Bilateral Parkinson’s disease model rats exhibit hyperalgesia to subcutaneous formalin administration into the vibrissa pad
Autoři:
Hiroharu Maegawa aff001; Nayuka Adachi aff001; Hiroshi Hanamoto aff001; Chiho Kudo aff001; Hitoshi Niwa aff001
Působiště autorů:
Department of Dental Anesthesiology, Osaka University Graduate School of Dentistry, Suita, Osaka, Japan
aff001
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225928
Souhrn
We bilaterally injected 6-hydroxydopamine (6-OHDA) into the medial forebrain bundle of rats and developed bilateral Parkinson’s disease (PD) model rats in order to experimentally investigate the neural mechanisms underlying the alteration of nociception in the orofacial region of patients with PD. We explored the effects of dopamine depletion on nociception by investigating behavioral responses (face rubbing) triggered by subcutaneous administration of formalin into the vibrissa pad. We also assessed the number of c-Fos–immunoreactive (c-Fos-IR) cells in the superficial layers of the trigeminal spinal subnucleus caudalis (Vc). Subcutaneous formalin administration evoked a two-phase increase in face rubbing. We observed the first increase 0–5 min after formalin administration (first phase) and the second increase 10–60 min after administration (second phase). The number of face rubbing behaviors of 6OHDA–injected rats did not significantly change compared with saline–injected rats in both phases. Significant increase of c-Fos-IR cells in the Vc was found in 6-OHDA–injected rats after formalin administration compared with those in saline–injected rats after formalin administration. We also assessed expression of c-Fos-IR cells in the paraventricular nucleus (PVN), and significant decrease of c-Fos-IR cells in the PVN of 6-OHDA–injected rats was found. Taken together, these findings suggest that bilateral dopaminergic denervation evoked by 6-OHDA administration causes hyperalgesia in the trigeminal region and the PVN may be involved in the hyperalgesia.
Klíčová slova:
Rats – Dopamine – Dopaminergics – Parkinson disease – Neostriatum – Nociception – Hyperalgesia – Vibrissae
Zdroje
1. Broen MP, Braaksma MM, Patijn J, Weber WE. Prevalence of pain in Parkinson’s disease: a systematic review using the modified QUADAS tool. Mov Disord. 2012; 27: 480–484. doi: 10.1002/mds.24054 22231908
2. Borsook D, Upadhyay J, Chudler EH, Brcerra L. A key role of the basal ganglia in pain and analgesia–insights gained through human functional imaging. Molecular Pain. 2010; 6: 27. doi: 10.1186/1744-8069-6-27 20465845
3. Maegawa H, Morimoto Y, Kudo C, Hanamoto H, Boku A, Sugimura M, et al. Neural mechanism underlying hyperalgesic response to orofacial pain in Parkinson’s disease model rats. Neurosci Res. 2015; 96: 59–68. doi: 10.1016/j.neures.2015.01.006 25637312
4. Ogata M, Noda K, Akita H, Ishibashi H. Characterization of nociceptive response to chemical, mechanical, and thermal stimuli in adolescent rats with neonatal dopamine depletion. Neurosci. 2015; 289: 43–55.
5. Takeda R, Ishida Y, Ebihara K, Abe H, Matsuo H, Ikeda T, et al. Intrastriatal grafts of fetal ventral mesencephalon improve allodynia-like withdrawal response to mechanical stimulation in a rat model of Parkinson’s disease. Neurosci Lett. 2014; 573: 19–23. doi: 10.1016/j.neulet.2014.05.007 24831182
6. Tassorelli C, Armentero MT, Greco R, Fancellu R, Sandrini J, Nappi G, et al. Behavioral responses and Fos activation following painful stimuli in a rodent model of Parkinson’s disease. Brain Res. 2007; 1176: 53–61. doi: 10.1016/j.brainres.2007.08.012 17884026
7. Cao LF, Peng XY, Huang Y, Wang B, Zhou FM, Cheng RX, et al. Restoring spinal noradrenergic inhibitory tone attenuates pain hypersensitivity in a rat model of Parkinson’s disease. Neural Plast. 2016; 2016: 6383240 doi: 10.1155/2016/6383240 27747105
8. Dieb W, Ouachikh O, Durif F, Hafidi A. Lesion of the dopaminergic nigrostriatal pathway induces trigeminal dynamic mechanical allodynia. Brain Behav. 2014; 4: 368–380. doi: 10.1002/brb3.214 24944866
9. Zengin-Toktas Y, Ferrier J, Durif F, Llorca PM, Authier N. Bilateral lesions of the nigrostriatal pathways are associated with chronic mechanical pain hypersensitivity in rats. Neurosci Res. 2013; 76: 261–264. doi: 10.1016/j.neures.2013.05.003 23684766
10. Deumens R, Blokland A, Prickaerts J. Modeling Parkinson’s disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol. 2002; 175: 303–317. doi: 10.1006/exnr.2002.7891 12061862
11. Blandini F, Armentero MT. Animal models of Parkinson’s disease. FEBS J. 2012; 279: 1156–1166. doi: 10.1111/j.1742-4658.2012.08491.x 22251459
12. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983; 16: 109–110. doi: 10.1016/0304-3959(83)90201-4 6877845
13. Bonato JM, Bassani TB, Milani H, Vital MABF, de Oliveira RMW. Pioglitazone reduced mortality, prevents depressive-like behavior, and impacts hippocampal neurogenesis in the 6-OHDA model of Parkinson’s disease in rats. Exp Neurol. 2018; 300: 188–200. doi: 10.1016/j.expneurol.2017.11.009 29162435
14. Yousofizadeh S, Tamaddonfard E, Farshid AA. The role of nicotinic acetylcholine and opioid systems of the ventral orbital cortex in modulation of formalin-induced orofacial pain in rats. Eur J Pharmacol. 2015; 758: 147–152. doi: 10.1016/j.ejphar.2015.04.002 25864612
15. Le Poul E, Bolea C, Girard F, Poli S, Charvin D, Campo B, et al. A potent and selective metabotropic glutamate receptor 4 positive allosteric modulator improves movement in rodent models of Parkinson’s disease. J Pharmacol Exp Ther. 2012; 343: 167–177. doi: 10.1124/jpet.112.196063 22787118
16. Abbadie C, Taylor BK, Peterson MA, Basbaum AI. Differential contribution of the two phases of the formalin test to the pattern of c-fos expression in the rat spinal cord: studies with remifentanil and lidocaine. Pain. 1997; 69: 101–110. doi: 10.1016/s0304-3959(96)03285-x 9060019
17. Kubo A, Shinoda M, Katagiri A, Takeda M, Suzuki T, Asaka J, et al. Oxytocin alleviates orofacial mechanical hypersensitivity associated with infraorbital nerve injury through vasopressin-1A receptors of the rat trigeminal ganglia. Pain. 2017; 158: 649–659. doi: 10.1097/j.pain.0000000000000808 28072605
18. Goodin BR, Ness TJ, Robbins MT. Oxytocin-a multifunctional analgesic for chronic deep tissue pain. Curr Pharm Des. 2015; 21: 906–913. doi: 10.2174/1381612820666141027111843 25345612
19. Juif PE, Poisbeau P. Neurohormonal effects of oxytocin and vasopressin receptor agonists on spinal pain processing in male rats. Pain. 2013; 154: 1449–1456. doi: 10.1016/j.pain.2013.05.003 23707282
20. Moreno-Lopez Y, Martinez-Lorenzana G, Condes-Lara M, Rojas-Piloni G. Identification of oxytocin receptor in the dorsal horn and nociceptive dorsal root ganglion neurons. Neuropeptides. 2013; 47: 117–123. doi: 10.1016/j.npep.2012.09.008 23102456
21. Tzabazis A, Mechanic J, Miller J, Klukinov M, Pascual C, Manering N, et al. Oxytocin receptor: expression in the trigeminal nociceptive system and potential role in the treatment of headache disorders. Cephalalgia. 2016; 36: 943–950. doi: 10.1177/0333102415618615 26590611
22. Purba JS, Hofman MA, Swaab DF. Decreased number of oxytocin-immunoreactive neurons in the paraventricular nucleus of the hypothalamus in Parkinson’s disease. Neurol. 1994; 44: 84–89.
23. Gomez-Paz A, Drucker-Colin R, Milan-Aldaco D, Palomero-Rivero M, Ambriz-Tututi M. Intrastriatal chromospheres’ transplant reduces nociception in hemiparkinsonian rats. Neurosci. 2018; 387: 123–134.
24. Jarcho JM, Mayer EA, Jiang ZK, Feier NA, London ED. Pain, affective symptoms, and cognitive deficits in patients with cerebral dopamine dysfunction. Pain. 2012; 153: 744–754. doi: 10.1016/j.pain.2012.01.002 22386471
25. Potvin S, Grignon S, Marchand S. Human evidence of a supra-spinal modulating role of dopamine on pain perception. Synapse. 2009; 63: 390–402. doi: 10.1002/syn.20616 19173266
26. Barcelo AC, Filippini B, Pazo JH. The striatum and pain modulation. Call Mol Neurobiol. 2012; 32: 1–12.
27. Cobacho N, de la Calle JL, Piano CL. Dopaminergic modulation of neuropathic pain: analgesia in rats by a D2-type receptor agonist. Brain Res Bull. 2014; 106: 62–71. doi: 10.1016/j.brainresbull.2014.06.003 24959942
28. Dang YH, Xing B, Zhao Y, Zhao XJ, Huo FQ, Tang JS, et al. The role of dopamine receptors in ventral orbital cortex-evoked antinociception in a rat formalin test model. Eur J Pharmacol. 2011; 657: 97–103. doi: 10.1016/j.ejphar.2011.01.064 21316357
29. Mann T, Zilles K, Dikow H, Hellfritsch A, Cremer M, Rosch F, et al. Dopamine, noradrenaline and serotonin receptor densities in the striatum of hemiparkinsonian rats following botulinum neurotoxin. Neurosci. 2018; 374: 184–204.
30. Emir UE, Tuite PJ, Oz G. Elevated pontine and putamental GABA levels in mild-moderate Parkinson disease detected by 7 tesla proton MRS. PLoS One. 2012; 7: e30918. doi: 10.1371/journal.pone.0030918 22295119
31. Sun Z, Jia J, Gong X, Jia Y, Deng J, Wang X. Inhibition of glutamate and acetylcholine release in behavioral improvement induced by electroacupuncture in parkinsonian rats. Neurosci Lett. 2012; 520: 32–37. doi: 10.1016/j.neulet.2012.05.021 22583765
32. Tong Q, Xu Q, Xia Q, Yuan Y, Zhang L, Sun H, et al. Correlations between plasma levels of amino acids and nonmotor symptoms in Parkinson’s disease. J Neural Transm. 2015; 122: 411–417. doi: 10.1007/s00702-014-1280-5 25059457
33. di Michele F, Luchetti S, Bernardi G, Romeo E, Longone P. Neurosteroid and neurotransmitter alterations in Parkinson’s disease. Front Neuroendocrinol. 2013; 34: 132–142. doi: 10.1016/j.yfrne.2013.03.001 23563222
34. Blaszczyk JW. Parkinson’s disease and neurodegeneration: GABA-collapse hypothesis. Front Neurosci. 2016; 10: 269. doi: 10.3389/fnins.2016.00269 27375426
35. Rangel-Barajas C, Silva I, Lopaz-Santiago LM, Aceves J, Erlij D, Floran B. L-DOPA-induced dyskinesia in hemiparkinsonian rats is associated with upregulation of adenyl cyclase type V/VI and increased GABA release in the substantia nigra reticulate. Neurobiol Dis. 2011; 41: 51–61. doi: 10.1016/j.nbd.2010.08.018 20736067
36. Yuan YS, Zhou XJ, Tong Q, Zhang L, Zhang L, Qi ZQ, et al. Change in plasma levels of amino acid neurotransmitters and its correlation with clinical heterogeneity in early Parkinson’s disease patients. CNS Neurosci Ther. 2013; 19: 889–896. doi: 10.1111/cns.12165 23981689
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts