Mechanisms of occurrence and chronicity of neuropathic pain in multiple sclerosis in clinical and experimental conditions

4 лютого 2022
1135
Спеціальності :
Резюме

Multiple sclerosis (MS) is a multifaceted, complex chronic neurological disease that leads to motor, sensory and cognitive impairment. The symptoms of MS are unpredictable and extremely variable. Pain is a frequent symptom of MS and is manifested by nociceptive or neuropathic pain (NP), even in the early stages of the disease. MS is one of the most debilitating symptoms that reduces the quality of life and interferes with daily activities, especially because conventional pharmacotherapeutic drugs do not adequately alleviate NP. Despite the achievements, the mechanisms underlying NP in MS remain unclear. Most studies examining the pathophysiology of NP associated with MS have been performed on experimental animal models that reproduce some of the clinical and neuropathological features of MS. Experimental allergic encephalomyelitis (EAE) is one of the most studied and most frequently used experimental models of MS. As in patients with MS, rodents affected by EAE have an increased sensitivity to pain, which can be assessed using well-proven tests. EAE studies have provided valuable information on the pathophysiology of NP. However, further research is needed to better understand the events that lead to and maintain NP in order to identify targets that may contribute to the development of more effective therapeutic interventions. The aim of this article is to review several mechanisms associated with NP in MS and EAE by summarizing published literature data.

References

  • 1. Simkins T.J., Duncan G.J., Bourdette D. (2021) Chronic demyelination and axonal degeneration in multiple sclerosis: pathogenesis and therapeutic implications. Curr. Neurol. Neurosci. Rep., 21: 26. DOI: 10.1007/s11910-021-01110-5
  • 2. Nefodov O., Dychko Ye., Zhytnii M., Chyrkin V. (2021) Experimental study of pharmacotherapy of neurological diseases for multiple sclerosis. Moderní věda, 5: 137–142.
  • 3. Wallin M.T., Culpepper W.J., Campbell J.D. et al. (2019) The prevalence of MS in the United States: a population-based estimate using health claims data. Neurology, 92: e1029–e1040. DOI: 10.1212/WNL.0000000000007035
  • 4. Kingwell E., Marriott J.J., Jetté N. et al. (2013) Incidence and prevalence of multiple sclerosis in Europe: a systematic review. BMC Neurol., 13: 128. DOI: 10.1186/1471-2377-13-128
  • 5. Cree B.A.C., Arnold D.L., Chataway J. et al. (2021) Secondary progressive multiple sclerosis: new insights. Neurology, 97: 378–388.
  • 6. Kalia L.V., O’Connor P.W. (2005) Severity of chronic pain and its relationship to quality of life in multiple sclerosis. Mult. Scler., 11: 322–327. DOI: 10.1191/1352458505ms1168oa.
  • 7. Нефьодов О.О., М’ясоєд Ю.П., Соломенко М.В. та ін. (2021) Фармакологія антиноцицепції за умов експериментального еквіваленту розсіяного склерозу. Вісн. пробл. біол. мед., 3(161): 131–136.
  • 8. Marrie R.A., Reingold S., Cohen J. et al. (2015) The incidence and prevalence of psychiatric disorders in multiple sclerosis: a systematic review. Mult. Scler., 21: 305–317. DOI: 10.1177/1352458514564487.
  • 9. Solaro P.C., Brichetto L.G., Amato L.M. et al. (2004) The prevalence of pain in multiple sclerosis: a multicenter cross-sectional study. Neurology, 63: 919–921. DOI: 10.1212/01. WNL.0000137047. 85868.D6.
  • 10. Truini A., Barbanti P., Pozzilli C., Cruccu G. (2013) A mechanism-based classification of pain in multiple sclerosis. J Neurol., 260: 351–367. DOI: 10.1007/s00415-012-6579-2.
  • 11. Kister I., Caminero A.B., Herbert J., Lipton R.B. (2010) Tension-type headache and migraine in multiple sclerosis. Curr. Pain Headache Rep., 14: 441–448. DOI: 10.1007/s11916-010-0143-5.
  • 12. Massot C., Donze C., Guyot M.A., Leteneur S. (2021) Low back pain in patients with multiple sclerosis: a systematic review and the prevalence in a French multiple sclerosis population. Rev. Neurol., 177: 349–358. DOI: 10.1016/j.neurol.2020.07.018.
  • 13. Kassirer M. (2000) Multiple sclerosis and pain: a medical focus. Int. J. MS Care, 2: 40–47. DOI: 10.7224/1537-2073-2.3.40.
  • 14. Patti F., Nicoletti A., Pappalardo A. et al. (2012) Frequency and severity of headache is worsened by Interferon-β therapy in patients with multiple sclerosis. Acta Neurol. Scand., 125: 91–95. DOI: 10.1111/j.1600-0404.2011.01532.x.
  • 15. Browne T.J., Hughes D.I., Dayas C.V. et al. (2020) Projection neuron axon collaterals in the dorsal horn: placing a new player in spinal cord pain processing. Front. Physiol., 11: 560802. DOI: 10.3389/fphys.2020.560802.
  • 16. Dworsky-Fried Z., Faig C.A., Vogel H.A. et al. (2021) Central amygdala inflammation drives pain hypersensitivity and attenuates morphine analgesia in experimental autoimmune encephalomyelitis. Pain, 10.1097/j.pain.0000000000002307.
  • 17. Jiang Y.Y., Shao S., Zhang Y. et al. (2018) Neural pathways in medial septal cholinergic modulation of chronic pain: distinct contribution of the anterior cingulate cortex and ventral hippocampus. Pain, 159: 1550–1561. DOI: 10.1097/j.pain.0000000000001240.
  • 18. Нефьодов О.О., М’ясоєд Ю.П., Соломенко М.В. та ін. (2021) Експериментальне вивчення лікування нейропатичного болю за умов моделювання розсіяного склерозу. Вісн.пробл. біол. мед., 4(162): 141–148.
  • 19. Smith E.S.J. (2018) Advances in understanding nociception and neuropathic pain. J. Neurol., 265: 231–238. DOI: 10.1007/s00415-017-8641-6.
  • 20. Arendt-Nielsen L., Morlion B., Perrot S. et al. (2018) Assessment and manifestation of central sensitisation across different chronic pain conditions. Eur. J. Pain, 22: 216–241. DOI: 10.1002/ejp.1140.
  • 21. Sanzarello I., Merlini L., Rosa M.A. et al. (2016) Central sensitization in chronic low back pain: a narrative review. J. Back Musculoskelet. Rehabil., 29: 625–633. DOI: 10.3233/BMR-160685.
  • 22. Doolen S., Iannitti T., Donahue R.R. et al. (2018) Fingolimod reduces neuropathic pain behaviors in a mouse model of multiple sclerosis by a sphingosine-1 phosphate receptor 1-dependent inhibition of central sensitization in the dorsal horn. Pain, 159: 224–238. DOI: 10.1097/j.pain.0000000000001106.
  • 23. van den Broeke E.N. (2018) Central sensitization and pain hypersensitivity: some critical considerations. F1000Res., 7: 1325. DOI: 10.12688/f1000 research.15956.2
  • 24. Baron R., Hans G., Dickenson A.H. (2013) Peripheral input and its importance for central sensitization. Ann. Neurol., 74: 630–636. DOI: 10.1002/ana.24017.
  • 25. Tao Y.X. (2012) AMPA receptor trafficking in inflammation-induced dorsal horn central sensitization. Neurosci. Bull., 28: 111–120. DOI: 10.1007/s12264-012-1204-z.
  • 26. Latremoliere A., Woolf C.J. (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain, 10: 895–926. 10.1016/j.jpain.2009.06.012.
  • 27. Kawasaki Y., Zhang L., Cheng J.K., Ji R.R. (2008) Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci., 28: 5189–5194. DOI: 10.1523/JNEUROSCI.3338-07.2008.
  • 28. Tang J., Bair M., Descalzi G. (2021) Reactive astrocytes: critical players in the development of chronic pain. Front. Psychiatr., 12: 682056. DOI: 10.3389/fpsyt.2021.682056
  • 29. Zhuo M. (2017) Descending facilitation. Mol. Pain, 13: 1744806917699212. DOI: 10.1177/1744806917699212.
  • 30. Ossipov M.H., Morimura K., Porreca F. (2014) Descending pain modulation and chronification of pain. Curr. Opin. Support Palliat. Care, 8: 143–151. DOI: 10.1097/SPC.0000000000000055.
  • 31. Papadopoulou A., Naegelin Y., Weier K. et al. (2014) MRI characteristics of periaqueductal lesions in multiple sclerosis. Mult. Scler. Relat. Disord., 3: 542–551. DOI: 10.1016/j.msard.2014.01.001.
  • 32. François A., Low S.A., Sypek E.I. et al. (2017) A brainstem-spinal cord inhibitory circuit for mechanical pain modulation by GABA and enkephalins. Neuron, 93: 822–839. DOI: 10.1016/j.neuron.2017.01.008.
  • 33. Gautam M., Prasoon P., Kumar R. et al. (2016) Role of neurokinin type 1 receptor in nociception at the periphery and the spinal level in the rat. Spinal. Cord, 54: 172–182. DOI: 10.1038/sc.2015.206.
  • 34. Barker P.A., Mantyh P., Arendt-Nielsen L. et al. (2020) Nerve growth factor signaling and its contribution to pain. J. Pain Res., 13: 1223–1241. DOI: 10.2147/JPR.S247472.
  • 35. Iyengar S., Johnson K.W., Ossipov M.H., Aurora S.K. (2019) CGRP and the trigeminal system in migraine. Headache, 59: 659–681. DOI: 10.1111/head.13529.
  • 36. Salzer I., Ray S., Schicker K., Boehm S. (2019) Nociceptor signalling through ion channel regulation via GPCRs. Int. J. Mol. Sci., 20: 2488. DOI: 10.3390/ijms20102488.
  • 37. Schaible H.G., Ebersberger A., Natura G. (2011) Update on peripheral mechanisms of pain: beyond prostaglandins and cytokines. Arthritis Res. Ther., 13: 210. DOI: 10.1186/ar3305.
  • 38. Di Stefano G., Maarbjerg S., Truini A. (2019) Trigeminal neuralgia secondary to multiple sclerosis: from the clinical picture to the treatment options. J. Headache Pain, 20: 20. DOI: 10.1186/s10194-019-0969-0.
  • 39. Khare S., Seth D. (2015) Lhermitte’s sign: the current status. Ann. Indian Acad. Neurol., 18: 154–156. DOI: 10.4103/0972-2327.150622
  • 40. Al-Araji A.H, Oger J. (2005) Reappraisal of lhermitte’s sign in multiple sclerosis. Mult. Scler., 11: 398–402.
  • 41. Khan N., Smith M.T. (2014) Multiple sclerosis-induced neuropathic pain: pharmacological management and pathophysiological insights from rodent EAE models. Inflammopharmacol., 22: 1–22.
  • 42. Нефьодов О.О., М’ясоєд Ю.П., Соломенко М.В. та ін. (2021) Фармакологія антиноцицепції за умов експериментального еквіваленту розсіяного склерозу. Вісн. пробл. біол. мед., 3(161): 131–136.
  • 43. Solaro C., Messmer Uccelli M. (2010) Pharmacological management of pain in patients with multiple sclerosis. Drugs, 70: 1245–1254.
  • 44. Cristino L., Bisogno T., Di Marzo V. (2020) Cannabinoids and the expanded endocannabinoid system in neurological disorders. Nat. Rev. Neurol., 16: 9–29.
  • 45. Murphy K.L., Bethea J.R., Fischer R. (2017) Neuropathic pain in multiple sclerosis — current therapeutic intervention and future treatment perspectives. In: Zagon I.S., McLaughlin P.J. (Eds.) Multiple Sclerosis: Perspectives in Treatment and Pathogenesis. Brisbane, QLD, 141 p.
  • 46. Abboud H., Hill E., Siddiqui J. et al. (2017) Neuromodulation in multiple sclerosis. Mult. Scler., 23: 1663–1676.
  • 47. Knotkova H., Hamani C., Sivanesan E. et al. (2021) Neuromodulation for chronic pain. Lancet, 397: 2111–2124.
  • 48. Young J., Zoghi M., Khan F., Galea M.P. (2020) The effect of transcranial direct current stimulation on chronic neuropathic pain in patients with multiple sclerosis: randomized controlled trial. Pain Medicine, 21: 3451–3457. DOI: 10.1093/pm/pnaa128
  • 49. Klein J., Siepmann T., Schackert G. et al. (2020) Peripheral nerve field stimulation in medically refractory trigeminal neuralgia attributed to multiple sclerosis. J. Neurosurg., 134: 1244–1250.
  • 50. Нефьодов О.О., М’ясоєд Ю.П., Соломенко М.В. та ін. (2021) Ефективність моделювання експериментального алергічного енцефаломієліту як експериментальної моделі розсіяного склерозу. Укр. журн. мед. біол. спорту, 6(6): 57–65.
  • 51. Steinman L., Zamvil S.S. (2006) How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis. Ann. Neurol., 60: 12–21.
  • 52. Steinman L., Zamvil S.S. (2005) Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol., 26: 565–571.
  • 53. Constantinescu C.S., Farooqi N., O’Brien K., Gran B. (2011) Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis. Br. J. Pharmacol., 164: 1079–1106.
  • 54. Burrows D.J., McGown A., Jain S.A. et al. (2019) Animal models of multiple sclerosis: from rodents to zebrafish. Mult. Scler., 25: 306–324.
  • 55. Procaccini C., De Rosa V., Pucino V. et al. (2015) Animal models of Multiple Sclerosis. Eur. J. Pharmacol., 759: 182–191.
  • 56. Lebar R., Lubetzki C., Vincent C. et al. (1986) The M2 autoantigen of central nervous system myelin, a glycoprotein present in oligodendrocyte membrane. Clin. Exp. Immunol., 66: 423–434.
  • 57. Hart B.A.T., Laman J.D., Bauer J. et al. (2004) Modelling of multiple sclerosis: lessons learned in a non-human primate. Lancet Neurol., 3: 588–597.
  • 58. Zamvil S.S., Nelson P.A., Mitchell D.J. et al. (1985) Encephalitogenic T cell clones specific for myelin basic protein. An unusual bias in antigen recognition. J. Exp. Med., 162: 2107–2124.
  • 59. Yokote H., Miyake S., Croxford J.L. et al. (2008) Cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am. J. Pathol., 173: 1714–1723.
  • 60. Ben-Nun A., Kaushansky N., Kawakami N. et al. (2014) From classic to spontaneous and humanized models of multiple sclerosis: impact on understanding pathogenesis and drug development. J. Autoimmun, 54: 33–50.
  • 61. Molnarfi N., Schulze-Topphoff U., Weber M.S. et al. (2013) MHC class II-dependent B cell APC function is required for induction of CNS autoimmunity independent of myelin-specific antibodies. J. Exp. Med., 210: 2921–2937.
  • 62. Faber H., Kurtoic D., Krishnamoorthy G. et al. (2020) Gene expression in spontaneous experimental autoimmune encephalomyelitis is linked to human multiple sclerosis risk genes. Front. Immunol., 11: 2165.
  • 63. Pöllinger B., Krishnamoorthy G., Berer K. et al. (2009) Spontaneous relapsing-remitting EAE in the SJL/J mouse: MOG-reactive transgenic T cells recruit endogenous MOG-specific B cells. J. Exp. Med., 206: 1303–1316.
  • 64. Нефедов А.А., Мамчур В.Й., Твердохлеб И.В. (2016) Особенности ультраструктуры фронтальной коры и гиппокампа крыс в условиях экспериментального аллергического энцефаломиелита. Morphologia, 10(1): 54–61.
  • 65. Bjartmar C., Kidd G., Mörk S. et al. (2000) Neurological disability correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients. Ann. Neurol., 48: 893–901.
  • 66. Takeuchi C., Yamagata K., Takemiya T. (2013) Variation in experimental autoimmune encephalomyelitis scores in a mouse model of multiple sclerosis. World J. Neurol., 3: 56–61.
  • 67. Migliore S., Ghazaryan A., Simonelli I. et al. (2017) Cognitive impairment in relapsing-remitting multiple sclerosis patients with very mild clinical disability. Behav. Neurol., 2017: 7404289.
  • 68. Lisi L., Navarra P., Cirocchi R. et al. (2012) Rapamycin reduces clinical signs and neuropathic pain in a chronic model of experimental autoimmune encephalomyelitis. J. Neuroimmunol., 243: 43–51.
  • 69. Damasceno A., Damasceno B., Cendes F. (2012) Brain cortical lesion load is related to cognitive dysfunction in multiple sclerosis patients. Neurology, 78. DOI: 10.1212/WNL.78.1_MeetingAbstracts.P03.079
  • 70. Lu J., Kurejova M., Wirotanseng L.N. et al. (2012) Pain in experimental autoimmune encephalitis: a comparative study between different mouse models. J. Neuroinflammation, 9: 233.
  • 71. Potter L.E., Paylor J.W., Suh J.S. et al. (2016) Altered excitatory-inhibitory balance within somatosensory cortex is associated with enhanced plasticity and pain sensitivity in a mouse model of multiple sclerosis. J. Neuroinflammation, 13: 142.
  • 72. Gao F., Yin X., Edden R.A.E. et al. (2018) Altered hippocampal GABA and glutamate levels and uncoupling from functional connectivity in multiple sclerosis. Hippocampus, 28: 813–823.
  • 73. Fletcher J.M., Lalor S.J., Sweeney C.M. et al. (2010) T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Exp. Immunol., 162: 1–11.
  • 74. Gold R., Linington C., Lassmann H. (2006) Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain, 129(Pt. 8): 1953–1971.
  • 75. Ortiz G.G., Pacheco-Moisés F.P., Bitzer-Quintero O.K. et al. (2013) Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clin. Dev. Immunol., 2013: 708659.
  • 76. Chen X., Guo C., Kong J. (2012) Oxidative stress in neurodegenerative diseases. Neural. Regen. Res., 7: 376–385. DOI: 10.3969/j.issn.1673-5374.2012.05.009.
  • 77. Witherick J., Wilkins A., Scolding N., Kemp K. (2010) Mechanisms of oxidative damage in multiple sclerosis and a cell therapy approach to treatment. Autoimmune Dis., 2011: 164608.
  • 78. Lassmann H., van Horssen J. (2016) Oxidative stress and its impact on neurons and glia in multiple sclerosis lesions. Biochim. Biophys. Acta, 1862: 506–510.
  • 79. Spaas J., van Veggel L., Schepers M. et al. (2021) Oxidative stress and impaired oligodendrocyte precursor cell differentiation in neurological disorders. Cell Mol. Life Sci., 78: 4615–4637.
  • 80. Meyer N., Rinholm J.E. (2021) Mitochondria in myelinating oligodendrocytes: slow and out of breath? Metabolites, 11: 359.
  • 81. Adamczyk B., Adamczyk-Sowa M. (2016) New insights into the role of oxidative stress mechanisms in the pathophysiology and treatment of multiple sclerosis. Oxid. Med. Cell Longev., 2016: 1973834.
  • 82. Zia S., Rawji K.S., Michaels N.J. et al. (2020) Microglia diversity in health and multiple sclerosis. Front. Immunol., 11: 588021.
  • 83. Robinson R.R., Dietz A.K., Maroof A.M. et al. (2019) The role of glial–neuronal metabolic cooperation in modulating progression of multiple sclerosis and neuropathic pain. Immunotherapy, 11: 129–147.
  • 84. Tsuda M., Inoue K. (2016) Neuron–microglia interaction by purinergic signaling in neuropathic pain following neurodegeneration. Neuropharmacology, 104: 76–81.
  • 85. Pegoretti V., Swanson K.A., Bethea J.R. et al. (2020) Inflammation and oxidative stress in multiple sclerosis: consequences for therapy development. Oxid. Med. Cell Longev., 2020: 7191080.
  • 86. Sarchielli P., Greco L., Floridi A. et al. (2003) Excitatory amino acids and multiple sclerosis: evidence from cerebrospinal fluid. Arch. Neurol., 60: 1082–1088.
  • 87. Rodriguez-Chavez V., Moran J., Molina-Salinas G. et al. (2021) Participation of glutamatergic ionotropic receptors in excitotoxicity: the neuroprotective role of prolactin. Neuroscience, 461: 180–193.
  • 88. Pereira V., Goudet C. (2019) Emerging trends in pain modulation by metabotropic glutamate receptors. Front. Mol. Neurosci., 11: 464.