Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 1, 2012, Pages 1-11

  Azad, Abul Kalam ^a,b   Yoshikawa, Naoki ^a   Ishikawa, Takahiro ^a   Sawa, Yoshihiro ^a   Shibata, Hitoshi ^a  

^a SHIMANE UNIVERSITY   (Japan)

^b SHAHJALAL UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Bangladesh)

Author keywords

Aquaporin; ar R selectivity filter; TgTIP; TIP homolog; Transport selectivity; Water channel activity

Indexed keywords

AQUAPORIN; ARGININE; CELL PROTEIN; COMPLEMENTARY DNA; HYDROGEN PEROXIDE; ISOLEUCINE; TONOPLAST INTRINSIC PROTEIN; UNCLASSIFIED DRUG; VALINE;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARTICLE; DNA SYNTHESIS; ENZYME SPECIFICITY; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PETAL; PHYLOGENETIC TREE; PICHIA PASTORIS; PLANT GROWTH; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; SPHEROPLAST; SURVIVAL; TONOPLAST; TULIP;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; AQUAPORINS; ARABIDOPSIS; BIOLOGICAL TRANSPORT; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PICHIA; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSDUCTION, GENETIC; TULIPA; WATER; ZEA MAYS;

ARABIDOPSIS; PICHIA PASTORIS; TULIPA; TULIPA GESNERIANA;

EID: 80054093905     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.09.014     Document Type: Article

References (61)

1. P. Agre, M. Bonhivers, and M.J. Borgnia The aquaporins, blueprints for cellular plumbing systems J. Biol. Chem. 273 1998 14659 14662 (Pubitemid 28272745)
2. D. Gomes, A. Agasse, P. Thiebaud, S. Delrot, H. Geros, and F. Chaumont Aquaporins are multifunctional water and solute transporters highly divergent in living organisms Biochim. Biophys. Acta 1788 2009 1213 1228
3. K. Jeyaseelan, S. Sepramaniam, A. Armugam, and E.M. Wintour Aquaporins: a promising target for drug development Expert Opin. Ther. Targets 10 2006 889 909 (Pubitemid 44816751)
4. J. Sakurai, F. Ishikawa, T. Yamaguchi, M. Uemura, and M. Maeshima Identification of 33 rice aquaporin genes and analysis of their expression and function Plant Cell Physiol. 46 2005 1568 1577 (Pubitemid 41436599)
5. A. Bansal, and R. Sankararamakrishnan Homology modeling of major intrinsic proteins in rice, maize and Arabidopsis: comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters BMC Struct. Biol. 7 2007 27
6. U. Johanson, M. Karlsson, I. Johansson, S. Gustavsson, S. Sjovall, L. Fraysse, A.R. Weig, and P. Kjellbom 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 2001 1358 1369 (Pubitemid 32752366)
7. F. Chaumont, F. Barrieu, E. Wojcik, M.J. Chrispeels, and R. Jung Aquaporins constitute a large and highly divergent protein family in maize Plant Physiol. 125 2001 1206 1215 (Pubitemid 32224611)
8. A.B. Gupta, and R. Sankararamakrishnan Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective BMC Plant Biol. 9 2009 134
9. C. Maurel, L. Verdoucq, D.T. Luu, and V. Santoni Plant aquaporins: membrane channels with multiple integrated functions Annu. Rev. Plant Biol. 59 2008 595 624 (Pubitemid 351813044)
10. P. Martre, R. Morillon, F. Barrieu, G.B. North, P.S. Nobel, and M.J. Chrispeels Plasma membrane aquaporins play a significant role during recovery from water deficit Plant Physiol. 130 2002 2101 2110 (Pubitemid 36035206)
11. C. Tournaire-Roux, M. Sutka, H. Javot, E. Gout, P. Gerbeau, D.T. Luu, R. Bligny, and C. Maurel Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins Nature 425 2003 393 397 (Pubitemid 37187267)
12. N. Uehlein, and R. Kaldenhoff Aquaporins and plant leaf movements Ann. Bot. 101 2008 1 4 (Pubitemid 350274513)
13. R.B. Heinen, Q. Ye, and F. Chaumont Role of aquaporins in leaf physiology J. Exp. Bot. 60 2009 2971 2985
14. F. Chaumont, F. Barrieu, E.M. Herman, and M.J. Chrispeels Characterization of a maize tonoplast aquaporin expressed in zones of cell division and elongation Plant Physiol. 117 1998 1143 1152 (Pubitemid 128652887)
15. A.K. Azad, Y. Sawa, T. Ishikawa, and H. Shibata Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals Plant Cell Physiol. 45 2004 608 617 (Pubitemid 38791244)
16. A.K. Azad, M. Katsuhara, Y. Sawa, T. Ishikawa, and H. Shibata Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation Plant Cell Physiol. 49 2008 1196 1208
17. H.B. Shao, L.Y. Chu, M.A. Shao, and C.X. Zhao Advances in functional regulation mechanisms of plant aquaporins: their diversity, gene expression, localization, structure and roles in plant soil-water relations (Review) Mol. Membr. Biol. 25 2008 179 191
18. H.B. Shao, L.Y. Chu, C.A. Jaleel, P. Manivannan, R. Panneerselvam, and M.A. Shao Understanding water deficit stress-induced changes in the basic metabolism of higher plants - biotechnologically and sustainably improving agriculture and the ecoenvironment in arid regions of the globe Crit. Rev. Biotechnol. 29 2009 131 151
19. C. Hachez, and F. Chaumont Aquaporins: a family of highly regulated multifunctional channels Adv. Exp. Med. Biol. 679 2010 1 17
20. M.M. Wudick, D.T. Luu, and C. Maurel A look inside: localization patterns and functions of intracellular plant aquaporins New Phytol. 184 2009 289 302
21. G.W. Li, Y.H. Peng, X. Yu, M.H. Zhang, W.M. Cai, W.N. Sun, and W.A. Su Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice J. Plant Physiol. 165 2008 1879 1888
22. P. Gerbeau, J. Guclu, P. Ripoche, and C. Maurel Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes Plant J. 18 1999 577 587
23. F. Klebl, M. Wolf, and N. Sauer A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana δ-TIP or γ-TIP FEBS Lett. 547 2003 69 74 (Pubitemid 36829380)
24. L.H. Liu, U. Ludewig, B. Gassert, W.B. Frommer, and N. von Wiren Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis Plant Physiol. 133 2003 1220 1228 (Pubitemid 37458020)
25. G. Soto, K. Alleva, M.A. Mazzella, G. Amodeo, and J.P. Muschietti AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea FEBS Lett. 582 2008 4077 4082
26. T.P. Jahn, A.L. Moller, T. Zeuthen, L.M. Holm, D.A. Klaerke, B. Mohsin, W. Kuhlbrandt, and J.K. Schjoerring Aquaporin homologues in plants and mammals transport ammonia FEBS Lett. 574 2004 31 36 (Pubitemid 39200890)
27. 3-pore in Aquaporin TIP2;2 from wheat FEBS Lett. 581 2007 5413 5417 (Pubitemid 350101516)
28. 3 transport into the vacuole Plant Physiol. 137 2005 671 680 (Pubitemid 43126695)
29. M. Dynowski, M. Mayer, O. Moran, and U. Ludewig Molecular determinants of ammonia and urea conductance in plant aquaporin homologs FEBS Lett. 582 2008 2458 2462
30. G.P. Bienert, A.L. Moller, K.A. Kristiansen, A. Schulz, I.M. Moller, J.K. Schjoerring, and T.P. Jahn Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes J. Biol. Chem. 282 2007 1183 1192 (Pubitemid 47076557)
31. I.S. Wallace, and D.M. Roberts Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter Plant Physiol. 135 2004 1059 1068 (Pubitemid 38819049)
32. E. Tajkhorshid, P. Nollert, M.O. Jensen, L.J. Miercke, J. O'Connell, R.M. Stroud, and K. Schulten Control of the selectivity of the aquaporin water channel family by global orientational tuning Science 296 2002 525 530 (Pubitemid 34413590)
33. D. Fu, A. Libson, L.J. 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
34. 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 (Pubitemid 34024731)
35. I.S. Wallace, and D.M. Roberts Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels Biochemistry 44 2005 16826 16834 (Pubitemid 43007211)
36. M.J. Daniels, and M. Yeager Phosphorylation of aquaporin PvTIP3;1 defined by mass spectrometry and molecular modeling Biochemistry 44 2005 14443 14454 (Pubitemid 41567452)
37. A.K. Azad, Y. Sawa, T. Ishikawa, and H. Shibata Heterologous expression of tulip petal plasma membrane aquaporins in Pichia pastoris for water channel analysis Appl. Environ. Microbiol. 75 2009 2792 2797
38. M.J. Tamas, K. Luyten, F.C. Sutherland, A. Hernandez, J. Albertyn, H. Valadi, H. Li, B.A. Prior, S.G. Kilian, J. Ramos, L. Gustafsson, J.M. Thevelein, and S. Hohmann Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation Mol. Microbiol. 31 1999 1087 1104 (Pubitemid 29082239)
39. +-pyrophosphatase J. Biol. Chem. 276 2001 7654 7660
40. D.F. Savage, and R.M. Stroud Structural basis of aquaporin inhibition by mercury J. Mol. Biol. 368 2007 607 617 (Pubitemid 46527629)
41. D. Kozono, X. Ding, I. Iwasaki, X. Meng, Y. Kamagata, P. Agre, and Y. Kitagawa Functional expression and characterization of an archaeal aquaporin. AqpM from Methanothermobacter marburgensis J. Biol. Chem. 278 2003 10649 10656 (Pubitemid 36805604)
42. G. Calamita, D. Ferri, P. Gena, G.E. Liquori, A. Cavalier, D. Thomas, and M. Svelto The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water J. Biol. Chem. 280 2005 17149 17153 (Pubitemid 41389180)
43. K. Liu, H. Nagase, C.G. Huang, G. Calamita, and P. Agre Purification and functional characterization of aquaporin-8 Biol. Cell 98 2006 153 161 (Pubitemid 43336807)
44. S. Tornroth-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 (Pubitemid 43237610)
45. P.A. Balk, and A.D. de Boer Rapid stalk elongation in tulip (Tulipa gesneriana L. cv. Apeldoorn) and the combined action of cold-induced invertase and the water-channel protein γTIP Planta 209 1999 346 354
46. G. Fischer, U. Kosinska-Eriksson, C. Aponte-Santamaria, M. Palmgren, C. Geijer, K. Hedfalk, S. Hohmann, B.L. de Groot, R. Neutze, and K. Lindkvist-Petersson Crystal structure of a yeast aquaporin at 1.15 angstrom reveals a novel gating mechanism PLoS Biol. 7 2009 e1000130
47. 2 Biochem. J. 414 2008 53 61
48. R.M. Stroud, D. Savage, L.J. Miercke, J.K. Lee, S. Khademi, and W. Harries Selectivity and conductance among the glycerol and water conducting aquaporin family of channels FEBS Lett. 555 2003 79 84 (Pubitemid 37431101)
49. M.J. Daniels, M.R. Wood, and M. Yeager In vivo functional assay of a recombinant aquaporin in Pichia pastoris Appl. Environ. Microbiol. 72 2006 1507 1514 (Pubitemid 43271265)
50. + permeability in aquaporin-expressing Xenopus oocytes Pflugers Arch. 450 2005 415 428 (Pubitemid 41380700)
51. S. Kojima, A. Bohner, and N. von Wiren Molecular mechanisms of urea transport in plants J. Membr. Biol. 212 2006 83 91 (Pubitemid 46292324)
52. E. Martinoia, M. Maeshima, and H.E. Neuhaus Vacuolar transporters and their essential role in plant metabolism J. Exp. Bot. 58 2007 83 102 (Pubitemid 46026250)
53. P.H. Nord-Larsen, T. Kichey, T.P. Jahn, C.S. Jensen, K.K. Nielsen, J.N. Hegelund, and J.K. Schjoerring Cloning, characterization and expression analysis of tonoplast intrinsic proteins and glutamine synthetase in ryegrass (Lolium perenne L.) Plant Cell Rep. 28 2009 1549 1562
54. B.G. Han, A.B. Guliaev, P.J. Walian, and B.K. Jap Water transport in AQP0 aquaporin: molecular dynamics studies J. Mol. Biol. 360 2006 285 296 (Pubitemid 43927822)
55. F. Zhu, E. Tajkhorshid, and K. Schulten Theory and simulation of water permeation in aquaporin-1 Biophys. J. 86 2004 50 57 (Pubitemid 38071799)
56. C. Maurel, J. Reizer, J.I. Schroeder, and M.J. Chrispeels The vacuolar membrane protein γ-TIP creates water specific channels in Xenopus oocytes EMBO J. 12 1993 2241 2247 (Pubitemid 23194173)
57. A.K. Azad, T. Ishikawa, Y. Sawa, and H. Shibata Intracellular energy depletion triggers programmed cell death during petal senescence in tulip J. Exp. Bot. 59 2008 2085 2095 (Pubitemid 351809645)
58. S.M. McInnis, R. Desikan, J.T. Hancock, and S.J. Hiscock Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytol. 172 2006 221 228 (Pubitemid 44414110)
59. A.R. Ros Barcelo, L.V. Gomes-Ros, C. Gabaldon, M. Lopez-Serrano, F. Pomar, J.S. Carrion, and M.A. Pedreno Basic peroxidase: the gateway for lignin evolution? Phytochem. Rev. 3 2004 61 78 (Pubitemid 41184541)
60. M.J. Daniels, F. Chaumont, T.E. Mirkov, and M.J. Chrispeels Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site Plant Cell 8 1996 587 599 (Pubitemid 126632543)
61. K. Tamura, J. Dudley, M. Nei, and S. Kumar MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 Mol. Biol. Evol. 24 2007 1596 1599 (Pubitemid 47236692)