Two distinct aquaporin 0s required for development and transparency of the zebrafish lens

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 12, 2010, Pages 6582-6592

  Froger, Alexandrine ^a   Clemens, Daniel ^a   Kalman, Katalin ^a   Németh Cahalan, Karin L ^a   Schilling, Thomas F ^b   Hall, James E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; AQUAPORIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; AQP0A GENE; AQP0B GENE; ARTICLE; CATARACTOGENESIS; CELL ASSAY; CONTROLLED STUDY; EYE DEVELOPMENT; GENE; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SILENCING; GENETIC VARIABILITY; IN SITU HYBRIDIZATION; LENS; LENS DEVELOPMENT; MICROINJECTION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; WESTERN BLOTTING; ZEBRA FISH;

ANIMALS; AQUAPORINS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LENS, CRYSTALLINE; OOCYTES; PERMEABILITY; WATER; XENOPUS LAEVIS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 79956037684     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-5626     Document Type: Article

References (81)

1. Resnikoff S, Pascolini D, Etya'ale D, et al. Global data on visual impairment in the year 2002. Bull World Health Organ. 2004;82: 844-851.
2. Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW. Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci U S A. 1993;90:11663-11667.
3. Broekhuyse RM, Kuhlmann ED, Winkens HJ. Lens membranes, VII: MIP is an immunologically specific component of lens fiber membranes and is identical with 26K band protein. Exp Eye Res. 1979;29:303-313.
4. McAvoy JW, Chamberlain CG, de Iongh RU, Hales AM, Lovicu FJ. Lens development. Eye. 1999;13(pt 3b):425-437.
5. Sue Menko A. Lens epithelial cell differentiation. Exp Eye Res. 2002;75:485-490.
6. Gorin MB, Yancey SB, Cline J, Revel JP, Horwitz J. The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell. 1984;39:49-59.
7. Huebert RC, Splinter PL, Garcia F, Marinelli RA, LaRusso NF. Expression and localization of aquaporin water channels in rat hepatocytes: evidence for a role in canalicular bile secretion. J Biol Chem. 2002;277:22710-22717.
8. Hermo L, Krzeczunowicz D, Ruz R. Cell specificity of aquaporins 0, 3, and 10 expressed in the testis, efferent ducts, and epididymis of adult rats. J Androl. 2004;25:494-505.
9. Preston GM, Carroll TP, Guggino WB, Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 1992;256:385-387.
10. Froger A, Tallur B, Thomas D, Delamarche C. Prediction of functional residues in water channels and related proteins. Protein Sci. 1998;7:1458-1468.
11. King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol. 2004;5:687-698.
12. Francis P, Chung JJ, Yasui M, et al. Functional impairment of lens aquaporin in two families with dominantly inherited cataracts. Hum Mol Genet. 2000;9:2329-2334.
13. Berry V, Francis P, Kaushal S, Moore A, Bhattacharya S. Missense mutations in MIP underlie autosomal dominant 'polymorphic' and lamellar cataracts linked to 12q. Nat Genet. 2000;25:15-17.
14. Gu F, Zhai H, Li D, et al. A novel mutation in major intrinsic protein of the lens gene (MIP) underlies autosomal dominant cataract in a Chinese family. Mol Vis. 2007;13:1651-1656.
15. Lin H, Hejtmancik JF, Qi Y. A substitution of arginine to lysine at the COOH-terminus of MIP caused a different binocular phenotype in a congenital cataract family. Mol Vis. 2007;13:1822-1827.
16. Shiels A, Bassnett S, Varadaraj K, et al. Optical dysfunction of the crystalline lens in aquaporin-0-deficient mice. Physiol Genomics.2001;7:179-186.
17. Shiels A, Mackay D, Bassnett S, Al-Ghoul K, Kuszak J. Disruption of lens fiber cell architecture in mice expressing a chimeric AQP0- LTR protein. FASEB J. 2000;14:2207-2212.
18. Kalman K, Nemeth-Cahalan KL, Froger A, Hall JE. AQP0-LTR of the cat Fr mouse alters water permeability and calcium regulation of wild type AQP0. Biochim Biophys Acta. 2006;1758:1094-1099.
19. Zampighi GA, Hall JE, Ehring GR, Simon SA. The structural organization and protein composition of lens fiber junctions. J Cell Biol. 1989;108:2255-2275.
20. Gonen T, Cheng Y, Kistler J, Walz T. Aquaporin-0 membrane junctions form upon proteolytic cleavage. J Mol Biol. 2004;342:1337-1345.
21. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature. 2004;429:193-197.
22. Chandy G, Zampighi GA, Kreman M, Hall JE. Comparison of the water transporting properties of MIP and AQP1. J Membr Biol. 1997;159:29-39.
23. Yang B, Verkman AS. Water and glycerol permeabilities of aquaporins 1-5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes. J Biol Chem. 1997;272:16140-16146.
24. Mulders SM, Van der Kemp AJ, Terlouw SA, Van Boxtel HA, Van Os CH, Deen PM. The exchange of functional domains among aquaporins with different transport characteristics. Pflugers Archiv Eur J Physiol. 1998;436:599-607.
25. Ne ́meth-Cahalan K, Kalman K, Hall JE. Molecular basis of pH and Ca2_ regulation of aquaporin water permeability. J Gen Physiol. 2004;123:573-580.
26. Németh-Cahalan KL, Hall JE. pH and calcium regulate the water permeability of aquaporin. J Biol Chem. 2000;275:6777-6782.
27. Varadaraj K, Kumari S, Shiels A, Mathias RT. Regulation of aquaporin water permeability in the lens. Invest Ophthalmol Vis Sci. 2005;46:1393-1402.
28. Rose KM, Wang Z, Magrath GN, Hazard ES, Hildebrandt JD, Schey KL. Aquaporin 0-calmodulin interaction and the effect of aquaporin phosphorylation. Biochemistry. 2008;47:339-347.
29. Kalman K, Nemeth-Cahalan KL, Froger A, Hall JE. Phosphorylation determines the calmodulin-mediated Ca2_ response and water permeability of AQP0. J Biol Chem. 2008;283:21278-21283.
30. Lindsey Rose KM, Gourdie RG, Prescott AR, Quinlan RA, Crouch RK, Schey KL. The C terminus of lens aquaporin 0 interacts with the cytoskeletal proteins filensin and CP49. Invest Ophthalmol Vis Sci. 2006;47:1562-1570.
31. Yu XS, Jiang JX. Interaction of major intrinsic protein (aquaporin- 0) with fiber connexins in lens development. J Cell Sci. 2004;117:871-880.
32. Yu XS, Yin X, Lafer EM, Jiang JX. Developmental regulation of the direct interaction between the intracellular loop of connexin 45.6 and the C terminus of major intrinsic protein (aquaporin-0). J Biol Chem. 2005;280:22081-22090.
33. Glass AS, Dahm R. The zebrafish as a model organism for eye development. Ophthalmic Res. 2004;36:4-24.
34. Easter SS Jr, Nicola GN. The development of vision in the zebrafish (Danio rerio). Dev Biol. 1996;180:646-663.
35. Easter SS Jr, Nicola GN. The development of eye movements in the zebrafish (Danio rerio). Dev Psychobiol. 1997;31:267-276.
36. Dahm R, Schonthaler HB, Soehn AS, van Marle J, Vrensen GF. Development and adult morphology of the eye lens in the zebrafish. Exp Eye Res. 2007;85:74-89.
37. Soules KA, Link BA. Morphogenesis of the anterior segment in the zebrafish eye. BMC Dev Biol. 2005;5:12.
38. Greiling TM, Clark JI. Early lens development in the zebrafish: a three-dimensional time-lapse analysis. Dev Dyn. 2009;238:2254-2265.
39. Postlethwait J, Amores A, Cresko W, Singer A, Yan YL. Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet. 2004;20:481-490.
40. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press; 2000.
41. Thisse C, Thisse B, Schilling TF, Postlethwait JH. Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development. 1993;119:1203-1215.
42. Thisse C, Thisse B. High-resolution in situ hybridization to whole mount zebrafish embryos. Nat Protoc. 2008;3:59-69.
43. Preston GM, Jung JS, Guggino WB, Agre P. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem. 1993;268:17-20.
44. Virkki LV, Cooper GJ, Boron WF. Cloning and functional expression of an MIP (AQP0) homolog from killifish (Fundulus heteroclitus) lens. Am J Physiol Regul Integr Comp Physiol. 2001;281: R1994-R2003.
45. Daniels MJ, Wood MR, Yeager M. In vivo functional assay of a recombinant aquaporin in Pichia pastoris. Appl Environ Microbiol. 2006;72:1507-1514.
46. Schiestl RH, Gietz RD. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989;16:339-346.
47. Sherman F. Getting started with yeast. Methods Enzymol. 2002; 350:3-41.
48. Amores A, Force A, Yan YL, et al. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998;282:1711-1714.
49. Postlethwait JH, Yan YL, Gates MA, et al. Vertebrate genome evolution and the zebrafish gene map. Nat Genet. 1998;18:345-349.
50. Postlethwait JH. The zebrafish genome: a review and msx gene case study. Genome Dyn. 2006;2:183-197.
51. Gates MA, Kim L, Egan ES, et al. A genetic linkage map for zebrafish: comparative analysis and localization of genes and expressed sequences. Genome Res. 1999;9:334-347.
52. Vihtelic TS, Fadool JM, Gao J, Thornton KA, Hyde DR, Wistow G. Expressed sequence tag analysis of zebrafish eye tissues for NEIBank. Mol Vis. 2005;11:1083-1100.
53. Gonnet GH, Cohen MA, Benner SA. Exhaustive matching of the\ entire protein sequence database. Science. 1992;256:1443-1445.
54. Harries WE, Akhavan D, Miercke LJ, Khademi S, Stroud RM. The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci U S A. 2004;101:14045-14050.
55. Ball LE, Garland DL, Crouch RK, Schey KL. Post-translational modifications of aquaporin 0 (AQP0) in the normal human lens: spatial and temporal occurrence. Biochemistry. 2004;43:9856-9865.
56. Knauf PA, Proverbio F, Hoffman JF. Chemical characterization and pronase susceptibility of the Na:K pump-associated phosphoprotein of human red blood cells. J Gen Physiol. 1974;63:305-323.
57. Methfessel C, Witzemann V, Takahashi T, Mishina M, Numa S, Sakmann B. Patch clamp measurements on Xenopus laevis oocytes: currents through endogenous channels and implanted acetylcholine receptor and sodium channels. Pflugers Arch. 1986; 407:577-588.
58. Laize V, Tacnet F, Ripoche P, Hohmann S. Polymorphism of Saccharomyces cerevisiae aquaporins. Yeast. 2000;16:897-903.
59. Lagree V, Froger A, Deschamps S, et al. Oligomerization state of water channels and glycerol facilitators. Involvement of loop E. J Biol Chem. 1998;273:33949-33953.
60. Latimer P. Light scattering vs. microscopy for measuring average cell size and shape. Biophys J. 1979;27:117-126.
61. Zhou L, Chen T, Church RL. Temporal expression of three mouse lens fiber cell membrane protein genes during early development. Mol Vis. 2002;8:143-148.
62. Tingaud-Sequeira A, Calusinska M, Finn RN, Chauvigne F, Lozano J, Cerda J. The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evol Biol. 10:38.
63. Al Ghoul KJ, Kirk T, Kuszak AJ, Zoltoski RK, Shiels A, Kuszak JR. Lens structure in MIP-deficient mice. Anat Rec. 2003;273A:714-730.
64. Zampighi GA, Eskandari S, Hall JE, Zampighi L, Kreman M. Microdomains of AQP0 in lens equatorial fibers. Exp Eye Res. 2002;75: 505-519.
65. Buzhynskyy N, Girmens JF, Faigle W, Scheuring S. Human cataract lens membrane at subnanometer resolution. J Mol Biol. 2007;374:162-169.
66. Zampighi G, Simon SA, Robertson JD, McIntosh TJ, Costello MJ. On the structural organization of isolated bovine lens fiber junctions. J Cell Biol. 1982;93:175-189.
67. Zampighi GA, Simon SA, Hall JE. The specialized junctions of the lens. Int Rev Cytol. 1992;136:185-225.
68. Michea LF, de la Fuente M, Lagos N. Lens major intrinsic protein (MIP) promotes adhesion when reconstituted into large unilamellar liposomes. Biochemistry. 1994;33:7663-7669.
69. Michea LF, Andrinolo D, Ceppi H, Lagos N. Biochemical evidence for adhesion-promoting role of major intrinsic protein isolated from both normal and cataractous human lenses. Exp Eye Res. 1995;61:293-301.
70. Gonen T, Cheng Y, Sliz P, et al. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature. 2005;438: 633-638.
71. Jensen MO, Dror RO, Xu H, et al. Dynamic control of slow water transport by aquaporin 0: implications for hydration and junction stability in the eye lens. Proc Natl Acad Sci U S A. 2008;105: 14430-14435.
72. Gong X, Cheng C, Xia CH. Connexins in lens development and cataractogenesis. J Membr Biol. 2007;218:9-12.
73. Tanaka M, Russell P, Smith S, Uga S, Kuwabara T, Kinoshita JH. Membrane alterations during cataract development in the Nakano mouse lens. Invest Ophthalmol Vis Sci. 1980;19:619-629.
74. Eastman SD, Chen TH, Falk MM, Mendelson TC, Iovine MK. Phylogenetic analysis of three complete gap junction gene families reveals lineage-specific duplications and highly supported gene classes. Genomics. 2006;87:265-274.
75. Cheng S, Shakespeare T, Mui R, White TW, Valdimarsson G. Connexin 48.5 is required for normal cardiovascular function and lens development in zebrafish embryos. J Biol Chem. 2004;279: 36993-37003.
76. Mulders JW, Stokkermans J, Leunissen JA, Benedetti EL, Bloemendal H, de Jong WW. Interaction of alpha-crystallin with lens plasma membranes: affinity for MP26. Eur J Biochem. 1985;152:721-728.
77. Liang JJ, Li XY. Spectroscopic studies on the interaction of calf lens membranes with crystallins. Exp Eye Res. 1992;54:719-724.
78. Fan J, Fariss RN, Purkiss AG, et al. Specific interaction between lens MIP/Aquaporin-0 and two members of the gamma-crystallin family. Mol Vis. 2005;11:76-87.
79. Liu BF, Liang JJ. Confocal fluorescence microscopy study of interaction between lens MIP26/AQP0 and crystallins in living cells. J Cell Biochem. 2008;104:51-58.
80. Posner M, Hawke M, Lacava C, Prince CJ, Bellanco NR, Corbin RW. A proteome map of the zebrafish (Danio rerio) lens reveals similarities between zebrafish and mammalian crystallin expression. Mol Vis. 2008;14:806-814.
81. Harding RL, Howley S, Baker LJ, et al. Lengsin expression and function during zebrafish lens formation. Exp Eye Res. 2008;86: 807-818.