Parkinson's disease and pain: Modulation of nociceptive circuitry in a rat model of nigrostriatal lesion
Carregando...
Citações na Scopus
38
Tipo de produção
article
Data de publicação
2019
Título da Revista
ISSN da Revista
Título do Volume
Editora
ACADEMIC PRESS INC ELSEVIER SCIENCE
Autores
DOMENICI, Roberta A.
CAMPOS, Aria Carolina P.
MACIEL, Soraya T.
BERZUINO, Miria B.
HERNANDES, Marina S.
PAGANO, Rosana L.
Citação
EXPERIMENTAL NEUROLOGY, v.315, p.72-81, 2019
Resumo
Parkinson's disease (PD) is a neurodegenerative disorder that causes progressive dysfunction of dopaminergic and non-dopaminergic neurons, generating motor and nonmotor signs and symptoms. Pain is reported as the most bothersome nonmotor symptom in PD; however, pain remains overlooked and poorly understood. In this study, we evaluated the nociceptive behavior and the descending analgesia circuitry in a rat model of PD. Three independent experiments were performed to investigate: i) thermal nociceptive behavior; ii) mechanical nociceptive behavior and dopaminergic repositioning; and iii) modulation of the pain control circuitry. The rat model of PD, induced by unilateral striatal 6-hydroxydopamine (6-OHDA), did not interfere with thermal nociceptive responses; however, the mechanical nociceptive threshold was decreased bilaterally compared to that of naive or striatal saline-injected rats. This response was reversed by apomorphine or levodopa treatment. Striatal 6-OHDA induced motor impairments and reduced dopaminergic neuron immunolabeling as well as the pattern of neuronal activation (c-Fos) in the substantia nigra ipsilateral (IPL) to the lesion. In the midbrain periaqueductal gray (PAG), 6-OHDA-induced lesion increased IPL and decreased contralateral PAG GABAergic labeling compared to control. In the dorsal horn of the spinal cord, lesioned rats showed bilateral inhibition of enkephalin and p-opioid receptor labeling. Taken together, we demonstrated that the unilateral 6-OHDA-induced PD model induces bilateral mechanical hypernociception, which is reversed by dopamine restoration, changes in the PAG circuitry, and inhibition of spinal opioidergic regulation, probably due to impaired descending analgesic control. A better understanding of pain mechanisms in PD patients is critical for developing better therapeutic strategies to improve their quality of life.
Palavras-chave
Dopaminergic agonists, Enkephalin, GABA, Pain, Parkinson's disease, Perlaqueductal gray, Spinal cord
Referências
- AGID Y, 1991, LANCET, V337, P1321, DOI 10.1016/0140-6736(91)92989-F
- ANGLADE P, 1995, ANN NEUROL, V37, P265, DOI 10.1002/ana.410370219
- Bannister K, 2016, CURR OPIN SUPPORT PA, V10, P143, DOI 10.1097/SPC.0000000000000207
- Barneoud P, 2000, EUR J NEUROSCI, V12, P322, DOI 10.1046/j.1460-9568.2000.00896.x
- BASBAUM AI, 1984, ANNU REV NEUROSCI, V7, P309, DOI 10.1146/annurev.ne.07.030184.001521
- Beiske AG, 2009, PAIN, V141, P173, DOI 10.1016/j.pain.2008.12.004
- Bianchi L, 2003, EUR J NEUROSCI, V18, P856, DOI 10.1046/j.1460-9568.2003.02795.x
- Blanchet PJ, 2018, PROG NEURO-PSYCHOPH, V87, P200, DOI 10.1016/j.pnpbp.2017.10.010
- Blandini Fabio, 2008, Parkinsonism Relat Disord, V14 Suppl 2, pS124, DOI 10.1016/j.parkreldis.2008.04.015
- Blaszczyk JW, 2016, FRONT NEUROSCI-SWITZ, V10, DOI 10.3389/fnins.2016.00269
- Brefel-Courbon C, 2005, MOVEMENT DISORD, V20, P1557, DOI 10.1002/mds.20629
- Broadhurst P. L., 1960, HDB ABNORMAL PSYCHOL, P726
- Budai D, 1998, J NEUROPHYSIOL, V79, P677
- Cao LF, 2016, NEURAL PLAST, DOI 10.1155/2016/6383240
- Carta M, 2007, BRAIN, V130, P1819, DOI 10.1093/brain/awm082
- CHAPLAN SR, 1994, J NEUROSCI METH, V53, P55, DOI 10.1016/0165-0270(94)90144-9
- Charles KA, 2018, MOVEMENT DISORD, V33, P1010, DOI 10.1002/mds.27377
- Chaudhuri KR, 2009, LANCET NEUROL, V8, P464, DOI 10.1016/S1474-4422(09)70068-7
- Chen CCV, 2013, NEUROBIOL DIS, V49, P99, DOI 10.1016/j.nbd.2012.07.020
- Chiou LC, 1999, J PHYSIOL-LONDON, V518, P551, DOI 10.1111/j.1469-7793.1999.0551p.x
- CHUDLER EH, 1995, PAIN, V60, P3, DOI 10.1016/0304-3959(94)00172-B
- Chudler EH, 2008, BRAIN RES, V1213, P41, DOI 10.1016/j.brainres.2008.03.053
- CODERRE TJ, 1993, PAIN, V52, P259, DOI 10.1016/0304-3959(93)90161-H
- D'amour FE, 1941, J PHARMACOL EXP THER, V72, P74
- Delaville C, 2011, FRONT SYST NEUROSCI, V5, DOI 10.3389/fnsys.2011.00031
- Dellapina E, 2011, MOVEMENT DISORD, V26, P153, DOI 10.1002/mds.23406
- Deumens R, 2002, EXP NEUROL, V175, P303, DOI 10.1006/exnr.2002.7891
- di Michele F, 2013, FRONT NEUROENDOCRIN, V34, P132, DOI 10.1016/j.yfrne.2013.03.001
- Dieb W, 2014, BRAIN BEHAV, V4, P368, DOI 10.1002/brb3.214
- DOLPHIN A, 1976, PHARMACOL BIOCHEM BE, V5, P431, DOI 10.1016/0091-3057(76)90107-6
- Factor SA, 2000, MOVEMENT DISORD, V15, P167, DOI 10.1002/1531-8257(200001)15:1<167::AID-MDS1029>3.0.CO;2-8
- FIELDS HL, 1991, ANNU REV NEUROSCI, V14, P219, DOI 10.1146/annurev.ne.14.030191.001251
- FLORAN B, 1988, EUR J PHARMACOL, V150, P277, DOI 10.1016/0014-2999(88)90008-8
- Flores JA, 2004, PAIN, V110, P205, DOI 10.1016/j.pain.2004.03.036
- Gee LE, 2016, EXP NEUROL, V283, P298, DOI 10.1016/j.expneurol.2016.06.031
- Gerdelat-Mas A, 2007, J NEUROL NEUROSUR PS, V78, P1140, DOI 10.1136/jnnp.2007.120212
- Goetz C G, 1986, Mov Disord, V1, P45, DOI 10.1002/mds.870010106
- Gonzalez-Hernandez T, 2000, J COMP NEUROL, V421, P107, DOI 10.1002/(SICI)1096-9861(20000522)421:1<107::AID-CNE7>3.0.CO;2-F
- Guo D, 2014, NEUROSCIENCE, V283, P95, DOI 10.1016/j.neuroscience.2014.09.032
- Hagelberg N, 2002, PAIN, V99, P273, DOI 10.1016/S0304-3959(02)00121-5
- Hahm ET, 2011, BMC NEUROSCI, V12, DOI 10.1186/1471-2202-12-41
- HARGREAVES K, 1988, PAIN, V32, P77, DOI 10.1016/0304-3959(88)90026-7
- Herdegen T, 1998, BRAIN RES REV, V28, P370, DOI 10.1016/S0165-0173(98)00018-6
- Hirsch EC, 2009, LANCET NEUROL, V8, P382, DOI 10.1016/S1474-4422(09)70062-6
- HOKFELT T, 1973, BRAIN RES, V60, P269, DOI 10.1016/0006-8993(73)90791-9
- Hornykiewicz O, 1987, Adv Neurol, V45, P19
- Jackson-Lewis Vernice, 2012, Parkinsonism Relat Disord, V18 Suppl 1, pS183, DOI 10.1016/S1353-8020(11)70057-8
- Jaskiw GE, 2004, PSYCHOPHARMACOLOGY, V171, P365, DOI 10.1007/s00213-003-1672-y
- JOHNSON RE, 1993, MED CARE, V31, P432, DOI 10.1097/00005650-199305000-00005
- Kalyuzhny AE, 1998, J COMP NEUROL, V392, P528
- Kaszuba BC, 2017, BRAIN RES, V1655, P233, DOI 10.1016/j.brainres.2016.10.025
- Kemp T, 1996, NEUROSCIENCE, V75, P1231, DOI 10.1016/0306-4522(96)00333-8
- Kim J. Y, 2014, J NEUROSCI, V22, P6307, DOI [10.1523/jneurosc.3481-14,2015, DOI 10.1523/JNEUROSC.3481-14.2015]
- Kirik D, 1998, EXP NEUROL, V152, P259, DOI 10.1006/exnr.1998.6848
- Lau BK, 2014, CURR OPIN NEUROBIOL, V29, P159, DOI 10.1016/j.conb.2014.07.010
- Magnusson JE, 2000, BRAIN RES, V855, P260, DOI 10.1016/S0006-8993(99)02396-3
- Marker CL, 2006, J NEUROSCI, V26, P12251, DOI 10.1523/JNEUROSCI.3693-06.2006
- MELZACK R, 1965, SCIENCE, V150, P971, DOI 10.1126/science.150.3699.971
- Millan MJ, 2002, PROG NEUROBIOL, V66, P355, DOI 10.1016/S0301-0082(02)00009-6
- Milligan ED, 2003, J NEUROSCI, V23, P1026
- MOLANDER C, 1984, J COMP NEUROL, V230, P133, DOI 10.1002/cne.902300112
- Nandhagopal R, 2010, PAIN MED, V11, P834, DOI 10.1111/j.1526-4637.2010.00866.x
- Nascimento GC, 2018, NEUROTOX RES, V34, P799, DOI 10.1007/s12640-018-9896-0
- Obese J. A, 2000, NEUROLOGY, V55
- Obeso JA, 2004, NEUROLOGY, V62, pS17, DOI 10.1212/WNL.62.1_suppl_1.S17
- Obeso JA, 2000, NEUROLOGY, V55, pS13
- Ossipov MH, 2010, J CLIN INVEST, V120, P3779, DOI 10.1172/JCI43766
- Pagano RL, 2012, PAIN, V153, P2359, DOI 10.1016/j.pain.2012.08.002
- Paxinos G., 2005, RAT BRAIN STEREOTAXI
- Pertovaara A, 2006, PROG NEUROBIOL, V80, P53, DOI 10.1016/j.pneurobio.2006.08.001
- Pertovaara A, 2006, HAND CLINIC, V81, P179, DOI 10.1016/S0072-9752(06)80017-5
- Polgar E, 2003, PAIN, V104, P229, DOI 10.1016/S0304-3959(03)00011-3
- PRZEDBORSKI S, 1995, NEUROSCIENCE, V67, P631, DOI 10.1016/0306-4522(95)00066-R
- Quittenbam BH, 2004, PARKINSONISM RELAT D, V10, P129, DOI 10.1016/j.parkreldis.2003.12.001
- Rana AQ, 2013, CLIN NEUROL NEUROSUR, V115, P2313, DOI 10.1016/j.clineuro.2013.08.022
- RANDALL LO, 1957, ARCH INT PHARMACOD T, V111, P409
- Rangel-Barajas C, 2008, NEUROPHARMACOLOGY, V55, P704, DOI 10.1016/j.neuropharm.2008.06.002
- RAYNOR K, 1994, MOL PHARMACOL, V45, P330
- RUDA MA, 1986, PROG BRAIN RES, V66, P219, DOI 10.1016/S0079-6123(08)64606-3
- Saade NE, 1997, BRAIN RES, V751, P1, DOI 10.1016/S0006-8993(96)01164-X
- SANBERG PR, 1980, NATURE, V284, P472, DOI 10.1038/284472a0
- SCATTON B, 1983, BRAIN RES, V275, P321, DOI 10.1016/0006-8993(83)90993-9
- Sgroi S, 2018, FRONT NEUROL, V9, DOI 10.3389/fneur.2018.00524
- Somers DL, 2002, NEUROSCI LETT, V323, P171, DOI 10.1016/S0304-3940(02)00157-X
- Stefano GB, 2012, MED SCI MONITOR, V18, pRA133, DOI 10.12659/MSM.883259
- Takeda R, 2014, NEUROSCI LETT, V573, P19, DOI 10.1016/j.neulet.2014.05.007
- Taniguchi W, 2011, PAIN, V152, P95, DOI 10.1016/j.pain.2010.09.034
- Tassorelli C, 2007, BRAIN RES, V1176, P53, DOI 10.1016/j.brainres.2007.08.012
- Taylor AMW, 2016, PAIN, V157, P1194, DOI 10.1097/j.pain.0000000000000494
- Todd AJ, 2010, NAT REV NEUROSCI, V11, P823, DOI 10.1038/nrn2947
- Tracey I, 2007, NEURON, V55, P377, DOI 10.1016/j.neuron.2007.07.012
- Vallone D, 2000, NEUROSCI BIOBEHAV R, V24, P125, DOI 10.1016/S0149-7634(99)00063-9
- Vanegas H, 2004, BRAIN RES REV, V46, P295, DOI 10.1016/j.brainresrev.2004.07
- Visser M, 2009, VALUE HEALTH, V12, P392, DOI 10.1111/j.1524-4733.2008.00430.x
- Wang B, 2018, FRONT MOL NEUROSCI, V11, DOI 10.3389/fnmol.2018.00120
- Wang CT, 2017, MOL PAIN, V13, DOI 10.1177/1744806917691525
- Wang Y, 2010, BRAIN RES, V1324, P54, DOI 10.1016/j.brainres.2010.02.008
- Wood Patrick B, 2008, Expert Rev Neurother, V8, P781, DOI 10.1586/14737175.8.5.781
- Zengin-Toktas Y, 2013, NEUROSCI RES, V76, P261, DOI 10.1016/j.neures.2013.05.003
- Zhang X, 2008, P NATL ACAD SCI USA, V105, P2163, DOI 10.1073/pnas.0711839105
- ZIGMOND MJ, 1984, ARCH NEUROL-CHICAGO, V41, P856, DOI 10.1001/archneur.1984.04050190062015
- ZIMMERMANN M, 1983, PAIN, V16, P109, DOI 10.1016/0304-3959(83)90201-4