A general anaesthetic propofol inhibits aquaporin-4 in the presence of Zn2+

Biochemical Journal

Volumn 454, Issue 2, 2013, Pages 275-282

  Kato, Jungo ^a   Hayashi, Mariko Kato ^a   Aizu, Shinnosuke ^a   Yukutake, Yoshinori ^a   Takeda, Junzo ^a   Yasui, Masato ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Aquaporin 4 (AQP4); Brain oedema; General anaesthetic; Water channel

Indexed keywords

AQUAPORIN 1; AQUAPORIN 4; CYSTEINE; PROPOFOL; PROTEOLIPOSOME; TETRAMER; ZINC ION;

ANALYSIS; ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; FLUIDIZATION; LIPID MEMBRANE; OSMOSIS; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SITE DIRECTED MUTAGENESIS; STOPPED FLOW ANALYSIS; WATER PERMEABILITY;

AMINO ACID SUBSTITUTION; ANESTHETICS, INTRAVENOUS; AQUAPORIN 1; AQUAPORIN 4; CYSTEINE; HUMANS; LIPID BILAYERS; LIPOSOMES; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OSMOLAR CONCENTRATION; PERMEABILITY; PROPOFOL; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; WATER; ZINC;

EID: 84881523690     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130046     Document Type: Article

References (43)

1. Fishman, R. A. (1975) Brain edema. N. Engl. J. Med. 293, 706-711
2. Nag, S., Manias, J. L. and Stewart, D. J. (2009) Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol. 118, 197-217
3. Kimelberg, H. K. (2005) Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 50, 389-397
4. Thrane, A. S., Rappold, P. M., Fujita, T., Torres, A., Bekar, L. K. and Takano, T. (2011) Signaling events elicited by cerebral edema. Proc. Natl. Acad. Sci. U.S.A. 108, 846-851
5. Nase, G., Helm, P. J., Enger, R. and Ottersen, O. P. (2008) Water entry into astrocytes during brain edema formation. Glia 56, 895-902
6. 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
7. Amiry-Moghaddam, M., Otsuka, T., Hurn, P. D., Traystman, R. J., Haug, F., Froehner, S. C., Adams, M. E., Neely, J. D., Agre, P., Ottersen, O. P. and Bhardwaj, A. (2002) An α-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc. Natl. Acad. Sci. U.S.A. 100, 2106-2111
8. Papadopoulos, M. C. and Verkman, A. S. (2007) Aquaporin-4 and brain edema. Pediatr. Nephrol. 22, 778-784
9. 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
10. 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
11. 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
12. Yukutake, Y., Tsuji, S., Hirano, Y., Adachi, T., Takahashi, T., Fujihara, K., Agre, P., Yasui, M. and Suematsu, M. (2008) Mercury chloride decreases the water permeability of biology of aquaporin-4-reconstituted proteoliposomes. Biol. Cell 100, 355-363
13. Yukutake, Y., Hirano, Y., Suematsu, M. and Yasui, M. (2009) Rapid and reversible inhibition of aquaporin-4 by zinc. Biochemistry 48, 12059-12061
14. Kruczek, C., Görg, B., Keitel, V., Pirev, E., Kröncke, K. D., Schliess, F. and Häussinger, D. (2009) Hypoosmotic swelling affects zinc homeostasis in cultured rat astrocytes. Glia 57, 79-92
15. Franks, N. P. (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci. 9, 370-386
16. Trapani, G., Altomare, C., Sanna, E. and Liso, G. (2000) Propofol in anesthesia. Mechanism of action, structure-activity relationships, and drug delivery. Curr. Med. Chem. 7, 249-271
17. Balasubramanian, S. V, Campbell, R. B. and Straubinger, R. M. (2002) Propofol, a general anesthetic, promotes the formation of fluid phase domains in model membranes. Chem. Phys. Lipids 114, 35-44
18. Tsuchiya, H. (2001) Structure-specific membrane fluidizing effect of propofol. Clin. Exp. Pharmacol. Physiol. 28, 292-299
19. Adembri, C., Venturi, L., Tani, A., Chiarugi, A., Gramigni, E., Cozzi, A., Pancani, T., De Gaudio, R. A. and Pellegrini-Giampietro, D. E. (2006) Neuroprotective effects of propofol in models of cerebral ischemia: inhibition of mitochondrial swelling as a possible mechanism. Anesthesiology 104, 80-89
20. Kotani, Y., Nakajima, Y., Hasegawa, T., Satoh, M., Nagase, H., Shimazawa, M., Yoshimura, S., Iwama, T. and Hara, H. (2008) Propofol exerts greater neuroprotection with disodium edetate than without it. J. Cereb. Blood Flow Metab. 28, 354-366
21. Yang, B., Van Hoek, A. N. and Verkman, A. S. (1997) Very high single channel water permeability of aquaporin-4 in baculovirus-infected insect cells and liposomes reconstituted with purified aquaporin-4. Biochemistry 36, 7625-7632
22. Zeidel, M. L., Albalak, A., Grossman, E. and Carrutherss, A. (1992) Role of glucose carrier in human erythrocyte water permeability. Biochemistry 31, 589-596
23. 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
24. Aarts, L., Van der Hee, R., Dekker, I., Jong, J., de Langemeijer, H. and Bast, A. (1995) The widely used anesthetic agent propofol can replace as an antioxidant-tocopherol. FEBS Lett. 357, 83-85
25. Vasileiou, I., Xanthos, T., Koudouna, E., Perrea, D., Klonaris, C., Katsargyris, A. and Papadimitriou, L. (2009) Propofol: a review of its non-anaesthetic effects. Eur. J. Pharmacol. 605, 1-8
26. Sorbo, J. G., Moe, S. E., Ottersen, O. P. and Holen, T. (2008) The molecular composition of square arrays. Biochemistry 48, 2631-2637
27. Nicchia, G. P., Rossi, A., Mola, M. G., Pisani, F., Stigliano, C., Basco, D., Mastrototaro, M., Svelto, M. and Frigeri, A. (2010) Higher order structure of aquaporin-4. Neuroscience 168, 903-914
28. Zheng, Y. Y., Lan, Y. P., Tang, H. F. and Zhu, S. M. (2008) Propofol pretreatment attenuates aquaporin-4 over-expression and alleviates cerebral edema after transient focal brain ischemia reperfusion in rats. Anesth. Analg. 107, 2009-2016
29. Zhu, S. M., Xiong, X. X., Zheng, Y. Y. and Pan, C. F. (2009) Propofol inhibits aquaporin 4 expression through a protein kinase C-dependent pathway in an astrocyte model of cerebral ischemia/reoxygenation. Anesth. Analg. 109, 1493-1499
30. Hiroaki, Y., Tani, K., Kamegawa, A., Gyobu, N., Nishikawa, K., Suzuki, H., Walz, T., Sasaki, S., Mitsuoka, K., Kimura, K. et al. (2006) Implications of the aquaporin-4 structure on array formation and cell adhesion. J. Mol. Biol. 355, 628-639
31. Maret, W. and Li, Y. (2009) Coordination dynamics of zinc in proteins. Chem. Rev. 109, 4682-4707
32. Gundelfinger, E. D., Boeckers, T. M., Baron, M. K. and Bowie, J. U. (2006) A role for zinc in postsynaptic density assembly and plasticity. Trends Biochem. Sci. 31, 366-373
33. Conrady, D. G., Brescia, C. C., Horii, K., Weiss, A. A., Hassett, D. J. and Herr, A. B. (2008) A zinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc. Natl. Acad. Sci. U.S.A. 105, 19456-19461
34. Momo, F., Fabris, S., Bindoli, A., Scutari, G. and Stevanato, R. (2002) Different effects of propofol and nitrosopropofol on DMPC multilamellar liposomes. Biophys. Chem. 95, 145-155
35. Crane, J. M. and Verkman, A. S. (2009) Reversible, temperature-dependent supramolecular assembly of aquaporin-4 orthogonal arrays in live cell membranes. Biophys. J. 97, 3010-3018
36. Furman, C. S., Gorelick-Feldman, D. A., Davidson, K. G. V, Yasumura, T., Neely, J. D., Agre, P. and Rash, J. E. (2003) Aquaporin-4 square array assembly: opposing actions of M1 and M23 isoforms. Proc. Natl. Acad. Sci. U.S.A. 100, 13609-13614
37. Rash, J. E., Davidson, K. G. V., Yasumura, T. and Furman, C. S. (2004) Freeze-fracture and immunogold analysis of aquaporin-4 (AQP4) square arrays, with models of AQP4 lattice assembly. Neuroscience 129, 915-934
38. Fenton, R. A, Moeller, H. B., Zelenina, M., Snaebjornsson, M. T., Holen, T. and MacAulay, N. (2010) Differential water permeability and regulation of three aquaporin 4 isoforms. Cell. Mol. Life Sci. 67, 829-840
39. Neely, J. D., Christensen, B. M., Nielsen, S. and Agre, P. (1999) Heterotetrameric composition of aquaporin-4 water channels. Biochemistry 38, 11156-11163
40. Silberstein, C., Bouley, R., Huang, Y., Fang, P., Pastor-Soler, N., Brown, D. and Van Hoek, A. N. (2004) Membrane organization and function of M1 and M23 isoforms of aquaporin-4 in epithelial cells. Am. J. Physiol. Renal Physiol. 287, F501-F511
41. Shafer, A., Doze, VA. and Shafer, S. W. P. (1988) Pharmacokinetics and pharmacodynamics of propofol infusions during general anesthesia. Anesthesiology 69, 348-356
42. Riu, P. L., Riu, G., Testa, C., Mulas, M., Caria, M. A., Mameli, S. and Mameli, O. (2000) Disposition of propofol between red blood cells, plasma, brain and cerebrospinal fluid in rabbits. Eur. J. Anaesthesiol. 17, 18-22
43. Wang, J., Yang, X., Camporesi, C. V, Yang, Z., Bosco, G., Chen, C. and Camporesi, E. M. (2002) Propofol reduces infarct size and striatal dopamine accumulation following transient middle cerebral artery occlusion: a microdialysis study. Eur. J. Pharmacol. 452, 303-308