nach oben

Journal of Neural Transmission

Erschienen in:

09.08.2016 | Neurology and Preclinical Neurological Studies - Original Article

Antinociceptive action of botulinum toxin type A in carrageenan-induced mirror pain

verfasst von: V. Drinovac Vlah, L. Bach-Rojecky, Z. Lacković

Erschienen in: Journal of Neural Transmission | Ausgabe 12/2016

Einloggen, um Zugang zu erhalten

Abstract

“Mirror pain” or mirror-image pain (MP) is pain opposite to the side of injury. Mechanism and frequency in humans are not known. There is no consent on therapy. Here we report that unilaterally injected botulinum toxin type A (BT-A) has bilateral effect in experimental MP, thus deserves to be investigated as therapy for this condition. We examined the localization of BT-A’s bilateral antinociceptive action in MP induced by 3 % carrageenan intramuscular injection in Wistar rats. BT-A was applied peripherally (5 U/kg), into ipsilateral or contralateral hind paw pad (i.pl.) and centrally (1 U/kg), at spinal (intrathecally, i.t.) or supraspinal (intracisternally, i.c.) level. Additionally, we examined the involvement of central opioid and GABAergic systems, as well as the contribution of peripheral capsaicin-sensitive neurons to BT-A’s bilateral antinociceptive effect. Ipsilateral i.pl. and i.t. BT-A reduced the bilateral mechanical sensitivity to von Frey filaments, while contralateral i.pl. and i.c. treatments had no effect on either tested side. Bilateral antinociceptive effect of ipsilateral i.pl. BT-A was prevented by μ-opioid antagonist naloxonazine (1.5 μg/10 μl) and GABA_A antagonist bicuculline (1 μg/10 μl) if applied at the spinal level, in contrast to supraspinal application of the same doses. Local treatment of sciatic nerve with 2 % capsaicin 5 days following BT-A i.pl. injection caused desensitization of sciatic capsaicin-sensitive fibers, but did not affect bilateral antinociceptive effect of BT-A and the presence of cleaved SNAP-25 at the spinal cord slices. Present experiments suggest segmental actions of peripheral BT-A at spinal level, which are probably not solely dependent on capsaicin-sensitive neurons.

Ainsworth L, Budelier K, Clinesmith M, Fiedler A, Landstrom R, Leeper BJ, Moeller L, Mutch S, O’Dell K, Ross J, Radhakrishnan R, Sluka KA (2006) Transcutaneous electrical nerve stimulation (TENS) reduces chronic hyperalgesia induced by muscle inflammation. Pain 120(1–2):182–187. doi:10.1016/j.pain.2005.10.030 CrossRefPubMed

Antonucci F, Rossi C, Gianfranceschi L, Rossetto O, Caleo M (2008) Long-distance retrograde effects of botulinum neurotoxin A. J Neurosci 28(14):3689–3696. doi:10.1523/jneurosci.0375-08.2008 CrossRefPubMed

Bach-Rojecky L, Lacković Z (2009) Central origin of the antinociceptive action of botulinum toxin type A. Pharmacol Biochem Behav 94(2):234–238. doi:10.1016/j.pbb.2009.08.012 CrossRefPubMed

Bach-Rojecky L, Relja M, Lacković Z (2005) Botulinum toxin type A in experimental neuropathic pain. J Neural Transm 112(2):215–219. doi:10.1007/s00702-004-0265-1 CrossRefPubMed

Bach-Rojecky L, Dominis M, Lacković Z (2008) Lack of anti-inflammatory effect of botulinum toxin type A in experimental models of inflammation. Fundam Clin Pharmacol 22(5):503–509. doi:10.1111/j.1472-8206.2008.00615.x CrossRefPubMed

Bach-Rojecky L, Šalković-Petrišić M, Lacković Z (2010) Botulinum toxin type A reduces pain supersensitivity in experimental diabetic neuropathy: bilateral effect after unilateral injection. Eur J Pharmacol 633(1–3):10–14. doi:10.1016/j.ejphar.2010.01.020 CrossRefPubMed

Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53(1):55–63. doi:10.1016/0165-0270(94)90144-9 CrossRefPubMed

Da Silva LF, Desantana JM, Sluka KA (2010) Activation of NMDA receptors in the brainstem, rostral ventromedial medulla, and nucleus reticularis gigantocellularis mediates mechanical hyperalgesia produced by repeated intramuscular injections of acidic saline in rats. J Pain 11(4):378–387. doi:10.1016/j.jpain.2009.08.006 CrossRefPubMed

de la Llave-Rincón AI, Fernández-de-las-Peñas C, Fernández-Carnero J, Padua L, Arendt-Nielsen L, Pareja JA (2009) Bilateral hand/wrist heat and cold hyperalgesia, but not hypoesthesia, in unilateral carpal tunnel syndrome. Exp Brain Res 198(4):455–463. doi:10.1007/s00221-009-1941-z CrossRefPubMed

DeSantana JM, Da Silva LF, De Resende MA, Sluka KA (2009) Transcutaneous electrical nerve stimulation at both high and low frequencies activates ventrolateral periaqueductal grey to decrease mechanical hyperalgesia in arthritic rats. Neuroscience 163(4):1233–1241. doi:10.1016/j.neuroscience.2009.06.056 CrossRefPubMedPubMedCentral

Drinovac V, Bach-Rojecky L, Matak I, Lacković Z (2013) Involvement of μ-opioid receptors in antinociceptive action of botulinum toxin type A. Neuropharmacology 70:331–337. doi:10.1016/j.neuropharm.2013.02.011 CrossRefPubMed

Drinovac V, Bach-Rojecky L, Lacković Z (2014) Association of antinociceptive action of botulinum toxin type A with GABA-A receptor. J Neural Transm 121(6):665–669. doi:10.1007/s00702-013-1150-6 CrossRefPubMed

Favre-Guilmard C, Auguet M, Chabrier PE (2009) Different antinociceptive effects of botulinum toxin type A in inflammatory and peripheral polyneuropathic rat models. Eur J Pharmacol 617(1–3):48–53. doi:10.1016/j.ejphar.2009.06.047 CrossRefPubMed

Fernández-de-las-Peñas C, de la Llave-Rincón AI, Fernández-Carnero J, Cuadrado ML, Arendt-Nielsen L, Pareja JA (2009) Bilateral widespread mechanical pain sensitivity in carpal tunnel syndrome: evidence of central processing in unilateral neuropathy. Brain 132(Pt 6):1472–1479. doi:10.1093/brain/awp050 CrossRefPubMed

Filipović B, Matak I, Bach-Rojecky L, Lacković Z (2012) Central action of peripherally applied botulinum toxin type A on pain and dural protein extravasation in rat model of trigeminal neuropathy. PLoS One 7(1):e29803. doi:10.1371/journal.pone.0029803 CrossRefPubMedPubMedCentral

Gale K, Casu M (1981) Dynamic utilization of GABA in substantia nigra: regulation by dopamine and GABA in the striatum, and its clinical and behavioral implications. Mol Cell Biochem 39:369–405. doi:10.1007/BF00232586 CrossRefPubMed

Gautam M, Benson CJ, Ranier JD, Light AR, Sluka KA (2012) ASICs do not play a role in maintaining hyperalgesia induced by repeated intramuscular acid injections. Pain Res Treat 2012:817347. doi:10.1155/2012/817347 PubMed

Huang D, Yu B (2010) The mirror-image pain: an unclered phenomenon and its possible mechanism. Neurosci Biobehav Rev 34(4):528–532. doi:10.1016/j.neubiorev.2009.10.011 CrossRefPubMed

Huge V, Lauchart M, Förderreuther S, Kaufhold W, Valet M, Azad SC, Beyer A, Magerl W (2008) Interaction of hyperalgesia and sensory loss in complex regional pain syndrome type I (CRPS I). PLoS One 3(7):e2742. doi:10.1371/journal.pone.0002742 CrossRefPubMedPubMedCentral

Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490(7419):201–207. doi:10.1038/nature11320 CrossRefPubMedPubMedCentral

Jancalek R (2011) Signaling mechanisms in mirror image pain pathogenesis. Ann Neurosci 18(3):123–127. doi:10.5214/ans.0972-7531.11183010 CrossRefPubMedPubMedCentral

Kalra A, Urban MO, Sluka KA (2001) Blockade of opioid receptors in rostral ventral medulla prevents antihyperalgesia produced by transcutaneous electrical nerve stimulation (TENS). J Pharmacol Exp Ther 298(1):257–263PubMed

Koltzenburg M, Wall PD, McMahon SB (1999) Does the right side know what the left is doing? Trends Neurosci 22(3):122–127. doi:10.1016/S0166-2236(98)01302-2 CrossRefPubMed

Konopka KH, Harbers M, Houghton A, Kortekaas R, van Vliet A, Timmerman W, den Boer JA, Struys MM, van Wijhe M (2012) Bilateral sensory abnormalities in patients with unilateral neuropathic pain; a quantitative sensory testing (QST) study. PLoS One 7(5):e37524. doi:10.1371/journal.pone.0037524 CrossRefPubMedPubMedCentral

Lacković Z, Filipović B, Matak I, Helyes Z (2016) Botulinum toxin type A activity in cranial dura: implications for treatment of migraine and other headaches. Br J Pharmacol 173(2):279–291. doi:10.1111/bph.13366 CrossRefPubMed

Ledeboer A, Mahoney JH, Milligan ED, Martin D, Maier SF, Watkins LR (2006) Spinal cord glia and interleukin-1 do not appear to mediate persistent allodynia induced by intramuscular acidic saline in rats. J Pain 7(10):757–767. doi:10.1016/j.jpain.2006.04.001 CrossRefPubMed

Ling GS, Simantov R, Clark JA, Pasternak GW (1986) Naloxonazine actions in vivo. Eur J Pharmacol 129(1–2):33–38. doi:10.1016/0014-2999(86)90333-X CrossRefPubMed

Matak I, Lacković Z (2014) Botulinum toxin A, brain and pain. Prog Neurobiol 119–120:39–59. doi:10.1016/j.pneurobio.2014.06.001 CrossRefPubMed

Matak I, Bach-Rojecky L, Filipović B, Lacković Z (2011) Behavioral and immunohistochemical evidence for central antinociceptive activity of botulinum toxin A. Neuroscience 186:201–207. doi:10.1016/j.neuroscience.2011.04.026 CrossRefPubMed

Matak I, Riederer P, Lacković Z (2012) Botulinum toxin’s axonal transport from periphery to the spinal cord. Neurochem Int 61(2):236–239. doi:10.1016/j.neuint.2012.05.001 CrossRefPubMed

Matak I, Rossetto O, Lacković Z (2014) Botulinum toxin type A selectivity for certain types of pain is associated with capsaicin-sensitive neurons. Pain 155(8):1516–1526. doi:10.1016/j.pain.2014.04.027 CrossRefPubMed

Noble EP, Wurtman RJ, Axelrod J (1967) A simple and rapid method for injecting H3-norepinephrine into the lateral ventricle of the rat brain. Life Sci 6(3):281–291. doi:10.1016/0024-3205(67)90157-9 CrossRefPubMed

Pavone F, Luvisetto S (2010) Botulinum neurotoxin for pain management: insights from animal models. Toxins 2(12):2890–2913. doi:10.3390/toxins2122890 CrossRefPubMedPubMedCentral

Pertovaara A (1988) Collateral sprouting of nociceptive C-fibers after cut or capsaicin treatment of the sciatic nerve in adult rats. Neurosci Lett 90(3):248–253. doi:10.1016/0304-3940(88)90197-8 CrossRefPubMed

Radhakrishnan R, Sluka KA (2009) Increased glutamate and decreased glycine release in the rostral ventromedial medulla during induction of a pre-clinical model of chronic widespread muscle pain. Neurosci Lett 457(3):141–145. doi:10.1016/j.neulet.2009.03.086 CrossRefPubMedPubMedCentral

Radhakrishnan R, Moore SA, Sluka KA (2003) Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats. Pain 104(3):567–577. doi:10.1016/S0304-3959(03)00114-3 CrossRefPubMedPubMedCentral

Radhakrishnan R, Bement MK, Skyba D, Sluka KA, Kehl LJ (2004) Models of muscle pain: carrageenan model and acidic saline model. Curr Protoc Pharmacol Chapter 5, Unit 5.35. doi:10.1002/0471141755.ph0535s25

Ren K, Dubner R (1996) Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J Neurophysiol 76(5):3025–3037PubMed

Shenker N, Haigh R, Roberts E, Mapp P, Harris N, Blake D (2003) A review of contralateral responses to a unilateral inflammatory lesion. Rheumatology 42(11):1279–1286. doi:10.1093/rheumatology/keg397 CrossRefPubMed

Skyba DA, King EW, Sluka KA (2002) Effects of NMDA and non-NMDA ionotropic glutamate receptor antagonists on the development and maintenance of hyperalgesia induced by repeated intramuscular injection of acidic saline. Pain 98(1–2):69–78. doi:10.1016/S0304-3959(01)00471-7 CrossRefPubMed

Skyba DA, Lisi TL, Sluka KA (2005) Excitatory amino acid concentrations increase in the spinal cord dorsal horn after repeated intramuscular injection of acidic saline. Pain 119(1–3):142–149. doi:10.1016/j.pain.2005.09.025 CrossRefPubMed

Sluka KA (2002) Stimulation of deep somatic tissue with capsaicin produces long-lasting mechanical allodynia and heat hypoalgesia that depends on early activation of the cAMP pathway. J Neurosci 22(13):5687–5693PubMed

Sluka KA, Kalra A, Moore SA (2001) Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24(1):37–46CrossRefPubMed

Sluka KA, Price MP, Breese NM, Stucky CL, Wemmie JA, Welsh MJ (2003) Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 106(3):229–239. doi:10.1016/S0304-3959(03)00269-0 CrossRefPubMed

Sluka KA, Radhakrishnan R, Benson CJ, Eshcol JO, Price MP, Babinski K, Audette KM, Yeomans DC, Wilson SP (2007) ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain 129(1–2):102–112. doi:10.1016/j.pain.2006.09.038 CrossRefPubMed

Tillu DV, Gebhart GF, Sluka KA (2008) Descending facilitatory pathways from the RVM initiate and maintain bilateral hyperalgesia after muscle insult. Pain 136(3):331–339. doi:10.1016/j.pain.2007.07.011 CrossRefPubMed

Werner MU, Ringsted TK, Kehlet H, Wildgaard K (2013) Sensory testing in patients with postthoracotomy pain syndrome: Part 1: mirror-image sensory dysfunction. Clin J Pain 29(9):775–783. doi:10.1097/AJP.0b013e318277b646 CrossRefPubMed

Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16(2):109–110CrossRefPubMed

Titel: Antinociceptive action of botulinum toxin type A in carrageenan-induced mirror pain
verfasst von: V. Drinovac Vlah
L. Bach-Rojecky
Z. Lacković
Publikationsdatum: 09.08.2016
Verlag: Springer Vienna
Erschienen in: Journal of Neural Transmission / Ausgabe 12/2016
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-016-1605-7

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

18.04.2024 | Arterielle Hypertonie | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Antinociceptive action of botulinum toxin type A in carrageenan-induced mirror pain

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Antihypertensiva schützen auch alte Menschen noch vor Demenz

Spinale Muskelatrophie: Neugeborenen-Screening lohnt sich

Manche Gestagene können das Risiko für Meningeome erhöhen

Parkinson: Größere Studie bestätigt Genauigkeit von Hauttest

Update Neurologie

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 12/2016

Low digit ratio (2D:4D) in male suicide victims

Increased neurogranin concentrations in cerebrospinal fluid of Alzheimer’s disease and in mild cognitive impairment due to AD

Theta burst stimulation over premotor cortex in Parkinson’s disease: an explorative study on manual dexterity

Clinical radiological correlation in E200K familial Creutzfeldt–Jakob disease

A systematic review of the effects of low-frequency repetitive transcranial magnetic stimulation on cognition

Prevalence of small intestinal bacterial overgrowth in Chinese patients with Parkinson’s disease

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Antihypertensiva schützen auch alte Menschen noch vor Demenz

Spinale Muskelatrophie: Neugeborenen-Screening lohnt sich

Manche Gestagene können das Risiko für Meningeome erhöhen

Parkinson: Größere Studie bestätigt Genauigkeit von Hauttest

Update Neurologie