Systemic and Peripheral Mechanisms of Cortical Stimulation-Induced Analgesia and Refractoriness in a Rat Model of Neuropathic Pain

Imagem de Miniatura
Arquivos
art_ASSIS_Systemic_and_Peripheral_Mechanisms_of_Cortical_StimulationInduced_Analgesia_2023.PDF (2.07 MB)
Citações na Scopus
2
Tipo de produção
article
Data de publicação
2023
DOI
Scopus
Web of Science
PubMed
Título da Revista
ISSN da Revista
Título do Volume
Editora
MDPI
Autores
ASSIS, Danielle V.
CAMPOS, Ana Carolina P.
PASCHOA, Amanda F. N.
SANTOS, Talita F.
PAGANO, Rosana L.
Citação
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, v.24, n.9, article ID 7796, 18p, 2023
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Epidural motor cortex stimulation (MCS) is an effective treatment for refractory neuropathic pain; however, some individuals are unresponsive. In this study, we correlated the effectiveness of MCS and refractoriness with the expression of cytokines, neurotrophins, and nociceptive mediators in the dorsal root ganglion (DRG), sciatic nerve, and plasma of rats with sciatic neuropathy. MCS inhibited hyperalgesia and allodynia in two-thirds of the animals (responsive group), and one-third did not respond (refractory group). Chronic constriction injury (CCI) increased IL-1 fi in the nerve and DRG, inhibited IL-4, IL-10, and IL-17A in the nerve, decreased beta-endorphin, and enhanced substance P in the plasma, compared to the control. Responsive animals showed decreased NGF and increased IL-6 in the nerve, accompanied by restoration of local IL-10 and IL-17A and systemic beta-endorphin. Refractory animals showed increased TNF- alpha and decreased IFN gamma in the nerve, along with decreased TNF- alpha and IL-17A in the DRG, maintaining low levels of systemic beta-endorphin. Our findings suggest that the effectiveness of MCS depends on local control of inflammatory and neurotrophic changes, accompanied by recovery of the opioidergic system observed in neuropathic conditions. So, understanding the refractoriness to MCS may guide an improvement in the efficacy of the technique, thus benefiting patients with persistent neuropathic pain.
Palavras-chave
motor cortex stimulation, neuropathic pain, sciatic nerve, inflammation, neurotrophins, substance P, beta-endorphin
URI
https://observatorio.fm.usp.br/handle/OPI/54723
Referências
  1. Afif Afif, 2022, J Neurosurg Sci, V66, P560, DOI 10.23736/S0390-5616.20.04991-7
  2. Ahmed MA, 2011, NEUROL RES, V33, P953, DOI 10.1179/1743132811Y.0000000045
  3. Ahmed S, 2008, P NATL ACAD SCI USA, V105, P14692, DOI 10.1073/pnas.0802675105
  4. Austin PJ, 2015, J NEUROINFLAMM, V12, DOI 10.1186/s12974-015-0318-4
  5. Austin PJ, 2013, NEUROPATHIC PAIN: CAUSES, MANAGEMENT, AND UNDERSTANDING, P77
  6. Bach FW, 1997, DAN MED BULL, V44, P274
  7. Bannwarth B, 2014, DRUGS, V74, P619, DOI 10.1007/s40265-014-0208-6
  8. Barker PA, 2020, J PAIN RES, V13, P1223, DOI 10.2147/JPR.S247472
  9. BENNETT GJ, 1988, PAIN, V33, P87, DOI 10.1016/0304-3959(88)90209-6
  10. Boadas-Vaello P, 2016, SPINAL CORD, V54, P330, DOI 10.1038/sc.2015.225
  11. Bobinski F, 2018, PAIN, V159, P437, DOI 10.1097/j.pain.0000000000001109
  12. Liu FY, 2012, BRAIN RES, V1427, P65, DOI 10.1016/j.brainres.2011.10.016
  13. Mannion RJ, 2000, CLIN J PAIN, V16, pS144
  14. Mantyh PW, 2011, ANESTHESIOLOGY, V115, P189, DOI 10.1097/ALN.0b013e31821b1ac5
  15. Martin SL, 2019, NEURAL REGEN RES, V14, P939, DOI 10.4103/1673-5374.250566
  16. Martucci C, 2008, PAIN, V137, P81, DOI 10.1016/j.pain.2007.08.017
  17. McKelvey L, 2013, J NEUROCHEM, V124, P276, DOI 10.1111/jnc.12093
  18. Millan MJ, 1999, PROG NEUROBIOL, V57, P1, DOI 10.1016/S0301-0082(98)00048-3
  19. Milligan ED, 2009, NAT REV NEUROSCI, V10, P23, DOI 10.1038/nrn2533
  20. Mueller M, 2001, AM J PATHOL, V159, P2187, DOI 10.1016/S0002-9440(10)63070-2
  21. Murray PJ, 2006, CURR OPIN PHARMACOL, V6, P379, DOI 10.1016/j.coph.2006.01.010
  22. Pagano RL, 2011, EUR J PAIN, V15, DOI 10.1016/j.ejpain.2010.08.003
  23. Narita M, 1998, JPN J PHARMACOL, V76, P233, DOI 10.1254/jjp.76.233
  24. Nguyen JP, 2008, BRAIN STIMUL, V1, P89, DOI 10.1016/j.brs.2008.03.007
  25. Nicolas N, 2018, WORLD NEUROSURG, V114, pE800, DOI 10.1016/j.wneu.2018.03.090
  26. Pagano RL, 2012, PAIN, V153, P2359, DOI 10.1016/j.pain.2012.08.002
  27. Palmer MT, 2010, NAT IMMUNOL, V11, P36, DOI 10.1038/ni.1802
  28. Pannell M, 2016, J NEUROINFLAMM, V13, DOI 10.1186/s12974-016-0735-z
  29. Pathak NN, 2013, INFLAMMATION, V36, P1468, DOI 10.1007/s10753-013-9688-x
  30. Perkins NM, 2000, NEUROSCIENCE, V101, P745, DOI 10.1016/S0306-4522(00)00396-1
  31. Petraschka M, 2007, NEUROSCIENCE, V146, P1795, DOI 10.1016/j.neuroscience.2007.03.029
  32. Peyron R, 2007, NEUROIMAGE, V34, P310, DOI 10.1016/j.neuroimage.2006.08.037
  33. RANDALL LO, 1957, ARCH INT PHARMACOD T, V111, P409
  34. Sacerdote P, 2008, NEUROSCI LETT, V436, P210, DOI 10.1016/j.neulet.2008.03.023
  35. Sacerdote P, 2013, J NEUROIMMUNE PHARM, V8, P202, DOI 10.1007/s11481-012-9428-2
  36. Silva GD, 2015, J NEUROINFLAMM, V12, DOI 10.1186/s12974-014-0216-1
  37. Saitoh Y, 2007, ACTA NEUROCHIR SUPPL, V97, P51
  38. Santos FM, 2018, BRAIN RES, V1687, P60, DOI 10.1016/j.brainres.2018.02.034
  39. Schnitzler A, 2000, J CLIN NEUROPHYSIOL, V17, P592, DOI 10.1097/00004691-200011000-00005
  40. Shubayev VI, 2001, J NEUROIMMUNOL, V114, P48, DOI 10.1016/S0165-5728(00)00453-7
  41. Slotty PJ, 2015, STEREOT FUNCT NEUROS, V93, P199, DOI 10.1159/000375177
  42. Stoll G, 2002, J PERIPHER NERV SYST, V7, P13, DOI 10.1046/j.1529-8027.2002.02002.x
  43. Sun J, 2008, AM J PHYSIOL-CELL PH, V294, pC1586, DOI 10.1152/ajpcell.00129.2008
  44. Torrance N, 2013, PAIN, V154, P690, DOI 10.1016/j.pain.2012.12.022
  45. Treede RD, 2008, NEUROLOGY, V70, P1630, DOI 10.1212/01.wnl.0000282763.29778.59
  46. Vaculin S, 2008, EXP BRAIN RES, V185, P331, DOI 10.1007/s00221-007-1158-y
  47. van Hecke O, 2014, PAIN, V155, P654, DOI 10.1016/j.pain.2013.11.013
  48. Velasco F, 2008, J NEUROSURG, V108, P698, DOI 10.3171/JNS/2008/108/4/0698
  49. Viisanen H, 2012, BRAIN RES BULL, V89, P133, DOI 10.1016/j.brainresbull.2012.08.002
  50. Watkins LR, 1999, ADV EXP MED BIOL, V461, P153
  51. Viisanen H, 2010, NEUROSCI LETT, V476, P133, DOI 10.1016/j.neulet.2010.04.014
  52. Volkers R, 2020, NEUROMODULATION, V23, P436, DOI 10.1111/ner.13119
  53. Wang H, 2014, NEUROLOGY, V83, P628, DOI 10.1212/WNL.0000000000000686
  54. Wang JA, 2020, CHINESE MED J-PEKING, V133, P190, DOI 10.1097/CM9.0000000000000619
  55. Weaver CT, 2007, ANNU REV IMMUNOL, V25, P821, DOI 10.1146/annurev.immunol.25.022106.141557
  56. Whitehead KJ, 2010, BRAIN BEHAV IMMUN, V24, P569, DOI 10.1016/j.bbi.2009.12.007
  57. Woolf CJ, 2000, SCIENCE, V288, P1765, DOI 10.1126/science.288.5472.1765
  58. Wu G, 2002, J NEUROSCI, V22, P7746
  59. Wu HY, 2018, BRAIN BEHAV IMMUN, V73, P504, DOI 10.1016/j.bbi.2018.06.015
  60. Xing Z, 1998, J CLIN INVEST, V101, P311, DOI 10.1172/JCI1368
  61. Yamada K, 2003, J PHARMACOL SCI, V91, P267
  62. Zhang RR, 2020, MILITARY MED RES, V7, DOI 10.1186/s40779-020-00286-0
  63. Zhang Y, 2018, INFLAMMATION, V41, P569, DOI 10.1007/s10753-017-0713-3
  64. Campana WM, 2007, BRAIN BEHAV IMMUN, V21, P522, DOI 10.1016/j.bbi.2006.12.008
  65. Zhang ZJ, 2017, CELL MOL LIFE SCI, V74, P3275, DOI 10.1007/s00018-017-2513-1
  66. Zhi MJ, 2017, J PAIN RES, V10, DOI 10.2147/JPR.S139324
  67. ZIMMERMANN M, 1983, PAIN, V16, P109, DOI 10.1016/0304-3959(83)90201-4
  68. Zizzo G, 2013, J IMMUNOL, V190, P5237, DOI 10.4049/jimmunol.1203017
  69. CHAPLAN SR, 1994, J NEUROSCI METH, V53, P55, DOI 10.1016/0165-0270(94)90144-9
  70. Charan J, 2013, J PHARMACOL PHARMACO, V4, P303, DOI 10.4103/0976-500X.119726
  71. Cioato Stefania Giotti, 2021, BrJP, V4, P99, DOI 10.5935/2595-0118.20210031
  72. Cohen SP, 2014, BMJ-BRIT MED J, V348, DOI 10.1136/bmj.f7656
  73. Colloca L, 2017, NAT REV DIS PRIMERS, V3, DOI 10.1038/nrdp.2017.2
  74. Cruccu G, 2007, EUR J NEUROL, V14, P952, DOI 10.1111/j.1468-1331.2007.01916.x
  75. Dailey AT, 1998, J NEUROSCI, V18, P6713
  76. Day YJ, 2014, PAIN, V155, P1293, DOI 10.1016/j.pain.2014.04.004
  77. de Andrade EM, 2020, J NEUROSURG, V132, P239, DOI 10.3171/2018.7.JNS173239
  78. Delavallee M, 2014, ACTA NEUROCHIR, V156, P2289, DOI 10.1007/s00701-014-2240-4
  79. Dubovy P, 2010, NEURON GLIA BIOL, V6, P73, DOI 10.1017/S1740925X10000074
  80. El Kasmi KC, 2006, J IMMUNOL, V177, P7880, DOI 10.4049/jimmunol.177.11.7880
  81. Fagundes-Pereyra WJ, 2010, ARQ NEURO-PSIQUIAT, V68, P923, DOI 10.1590/S0004-282X2010000600018
  82. Fonoff ET, 2009, BEHAV BRAIN RES, V202, P138, DOI 10.1016/j.bbr.2009.03.018
  83. Fonoff ET, 2009, BEHAV BRAIN RES, V196, P63, DOI 10.1016/j.bbr.2008.07.027
  84. Fontaine D, 2009, J NEUROSURG, V110, P251, DOI 10.3171/2008.6.17602
  85. Gao YJ, 2003, BRAIN RES BULL, V61, P587, DOI 10.1016/S0361-9230(03)00215-6
  86. Gao YJ, 2010, NEUROTHERAPEUTICS, V7, P482, DOI 10.1016/j.nurt.2010.05.016
  87. Garcia-Larrea L, 1999, PAIN, V83, P259, DOI 10.1016/S0304-3959(99)00114-1
  88. Garcia-Larrea L, 2007, NEUROIMAGE, V37, pS71, DOI 10.1016/j.neuroimage.2007.05.062
  89. Girach A, 2019, PAIN RES MANAG, V2019, DOI 10.1155/2019/2091960
  90. Grace PM, 2014, NAT REV IMMUNOL, V14, P217, DOI 10.1038/nri3621
  91. Guerios SD, 2008, AM J PHYSIOL-REG I, V295, pR111, DOI 10.1152/ajpregu.00728.2007
  92. Guo CJ, 2002, J NEUROIMMUNOL, V131, P160, DOI 10.1016/S0165-5728(02)00277-1
  93. Hamani C, 2021, BRAIN, V144, P2994, DOI 10.1093/brain/awab189
  94. Hanani M, 2005, BRAIN RES REV, V48, P457, DOI 10.1016/j.brainresrev.2004.09.001
  95. Hansson PT, 2009, EUR J PAIN, V13, P439, DOI 10.1016/j.ejpain.2009.02.008
  96. Hartwig A C, 1991, Anesth Prog, V38, P75
  97. Hegazy N, 2020, BASIC CLIN PHARMACOL, V127, P451, DOI 10.1111/bcpt.13453
  98. Henssen D, 2020, SCI REP-UK, V10, DOI 10.1038/s41598-020-64177-z
  99. Holzer P, 1997, PHARMACOL THERAPEUT, V73, P219, DOI 10.1016/S0163-7258(96)00196-9
  100. Huang EJ, 2001, ANNU REV NEUROSCI, V24, P677, DOI 10.1146/annurev.neuro.24.1.677
  101. Ji RR, 2002, NEURON, V36, P57, DOI 10.1016/S0896-6273(02)00908-X
  102. Julius D, 2001, NATURE, V413, P203, DOI 10.1038/35093019
  103. Katz N, 2011, PAIN, V152, P2248, DOI 10.1016/j.pain.2011.05.003
  104. Kemper C, 2007, NAT REV IMMUNOL, V7, P9, DOI 10.1038/nri1994
  105. Khan J, 2015, NEUROSCI LETT, V592, P99, DOI 10.1016/j.neulet.2015.03.001
  106. Kilkenny C, 2010, J GENE MED, V12, P561, DOI [10.1002/jgm.1473, 10.1111/j.1476-5381.2010.00872.x, 10.1113/jphysiol.2010.192278]
  107. Kim CF, 2011, J PAIN, V12, P370, DOI 10.1016/j.jpain.2010.08.003
  108. Kim J, 2016, J NEUROSURG, V124, P866, DOI 10.3171/2015.1.JNS14891
  109. Kleinschnitz C, 2006, EXP NEUROL, V200, P480, DOI 10.1016/j.expneurol.2006.03.014
  110. La Rana G, 2008, NEUROPHARMACOLOGY, V54, P521, DOI 10.1016/j.neuropharm.2007.10.021
  111. Labuz D, 2010, BRAIN BEHAV IMMUN, V24, P1045, DOI 10.1016/j.bbi.2010.04.001
  112. Lefaucheur JP, 2009, BRAIN, V132, P1463, DOI 10.1093/brain/awp035
  113. Lima MC, 2008, NEUROLOGY, V70, P2329, DOI 10.1212/01.wnl.0000314649.38527.93
  114. Lindborg JA, 2018, J NEUROINFLAMM, V15, DOI 10.1186/s12974-018-1222-5

Coleções
Artigos e Materiais de Revistas Científicas - FM/MNE
Artigos e Materiais de Revistas Científicas - HC/ICHC
Artigos e Materiais de Revistas Científicas - LIM/45