Regulation of AQP0 water permeability is enhanced by cooperativity

Journal of General Physiology

Volumn 141, Issue 3, 2013, Pages 287-295

  Németh Cahalan, Karin L ^a   Clemens, Daniel M ^a   Hall, James E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; AQUAPORIN 0; CALCIUM; EYE PROTEIN; HYDROGEN; WATER;

ANIMAL; ARTICLE; LENS; METABOLISM; OOCYTE; PERMEABILITY; PH; XENOPUS LAEVIS;

ANIMALS; AQUAPORINS; CALCIUM; EYE PROTEINS; HYDROGEN; HYDROGEN-ION CONCENTRATION; LENS, CRYSTALLINE; OOCYTES; PERMEABILITY; WATER; XENOPUS LAEVIS;

EID: 84874735379     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210884     Document Type: Article

References (34)

1. Ball, L.E., D.L. Garland, R.K. Crouch, and K.L. Schey. 2004. Posttranslational modifications of aquaporin 0 (AQP0) in the normal human lens: spatial and temporal occurrence. Biochemistry. 43: 9856-9865. http://dx.doi.org/10.1021/bi0496034
2. Bassnett, S., and G. Duncan. 1985. Direct measurement of pH in the rat lens by ion-sensitive microelectrodes. Exp. Eye Res. 40:585-590.
3. Chandy, G., G.A. Zampighi, M. Kreman, and J.E. Hall. 1997. Comparison of the water transporting properties of MIP and AQP1. J. Membr. Biol. 159:29-39. http://dx.doi.org/10.1007/s002329900266
4. Chrispeels, M.J., and P. Agre. 1994. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem. Sci. 19:421-425. http://dx.doi.org/10.1016/0968-0004(94)90091-4
5. Ding, S., L. Ingleby, C.A. Ahern, and R. Horn. 2005. Investigating the putative glycine hinge in Shaker potassium channel. J. Gen. Physiol. 126:213-226.
6. Donaldson, P.J., L.S. Musil, and R.T. Mathias. 2010. Point: A critical appraisal of the lens circulation model-an experimental paradigm for understanding the maintenance of lens transparency? Invest. Ophthalmol. Vis. Sci. 51:2303-2306. http://dx.doi.org/10.1167/iovs.10-5350
7. Duncan, G., and T.J. Jacob. 1984. Calcium and the physiology of cataract. Ciba Found. Symp. 106:132-152.
8. Engel, A., Y. Fujiyoshi, T. Gonen, and T. Walz. 2008. Junctionforming aquaporins. Curr. Opin. Struct. Biol. 18:229-235.
9. Gold, M.G., S.L. Reichow, S.E. O'Neill, C.R. Weisbrod, L.K. Langeberg, J.E. Bruce, T. Gonen, and J.D. Scott. 2012. AKAP2 anchors PKA with aquaporin-0 to support ocular lens transparency. EMBO Mol Med. 4:15-26. http://dx.doi.org/10.1002/emmm .201100184
10. Gonen, T., Y. Cheng, J. Kistler, and T. Walz. 2004a. Aquaporin-0 membrane junctions form upon proteolytic cleavage. J. Mol. Biol. 342:1337-1345. http://dx.doi.org/10.1016/j.jmb.2004.07.076
11. Gonen, T., P. Sliz, J. Kistler, Y. Cheng, and T. Walz. 2004b. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature. 429:193-197. http://dx.doi.org/10.1038/nature02503
12. Grey, A.C., L. Li, M.D. Jacobs, K.L. Schey, and P.J. Donaldson. 2009. Differentiation-dependent modification and subcellular distribution of aquaporin-0 suggests multiple functional roles in the rat lens. Differentiation. 77:70-83. http://dx.doi.org/10.1016/j.diff.2008.09.003
13. Hall, J.E. 2012. Through a glass darkly. EMBO Mol Med. 4:1-2. http://dx.doi.org/10.1002/emmm.201100188
14. Harries, W.E., D. Akhavan, L.J. Miercke, S. Khademi, and R.M. Stroud. 2004. The channel architecture of aquaporin 0 at a 2.2-Å resolution. Proc. Natl. Acad. Sci. USA. 101:14045-14050.
15. Kalman, K., K.L. Németh-Cahalan, A. Froger, and J.E. Hall. 2008. Phosphorylation determines the calmodulin-mediated Ca2+ response and water permeability of AQP0. J. Biol. Chem. 283:21278-21283. http://dx.doi.org/10.1074/jbc.M801740200
16. Kumari, S.S., and K. Varadaraj. 2009. Intact AQP0 performs cell-tocell adhesion. Biochem. Biophys. Res. Commun. 390:1034-1039.
17. Kumari, S.S., M. Varadaraj, V.S. Yerramilli, A.G. Menon, and K. Varadaraj. 2012. Spatial expression of aquaporin 5 in mammalian cornea and lens, and regulation of its localization by phosphokinase A. Mol. Vis. 18:957-967.
18. Lagree, V., A. Froger, S. Deschamps, I. Pellerin, C. Delamarche, G. Bonnec, J. Gouranton, D. Thomas, and J.F. Hubert. 1998. Oligomerization state of water channels and glycerol facilitators. Involvement of loop E. J. Biol. Chem. 273:33949-33953.
19. Lampe, P.D., M.D. Bazzi, G.L. Nelsestuen, and R.G. Johnson. 1986. Phosphorylation of lens intrinsic membrane proteins by protein kinase C. Eur. J. Biochem. 156:351-357. http://dx.doi.org/10 .1111/j.1432-1033.1986.tb09590.x
20. Mathai, J.C., and P. Agre. 1999. Hourglass pore-forming domains restrict aquaporin-1 tetramer assembly. Biochemistry. 38:923-928. http://dx.doi.org/10.1021/bi9823683
21. Mathias, R.T., G. Riquelme, and J.L. Rae. 1991. Cell to cell communication and pH in the frog lens. J. Gen. Physiol. 98:1085-1103.
22. Mathias, R.T., J. Kistler, and P. Donaldson. 2007. The lens circulation. J. Membr. Biol. 216:1-16. http://dx.doi.org/10.1007/s00232-007-9019-y
23. Murata, K., K. Mitsuoka, T. Hirai, T. Walz, P. Agre, J.B. Heymann, A. Engel, and Y. Fujiyoshi. 2000. Structural determinants of water permeation through aquaporin-1. Nature. 407:599-605. http://dx.doi.org/10.1038/35036519
24. Németh-Cahalan, K.L., and J.E. Hall. 2000. pH and calcium regulate the water permeability of aquaporin 0. J. Biol. Chem. 275:6777-6782. http://dx.doi.org/10.1074/jbc.275.10.6777
25. Németh-Cahalan, K.L., K. Kalman, and J.E. Hall. 2004. Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J. Gen. Physiol. 123:573-580. http://dx.doi.org/10.1085/jgp.200308990
26. Németh-Cahalan, K.L., K. Kalman, A. Froger, and J.E. Hall. 2007. Zinc modulation of water permeability reveals that aquaporin 0 functions as a cooperative tetramer. J. Gen. Physiol. 130:457-464. http://dx.doi.org/10.1085/jgp.200709826
27. Reichow, S.L., and T. Gonen. 2008. Noncanonical binding of calmodulin to aquaporin-0: implications for channel regulation. Structure. 16:1389-1398. http://dx.doi.org/10.1016/j.str.2008.06.011
28. Rose, K.M., Z. Wang, G.N. Magrath, E.S. Hazard, J.D. Hildebrandt, and K.L. Schey. 2008. Aquaporin 0-calmodulin interaction and the effect of aquaporin 0 phosphorylation. Biochemistry. 47:339-347. http://dx.doi.org/10.1021/bi701980t
29. Schey, K.L., J.G. Fowler, J.C. Schwartz, M. Busman, J. Dillon, and R.K. Crouch. 1997. Complete map and identification of the phosphorylation site of bovine lens major intrinsic protein. Invest. Ophthalmol. Vis. Sci. 38:2508-2515.
30. Schey, K.L., D.B. Gutierrez, Z. Wang, J. Wei, and A.C. Grey. 2010. Novel fatty acid acylation of lens integral membrane protein aquaporin-0. Biochemistry. 49:9858-9865. http://dx.doi.org/10 .1021/bi101415w
31. Shiels, A., and S. Bassnett. 1996. Mutations in the founder of the MIP gene family underlie cataract development in the mouse. Nat. Genet. 12:212-215.
32. Varadaraj, K., C. Kushmerick, G.J. Baldo, S. Bassnett, A. Shiels, and R.T. Mathias. 1999. The role of MIP in lens fiber cell membrane transport. J. Membr. Biol. 170:191-203.
33. Varadaraj, K., S. Kumari, A. Shiels, and R.T. Mathias. 2005. Regulation of aquaporin water permeability in the lens. Invest. Ophthalmol. Vis. Sci. 46:1393-1402. http://dx.doi.org/10.1167/iovs.04-1217
34. Yap, K.L., T. Yuan, T.K. Mal, H.J. Vogel, and M. Ikura. 2003. Structural basis for simultaneous binding of two carboxy-terminal peptides of plant glutamate decarboxylase to calmodulin. J. Mol. Biol. 328:193-204.