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Co-axial association of recombinant eye lens aquaporin-0 observed in loosely packed 3D crystals.

Palanivelu DV, Kozono DE, Engel A, Suda K, Lustig A, Agre P, Schirmer T
J Mol Biol 355 605-11 (2006)
Cited: 21 times
EuropePMC logo PMID: 16309700

Abstract

Aquaporin-0 (AQP0) is the major membrane protein in vertebrate eye lenses. It has been proposed that AQP0 tetramers mediate contact between membranes of adjacent lens fiber cells, which would be consistent with the extraordinarily narrow inter-cellular spacing. We have obtained 3D crystals of recombinant bovine AQP0 that diffract to 7.0 A resolution. The crystal packing was determined by molecular replacement and shows that, within the cubic lattice, AQP0 tetramers are associated head-to-head along their 4-fold axes. Oligomeric states larger than the tetramer were also observed in solution by native gel electrophoresis and analytical ultracentrifugation methods. In the crystals, there are no direct contacts between octamers, and it can thus be inferred that crystalline order is mediated solely by the detergent belts surrounding the membrane protein. Across the tetramer-tetramer interface, extracellular loops A and C interdigitate at the center and the perimeter of the octamer, respectively. The octamer structure is compared with that of the recently determined structure of truncated ovine AQP0 derived from electron diffraction of 2D crystals. Intriguingly, also in these crystals, octamers are observed, but with significantly different relative tetramer-tetramer orientations. The interactions observed in the loosely packed 3D crystals reported here may in fact represent an in vivo association mode between AQP0 tetramers from juxtaposed membranes in the eye lens.

Reviews - 2c32 mentioned but not cited (4)

  1. Protein crystallography for non-crystallographers, or how to get the best (but not more) from published macromolecular structures. Wlodawer A, Minor W, Dauter Z, Jaskolski M. FEBS J 275 1-21 (2008)
  2. Junction-forming aquaporins. Engel A, Fujiyoshi Y, Gonen T, Walz T. Curr Opin Struct Biol 18 229-235 (2008)
  3. Revival of electron crystallography. Hite RK, Raunser S, Walz T. Curr Opin Struct Biol 17 389-395 (2007)
  4. Aquaporin Gating: A New Twist to Unravel Permeation through Water Channels. Ozu M, Alvear-Arias JJ, Fernandez M, Caviglia A, Peña-Pichicoi A, Carrillo C, Carmona E, Otero-Gonzalez A, Garate JA, Amodeo G, Gonzalez C. Int J Mol Sci 23 12317 (2022)

Articles - 2c32 mentioned but not cited (1)

  1. Functional Annotation Analytics of Rhodopseudomonas palustris Genomes. Simmons SS, Isokpehi RD, Brown SD, McAllister DL, Hall CC, McDuffy WM, Medley TL, Udensi UK, Rajnarayanan RV, Ayensu WK, Cohly HH. Bioinform Biol Insights 5 115-129 (2011)


Reviews citing this publication (5)

  1. Aquaporin gating. Hedfalk K, Törnroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P, Neutze R. Curr Opin Struct Biol 16 447-456 (2006)
  2. Breaking the bottleneck: eukaryotic membrane protein expression for high-resolution structural studies. Midgett CR, Madden DR. J Struct Biol 160 265-274 (2007)
  3. Plant and Mammal Aquaporins: Same but Different. Laloux T, Junqueira B, Maistriaux LC, Ahmed J, Jurkiewicz A, Chaumont F. Int J Mol Sci 19 E521 (2018)
  4. Genetic variation in human aquaporins and effects on phenotypes of water homeostasis. Sorani MD, Manley GT, Giacomini KM. Hum Mutat 29 1108-1117 (2008)
  5. Aquaporins and Ion Channels as Dual Targets in the Design of Novel Glioblastoma Therapeutics to Limit Invasiveness. Varricchio A, Yool AJ. Cancers (Basel) 15 849 (2023)

Articles citing this publication (11)

  1. Intact AQP0 performs cell-to-cell adhesion. Kumari SS, Varadaraj K. Biochem Biophys Res Commun 390 1034-1039 (2009)
  2. Dynamic control of slow water transport by aquaporin 0: implications for hydration and junction stability in the eye lens. Jensen MØ, Dror RO, Xu H, Borhani DW, Arkin IT, Eastwood MP, Shaw DE. Proc Natl Acad Sci U S A 105 14430-14435 (2008)
  3. Membrane stiffness is modified by integral membrane proteins. Fowler PW, Hélie J, Duncan A, Chavent M, Koldsø H, Sansom MS. Soft Matter 12 7792-7803 (2016)
  4. Differentiation-dependent modification and subcellular distribution of aquaporin-0 suggests multiple functional roles in the rat lens. Grey AC, Li L, Jacobs MD, Schey KL, Donaldson PJ. Differentiation 77 70-83 (2009)
  5. Verification and spatial localization of aquaporin-5 in the ocular lens. Grey AC, Walker KL, Petrova RS, Han J, Wilmarth PA, David LL, Donaldson PJ, Schey KL. Exp Eye Res 108 94-102 (2013)
  6. Unique and analogous functions of aquaporin 0 for fiber cell architecture and ocular lens transparency. Kumari SS, Eswaramoorthy S, Mathias RT, Varadaraj K. Biochim Biophys Acta 1812 1089-1097 (2011)
  7. Spatial distributions of AQP5 and AQP0 in embryonic and postnatal mouse lens development. Petrova RS, Schey KL, Donaldson PJ, Grey AC. Exp Eye Res 132 124-135 (2015)
  8. Eph-ephrin Signaling Affects Eye Lens Fiber Cell Intracellular Voltage and Membrane Conductance. Cheng C, Gao J, Sun X, Mathias RT. Front Physiol 12 772276 (2021)
  9. Cryo-electron microscopic and X-ray crystallographic analysis of the light-driven proton pump proteorhodopsin reveals a pentameric assembly. Hirschi S, Kalbermatter D, Ucurum Z, Fotiadis D. J Struct Biol X 4 100024 (2020)
  10. Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development. Chauvigné F, Fjelldal PG, Cerdà J, Finn RN. PLoS One 11 e0154592 (2016)
  11. The effects of a protein osmolyte on the stability of the integral membrane protein glycerol facilitator. Baturin S, Galka JJ, Piyadasa H, Gajjeraman S, O'Neil JD. Biochem Cell Biol 92 564-575 (2014)


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