration Center for Drug Evaluation and Research. Guidance for Industry: Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. 2005. http://www.fda.gov/downloads/Drugs/.../Guidances/ UCM078932.pdf.
26. Needleman P. Tolerance to the vascular effects of glyceryl trinitrate. J Pharmacol Exp Ther. 1970 ; 171: 98-102
27. Jones MG, Lever I, Bingham S, Read S, McMahon SB, Parsons A. Nitric oxide potentiates response of trigeminal neurones to dural or facial stimulation in the rat. Cephalalgia. 2001 ; 21: 643-655 (Pubitemid 32762787)
28. Oshinsky ML, Gomonchareonsiri S. Episodic dural stimulation in awake rats: a model for recurrent headache. Headache. 2007 ; 47: 1026-1036 (Pubitemid 47057229)
29. Hossaini M, Duraku LS, Sarac C, Jongen JL, Holstege JC. Differential distribution of activated spinal neurons containing glycine and/or GABA and expressing c-fos in acute and chronic pain models. Pain. 2010 ; 151: 356-365
30. Pinto M, Lima D, Tavares I. Neuronal activation at the spinal cord and medullary pain control centers after joint stimulation: a c-fos study in acute and chronic articular inflammation. Neuroscience. 2007 ; 147: 1076-1089 (Pubitemid 47102552)
31. Bullitt E. Somatotopy of spinal nociceptive processing. J Comp Neurol. 1991 ; 312: 279-290
32. Hunt SP, Pini A, Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 1987 ; 328: 632-634 (Pubitemid 17103967)
33. Ter Horst GJ, Meijler WJ, Korf J, Kemper RH. Trigeminal nociception-induced cerebral Fos expression in the conscious rat. Cephalalgia. 2001 ; 21: 963-975 (Pubitemid 34626033)
34. Strassman AM, Mineta Y, Vos BP. Distribution of fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood vessels in the rat. J Neurosci. 1994 ; 14: 3725-3735 (Pubitemid 24174119)
35. Moskowitz MA, Nozaki K, Kraig RP. Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J Neurosci. 1993 ; 13: 1167-1177 (Pubitemid 23067603)
36. Nozaki K, Moskowitz MA, Boccalini P. CP-93,129, sumatriptan, dihydroergotamine block c-fos expression within rat trigeminal nucleus caudalis caused by chemical stimulation of the meninges. Br J Pharmacol. 1992 ; 106: 409-415
37. Strassman AM, Vos BP. Somatotopic and laminar organization of fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J Comp Neurol. 1993 ; 331: 495-516 (Pubitemid 23133541)
38. Ray BS, Wolff HG. Experimental studies on headache; pain-sensitive structures of the head and their significance in headache. Arch Surg. 1940 ; 41: 813-856
39. Thomsen LL, Brennum J, Iversen HK, Olesen J. Effect of a nitric oxide donor (glyceryl trinitrate) on nociceptive thresholds in man. Cephalalgia. 1996 ; 16: 169-174 (Pubitemid 26163559)
40. Devor M Proceedings of the Vth World Congress on Pain. Dubner R Gebhart GF Bond MR, ed. Amsterdam: Elsevier Science ; 1988: 114-128.
41. Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science. 2000 ; 288: 1765-1769
42. Iversen HK, Olesen J. Headache induced by a nitric oxide donor (nitroglycerin) responds to sumatriptan. A human model for development of migraine drugs. Cephalalgia. 1996 ; 16: 412-418 (Pubitemid 26338471)
43. Asghar MS, Hansen AE, Amin FM, van der Geest RJ, Koning P, Larsson HB, et al. Evidence for a vascular factor in migraine. Ann Neurol. 2011 ; 69: 635-645
44. Goadsby PJ, Edvinsson L. The trigeminovascular system and migraine: studies characterizing cerebrovascular and neuropeptide changes seen in humans and cats. Ann Neurol. 1993 ; 33: 48-56 (Pubitemid 23009909)
45. Kaube H, Hoskin KL, Goadsby PJ. Inhibition by sumatriptan of central trigeminal neurones only after blood-brain barrier disruption. Br J Pharmacol. 1993 ; 109: 788-792 (Pubitemid 23181062)