PALS1 is essential for retinal pigment epithelium structure and neural retina stratification

Journal of Neuroscience

Volumn 31, Issue 47, 2011, Pages 17230-17241

  Park, Bokyung ^a   Alves, Celso Henrique ^a   Lundvig, Ditte M ^a   Tanimoto, Naoyuki ^b   Beck, Susanne C ^b   Huber, Gesine ^b   Richard, Fabrice ^c   Klooster, Jan ^a   Andlauer, Till F M ^a   Swindell, Eric C ^d   Jamrich, Milan ^e   le Bivic, André ^c   Seeliger, Mathias W ^b   Wijnholds, Jan ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; PROTEIN ASSOCIATED WITH LIN7; UNCLASSIFIED DRUG;

ALPHA RHYTHM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BETA RHYTHM; CELL JUNCTION; CELL NUCLEUS; CONTROLLED STUDY; DISEASE COURSE; ELECTRORETINOGRAPHY; GLIOSIS; HISTOPATHOLOGY; MOUSE; MUTANT; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; OUTER PLEXIFORM LAYER; PHOTORECEPTOR CELL; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEPLETION; RETINA; RETINA DEGENERATION; RETINA DEVELOPMENT; RETINA DISEASE; ROSETTE FORMATION; SCANNING LASER OPHTHALMOSCOPY; SYNAPSE; TISSUE STRUCTURE; UPREGULATION; VISUAL NERVOUS SYSTEM;

ANIMALS; FEMALE; MALE; MARMOTA; MEMBRANE PROTEINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; NUCLEOSIDE-PHOSPHATE KINASE; OPHTHALMOSCOPY; RETINA; RETINAL PIGMENT EPITHELIUM; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 81855184636     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4430-11.2011     Document Type: Article

References (46)

1. Ashburn FS Jr, Pilkerton AR, Rao NA, Marak GE (1980) The effects of iodate and iodoacetate on the retinal adhesion. Invest Ophthalmol Vis Sci 19:1427-1432.
2. Berger S, Bulgakova NA, Grawe F, Johnson K, Knust E (2007) Unraveling the genetic complexity of Drosophila stardust during photoreceptor morphogenesis and prevention of light-induced degeneration. Genetics 176:2189-2200.
3. Bok D (1993) The retinal pigment epithelium: a versatile partner in vision. J Cell Sci Suppl 17:189-195.
4. Bonilha VL, Bhattacharya SK, West KA, Crabb JS, Sun J, Rayborn ME, Nawrot M, Saari JC, Crabb JW (2004) Support for a proposed retinoidprocessing protein complex in apical retinal pigment epithelium. Exp Eye Res 79:419-422.
5. Bulgakova NA, Kempkens O, Knust E (2008) Multiple domains of Stardust differentially mediate localisation of the Crumbs-Stardust complex during photoreceptor development in Drosophila. J Cell Sci 121:2018-2026.
6. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D (1996) Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A 93:589-595.
7. Delmas V, Martinozzi S, Bourgeois Y, Holzenberger M, Larue L (2003) Cre-mediated recombination in the skin melanocyte lineage. Genesis 36:73-80.
8. den Hollander AI, ten Brink JB, de Kok YJ, van Soest S, van den Born LI, van Driel MA, van de Pol DJ, Payne AM, Bhattacharya SS, Kellner U, Hoyng CB, Westerveld A, Brunner HG, Bleeker-Wagemakers EM, Deutman AF, Heckenlively JR, Cremers FP, Bergen AA (1999) Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet 23:217-221.
9. den Hollander AI, Davis J, van der Velde-Visser SD, Zonneveld MN, Pierrottet CO, Koenekoop RK, Kellner U, van den Born LI, Heckenlively JR, Hoyng CB, Handford PA, Roepman R, Cremers FP (2004) CRB1 mutation spectrum in inherited retinal dystrophies. Hum Mutat 24:355-369.
10. Fischer MD, Huber G, Beck SC, Tanimoto N, Muehlfriedel R, Fahl E, Grimm C, Wenzel A, Remé CE, van de Pavert SA, Wijnholds J, Pacal M, Bremner R, Seeliger MW (2009) Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography. PLoS One 4:e7507
11. Funke L, Dakoji S, Bredt DS (2005) Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu Rev Biochem 74:219-245.
12. Gosens I, den Hollander AI, Cremers FP, Roepman R (2008) Composition and function of the Crumbs protein complex in the mammalian retina. Exp Eye Res 86:713-726.
13. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788.
14. Hong Y, Ackerman L, Jan LY, Jan YN (2003) Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc Natl Acad Sci U S A 100:12712-12717.
15. Johnson K, Grawe F, Grzeschik N, Knust E (2002) Drosophila crumbs is required to inhibit light-induced photoreceptor degeneration. Curr Biol 12:1675-1680.
16. Kamberov E, Makarova O, Roh M, Liu A, Karnak D, Straight S, Margolis B (2000) Molecular cloning and characterization of Pals, proteins associated with mLin-7. J Biol Chem 275:11425-11431.
17. Kim S, Lehtinen MK, Sessa A, Zappaterra MW, Cho SH, Gonzalez D, Boggan B, Austin CA, Wijnholds J, Gambello MJ, Malicki J, LaMantia AS, Broccoli V, Walsh CA (2010) The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66:69-84.
18. Klooster J, Yazulla S, Kamermans M (2009) Ultrastructural analysis of the glutamatergic system in the outer plexiform layer of zebrafish retina. J Chem Neuroanat 37:254-265.
19. Korte GE, Reppucci V, Henkind P (1984) RPE destruction causes choriocapillary atrophy. Invest Ophthalmol Vis Sci 25:1135-1145.
20. Longbottom R, Fruttiger M, Douglas RH, Martinez-Barbera JP, Greenwood J, Moss SE (2009) Genetic ablation of retinal pigment epithelial cells reveals the adaptive response of the epithelium and impact on photoreceptors. Proc Natl Acad Sci U S A 106:18728-18733.
21. Makarova O, Roh MH, Liu CJ, Laurinec S, Margolis B (2003) Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene 302:21-29.
22. Mehalow AK, Kameya S, Smith RS, Hawes NL, Denegre JM, Young JA, Bechtold L, Haider NB, Tepass U, Heckenlively JR, Chang B, Naggert JK, Nishina PM (2003) CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet 12:2179-2189.
23. Mori M, Metzger D, Garnier JM, Chambon P, Mark M (2002) Site-specific somatic mutagenesis in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 43:1384-1388.
24. Nam SC, Choi KW (2003) Interaction of Par-6 and Crumbs complexes is essential for photoreceptor morphogenesis in Drosophila. Development 130:4363-4372.
25. Omori Y, Malicki J (2006) oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr Biol 16:945-957.
26. Randlett O, Norden C, Harris WA (2011) The vertebrate retina: a model for neuronal polarization in vivo. Dev Neurobiol 71:567-583.
27. Reese BE (2011) Development of the retina and optic pathway. Vision Res 51:613-632.
28. Richard M, Roepman R, Aartsen WM, van Rossum AG, den Hollander AI, Knust E, Wijnholds J, Cremers FP (2006) Towards understanding CRUMBS function in retinal dystrophies. Hum Mol Genet 15 [Spec No 2]:R235-R243.
29. Roh MH, Makarova O, Liu CJ, Shin K, Lee S, Laurinec S, Goyal M, Wiggins R, Margolis B (2002) The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J Cell Biol 157:161-172.
30. Rowan S, Cepko CL (2004) Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev Biol 271:388-402.
31. Seeliger MW, Zrenner E, Apfelstedt-Sylla E, Jaissle GB (2001) Identification of Usher syndrome subtypes byERGimplicit time. Invest Ophthalmol Vis Sci 42:3066-3071.
32. Seeliger MW, Beck SC, Pereyra-Muñoz N, Dangel S, Tsai JY, Luhmann UF, van de Pavert SA, Wijnholds J, Samardzija M, Wenzel A, Zrenner E, Narfström K, Fahl E, Tanimoto N, Acar N, Tonagel F (2005) In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy. Vision Res 45:3512-3519.
33. Swindell EC, Bailey TJ, Loosli F, Liu C, Amaya-Manzanares F, Mahon KA, Wittbrodt J, Jamrich M (2006) Rx-Cre, a tool for inactivation of gene expression in the developing retina. Genesis 44:361-363.
34. Tanimoto N, Muehlfriedel RL, Fischer MD, Fahl E, Humphries P, Biel M, Seeliger MW (2009) Vision tests in the mouse: Functional phenotyping with electroretinography. Front Biosci 14:2730-2737.
35. van de Pavert SA, Kantardzhieva A, Malysheva A, Meuleman J, Versteeg I, Levelt C, Klooster J, Geiger S, Seeliger MW, Rashbass P, Le Bivic A, Wijnholds J (2004) Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci 117:4169-4177.
36. van de Pavert SA, Meuleman J, Malysheva A, Aartsen WM, Versteeg I, Tonagel F, Kamphuis W, McCabe CJ, Seeliger MW, Wijnholds J (2007a) A single amino acid substitution (Cys249Trp) in Crb1 causes retinal degeneration and deregulates expression of pituitary tumor transforming gene Pttg1. J Neurosci 27:564-573.
37. van de Pavert SA, Sanz AS, Aartsen WM, Vos RM, Versteeg I, Beck SC, Klooster J, Seeliger MW, Wijnholds J (2007b) Crb1 is a determinant of retinal apical Muller glia cell features. Glia 55:1486-1497.
38. van Rossum AG, Aartsen WM, Meuleman J, Klooster J, Malysheva A, Versteeg I, Arsanto JP, Le Bivic A, Wijnholds J (2006) Pals1/Mpp5 is re-quired for correct localization of Crb1 at the subapical region in polarized Muller glia cells. Hum Mol Genet 15:2659-2672.
39. Vecino E, Hernández M, García M (2004) Cell death in the developing vertebrate retina. Int J Dev Biol 48:965-974.
40. Ventura A, Meissner A, Dillon CP, McManus M, Sharp PA, Van Parijs L, Jaenisch R, Jacks T (2004) Cre-lox-regulated conditional RNA interference from transgenes. Proc Natl Acad Sci U S A 101:10380-10385.
41. Wei X, Malicki J (2002) nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat Genet 31:150-157.
42. Wei X, Zou J, Takechi M, Kawamura S, Li L (2006) Nok plays an essential role in maintaining the integrity of the outer nuclear layer in the zebrafish retina. Exp Eye Res 83:31-44.
43. Young RW (1984) Cell death during differentiation of the retina in the mouse. J Comp Neurol 229:362-373.
44. Zhao C, Yasumura D, Li X, Matthes M, Lloyd M, Nielsen G, Ahern K, Snyder M, Bok D, Dunaief JL, LaVail MM, Vollrath D (2011) mTOR-mediated dedifferentiation of the retinal pigment epithelium initiates photoreceptor degeneration in mice. J Clin Invest 121:369-383.
45. Zolessi FR, Poggi L, Wilkinson CJ, Chien CB, Harris WA (2006) Polarization and orientation of retinal ganglion cells in vivo. Neural Dev 1:2.
46. Zou J, Lathrop KL, Sun M, Wei X (2008) Intact retinal pigment epithelium maintained by Nok is essential for retinal epithelial polarity and cellular patterning in zebrafish. J Neurosci 28:13684-13695.