Neuromyelitis optica study model based on chronic infusion of autoantibodies in rat cerebrospinal fluid

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Marignier, R ^a,b,c   Ruiz, A ^a,b   Cavagna, S ^a,b   Nicole, A ^a   Watrin, C ^a,b   Touret, M ^a,b   Parrot, S ^a,b   Malleret, G ^a,b   Peyron, C ^a,b   Benetollo, C ^a,b   Auvergnon, N ^a,b   Vukusic, S ^a,b,c   Giraudon, P ^a,b  

^a LYON NEUROSCIENCE RESEARCH CENTER   (France)

^b UNIVERSITÉ LYON 1   (France)

^c HÔPITAL NEUROLOGIQUE   (France)

Author keywords

Animal model; Aquaporin 4; Astrocyte; Autoantibodies; Autoimmune diseases; Glutamate; Neuromyelitis optica

Indexed keywords

AQUAPORIN 4; AUTOANTIBODY; IMMUNOGLOBULIN G; MYELIN; MYELIN BASIC PROTEIN; NEUROFILAMENT PROTEIN; AQP4 PROTEIN, HUMAN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL INFILTRATION; CONTROLLED STUDY; EMBRYO; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IN VIVO STUDY; LOCOMOTION; MALE; MICROGLIA; MOTOR DYSFUNCTION; MYELOOPTIC NEUROPATHY; NONHUMAN; PROTEIN EXPRESSION; RAT; ROTAROD TEST; ANIMAL; AXON; CELL CULTURE; CEREBROSPINAL FLUID; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; MYELIN SHEATH; NEUROMYELITIS OPTICA; NEWBORN; OPTIC NERVE; PATHOLOGY; PHYSIOLOGY; SPINAL CORD; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; AQUAPORIN 4; ASTROCYTES; AXONS; CELLS, CULTURED; CEREBROSPINAL FLUID; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; HUMANS; IMMUNOGLOBULIN G; MOVEMENT DISORDERS; MYELIN BASIC PROTEIN; MYELIN SHEATH; NEUROMYELITIS OPTICA; OPTIC NERVE; RATS; SPINAL CORD;

EID: 84974528107     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0577-8     Document Type: Article

References (53)

1. Sharma R, Fischer MT, Bauer J, Felts PA, Smith KJ, Misu T, Fujihara K, Bradl M, Lassmann H. Inflammation induced by innate immunity in the central nervous system leads to primary astrocyte dysfunction followed by demyelination. Acta Neuropathol. 2010;120:223-36.
2. Takano R, Misu T, Takahashi T, Sato S, Fujihara K, Itoyama Y. Astrocytic damage is far more severe than demyelination in NMO: a clinical CSF biomarker study. Neurology. 2010;75:208-16.
3. Kuroda H, Fujihara K, Takano R, Takai Y, Takahashi T, Misu T, Nakashima I, Sato S, Itoyama Y, Aoki M. Increase of complement fragment C5a in cerebrospinal fluid during exacerbation of neuromyelitis optica. J Neuroimmunol. 2013;254:178-82.
4. Howe CL, Kaptzan T, Magana SM, Ayers-Ringler JR, LaFrance-Corey RG, Lucchinetti CF. Neuromyelitis optica IgG stimulates an immunological response in rat astrocyte cultures. Glia. 2014;62:692-708.
5. Lucchinetti CF, Guo Y, Popescu BF, Fujihara K, Itoyama Y, Misu T. The pathology of an autoimmune astrocytopathy: lessons learned from neuromyelitis optica. Brain Pathol. 2014;24:83-97.
6. Roemer SF, Parisi JE, Lennon VA, Benarroch EE, Lassmann H, Bruck W, Mandler RN, Weinshenker BG, Pittock SJ, Wingerchuk DM, Lucchinetti CF. Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain. 2007;130:1194-205.
7. Misu T, Fujihara K, Kakita A, Konno H, Nakamura M, Watanabe S, Takahashi T, Nakashima I, Takahashi H, Itoyama Y. Loss of aquaporin 4 in lesions of neuromyelitis optica: distinction from multiple sclerosis. Brain. 2007;130:1224-34.
8. Hinson SR, Pittock SJ, Lucchinetti CF, Roemer SF, Fryer JP, Kryzer TJ, Lennon VA. Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica. Neurology. 2007;69:2221-31.
9. Sabater L, Giralt A, Boronat A, Hankiewicz K, Blanco Y, Llufriu S, Alberch J, Graus F, Saiz A. Cytotoxic effect of neuromyelitis optica antibody (NMO-IgG) to astrocytes: an in vitro study. J Neuroimmunol. 2009;215:31-5.
10. Diamond B, Huerta PT, Mina-Osorio P, Kowal C, Volpe BT. Losing your nerves? Maybe it's the antibodies. Nat Rev Immunol. 2009;9:449-56.
11. Popescu BF, Lucchinetti CF. Pathology of demyelinating diseases. Annu Rev Pathol. 2012;7:185-217.
12. Vincent T, Saikali P, Cayrol R, Roth AD, Bar-Or A, Prat A, Antel JP. Functional consequences of neuromyelitis optica-IgG astrocyte interactions on blood-brain barrier permeability and granulocyte recruitment. J Immunol. 2008;181:5730-7.
13. Hinson SR, Roemer SF, Lucchinetti CF, Fryer JP, Kryzer TJ, Chamberlain JL, Howe CL, Pittock SJ, Lennon VA. Aquaporin-4-binding autoantibodies in patients with neuromyelitis optica impair glutamate transport by down-regulating EAAT2. J Exp Med. 2008;205:2473-81.
14. Hinson SR, Romero MF, Popescu BF, Lucchinetti CF, Fryer JP, Wolburg H, Fallier-Becker P, Noell S, Lennon VA. Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci U S A. 2012;109:1245-50.
15. Misu T, Hoftberger R, Fujihara K, Wimmer I, Takai Y, Nishiyama S, Nakashima I, Konno H, Bradl M, Garzuly F, et al. Presence of six different lesion types suggests diverse mechanisms of tissue injury in neuromyelitis optica. Acta Neuropathol. 2013;125:815-27.
16. Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, Glogowska M, Case D, Antel JP, Owens GP, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol. 2009;66:617-29.
17. Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, Adzemovic M, Bauer J, Berger T, Fujihara K, et al. Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol. 2009;66:630-43.
18. 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;133:349-61.
19. Ratelade J, Verkman AS. Neuromyelitis optica: aquaporin-4 based pathogenesis mechanisms and new therapies. Int J Biochem Cell Biol. 2012;44:1519-30.
20. Zhang H, Bennett JL, Verkman AS. Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann Neurol. 2011;70:943-54.
21. Geis C, Ritter C, Ruschil C, Weishaupt A, Grunewald B, Stoll G, Holmoy T, Misu T, Fujihara K, Hemmer B, et al. The intrinsic pathogenic role of autoantibodies to aquaporin 4 mediating spinal cord disease in a rat passive-transfer model. Exp Neurol. 2015;265:8-21.
22. Wingerchuk DM. Diagnosis and treatment of neuromyelitis optica. Neurologist. 2007;13:2-11.
23. Marignier R, Bernard-Valnet R, Giraudon P, Collongues N, Papeix C, Zephir H, Cavillon G, Rogemond V, Casey R, Frangoulis B, et al. Aquaporin-4 antibody-negative neuromyelitis optica: distinct assay sensitivity-dependent entity. Neurology. 2013;80:2194-200.
24. Marignier R, Nicolle A, Watrin C, Touret M, Cavagna S, Varrin-Doyer M, Cavillon G, Rogemond V, Confavreux C, Honnorat J, Giraudon P. Oligodendrocytes are damaged by neuromyelitis optica immunoglobulin G via astrocyte injury. Brain. 2010;133:2578-91.
25. Varrin-Doyer M, Nicolle A, Marignier R, Cavagna S, Benetollo C, Wattel E, Giraudon P. Human T lymphotropic virus type 1 increases T lymphocyte migration by recruiting the cytoskeleton organizer CRMP2. J Immunol. 2012;188:1222-33.
26. Touret M, Parrot S, Denoroy L, Belin MF, Didier-Bazes M. Glutamatergic alterations in the cortex of genetic absence epilepsy rats. BMC Neurosci. 2007;8:69.
27. Bert L, Favale D, Jego G, Greve P, Guilloux JP, Guiard BP, Gardier AM, Suaud-Chagny MF, Lestage P. Rapid and precise method to locate microdialysis probe implantation in the rodent brain. J Neurosci Methods. 2004;140:53-7.
28. Nolan MF, Malleret G, Lee KH, Gibbs E, Dudman JT, Santoro B, Yin D, Thompson RF, Siegelbaum SA, Kandel ER, Morozov A. The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell. 2003;115:551-64.
29. Metz GA, Whishaw IQ. Drug-induced rotation intensity in unilateral dopamine-depleted rats is not correlated with end point or qualitative measures of forelimb or hindlimb motor performance. Neuroscience. 2002;111:325-36.
30. Petzold A, Tozer DJ, Schmierer K. Axonal damage in the making: neurofilament phosphorylation, proton mobility and magnetisation transfer in multiple sclerosis normal appearing white matter. Exp Neurol. 2011;232:234-9.
31. Asavapanumas N, Ratelade J, Papadopoulos MC, Bennett JL, Levin MH, Verkman AS. Experimental mouse model of optic neuritis with inflammatory demyelination produced by passive transfer of neuromyelitis optica-immunoglobulin G. J Neuroinflammation. 2014;11:16.
32. Saji E, Arakawa M, Yanagawa K, Toyoshima Y, Yokoseki A, Okamoto K, Otsuki M, Akazawa K, Kakita A, Takahashi H, et al. Cognitive impairment and cortical degeneration in neuromyelitis optica. Ann Neurol. 2013;73:65-76.
33. Chan KH, Zhang R, Kwan JS, Guo VY, Ho PW, Ho JW, Chu AC. Aquaporin-4 autoantibodies cause asymptomatic aquaporin-4 loss and activate astrocytes in mouse. J Neuroimmunol. 2012;245:32-8.
34. Geis C. Effects of pooled human immunoglobulins in an animal model of neuromyelitis optica with chronic application of autoantibodies to aquaporin 4. Clin Exp Immunol. 2014;178 Suppl 1:130-1.
35. Planaguma J, Leypoldt F, Mannara F, Gutierrez-Cuesta J, Martin-Garcia E, Aguilar E, Titulaer MJ, Petit-Pedrol M, Jain A, Balice-Gordon R, et al. Human N-methyl D-aspartate receptor antibodies alter memory and behaviour in mice. Brain. 2015;138:94-109.
36. Jarius S, Franciotta D, Paul F, Ruprecht K, Bergamaschi R, Rommer PS, Reuss R, Probst C, Kristoferitsch W, Wandinger KP, Wildemann B. Cerebrospinal fluid antibodies to aquaporin-4 in neuromyelitis optica and related disorders: frequency, origin, and diagnostic relevance. J Neuroinflammation. 2010;7:52.
37. Dujmovic I, Mader S, Schanda K, Deisenhammer F, Stojsavljevic N, Kostic J, Berger T, Drulovic J, Reindl M. Temporal dynamics of cerebrospinal fluid anti-aquaporin-4 antibodies in patients with neuromyelitis optica spectrum disorders. J Neuroimmunol. 2011;234:124-30.
38. Nishiyama S, Ito T, Misu T, Takahashi T, Kikuchi A, Suzuki N, Jin K, Aoki M, Fujihara K, Itoyama Y. A case of NMO seropositive for aquaporin-4 antibody more than 10 years before onset. Neurology. 2009;72:1960-1.
39. Kitic M, Hochmeister S, Wimmer I, Bauer J, Misu T, Mader S, Reindl M, Fujihara K, Lassmann H, Bradl M. Intrastriatal injection of interleukin-1 beta triggers the formation of neuromyelitis optica-like lesions in NMO-IgG seropositive rats. Acta Neuropathol Commun. 2013;1:5.
40. Pohl M, Kawakami N, Kitic M, Bauer J, Martins R, Fischer MT, Machado-Santos J, Mader S, Ellwart JW, Misu T, et al. T cell-activation in neuromyelitis optica lesions plays a role in their formation. Acta Neuropathol Commun. 2013;1:85.
41. Chihara N, Aranami T, Sato W, Miyazaki Y, Miyake S, Okamoto T, Ogawa M, Toda T, Yamamura T. Interleukin 6 signaling promotes anti-aquaporin 4 autoantibody production from plasmablasts in neuromyelitis optica. Proc Natl Acad Sci U S A. 2011;108:3701-6.
42. Zekeridou A, Lennon VA. Aquaporin-4 autoimmunity. Neurol Neuroimmunol Neuroinflamm. 2015;2:e110.
43. Li YK, Wang F, Wang W, Luo Y, Wu PF, Xiao JL, Hu ZL, Jin Y, Hu G, Chen JG. Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: involvement of downregulation of glutamate transporter-1 expression. Neuropsychopharmacology. 2012;37:1867-78.
44. Talantova M, Sanz-Blasco S, Zhang X, Xia P, Akhtar MW, Okamoto S, Dziewczapolski G, Nakamura T, Cao G, Pratt AE, et al. Abeta induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci U S A. 2013;110:E2518-27.
45. De Pitta M, Volman V, Berry H, Ben-Jacob E. A tale of two stories: astrocyte regulation of synaptic depression and facilitation. PLoS Comput Biol. 2011;7:e1002293.
46. Ficker C, Rozmer K, Kato E, Ando RD, Schumann L, Krugel U, Franke H, Sperlagh B, Riedel T, Illes P. Astrocyte-neuron interaction in the substantia gelatinosa of the spinal cord dorsal horn via P2X7 receptor-mediated release of glutamate and reactive oxygen species. Glia. 2014;62:1671-86.
47. Parpura V, Verkhratsky A. Astrocytes revisited: concise historic outlook on glutamate homeostasis and signaling. Croat Med J. 2012;53:518-28.
48. Orellana JA, Stehberg J. Hemichannels: new roles in astroglial function. Front Physiol. 2014;5:193.
49. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci. 2003;23:3588-96.
50. Li T, Giaume C, Xiao L. Connexins-mediated glia networking impacts myelination and remyelination in the central nervous system. Mol Neurobiol. 2014;49:1460-71.
51. Masaki K, Suzuki SO, Matsushita T, Matsuoka T, Imamura S, Yamasaki R, Suzuki M, Suenaga T, Iwaki T, Kira J. Connexin 43 astrocytopathy linked to rapidly progressive multiple sclerosis and neuromyelitis optica. PLoS One. 2013;8:e72919.
52. Linker RA, Lee DH, Ryan S, van Dam AM, Conrad R, Bista P, Zeng W, Hronowsky X, Buko A, Chollate S, et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain. 2011;134:678-92.
53. Bruck W, Zamvil SS. Laquinimod, a once-daily oral drug in development for the treatment of relapsing-remitting multiple sclerosis. Expert Rev Clin Pharmacol. 2012;5:245-56.