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

Journal of Neural Transmission

Volumn 123, Issue 12, 2016, Pages 1403-1413

  Drinovac Vlah, V ^a   Bach Rojecky, L ^a   Lackovic Z ^b  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

BICUCULLINE; BOTULINUM TOXIN A; CAPSAICIN; CARRAGEENAN; NALOXONAZINE; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; ANALGESIC AGENT; CALCITONIN GENE RELATED PEPTIDE; NALOXONE;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; DRUG ACTIVITY; IMMUNOHISTOCHEMISTRY; MALE; MIRROR PAIN; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RAT; SCIATIC NERVE; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG ADMINISTRATION ROUTE; DRUG EFFECTS; HEMISPHERIC DOMINANCE; HYPERALGESIA; METABOLISM; PAIN MEASUREMENT; PATHOLOGY; PATHOPHYSIOLOGY; SPINAL CORD; WISTAR RAT;

ANALGESICS; ANIMALS; BICUCULLINE; BOTULINUM TOXINS, TYPE A; CALCITONIN GENE-RELATED PEPTIDE; CAPSAICIN; CARRAGEENAN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; FUNCTIONAL LATERALITY; HYPERALGESIA; MALE; NALOXONE; PAIN; PAIN MEASUREMENT; RATS; RATS, WISTAR; SPINAL CORD; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 84981213455     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-016-1605-7     Document Type: Article

References (48)

1. 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
2. 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
3. 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. 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
20. Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490(7419):201–207. doi:10.1038/nature11320
21. Jancalek R (2011) Signaling mechanisms in mirror image pain pathogenesis. Ann Neurosci 18(3):123–127. doi:10.5214/ans.0972-7531.11183010
22. 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):257–263
23. 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
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. 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
31. 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
32. 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
33. Pavone F, Luvisetto S (2010) Botulinum neurotoxin for pain management: insights from animal models. Toxins 2(12):2890–2913. doi:10.3390/toxins2122890
34. 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
35. 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
36. 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
37. 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
38. Ren K, Dubner R (1996) Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J Neurophysiol 76(5):3025–3037
39. 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
40. 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
41. 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
42. 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):5687–5693
43. Sluka KA, Kalra A, Moore SA (2001) Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24(1):37–46
44. 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
45. 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
46. 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
47. 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
48. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16(2):109–110