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Published in: The Journal of Headache and Pain 1/2017

Open Access 01-12-2017 | Research article

The role of the transient receptor potential ankyrin type-1 (TRPA1) channel in migraine pain: evaluation in an animal model

Authors: Chiara Demartini, Cristina Tassorelli, Anna Maria Zanaboni, Germana Tonsi, Oscar Francesconi, Cristina Nativi, Rosaria Greco

Published in: The Journal of Headache and Pain | Issue 1/2017

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Abstract

Background

Clinical and experimental studies have pointed to the possible involvement of the transient receptor potential ankyrin type-1 (TRPA1) channels in migraine pain. In this study, we aimed to further investigate the role of these channels in an animal model of migraine using a novel TRPA1 antagonist, ADM_12, as a probe.

Methods

The effects of ADM_12 on nitroglycerin-induced hyperalgesia at the trigeminal level were investigated in male rats using the quantification of nocifensive behavior in the orofacial formalin test. The expression levels of the genes coding for c-Fos, TRPA1, calcitonin gene-related peptide (CGRP) and substance P (SP) in peripheral and central areas relevant for migraine pain were analyzed. CGRP and SP protein immunoreactivity was also evaluated in trigeminal nucleus caudalis (TNC).

Results

In rats bearing nitroglycerin-induced hyperalgesia, ADM_12 showed an anti-hyperalgesic effect in the second phase of the orofacial formalin test. This effect was associated to a significant inhibition of nitroglycerin-induced increase in c-Fos, TRPA1 and neuropeptides mRNA levels in medulla-pons area, in the cervical spinal cord and in the trigeminal ganglion. No differences between groups were seen as regards CGRP and SP protein expression in the TNC.

Conclusions

These findings support a critical involvement of TRPA1 channels in the pathophysiology of migraine, and show their active role in counteracting hyperalgesia at the trigeminal level.
Literature
2.
go back to reference Nassini R, Materazzi S, Benemei S, Geppetti P (2014) The TRPA1 channel in inflammatory and neuropathic pain and migraine. Rev Physiol Biochem Pharmacol 167:1–43CrossRefPubMed Nassini R, Materazzi S, Benemei S, Geppetti P (2014) The TRPA1 channel in inflammatory and neuropathic pain and migraine. Rev Physiol Biochem Pharmacol 167:1–43CrossRefPubMed
3.
go back to reference Lima AM, Sapienza GB, Giraud Vde O, Fragoso YD (2011) Odors as triggering and worsening factors for migraine in men. Arq Neuropsiquiatr 69:324–327CrossRefPubMed Lima AM, Sapienza GB, Giraud Vde O, Fragoso YD (2011) Odors as triggering and worsening factors for migraine in men. Arq Neuropsiquiatr 69:324–327CrossRefPubMed
4.
go back to reference Kandasamy R, Lee AT, Morgan MM (2017) Depression of home cage wheel running: a reliable and clinically relevant method to assess migraine pain in rats. J Headache Pain 18(1):5CrossRefPubMedPubMedCentral Kandasamy R, Lee AT, Morgan MM (2017) Depression of home cage wheel running: a reliable and clinically relevant method to assess migraine pain in rats. J Headache Pain 18(1):5CrossRefPubMedPubMedCentral
5.
go back to reference Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112(6):819–829CrossRefPubMed Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112(6):819–829CrossRefPubMed
6.
go back to reference Barabas ME, Kossyreva EA, Stucky CL (2012) TRPA1 is functionally expressed primarily by IB4-binding, non-peptidergic mouse and rat sensory neurons. PLoS One 7(10):e47988CrossRefPubMedPubMedCentral Barabas ME, Kossyreva EA, Stucky CL (2012) TRPA1 is functionally expressed primarily by IB4-binding, non-peptidergic mouse and rat sensory neurons. PLoS One 7(10):e47988CrossRefPubMedPubMedCentral
7.
go back to reference Nicoletti P, Trevisani M, Manconi M, Gatti R, De SG, Zagli G, Benemei S, Capone JA, Geppetti P, Pini LA (2008) Ethanol causes neurogenic vasodilation by TRPV1 activation and CGRP release in the trigeminovascular system of the guinea pig. Cephalalgia 28:9–17CrossRefPubMed Nicoletti P, Trevisani M, Manconi M, Gatti R, De SG, Zagli G, Benemei S, Capone JA, Geppetti P, Pini LA (2008) Ethanol causes neurogenic vasodilation by TRPV1 activation and CGRP release in the trigeminovascular system of the guinea pig. Cephalalgia 28:9–17CrossRefPubMed
8.
go back to reference Kunkler PE, Ballard CJ, Oxford GS, Hurley JH (2011) TRPA1 receptors mediate environmental irritant-induced meningeal vasodilatation. Pain 152(1):38–44CrossRefPubMed Kunkler PE, Ballard CJ, Oxford GS, Hurley JH (2011) TRPA1 receptors mediate environmental irritant-induced meningeal vasodilatation. Pain 152(1):38–44CrossRefPubMed
9.
go back to reference Amaya F, Oh-hashi K, Naruse Y, Iijima N, Ueda M, Shimosato G, Tominaga M, Tanaka Y, Tanaka M (2003) Local inflammation increases vanilloid receptor 1 expression within distinct subgroups of DRG neurons. Brain Res 963(1–2):190–196CrossRefPubMed Amaya F, Oh-hashi K, Naruse Y, Iijima N, Ueda M, Shimosato G, Tominaga M, Tanaka Y, Tanaka M (2003) Local inflammation increases vanilloid receptor 1 expression within distinct subgroups of DRG neurons. Brain Res 963(1–2):190–196CrossRefPubMed
10.
go back to reference Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12(1):89–94CrossRefPubMed Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12(1):89–94CrossRefPubMed
11.
go back to reference Nassini R, Materazzi S, Vriens J, Prenen J, Benemei S, De Siena G, la Marca G, Andrè E, Preti D, Avonto C, Sadofsky L, Di Marzo V, De Petrocellis L, Dussor G, Porreca F, Taglialatela-Scafati O, Appendino G, Nilius B, Geppetti P (2012) The ‘headache tree’ via umbellulone and TRPA1 activates the trigeminovascular system. Brain 135:376–390CrossRefPubMed Nassini R, Materazzi S, Vriens J, Prenen J, Benemei S, De Siena G, la Marca G, Andrè E, Preti D, Avonto C, Sadofsky L, Di Marzo V, De Petrocellis L, Dussor G, Porreca F, Taglialatela-Scafati O, Appendino G, Nilius B, Geppetti P (2012) The ‘headache tree’ via umbellulone and TRPA1 activates the trigeminovascular system. Brain 135:376–390CrossRefPubMed
13.
go back to reference Dux M, Will C, Vogler B, Filipovic MR, Messlinger K (2016) Meningeal blood flow is controlled by H2 S-NO crosstalk activating a HNO-TRPA1-CGRP signalling pathway. Br J Pharmacol 173(3):431–445CrossRefPubMed Dux M, Will C, Vogler B, Filipovic MR, Messlinger K (2016) Meningeal blood flow is controlled by H2 S-NO crosstalk activating a HNO-TRPA1-CGRP signalling pathway. Br J Pharmacol 173(3):431–445CrossRefPubMed
14.
go back to reference Marics B, Peitl B, Varga A, Pázmándi K, Bácsi A, Németh J, Szilvássy Z, Jancsó G, Dux M (2017) Diet-induced obesity alters dural CGRP release and potentiates TRPA1-mediated trigeminovascular responses. Cephalalgia 37(6):581–591CrossRefPubMed Marics B, Peitl B, Varga A, Pázmándi K, Bácsi A, Németh J, Szilvássy Z, Jancsó G, Dux M (2017) Diet-induced obesity alters dural CGRP release and potentiates TRPA1-mediated trigeminovascular responses. Cephalalgia 37(6):581–591CrossRefPubMed
15.
go back to reference Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Högestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427(6971):260–265CrossRefPubMed Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Högestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427(6971):260–265CrossRefPubMed
16.
go back to reference Tassorelli C, Greco R, Wang D, Sandrini M, Sandrini G, Nappi G (2003) Nitroglycerin induces hyperalgesia in rats--a time-course study. Eur J Pharmacol 464(2–3):159–162CrossRefPubMed Tassorelli C, Greco R, Wang D, Sandrini M, Sandrini G, Nappi G (2003) Nitroglycerin induces hyperalgesia in rats--a time-course study. Eur J Pharmacol 464(2–3):159–162CrossRefPubMed
17.
go back to reference Greco R, Gasperi V, Sandrini G, Bagetta G, Nappi G, Maccarrone M, Tassorelli C (2010) Alterations of the endocannabinoid system in an animal model of migraine: evaluation in cerebral areas of rat. Cephalalgia 30(3):296–302CrossRefPubMed Greco R, Gasperi V, Sandrini G, Bagetta G, Nappi G, Maccarrone M, Tassorelli C (2010) Alterations of the endocannabinoid system in an animal model of migraine: evaluation in cerebral areas of rat. Cephalalgia 30(3):296–302CrossRefPubMed
18.
go back to reference Greco R, Mangione AS, Sandrini G, Maccarrone M, Nappi G, Tassorelli C (2011) Effects of anandamide in migraine: data from an animal model. J Headache Pain 12(2):177–183CrossRefPubMedPubMedCentral Greco R, Mangione AS, Sandrini G, Maccarrone M, Nappi G, Tassorelli C (2011) Effects of anandamide in migraine: data from an animal model. J Headache Pain 12(2):177–183CrossRefPubMedPubMedCentral
19.
go back to reference Greco R, Mangione AS, Sandrini G, Nappi G, Tassorelli C (2014) Activation of CB2 receptors as a potential therapeutic target for migraine: evaluation in an animal model. J Headache Pain 15:14CrossRefPubMedPubMedCentral Greco R, Mangione AS, Sandrini G, Nappi G, Tassorelli C (2014) Activation of CB2 receptors as a potential therapeutic target for migraine: evaluation in an animal model. J Headache Pain 15:14CrossRefPubMedPubMedCentral
20.
go back to reference Greco R, Bandiera T, Mangione A, Demartini C, Siani F, Nappi G, Sandrini G, Guijarro A, Armirotti A, Piomelli D, Tassorelli C (2015) Effects of peripheral FAAH blockade on NTG-induced hyperalgesia-evaluation of URB937 in an animal model of migraine. Cephalalgia 35(12):1065–1076CrossRefPubMed Greco R, Bandiera T, Mangione A, Demartini C, Siani F, Nappi G, Sandrini G, Guijarro A, Armirotti A, Piomelli D, Tassorelli C (2015) Effects of peripheral FAAH blockade on NTG-induced hyperalgesia-evaluation of URB937 in an animal model of migraine. Cephalalgia 35(12):1065–1076CrossRefPubMed
21.
go back to reference Greco R, Demartini C, Zanaboni AM, Redavide E, Pampalone S, Toldi J, Fülöp F, Blandini F, Nappi G, Sandrini G, Vécsei L, Tassorelli C (2016) Effects of kynurenic acid analogue 1 (KYNA-A1) in nitroglycerin-induced hyperalgesia: targets and anti-migraine mechanisms. Cephalalgia. doi:10.1177/0333102416678000. Greco R, Demartini C, Zanaboni AM, Redavide E, Pampalone S, Toldi J, Fülöp F, Blandini F, Nappi G, Sandrini G, Vécsei L, Tassorelli C (2016) Effects of kynurenic acid analogue 1 (KYNA-A1) in nitroglycerin-induced hyperalgesia: targets and anti-migraine mechanisms. Cephalalgia. doi:10.​1177/​0333102416678000​.
22.
go back to reference Zimmerman M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109–110CrossRef Zimmerman M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109–110CrossRef
23.
go back to reference Gualdani R, Ceruti S, Magni G, Merli D, Di Cesare ML, Francesconi O, Richichi B, la Marca G, Ghelardini C, Moncelli MR, Nativi C (2015) Lipoic-based TRPA1/TRPV1 antagonist to treat orofacial pain. ACS Chem Neurosci 6(3):380–385CrossRefPubMed Gualdani R, Ceruti S, Magni G, Merli D, Di Cesare ML, Francesconi O, Richichi B, la Marca G, Ghelardini C, Moncelli MR, Nativi C (2015) Lipoic-based TRPA1/TRPV1 antagonist to treat orofacial pain. ACS Chem Neurosci 6(3):380–385CrossRefPubMed
24.
25.
go back to reference Greco R, Ferrigno A, Demartini C, Zanaboni A, Mangione AS, Blandini F, Nappi G, Vairetti M, Tassorelli C (2015) Evaluation of ADMA-DDAH-NOS axis in specific brain areas following nitroglycerin administration: study in an animal model of migraine. J Headache Pain 16(1):560CrossRefPubMed Greco R, Ferrigno A, Demartini C, Zanaboni A, Mangione AS, Blandini F, Nappi G, Vairetti M, Tassorelli C (2015) Evaluation of ADMA-DDAH-NOS axis in specific brain areas following nitroglycerin administration: study in an animal model of migraine. J Headache Pain 16(1):560CrossRefPubMed
26.
go back to reference Greco R, Siani F, Demartini C, Zanaboni A, Nappi G, Davinelli S, Scapagnini G, Tassorelli C (2016) Andrographis Paniculata shows anti-nociceptive effects in an animal model of sensory hypersensitivity associated with migraine. Funct Neurol 31(1):53–60PubMedPubMedCentral Greco R, Siani F, Demartini C, Zanaboni A, Nappi G, Davinelli S, Scapagnini G, Tassorelli C (2016) Andrographis Paniculata shows anti-nociceptive effects in an animal model of sensory hypersensitivity associated with migraine. Funct Neurol 31(1):53–60PubMedPubMedCentral
27.
go back to reference Greco R, Tassorelli C, Sandrini G, Di Bella P, Buscone S, Nappi G (2008) Role of calcitonin gene-related peptide and substance P in different models of pain. Cephalalgia 28(2):114–126PubMed Greco R, Tassorelli C, Sandrini G, Di Bella P, Buscone S, Nappi G (2008) Role of calcitonin gene-related peptide and substance P in different models of pain. Cephalalgia 28(2):114–126PubMed
28.
go back to reference Tajti J, Szok D, Majláth Z, Tuka B, Csáti A, Vécsei L (2015) Migraine and neuropeptides. Neuropeptides 52:19–30CrossRefPubMed Tajti J, Szok D, Majláth Z, Tuka B, Csáti A, Vécsei L (2015) Migraine and neuropeptides. Neuropeptides 52:19–30CrossRefPubMed
29.
go back to reference Greco R, Mangione AS, Siani F, Blandini F, Vairetti M, Nappi G, Sandrini G, Buzzi MG, Tassorelli C (2014) Effects of CGRP receptor antagonism in nitroglycerin-induced hyperalgesia. Cephalalgia 34(8):594–604CrossRefPubMed Greco R, Mangione AS, Siani F, Blandini F, Vairetti M, Nappi G, Sandrini G, Buzzi MG, Tassorelli C (2014) Effects of CGRP receptor antagonism in nitroglycerin-induced hyperalgesia. Cephalalgia 34(8):594–604CrossRefPubMed
30.
go back to reference Greco R, Tassorelli C, Armentero MT, Sandrini G, Nappi G, Blandini F (2008) Role of central dopaminergic circuitry in pain processing and nitroglycerin-induced hyperalgesia. Brain Res 1238:215–223CrossRefPubMed Greco R, Tassorelli C, Armentero MT, Sandrini G, Nappi G, Blandini F (2008) Role of central dopaminergic circuitry in pain processing and nitroglycerin-induced hyperalgesia. Brain Res 1238:215–223CrossRefPubMed
31.
go back to reference McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM, Fanger CM (2007) TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 104(33):13525–13530CrossRefPubMedPubMedCentral McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM, Fanger CM (2007) TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 104(33):13525–13530CrossRefPubMedPubMedCentral
32.
go back to reference Tassorelli C, Armentero M-T, Greco R, Fancellu R, Sandrini G, Nappi G, Blandini F (2007) Behavioral responses and Fos activation following painful stimuli in a rodent model of Parkinson's disease. Brain Res 1176(1):53–61CrossRefPubMed Tassorelli C, Armentero M-T, Greco R, Fancellu R, Sandrini G, Nappi G, Blandini F (2007) Behavioral responses and Fos activation following painful stimuli in a rodent model of Parkinson's disease. Brain Res 1176(1):53–61CrossRefPubMed
33.
go back to reference Launay PS, Reboussin E, Liang H, Kessal K, Godefroy D, Rostene W, Sahel JA, Baudouin C, Melik Parsadaniantz S, Reaux Le Goazigo A (2016) Ocular inflammation induces trigeminal pain, peripheral and central neuroinflammatory mechanisms. Neurobiol Dis 88:16–28CrossRefPubMed Launay PS, Reboussin E, Liang H, Kessal K, Godefroy D, Rostene W, Sahel JA, Baudouin C, Melik Parsadaniantz S, Reaux Le Goazigo A (2016) Ocular inflammation induces trigeminal pain, peripheral and central neuroinflammatory mechanisms. Neurobiol Dis 88:16–28CrossRefPubMed
34.
go back to reference Lambert GA, Donaldson C, Boers PM, Zagami AS (2000) Activation of trigeminovascular neurons by glyceryl trinitrate. Brain Res 887(1):203–210CrossRefPubMed Lambert GA, Donaldson C, Boers PM, Zagami AS (2000) Activation of trigeminovascular neurons by glyceryl trinitrate. Brain Res 887(1):203–210CrossRefPubMed
35.
go back to reference Imbe H, Iwata K, Zhou QQ, Zou S, Dubner R, Ren K (2001) Orofacial deep and cutaneous tissue inflammation and trigeminal neuronal activation. Implications for persistent temporomandibular pain. Cells Tissues Organs 169(3):238–247CrossRefPubMed Imbe H, Iwata K, Zhou QQ, Zou S, Dubner R, Ren K (2001) Orofacial deep and cutaneous tissue inflammation and trigeminal neuronal activation. Implications for persistent temporomandibular pain. Cells Tissues Organs 169(3):238–247CrossRefPubMed
36.
go back to reference Zhuang D, Kawajiri H, Takahashi Y, Yoshimoto T (2000) Suppression of prostaglandin E(2)-mediated c-fos mRNA induction by interleukin-4 in murine macrophages. J Biochem 127(3):451–456CrossRefPubMed Zhuang D, Kawajiri H, Takahashi Y, Yoshimoto T (2000) Suppression of prostaglandin E(2)-mediated c-fos mRNA induction by interleukin-4 in murine macrophages. J Biochem 127(3):451–456CrossRefPubMed
37.
go back to reference Nummenmaa E, Hämäläinen M, Moilanen LJ, Paukkeri EL, Nieminen RM, Moilanen T, Vuolteenaho K, Moilanen E (2016) Transient receptor potential ankyrin 1 (TRPA1) is functionally expressed in primary human osteoarthritic chondrocytes. Arthritis Res Ther 18(1):185CrossRefPubMedPubMedCentral Nummenmaa E, Hämäläinen M, Moilanen LJ, Paukkeri EL, Nieminen RM, Moilanen T, Vuolteenaho K, Moilanen E (2016) Transient receptor potential ankyrin 1 (TRPA1) is functionally expressed in primary human osteoarthritic chondrocytes. Arthritis Res Ther 18(1):185CrossRefPubMedPubMedCentral
38.
go back to reference Torfgard K, Ahnler J, Axelsson KL, Norlander B, Bertler A (1989) Tissue distribution of glyceryl trinitrate and the effect on cGMP levels in rat. Pharmacol Toxicol 64:369–372CrossRefPubMed Torfgard K, Ahnler J, Axelsson KL, Norlander B, Bertler A (1989) Tissue distribution of glyceryl trinitrate and the effect on cGMP levels in rat. Pharmacol Toxicol 64:369–372CrossRefPubMed
39.
go back to reference Reuter U, Bolay H, Jansen-Olesen I, Chiarugi A, Sanchez del Rio M, Letourneau R, Theoharides TC, Waeber C, Moskowitz MA (2001) Delayed inflammation in rat meninges: implications for migraine pathophysiology. Brain 124(Pt 12):2490–2502CrossRefPubMed Reuter U, Bolay H, Jansen-Olesen I, Chiarugi A, Sanchez del Rio M, Letourneau R, Theoharides TC, Waeber C, Moskowitz MA (2001) Delayed inflammation in rat meninges: implications for migraine pathophysiology. Brain 124(Pt 12):2490–2502CrossRefPubMed
40.
go back to reference Greco R, Tassorelli C, Cappelletti D, Sandrini G, Nappi G (2005) Activation of the transcription factor NF-kappaB in the nucleus trigeminalis caudalis in an animal model of migraine. Neurotoxicology 26(5):795–800CrossRefPubMed Greco R, Tassorelli C, Cappelletti D, Sandrini G, Nappi G (2005) Activation of the transcription factor NF-kappaB in the nucleus trigeminalis caudalis in an animal model of migraine. Neurotoxicology 26(5):795–800CrossRefPubMed
41.
go back to reference Diogenes A, Akopian AN, Hargreaves KM (2007) NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 86(6):550–555CrossRefPubMed Diogenes A, Akopian AN, Hargreaves KM (2007) NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 86(6):550–555CrossRefPubMed
42.
go back to reference Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, Mori Y (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596–607CrossRefPubMed Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, Mori Y (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596–607CrossRefPubMed
43.
go back to reference Miyamoto T, Dubin AE, Petrus MJ, Patapoutian A (2009) TRPV1 and TRPA1 mediate peripheral nitric oxide-induced nociception in mice. PLoS One 4(10):e7596CrossRefPubMedPubMedCentral Miyamoto T, Dubin AE, Petrus MJ, Patapoutian A (2009) TRPV1 and TRPA1 mediate peripheral nitric oxide-induced nociception in mice. PLoS One 4(10):e7596CrossRefPubMedPubMedCentral
45.
go back to reference Bonet IJ, Fischer L, Parada CA, Tambeli CH (2013) The role of transient receptor potential a 1 (TRPA1) in the development and maintenance of carrageenan-induced hyperalgesia. Neuropharmacology 65:206–212CrossRefPubMed Bonet IJ, Fischer L, Parada CA, Tambeli CH (2013) The role of transient receptor potential a 1 (TRPA1) in the development and maintenance of carrageenan-induced hyperalgesia. Neuropharmacology 65:206–212CrossRefPubMed
46.
go back to reference Hatano N, Itoh Y, Suzuki H, Muraki Y, Hayashi H, Onozaki K, Wood IC, Beech DJ, Muraki K (2012) Hypoxia-inducible factor-1α (HIF1α) switches on transient receptor potential ankyrin repeat 1 (TRPA1) gene expression via a hypoxia response element-like motif to modulate cytokine release. J Biol Chem 287(38):31962–31972CrossRefPubMedPubMedCentral Hatano N, Itoh Y, Suzuki H, Muraki Y, Hayashi H, Onozaki K, Wood IC, Beech DJ, Muraki K (2012) Hypoxia-inducible factor-1α (HIF1α) switches on transient receptor potential ankyrin repeat 1 (TRPA1) gene expression via a hypoxia response element-like motif to modulate cytokine release. J Biol Chem 287(38):31962–31972CrossRefPubMedPubMedCentral
47.
go back to reference Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA (2007) Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 10(3):277–279CrossRefPubMed Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA (2007) Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 10(3):277–279CrossRefPubMed
48.
go back to reference Mandadi S, Armati PJ, Roufogalis BD (2011) Protein kinase C modulation of thermo-sensitive transient receptor potential channels: implications for pain signaling. J Nat Sci Biol Med 2(1):13–25CrossRefPubMedPubMedCentral Mandadi S, Armati PJ, Roufogalis BD (2011) Protein kinase C modulation of thermo-sensitive transient receptor potential channels: implications for pain signaling. J Nat Sci Biol Med 2(1):13–25CrossRefPubMedPubMedCentral
49.
go back to reference Roza C, Reeh PW (2001) Substance P, calcitonin gene related peptide and PGE2 co-released from the mouse colon: a new model to study nociceptive and inflammatory responses in viscera, in vitro. Pain 93(3):213–219CrossRefPubMed Roza C, Reeh PW (2001) Substance P, calcitonin gene related peptide and PGE2 co-released from the mouse colon: a new model to study nociceptive and inflammatory responses in viscera, in vitro. Pain 93(3):213–219CrossRefPubMed
50.
go back to reference Juránek I, Lembeck F (1997) Afferent C-fibres release substance P and glutamate. Can J Physiol Pharmacol 75(6):661–664CrossRefPubMed Juránek I, Lembeck F (1997) Afferent C-fibres release substance P and glutamate. Can J Physiol Pharmacol 75(6):661–664CrossRefPubMed
51.
go back to reference Huang D, Li S, Dhaka A, Story GM, Cao YQ (2012) Expression of the transient receptor potential channels TRPV1, TRPA1 and TRPM8 in mouse trigeminal primary afferent neurons innervating the dura. Mol Pain 8:66CrossRefPubMedPubMedCentral Huang D, Li S, Dhaka A, Story GM, Cao YQ (2012) Expression of the transient receptor potential channels TRPV1, TRPA1 and TRPM8 in mouse trigeminal primary afferent neurons innervating the dura. Mol Pain 8:66CrossRefPubMedPubMedCentral
52.
go back to reference Fischer MJ, Soller KJ, Sauer SK, Kalucka J, Veglia G, Reeh PW (2015) Formalin evokes calcium transients from the endoplasmatic reticulum. PLoS One 10(4):e0123762CrossRefPubMedPubMedCentral Fischer MJ, Soller KJ, Sauer SK, Kalucka J, Veglia G, Reeh PW (2015) Formalin evokes calcium transients from the endoplasmatic reticulum. PLoS One 10(4):e0123762CrossRefPubMedPubMedCentral
53.
go back to reference Schaible HG, Schmidt RF (1988) Excitation and sensitization of fine articular afferents from cat's knee joint by prostaglandin E2. J Physiol 403:91–104CrossRefPubMedPubMedCentral Schaible HG, Schmidt RF (1988) Excitation and sensitization of fine articular afferents from cat's knee joint by prostaglandin E2. J Physiol 403:91–104CrossRefPubMedPubMedCentral
54.
go back to reference Binshtok AM, Wang H, Zimmermann K, Amaya F, Vardeh D, Shi L, Brenner GJ, Ji RR, Bean BP, Woolf CJ, Samad TA (2008) Nociceptors are interleukin-1beta sensors. J Neurosci 28(52):14062–14073CrossRefPubMedPubMedCentral Binshtok AM, Wang H, Zimmermann K, Amaya F, Vardeh D, Shi L, Brenner GJ, Ji RR, Bean BP, Woolf CJ, Samad TA (2008) Nociceptors are interleukin-1beta sensors. J Neurosci 28(52):14062–14073CrossRefPubMedPubMedCentral
55.
go back to reference Kun J, Szitter I, Kemény A, Perkecz A, Kereskai L, Pohóczky K, Vincze A, Gódi S, Szabó I, Szolcsányi J, Pintér E, Helyes Z (2014) Upregulation of the transient receptor potential ankyrin 1 ion channel in the inflamed human and mouse colon and its protective roles. PLoS One 9(9):e108164CrossRefPubMedPubMedCentral Kun J, Szitter I, Kemény A, Perkecz A, Kereskai L, Pohóczky K, Vincze A, Gódi S, Szabó I, Szolcsányi J, Pintér E, Helyes Z (2014) Upregulation of the transient receptor potential ankyrin 1 ion channel in the inflamed human and mouse colon and its protective roles. PLoS One 9(9):e108164CrossRefPubMedPubMedCentral
56.
go back to reference Billeter AT, Galbraith N, Walker S, Lawson C, Gardner SA, Sarojini H, Galandiuk S, Polk HC Jr (2015) TRPA1 mediates the effects of hypothermia on the monocyte inflammatory response. Surgery 158(3):646–654CrossRefPubMed Billeter AT, Galbraith N, Walker S, Lawson C, Gardner SA, Sarojini H, Galandiuk S, Polk HC Jr (2015) TRPA1 mediates the effects of hypothermia on the monocyte inflammatory response. Surgery 158(3):646–654CrossRefPubMed
57.
go back to reference Helyes Z, Németh J, Pintér E, Szolcsányi J (1997) Inhibition by nociception of neurogenic inflammation and the release of SP and CGRP from sensory nerve terminals. Br J Pharmacol 121:613–615CrossRefPubMedPubMedCentral Helyes Z, Németh J, Pintér E, Szolcsányi J (1997) Inhibition by nociception of neurogenic inflammation and the release of SP and CGRP from sensory nerve terminals. Br J Pharmacol 121:613–615CrossRefPubMedPubMedCentral
58.
go back to reference Chen Y, Boettger MK, Reif A, Schmitt A, Uçeyler N, Sommer C (2010) Nitric oxide synthase modulates CFA-induced thermal hyperalgesia through cytokine regulation in mice. Mol Pain 6:13–23PubMedPubMedCentral Chen Y, Boettger MK, Reif A, Schmitt A, Uçeyler N, Sommer C (2010) Nitric oxide synthase modulates CFA-induced thermal hyperalgesia through cytokine regulation in mice. Mol Pain 6:13–23PubMedPubMedCentral
59.
go back to reference Neubert JK, Maidment NT, Matsuka Y, Adelson DW, Kruger L (2000) Spigelman I. Inflammation-induced changes in primary afferent-evoked release of substance P within trigeminal ganglia in vivo Brain Res 871:181–191PubMed Neubert JK, Maidment NT, Matsuka Y, Adelson DW, Kruger L (2000) Spigelman I. Inflammation-induced changes in primary afferent-evoked release of substance P within trigeminal ganglia in vivo Brain Res 871:181–191PubMed
60.
go back to reference Lu X, Geng X, Zhang L, Zeng Y, Dong H, Yu H (2009) Substance P expression in the distal cerebrospinal fluid-contacting neurons and spinal trigeminal nucleus in formalin-induced the orofacial inflammatory pain in rats. Brain Res Bull 78(4–5):139–144CrossRefPubMed Lu X, Geng X, Zhang L, Zeng Y, Dong H, Yu H (2009) Substance P expression in the distal cerebrospinal fluid-contacting neurons and spinal trigeminal nucleus in formalin-induced the orofacial inflammatory pain in rats. Brain Res Bull 78(4–5):139–144CrossRefPubMed
61.
go back to reference Nakamura Y, Une Y, Miyano K, Abe H, Hisaoka K, Morioka N, Nakata Y (2012) Activation of transient receptor potential ankyrin 1 evokes nociception through substance P release from primary sensory neurons. J Neurochem 120:1036–1047PubMed Nakamura Y, Une Y, Miyano K, Abe H, Hisaoka K, Morioka N, Nakata Y (2012) Activation of transient receptor potential ankyrin 1 evokes nociception through substance P release from primary sensory neurons. J Neurochem 120:1036–1047PubMed
Metadata
Title
The role of the transient receptor potential ankyrin type-1 (TRPA1) channel in migraine pain: evaluation in an animal model
Authors
Chiara Demartini
Cristina Tassorelli
Anna Maria Zanaboni
Germana Tonsi
Oscar Francesconi
Cristina Nativi
Rosaria Greco
Publication date
01-12-2017
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 1/2017
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1186/s10194-017-0804-4

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