Structural mechanism of plant aquaporin gating

Nature

Volumn 439, Issue 7077, 2006, Pages 688-694

  Törnroth Horsefield, Susanna ^a   Wang, Yi ^b   Hedfalk, Kristina ^a   Johanson, Urban ^c   Karlsson, Maria ^c   Tajkhorshid, Emad ^b   Neutze, Richard ^a   Kjellbom, Per ^c  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; COMPUTER SIMULATION; CYTOLOGY; MOLECULAR DYNAMICS; PH EFFECTS;

CYTOPLASMIC PH; DEPHOSPHORYLATION; PLANT AQUAPORIN GATING; SPINACH PLASMA MEMBRANE;

PLANTS (BOTANY);

AQUAPORIN; SERINE;

PLANT;

ARTICLE; CELL MEMBRANE; CONFORMATION; CRYSTAL STRUCTURE; CYTOPLASM; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIMULATION; SPINACH; STATISTICAL SIGNIFICANCE; X RAY ANALYSIS;

SPINACIA OLERACEA;

EID: 32544450674     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04316     Document Type: Article

References (47)

1. Preston, G. M., Carroll, T. P., Guggino, W. B. & Agre, P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256, 385-387 (1992).
2. Johansson, I., Karlsson, M., Johanson, U., Larsson, C. & Kjellbom, P. The role of aquaporins in cellular and whole plant water balance. Biochim. Biophys. Acta 1465, 324-342 (2000).
3. Agre, P. & Kozono, D. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett. 555, 72-78 (2003).
4. King, L. S., Kozono, D. & Agre, P. From structure to disease: the evolving tale of aquaporin biology. Nature Rev. Mol. Cell Biol. 5, 687-698 (2004).
5. Tamas, M. J. et al. A short regulatory domain restricts glycerol transport through yeast Fps1p. J. Biol. Chem. 278, 6337-6345 (2003).
6. Johanson, U. et al. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol. 126, 1358-1369 (2001).
7. Morishita, Y., Sakube, Y., Sasaki, S. & Ishibashi, K. Molecular mechanisms and drug development in aquaporin water channel diseases: aquaporin superfamily (superaquaporins): expansion of aquaporins restricted to multicellular organisms. J. Pharmacol. Sci. 96, 276-279 (2004).
8. Borstlap, A. C. Early diversification of plant aquaporins. Trends Plant Sci. 7, 529-530 (2002).
9. Johansson, I. et al. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10, 451-459 (1998).
10. 2+ and apoplastic water potential. Plant Cell 8, 1181-1191 (1996).
11. Tournaire-Roux, C. et al. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393-397 (2003).
12. Murata, K. et al. Structural determinants of water permeation through aquaporin-1. Nature 407, 599-605 (2000).
13. Sui, H., Han, B. G., Lee, J. K., Walian, P. & Jap, B. K. Structural basis of water-specific transport through the AQP1 water channel. Nature 414, 872-878 (2001).
14. Savage, D. F., Egea, P. F., Robles-Colmenares, Y., O'Connell, J. D. & Stroud, R. M. Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z. PLoS Biol. 1, E72 (2003).
15. Gonen, T., Sliz, P., Kistler, J., Cheng, Y. & Walz, T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429, 193-197 (2004).
16. Harries, W. E., Akhavan, D., Miercke, L. J., Khademi, S. & Stroud, R. M. The channel architecture of aquaporin 0 at a 2.2 Å resolution. Proc. Natl Acad. Sci. USA 101, 14045-14050 (2004).
17. Fu, D. et al. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486 (2000).
18. Tajkhorshid, E. et al. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296, 525-530 (2002).
19. de Groot, B. L. & Grubmuller, H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294, 2353-2357 (2001).
20. Jensen, M. O., Tajkhorshid, E. & Schulten, K. The mechanism of glycerol conduction in aquaglyceroporins. Structure 9, 1083-1093 (2001).
21. Jensen, M. O., Park, S., Tajkhorshid, E. & Schulten, K. Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc. Natl Acad. Sci. USA 99, 6731-6736 (2002).
22. Daniels, M. J., Chrispeels, M. J. & Yeager, M. Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J. Mol. Biol. 294, 1337-1349 (1999).
23. Kukulski, W. et al. The 5 Å structure of heterologously expressed plant aquaporin SoPIP2;1. J. Mol. Biol. 350, 611-616 (2005).
24. Hedges, S. B., Blair, J. E., Venturi, M. L. & Shoe, J. L. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 4, 2 (2004).
25. Jung, J. S., Preston, G. M., Smith, B. L., Guggino, W. B. & Agre, P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J. Biol. Chem. 269, 14648-14654 (1994).
26. Wang, Y., Schulten, K. & Tajkhorshid, E. What makes an aquaporin a glycerol channel: A comparative study of AqpZ and GlpF. Structure 13, 1107-1118 (2005).
27. de Groot, B. L., Frigato, T., Helms, V. & Grubmuller, H. The mechanism of proton exclusion in the aquaporin-1 water channel. J. Mol. Biol. 333, 279-293 (2003).
28. Jensen, M. O., Tajkhorshid, E. & Schulten, K. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85, 2884-2899 (2003).
29. Chakrabarti, N., Tajkhorshid, E., Roux, B. & Pomes, R. Molecular basis of proton blockage in aquaporins. Structure 12, 65-74 (2004).
30. Ilan, B., Tajkhorshid, E., Schulten, K. & Voth, G. A. The mechanism of proton exclusion in aquaporin channels. Proteins 55, 223-228 (2004).
31. de Groot, B. L. & Grubmüller, H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr. Opin. Struct. Biol. 15, 176-183 (2005).
32. Smart, O. S., Goodfellow, J. M. & Wallace, B. A. The pore dimensions of gramicidin A. Biophys. J. 65, 2455-2460 (1993).
33. Nemeth-Cahalan, K. L. & Hall, J. E. pH and calcium regulate the water permeability of aquaporin 0. J. Biol. Chem. 275, 6777-6782 (2000).
34. Zelenina, M., Bondar, A. A., Zelenin, S. & Aperia, A. Nickel and extracellular acidification inhibit the water permeability of human aquaporin-3 in lung epithelial cells. J. Biol. Chem. 278, 30037-30043 (2003).
35. Zelenina, M., Tritto, S., Bondar, A. A., Zelenin, S. & Aperia, A. Copper inhibits the water and glycerol permeability of aquaporin-3. J. Biol. Chem. 279, 51939-51943 (2004).
36. Madsen, D. & Kleywegt, G. J. Interactive motif and fold recognition in protein structures. J. Appl. Crystallogr. 35, 137-139 (2001).
37. Karlsson, M. et al. Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett. 537, 68-72 (2003).
38. Bailey, S. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
39. Morris, R. J., Perrakis, A. & Lamzin, V. S. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol. 374, 229-244 (2003).
40. Brunger, A. T. et al. Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
41. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. & Thornton, J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (1996).
42. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
43. Kalé, L. et al. NAMD2: Greater scalability for parallel molecular dynamics. J. Comp. Phys. 151, 283-312 (1999).
44. MacKerell, A. D. et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616 (1998).
45. Schlenkrich, M., Brickmann, J., MacKerell, A. D. & Karplus, M. in Biological Membranes: A Molecular Perspective from Computation and Experiment (eds Merz, K. M. & Roux, B.) 31-81 (Birkhauser, Boston, Massachusetts, 1996).
46. Darden, T., York, D. & Pedersen, L. Particle Mesh Ewald - an N.log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092 (1993).
47. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).