H95 Is a pH-Dependent Gate in Aquaporin 4

Structure

Volumn 23, Issue 12, 2015, Pages 2309-2318

  Kaptan, Shreyas ^a   Assentoft, Mette ^b   Schneider, Hans Peter ^c   Fenton, Robert A ^d   Deitmer, Joachim W ^c   MacAulay, Nanna ^b   De Groot, Bert L ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c University of Koblenz Landau   (Germany)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; HISTIDINE; HISTIDINE RESIDUE 95; UNCLASSIFIED DRUG; AQP4 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; COMPUTER MODEL; COMPUTER SIMULATION; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; MOLECULAR DYNAMICS; NONHUMAN; OOCYTE; PH; PRIORITY JOURNAL; PROTON TRANSPORT; WATER PERMEABILITY; XENOPUS; AMINO ACID SEQUENCE; CHANNEL GATING; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; AQUAPORIN 4; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; OOCYTES;

EID: 84949227944     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.08.020     Document Type: Article

References (82)

1. P. Agre The aquaporin water channels Proc. Am. Thorac. Soc. 3 2006 5 13
2. P. Agre, L.S. King, M. Yasui, W.B. Guggino, O.P. Ottersen, Y. Fujiyoshi, A. Engel, and S. Nielsen Aquaporin water channels - from atomic structure to clinical medicine J. Physiol. 542 2002 3 16
3. D. Alberga, O. Nicolotti, G. Lattanzi, G.P. Nicchia, A. Frigeri, F. Pisani, V. Benfenati, and G.F. Mangiatordi A new gating site in human aquaporin-4: insights from molecular dynamics simulations Biochim. Biophys. Acta 1838 2014 3052 3060
4. A. Amadei, A.B.M. Linssen, and H.J.C. Berendsen Essential dynamics of proteins Proteins 17 1993 412 425
5. A. Amadei, A.B.M. Linssen, B.L. de Groot, D.M.F. van Aalten, and H.J.C. Berendsen An efficient method for sampling the essential subspace of proteins J. Biomol. Struct. Dyn. 13 1996 615 625
6. M. Amiry-Moghaddam, and O.P. Ottersen The molecular basis of water transport in the brain Nat. Rev. Neurosci. 4 2003 991 1001
7. M. Assentoft, S. Kaptan, R.A. Fenton, S.Z. Hua, B.L. de Groot, and N. MacAulay Phosphorylation of rat aquaporin-4 at Ser111 is not required for channel gating Glia 61 2013 1101 1112
8. M. Assentoft, B.R. Larsen, E.T. Olesen, R.A. Fenton, and N. MacAulay AQP4 plasma membrane trafficking or channel gating is not significantly modulated by phosphorylation at COOH-terminal serine residues Am J Physiol Cell Physiol. 307 10 2014 C957 965
9. F. Autore, B. Pagano, A. Fornili, K. Rittinger, and F. Fraternali In silico phosphorylation of the autoinhibited form of p47phox: insights into the mechanism of activation Biophys. J. 99 2010 3716 3725
10. + buffering mediated by sodium bicarbonate cotransport expressed in Xenopus oocytes J. Biol. Chem. 279 2004 28057 28062
11. E. Beitz, S. Pavlovic-Djuranovic, M. Yasui, P. Agre, and J.E. Schultz Molecular dissection of water and glycerol permeability of the aquaglyceroporin from Plasmodium falciparum by mutational analysis Proc. Natl. Acad. Sci. USA 101 2004 1153 1158
12. K. Beppu, T. Sasaki, K.F. Tanaka, A. Yamanaka, Y. Fukazawa, R. Shigemoto, and K. Matsui Optogenetic countering of glial acidosis suppresses glial glutamate release and ischemic brain damage Neuron 81 2014 314 320
13. H.J.C. Berendsen, J.R. Grigera, and T.P. Straatsma The missing term in effective pair potentials J. Phys. Chem. 91 1987 6269 6271
14. O. Berger, O. Edholm, and F. Jahnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
15. S. Bröer, H.P. Schneider, A. Bröer, B. Rahman, B. Hamprecht, and J.W. Deitmer Characterization of the monocarboxylate transporter 1 expressed in Xenopus laevis oocytes by changes in cytosolic pH Biochem. J. 333 1998 167 174
16. B.C. Burckhardt, and E. Frömter Pathways of NH3/NH4+ permeation across Xenopus laevis oocyte cell membrane Pflugers Arch. 420 1992 83 86
17. A. Burykin, and A. Warshel On the origin of the electrostatic barrier for proton transport in aquaporin FEBS Lett. 570 2004 41 46
18. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101
19. G.J. Cooper, Y. Zhou, P. Bouyer, I.I. Grichtchenko, and W.F. Boron Transport of volatile solutes through AQP1 J. Physiol. 542 2002 17 29
20. Y. Cui, and D.A. Bastien Water transport in human aquaporin-4: molecular dynamics (MD) simulations Biochem. Biophys. Res. Commun. 412 2011 654 659
21. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
22. B.L. de Groot, and H. Grubmüller Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF Science 294 2001 2353 2357
23. B.L. de Groot, and H. Grubmüller The dynamics and energetics of water permeation and proton exclusion in aquaporins Curr. Opin. Struct. Biol. 15 2005 176 183
24. B.L. de Groot, T. Frigato, V. Helms, and H. Grubmüller The mechanism of proton exclusion in the aquaporin-1 water channel J. Mol. Biol. 333 2003 279 293
25. J.W. Deitmer Electrogenic sodium-dependent bicarbonate secretion by glial cells of the leech central nervous system J. Gen. Physiol. 98 1991 637 655
26. 2 transport across the human erythrocyte membrane FASEB J. 20 2006 1974 1981
27. K.A. Feenstra, B. Hess, and H.J.C. Berendsen Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems J. Comput. Chem. 20 1999 786 798
28. R.A. Fenton, H.B. Moeller, M. Zelenina, M.T. Snaebjornsson, T. Holen, and N. MacAulay Differential water permeability and regulation of three aquaporin 4 isoforms Cell Mol. Life Sci. 67 2010 829 840
29. A. Frick, M. Järvå, and S. Törnroth-Horsefield Structural basis for pH gating of plant aquaporins FEBS Lett. 587 2013 989 993
30. A. Frick, U.K. Eriksson, F. de Mattia, F. Oberg, K. Hedfalk, R. Neutze, W.J. de Grip, P.M.T. Deen, and S. Törnroth-Horsefield X-Ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking Proc. Natl. Acad. Sci. USA 111 2014 6305 6310
31. D. Fu, A. Libson, L.J.W. Miercke, C. Weitzman, P. Nollert, J. Krucinski, and R.M. Stroud Structure of a glycerol-conducting channel and the basis for its selectivity Science 290 2000 481 486
32. J.-A. Garate, N.J. English, and J.M.D. MacElroy Human aquaporin 4 gating dynamics in dc and ac electric fields: a molecular dynamics study J. Chem. Phys. 134 2011 055110
33. T. Gonen, Y. Cheng, P. Sliz, Y. Hiroaki, Y. Fujiyoshi, S.C. Harrison, and T. Walz Lipid-protein interactions in double-layered two-dimensional AQP0 crystals Nature 438 2005 633 638
34. E. Gunnarson, M. Zelenina, G. Axehult, Y. Song, A. Bondar, P. Krieger, H. Brismar, S. Zelenin, and A. Aperia Identification of a molecular target for glutamate regulation of astrocyte water permeability Glia 56 2008 587 596
35. W.E.C. Harries, D. Akhavan, L.J.W. Miercke, S. Khademi, and R.M. Stroud The channel architecture of aquaporin 0 at a 2.2-Å resolution Proc. Natl. Acad. Sci. USA 101 2004 14045 14050
36. B. Hess P-LINCS: a parallel linear constraint solver for molecular simulation J. Chem. Theor. Comput. 4 2008 116 122
37. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theor. Comput. 4 2008 435 447
38. J.B. Heymann, and A. Engel Aquaporins: phylogeny, structure, and physiology of water channels News Physiol. Sci. 14 1999 187 193
39. J.D. Ho, R. Yeh, A. Sandstrom, I. Chorny, W.E.C. Harries, R.A. Robbins, L.J.W. Miercke, and R.M. Stroud Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance Proc. Natl. Acad. Sci. USA 106 2009 7437 7442
40. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65 2006 712 725
41. R. Horsefield, K. Nordén, M. Fellert, A. Backmark, S. Törnroth-Horsefield, A.C.T.v. Scheltinga, J. Kvassman, P. Kjellbom, U. Johanson, and R. Neutze High-resolution x-ray structure of human aquaporin 5 Proc. Natl. Acad. Sci. USA 105 2008 13327 13332
42. J.S. Hub, and B.L. de Groot Mechanism of selectivity in aquaporins and aquaglyceroporins Proc. Natl. Acad. Sci. USA 105 2008 1198 1203
43. J.S. Hub, and B.L. de Groot Detection of functional modes in protein dynamics PLoS Comput. Biol. 5 2009 e1000480
44. J.S. Hub, H. Grubmüller, and B.L. de Groot Dynamics and energetics of permeation through aquaporins. What do we learn from molecular dynamics simulations? Handb. Exp. Pharmacol. 190 2009 57 76
45. L. Janosi, and M. Ceccarelli The gating mechanism of the human aquaporin 5 revealed by molecular dynamics simulations PLoS One 8 2013 e59897
46. R.P. Kraig, and M. Chesler Astrocytic acidosis in hyperglycemic and complete ischemia J. Cereb. Blood Flow Metab. 10 1990 104 114
47. T. Krivobokova, R. Briones, J.S. Hub, A. Munk, and B.L. de Groot Partial least-squares functional mode analysis: application to the membrane proteins AQP1, Aqy1, and CLC-ec1 Biophys. J. 103 2012 786 796
48. C. Lascola, and R.P. Kraig Astroglial acid-base dynamics in hyperglycemic and normoglycemic global ischemia Neurosci. Biobehav. Rev. 21 1997 143 150
49. J.K. Lee, D. Kozono, J. Remis, Y. Kitagawa, P. Agre, and R.M. Stroud Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 Å Proc. Natl. Acad. Sci. USA 102 2005 18932 18937
50. Y. Lin, Z. Cao, and Y. Mo Molecular dynamics simulations on the Escherichia coli ammonia channel protein AmtB: mechanism of ammonia/ammonium transport J. Am. Chem. Soc. 128 2006 10876 10884
51. T. Linder, B.L. de Groot, and A. Stary-Weinzinger Probing the energy landscape of activation gating of the bacterial potassium channel KcsA PLoS Comput. Biol. 9 2013 e1003058
52. K. Lindorff-Larsen, S. Piana, K. Palmo, P. Maragakis, J.L. Klepeis, R.O. Dror, and D.E. Shaw Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 78 2010 1950 1958
53. M. Lu, M.D. Lee, B.L. Smith, J.S. Jung, P. Agre, M.A. Verdijk, G. Merkx, J.P. Rijss, and P.M. Deen The human AQP4 gene: definition of the locus encoding two water channel polypeptides in brain Proc. Natl. Acad. Sci. USA 93 1996 10908 10912
54. A.K. Meinild, D.A. Klaerke, and T. Zeuthen Bidirectional water fluxes and specificity for small hydrophilic molecules in aquaporins 0-5 J. Biol. Chem. 273 1998 32446 32451
55. K. Murata, K. Mitsuoka, T. Hirai, T. Walz, P. Agre, J.B. Heymann, A. Engel, and Y. Fujiyoshi Structural determinants of water permeation through aquaporin-1 Nature 407 2000 599 605
56. K.L. Németh-Cahalan, and J.E. Hall pH and calcium regulate the water permeability of aquaporin 0 J. Biol. Chem. 275 2000 6777 6782
57. 2+ regulation of aquaporin water permeability J. Gen. Physiol. 123 2004 573 580
58. Z.E.R. Newby, J. O'Connell Iii, Y. Robles-Colmenares, S. Khademi, L.J. Miercke, and R.M. Stroud Crystal structure of the aquaglyceroporin PfAQP from the malarial parasite Plasmodium falciparum Nat. Struct. Mol. Biol. 15 2008 619 625
59. S. Nielsen, E.A. Nagelhus, M. Amiry-Moghaddam, C. Bourque, P. Agre, and O.P. Ottersen Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain J. Neurosci. 17 1997 171 180
60. R. Reale, N.J. English, J.-A. Garate, P. Marracino, M. Liberti, and F. Apollonio Human aquaporin 4 gating dynamics under and after nanosecond-scale static and alternating electric-field impulses: a molecular dynamics study of field effects and relaxation J. Chem. Phys. 139 2013 205101
61. F. Ringel, R.C. Chang, F. Staub, A. Baethmann, and N. Plesnila Contribution of anion transporters to the acidosis-induced swelling and intracellular acidification of glial cells J. Neurochem. 75 2000 125 132
62. R. Sachdeva, and B. Singh Insights into structural mechanisms of gating induced regulation of aquaporins Prog. Biophys. Mol. Biol. 114 2014 69 79
63. R. Sachdeva, and B. Singh Phosphorylation of Ser-180 of rat aquaporin-4 shows marginal affect on regulation of water permeability: molecular dynamics study J. Biomol. Struct. Dyn. 32 2014 555 566
64. D.F. Savage, P.F. Egea, Y. Robles-Colmenares, J.D. O'Connell, and R.M. Stroud Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z PLoS Biol. 1 2003 E72
65. O.S. Smart, J.M. Goodfellow, and B.A. Wallace The pore dimensions of gramicidin A Biophys. J. 65 1993 2455 2460
66. A.K. Stewart, M.N. Chernova, Y.Z. Kunes, and S.L. Alper Regulation of AE2 anion exchanger by intracellular pH: critical regions of the NH(2)-terminal cytoplasmic domain Am. J. Physiol. Cell Physiol. 281 2001 C1344 C1354
67. H. Sui, B.-G. Han, J.K. Lee, P. Walian, and B.K. Jap Structural basis of water-specific transport through the AQP1 water channel Nature 414 2001 872 878
68. S. Törnroth-Horsefield, Y. Wang, K. Hedfalk, U. Johanson, M. Karlsson, E. Tajkhorshid, R. Neutze, and P. Kjellbom Structural mechanism of plant aquaporin gating Nature 439 2006 688 694
69. A.S. Verkman Does aquaporin-1 pass gas? An opposing view J. Physiol. 542 2002 31
70. G. Vriend WHAT IF: a molecular modeling and drug design program J. Mol. Graph. 8 1990 52 56
71. Y. Wang, and E. Tajkhorshid Nitric oxide conduction by the brain aquaporin AQP4 Proteins 78 2010 661 670
72. A.M. Waterhouse, J.B. Procter, D.M.A. Martin, M. Clamp, and G.J. Barton Jalview version 2 - a multiple sequence alignment editor and analysis workbench Bioinformatics 25 2009 1189 1191
73. M.G. Wolf, M. Hoefling, C. Aponte-Santamaría, H. Grubmüller, and G. Groenhof g-membed: efficient insertion of a membrane protein into an equilibrated lipid bilayer with minimal perturbation J. Comput. Chem. 31 2010 2169 2174
74. M. Yasui, A. Hazama, T.H. Kwon, S. Nielsen, W.B. Guggino, and P. Agre Rapid gating and anion permeability of an intracellular aquaporin Nature 402 1999 184 187
75. J. Yu, A.J. Yool, K. Schulten, and E. Tajkhorshid Mechanism of gating and ion conductivity of a possible tetrameric pore in Aquaporin-1 Structure 14 2006 1411 1423
76. Z. Zador, S. Stiver, V. Wang, and G.T. Manley Role of aquaporin-4 in cerebral edema and stroke Handb. Exp. Pharmacol. 190 2009 159 170
77. G.A. Zampighi, M. Kreman, K.J. Boorer, D.D. Loo, F. Bezanilla, G. Chandy, J.E. Hall, and E.M. Wright A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes J. Membr. Biol. 148 1995 65 78
78. M. Zelenina, S. Zelenin, A.A. Bondar, H. Brismar, and A. Aperia Water permeability of aquaporin 4 is decreased by protein kinase C and dopamine Am. J. Physiol. Renal Physiol. 283 2002 F309 F318
79. M. Zelenina, A.A. Bondar, S. Zelenin, and A. Aperia Nickel and extracellular acidification inhibit the water permeability of human aquaporin-3 in lung epithelial cells J. Biol. Chem. 278 2003 30037 30043
80. + J. Biol. Chem. 274 1999 21631 21636
81. T. Zeuthen, B. Belhage, and E. Zeuthen Water transport by Na+-coupled cotransporters of glucose (SGLT1) and of iodide (NIS). The dependence of substrate size studied at high resolution J. Physiol. 570 2006 485 499
82. F. Zhu, E. Tajkhorshid, and K. Schulten Collective diffusion model for water permeation through microscopic channels Phys. Rev. Lett. 93 2004 224501