Effect of Subthalamic Stimulation and Electrode Implantation in the Striatal Microenvironment in a Parkinson's Disease Rat Model
Carregando...
Citações na Scopus
5
Tipo de produção
article
Data de publicação
2022
Título da Revista
ISSN da Revista
Título do Volume
Editora
MDPI
Autores
CAMPOS, Ana Carolina Pinheiro
AUADA, Aline Vivian Vatti
LEBRUN, Ivo
HAMANI, Clement
PAGANO, Rosana Lima
Citação
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, v.23, n.20, article ID 12116, 17p, 2022
Resumo
Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is considered the gold-standard treatment for PD; however, underlying therapeutic mechanisms need to be comprehensively elucidated, especially in relation to glial cells. We aimed to understand the effects of STN-microlesions and STN-DBS on striatal glial cells, inflammation, and extracellular glutamate/GABAergic concentration in a 6-hydroxydopamine (6-OHDA)-induced PD rat model. Rats with unilateral striatal 6-OHDA and electrodes implanted in the STN were divided into two groups: DBS OFF and DBS ON (5 days/2 h/day). Saline and 6-OHDA animals were used as control. Akinesia, striatal reactivity for astrocytes, microglia, and inflammasome, and expression of cytokines, cell signaling, and excitatory amino acid transporter (EAAT)-2 were examined. Moreover, striatal microdialysis was performed to evaluate glutamate and GABA concentrations. The PD rat model exhibited akinesia, increased inflammation, glutamate release, and decreased glutamatergic clearance in the striatum. STN-DBS (DBS ON) completely abolished akinesia. Both STN-microlesion and STN-DBS decreased striatal cytokine expression and the relative concentration of extracellular glutamate. However, STN-DBS inhibited morphological changes in astrocytes, decreased inflammasome reactivity, and increased EAAT2 expression in the striatum. Collectively, these findings suggest that the beneficial effects of DBS are mediated by a combination of stimulation and local microlesions, both involving the inhibition of glial cell activation, neuroinflammation, and glutamate excitotoxicity.
Palavras-chave
Parkinson's disease, deep brain stimulation, subthalamic stimulation, neuroinflammation, astrocytes, glutamate excitotoxicity
Referências
- Akwa Y, 2022, AUTOPHAGY, DOI 10.1080/15548627.2022.2095791
- Alvarez L, 2005, BRAIN, V128, P570, DOI 10.1093/brain/awh397
- Ambrosi G, 2014, J NEURAL TRANSM, V121, P849, DOI 10.1007/s00702-013-1149-z
- Amorim BO, 2015, J NEUROINFLAMM, V12, DOI 10.1186/s12974-015-0384-7
- Anderson CM, 2000, GLIA, V32, P1
- Araque A, 1999, TRENDS NEUROSCI, V22, P208, DOI 10.1016/S0166-2236(98)01349-6
- Bartels AL, 2010, PARKINSONISM RELAT D, V16, P57, DOI 10.1016/j.parkreldis.2009.05.005
- BENABID AL, 1994, STEREOT FUNCT NEUROS, V62, P76, DOI 10.1159/000098600
- Benabid AL, 2003, CURR OPIN NEUROBIOL, V13, P696, DOI 10.1016/j.conb.2003.11.001
- Benabid AL, 2009, LANCET NEUROL, V8, P67, DOI 10.1016/S1474-4422(08)70291-6
- BENAZZOUZ A, 1995, NEUROSCI LETT, V189, P77, DOI 10.1016/0304-3940(95)11455-6
- Bezard E, 2001, NAT REV NEUROSCI, V2, P577, DOI 10.1038/35086062
- Centonze D, 2005, NEUROSCIENCE, V133, P831, DOI 10.1016/j.neuroscience.2005.03.006
- Charan J, 2013, J PHARMACOL PHARMACO, V4, P303, DOI 10.4103/0976-500X.119726
- Chen YM, 2001, J NEUROCHEM, V77, P1601, DOI 10.1046/j.1471-4159.2001.00374.x
- Chudler EH, 2008, BRAIN RES, V1213, P41, DOI 10.1016/j.brainres.2008.03.053
- Chung EKY, 2008, J COMP NEUROL, V511, P421, DOI 10.1002/cne.21852
- Ferrari CC, 2006, NEUROBIOL DIS, V24, P183, DOI 10.1016/j.nbd.2006.06.013
- Dafsari HS, 2016, BRAIN STIMUL, V9, P78, DOI 10.1016/j.brs.2015.08.005
- de Andrade EM, 2020, J NEUROSURG, V132, P239, DOI 10.3171/2018.7.JNS173239
- Domenici RA, 2019, EXP NEUROL, V315, P72, DOI 10.1016/j.expneurol.2019.02.007
- Dvorzhak A, 2013, PLOS ONE, V8, DOI 10.1371/journal.pone.0082191
- Elias WJ, 2016, NEW ENGL J MED, V375, P730, DOI 10.1056/NEJMoa1600159
- Escartin C, 2021, NAT NEUROSCI, V24, P312, DOI 10.1038/s41593-020-00783-4
- Eulenburg V, 2010, BRAIN RES REV, V63, P103, DOI 10.1016/j.brainresrev.2010.01.003
- Fahn S, 1999, ARCH NEUROL-CHICAGO, V56, P529, DOI 10.1001/archneur.56.5.529
- Fenoy AJ, 2014, CNS NEUROSCI THER, V20, P191, DOI 10.1111/cns.12223
- Freeman L, 2017, J EXP MED, V214, P1351, DOI 10.1084/jem.20150237
- Gerhard A, 2006, NEUROBIOL DIS, V21, P404, DOI 10.1016/j.nbd.2005.08.002
- Hamani C, 2017, ENEURO, V4, DOI 10.1523/ENEURO.0140-17.2017
- Hardingham GE, 2010, NAT REV NEUROSCI, V11, P682, DOI 10.1038/nrn2911
- Herrington TM, 2016, J NEUROPHYSIOL, V115, P19, DOI 10.1152/jn.00281.2015
- Higuchi Y, 2017, MOVEMENT DISORD, V32, P28, DOI 10.1002/mds.26625
- Hirsch EC, 2009, LANCET NEUROL, V8, P382, DOI 10.1016/S1474-4422(09)70062-6
- Holiga S, 2015, NEUROIMAGE-CLIN, V9, P264, DOI 10.1016/j.nicl.2015.08.008
- Hornykiewicz O, 1987, Adv Neurol, V45, P19
- Iovino L, 2020, J PHARMACOL SCI, V144, P151, DOI 10.1016/j.jphs.2020.07.011
- Jech R, 2012, PLOS ONE, V7, DOI 10.1371/journal.pone.0049056
- Juri C, 2010, J NEUROL SCI, V289, P60, DOI 10.1016/j.jns.2009.08.018
- Kim KI, 2021, GLIA, V69, P2133, DOI 10.1002/glia.24013
- Kimelberg HK, 2010, NEUROTHERAPEUTICS, V7, P338, DOI 10.1016/j.nurt.2010.07.006
- Kofler J, 2011, TOXICOL PATHOL, V39, P103, DOI 10.1177/0192623310387619
- Krack P, 2003, NEW ENGL J MED, V349, P1925, DOI 10.1056/NEJMoa035275
- Kumar R, 1998, NEUROLOGY, V51, P850, DOI 10.1212/WNL.51.3.850
- Lee KJ, 2017, J KOREAN NEUROSURG S, V60, P138, DOI 10.3340/jkns.2016.0202.020
- Lehre KP, 1998, J NEUROSCI, V18, P8751, DOI 10.1523/jneurosci.18-21-08751.1998
- Liddelow SA, 2017, NATURE, V541, P481, DOI 10.1038/nature21029
- Luo B, 2021, FRONT NEUROSCI-SWITZ, V15, DOI 10.3389/fnins.2021.699010
- Mallet N, 2006, J NEUROSCI, V26, P3875, DOI 10.1523/JNEUROSCI.4439-05.2006
- Martinez RCR, 2013, MOVEMENT DISORD, V28, P2027, DOI 10.1002/mds.25691
- Mccoy MK, 2006, J NEUROSCI, V26, P9365, DOI 10.1523/JNEUROSCI.1504-06.2006
- McGeer P.L., 2001, ADV NEUROL, V86
- McGeer PL, 2008, MOVEMENT DISORD, V23, P474, DOI 10.1002/mds.21751
- MCGEER PL, 1988, NEUROLOGY, V38, P1285, DOI 10.1212/WNL.38.8.1285
- Meshul CK, 1999, NEUROSCIENCE, V88, P1, DOI 10.1016/S0306-4522(98)00189-4
- Newman EA, 2003, TRENDS NEUROSCI, V26, P536, DOI 10.1016/S0166-2236(03)00237-6
- Obeso JA, 2000, TRENDS NEUROSCI, V23, pS8, DOI 10.1016/S1471-1931(00)00028-8
- Parsons MP, 2014, NEURON, V82, P279, DOI 10.1016/j.neuron.2014.03.030
- Paxinos G, 1998, RAT BRAIN IN STEREOTAXIC COORDINATES, FOURTH ED., pix
- Pekny M, 2005, GLIA, V50, P427, DOI 10.1002/glia.20207
- Pelvig DP, 2008, NEUROBIOL AGING, V29, P1754, DOI 10.1016/j.neurobiolaging.2007.04.013
- Pereira JLB, 2016, BASAL GANGLIA, V6, P83, DOI 10.1016/j.baga.2016.01.003
- Campos ACP, 2020, CELL MOL NEUROBIOL, V40, P939, DOI 10.1007/s10571-019-00784-3
- Campos ACP, 2019, EXP NEUROL, V318, P12, DOI 10.1016/j.expneurol.2019.04.015
- Rascol O, 2000, NEW ENGL J MED, V342, P1484, DOI 10.1056/NEJM200005183422004
- Robinson S, 2003, EXP NEUROL, V180, P73, DOI 10.1016/S0014-4886(02)00050-X
- Rose CR, 2018, BRAIN RES BULL, V136, P3, DOI 10.1016/j.brainresbull.2016.12.013
- Rothstein JD, 1996, NEURON, V16, P675, DOI 10.1016/S0896-6273(00)80086-0
- Saijo K, 2009, CELL, V137, P47, DOI 10.1016/j.cell.2009.01.038
- SANBERG PR, 1980, NATURE, V284, P472, DOI 10.1038/284472a0
- Sood A, 2021, J NEUROSCI RES, V99, P3148, DOI 10.1002/jnr.24977
- Tawfik VL, 2010, NEUROSURGERY, V67, P367, DOI 10.1227/01.NEU.0000371988.73620.4C
- Tritsch NX, 2012, NATURE, V490, P262, DOI 10.1038/nature11466
- Ventura R, 1999, J NEUROSCI, V19, P6897, DOI 10.1523/JNEUROSCI.19-16-06897.1999
- Wei L, 2019, NEURAL PLAST, V2019, DOI 10.1155/2019/1247276
- Weintraub D, 2017, MOVEMENT DISORD, V32, P20, DOI 10.1002/mds.26599
- Yang H, 2006, LIFE SCI, V78, P1940, DOI 10.1016/j.lfs.2005.08.001
- Zhang W, 2005, FASEB J, V19, P533, DOI 10.1096/fj.04-2751com