Genetic ablation of Pals1 in retinal progenitor cells models the retinal pathology of leber congenital amaurosis

Human Molecular Genetics

Volumn 21, Issue 12, 2012, Pages 2663-2676

  Cho, Seo Hee ^a,d   Kim, Jin Young ^a,d   Simons, David L ^b   Song, Ji Yun ^a,d   Le, Julie H ^a   Swindell, Eric C ^a   Jamrich, Milan ^c   Wu, Samuel M ^b   Kim, Seonhee ^a,d  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b CULLEN EYE INSTITUTE   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CELL POLARITY; CELL SURVIVAL; CONTROLLED STUDY; CRUMBS HOMOLOG 1 GENE; DISEASE MODEL; ELECTRORETINOGRAM; EPITHELIUM CELL; GENE; GENE DELETION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN GENOME; LEBER CONGENITAL AMAUROSIS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSOCIATED WITH LIN SEVEN 1 GENE; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RETINA; RETINA CELL; RETINA DEGENERATION; RETINA NERVE CELL; STEM CELL; VISUAL IMPAIRMENT;

ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; ELECTRORETINOGRAPHY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LEBER CONGENITAL AMAUROSIS; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; NUCLEOSIDE-PHOSPHATE KINASE; RETINA; STEM CELLS; VISUAL ACUITY;

EID: 84861744571     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds091     Document Type: Article

References (65)

1. Westfall, J.E., Hoyt, C., Liu, Q., Hsiao, Y.C., Pierce, E.A., Page-McCaw, P.S. and Ferland, R.J. (2010) Retinal degeneration and failure of photoreceptor outer segment formation in mice with targeted deletion of the Joubert syndrome gene, Ahi1. J. Neurosci., 30, 8759-8768.
2. Furukawa, T., Morrow, E.M., Li, T., Davis, F.C. and Cepko, C.L. (1999) Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat. Genet., 23, 466-470.
3. Omri, S., Omri, B., Savoldelli, M., Jonet, L., Thillaye-Goldenberg, B., Thuret, G., Gain, P., Jeanny, J.C., Crisanti, P. and Behar-Cohen, F. (2010) The outer limiting membrane (OLM) revisited: clinical implications. Clin. Ophthalmol., 4, 183-195.
4. den Hollander, A.I., Roepman, R., Koenekoop, R.K. and Cremers, F.P. (2008) Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog. Retin. Eye Res., 27, 391-419.
5. den Hollander, A.I., ten Brink, J.B., de Kok, Y.J., van Soest, S., van den Born, L.I., van Driel, M.A., van de Pol, D.J., Payne, A.M., Bhattacharya, S.S., Kellner, U. et al. (1999) Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat. Genet., 23, 217-221.
6. Pellikka, M., Tanentzapf, G., Pinto, M., Smith, C., McGlade, C.J., Ready, D.F. and Tepass, U. (2002) Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature, 416, 143-149.
7. Lotery, A.J., Jacobson, S.G., Fishman, G.A., Weleber, R.G., Fulton, A.B., Namperumalsamy, P., Heon, E., Levin, A.V., Grover, S., Rosenow, J.R. et al. (2001) Mutations in the CRB1 gene cause Leber congenital amaurosis. Arch. Ophthalmol., 119, 415-420.
8. Richard, M., Roepman, R., Aartsen, W.M., van Rossum, A.G., den Hollander, A.I., Knust, E., Wijnholds, J. and Cremers, F.P. (2006) Towards understanding CRUMBS function in retinal dystrophies. Hum. Mol. Genet., 15 (Spec no. 2), R235-R243.
9. Kamberov, E., Makarova, O., Roh, M., Liu, A., Karnak, D., Straight, S. and Margolis, B. (2000) Molecular cloning and characterization of Pals, proteins associated with mLin-7. J. Biol. Chem., 275, 11425-11431.
10. Roh, M.H., Makarova, O., Liu, C.J., Shin, K., Lee, S., Laurinec, S., Goyal, M., Wiggins, R. and 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.
11. Michel, D., Arsanto, J.P., Massey-Harroche, D., Beclin, C., Wijnholds, J. and Le Bivic, A. (2005) PATJ connects and stabilizes apical and lateral components of tight junctions in human intestinal cells. J. Cell Sci., 118, 4049-4057.
12. Gosens, I., den Hollander, A.I., Cremers, F.P. and Roepman, R. (2008) Composition and function of the Crumbs protein complex in the mammalian retina. Exp. Eye Res., 86, 713-726.
13. Bulgakova, N.A. and Knust, E. (2009) The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J. Cell Sci., 122, 2587-2596.
14. van Rossum, A.G., Aartsen, W.M., Meuleman, J., Klooster, J., Malysheva, A., Versteeg, I., Arsanto, J.P., Le Bivic, A. and Wijnholds, J. (2006) Pals1/Mpp5 is required for correct localization of Crb1 at the subapical region in polarized Muller glia cells. Hum. Mol. Genet., 15, 2659-2672.
15. Bazellieres, E., Assemat, E., Arsanto, J.P., Le Bivic, A. and Massey-Harroche, D. (2009) Crumbs proteins in epithelial morphogenesis. Front. Biosci., 14, 2149-2169.
16. Wang, Q. and Margolis, B. (2007) Apical junctional complexes and cell polarity. Kidney Int., 72, 1448-1458.
17. Wang, Q., Hurd, T.W. and Margolis, B. (2004) Tight junction protein Par6 interacts with an evolutionarily conserved region in the amino terminus of PALS1/stardust. J. Biol. Chem., 279, 30715-30721.
18. Hurd, T.W., Gao, L., Roh, M.H., Macara, I.G. and Margolis, B. (2003) Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell Biol., 5, 137-142.
19. Assemat, E., Bazellieres, E., Pallesi-Pocachard, E., Le Bivic, A. and Massey-Harroche, D. (2008) Polarity complex proteins. Biochim. Biophys. Acta, 1778, 614-630.
20. van de Pavert, S.A., Meuleman, J., Malysheva, A., Aartsen, W.M., Versteeg, I., Tonagel, F., Kamphuis, W., McCabe, C.J., Seeliger, M.W. and Wijnholds, J. (2007) 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.
21. Mehalow, A.K., Kameya, S., Smith, R.S., Hawes, N.L., Denegre, J.M., Young, J.A., Bechtold, L., Haider, N.B., Tepass, U., Heckenlively, J.R. et al. (2003) CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum. Mol. Genet., 12, 2179-2189.
22. van den Hurk, J.A., Rashbass, P., Roepman, R., Davis, J., Voesenek, K.E., Arends, M.L., Zonneveld, M.N., van Roekel, M.H., Cameron, K., Rohrschneider, K. et al. (2005) Characterization of the Crumbs homolog 2 (CRB2) gene and analysis of its role in retinitis pigmentosa and Leber congenital amaurosis. Mol. Vis., 11, 263-273.
23. Straight, S.W., Shin, K., Fogg, V.C., Fan, S., Liu, C.J., Roh, M. and Margolis, B. (2004) Loss of PALS1 expression leads to tight junction and polarity defects. Mol. Biol. Cell, 15, 1981-1990.
24. Kim, S., Lehtinen, M.K., Sessa, A., Zappaterra, M.W., Cho, S.H., Gonzalez, D., Boggan, B., Austin, C.A., Wijnholds, J., Gambello, M.J. et al. (2010) The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron, 66, 69-84.
25. den Hollander, A.I., Ghiani, M., de Kok, Y.J., Wijnholds, J., Ballabio, A., Cremers, F.P. and Broccoli, V. (2002) Isolation of Crb1, a mouse homologue of Drosophila crumbs, and analysis of its expression pattern in eye and brain. Mech. Dev., 110, 203-207.
26. Swindell, E.C., Bailey, T.J., Loosli, F., Liu, C., Amaya-Manzanares, F., Mahon, K.A., Wittbrodt, J. and Jamrich, M. (2006) Rx-Cre, a tool for inactivation of gene expression in the developing retina. Genesis, 44, 361-363.
27. Rowan, S. and Cepko, C.L. (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.
28. Koike, C., Nishida, A., Akimoto, K., Nakaya, M.A., Noda, T., Ohno, S. and Furukawa, T. (2005) Function of atypical protein kinase C lambda in differentiating photoreceptors is required for proper lamination of mouse retina. J. Neurosci., 25, 10290-10298.
29. Wei, X. and Malicki, J. (2002) nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat. Genet., 31, 150-157.
30. Omori, Y. and Malicki, J. (2006) oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr. Biol., 16, 945-957.
31. van de Pavert, S.A., Kantardzhieva, A., Malysheva, A., Meuleman, J., Versteeg, I., Levelt, C., Klooster, J., Geiger, S., Seeliger, M.W., Rashbass, P. et al. (2004) Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J. Cell Sci., 117, 4169-4177.
32. Louie, C.M., Caridi, G., Lopes, V.S., Brancati, F., Kispert, A., Lancaster, M.A., Schlossman, A.M., Otto, E.A., Leitges, M., Grone, H.J. et al. (2010) AHI1 is required for photoreceptor outer segment development and is a modifier for retinal degeneration in nephronophthisis. Nat. Genet., 42, 175-180.
33. Gao, J., Cheon, K., Nusinowitz, S., Liu, Q., Bei, D., Atkins, K., Azimi, A., Daiger, S.P., Farber, D.B., Heckenlively, J.R. et al. (2002) Progressive photoreceptor degeneration, outer segment dysplasia, and rhodopsin mislocalization in mice with targeted disruption of the retinitis pigmentosa-1 (Rp1) gene. Proc. Natl Acad. Sci. USA, 99, 5698-5703.
34. Medina, E., Williams, J., Klipfell, E., Zarnescu, D., Thomas, G. and Le Bivic, A. (2002) Crumbs interacts with moesin and beta(Heavy)-spectrin in the apical membrane skeleton of Drosophila. J. Cell Biol., 158, 941-951.
35. Wodarz, A. (2005) Molecular control of cell polarity and asymmetric cell division in Drosophila neuroblasts. Curr. Opin. Cell Biol., 17, 475-481.
36. Ceron, J., Gonzalez, C. and Tejedor, F.J. (2001) Patterns of cell division and expression of asymmetric cell fate determinants in postembryonic neuroblast lineages of Drosophila. Dev. Biol., 230, 125-138.
37. Wohl, S.G., Schmeer, C.W., Friese, T., Witte, O.W. and Isenmann, S. (2011) In situ dividing and phagocytosing retinal microglia express nestin, vimentin, and NG2 in vivo. PLoS One, 6, e22408.
38. Chen, H. and Weber, A.J. (2002) Expression of glial fibrillary acidic protein and glutamine synthetase by Muller cells after optic nerve damage and intravitreal application of brain-derived neurotrophic factor. Glia, 38, 115-125.
39. Langmann, T. (2007) Microglia activation in retinal degeneration. J. Leukoc. Biol., 81, 1345-1351.
40. Imai, Y. and Kohsaka, S. (2002) Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia, 40, 164-174.
41. Zeiss, C.J. and Johnson, E.A. (2004) Proliferation of microglia, but not photoreceptors, in the outer nuclear layer of the rd-1 mouse. Invest. Ophthalmol. Vis. Sci., 45, 971-976.
42. Zeng, H.Y., Zhu, X.A., Zhang, C., Yang, L.P., Wu, L.M. and Tso, M.O. (2005) Identification of sequential events and factors associated with microglial activation, migration, and cytotoxicity in retinal degeneration in rd mice. Invest. Ophthalmol. Vis. Sci., 46, 2992-2999.
43. Fan, S., Hurd, T.W., Liu, C.J., Straight, S.W., Weimbs, T., Hurd, E.A., Domino, S.E. and Margolis, B. (2004) Polarity proteins control ciliogenesis via kinesin motor interactions. Curr. Biol., 14, 1451-1461.
44. Richardson, E.C. and Pichaud, F. (2010) Crumbs is required to achieve proper organ size control during Drosophila head development. Development, 137, 641-650.
45. Karp, C.M., Tan, T.T., Mathew, R., Nelson, D., Mukherjee, C., Degenhardt, K., Karantza-Wadsworth, V. and White, E. (2008) Role of the polarity determinant crumbs in suppressing mammalian epithelial tumor progression. Cancer Res., 68, 4105-4115.
46. Olsen, O., Funke, L., Long, J.F., Fukata, M., Kazuta, T., Trinidad, J.C., Moore, K.A., Misawa, H., Welling, P.A., Burlingame, A.L. et al. (2007) Renal defects associated with improper polarization of the CRB and DLG polarity complexes in MALS-3 knockout mice. J. Cell Biol., 179, 151-164.
47. van de Pavert, S.A., Sanz, A.S., Aartsen, W.M., Vos, R.M., Versteeg, I., Beck, S.C., Klooster, J., Seeliger, M.W. and Wijnholds, J. (2007) Crb1 is a determinant of retinal apical Muller glia cell features. Glia, 55, 1486-1497.
48. Wei, X., Zou, J., Takechi, M., Kawamura, S. and 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.
49. Zou, J., Lathrop, K.L., Sun, M. and 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.
50. Malicki, J. and Driever, W. (1999) oko meduzy mutations affect neuronal patterning in the zebrafish retina and reveal cell-cell interactions of the retinal neuroepithelial sheet. Development, 126, 1235-1246.
51. Pujic, Z. and Malicki, J. (2001) Mutation of the zebrafish glass onion locus causes early cell-nonautonomous loss of neuroepithelial integrity followed by severe neuronal patterning defects in the retina. Dev. Biol., 234, 454-469.
52. Malicki, J., Jo, H. and Pujic, Z. (2003) Zebrafish N-cadherin, encoded by the glass onion locus, plays an essential role in retinal patterning. Dev. Biol., 259, 95-108.
53. Wodarz, A., Grawe, F. and Knust, E. (1993) CRUMBS is involved in the control of apical protein targeting during Drosophila epithelial development. Mech. Dev., 44, 175-187.
54. Igaki, T., Pagliarini, R.A. and Xu, T. (2006) Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr. Biol., 16, 1139-1146.
55. Javier, R.T. (2008) Cell polarity proteins: common targets for tumorigenic human viruses. Oncogene, 27, 7031-7046.
56. Storrs, C.H. and Silverstein, S.J. (2007) PATJ, a tight junction-associated PDZ protein, is a novel degradation target of high-risk human papillomavirus E6 and the alternatively spliced isoform 18 E6. J. Virol., 81, 4080-4090.
57. Pignatelli, V., Cepko, C.L. and Strettoi, E. (2004) Inner retinal abnormalities in a mouse model of Leber's congenital amaurosis. J. Comp. Neurol., 469, 351-359.
58. Deuel, T.A., Liu, J.S., Corbo, J.C., Yoo, S.Y., Rorke-Adams, L.B. and Walsh, C.A. (2006) Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron, 49, 41-53.
59. Koizumi, H., Tanaka, T. and Gleeson, J.G. (2006) Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron, 49, 55-66.
60. Jacobson, S.G., Cideciyan, A.V., Aleman, T.S., Pianta, M.J., Sumaroka, A., Schwartz, S.B., Smilko, E.E., Milam, A.H., Sheffield, V.C. and Stone, E.M. (2003) Crumbs homolog 1 (CRB1) mutations result in a thick human retina with abnormal lamination. Hum. Mol. Genet., 12, 1073-1078.
61. Aleman, T.S., Cideciyan, A.V., Aguirre, G.K., Huang, W.C., Mullins, C.L., Roman, A.J., Sumaroka, A., Olivares, M.B., Tsai, F.F., Schwartz, S.B. et al. (2011) Human CRB1-associated retinal degeneration: comparison with the rd8 Crb1-mutant mouse model. Invest. Ophthalmol. Vis. Sci., 52, 6898-6910.
62. Henderson, R.H., Mackay, D.S., Li, Z., Moradi, P., Sergouniotis, P., Russell-Eggitt, I., Thompson, D.A., Robson, A.G., Holder, G.E., Webster, A.R. et al. (2011) Phenotypic variability in patients with retinal dystrophies due to mutations in CRB1. Br. J. Ophthalmol., 95, 811-817.
63. Park, B., Alves, C.H., Lundvig, D.M., Tanimoto, N., Beck, S.C., Huber, G., Richard, F., Klooster, J., Andlauer, T.F., Swindell, E.C. et al. (2011) PALS1 is essential for retinal pigment epithelium structure and neural retina stratification. J. Neurosci., 31, 17230-17241.
64. Molday, R.S. and MacKenzie, D. (1983) Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry, 22, 653-660.
65. Abd-El-Barr, M.M., Pennesi, M.E., Saszik, S.M., Barrow, A.J., Lem, J., Bramblett, D.E., Paul, D.L., Frishman, L.J. and Wu, S.M. (2009) Genetic dissection of rod and cone pathways in the darkadapted mouse retina. J. Neurophysiol., 102, 1945-1955.