Gating in plant plasma membrane aquaporins: the involvement of leucine in the formation of a pore constriction in the closed state.
aquaporin
gating
leucine plug
molecular dynamics
water transport
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
09 2019
09 2019
Historique:
received:
18
02
2019
revised:
25
04
2019
accepted:
08
05
2019
pubmed:
12
5
2019
medline:
27
5
2020
entrez:
12
5
2019
Statut:
ppublish
Résumé
The control of water permeability in plant PIP2 aquaporins has become a paradigmatic case study of the capping mechanism for pore closure in water channels. From structural data, it has been postulated that the gating process in PIP2 involves a conformational rearrangement in cytosolic loopD that generates an obstruction to the transport of water molecules inside the aquaporin pore. BvPIP2;2 is a PIP2 aquaporin from Beta vulgaris whose pH response has been thoroughly characterized. In this work, we study the participation of Leu206 in BvPIP2;2 gating triggered by cytosolic acidification and show that this residue acts as a plug that blocks water transport. Based on data obtained from in silico and in vitro studies, we demonstrate that Leu206, one of the residues lining the pore, is responsible for ~ 60% of water blockage. Cell osmotic swelling experiments and atomistic molecular dynamics simulations indicate that the replacement of Leu206 by an Ala residue maintains high water permeability under conditions where the pore is expected to be closed. The present work demonstrates that Leu206, located at the cytoplasmic entry of the channel, constitutes a crucial pH-sensitive steric gate regulating water transport in PIP aquaporins.
Substances chimiques
Aquaporins
0
Plant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3473-3487Subventions
Organisme : ANPCYT
ID : PICT 2017-0244
Pays : International
Organisme : ANPCYT
ID : PICT 2015-2761
Pays : International
Organisme : UBA
ID : UBACYT 20020170100178BA01
Pays : International
Organisme : UBA
ID : UBACYT 20020120300025B
Pays : International
Organisme : UNHAUR
ID : PIUNHAUR-5 2018
Pays : International
Organisme : Agencia Nacional de Investigación e Innovación (ANII)
Pays : International
Informations de copyright
© 2019 Federation of European Biochemical Societies.
Références
Agre P (2006) The aquaporin water channels. Proc Am Thorac Soc 3, 5-13.
Fujiyoshi Y, Mitsuoka K, de Groot BL, Philippsen A, Grubmüller H, Agre P & Engel A (2002) Structure and function of water channels. Curr Opin Struct Biol 12, 509-515.
Anderberg HI, Kjellbom P & Johanson U (2012) Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Front Plant Sci 3, 33.
Chaumont F & Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164, 1600-1618.
Maurel C, Boursiac Y, Luu D, Santoni V, Shahzad Z & Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95, 1321-1358.
Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A & Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407, 599-605.
Sui H, Han BG, Lee JK, Walian P & Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414, 872-878.
Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P, Krucinski J & Stroud RM (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486.
Harries WEC, Akhavan D, Miercke LJW, Khademi S & Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci USA 101, 14045-14050.
Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R & Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439, 688-694.
Newby ZER, O'Connell J III, Robles-Colmenares Y, Khademi S, Miercke LJ & Stroud RM (2008) Crystal structure of the aquaglyceroporin PfAQP from the malarial parasite Plasmodium falciparum. Nat Struct Mol Biol 15, 619-625.
Frick A, Eriksson UK, de Mattia F, Oberg F, Hedfalk K, Neutze R, de Grip WJ, Deen PMT & Törnroth-Horsefield S (2014) X-ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking. Proc Natl Acad Sci USA 111, 6305-6310.
Kirscht A, Kaptan S, Bienert G, Chaumont F, Nissen P, De Groot D, Kjellbom P, Gourdon P & Johanson U (2016) Crystal structure of an ammonia-permeable aquaporin. PLoS Biol 14, e1002411.
Preston GM, Jung JS, Guggino WB & Agre P (1994) Membrane topology of aquaporin CHIP. Analysis of functional epitope-scanning mutants by vectorial proteolysis. J Biol Chem 269, 1668-1673.
Hedfalk K, Törnroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P & Neutze R (2006) Aquaporin gating. Curr Opin Struct Biol 16, 447-456.
Nyblom M, Frick A, Wang Y, Ekvall M, Hallgren K, Hedfalk K, Neutze R, Tajkhorshid E & Törnroth-Horsefield S (2009) Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J Mol Biol 387, 653-668.
Fischer M & Kaldenhoff R (2008) On the pH regulation of plant aquaporins. J Biol Chem 283, 33889-33892.
Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P & Maurel C (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 30, 71-81.
Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DTD-T, Bligny R & Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393-397.
Alleva K, Niemietz CM, Sutka M, Maurel C, Parisi M, Tyerman SD & Amodeo G (2006) Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 57, 609-621.
Verdoucq L, Grondin A & Maurel C (2008) Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons. Biochem J 415, 409-416.
Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C & Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10, 451-459.
Kaptan S, Assentoft M, Schneider HP, Fenton RA, Deitmer JW, MacAulay N & De Groot BL (2015) H95 is a pH-dependent gate in aquaporin 4. Structure 23, 2309-2318.
Mósca A, de Almeida A, Wragg D, Martins A, Sabir F, Leoni S, Moura T, Prista C, Casini A & Soveral G (2018) Molecular basis of aquaporin-7 permeability regulation by pH. Cells 7, 207.
Soto G, Fox R, Ayub N, Alleva K, Guaimas F, Erijman EJ, Mazzella A, Amodeo G & Muschietti J (2010) TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is likely involved in nitrogen remobilization in Arabidopsis thaliana. Plant J 64, 1038-1047.
Leitão L, Prista C, Moura TF, Loureiro-Dias MC & Soveral G (2012) Grapevine aquaporins: gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH. PLoS One 7, e33219.
Rodrigues C, Mósca AF, Martins AP, Nobre T, Prista C, Antunes F, Gasparovic AC & Soveral G (2016) Rat aquaporin-5 is pH-gated induced by phosphorylation and is implicated in oxidative stress. Int J Mol Sci 17, 2090.
Zeuthen T & Klaerke DA (1999) Transport of water and glycerol in aquaporin 3 is gated by H(+). J Biol Chem 274, 21631-21636.
Alleva K, Marquez M, Villarreal N, Mut P, Bustamante C, Bellati J, Martínez G, Civello M & Amodeo G (2010) Cloning, functional characterization, and co-expression studies of a novel aquaporin (FaPIP2;1) of strawberry fruit. J Exp Bot 61, 3935-3945.
Bellati J, Alleva K, Soto G, Vitali V, Jozefkowicz C & Amodeo G (2010) Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol Biol 74, 105-118.
Jozefkowicz C, Sigaut L, Scochera F, Soto G, Ayub N, Pietrasanta LI, Amodeo G & González Flecha FL (2016) PIP water transport and its pH dependence are regulated by tetramer stoichiometry. Biophys J 110, 1312-1321.
Yaneff A, Sigaut L, Marquez M, Alleva K, Pietrasanta LI & Amodeo G (2014) Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci USA 111, 231-236.
Shelden MC, Howitt SM, Kaiser BN & Tyerman SD (2009) Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. Funct Plant Biol 36, 1065-1078.
Frick A, Järvå M & Törnroth-Horsefiel S (2013) Structural basis for pH gating of plant aquaporins. FEBS Lett 587, 989-993.
Vitali V, Jozefkowicz C, Canessa Fortuna A, Soto G, González Flecha FL & Alleva K (2019) Cooperativity in proton sensing by PIP aquaporins. FEBS J 286, 991-1002.
Horsefield R, Norden K, Fellert M, Backmark A, Tornroth-Horsefield S, Terwisscha van Scheltinga AC, Kvassman J, Kjellbom P, Johanson U & Neutze R (2008) High-resolution x-ray structure of human aquaporin 5. Proc Natl Acad Sci USA 105, 13327-13332.
Horner A, Zocher F, Preiner J, Ollinger N, Siligan C, Akimov SA & Pohl P (2015) The mobility of single-file water molecules is governed by the number of H-bonds they may form with channel-lining residues. Sci Adv 1, 1-6.
Xin L, Su H, Nielsen CH, Tang C, Torres J & Mu Y (2011) Water permeation dynamics of AqpZ: a tale of two states. Biochim Biophys Acta 1808, 1581-1586.
Zhu F, Tajkhorshid E & Schulten K (2004) Theory and simulation of water permeation in aquaporin-1. Biophys J 86, 50-57.
Khandelia H, Jensen MOØ & Mouritsen OG (2009) To gate or not to gate: using molecular dynamics simulations to morph gated plant aquaporins into constitutively open conformations. J Phys Chem B 113, 5239-5244.
Fetter K, Van Wilder V, Moshelion M & Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16, 215-228.
Jozefkowicz C, Berny MC, Chaumont F & Alleva K (2017) Heteromerization of plant aquaporins. In Plant Aquaporins, From Transport to Signalling (Chaumont F & Tyerman S, eds), pp. 29-46. Springer, Berlin.
Berny MC, Gilis D, Rooman M & Chaumont F (2016) Single mutations in the transmembrane domains of maize plasma membrane aquaporins affect the activity of monomers within a heterotetramer. Mol Plant 9, 986-1003.
Vajpai M, Mukherjee M & Sankararamakrishnan R (2018) Cooperativity in plant plasma membrane intrinsic proteins (PIPs): mechanism of increased water transport in maize PIP1 channels in hetero-tetramers. Sci Rep 8, 12055.
Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M, Belastegui-Macadam X, Heckwolf M, Lachnit M, Pede N, Priem N et al. (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 285, 31253-31260.
Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW, Qiu J, Gilliham M, Schultz C, Schwarz M, Ramesh SA et al. (2016) Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant, Cell Environ 40, 802-815.
Fischer G, Kosinska-Eriksson U, Aponte-Santamaría C, Palmgren M, Geijer C, Hedfalk K, Hohmann S, de Groot BL, Neutze R & Lindkvist-Petersson K (2009) Crystal structure of a yeast aquaporin at 1.15 angstrom reveals a novel gating mechanism. PLoS Biol 7, e1000130.
Aponte-Santamaría C, Fischer G, Bath P, Neutze R & De Groot BL (2017) Temperature dependence of protein-water interactions in a gated yeast aquaporin. Sci Rep 7, 1-14.
Nyblom M & Tornroth-Horsefield S (2016) Regulation of eukaryotic aquaporins. In Aquaporins in Health and Disease: New Molecular Targets for Drug Discovery (Graca S, Nielsen S & Casini A, eds), pp. 53-76. CRC Press, Taylor & Francis Group, Boca Raton, FL.
Gonen T, Sliz P, Kistler J, Cheng Y & Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429, 193-197.
Reichow SL, Clemens DM, Freites JA, Németh-Cahalan KL, Heyden M, Tobias DJ, Hall JE & Gonen T (2013) Allosteric mechanism of water-channel gating by Ca2+-calmodulin. Nat Struct Mol Biol 20, 1085-1092.
Saboe PO, Rapisarda C, Kaptan S, Hsiao YS, Summers SR, De Zorzi R, Dukovski D, Yu J, de Groot BL, Kumar M et al. (2017) Role of pore-lining residues in defining the rate of water conduction by aquaporin-0. Biophys J 112, 953-965.
Janosi L & Ceccarelli M (2013) The gating mechanism of the human aquaporin 5 revealed by molecular dynamics simulations. PLoS One 8, e59897.
Alberga D, Nicolotti O, Lattanzi G, Nicchia GP, Frigeri A, Pisani F, Benfenati V & Mangiatordi GF (2014) A new gating site in human aquaporin-4: insights from molecular dynamics simulations. Biochim Biophys Acta 1838, 3052-3060.
Gotfryd K, Mósca AF, Missel JW & Truelsen SF (2018) Human adipose glycerol flux is regulated by a pH gate in AQP10. Nat Commun 9, 47-49.
Beckstein O, Biggin PC & Sansom MSP (2001) A hydrophobic gating mechanism for nanopores. J Phys Chem B 105, 12902-12905.
Zhu F & Hummer G (2012) Drying transition in the hydrophobic gate of the GLIC channel blocks ion conduction. Biophys J 103, 219-227.
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7, 539.
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, De Beer TAP, Rempfer C, Bordoli L et al. (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46, 296-303.
Jo S, Kim T, Iyer WG & Im W (2008) CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem 29, 1859-1865.
Wu EL, Cheng X, Jo S, Rui H, Song KC, Dávila-Contreras EM, Qi Y, Lee J, Monje-Galvan V, Venable RM et al. (2014) CHARMM-GUI membrane builder toward realistic biological membrane simulations. J Comput Chem 35, 1997-2004.
Jo S, Lim JB, Klauda JB & Im W (2009) CHARMM-GUI membrane builder for mixed bilayers and its application to yeast membranes. Biophys J 97, 50-58.
Jo S, Kim T & Im W (2007) Automated builder and database of protein/membrane complexes for molecular dynamics simulations. PLoS One 2, e880.
Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW & Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79, 461-470.
Case D, Babin V, Berryman J, Betz R, Cai Q, Cerutti D, Cheatham T, Darden T, Duke R, Gohlke H et al. (2014) AMBER 14. University of California, San Francisco, CA.
Case DA, Betz RM, Cerutti DS, Cheatham TE III, Darden TA, Duke RE, Giese TJ, Gohlke H, Goetz AW, Homeyer N et al. (2016) AMBER 16. University of California, San Francisco, CA.
Maier JA, Martinez C, Kasavajhala K, Wickstrom L, Hauser K & Simmerling C (2015) ff14SB : improving the accuracy of protein side chain and backbone parameters from ff99SB. J Chem Theory Comput 11, 3696-3713.
Gowers R, Linke M, Barnoud J, Reddy T, Melo M, Seyler S, Domański J, Dotson D, Buchoux S, Kenney I et al. (2016) MDAnalysis: a Python package for the rapid analysis of molecular dynamics simulations. In Proceedings of the 15th Python in Science Conference (Benthall S & Rostrup S, eds), pp. 98-105. Austin, TX. http://conference.scipy.org/proceedings/scipy2016/
Michaud-Agrawal N, Denning EJ, Woolf TB & Beckstein O (2011) MDAnalysis: a toolkit for the analysis of molecular dynamics simulations. J Comput Chem 32, 2319-2327.
Smart OS, Neduvelil JG, Wang X, Wallace BA & Sansom MSP (1996) HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 14, 354-360.
Zhu F, Tajkhorshid E & Schulten K (2004) Collective diffusion model for water permeation through microscopic channels. Phys Rev Lett 93, 1-4.
Jozefkowicz C, Rosi P, Sigaut L, Soto G, Pietrasanta LI, Amodeo G & Alleva K (2013) Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins. PLoS One 8, e57993.
Zhang RB & Verkman AS (1991) Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol 260, C26-C34.
Yaneff A, Sigaut L, Gómez N, Aliaga Fandiño C, Alleva K, Pietrasanta LI & Amodeo G (2016) Loop B serine of a plasma membrane aquaporin type PIP2 but not PIP1 plays a key role in pH sensing. Biochim Biophys Acta 1858, 2778-2787.