Experimental autoimmune encephalomyelitis

Experimental autoimmune encephalomyelitis, sometimes experimental allergic encephalomyelitis (EAE), is an animal model of brain inflammation. It is an inflammatory demyelinating disease of the central nervous system (CNS). It is mostly used with rodents and is widely studied as an animal model of the human CNS demyelinating diseases, including multiple sclerosis (MS) and acute disseminated encephalomyelitis (ADEM). EAE is also the prototype for T-cell-mediated autoimmune disease in general.[citation needed]

EAE development was motivated by observations during the convalescence from viral diseases by Thomas M. Rivers, D. H. Sprunt and G. P. Berry in 1933. Their findings upon a transfer of inflamed patient tissue to primates was published in the Journal of Experimental Medicine.[1][2] An acute monophasic illness, it has been suggested that EAE is far more similar to ADEM than to MS.[3]

Types of EAE

EAE can be induced in a number of species, including mice, rats, guinea pigs, rabbits and primates.

The most commonly used antigens in rodents are spinal cord homogenate (SCH), purified myelin, myelin protein such as MBP, PLP, and MOG, or peptides of these proteins, all resulting in distinct models with different disease characteristics regarding both immunology and pathology.[4][5] It may also be induced by the passive transfer of T cells specifically reactive to these myelin antigens.[6]

Depending on the antigen used and the genetic make-up of the animal, rodents can display a monophasic bout of EAE, a relapsing-remitting form, or chronic EAE. The typical susceptible rodent will debut with clinical symptoms around two weeks after immunization and present with a relapsing-remitting disease. The archetypical first clinical symptom is weakness of tail tonus that progresses to paralysis of the tail, followed by a progression up the body to affect the hind limbs and finally the forelimbs.[citation needed]

However, similar to MS, the disease symptoms reflect the anatomical location of the inflammatory lesions, and may also include emotional lability, sensory loss, optic neuritis, difficulties with coordination and balance (ataxia), and muscle weakness and spasms. Recovery from symptoms can be complete or partial and the time varies with symptoms and disease severity. Depending on the relapse-remission intervals, rats can have up to three bouts of disease within an experimental period.[citation needed]

In mice

Demyelination is produced by injection of brain extracts, CNS proteins (such as myelin basic protein), or peptides from such protein emulsified in an adjuvant such as complete Freund's adjuvant. The presence of the adjuvant allows the generation of inflammatory responses to the protein/peptides. In many protocols, mice are coinjected with pertussis toxin to break down the blood-brain barrier and allow immune cells access to the CNS tissue. This immunisation leads to multiple small disseminated lesions of demyelination (as well as micro-necroses) in the brain and spinal cord and the onset of clinical symptoms.[citation needed]

Although sharing some features, mostly demyelination, this model, first introduced in the 1930s, differs from human MS in several ways. EAE either kills animals or leaves them with permanent disabilities; animals with EAE also suffer severe nerve inflammation, and the time course of EAE is entirely different from MS, being the main antigen (MBP) in charge. Some key differences between EAE in mice, and MS in humans include:

  • B-cells: Some research points to anti-CD20 B-cells being the basis of the autoimmune attacks. This has been shown to be completely different in EAE and MS.[7]
  • oxidative injury: Mitochondrial injury is seen in EAE and MS, but mitochondrial gene deletions have so far only been detected in MS lesions.[8]
  • microglia behaviour: In contrast to experimental models of inflammatory demyelination, lesion formation in multiple sclerosis occurs on a background of pro-inflammatory microglia activation, which is seen already in the normal white matter of age-matched controls, and this may contribute to neurodegeneration in the disease.[9]
  • pathological patterns: EAE is unable to reproduce MS pathological patterns III and IV.[10]

Secondary damage

Given that some conditions as MS show cortical damage together with the WM damage, there has been interest if this can appear as a secondary damage of the WM.[11]

Human Anti-MOG in mice

Anti-MOG associated encephalomyelitis can be passed from humans to mice, inducing MS type II demyelination (pattern II)[12]

Immunogenetic interactions

Deficiency of TBX21 or STAT4 provides resistance against EAE, while interferon-γ-, interferon-γ-receptor-, interleukin-12 subunit α-, interleukin 12 receptor, β 2 subunit-, and interleukin 18-deficiency exacerbated disease.[13]

In humans

Sometimes the human equivalent to EAE has been triggered in humans by accident or medical mistake. The reactions have been diverse according to the sources of the disease[14][15][16] The researchers in the last report have termed the condition "human autoimmune encephalitis" (HAE).

The damage in the second report fulfilled all pathological diagnostic criteria of MS and can therefore be classified as MS in its own right. The lesions were classified as pattern II in the Lucchinetti system. This case of human EAE also showed Dawson fingers.[16]

Using the confluent demyelination as barrier between MS and ADEM,[17] some other reports about EAE in humans classify its effects as ADEM but not always. In Japanese patients exposed to rabies vaccine that contained neural tissue, the clinical presentation resembled ADEM more than MS but the lesions were like acute multiple sclerosis (Uchimura and Shiraki, 1957).[18]

Anti-TNF demyelination

Main article: TNF_inhibitor

Recent problems with monoclonal antibodies point to an involvement of tumor necrosis factor alpha in the multiple sclerosis onset. Specifically, a monoclonal antibody against TNF-α (adalimumab) has been reported to induce a MS-like disease[19][20]

Also some experimental therapies for other diseases has produced MS artificially in patients. Specifically, monoclonal antibodies treating cancer like pembrolizumab[21] and infliximab[22] have been reported to produce MS artificially.

Specific forms of EAE

Since the discovery of the four lucchinetti patterns, new EAE models have been published, specifically mimicking the patterns I and II. DTH-EAE for pattern I (T cell and macrophage-mediated delayed-type hypersensitivity) and fMOG-EAE for pattern II (antibody-mediated focal myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalitis)[23]

Also a model for pattern III lesions has been developed in which mitochondrial metabolism is impaired, resulting in a tissue energy deficiency, a mechanism later termed "virtual hypoxia". The demyelination, characterized by loss of myelin-associated glycoprotein, has been described as "hypoxia-like".[24] Thanks to these pattern III models some specific experimental treatments have appeared[25]

The model for primary progressive MS is the Theiler's virus model. This model presents features not available in others, like microglial activation.[26]

Alternatives

Recently it has been found that CSF from MS patients can carry the disease to rodents, opening the door to an alternative model.[27]

Meningoencephalitis of unknown origin (MUO) in dogs shares some similarities[28]

References

  1. ^ Rivers TM, Spunt DH, Berry GP (1933). "Observations on Attempts to Produce Acute Disseminated Encephalomyelitis in Monkeys". Journal of Experimental Medicine. 58 (1): 39–53. CiteSeerX 10.1.1.274.2997. doi:10.1084/jem.58.1.39. PMC 2132279. PMID 19870180.
  2. ^ Rivers TM, Schwentker FF (1935). "Encephalomyelitis accompanied by myelin destruction experimentally produced in monkeys". Journal of Experimental Medicine. 61 (5): 689–701. doi:10.1084/jem.61.5.689. PMC 2133246. PMID 19870385.
  3. ^ Sriram S, Steiner I (2005). "Experimental Allergic Encephalomyelitis: A misleading model of Multiple Sclerosis". Annals of Neurology. 58 (6): 939–945. doi:10.1002/ana.20743. PMID 16315280. S2CID 12141651.
  4. ^ MANNIE, M., R. H. SWANBORG and J. A. STEPANIAK, 2009,"Experimental autoimmune encephalomyelitis in the rat." Curr Protoc Immunol, Chapter 15: Unit 15 12
  5. ^ MILLER, S. D., and W. J. KARPUS, 2007. "Experimental autoimmune encephalomyelitis in the mouse." Curr Protoc Immunol, Chapter 15: Unit 15 11
  6. ^ Ellwardt, Erik; Zipp, Frauke (2014). "Molecular mechanisms linking neuroinflammation and neurodegeneration in MS". Experimental Neurology. 262: 8–17. doi:10.1016/j.expneurol.2014.02.006. PMID 24530639. S2CID 34157793.
  7. ^ Sefia Eseberuo, Pryce Gareth, Meier Ute-Christiane, Giovannoni Gavin, Baker David (2017). "Depletion of CD20 B cells fails to inhibit relapsing mouse experimental autoimmune encephalomyelitis". Multiple Sclerosis and Related Disorders. 14: 46–50. doi:10.1016/j.msard.2017.03.013. PMID 28619431.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  8. ^ Hans Lassmann, Jack van Horssen, "Oxidative stress and its impact on neurons and glia in multiple sclerosis lesions", Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Volume 1862, Issue 3, March 2016, Pages 506-510, https://doi.org/10.1016/j.bbadis.2015.09.018
  9. ^ Tobias Zrzavy Simon Hametner Isabella Wimmer Oleg Butovsky Howard L. Weiner Hans Lassmann, Loss of 'homeostatic’ microglia and patterns of their activation in active multiple sclerosis, Brain, Volume 140, Issue 7, 1 July 2017, Pages 1900–1913, https://doi.org/10.1093/brain/awx113
  10. ^ Reza Rahmanzadeh, Wolfgang Brück, Alireza Minagar, Mohammad Ali Sahraian, Multiple sclerosis pathogenesis: missing pieces of an old puzzle, 2018-06-08, DOI: https://doi.org/10.1515/revneuro-2018-0002, [1]
  11. ^ Zipp Frauke; Ellwardt Erik; Pramanik Guatam; Mittmann Thomas; Stroh Albrecht (2016). "Cortical Hyperactivity beyond the Immune Attack: Starting Point of Neurodegeneration". Neurology. 86 (16 Supplement): S2.002.
  12. ^ Marti Fernandez I; et al. (2019). "The Glycosylation Site of Myelin Oligodendrocyte Glycoprotein Affects Autoantibody Recognition in a Large Proportion of Patients". Front Immunol. 10: 1189. doi:10.3389/fimmu.2019.01189. PMC 6579858. PMID 31244828.
  13. ^ Korn, Thomas; Bettelli, Estelle; Oukka, Mohamed; Kuchroo, Vijay K. (2009). "IL-17 and Th17 Cells". Annual Review of Immunology. 27 (1). Annual Reviews: 485–517. doi:10.1146/annurev.immunol.021908.132710. ISSN 0732-0582. PMID 19132915. (VK ORCID: 0000-0001-7177-2110 GS: h6h5FdoAAAAJ).
  14. ^ Lassman Hans (Feb 2010). "Acute disseminated encephalomyelitis and multiple sclerosis". Brain. 133 (2): 317–319. doi:10.1093/brain/awp342. PMID 20129937.
  15. ^ Vicente L. Gómez; et al. (2016). "Relapse in a paucisymptomatic form of multiple sclerosis in a patient treated with nivolumab". Neuro Oncol. 18: iv25. doi:10.1093/neuonc/now188.085. PMC 5782583.
  16. ^ a b Höftberger R, Leisser M, Bauer J, Lassmann H (Dec 2015). "Autoimmune encephalitis in humans: how closely does it reflect multiple sclerosis?". Acta Neuropathol Commun. 3 (1): 80. doi:10.1186/s40478-015-0260-9. PMC 4670499. PMID 26637427.
  17. ^ Young NP, Weinshenker BG, Parisi JE, Scheithauer B, Giannini C, Roemer SF, Thomsen KM, Mandrekar JN, Erickson BJ, Lucchinetti CF (2010). "Perivenous demyelination: association with clinically defined acute disseminated encephalomyelitis and comparison with pathologically confirmed multiple sclerosis". Brain. 133 (2): 333–348. doi:10.1093/brain/awp321. PMC 2822631. PMID 20129932.
  18. ^ Lassmann H (2010). "Acute disseminated encephalomyelitis and multiple sclerosis". Brain. 133 (2): 317–9. doi:10.1093/brain/awp342. PMID 20129937.
  19. ^ Sinah Engel et al., PPMS onset upon adalimumab treatment extends the spectrum of anti-TNF-α therapy-associated demyelinating disorders, January 2, 2020 [2]
  20. ^ Rana Alnasser Alsukhni, Ziena Jriekh and Yasmin Aboras, 2016. "Adalimumab Induced or Provoked MS in Patient with Autoimmune Uveitis: A Case Report and Review of the Literature." Case Reports in Medicine, Volume 2016 (2016), Article ID 1423131, doi https://dx.doi.org/10.1155/2016/1423131
  21. ^ Marzia Anita Lucia Romeo et al, Multiple sclerosis associated with pembrolizumab in a patient with non-small cell lung cancer, Journal of Neurology, pp 1–4, 04 October 2019
  22. ^ Alicja Kalinowska-Lyszczarz, Mahboobeh Fereidan-Esfahani, Yong Guo, Pathological findings in central nervous system demyelination associated with infliximab, https://doi.org/10.1177/1352458519894710
  23. ^ D. Anthony et al. "Anti-CD20 Therapy Down-Regulates Lesion Formation And Microglial Activation In Pattern I And Pattern II Rat Models Of Multiple Sclerosis." Neurology, April 2014.
  24. ^ Desai RA, Davies AL, Tachrount M, Kasti M, Laulund F, Golay X, Smith KJ (2016). "Cause and prevention of demyelination in a model multiple sclerosis lesion". Annals of Neurology. 79 (4): 591–604. doi:10.1002/ana.24607. PMC 4949637. PMID 26814844.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  25. ^ Desai, RA; Davies, AL; Tachrount, M; Golay, X; Smith, KJ; (2015) Normobaric hyperoxia protects against demyelination in an experimental model of pattern III multiple sclerosis lesions. In: (Proceedings) 116th Meeting of the British-Neuropathological-Society. (pp. p. 28). WILEY-BLACKWELL
  26. ^ Mack CL, Vanderlugt-Castaneda CL, Neville KL, Miller SD (2003). "Microglia are activated to become competent antigen presenting and effector cells in the inflammatory environment of the Theiler's virus model of multiple sclerosis". Journal of Neuroimmunology. 144 (1–2): 68–79. doi:10.1016/j.jneuroim.2003.08.032. PMID 14597100. S2CID 24384220.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  27. ^ Cristofanilli M, Rosenthal H, Cymring B, Gratch D, Pagano B, Xie B, Sadiq SA (2014). "Progressive multiple sclerosis cerebrospinal fluid induces inflammatory demyelination, axonal loss, and astrogliosis in mice". Exp Neurol. 261: 620–32. doi:10.1016/j.expneurol.2014.07.020. PMID 25111532. S2CID 21263405.
  28. ^ Prümmer, Julia K.; Stein, Veronika M.; Marti, Eliane; Lutterotti, Andreas; Jelcic, Ilijas; Schüpbach-Regula, Gertraud; Buch, Thorsten; Maiolini, Arianna (25 January 2023). "Assessment of oligoclonal bands in cerebrospinal fluid and serum of dogs with meningoencephalitis of unknown origin". PLOS ONE. 18 (1): e0280864. doi:10.1371/journal.pone.0280864. PMC 9876372. PMID 36696385.
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