Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation

FASEB Journal

Volumn 25, Issue 5, 2011, Pages 1556-1566

  Li, Lihua ^a,b   Zhang, Hua ^a,b   Varrin Doyer, Michel ^a   Zamvil, Scott S ^a   Verkman, A S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocyte; EAE; Neuromyelitis optics; Water channel

Indexed keywords

AQUAPORIN 4; CYTOKINE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ACTIVE IMMUNIZATION; ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOIMMUNE DISEASE; CELL MIGRATION; CELL SWELLING; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; IMMUNOCOMPETENT CELL; LEUKOCYTE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; WATER PERMEABILITY; WILD TYPE;

ADENOVIRIDAE; ANIMALS; AQUAPORIN 4; BLOOD-BRAIN BARRIER; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

ADENOVIRIDAE; MUS;

EID: 79955651800     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-177279     Document Type: Article

References (39)

1. Ransohoff, R. M. (2006) A mighty mouse: building a better model of multiple sclerosis. J. Clin. Invest. 116, 2313-2316
2. Korn, T., Bettelli, E., Oukka, M., and Kuchroo, V. K. (2009) IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517
3. Kroenke, M. A., Carlson, T. J., Andjelkovic, A. V., and Segal, B. M. (2008) IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 205, 1535-1541
4. Lyons, J. A., Ramsbottom, M. J., and Cross, A. H. (2002) Critical role of antigen-specific antibody in experimental autoimmune encephalomyelitis induced by recombinant myelin oligodendrocyte glycoprotein. Eur. J. Immunol. 32, 1905-1913
5. Weber, M. S., Prod'homme, T., Patarroyo, J. C., Molnarfi, N., Karnezis, T., Lehmann-Horn, K., Danilenko, D. M., Eastham-Anderson, J., Slavin, A. J., Linington, C., Bernard, C. C., Martin, F., and Zamvil, S. S. (2010) B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann. Neurol. 68, 369-383
6. Lennon, V. A., Kryzer, T. J., Pittock, S. J., Verkman, A. S., and Hinson, S. R. (2005) IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J. Exp. Med. 202, 473-477
7. Bennett, J. L., Lam, C., Kalluri, S. R., Saikali, P., Bautista, K., Dupree, C., Glogowska, M., Case, D., Antel, J. P., Owens, G. P., Gilden, D., Nessler, S., Stadelmann, C., and Hemmer, B. (2009) Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann. Neurol. 66, 617-629
8. Kinoshita, M., Nakatsuji, Y., Kimura, T., Moriya, M., Takata, K., Okuno, T., Kumanogoh, A., Kajiyama, K., Yoshikawa, H., and Sakoda, S. (2009) Neuromyelitis optica: passive transfer to rats by human immunoglobulin. Biochem. Biophys. Res. Commun. 386, 623-627
9. Saadoun, S., Waters, P., Bell, B. A., Vincent, A., Verkman, A. S., and Papadopoulos, M. C. (2010) Intra-cerebral injection of neuromyelitis optica immunoglobulin G and human complement produces neuromyelitis optica lesions in mice. Brain 133, 349-361
10. Verkman, A. S., Binder, D. K., Bloch, O., Auguste, K., and Papadopoulos, M. C. (2006) Three distinct roles of aquaporin-4 in brain function revealed by knockout mice. Biochim. Biophys. Acta 1758, 1085-1093
11. Li, L., Zhang, H., and Verkman, A. S. (2009) Greatly attenuated experimental autoimmune encephalomyelitis in aquaporin-4 knockout mice. BMC Neurosci. 10, 94
12. Manley, G. T., Fujimura, M., Ma, T., Noshita, N., Filiz, F., Bollen, A. W., Chan, P., and Verkman, A. S. (2000) Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 6, 159-163 (Pubitemid 30082359)
13. Papadopoulos, M. C., Manley, G. T., Krishna, S., and Verkman, A. S. (2004) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 18, 1291-1293 (Pubitemid 39561580)
14. Saadoun, S., Tait, M. J., Reza, A., Davies, D. C., Bell, B. A., Verkman, A. S., and Papadopoulos, M. C. (2009) AQP4 gene deletion in mice does not alter blood-brain barrier integrity or brain morphology. Neuroscience 161, 764-772
15. Yao, X., Hrabetova, S., Nicholson, C., and Manley, G. T. (2008) Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J. Neurosci. 28, 5460-5464
16. Zhang, H., and Verkman, A. S. (2010) Microfiberoptic measurements of extracellular space volume in brain and tumor slices based on fluorescent dye partitioning. Biophys. J. 99, 1284-1291
17. Papadopoulos, M. C., and Verkman, A. S. (2005) Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J. Biol. Chem. 280, 13906-13912 (Pubitemid 40517291)
18. Bloch, O., Auguste, K. I., Manley, G. T., and Verkman, A. S. (2006) Accelerated progression of kaolin-induced hydrocephalus in aquaporin-4-deficient mice. J. Cereb. Blood Flow Metab. 26, 1527-1537 (Pubitemid 44809082)
19. Auguste, K. I., Jin, S., Uchida, K., Yan, D., Manley, G. T., Papadopoulos, M. C., and Verkman, A. S. (2007) Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J. 21, 108-116 (Pubitemid 46052550)
20. Saadoun, S., Papadopoulos, M. C., Watanabe, H., Yan, D., Manley, G. T., and Verkman, A. S. (2005) Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J. Cell Sci. 118, 5691-5698 (Pubitemid 43079263)
21. Binder, D. K., Yao, X., Zador, Z., Sick, T. J., Verkman, A. S., and Manley, G. T. (2006) Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53, 631-636
22. Ma, T., Yang, B., Gillespie, A., Carlson, E. J., Epstein, C. J., and Verkman, A. S. (1997) Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. J. Clin. Invest. 100, 957-962
23. Miller, S. D., Karpus, W. J., and Davidson, T. S. (2010). Experimental autoimmune encephalomyelitis in the mouse. Curr. Protoc. Immunol. Chap. 15, unit 15-11
24. Swanson, R. A., Liu, J., Miller, J. W., Rothstein, J. D., Farrell, K., Stein, B. A., and Longuemare, M. C. (1997) Neuronal regulation of glutamate transporter subtype expression in astrocytes. J. Neurosci. 17, 932-940
25. Bartholomaus, I., Kawakami, N., Odoardi, F., Schlager, C., Miljkovic, D., Ellwart, J. W., Klinkert, W. E., Flugel-Koch, C., Issekutz, T. B., Wekerle, H., and Flugel, A. (2009) Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462, 94-98
26. Tomas-Camardiel, M., Venero, J. L., de Pablos, R. M., Rite, I., Machado, A., and Cano, J. (2004) In vivo expression of aquaporin-4 by reactive microglia. J. Neurochem. 91, 891-899 (Pubitemid 39507366)
27. Martin Mdel, P., and Monson, N. L. (2007) Potential role of humoral immunity in the pathogenesis of multiple sclerosis (MS) and experimental autoimmune encephalomyelitis (EAE). Front. Biosci. 12, 2735-2749
28. Saadoun, S., Bell, B. A., Verkman, A. S., and Papadopoulos, M. C. (2008) Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice. Brain 131, 1087-1098
29. Kimura, A., Hsu, M., Seldin, M., Verkman, A. S., Scharfman, H. E., and Binder, D. K. (2010) Protective role of aquaporin-4 water channels after contusion spinal cord injury. Ann. Neurol. 67, 794-801
30. Solenov, E., Watanabe, H., Manley, G. T., and Verkman, A. S. (2004) Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am. J. Physiol. Cell Physiol. 286, C426-C432 (Pubitemid 38146367)
31. Cho, S. J., Sattar, A. K., Jeong, E. H., Satchi, M., Cho, J. A., Dash, S., Mayes, M. S., Stromer, M. H., and Jena, B. P. (2002) Aquaporin 1 regulates GTP-induced rapid gating of water in secretory vesicles. Proc. Natl. Acad. Sci. U. S. A. 99, 4720-4724 (Pubitemid 34286051)
32. Sugiya, H., and Matsuki, M. (2006) AQPs and control of vesicle volume in secretory cells. J. Membr. Biol. 210, 155-159 (Pubitemid 44337056)
33. +-sensing fluorescent indicator. Nat. Meth. 2, 825-827
34. Li, J., Patil, R. V., and Verkman, A. S. (2002) Mildly abnormal retinal function in transgenic mice without Muller cell aquaporin- 4 water channels. Invest. Ophthalmol. Vis. Sci. 43, 573-579 (Pubitemid 34113244)
35. Li, J., and Verkman, A. S. (2001) Impaired hearing in mice lacking aquaporin-4 water channels. J. Biol. Chem. 276, 31233-31237 (Pubitemid 37384992)
36. Lu, D. C., Zhang, H., Zador, Z., and Verkman, A. S. (2008) Impaired olfaction in mice lacking aquaporin-4 water channels. FASEB J. 22, 3216-3223
37. Weinshenker, B. G., Wingerchuk, D. M., Pittock, S. J., Lucchinetti, C. F., and Lennon, V. A. (2006) NMO-IgG: a specific biomarker for neuromyelitis optica. Dis. Markers 22, 197-206
38. Roemer, S. F., Parisi, J. E., Lennon, V. A., Benarroch, E. E., Lassmann, H., Bruck, W., Mandler, R. N., Weinshenker, B. G., Pittock, S. J., Wingerchuk, D. M., and Lucchinetti, C. F. (2007) Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain 130, 194-205
39. Misu, T., Fujihara, K., Kakita, A., Konno, H., Nakamura, M., Watanabe, S., Takahashi, T., Nakashima, I., Takahashi, H., and Itoyama, Y. (2007) Loss of aquaporin 4 in lesions of neuromyelitis optica: distinction from multiple sclerosis. Brain 130, 1224-1234 (Pubitemid 47355951)