PIP aquaporin pH-sensing is regulated by the length and charge of the C-terminal region.


Journal

The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646

Informations de publication

Date de publication:
01 2022
Historique:
revised: 01 07 2021
received: 19 05 2021
accepted: 21 07 2021
pubmed: 23 7 2021
medline: 26 2 2022
entrez: 22 7 2021
Statut: ppublish

Résumé

Plant PIP aquaporins play a central role in controlling plant water status. The current structural model for PIP pH-gating states that the main pH sensor is located in loopD and that all the mobile cytosolic elements participate in a complex interaction network that ensures the closed structure. However, the precise participation of the last part of the C-terminal domain (CT) in PIP pH gating remains unknown. This last part has not been resolved in PIP crystal structures and is a key difference between PIP1 and PIP2 paralogues. Here, by a combined experimental and computational approach, we provide data about the role of CT in pH gating of Beta vulgaris PIP. We demonstrate that the length of CT and the positive charge located among its last residues modulate the pH at which the open/closed transition occurs. We also postulate a molecular-based mechanism for the differential pH sensing in PIP homo- or heterotetramers by performing atomistic molecular dynamics simulations (MDS) on complete models of PIP tetramers. Our findings show that the last part of CT can affect the environment of loopD pH sensors in the closed state. Results presented herein contribute to the understanding of how the characteristics of CT in PIP channels play a crucial role in determining the pH at which water transport through these channels is blocked, highlighting the relevance of the differentially conserved very last residues in PIP1 and PIP2 paralogues.

Identifiants

pubmed: 34293244
doi: 10.1111/febs.16134
doi:

Substances chimiques

Aquaporins 0
Membrane Proteins 0
Plant Proteins 0
Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

246-261

Informations de copyright

© 2021 Federation of European Biochemical Societies.

Références

Verdoucq L & Maurel C (2018) Chapter Two - Plant aquaporins. In Advances in Botanical Research (Maurel C, ed.), 1st edn, Vol. 87, pp. 25-56. Academic Press. https://www.sciencedirect.com/science/article/pii/S0065229618300557
Chaumont F & Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164, 1600-1618.
Jozefkowicz C, Berny MC, Chaumont F & Alleva K (2017) Heteromerization of plant aquaporins. In Signaling and Communication in Plants (Chaumont F & Tyerman S, eds), pp. 29-46. Springer, Cham. https://doi.org/10.1007/978-3-319-49395-4_2
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.
Frick A, Järvå M & Törnroth-Horsefiel S (2013) Structural basis for pH gating of plant aquaporins. FEBS Lett 587, 989-993.
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.
Bienert MD, Diehn TA, Richet N, Chaumont F & Bienert GP (2018) Heterotetramerization of Plant PIP1 and PIP2 aquaporins is an evolutionary ancient feature to guide PIP1 plasma membrane localization and function. Front Plant Sci 9, 1-15.
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.
Soto G, Alleva K, Amodeo G, Muschietti J & Ayub ND (2012) New insight into the evolution of aquaporins from flowering plants and vertebrates: Orthologous identification and functional transfer is possible. Gene 503, 165-176.
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 111, 231-236.
Jozefkowicz C, Sigaut L, Scochera F, Soto G, Ayub N, Pietrasanta LI, Amodeo G, González Flecha FL & Alleva K (2016) PIP water transport and its pH dependence are regulated by tetramer stoichiometry. Biophys J 110, 1312-1321.
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.
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.
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.
Bienert GP, Cavez D, Besserer A, Berny MC, Gilis D, Rooman M & Chaumont F (2012) A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem J 445, 101-111.
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.
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.
Canessa Fortuna A, Zerbetto De Palma G, Aliperti Car L, Armentia L, Vitali V, Zeida A, Estrin DA & Alleva K (2019) Gating in plant plasma membrane aquaporins: the involvement of leucine in the formation of a pore constriction in the closed state. FEBS J 286, 3473-3487.
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. https://doi.org/10.1074/jbc.m803865200
Wang H, Schoebel S, Schmitz F, Dong H & Hedfalk K (2020) Characterization of aquaporin-driven hydrogen peroxide transport. BBA - Biomembr 1862, 183065.
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.
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.
Prak S, Hem S, Boudet J, Viennois G, Sommerer N, Rossignol M, Maurel C & Santoni V (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins. Mol Cell Proteomics 7, 1019-1030. https://doi.org/10.1074/mcp.m700566-mcp200
Tyerman SD, McGaughey SA, Qiu J, Yool AJ & Byrt CS (2021) Adaptable and multifunctional ion-conducting aquaporins. Annu Rev Plant Biol 72, 1-34.
Qiu J, McGaughey SA, Groszmann M, Tyerman SD & Byrt CS (2020) Phosphorylation influences water and ion channel function of AtPIP2;1. Plant Cell Environ 43, 2428-2442.
Glitsos G (2017) N- and C-terminal domains in tobacco aquaporins -Analysis of protein-mediated water permeability in vitro and in silico. Darmstadt, Technische Universität Darmstadt, [Ph.D. Thesis]. https://tuprints.ulb.tu-darmstadt.de/id/eprint/6124
Shibasaka M, Horie T & Katsuhara M (2021) Mechanisms activating latent functions of PIP aquaporin water channels via the interaction between PIP1 and PIP2 proteins. Plant Cell Physiol 62, 92-99. https://doi.org/10.1093/pcp/pcaa142
Zelazny E, Miecielica U, Borst JW, Hemminga MA & Chaumont F (2009) An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 57, 346-355.
Jozefkowicz C, Scochera F & Alleva K (2016) Two aquaporins, multiple ways of assembly. Channels 10, 438-439.
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.
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.
Fox AR, Scochera F, Laloux T, Filik K, Degand H, Morsomme P, Alleva K & Chaumont F (2020) Plasma membrane aquaporins interact with the endoplasmic reticulum resident VAP27 proteins at ER-PM contact sites and endocytic structures. New Phytol 228, 973-988.
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.
Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G, Maurel C & Santoni V (2016) Novel aquaporin regulatory mechanisms revealed by interactomics. Mol Cell Proteomics 15, 3473-3487.
Prado K, Cotelle V, Li G, Bellati J, Tang N, Tournaire-Roux C, Martinière A, Santoni V & Maurela C (2019) Oscillating aquaporin phosphorylation and 14-3-3 proteins mediate the circadian regulation of leaf hydraulics. Plant Cell 31, 417-429.
Shen W, Le S, Li Y & Hu F (2016) SeqKit: A cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS One 11, 1-10.
Waterhouse AM, Procter JB, Martin DMA, Clamp M & Barton GJ (2009) Jalview Version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191. https://doi.org/10.1093/bioinformatics/btp033
Zhang R & Verkman AS (1991) Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol Cell Physiol 260, C26-C34.
Webb B & Sali A (2016) Comparative protein structure modeling using MODELLER. Curr Protoc Bioinforma 54, 5.6.1-5.6.37.
Song Y, Dimaio F, Wang RYR, Kim D, Miles C, Brunette T, Thompson J & Baker D (2013) High-resolution comparative modeling with RosettaCM. Structure 21, 1735-1742.
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, W296-W303. https://doi.org/10.1093/nar/gky427
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.
Humphrey W, Dalke A & Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14, 33-38.
Case D, Ben-Shalom IY, Brozell SR, Cerutti DS, Cheatham TEI, Cruzeiro VW, Darden TA, Duke RE, Ghoreishi D, Gilson MK et al. (2018) AMBER 18. University of California, San Francisco.
Maier JA, Martinez C, Kasavajhala K, Wickstrom L, Hauser KE & Simmerling C (2015) ff14SB : improving the accuracy of protein side chain and backbone parameters from ff99SB. J Chem Theory Comput 11, 3696-3713. https://doi.org/10.1021/acs.jctc.5b00255
Dickson CJ, Madej BD, Skjevik ÅA, Betz RM, Teigen K, Gould IR & Walker RC (2014) Lipid14: the amber lipid force field. J Chemital Theory Comput 10, 865-879.
Martínez L (2015) Automatic identification of mobile and rigid substructures in molecular dynamics simulations and fractional structural fluctuation analysis. PLoS One 10, 1-10.
Socher E & Sticht H (2016) Mimicking titration experiments with MD simulations: a protocol for the investigation of pH-dependent effects on proteins. Sci Rep 6, 1-13.

Auteurs

Florencia Scochera (F)

Facultad de Farmacia y Bioquímica, Departamento de Fisicomatemática, Universidad de Buenos Aires, Argentina.

Gerardo Zerbetto De Palma (G)

Facultad de Farmacia y Bioquímica, Departamento de Fisicomatemática, Universidad de Buenos Aires, Argentina.
Instituto de Química y Fisicoquímica Biológica (IQUIFIB), Facultad de Farmacia y Bioquímica, CONICET, Universidad de Buenos Aires, Argentina.
Instituto de Biotecnología, Universidad Nacional de Hurlingham, Villa Tesei, Argentina.

Agustina Canessa Fortuna (A)

Facultad de Farmacia y Bioquímica, Departamento de Fisicomatemática, Universidad de Buenos Aires, Argentina.

Jonathan Chevriau (J)

Instituto de Química y Fisicoquímica Biológica (IQUIFIB), Facultad de Farmacia y Bioquímica, CONICET, Universidad de Buenos Aires, Argentina.

Roxana Toriano (R)

Facultad de Medicina, CONICET, Instituto de Fisiología y Biofísica "Bernardo Houssay" (IFIBIO "Houssay"), Universidad de Buenos Aires, Argentina.

Gabriela Soto (G)

Instituto de Agrobiotecnología y Biología Molecular (INTA-CONICET), Buenos Aires, Argentina.
Instituto de Genética (INTA), Buenos Aires, Argentina.

Ari Zeida (A)

Departamento de Bioquímica and Centro de Investigaciones Biomédicas (Ceinbio), Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.

Karina Alleva (K)

Facultad de Farmacia y Bioquímica, Departamento de Fisicomatemática, Universidad de Buenos Aires, Argentina.
Instituto de Química y Fisicoquímica Biológica (IQUIFIB), Facultad de Farmacia y Bioquímica, CONICET, Universidad de Buenos Aires, Argentina.

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