Plant plasma membrane water channels conduct the signalling molecule H2O2

Biochemical Journal

Volumn 414, Issue 1, 2008, Pages 53-61

  Dynowski, Marek ^a   Schaaf, Gabriel ^a,c   Loque, Dominique ^a,d   Moran, Oscar ^b   Ludewig, Uwe ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b CNR   (Italy)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Aquaglyceroporins; Aquaporin; Hydrogen peroxide; Reactive oxygen species (ROS)

Indexed keywords

AQUAGLYCEROPORINS; AQUAPORIN; HYDROGEN PEROXIDE; PLASMA MEMBRANE; REACTIVE OXYGEN SPECIES (ROS); WATER CHANNELS;

CELL MEMBRANES;

AQUAPORIN; CELL MEMBRANE PROTEIN; FLUORESCENT DYE; HYDROGEN PEROXIDE; MONOMER; PLASMA MEMBRANE INTRINSIC PROTEIN; TETRAMER; UREA; WATER; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE ANALYSIS; FUNGUS MUTATION; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PHYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN TRANSPORT; RESIDUE ANALYSIS; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SPINACH; WATER TRANSPORT; YEAST; CELL MEMBRANE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS; SPINACIA OLERACEA;

AQUAPORINS; ARABIDOPSIS; CELL MEMBRANE; HYDROGEN PEROXIDE; PLANT PROTEINS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SPINACIA OLERACEA;

EID: 49649083896     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20080287     Document Type: Article

References (47)

1. Maurel, C. (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett. 581, 2227-2236
2. Kaldenhoff, R. and Fischer, M. (2006) Functional aquaporin diversity in plants. Biochim. Biophys. Acta 1758, 1134-1141
3. Chaumont, F., Moshelion, M. and Daniels, M. J. (2005) Regulation of plant aqualporin activity. Biol. Cell 97, 749-764
4. Liu, L. H., Ludewig, U., Gassert, B., Frommer, W. B. and Von Wiren, N. (2003) Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol. 133, 1220-1228
5. Loqué, D., Ludewig, U., Yuan, L. and von Wiren, N. (2005) Tonoplast aquaporins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol. 137, 671-680
6. Johansson, I., Karlsson, M., Shukla, V. K., Chrispeels, M. J., Larsson, C. and Kjellbom, P. (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10, 451-459
7. Lee, J. W., Zhang, Y., Weaver, C. D., Shomer, N. H., Louis, C. F. and Roberts, D. M. (1995) Phosphorylation of nodulin 26 on serine 262 affects its voltage-sensitive channel activity in planar lipid bilayers. J. Biol. Chem. 270, 27051-27057
8. Gerbeau, P., Amodeo, G., Henzler, T., Santoni, V., Ripoche, P. and Maurel, C. (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J. 30, 71-81
9. 1. J. Biol. Chem. 274, 21631-21636
10. Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau. P., Luu, D. T., Bligny, R. and Maurel, C. (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393-397
11. Tornroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Neutze, R. and Kjellbom, P. (2006) Structural mechanism of plant aquaporin gating. Nature 439, 688-694
12. Hancock, J. T., Desikan, R. and Neill. S. J. (2001) Role of reactive oxygen species in cell signalling pathways. Biochem. Soc. Trans. 29, 345-350
13. Bienert, G. P., Schjoerring, J. K. and Jahn, T. P. (2006) Membrane transport of hydrogen peroxide. Biochim. Biophys. Acta 1758, 994-1003
14. Huckelhoven, R., Fodor, J., Preis, C. and Kogel, K. H. (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol. 119, 1251-1260
15. Shin, R. and Schachtman, D. P. (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc. Natl. Acad. Sci. U.S.A. 101, 8827-8832
16. Gechev, T. S. and Hille, J. (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J. Cell Biol. 168, 17-20
17. 2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol. 135, 702-708
18. Carol, R. J., Takeda, S., Linstead, P., Durrant, M. C., Kakesova, H., Derbyshire, P., Drea, S., Zarsky, V. and Dolan, L. (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438, 1013-1016
19. Bienert, G. P., Moller, A. L., Kristiansen, K. A., Schulz, A., Moller, I. M., Schjoerring, J. K. and Jahn, T. P. (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183-1192
20. Phillips, J. C., Braun, R., Wang, W, Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeet, R. D., Kale, L. and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802
21. 2 across water channels. J. Exp. Bot. 51, 2053-2066
22. + symporter in Arabidopsis thaliana. Plant Cell 15, 790-800
23. Reference deleted
24. Craft, Jr, J. W. and Legge, G. B. (2005) An AMBER/DYANA/MOLMOL phosphorylated amino acid library set and incorporation into NMR structure calculations. J. Biomol. NMR 33, 15-24
25. Jensen, M. O., Park, S., Tajkhorshid, E. and Schulten, K. (2002) Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc. Natl. Acad. Sci. U.S.A. 99, 6731-6736
26. Johnson, F. H., Eyring, H. and Stover. B. J. (1974) The Theory of Rate Processes in Biology and Medicine, Wiley, New York
27. Yurkow, E. J. and McKenzie, M. A. (1993) Characterization of hypoxia-dependent peroxide production in cultures of Saccharomyces cerevisiae using flow cytometry: a model for ischemic tissue destruction. Cytometry 14, 287-293
28. Madeo, F, Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K.. Sigrist, S. J.. Wesselborg, S. and Frohlich, K. U. (2002) A caspase-related protease regulates apoptosis in yeast. Mol. Cell 9, 911-917
29. Wallace, I. S. and Roberts, D. M. (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44, 16826-16834
30. Tajkhorshid, E., Nollert, R, Jensen, M. O., Miercke, L. J., O'Connell, J., Stroud, R. M. and Schulten, K. (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296, 525-530
31. Takano. J., Wada. M.. Ludewig, U.. Schaaf, G., von Wiren, N. and Fujiwara, T. (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18, 1498-1509
32. Weig, A. R. and Jakob, C. (2000) Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLIM2 proteins by heterologous expression in Saccharomyces cerevisiae, FEBS Lett. 481, 293-298
33. de Groot. B. L. and Grubmuller, H. (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GIpF. Science 294, 2353-2357
34. Wang, Y, Cohen, J., Boron, W. F, Schulten, K. and Tajkhorshid, E. (2007) Exploring gas permeability of cellular membranes and membrane channels with molecular dynamics. J. Struct. Biol. 157, 534-544
35. Han, B. G., Guliaev, A. B., Walian, P. J. and Jap, B. K. (2006) Water transport in AOP0 aquaporin: molecular dynamics studies. J. Mol. Biol. 360, 285-296
36. Zhu. F, Tajkhorshid, E. and Schulten. K. (2004) Theory and simulation of water permeation in aquaporin-1. Biophys. J. 86, 50-57
37. Zhu, F, Tajkhorshid, E. and Schulten. K. (2002) Pressure-induced water transport in membrane channels studied by molecular dynamics. Biophys. J. 83, 154-160
38. Dynowski, M. and Ludewig, U. (2006) TrpAQP: computer simulations to determine the selectivity of aquaporins. High Performance Computing in Science and Engineering '06 (Nagel, W. E., Jager, W. and Resch, M., eds), pp. 187-197, Springer-Verlag, New York
39. 2 in Saccharomyces cerevisiae. J. Biol. Chem. 279, 6501-6506
40. Jamieson, D. J. (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14, 1511-1527
41. 2 gradients across biomembranes. FEES Lett. 475, 121-126
42. Seaver, L. C. and Imlay, J. A. (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 183, 7182-7189
43. Carbrey. J. M., Bonhivers. M., Boeke, J. D. and Agre, P. (2001) Aquaporins in Saccharomyces: characterization of a second functional water channel protein. Proc. Natl. Acad. Sci. U.S.A. 98, 1000-1005
44. Walter, A. and Gutknecht, J. (1986) Permeability of small nonelectrolytes through lipid bilayer membranes. J. Membr. Biol. 90, 207-217
45. Uemura, M., Joseph, R. A. and Steponkus, P. L. (1995) Cold acclimation of Arabidopsis thaliana. Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 109, 15-30
46. Law, R. J. and Sansom, M. S. (2004) Homology modelling and molecular dynamics simulations: comparative studies of human aquaporin-1. Eur. Biophys. J. 33, 477-489
47. Savage, D. F, Egea, P. F. Robles-Colmenares, Y, Iii, J. D. and Stroud. R. M. (2003) Architecture and selectivity in aquaporins: 2.5 Å x-ray structure of aqualporin z. PLoS Biol. 1, e72