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DOI :10.26650/B/LSB44.2024.037.002   IUP :10.26650/B/LSB44.2024.037.002    Full Text (PDF)

The Experimental Animal Models for the Research of Neuroimmunological Diseases

Ece AkbayırCanan Aysel UlusoyJudith CossinsErdem Tüzün

Neuroimmunological diseases may have been known for centuries in medical practice, but they are still both challenging and emerging topics even in this modern medicine era, since they are quite heterogeneous and hard to differentiate one particular neuroimmune disease from another neurological ones, which make them hard to diagnose and treat. Experimental animal models have always been a good tool for researching pathogenesis and treatment strategies of these diseases. In the last decades, as the cutting-edge technologies develop, in vivo studies have seen lots of improvements like transgenic models, spontaneous animal models, and also the experimental equipments used in in vivo studies and laboratory animal welfare. However also in vitro assays, like genetic manipulations in cell culture, organ-on-a-chip and advanced biochemical and genetic technologies have been developed and they have being discussed whether these technologies may take place of experimental animal models. Despite of ongoing arguments, animal models for human diseases are still one of the best and widely-used experimental approaches to reveal the pathological mechanisms and develop new treatment strategies in systemic action. In this chapter, we are going to discuss briefly the most common experimental animal models of wellknown neuroimmunological diseases to give the readers the main concept of how to study these diseases in vivo.



References

  • 1. Lassmann H, Bradl M. Multiple sclerosis: experimental models and reality. Acta Neuropathol. 2017;133(2):223-244. google scholar
  • 2. Hassani A, Khan G. What do animal models tell us about the role of EBV in the pathogenesis of multiple sclerosis?. Front Immunol. 2022;13:1036155. google scholar
  • 3. Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O. Multiple sclerosis. Lancet. 2018;391(10130):1622-1636. google scholar
  • 4. Burrows D J, McGown, A., Jain, S. A., De Felice, M., Ramesh, T. M., Sharrack, B., & Majid, A. Animal models of multiple sclerosis: From rodents to zebrafish. Multiple sclerosis 2019;25(3),306-324. google scholar
  • 5. Mendel I, Kerlero de Rosbo N, Ben-Nun A. A myelin oligodendrocyte glycoprotein peptide induces typical chronic experimental autoimmune encephalomyelitis in H-2b mice: fine specificity and T cell receptor V beta expression of encephalitogenic T cells. Eur J Immunol. 1995;25(7):1951-1959. google scholar
  • 6. Berard JL, Wolak K, Fournier S, David S. Characterization of relapsing-remitting and chronic forms of experimental autoimmune encephalomyelitis in C57BL/6 mice. Glia. 2010;58(4):434-445. google scholar
  • 7. Jones MV, Nguyen TT, Deboy CA, Griffin JW, Whartenby KA, Kerr DA et al., Behavioral and pathological outcomes in MOG 35-55 experimental autoimmune encephalomyelitis. J Neuroimmunol. 2008;199(1-2):83-93. google scholar
  • 8. McRae BL, Kennedy MK, Tan LJ, Dal Canto MC, Picha KS, Miller SD. Induction of active and adoptive relapsing experimental autoimmune encephalomyelitis (EAE) using an encephalitogenic epitope of prote-olipid protein. J Neuroimmunol. 1992;38(3):229-240. google scholar
  • 9. Shin T, Ahn M, Matsumoto Y. Mechanism of experimental autoimmune encephalomyelitis in Lewis rats: recent insights from macrophages. Anat Cell Biol. 2012;45(3):141-148. google scholar
  • 10. Şekerdağ-Kılıç E, Ulusoy C, Atak D, Özkan E, Gökyüzü AB, Seyaj S, Deniz G, Uçar EA, Budan AS, Zeybel M, Öztop-Çakmak Ö, Vural A, Tuncer A, Karabudak R, Kücükali CI, Tüzün E, Gürsoy-Özdemir Y. Perivascular PDGFRB+ cells accompany lesion formation and clinical evolution differentially in two different EAE models. Mult Scler Relat Disord. 2023;69:104428. google scholar
  • 11. Su SB, Silver PB, Grajewski RS, Agarwal RK, Tang J, Chan CC et al. Essential role of the MyD88 pat-hway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoim-munity. J Immunol. 2005;175(10):6303-6310. google scholar
  • 12. Huseby ES, Liggitt D, Brabb T, Schnabel B, Ohlen C, Goverman J. A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J Exp Med. 2001;194(5):669-676. google scholar
  • 13. Ransohoff RM. Animal models of multiple sclerosis: the good, the bad and the bottom line. Nat Neurosci. 2012;15(8):1074-1077. google scholar
  • 14. Constantinescu CS, Farooqi N, O’Brien K, Gran B. Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). Br J Pharmacol. 2011;164(4):1079-1106. google scholar
  • 15. Lassmann H, Ransohoff RM. The CD4-Th1 model for multiple sclerosis: a critical [correction of crucial] re-appraisal [published correction appears in Trends Immunol. 2004 Jun;25(6):275]. Trends Immunol. 2004;25(3):132-137. google scholar
  • 16. Stimmer L, Fovet CM, Serguera C. Experimental Models of Autoimmune Demyelinating Diseases in Nonhuman Primates. Vet Pathol. 2018;55(1):27-41. google scholar
  • 17. Rose LM, Richards T, Alvord EC Jr. Experimental allergic encephalomyelitis (EAE) in nonhuman prima-tes: a model of multiple sclerosis. Lab Anim Sci. 1994;44(5):508-512. google scholar
  • 18. Stewart WA, Alvord EC Jr, Hruby S, Hall LD, Paty DW. Magnetic resonance imaging of experimental allergic encephalomyelitis in primates. Brain. 1991;114 ( Pt 2):1069-1096. google scholar
  • 19. Brok HP, Bauer J, Jonker M, et al. Non-human primate models of multiple sclerosis. Immunol Rev. 2001;183:173-185. google scholar
  • 20. Kulkarni P, Yellanki S, Medishetti R, Sriram D, Saxena U, Yogeeswari P. Novel Zebrafish EAE model: A quick in vivo screen for multiple sclerosis. Mult Scler Relat Disord. 2017;11:32-39. google scholar
  • 21. Marusic S, Leach MW, Pelker JW, Azoitei ML, Uozumi N, Cui J et al. Cytosolic phospholipase A2 alpha-de-ficient mice are resistant to experimental autoimmune encephalomyelitis. J Exp Med. 2005;202(6):841-851. google scholar
  • 22. Stromnes IM, Goverman JM. Passive induction of experimental allergic encephalomyelitis. Nat Protoc. 2006;1(4):1952-1960. google scholar
  • 23. Smith P. Animal Models of Multiple Sclerosis. Curr Protoc. 2021;1(6):e185. google scholar
  • 24. Matsushima GK, Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyeli-nation in the central nervous system. Brain Pathol. 2001;11(1):107-116. google scholar
  • 25. Faizi M, Salimi A, Seydi E, Naserzadeh P, Kouhnavard M, Rahimi A et al. Toxicity of cuprizone a Cu(2+) chelating agent on isolated mouse brain mitochondria: a justification for demyelination and subsequent behavioral dysfunction. Toxicol Mech Methods. 2016;26(4):276-283. google scholar
  • 26. Stidworthy MF, Genoud S, Suter U, Mantei N, Franklin RJ. Quantifying the early stages of remyelination following cuprizone-induced demyelination. Brain Pathol. 2003;13(3):329-339. google scholar
  • 27. Hiremath MM, Saito Y, Knapp GW, Ting JP, Suzuki K, Matsushima GK. Microglial/macrophage accumu-lation during cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol. 1998;92(1-2):38-49. google scholar
  • 28. Gharagozloo M, Mace JW, Calabresi PA. Animal models to investigate the effects of inflammation on remyelination in multiple sclerosis. Front Mol Neurosci. 2022;15:995477. google scholar
  • 29. Praet J, Guglielmetti C, Berneman Z, Van der Linden A, Ponsaerts P. Cellular and molecular neuropat-hology of the cuprizone mouse model: clinical relevance for multiple sclerosis. Neurosci Biobehav Rev. 2014;47:485-505. google scholar
  • 30. Allt G, Ghabriel MN, Sikri K. Lysophosphatidyl choline-induced demyelination. A freeze-fracture study. Acta Neuropathol. 1988;75(5):456-464. google scholar
  • 31. Keough MB, Jensen SK, Yong VW. Experimental demyelination and remyelination of murine spinal cord by focal injection of lysolecithin. J Vis Exp. 2015;(97):52679. google scholar
  • 32. Bjelobaba I, Begovic-Kupresanin V, Pekovic S, Lavrnja I. Animal models of multiple sclerosis: Focus on experimental autoimmune encephalomyelitis. J Neurosci Res. 2018;96(6):1021-1042. google scholar
  • 33. Popko B. Myelin maintenance: axonal support required. Nat Neurosci. 2010;13(3):275-277. google scholar
  • 34. Plemel JR, Liu WQ, Yong VW. Remyelination therapies: a new direction and challenge in multiple scle-rosis. Nat Rev Drug Discov. 2017;16(9):617-634. google scholar
  • 35. Theiler M. Spontaneous encephalomyelitis of mice--a new Virus disease. Science. 1934;80(2066):122. google scholar
  • 36. Oleszak EL, Chang JR, Friedman H, Katsetos CD, Platsoucas CD. Theiler’s virus infection: a model for multiple sclerosis. Clin Microbiol Rev. 2004;17(1):174-207. google scholar
  • 37. McGavern DB, Murray PD, Rivera-Quinones C, Schmelzer JD, Low PA, Rodriguez M. Axonal loss results in spinal cord atrophy, electrophysiological abnormalities and neurological deficits following demyelina-tion in a chronic inflammatory model of multiple sclerosis. Brain. 2000;123 Pt 3(Pt 3):519-531. google scholar
  • 38. Bender SJ, Weiss SR. Pathogenesis of murine coronavirus in the central nervous system. J Neuroimmune Pharmacol. 2010;5(3):336-354. google scholar
  • 39. Stohlman SA, Weiner LP. Chronic central nervous system demyelination in mice after JHM virus infecti-on. Neurology. 1981;31(1):38-44. google scholar
  • 40. Wu GF, Perlman S. Macrophage infiltration, but not apoptosis, is correlated with immune-mediated dem-yelination following murine infection with a neurotropic coronavirus. J Virol. 1999;73(10):8771-8780. google scholar
  • 41. Tuzun E, Berrih-Aknin S, Brenner T, Kusner LL, Le Panse R, Yang H, et al. Guidelines for standard preclinical experiments in the mouse model of myasthenia gravis induced by acetylcholine receptor im-munization. Exp Neurol. 2015;270:11-17. google scholar
  • 42. Lazaridis K, Tzartos SJ. Autoantibody Specificities in Myasthenia Gravis; Implications for Improved Diagnostics and Therapeutics. Front Immunol. 2020;11:212. google scholar
  • 43. Hoch W, McConville J, Helms S, Newsom-Davis J, Melms A, Vincent A. Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat Med. 2001;7(3):365-368. google scholar
  • 44. Zisimopoulou P, Evangelakou P, Tzartos J, Lazaridis K, Zouvelou V; Mantegazza R et al. A comprehensive analysis of the epidemiology and clinical characteristics of anti-LRP4 in myasthenia gravis. J Autoimmun. 2014;52:139-145. google scholar
  • 45. Chen, Y.; Tao, X.; Wang, Y.; Xu, S.; Yang, Y.; Han, J.; Qiu, F. Clinical Characteristics and Prognosis of Anti-AChR Positive Myasthenia Gravis Combined With Anti-LRP4 or Anti-Titin Antibody. Front. Neurol. 2022, 13, 873599. google scholar
  • 46. Skeie GO, Aarli JA, Gilhus NE. Titin and ryanodine receptor antibodies in myasthenia gravis. Acta Neurol Scand Suppl. 2006;183:19-23. google scholar
  • 47. Nair SS, Jacob S. Novel Immunotherapies for Myasthenia Gravis. Immunotargets Ther. 2023;12:25-45. google scholar
  • 48. Mantegazza R, Cordiglieri C, Consonni A, Baggi F. Animal models of myasthenia gravis: utility and limitations. Int J Gen Med. 2016;9:53-64. google scholar
  • 49. Conti-Fine BM, Milani M, Kaminski HJ. Myasthenia gravis: past, present, and future. J Clin Invest. 2006;116(11):2843-2854. google scholar
  • 50. Ulusoy C, Kim E, Tüzün E, Huda, R., Yılmaz, V., Poulas, K., et al. Preferential production of IgG1, IL-4 and IL-10 in MuSK-immunized mice. Clin Immunol. 2014;151(2):155-163. google scholar
  • 51. Ulusoy C, Çavuş F, Yılmaz V, Tüzün E. Immunization with Recombinantly Expressed LRP4 Induces Experimental Autoimmune Myasthenia Gravis in C57BL/6 Mice. Immunol Invest. 2017;46(5):490-499. google scholar
  • 52. Billiau A, Matthys P. Modes of action of Freund’s adjuvants in experimental models of autoimmune dise-ases. J Leukoc Biol. 2001;70(6):849-860. google scholar
  • 53. Robinet M, Maillard S, Cron MA, Berrih-Aknin S, Le Panse R. Review on Toll-Like Receptor Activation in Myasthenia Gravis: Application to the Development of New Experimental Models. Clin Rev Allergy Immunol. 2017;52(1):133-147. google scholar
  • 54. Verschuuren JJGM, Plomp JJ, Burden SJ, Zhang W, Fillie-Grijpma YE, Stienstra-van Es IE,et al. Pas-sive transfer models of myasthenia gravis with muscle-specific kinase antibodies. Ann N Y Acad Sci. 2018;1413(1):111-118. google scholar
  • 55. Matthews-Bellinger JA, Salpeter MM. Fine structural distribution of acetylcholine receptors at developing mouse neuromuscular junctions. J Neurosci. 1983;3(3):644-657. google scholar
  • 56. Rodriguez Cruz PM, Ravenscroft G, Natera D, Carr A, Manzur A, Liu WW, et al. A novel phenotype of AChR-deficiency syndrome with predominant facial and distal weakness resulting from the inclusion of an evolutionary alternatively-spliced exon in CHRNA1. Neuromuscul Disord. 2023;33(2):161-8. google scholar
  • 57. Hesselmans LF, Jennekens FG, Van den Oord CJ, Veldman H, Vincent A. Development of innervation of skeletal muscle fibers in man: relation to acetylcholine receptors. Anat Rec. 1993;236(3):553-62. google scholar
  • 58. Missias AC, Chu GC, Klocke BJ, Sanes JR, Merlie JP. Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR gamma-to-epsilon switch. Dev Biol. 1996;179(1):223-38. google scholar
  • 59. Witzemann V, Schwarz H, Koenen M, Berberich C, Villarroel A, Wernig A, et al. Acetylcholine receptor epsilon-subunit deletion causes muscle weakness and atrophy in juvenile and adult mice. Proc Natl Acad Sci U S A. 1996;93(23):13286-91. google scholar
  • 60. Missias AC, Mudd J, Cunningham JM, Steinbach JH, Merlie JP, Sanes JR. Deficient development and maintenance of postsynaptic specializations in mutant mice lacking an adult acetylcholine receptor subunit. Development. 1997;124(24):5075-86. google scholar
  • 61. MacLennan C, Beeson D, Buijs AM, Vincent A, Newsom-Davis J. Acetylcholine receptor expression in human extraocular muscles and their susceptibility to myasthenia gravis. Ann Neurol. 1997;41(4):423-31. google scholar
  • 62. Cossins J, Webster R, Maxwell S, Burke G, Vincent A, Beeson D. A mouse model of AChR deficiency syndrome with a phenotype reflecting the human condition. Hum Mol Genet. 2004;13(23):2947-57. google scholar
  • 63. Vanhaesebrouck AE, Webster R, Maxwell S, Rodriguez Cruz PM, Cossins J, Wickens J, et al. beta2-Ad-renergic receptor agonists ameliorate the adverse effect of long-term pyridostigmine on neuromuscular junction structure. Brain. 2019;142(12):3713-27. google scholar
  • 64. Gomez CM, Bhattacharyya BB, Charnet P, Day JW, Labarca C, Wollmann RL, et al. A transgenic mouse model of the slow-channel syndrome. Muscle Nerve. 1996;19(1):79-87. google scholar
  • 65. Gomez CM, Maselli R, Gundeck JE, Chao M, Day JW, Tamamizu S, et al. Slow-channel transge-nic mice: a model of postsynaptic organellar degeneration at the neuromuscular junction. J Neurosci. 1997;17(11):4170-9. google scholar
  • 66. Webster RG, Cossins J, Lashley D, Maxwell S, Liu WW, Wickens JR, et al. A mouse model of the slow channel myasthenic syndrome: Neuromuscular physiology and effects of ephedrine treatment. Experimen-tal neurology. 2013;248:286-98. google scholar
  • 67. Chevessier F, Peter C, Mersdorf U, Girard E, Krejci E, McArdle JJ, et al. A new mouse model for the slow-channel congenital myasthenic syndrome induced by the AChR epsilonL221F mutation. Neurobiol Dis. 2012;45(3):851-61. google scholar
  • 68. Grajales-Reyes JG, Garcia-Gonzalez A, Maria-Rios JC, Grajales-Reyes GE, Delgado-Velez M, Baez-Pagan CA, et al. A Panel of Slow-Channel Syndrome Mice Reveals a Unique Locomotor Behavioral Signature. J Neuromuscul Dis. 2017;4(4):341-7. google scholar
  • 69. Gomez CM, Maselli RA, Groshong J, Zayas R, Wollmann RL, Cens T, et al. Active calcium accumulation underlies severe weakness in a panel of mice with slow-channel syndrome. J Neurosci. 2002;22(15):6447-57. google scholar
  • 70. Bhattacharyya BJ, Day JW, Gundeck JE, Leonard S, Wollmann RL, Gomez CM. Desensitization of mu-tant acetylcholine receptors in transgenic mice reduces the amplitude of neuromuscular synaptic currents. Synapse. 1997;27(4):367-77. google scholar
  • 71. Zhu H, Grajales-Reyes GE, Alicea-Vazquez V, Grajales-Reyes JG, Robinson K, Pytel P, et al. Fluoxetine is neuroprotective in slow-channel congenital myasthenic syndrome. Exp Neurol. 2015;270:88-94. google scholar
  • 72. Palace J, Lashley D, Bailey S, Jayawant S, Carr A, McConville J, et al. Clinical features in a series of fast channel congenital myasthenia syndrome. Neuromuscul Disord. 2012;22(2):112-7. google scholar
  • 73. Burke G, Cossins J, Maxwell S, Owens G, Vincent A, Robb S, et al. Rapsyn mutations in hereditary myasthenia: distinct early- and late-onset phenotypes. Neurology. 2003;61(6):826-8. google scholar
  • 74. Milone M, Shen XM, Selcen D, Ohno K, Brengman J, Iannaccone ST, et al. Myasthenic syndrome due to defects in rapsyn: Clinical and molecular findings in 39 patients. Neurology. 2009;73(3):228-35. google scholar
  • 75. Xing G, Jing H, Zhang L, Cao Y, Li L, Zhao K, et al. A mechanism in agrin signaling revealed by a preva-lent Rapsyn mutation in congenital myasthenic syndrome. Elife. 2019;8. google scholar
  • 76. Li L, Cao Y, Wu H, Ye X, Zhu Z, Xing G, et al. Enzymatic Activity of the Scaffold Protein Rapsyn for Synapse Formation. Neuron. 2016;92(5):1007-19. google scholar
  • 77. Arimura S, Okada T, Tezuka T, Chiyo T, Kasahara Y, Yoshimura T, et al. Neuromuscular disease. DOK7 gene therapy benefits mouse models of diseases characterized by defects in the neuromuscular junction. Science. 2014;345(6203):1505-8. google scholar
  • 78. Chevessier F, Girard E, Molgo J, Bartling S, Koenig J, Hantai D, et al. A mouse model for congenital myasthenic syndrome due to MuSK mutations reveals defects in structure and function of neuromuscular junctions. Hum Mol Genet. 2008;17(22):3577-95. google scholar
  • 79. Huze C, Bauche S, Richard P, Chevessier F, Goillot E, Gaudon K, et al. Identification of an agrin mutation that causes congenital myasthenia and affects synapse function. Am J Hum Genet. 2009;85(2):155-67. google scholar
  • 80. Cossins J, Webster R, Maxwell S, Rodriguez Cruz PM, Knight R, Llewelyn JG, et al. Congenital myast-henic syndrome due to a TOR1AIP1 mutation: a new disease pathway for impaired synaptic transmission. Brain Commun. 2020;2(2):fcaa174. google scholar
  • 81. Malfatti E, Catchpool T, Nouioua S, Sihem H, Fournier E, Carlier RY, et al. A TOR1AIP1 variant segrega-ting with an early onset limb girdle myasthenia-Support for the role of LAP1 in NMJ function and disease. Neuropathol Appl Neurobiol. 2022;48(1):e12743. google scholar
  • 82. Shin JY, Mendez-Lopez I, Wang Y, Hays AP, Tanji K, Lefkowitch JH, et al. Lamina-associated polypepti-de-1 interacts with the muscular dystrophy protein emerin and is essential for skeletal muscle maintenance. Dev Cell. 2013;26(6):591-603. google scholar
  • 83. Duan T, Verkman AS. Experimental animal models of aquaporin-4-IgG-seropositive neuromyelitis optica spectrum disorders: progress and shortcomings. Brain Pathol. 2020;30(1):13-25. google scholar
  • 84. Bagherieh S, Afshari-Safavi A, Vaheb S, Kiani M, Ghaffary EM, Barzegar M, Shaygannejad V, Zabeti A, Mirmosayyeb O. Worldwide prevalence of neuromyelitis optica spectrum disorder (NMOSD) and neuromyelitis optica (NMO): a systematic review and meta-analysis. Neurol Sci. 2023;44(6):1905-1915. google scholar
  • 85. da Silva APB, Silva RBM, Goi LDS, Molina RD, Machado DC, Sato DK. Experimental Models of Neuro-immunological Disorders: A Review. Front Neurol. 2020;11:389. google scholar
  • 86. Bradl M, Misu T, Takahashi T, Watanabe, M., Mader, S., Reindl, M., et al. Neuromyelitis optica: pathoge-nicity of patient immunoglobulin in vivo. Ann Neurol. 2009;66(5):630-643. google scholar
  • 87. Saini H, Rifkin R, Gorelik M, Huang H, Ferguson Z, Jones MV, Levy M. Passively transferred human NMO-IgG exacerbates demyelination in mouse experimental autoimmune encephalomyelitis. BMC Neurol. 2013;13:104. google scholar
  • 88. Kinoshita M, Nakatsuji Y, Kimura T, Moriya M, Takata K, Okuno T, Kumanogoh A, Kajiyama K, Yos-hikawa H, Sakoda S. Neuromyelitis optica: Passive transfer to rats by human immunoglobulin. Biochem Biophys Res Commun. 2009;386(4):623-7. google scholar
  • 89. Kurosawa K, Misu T, Takai Y, Sato DK, Takahashi T, Abe Y, et al. Severely exacerbated neuromyelitis optica rat model with extensive astrocytopathy by high affinity anti-aquaporin-4 monoclonal antibody. Acta Neuropathol Commun. 2015;3:82. google scholar
  • 90. Saadoun S, Waters P, Bell BA, Vincent A, Verkman AS, Papadopoulos MC. Intra-cerebral injection of neuromyelitis optica immunoglobulin G and human complement produces neuromyelitis optica lesions in mice. Brain. 2010;133(Pt 2):349-61. google scholar
  • 91. Asavapanumas N, Ratelade J, Verkman AS. Unique neuromyelitis optica pathology produced in naıve rats by intracerebral administration of NMO-IgG. Acta Neuropathol. 2014;127(4):539-51. google scholar
  • 92. Marignier R, Ruiz A, Cavagna , Nicole A, Watrin C, Touret M, et al. Neuromyelitis optica study model ba-sed on chronic infusion of autoantibodies in rat cerebrospinal fluid. J Neuroinflammation. 2016;13(1):111. google scholar
  • 93. Wingerchuk DM. The clinical course of acute disseminated encephalomyelitis. Neurol Res. 2006;28(3):341-7. google scholar
  • 94. Taghdiri MM, Amouzadeh MH, Esmail Nejad SS, Abasi E, Alipour A, Akhavan M. Epidemiological, Clini-cal, and Laboratory Characteristics of Acute Disseminated Encephalomyelitis in Children: A Retrospective Study. Iran J Child Neurol. 2019;13(4):65-73. google scholar
  • 95. Cole J, Evans E, Mwangi M, Mar S. Acute Disseminated Encephalomyelitis in Children: An Updated Review Based on Current Diagnostic Criteria. Pediatr Neurol. 2019;100:26-34. google scholar
  • 96. Höftberger R, Lassmann H. Inflammatory demyelinating diseases of the central nervous system. Handb Clin Neurol. 2017;145:263-283. google scholar
  • 97. ‘t Hart BA, Bauer J, Brok HP, Amor S. Non-human primate models of experimental autoimmune encep-halomyelitis: Variations on a theme. J Neuroimmunol. 2005;168(1-2):1-12. google scholar
  • 98. Haanstra KG, Jagessar SA, Bauchet AL, Doussau M, Fovet CM, Heijmans N, Hofman SO, et al., Induction of experimental autoimmune encephalomyelitis with recombinant human myelin oligodendrocyte gly-coprotein in incomplete Freund’s adjuvant in three non-human primate species. J Neuroimmune Pharmacol. 2013;8(5):1251-64. google scholar
  • 99. Lancaster E, Dalmau J. Neuronal autoantigens--pathogenesis, associated disorders and antibody testing. Nat Rev Neurol. 2012;8(7):380-90. google scholar
  • 100. Nguyen L, Wang C. Anti-NMDA Receptor Autoimmune Encephalitis: Diagnosis and Management Stra-tegies. Int J Gen Med. 2023;16:7-21. google scholar
  • 101. Dalmau J, Tüzün E, Wu HY, Masjuan J, Rossi JE, Voloschin A, Baehring JM, et al. Paraneoplas-tic anti-N-methyl-D- aspartate receptor encephalitis associated with ovarian teratoma. Ann Neurol. 2007;61(1):25-36. google scholar
  • 102. Ladepeche L, Planaguma J, Thakur S, Suarez I, Hara M, Borbely JS, Sandoval A,et al. NMDA Receptor Autoantibodies in Autoimmune Encephalitis Cause a Subunit-Specific Nanoscale Redistribution of NMDA Receptors. Cell Rep. 2018;23(13):3759- 3768. google scholar
  • 103. Ciano-Petersen NL, Muniz-Castrillo S, Birzu C, Vogrig A, Farina A, Villagran-Garda M, Joubert B, et al. Cytokine dynamics and targeted immunotherapies in autoimmune encephalitis. Brain Commun. 2022;4(4):fcac196. google scholar
  • 104. Planaguma J, Leypoldt F, Mannara F, Gutierrez-Cuesta J, Martm-Garda E, Aguilar E, Titulaer MJ, et al. Human N- methyl D-aspartate receptor antibodies alter memory and behaviour in mice. Brain. 2015;138(Pt 1):94-109. google scholar
  • 105. Li Y, Tanaka K, Wang L, Ishigaki Y, Kato N. Induction of Memory Deficit in Mice with Chronic Exposure to Cerebrospinal Fluid from Patients with Anti-N-Methyl-D-Aspartate Receptor Encephalitis. Tohoku J Exp Med. 2015;237(4):329-38. google scholar
  • 106. Taraschenko O, Fox HS, Pittock SJ, Zekeridou A, Gafurova M, Eldridge E, Liu J, et al. A mouse model of seizures in anti-N-methyl-d-aspartate receptor encephalitis. Epilepsia. 2019;60(3):452-463. google scholar
  • 107. Jones BE, Tovar KR, Goehring A, Jalali-Yazdi F, Okada NJ, Gouaux E, Westbrook GL. Autoimmune re-ceptor encephalitis in mice induced by active immunization with conformationally stabilized holoreceptors. Sci Transl Med. 2019;11(500):eaaw0044. google scholar
  • 108. Jurynczyk M, Jacob A, Fujihara K, Palace J. Myelin oligodendrocyte glycoprotein (MOG) antibody- as-sociated disease: practical considerations. Pract Neurol. 2019;19(3):187-195. google scholar
  • 109. Ambrosius W, Michalak S, Kozubski W, Kalinowska A. Myelin Oligodendrocyte Glycoprotein Antibod-y-Associated Disease: Current Insights into the Disease Pathophysiology, Diagnosis and Management. Int J Mol Sci. 2020;22(1):100. google scholar
  • 110. Krishnamoorthy G, Lassmann H, Wekerle H, Holz A. Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation. J Clin Invest. 2006;116(9):2385-92. google scholar
  • 111. Graber DJ, Levy M, Kerr D, Wade WF. Neuromyelitis optica pathogenesis and aquaporin 4. J Neuroinf-lammation. 2008;5:22. google scholar


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