Neuromyelitis optica pathology in rats following intraperitoneal injection of NMO-IgG and intracerebral needle injury

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Asavapanumas, Nithi ^a   Verkman, AS ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aquaporin 4; Astrocyte; Complement; Neuroinflammation; NMO

Indexed keywords

ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; AQP4 PROTEIN, HUMAN; AQUAPORIN 4; CALCIUM BINDING PROTEIN; COMPLEMENT MEMBRANE ATTACK COMPLEX; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN G; LEUKOCYTE ANTIGEN; LY ANTIGEN; MYELIN BASIC PROTEIN;

ANIMAL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; BLOOD; CHO CELL LINE; COMPLICATION; CRICETULUS; DISEASE MODEL; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; LEWIS RAT; METABOLISM; MYELOOPTIC NEUROPATHY; PATHOLOGY; RAT; TIME;

ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD; ANTIGENS, LY; AQUAPORIN 4; CALCIUM-BINDING PROTEINS; CHO CELLS; COMPLEMENT MEMBRANE ATTACK COMPLEX; CRICETULUS; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMMUNOGLOBULIN G; INJECTIONS, INTRAPERITONEAL; MICROFILAMENT PROTEINS; MYELIN BASIC PROTEIN; NEUROMYELITIS OPTICA; RATS; RATS, INBRED LEW; TIME FACTORS; TRANSFECTION;

EID: 84921689305     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-2-48     Document Type: Article

References (49)

1. Jacob A, McKeon A, Nakashima I, Sato DK, Elsone L, Fujihara K, De Seze J: Current concept of neuromyelitis optica (NMO) and NMO spectrum disorders. J Neurol Neurosurg Psychiatry 2013, 84(8):922-930. doi:10.1136/jnnp-2012-302310
2. Jarius S, Paul F, Franciotta D, Waters P, Zipp F, Hohlfeld R, Vincent A, Wildemann B: Mechanisms of disease: aquaporin-4 antibodies in neuromyelitis optica. Nat Clin Pract Neurol 2008, 4(4):202-214. doi:10.1038/ncpneuro0764
3. Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG: The spectrum of neuromyelitis optica. Lancet Neurol 2007, 6(9):805-815. doi:S1474-4422(07)70216-8 10.1016/S1474-4422(07)70216-8
4. Jarius S, Wildemann B: AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat Rev Neurol 2010, 6(7):383-392. doi:10.1038/nrneurol.2010.72 10.1038/nrneurol.2010.72
5. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR: IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 2005, 202(4):473-477. doi:jem.20050304 10.1084/jem.20050304
6. Papadopoulos MC, Verkman AS: Aquaporin water channels in the nervous system. Nat Rev Neurosci 2013, 14(4):265-277. doi:10.1038/nrn3468 10.1038/nrn3468
7. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP: Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 1997, 17(1):171-180.
8. Frigeri A, Gropper MA, Turck CW, Verkman AS: Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc Natl Acad Sci U S A 1995, 92(10):4328-4331. 10.1073/pnas.92.10.4328
9. Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, Verkman AS: Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci 1995, 108(Pt 9):2993-3002.
10. Papadopoulos MC, Verkman AS: Aquaporin 4 and neuromyelitis optica. Lancet Neurol 2012, 11(6):535-544. doi:10.1016/S1474-4422(12)70133-3 10.1016/S1474-4422(12)70133-3
11. 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(Pt 5):1194-1205. doi:awl371
12. Hengstman GJ, Wesseling P, Frenken CW, Jongen PJ: Neuromyelitis optica with clinical and histopathological involvement of the brain. Mult Scler 2007, 13(5):679-682. doi:1352458506070145 10.1177/1352458506070145
13. Kira J: Autoimmunity in neuromyelitis optica and opticospinal multiple sclerosis: astrocytopathy as a common denominator in demyelinating disorders. J Neurol Sci 2011, 311(1-2):69-77. doi:10.1016/j.jns.2011.08.043
14. 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(Pt 5):1224-1234. doi:awm047
15. Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, RansohoffRM, Trebst C, Weinshenker B, Wingerchuk D, Parisi JE, Lassmann H: A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 2002, 125(Pt 7):1450-1461.
16. Ratelade J, Asavapanumas N, Ritchie AM, Wemlinger S, Bennett JL, Verkman AS: Involvement of antibody-dependent cell-mediated cytotoxicity in inflammatory demyelination in a mouse model of neuromyelitis optica. Acta Neuropathol 2013, 126(5):699-709. doi:10.1007/s00401-013-1172-z 10.1007/s00401-013-1172-z
17. Pohl M, Kawakami N, Kitic M, Bauer J, Martins R, Fischer MT, Machado-Santos J, Mader S, Ellwart JW, Misu T, Fujihara K, Wekerle H, Reindl M, Lassmann H, Bradl M: T cell-activation in neuromyelitis optica lesions plays a role in their formation. Acta Neuropathol Commun 2013, 1(1):85. doi:10.1186/2051-5960-1-85 10.1186/2051-5960-1-85
18. 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(1):5. doi:10.1186/2051-5960-1-5 10.1186/2051-5960-1-5
19. 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):349-361. doi:10.1093/brain/awp309
20. Jones MV, Collongues N, De Seze J, Kinoshita M, Nakatsuji Y, Levy M: Review of animal models of neuromyelitis optica. Mult Scler Relat Disord 2012, 1(4):174-179. doi:10.1016/j.msard.2012.06.003 10.1016/j.msard.2012.06.003
21. Bradl M, Lassmann H: Experimental models of neuromyelitis optica. Brain Pathol 2014, 24(1):74-82. doi:10.1111/bpa.12098 10.1111/bpa.12098
22. Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, Glogowska M, Case D, Antel JP, Owens GP, Gilden D, Nessler S, Stadelmann C, Hemmer B: Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol 2009, 66(5):617-629. doi:10.1002/ana.21802 10.1002/ana.21802
23. Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, Adzemovic M, Bauer J, Berger T, Fujihara K, Itoyama Y, Lassmann H: Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann Neurol 2009, 66(5):630-643. doi:10.1002/ana.21837 10.1002/ana.21837
24. Kinoshita M, Nakatsuji Y, Kimura T, Moriya M, Takata K, Okuno T, Kumanogoh A, Kajiyama K, Yoshikawa H, Sakoda S: Neuromyelitis optica: passive transfer to rats by human immunoglobulin. Biochem Biophys Res Commun 2009, 386(4):623-627. doi:10.1016/j.bbrc.2009.06.085 10.1016/j.bbrc.2009.06.085
25. Kinoshita M, Nakatsuji Y, Kimura T, Moriya M, Takata K, Okuno T, Kumanogoh A, Kajiyama K, Yoshikawa H, Sakoda S: Anti-aquaporin-4 antibody induces astrocytic cytotoxicity in the absence of CNS antigen-specific T cells. Biochem Biophys Res Commun 2010, 394(1):205-210. doi:10.1016/j.bbrc.2010.02.157 10.1016/j.bbrc.2010.02.157
26. Ratelade J, Zhang H, Saadoun S, Bennett JL, Papadopoulos MC, Verkman AS: Neuromyelitis optica IgG and natural killer cells produce NMO lesions in mice without myelin loss. Acta Neuropathol 2012, 123(6):861-872. doi:10.1007/s00401-012-0986-4 10.1007/s00401-012-0986-4
27. Saadoun S, Waters P, MacDonald C, Bell BA, Vincent A, Verkman AS, Papadopoulos MC: Neutrophil protease inhibition reduces neuromyelitis optica-immunoglobulin G-induced damage in mouse brain. Ann Neurol 2012, 71(3):323-333. doi:10.1002/ana.22686 10.1002/ana.22686
28. Zhang H, Bennett JL, Verkman AS: Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann Neurol 2011, 70(6):943-954. doi:10.1002/ana.22551 10.1002/ana.22551
29. Zhang H, Verkman AS: Eosinophil pathogenicity mechanisms and therapeutics in neuromyelitis optica. J Clin Invest 2013, 123(5):2306-2316. doi:10.1172/JCI67554 10.1172/JCI67554
30. 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. doi:10.1186/1742-2094-11-16 10.1186/1742-2094-11-16
31. Zhang H, Verkman AS: Longitudinally extensive NMO spinal cord pathology produced by passive transfer of NMO-IgG in mice lacking complement inhibitor CD59. J Autoimmun 2014. doi: 10.1016/j.jaut.2014.02.011. [Epub ahead of print]
32. Bergman I, Basse PH, Barmada MA, Griffin JA, Cheung NK: Comparison of in vitro antibody-targeted cytotoxicity using mouse, rat and human effectors. Cancer Immunol Immunother 2000., 49:
33. Asavapanumas N, Ratelade J, Verkman AS: Unique neuromyelitis optica pathology produced in naive rats by intracerebral administration of NMO-IgG. Acta Neuropathol 2014, 127(4):539-551. doi:10.1007/s00401-013-1204-8 10.1007/s00401-013-1204-8
34. Tradtrantip L, Zhang H, Saadoun S, Phuan PW, Lam C, Papadopoulos MC, Bennett JL, Verkman AS: Anti-aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica. Ann Neurol 2012, 71(3):314-322. doi:10.1002/ana.22657 10.1002/ana.22657
35. Tradtrantip L, Ratelade J, Zhang H, Verkman AS: Enzymatic deglycosylation converts pathogenic neuromyelitis optica anti-aquaporin-4 immunoglobulin G into therapeutic antibody. Ann Neurol 2013, 73(1):77-85. doi:10.1002/ana.23741 10.1002/ana.23741
36. Tradtrantip L, Asavapanumas N, Verkman AS: Therapeutic cleavage of anti-aquaporin-4 autoantibody in neuromyelitis optica by an IgG-selective proteinase. Mol Pharmacol 2013, 83(6):1268-1275. doi:10.1124/mol.113.086470 10.1124/mol.113.086470
37. Phuan PW, Zhang H, Asavapanumas N, Leviten M, Rosenthal A, Tradtrantip L, Verkman AS: C1q-targeted monoclonal antibody prevents complement-dependent cytotoxicity and neuropathology in in vitro and mouse models of neuromyelitis optica. Acta Neuropathol 2013, 125(6):829-840. doi:10.1007/s00401-013-1128-3 10.1007/s00401-013-1128-3
38. Pittock SJ, Lennon VA, McKeon A, Mandrekar J, Weinshenker BG, Lucchinetti CF, O'Toole O, Wingerchuk DM: Eculizumab in AQP4-IgG-positive relapsing neuromyelitis optica spectrum disorders: an open-label pilot study. Lancet Neurol 2013, 12(6):554-562. doi:10.1016/S1474-4422(13)70076-0 10.1016/S1474-4422(13)70076-0
39. Crane JM, Lam C, Rossi A, Gupta T, Bennett JL, Verkman AS: Binding affinity and specificity of neuromyelitis optica autoantibodies to aquaporin-4 M1/M23 isoforms and orthogonal arrays. J Biol Chem 2011, 286(18):16516-16524. doi:10.1074/jbc. M111.227298 10.1074/jbc. M111.227298
40. Phuan PW, Ratelade J, Rossi A, Tradtrantip L, Verkman AS: Complement-dependent cytotoxicity in neuromyelitis optica requires aquaporin-4 protein assembly in orthogonal arrays. J Biol Chem 2012, 287(17):13829-13839. doi:10.1074/jbc. M112.344325 10.1074/jbc. M112.344325
41. Levin ME, Jin JG, Ji RR, Tong J, Pomonis JD, Lavery DJ, Miller SW, Chiang LW: Complement activation in the peripheral nervous system following the spinal nerve ligation model of neuropathic pain. Pain 2008, 137(1):182-201. doi:S0304-3959(07)00672-0 10.1016/j.pain.2007.11.005
42. Vogel CW, Fritzinger DC: Cobra venom factor: Structure, function, and humanization for therapeutic complement depletion. Toxicon 2010, 56(7):1198-1222. doi:10.1016/j.toxicon.2010.04.007 10.1016/j.toxicon.2010.04.007
43. Ratelade J, Bennett JL, Verkman AS: Intravenous neuromyelitis optica autoantibody in mice targets aquaporin-4 in peripheral organs and area postrema. PLoS One 2011, 6(11):e27412. doi:10.1371/journal.pone.0027412 10.1371/journal.pone.0027412
44. Singhrao SK, Neal JW, Rushmere NK, Morgan BP, Gasque P: Differential expression of individual complement regulators in the brain and choroid plexus. Lab Invest 1999, 79(10):1247-1259.
45. Baalasubramanian S, Harris CL, Donev RM, Mizuno M, Omidvar N, Song WC, Morgan BP: CD59a is the primary regulator of membrane attack complex assembly in the mouse. J Immunol 2004, 173(6):3684-3692. doi:173/6/3684 10.4049/jimmunol.173.6.3684
46. Van Beek J, Van Meurs M, t Hart BA, Brok HP, Neal JW, Chatagner A, Harris CL, Omidvar N, Morgan BP, Laman JD, Gasque P: Decay-accelerating factor (CD55) is expressed by neurons in response to chronic but not acute autoimmune central nervous system inflammation associated with complement activation. J Immunol 2005, 174(4):2353-2365. doi:174/4/2353 10.4049/jimmunol.174.4.2353
47. Gelderman KA, Zijlmans HJ, Vonk MJ, Gorter A: CD55 expression patterns on intestinal neuronal tissue are divergent from the brain. Gut 2004, 53(4):507-513. 10.1136/gut.2003.026773
48. 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(22):1960-1961. doi:10.1212/WNL.0b013e3181a82621 10.1212/WNL.0b013e3181a82621
49. Tradtrantip L, Zhang H, Anderson MO, Saadoun S, Phuan PW, Papadopoulos MC, Bennett JL, Verkman AS: Small-molecule inhibitors of NMO-IgG binding to aquaporin-4 reduce astrocyte cytotoxicity in neuromyelitis optica. FASEB J 2012, 26(5):2197-2208. doi:10.1096/fj.11-201608 10.1096/fj.11-201608