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Allosteric mechanism of water-channel gating by Ca2+-calmodulin.

Reichow SL, Clemens DM, Freites JA, Németh-Cahalan KL, Heyden M, Tobias DJ, Hall JE, Gonen T
Nat Struct Mol Biol 20 1085-92 (2013)
Cited: 62 times
EuropePMC logo PMID: 23893133

Abstract

Calmodulin (CaM) is a universal regulatory protein that communicates the presence of calcium to its molecular targets and correspondingly modulates their function. This key signaling protein is important for controlling the activity of hundreds of membrane channels and transporters. However, understanding of the structural mechanisms driving CaM regulation of full-length membrane proteins has remained elusive. In this study, we determined the pseudoatomic structure of full-length mammalian aquaporin-0 (AQP0, Bos taurus) in complex with CaM, using EM to elucidate how this signaling protein modulates water-channel function. Molecular dynamics and functional mutation studies reveal how CaM binding inhibits AQP0 water permeability by allosterically closing the cytoplasmic gate of AQP0. Our mechanistic model provides new insight, only possible in the context of the fully assembled channel, into how CaM regulates multimeric channels by facilitating cooperativity between adjacent subunits.

Reviews - 3j41 mentioned but not cited (4)

  1. Aquaporin Protein-Protein Interactions. Roche JV, Törnroth-Horsefield S. Int J Mol Sci 18 (2017)
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Articles - 3j41 mentioned but not cited (6)

  1. Allosteric mechanism of water-channel gating by Ca2+-calmodulin. Reichow SL, Clemens DM, Freites JA, Németh-Cahalan KL, Heyden M, Tobias DJ, Hall JE, Gonen T. Nat. Struct. Mol. Biol. 20 1085-1092 (2013)
  2. Calmodulin Gates Aquaporin 0 Permeability through a Positively Charged Cytoplasmic Loop. Fields JB, Németh-Cahalan KL, Freites JA, Vorontsova I, Hall JE, Tobias DJ. J. Biol. Chem. 292 185-195 (2017)
  3. Cooperativity and allostery in aquaporin 0 regulation by Ca2. Freites JA, Németh-Cahalan KL, Hall JE, Tobias DJ. Biochim Biophys Acta Biomembr 1861 988-996 (2019)
  4. Variability of Protein Structure Models from Electron Microscopy. Monroe L, Terashi G, Kihara D. Structure 25 592-602.e2 (2017)
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  6. Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development. Chauvigné F, Fjelldal PG, Cerdà J, Finn RN. PLoS ONE 11 e0154592 (2016)


Reviews citing this publication (19)

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Articles citing this publication (33)

  1. X-ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking. Frick A, Eriksson UK, de Mattia F, Oberg F, Hedfalk K, Neutze R, de Grip WJ, Deen PM, Törnroth-Horsefield S. Proc. Natl. Acad. Sci. U.S.A. 111 6305-6310 (2014)
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  12. Native Mass Spectrometry and Surface Induced Dissociation Provide Insight into the Post-Translational Modifications of Tetrameric AQP0 Isolated from Bovine Eye Lens. Harvey SR, O'Neale C, Schey KL, Wysocki VH. Anal Chem 94 1515-1519 (2022)
  13. Applying bimolecular fluorescence complementation to screen and purify aquaporin protein:protein complexes. Sjöhamn J, Båth P, Neutze R, Hedfalk K. Protein Sci. 25 2196-2208 (2016)
  14. Single-file transport of water through membrane channels. Horner A, Pohl P. Faraday Discuss. 209 9-33 (2018)
  15. BFSP1 C-terminal domains released by post-translational processing events can alter significantly the calcium regulation of AQP0 water permeability. Tapodi A, Clemens DM, Uwineza A, Jarrin M, Goldberg MW, Thinon E, Heal WP, Tate EW, Nemeth-Cahalan K, Vorontsova I, Hall JE, Quinlan RA. Exp Eye Res 185 107585 (2019)
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  17. Role of Pore-Lining Residues in Defining the Rate of Water Conduction by Aquaporin-0. Saboe PO, Rapisarda C, Kaptan S, Hsiao YS, Summers SR, De Zorzi R, Dukovski D, Yu J, de Groot BL, Kumar M, Walz T. Biophys. J. 112 953-965 (2017)
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  20. Unraveling Human AQP5-PIP Molecular Interaction and Effect on AQP5 Salivary Glands Localization in SS Patients. Chivasso C, Nesverova V, Järvå M, Blanchard A, Rose KL, Öberg FK, Wang Z, Martin M, Lhotellerie F, Zindy E, Junqueira B, Leroy K, Vanhollebeke B, Delforge V, Bolaky N, Perret J, Soyfoo MS, Moscato S, Baldini C, Chaumont F, Mattii L, Schey KL, Myal Y, Törnroth-Horsefield S, Delporte C. Cells 10 2108 (2021)
  21. Aqp0a Regulates Suture Stability in the Zebrafish Lens. Vorontsova I, Gehring I, Hall JE, Schilling TF. Invest. Ophthalmol. Vis. Sci. 59 2869-2879 (2018)
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  25. Cloning and Stress-Induced Expression Analysis of Calmodulin in the Antarctic Alga Chlamydomonas sp. ICE-L. He YY, Wang YB, Zheng Z, Liu FM, An ML, He XD, Qu CF, Li LL, Miao JL. Curr. Microbiol. 74 921-929 (2017)
  26. Cortisol Interaction with Aquaporin-2 Modulates Its Water Permeability: Perspectives for Non-Genomic Effects of Corticosteroids. Mom R, Réty S, Auguin D. Int J Mol Sci 24 1499 (2023)
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  30. Proteomic analysis showing the signaling pathways involved in the rhizome enlargement process in Nelumbo nucifera. Cao D, Damaris RN, Zhang Y, Liu M, Li M, Yang P. BMC Genomics 20 766 (2019)
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  32. TMT-based quantitative proteomic analysis unveils uterine fluid difference in hens producing normal and pimpled eggs. Song L, Weng K, Bao Q, Wu J, Zhang Y, Xu Q, Zhang Y. Poult Sci 102 103081 (2023)
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