Literature DB >> 23800763

In vivo analysis of aquaporin 0 function in zebrafish: permeability regulation is required for lens transparency.

Daniel M Clemens1, Karin L Németh-Cahalan, Lien Trinh, Tailin Zhang, Thomas F Schilling, James E Hall.   

Abstract

PURPOSE: The zebrafish lens is well suited for studies of physiology and development due to its rapid formation in the embryo and genetic accessibility. Aquaporin 0 (AQP0), a lens-specific membrane protein, is required for lens clarity. Zebrafish have two copies of AQP0 (Aqp0a and b), whereas mammals have a single, multifunctional protein. Here we demonstrate a reliable knockdown/rescue system in zebrafish and use it to provide evidence for subfunctionalization of Aqp0a and b, as well as to show that calcium-mediated regulation of Aqp0a in zebrafish lenses is necessary for transparency.
METHODS: Coinjection of antisense oligonucleotides and DNA rescue constructs into zebrafish embryos, followed by evaluation of the developing fish for cataracts, was used to analyze the functions of Aqp0a and b. The water permeability and regulation characteristics of each rescue protein were tested in a Xenopus oocyte swelling assay.
RESULTS: Both copies of AQP0 are necessary for lens clarity in the zebrafish, and neither is sufficient. Water permeability is necessary but also insufficient. Phosphorylation and regulation of Aqp0a are required for its function.
CONCLUSIONS: In the zebrafish lens, the two closely related AQP0s have acquired distinct functions that are both necessary for lens development and clarity. Regulation of AQP0 water permeability, a well-studied phenomenon in vitro, may be physiologically relevant in the living lens.

Entities:  

Keywords:  AQP0; cataract; subfunctionalization; zebrafish

Mesh:

Substances:

Year:  2013        PMID: 23800763      PMCID: PMC3729242          DOI: 10.1167/iovs.13-12337

Source DB:  PubMed          Journal:  Invest Ophthalmol Vis Sci        ISSN: 0146-0404            Impact factor:   4.799


  37 in total

1.  Regional distribution of the Na(+) and K(+) currents around the crystalline lens of rabbit.

Authors:  Oscar A Candia; Aldo C Zamudio
Journal:  Am J Physiol Cell Physiol       Date:  2002-02       Impact factor: 4.249

2.  pH and calcium regulate the water permeability of aquaporin 0.

Authors:  K L Németh-Cahalan; J E Hall
Journal:  J Biol Chem       Date:  2000-03-10       Impact factor: 5.157

3.  Water and ion permeation of aquaporin-1 in planar lipid bilayers. Major differences in structural determinants and stoichiometry.

Authors:  S M Saparov; D Kozono; U Rothe; P Agre; P Pohl
Journal:  J Biol Chem       Date:  2001-06-15       Impact factor: 5.157

4.  Cloning and functional expression of an MIP (AQP0) homolog from killifish (Fundulus heteroclitus) lens.

Authors:  L V Virkki; G J Cooper; W F Boron
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2001-12       Impact factor: 3.619

5.  Molecular basis of pH and Ca2+ regulation of aquaporin water permeability.

Authors:  Karin L Németh-Cahalan; Katalin Kalman; James E Hall
Journal:  J Gen Physiol       Date:  2004-04-12       Impact factor: 4.086

6.  Aquaporin-0 membrane junctions form upon proteolytic cleavage.

Authors:  Tamir Gonen; Yifan Cheng; Joerg Kistler; Thomas Walz
Journal:  J Mol Biol       Date:  2004-09-24       Impact factor: 5.469

Review 7.  Subfunction partitioning, the teleost radiation and the annotation of the human genome.

Authors:  John Postlethwait; Angel Amores; William Cresko; Amy Singer; Yi-Lin Yan
Journal:  Trends Genet       Date:  2004-10       Impact factor: 11.639

8.  AKAP2 anchors PKA with aquaporin-0 to support ocular lens transparency.

Authors:  Matthew G Gold; Steve L Reichow; Susan E O'Neill; Chad R Weisbrod; Lorene K Langeberg; James E Bruce; Tamir Gonen; John D Scott
Journal:  EMBO Mol Med       Date:  2011-11-16       Impact factor: 12.137

9.  Through a glass darkly.

Authors:  James E Hall
Journal:  EMBO Mol Med       Date:  2011-12-19       Impact factor: 12.137

10.  The structural organization and protein composition of lens fiber junctions.

Authors:  G A Zampighi; J E Hall; G R Ehring; S A Simon
Journal:  J Cell Biol       Date:  1989-06       Impact factor: 10.539

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  15 in total

1.  Functional characterization of an AQP0 missense mutation, R33C, that causes dominant congenital lens cataract, reveals impaired cell-to-cell adhesion.

Authors:  Sindhu S Kumari; Jason Gandhi; Mohammed H Mustehsan; Semih Eren; Kulandaiappan Varadaraj
Journal:  Exp Eye Res       Date:  2013-10-09       Impact factor: 3.467

2.  Aquaporin-0 targets interlocking domains to control the integrity and transparency of the eye lens.

Authors:  Woo-Kuen Lo; Sondip K Biswas; Lawrence Brako; Alan Shiels; Sumin Gu; Jean X Jiang
Journal:  Invest Ophthalmol Vis Sci       Date:  2014-03-03       Impact factor: 4.799

Review 3.  The aquaporin zero puzzle.

Authors:  James E Hall; Richard T Mathias
Journal:  Biophys J       Date:  2014-07-01       Impact factor: 4.033

4.  Single cell transcriptomics of the developing zebrafish lens and identification of putative controllers of lens development.

Authors:  Dylan R Farnsworth; Mason Posner; Adam C Miller
Journal:  Exp Eye Res       Date:  2021-03-09       Impact factor: 3.467

5.  The pH sensitivity of Aqp0 channels in tetraploid and diploid teleosts.

Authors:  François Chauvigné; Cinta Zapater; Jon Anders Stavang; Geir Lasse Taranger; Joan Cerdà; Roderick Nigel Finn
Journal:  FASEB J       Date:  2015-02-09       Impact factor: 5.191

6.  The zebrafish as a model system for analyzing mammalian and native α-crystallin promoter function.

Authors:  Mason Posner; Kelly L Murray; Matthew S McDonald; Hayden Eighinger; Brandon Andrew; Amy Drossman; Zachary Haley; Justin Nussbaum; Larry L David; Kirsten J Lampi
Journal:  PeerJ       Date:  2017-11-27       Impact factor: 2.984

7.  Aqp0a Regulates Suture Stability in the Zebrafish Lens.

Authors:  Irene Vorontsova; Ines Gehring; James E Hall; Thomas F Schilling
Journal:  Invest Ophthalmol Vis Sci       Date:  2018-06-01       Impact factor: 4.799

8.  Zebrafish Models of Human Disease: Gaining Insight into Human Disease at ZFIN.

Authors:  Yvonne M Bradford; Sabrina Toro; Sridhar Ramachandran; Leyla Ruzicka; Douglas G Howe; Anne Eagle; Patrick Kalita; Ryan Martin; Sierra A Taylor Moxon; Kevin Schaper; Monte Westerfield
Journal:  ILAR J       Date:  2017-07-01

9.  Why does the zebrafish cloche mutant develop lens cataract?

Authors:  Mason Posner; Matthew S McDonald; Kelly L Murray; Andor J Kiss
Journal:  PLoS One       Date:  2019-03-12       Impact factor: 3.240

10.  Lens extrusion from Laminin alpha 1 mutant zebrafish.

Authors:  Mallika Pathania; Elena V Semina; Melinda K Duncan
Journal:  ScientificWorldJournal       Date:  2014-01-15
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