Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis

Brain

Volumn 130, Issue 5, 2007, Pages 1194-1205

  Roemer, Shanu F ^a   Parisi, Joseph E ^a   Lennon, Vanda A ^a   Benarroch, Eduardo E ^a   Lassmann, Hans ^b   Bruck, Wolfgang ^c   Mandler, Raul N ^d   Weinshenker, Brian G ^a   Pittock, Sean J ^a   Wingerchuk, Dean M ^e   Lucchinetti, Claudia F ^a  

^a MAYO CLINIC   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c MAYO CLINIC   (United States)

^d Medical University of Vienna   (Austria)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Aquaporin 4; Astrocyte; Blood brain barrier; Demyelination; Multiple sclerosis; Neuromyelitis optica

Indexed keywords

AQUAPORIN 4; AUTOANTIBODY; IMMUNOGLOBULIN G;

ADULT; AGED; ANTIGEN ANTIBODY COMPLEX; ARTICLE; BRAIN INFARCTION; CENTRAL NERVOUS SYSTEM; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROL GROUP; CONTROLLED STUDY; DEMYELINATION; DIFFERENTIAL DIAGNOSIS; EDEMA; FEMALE; HUMAN; IMMUNOREACTIVITY; INFLAMMATION; MALE; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPINAL CORD; TISSUE NECROSIS; ADOLESCENT; ASTROCYTE; BRAIN; CASE CONTROL STUDY; DISEASE COURSE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; MACROPHAGE; MIDDLE AGED; MYELIN SHEATH; OLIGODENDROGLIA;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AQUAPORIN 4; ASTROCYTES; AUTOANTIBODIES; BRAIN; CASE-CONTROL STUDIES; DIAGNOSIS, DIFFERENTIAL; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; MYELIN SHEATH; NEUROMYELITIS OPTICA; OLIGODENDROGLIA; OPTIC NERVE; SPINAL CORD;

EID: 34249650146     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awl371     Document Type: Article

References (37)

1. Amiry-Moghaddam M, Ottersen OP. The molecular basis of water transport in the brain. [Review]. Nat Rev Neurosci 2003; 4: 991-1001.
2. Aoki K, Uchihara T, Duyckaerts C, Nakamura A, Hauw JJ, Wakayama Y. Enhanced expression of aquaporin-4 in human brain with inflammatory diseases. Acta Neuropathol (Berl) 2005; 110: 281-8.
3. Aoki K, Uchihara T, Tsuchiya K, Nakamura A, Ikeda K, Wakayama Y. Enhanced expression of aquaporin-4 in human brain with infarction. Acta Neuropathol (Berl) 2003; 106: 121-4.
4. Brimijoin S, Balm M, Hammond P, Lennon VA. Selective complexing of acetylcholinesterase in brain by intravenously administered monoclonal antibody. J Neurochem 1990; 54: 236-41.
5. Bruck W, Porada P, Poser S, Rieckmann P, Hanefeld F, Kretzschmar HA, et al. Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann Neurol 1995; 38: 788-96.
6. Bushong EA, Martone ME, Jones YZ, Ellisman MH. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 2002; 22: 183-92.
7. 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 USA 1995; 92: 4328-31.
8. Goren O, Adorjan I, Kalman M. Heterogeneous occurrence of aquaporin-4 in the ependyma and in the circumventricular organs in rat and chicken. Anat Embryol (Berl) 2006; 211: 155-72.
9. Jung J, Bhat R, Preston G, Guggino W, Baraban J, Agre P. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA 1994; 91: 13052-6.
10. Keegan M, Pineda AA, McClelland RL, Darby CH, Rodriguez M, Weinshenker BG. Plasma exchange for severe attacks of CNS demyelination: predictors of response. Neurology 2002; 58: 143-6.
11. Lennon VA. Myasthenia gravis: a prototype immunopharmacological disease. In: Miescher PA, editor. The Menarini series on immunopathology. Vol. . Basel: Schwabe & Co; 1978. p. 178-98.
12. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. IgG marker of optic-spinal MS binds to the aquaporin-4 water channel. J Exp Med 2005; 202: 473-7.
13. Lennon VA, Lambert EH, Griesmann GE. Membrane array of acetylcholine receptors determines complement-dependent mononuclear phagocytosis in experimental myasthenia gravis. Fed Proc 1984; 43: 1764.
14. 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: 2106-12.
15. Lucchinetti C, Parisi J, Bruck W. The pathology of multiple sclerosis. Neurol Clin 2005; 23: 77-105.
16. Lucchinetti CF, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol 2000; 47: 707-17.
17. Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, Ransohoff RM, et al. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 2002; 125: 1450-61.
18. Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, et al. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 2000; 6: 159-63.
19. Misu T, Fujihara K, Nakamura M, Murakami K, Endo M, Konno H, et al. Loss of aquaporin-4 in active perivascular neuromyelitis optica: a case report. Tohoku J Exp Med 2006; 209: 269-75.
20. Misu T, Fujihara K, Nakashima I, Sato S, Itoyama Y. Intractable hiccup and nausea with periaqueductal lesions in neuromyelitis optica. Neurology 2005; 65: 1479-82.
21. Nicchia GP, Nico B, Camassa LMA, Mola MG, Loh N, Dermietzel R, et al. The role of aquaporin-4 in blood-brain barrier development and integrity: studies in animal and cell culture models. Neuroscience 2004; 129: 935-45.
22. 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: 171-80.
23. O'Riordan JI, Gallagher HL, Thompson AJ, Howard RS, Kingsley DP, Thompson EJ, et al. Clinical, CSF, and MRI findings in Devic's neuromyelitis optica. J Neurol Neurosurg Psychiatry 1996; 60: 382-7.
24. Pittock SJ, Weinshenker BG, Lucchinetti CF, Wingerchuk DM, Corboy JR, Lennon VA. Neuromyelitis optica brain lesions localized to sites of high aquaporin-4 expression. Arch Neurol 2006a; 63: 964-8.
25. Pittock SJ, Lennon VA, Krecke K, Wingerchuk DM, Lucchinetti CF, Weinshenker BG. Brain abnormalities in neuromyelitis optica. Arch Neurol 2006b; 63: 390-6.
26. Saadoun S, Papdopoulos MC, Davies DC, Krishna S, Bell BA. Aquaporin-4 expression is increased in oedematous human brain tumors. J Neurol Neurosurg Psychiatry 2002; 72: 262-5.
27. Simard M, Arcuino G, Takano T, Liu Q, Nedergaard M. Signaling at the gliovascular interface. J Neurosci 2003; 23: 9254-62.
28. Simard M, Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 2004; 129: 877-96.
29. Taniguchi M, Yamashita T, Kumura E, Tamatani M, Kobayashi A, Yokawa T, et al. Induction of aquaporin-4 water channel mRNA after focal ischemia in rat. Brain Res Mol Brain Res 2000; 78: 131-7.
30. Vajda Z, Pedersen M, Fuchtbauer EM, Wertz K, Stodkilde-Jorgensen H, Sulyok E, et al. Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice. Proc Natl Acad Sci USA 2002; 99: 13131-6.
31. Vass K, Lassmann H, Wekerle H, Wisniewski HM. The distribution of Ia antigen in the lesions of rat acute experimental allergic encephalomyelitis. Acta Neuropathol (Berl) 1986; 70: 149-60.
32. Venero JL, Vizuete ML, Ilundain AA, Machado A, Echevarra M, Cano J. Detailed localization of aquaporin-4 messenger RNA in the CNS; preferential expression in periventricular organs. Neuroscience 1999; 94: 239-50.
33. Venero JL, Vizuete ML, Machado A, Cano J. Aquaporins in the central nervous system. [Review]. Prog Neurobiol 2001; 63: 321-36.
34. Vernant JC, Cabre P, Smadja D, Merle H, Caubarrere I, Mikol J, et al. Recurrent optic neuromyelitis with endocrinopathies: a new syndrome. Neurology 1997; 48: 58-64.
35. Warth A, Mittlebronn M, Wolburg H. Redistribution of the water channel protein aquaporin-4 and the K+ channel protein Kir4.1 differs in low and high grade human brain tumors. Acta Neuropathol (Berl) 2005; 109: 418-26.
36. Wingerchuk DM, Hogancamp WF, O'Brien PC, Weinshenker BG. The clinical course of neuromyelitis optica (Devic's syndrome). Neurology 1999; 53: 1107-14.
37. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006; 66: 1485-9.