Small-molecule inhibitors of NMO-IgG binding to aquaporin-4 reduce astrocyte cytotoxicity in neuromyelitis optica

FASEB Journal

Volumn 26, Issue 5, 2012, Pages 2197-2208

  Tradtrantip, Lukmanee ^a,b   Zhang, Hua ^a,b   Anderson, Marc O ^c   Saadoun, Samira ^d   Phuan, Puay Wah ^a,b   Papadopoulos, Marios C ^d   Bennett, Jeffrey L ^e,f   Verkman, A S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO STATE UNIVERSITY   (United States)

^d ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF COLORADO   (United States)

Author keywords

Autoantibody; Devic's disease; Drug discovery; Water channel

Indexed keywords

ALKALOID; ANTIVIRUS AGENT; AQUAPORIN 4; ARBIDOL; AUTOANTIBODY; BERBAMINE; FLAVONOID; GANGLIOSIDE GD3; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; NATURAL PRODUCT; TAMARIXETIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BINDING SITE; CELL MEDIATED CYTOTOXICITY; CHO CELL; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; CYTOTOXICITY; DISEASE SEVERITY; EX VIVO STUDY; FLUORESCENCE MICROSCOPY; HIGH THROUGHPUT SCREENING; MOLECULAR DOCKING; MOUSE; MYELOOPTIC NEUROPATHY; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; SPINAL CORD; THYROID CELL; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY;

ANIMALS; AQUAPORIN 4; ASTROCYTES; IMMUNOGLOBULIN G; MICE; NEUROMYELITIS OPTICA; RATS; RATS, INBRED F344; SMALL MOLECULE LIBRARIES;

MUS; RATTUS;

EID: 84860898728     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-201608     Document Type: Article

References (52)

1. Wingerchuk, D. M., Lennon, V. A., Lucchinetti, C. F., Pittock, S. J., and Weinshenker, B. G. (2007) The spectrum of neuromyelitis optica. Lancet Neurol. 6, 805-815 (Pubitemid 47238676)
2. 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 (Pubitemid 41186945)
3. Nielsen, S., Nagelhus, E. A., Amiry-Moghaddam, M., Bourque, C., Agre, P., and Ottersen, O. P. (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17, 171-180 (Pubitemid 27008860)
4. Verkman, A. S., Ratelade, J., Rossi, A., Zhang, H., and Tradtrantip, L. (2011) Aquaporin-4: orthogonal array assembly, CNS functions, and role in neuromyelitis optica. Acta Pharmacol. Sin. 32, 702-710
5. 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)
6. 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)
7. 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
8. +-sensing fluorescent indicator. Nat. Methods 2, 825-827
9. 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)
10. 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)
11. Li, L., Zhang, H., Varrin-Doyer, M., Zamvil, S. S., and Verkman, A. S. (2011) Proinflammatory role of aquaporin-4 in autoimmune neuroinflammation. FASEB J. 25, 1556-1566
12. Cree, B. (2008) Neuromyelitis optica: diagnosis, pathogenesis, and treatment. Curr. Neurol. Neurosci. Rep. 8, 427-433
13. Jarius, S., Paul, F., Franciotta, D., Waters, P., Zipp, F., Hohlfeld, R., Vincent, A., and Wildemann, B. (2008) Mechanisms of disease: aquaporin-4 antibodies in neuromyelitis optica. Nat. Clin. Pract. Neurol. 4, 202-214 (Pubitemid 351516748)
14. 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
15. Bradl, M., Misu, T., Takahashi, T., Watanabe, M., Mader, S., Reindl, M., Adzemovic, M., Bauer, J., Berger, T., Fujihara, K., Itoyama, Y., and Lassmann, H. (2009) Neuromyelitis optica: pathogenicity of patient immunoglobulin in vivo. Ann. Neurol. 66, 630-643
16. 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
17. Saadoun, S., MacDonald, C., Waters, P., Bell, B. A., Vincent, A., Verkman, A. S., and Papadopoulos, M. C. (2012) Neutrophil protease inhibition greatly reduces NMO-IgG-induced inflammation and myelin loss in mouse brain. [E-pub ahead of print] Ann. Neurol. doi: 10.1002/ana.22686
18. 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
19. Zhang, H., Bennett, J. L., and Verkman, A. S. (2011) Ex vivo spinal cord slice model of neuromyelitis optica reveals novel immunopathogenic mechanisms. Ann. Neurol. 70, 943-954
20. Hinson, S. R., Pittock, S. J., Lucchinetti, C. F., Roemer, S. F., Fryer, J. P., Kryzer, T. J., and Lennon, V. A. (2007) Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica. Neurology 69, 2221-2231 (Pubitemid 350294677)
21. Marignier, R., Nicolle, A., Watrin, C., Touret, M., Cavagna, S., Varrin-Doyer, M., Cavillon, G., Rogemond, V., Confavreux, C., Honnorat, J., and Giraudon, P. (2010) Oligodendrocytes are damaged by neuromyelitis optica immunoglobulin G via astrocyte injury. Brain 133, 2578-2591
22. Parratt, J. D., and Prineas, J. W. (2010) Neuromyelitis optica: a demyelinating disease characterized by acute destruction and regeneration of perivascular astrocytes. Mult. Scler. 16, 1156-1172
23. Tradtrantip, L., Zhang, H., Saadoun, S., Phuan, P., Lam, C., Papadopoulos, M. C., Bennett, J. L., and Verkman, A. S. (2012) Anti-aquaporin-4 monoclonal antibody blocker therapy for neuromyelitis optica. [E-pub ahead of print] Ann. Neurol. doi: 10.1002/ana.22657
24. Crane, J. M., Lam, C., Rossi, A., Gupta, T., Bennett, J. L., and Verkman, A. S. (2011) Binding affinity and specificity of neuromyelitis optica autoantibodies to aquaporin-4 M1/M23 isoforms and orthogonal arrays. J. Biol. Chem. 286, 16516-16524
25. Wingerchuk, D. M., Lennon, V. A., Pittock, S. J., Lucchinetti, C. F., and Weinshenker, B. G. (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66, 1485-1489 (Pubitemid 43958540)
26. Crane, J. M., Bennett, J. L., and Verkman, A. S. (2009) Live cell analysis of aquaporin-4 M1/M23 interactions and regulated orthogonal array assembly in glial cells. J. Biol. Chem. 284, 35850-35860
27. Tajima, M., Crane, J. M., and Verkman, A. S. (2010) Aquaporin-4 (AQP4) associations and array dynamics probed by photobleaching and single-molecule analysis of green fluorescent protein-AQP4 chimeras. J. Biol. Chem. 285, 8163-8170
28. Yang, B., Zhang, H., and Verkman, A. S. (2008) Lack of aquaporin-4 water transport inhibition by antiepileptics and arylsulfonamides. Bioorg. Med. Chem. 16, 7489-7493
29. 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 (Pubitemid 27386279)
30. Ho, J. D., Yeh, R., Sandstrom, A., Chorny, I., Harries, W. E., Robbins, R. A., Miercke, L. J., and Stroud, R. M. (2009) Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance. Proc. Natl. Acad. Sci. U. S. A. 106, 7437-7442
31. Jin, B. J., Rossi, A., and Verkman, A. S. (2011) Model of aquaporin-4 supramolecular assembly in orthogonal arrays based on heterotetrameric association of M1-M23 isoforms. Biophys. J. 100, 2936-2945
32. Mader, S., Lutterotti, A., Di Pauli, F., Kuenz, B., Schanda, K., Aboul-Enein, F., Khalil, M., Storch, M. K., Jarius, S., Kristoferitsch, W., Berger, T., and Reindl, M. (2010) Patterns of antibody binding to aquaporin-4 isoforms in neuromyelitis optica. PLoS One 5, e10455
33. Wolburg, H., Wolburg-Buchholz, K., Fallier-Becker, P., Noell, S., and Mack, A. F. (2011) Structure and functions of aquaporin-4-based orthogonal arrays of particles. Int. Rev. Cell Mol. Biol. 287, 1-41
34. Jarius, S., and Wildemann, B. (2010) AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat. Rev. Neurol. 6, 383-392
35. Pukel, C. S., Lloyd, K. O., Travassos, L. R., Dippold, W. G., Oettgen, H. F., and Old, L.J. (1982) GD3, a prominent ganglioside of human melanoma. J. Exp. Med. 155, 1133-1147
36. Crane, J. M., and Verkman, A. S. (2009) Determinants of aquaporin-4 assembly in orthogonal arrays revealed by live-cell single-molecule fluorescence imaging. J. Cell Sci. 122, 813-821
37. Ren, Y., Lu, L., Guo, T. B., Qiu, J., Yang, Y., Liu, A., and Zhang, J. Z. (2008) Novel immunomodulatory properties of berbamine through selective down-regulation of STAT4 and action of IFN-gamma in experimental autoimmune encephalomyelitis. J. Immunol. 181, 1491-1498
38. Li, Q. L., Xu, Y. H., Zhou, Z. S., Chen, X. W., Huang, X. G., Chen, S. L., and Zhan, C. X. (1981) The therapeutic effect of tetrandrine on silicosis. Chin. J. Tuberc. Resp. Dis. 4, 321-328
39. Liu, C. X., Xiao, P. G., and Liu, G. S. (1991) Studies on plant resources, pharmacology and clinical treatment with berbamine. Phytother. Res. 5, 228-230
40. Wei, Y. L., Xu, L., Liang, Y., Xu, X. H., and Zhao, X. Y. (2009) Berbamine exhibits potent antitumor effects on imatinib-resistant CML cells in vitro and in vivo. Acta Pharmacol. Sin. 30, 451-457
41. Xu, W. L., Shen, H. L., Ao, Z. F., Chen, B. A., Xia, W., Gao, F., and Zhang, Y. N. (2006) Combination of tetrandrine as a potential-reversing agent with daunorubicin, etoposide and cytarabine for the treatment of refractory and relapsed acute myelogenous leukemia. Leukemia Res. 30, 407-413 (Pubitemid 43254962)
42. Arts, I. C., and Hollman, P. C. (2005) Polyphenols and disease risk in epidemiologic studies. Am. J. Clin. Nutr. 81, 317S-325S
43. Hertog, M. G., Feskens, E. J., Hollman, P. C., Katan, M. B., and Kromhout, D. (1993) Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen Elderly Study. Lancet 342, 1007-1011 (Pubitemid 23314801)
44. Van der Woude, H., Boersma, M. G., Vervoort, J., and Rietjens, I. M. (2004) Identification of 14 quercetin phase II mono- and mixed conjugates and their formation by rat and human phase II in vitro model systems. Chem. Res. Toxicol. 17, 1520-1530 (Pubitemid 39532321)
45. Schulz, H. U., Schurer, M., Bassler, D., and Weiser, D. (2005) Investigation of pharmacokinetic data of hypericin, pseudohypericin, hyperforin and the flavonoids quercetin and isorhamnetin revealed from single and multiple oral dose studies with a hypericum extract containing tablet in healthy male volunteers. Arzneimittelforschung 55, 561-568 (Pubitemid 41546100)
46. de Boer, V. C., Dihal, A. A., van der Woude, H., Arts, I. C., Wolffram, S., Alink, G. M., Rietjens, I. M., Keijer, J., and Hollman, P. C. (2005) Tissue distribution of quercetin in rats and pigs. J. Nutr. 135, 1718-1725 (Pubitemid 40980724)
47. Boriskin, Y. S., Leneva, I. A., Pecheur, E. I., and Polyak, S. J. (2008) Arbidol: a broad-spectrum antiviral compound that blocks viral fusion. Curr. Med. Chem. 15, 997-1005 (Pubitemid 351736402)
48. Boriskin, Y. S., Pecheur, E. I., and Polyak, S. J. (2006) Arbidol: a broad-spectrum antiviral that inhibits acute and chronic HCV infection. Virol. J. 3, 56
49. Chai, H., Zhao, Y., Zhao, C., and Gong, P. (2006) Synthesis and in vitro anti-hepatitis B virus activities of some ethyl 6-bromo-5-hydroxy-1Hindole- 3-carboxylates. Bioorg. Med. Chem. 14, 911-917 (Pubitemid 43059782)
50. Lavillette, D., Bartosch, B., Nourrisson, D., Verney, G., Cosset, F. L., Penin, F., and Pecheur, E. I. (2006) Hepatitis C virus glycoproteins mediate low pH-dependent membrane fusion with liposomes. J. Biol. Chem. 281, 3909-3917 (Pubitemid 43847814)
51. Glushkov, R.G. (1992) Arbidol antiviral immunostimulant interferon inducer. Drugs Fut. 17, 1079-1081
52. Liu, M. Y., Wang, S., Yao, W. F., Wu, H. Z., Meng, S. N., and Wei, M. J. (2009) Pharmacokinetic properties and bioequivalence of two formulations of arbidol: an open-label, single-dose, randomized-sequence, two-period crossover study in healthy Chinese male volunteers. Clin. Ther. 31, 784-792