NMO sera down-regulate AQP4 in human astrocyte and induce cytotoxicity independent of complement

Journal of the Neurological Sciences

Volumn 331, Issue 1-2, 2013, Pages 136-144

  Haruki, Hiroyo ^a   Sano, Yasuteru ^a   Shimizu, Fumitaka ^a   Omoto, Masatoshi ^a   Tasaki, Ayako ^a   Oishi, Mariko ^a   Koga, Michiaki ^a   Saito, Kazuyuki ^a,b   Takahashi, Toshiyuki ^c   Nakada, Tsutomu ^d   Kanda, Takashi ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

Author keywords

Aquaporin 4; Astrocyte; Blood brain barrier; Co culture; Cytokine; Endothelial cell; Neuromyelitis optica

Indexed keywords

AQUAPORIN 4; COMPLEMENTARY DNA; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; MESSENGER RNA; NEUTRALIZING ANTIBODY; RETROVIRUS VECTOR; TUMOR NECROSIS FACTOR ALPHA; VIRUS ANTIGEN;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL IMMORTALIZATION; CELL MEMBRANE; COCULTURE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOCYTOCHEMISTRY; MYELOOPTIC NEUROPATHY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIMIAN VIRUS 40; TEMPERATURE SENSITIVITY; UPREGULATION; WESTERN BLOTTING;

EID: 84882453120     PISSN: 0022510X     EISSN: 18785883     Source Type: Journal    
DOI: 10.1016/j.jns.2013.05.035     Document Type: Article

References (38)

1. Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG. Spectrum of neuromyelitis optica. Lancet Neurol 2007;6(9):805-15.
2. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, et al. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004;364(9451):2106-12.
3. 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): 473-7.
4. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci U S A 1994;91(26):13052-6.
5. Neely JD, Christensen BM, Nielsen S, Agre P. Heterotetrameric composition of aquaporin-4 water channels. Biochemistry 1999;38(34):11156-63.
6. Furman CS, Gorelick-Feldman DA, Davidson KG, Yasumura T, Neely JD, Agre P, et al. Aquaporin-4 square array assembly: opposing actions of M1 and M23 isoforms. Proc Natl Acad Sci U S A 2003;100(23):13609-14.
7. Hinson SR, Pittock SJ, Lucchinetti CF, Roemer SF, Fryer JP, Kryzer TJ, et al. Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica. Neurology 2007;69(24):2221-31.
8. Hinson SR, Roemer SF, Lucchinetti CF, Fryer JP, Kryzer TJ, Chamberlain JL, et al. Aquaporin-4-binding autoantibodies in patients with neuromyelitis optica impair glutamate transport by down-regulating EAAT2. J Exp Med 2008;205(11): 2473-81.
9. Marignier R, Nicolle A, Watrin C, Touret M, Cavagna S, Varrin-Doyer M, et al. Oligodendrocytes are damaged by neuromyelitis optica immunoglobulin G via astrocyte injury. Brain 2010;133(9):2578-91.
10. Hinson SR, Romero MF, Popescu BF, Lucchinetti CF, Fryer JP, Wolburg H, et al. Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci U S A 2012;109(4):1245-50.
11. Ratelade J, Bennett JL, Verkman AS. Evidence against cellular internalization in vivo of NMO-IgG, aquaporin-4, and excitatory amino acid transporter 2 in neuromyelitis optica. J Biol Chem 2011;286(52):45156-64.
12. Vincent T, Saikali P, Cayrol R, Roth AD, Bar-Or A, Prat A, et al. Functional consequences of neuromyelitis optica-IgG astrocyte interactions on blood-brain barrier permeability and granulocyte recruitment. J Immunol 2008;181(8):5730-7.
13. Sano Y, Kashiwamura Y, Abe M, Dieu LH, Huwyler J, Shimizu F, et al. Stable human brain microvascular endothelial cell line retaining its barrier-specific nature independent of the passage number. Clin Exp Neuroimmunol 2012;3: 1-12.
14. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006;66(10):1485-9.
15. Takahashi T, Fujihara K, Nakashima I, Misu T, Miyazawa I, Nakamura M, et al. Establishment of a new sensitive assay for anti-human aquaporin-4 antibody in neuromyelitis optica. Tohoku J Exp Med 2006;210(4):307-13.
16. Kashiwamura Y, Sano Y, Abe M, Shimizu F, Haruki H, Maeda T, et al. Hydrocortisone enhances the function of the blood-nerve barrier through the up-regulation of claudin-5. Neurochem Res 2011;36(5):849-55.
17. Tani T, Sakimura M, Tsujita T, Nakada T, TanakaM, Nishizawa M, et al. Identification of binding sites for anti-aquaporin 4 antibodies in patientswith neuromyelitis optica. J Neuroimmunol 2009;211(1-2):110-3.
18. Tetsuka K, Hosoya KI, Ohtsuki S, Takanaga H, Yanai N, Ueda M, et al. Acidic amino acid transport characteristics of a newly developed conditionally immortalized rat type 2 astrocyte cell line (TR-AST). Cell Struct Funct 2001;26(4):197-203.
19. Terasaki T, Hosoya K. Conditionally immortalized cell lines as a new in vitro model for the study of barrier functions. Biol Pharm Bull 2001;24(2):111-8.
20. Wang D, Owler BK. Expression of AQP1 and AQP4 in paediatric brain tumors. J Clin Neurosci 2011;18(1):122-7.
21. Ye L, Martin TA, Parr C, Harrison GM, Mansel RE, Jiang WG. Biphasic effects of 17-beta-estradiol on expression of occludin and transendothelial resistance and paracellular permeability in human vascular endothelial cells. J Cell Physiol 2003;196(2):362-9.
22. Zhang ZL, Liu ZS, Sun Q. Expression of angiopoietins, Tie2 and vascular endothelial growth factor in angiogenesis and progression of hepatocellular carcinoma. World J Gastroenterol 2006;12(26):4241-5.
23. Tsao CW, Lin YS, Chen CC, Bai CH, Wu SR. Cytokines and serotonin transporter in patients with major depression. Prog Neuropsychopharmacol Biol Psychiatry 2006;30(5):899-905.
24. León AJ, Gómez E, Garrote JA, Bernardo D, Barrera A, Marcos JL, et al. High levels of proinflammatory cytokines, but notmarkers of tissue injury, in unaffected intestinal areas from patients with IBD. Mediators Inflamm 2009;2009:1-10.
25. Wolburg H, Wolburg-Buchholz K, Fallier-Becker P, Noell S, Mack AF. Structure and functions of aquaporin-4-based orthogonal arrays of particles. Int Rev Cell Mol Biol 2011;287:1-41.
26. Crane JM, Verkman AS. Determinants of aquaporin-4 assembly in orthogonal arrays revealed by live-cell single-molecule fluorescence imaging. J Cell Sci 2009;122(Pt. 6): 813-21.
27. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME. Syntrophin-dependent expression and localization of aquaporin-4 water channel protein. Proc Natl Acad Sci U S A 2001;98(24):14108-13.
28. Shimizu F, Sano Y, Takahashi T, Haruki H, Saito K, Koga M, et al. Sera from neuromyelitis optica patients disrupt the blood-brain barrier. J Neurol Neurosurg Psychiatry 2012;83(3):288-97.
29. Kinoshita M, Nakatsuji Y, Moriya M, Okuno T, Kumanogoh A, Nakano M, et al. Astrocytic necrosis is induced by anti-aquaporin-4 antibody-positive serum. Neuroreport 2009;20(5):508-12.
30. Sabater L, Giralt A, Boronat A, Hankiewicz K, Blanco Y, Llufriu S, et al. Cytotoxic effect of neuromyelitis optica antibody (NMO-IgG) to astrocytes: an in vitro study. J Neuroimmunol 2009;215(1-2):31-5.
31. Crane JM, LamC, 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):16516-24.
32. van Neerven S, Nemes A, Imholz P, Regen T, Denecke B, Johann S, et al. Inflammatory cytokine release of astrocytes in vitro is reduced by all-trans retinoic acid. J Neuroimmunol 2010;229(1-2):169-79.
33. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, McCrea E, et al. TLR signaling tailors innate immune responses in human microglia and astrocytes. J Immunol 2005;175(7):4320-30.
34. Park C, Lee S, Cho IH, Lee HK, Kim D, Choi SY, et al. TLR3-mediated signal induces proinflammatory cytokine and chemokine gene expression in astrocytes: differential signaling mechanisms of TLR3-induced IP-10 and IL-8 gene expression. Glia 2006;53(3):248-56.
35. Uzawa A, Mori M, Arai K, Sato Y, Hayakawa S, Masuda S, et al. Cytokine and chemokine profiles in neuromyelitis optica: significance of interleukin-6. Mult Scler 2010;16(12):1443-52.
36. Zhang H, Bennett JL, Verkman AS. Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann Neurol 2011;70(6): 943-54.
37. ZengXN, Sun XL, Gao L, Fan Y, Ding JH, Hu G. Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol Cell Neurosci 2007;34(1): 34-9.
38. Misu T, Fujihara K, Nakamura M, Murakami K, Endo M, Konno H, et al. Loss of aquaporin-4 in active perivascular lesions in neuromyelitis optica: a case report. Tohoku J Exp Med 2006;209(3):269-75.