Crumbs3 Is Essential for Proper Epithelial Development and Viability

REFERENCES

• Dow LE, Humbert PO. 2007. Polarity regulators and the control of epithelial architecture, cell migration, and tumorigenesis. Int. Rev. Cytol. 262:253–302. http://dx.doi.org/10.1016/S0074-7696(07)62006-3.
   PubMedGoogle Scholar
• Pieczynski J, Margolis B. 2011. Protein complexes that control renal epithelial polarity. Am. J. Physiol. Renal Physiol. 300:F589–F601. http://dx.doi.org/10.1152/ajprenal.00615.2010.
   PubMedGoogle Scholar
• Datta A, Bryant DM, Mostov KE. 2011. Molecular regulation of lumen morphogenesis. Curr. Biol. 21:R126–R136. http://dx.doi.org/10.1016/j.cub.2010.12.003.
   PubMed Web of Science ®Google Scholar
• Tepass U. 2012. The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu. Rev. Cell Dev. Biol. 28:655–685. http://dx.doi.org/10.1146/annurev-cellbio-092910-154033.
   PubMedGoogle Scholar
• Bulgakova N, Knust E. 2009. The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J. Cell Sci. 122:2587–2596. http://dx.doi.org/10.1242/jcs.023648.
   PubMed Web of Science ®Google Scholar
• Joberty G, Petersen C, Gao L, Macara IG. 2000. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2:531–539. http://dx.doi.org/10.1038/35019573.
   PubMed Web of Science ®Google Scholar
• Horikoshi Y, Suzuki A, Yamanaka T, Sasaki K, Mizuno K, Sawada H, Yonemura S, Ohno S. 2009. Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J. Cell Sci. 122:1595–1606. http://dx.doi.org/10.1242/jcs.043174.
   PubMed Web of Science ®Google Scholar
• Medina E, Williams J, Klipfell E, Zarnescu D, Thomas G, 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. http://dx.doi.org/10.1083/jcb.200203080.
   PubMed Web of Science ®Google Scholar
• Laprise P, Beronja S, Silva-Gagliardi NF, Pellikka M, Jensen AM, McGlade CJ, Tepass U. 2006. The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev. Cell 11:363–374. http://dx.doi.org/10.1016/j.devcel.2006.06.001.
   PubMed Web of Science ®Google Scholar
• Laprise P, Lau KM, Harris KP, Silva-Gagliardi NF, Paul SM, Beronja S, Beitel GJ, McGlade CJ, Tepass U. 2009. Yurt, Coracle, Neurexin IV and the Na(+),K(+)-ATPase form a novel group of epithelial polarity proteins. Nature 459:1141–1145. http://dx.doi.org/10.1038/nature08067.
   PubMedGoogle Scholar
• Christensen A, Jensen A. 2008. Tissue-specific requirements for specific domains in the FERM protein Moe/Epb4.1l5 during early zebrafish development. BMC Dev. Biol. 8:3. http://dx.doi.org/10.1186/1471-213X-8-3.
   PubMedGoogle Scholar
• Ling C, Zheng Y, Yin F, Yu J, Huang J, Hong Y, Wu S, Pan D. 2010. The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc. Natl. Acad. Sci. U. S. A. 107:10532–10537. http://dx.doi.org/10.1073/pnas.1004279107.
   PubMed Web of Science ®Google Scholar
• Grzeschik N, Parsons L, Allott M, Harvey K, Richardson H. 2010. Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr. Biol. 20:573–581. http://dx.doi.org/10.1016/j.cub.2010.01.055.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1038/13848.
   PubMed Web of Science ®Google Scholar
• Xiao Z, Patrakka J, Nukui M, Chi L, Niu D, Betsholtz C, Pikkarainen T, Vainio S, Tryggvason K. 2011. Deficiency in crumbs homolog 2 (Crb2) affects gastrulation and results in embryonic lethality in mice. Dev. Dyn. 240:2646–2656. http://dx.doi.org/10.1002/dvdy.22778.
   PubMed Web of Science ®Google Scholar
• Schmidt-Ott K, Yang J, Chen X, Wang H, Paragas N, Mori K, Li J-Y, Lu B, Costantini F, Schiffer M, Bottinger E, Barasch J. 2005. Novel regulators of kidney development from the tips of the ureteric bud. J. Am. Soc. Nephrol. 16:1993–2002. http://dx.doi.org/10.1681/ASN.2004121127.
   PubMed Web of Science ®Google Scholar
• Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, Mikulits W, Brabletz T, Strand D, Obrist P, Sommergruber W, Schweifer N, Wernitznig A, Beug H, Foisner R, Eger A. 2007. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26:6979–6988. http://dx.doi.org/10.1038/sj.onc.1210508.
   PubMed Web of Science ®Google Scholar
• Whiteman EL, Liu CJ, Fearon ER, Margolis B. 2008. The transcription factor snail represses Crumbs3 expression and disrupts apico-basal polarity complexes. Oncogene 27:3875–3879. http://dx.doi.org/10.1038/onc.2008.9.
   PubMedGoogle Scholar
• Torkko JM, Manninen A, Schuck S, Simons K. 2008. Depletion of apical transport proteins perturbs epithelial cyst formation and ciliogenesis. J. Cell Sci. 121:1193–1203. http://dx.doi.org/10.1242/jcs.015495.
   PubMedGoogle Scholar
• Schlüter MA, Pfarr CS, Pieczynski J, Whiteman EL, Hurd TW, Fan S, Liu CJ, Margolis B. 2009. Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol. Biol. Cell 20:4652–4663. http://dx.doi.org/10.1091/mbc.E09-02-0137.
   PubMed Web of Science ®Google Scholar
• Hiraoka M, Abe A, Lu Y, Yang K, Han X, Gross RW, Shayman JA. 2006. Lysosomal phospholipase A2 and phospholipidosis. Mol. Cell. Biol. 26:6139–6148. http://dx.doi.org/10.1128/MCB.00627-06.
   PubMed Web of Science ®Google Scholar
• Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 90:8424–8428. http://dx.doi.org/10.1073/pnas.90.18.8424.
   PubMed Web of Science ®Google Scholar
• Marshall OJ. 2004. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471–2472. http://dx.doi.org/10.1093/bioinformatics/bth254.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/S0378111902010843.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1083/jcb.200109010.
   PubMed Web of Science ®Google Scholar
• Harder JL, Whiteman EL, Pieczynski JN, Liu CJ, Margolis B. 2012. Snail destabilizes cell surface Crumbs3a. Traffic 13:1170–1185. http://dx.doi.org/10.1111/j.1600-0854.2012.01376.x.
   PubMedGoogle Scholar
• Kee HL, Dishinger JF, Blasius TL, Liu CJ, Margolis B, Verhey KJ. 2012. A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat. Cell Biol. 14:431–437. http://dx.doi.org/10.1038/ncb2450.
   PubMed Web of Science ®Google Scholar
• Sheehan DC, Hrapchak BB. 1981. Theory and practice of histotechnology, 2nd ed, p 474. C. V. Mosby, St. Louis, MO.
   Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671–675. http://dx.doi.org/10.1038/nmeth.2089.
   PubMed Web of Science ®Google Scholar
• Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. U. S. A. 93:5860–5865. http://dx.doi.org/10.1073/pnas.93.12.5860.
   PubMed Web of Science ®Google Scholar
• Straight SW, Shin K, Fogg VC, Fan S, Liu CJ, Roh M, Margolis B. 2004. Loss of PALS1 expression leads to tight junction and polarity defects. Mol. Biol. Cell 15:1981–1990. http://dx.doi.org/10.1091/mbc.E03-08-0620.
   PubMed Web of Science ®Google Scholar
• Wang Q, Margolis B. 2007. Apical junctional complexes and cell polarity. Kidney Int. 72:1448–1458. http://dx.doi.org/10.1038/sj.ki.5002579.
   PubMed Web of Science ®Google Scholar
• Robinson BS, Huang J, Hong Y, Moberg KH. 2010. Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr. Biol. 20:582–590. http://dx.doi.org/10.1016/j.cub.2010.03.019.
   PubMed Web of Science ®Google Scholar
• Chen CL, Gajewski KM, Hamaratoglu F, Bossuyt W, Sansores-Garcia L, Tao C, Halder G. 2010. The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 107:15810–15815. http://dx.doi.org/10.1073/pnas.1004060107.
   PubMed Web of Science ®Google Scholar
• Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL. 2010. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev. Cell 19:831–844. http://dx.doi.org/10.1016/j.devcel.2010.11.012.
   PubMed Web of Science ®Google Scholar
• Herranz H, Stamataki E, Feiguin F, Milan M. 2006. Self-refinement of Notch activity through the transmembrane protein Crumbs: modulation of gamma-secretase activity. EMBO Rep. 7:297–302. http://dx.doi.org/10.1038/sj.embor.7400617.
   PubMed Web of Science ®Google Scholar
• Mitsuishi Y, Hasegawa H, Matsuo A, Araki W, Suzuki T, Tagami S, Okochi M, Takeda M, Roepman R, Nishimura M. 2010. Human CRB2 inhibits gamma-secretase cleavage of amyloid precursor protein by binding to the presenilin complex. J. Biol. Chem. 285:14920–14931. http://dx.doi.org/10.1074/jbc.M109.038760.
   PubMedGoogle Scholar
• Richardson EC, Pichaud F. 2010. Crumbs is required to achieve proper organ size control during Drosophila head development. Development 137:641–650. http://dx.doi.org/10.1242/dev.041913.
   PubMed Web of Science ®Google Scholar
• Mathan M, Moxey PC, Trier JS. 1976. Morphogenesis of fetal rat duodenal villi. Am. J. Anat. 146:73–92. http://dx.doi.org/10.1002/aja.1001460104.
   PubMedGoogle Scholar
• Grosse AS, Pressprich MF, Curley LB, Hamilton KL, Margolis B, Hildebrand JD, Gumucio DL. 2011. Cell dynamics in fetal intestinal epithelium: implications for intestinal growth and morphogenesis. Development 138:4423–4432. http://dx.doi.org/10.1242/dev.065789.
   PubMedGoogle Scholar
• Saotome I, Curto M, McClatchey AI. 2004. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 6:855–864. http://dx.doi.org/10.1016/j.devcel.2004.05.007.
   PubMedGoogle Scholar
• Casaletto JB, Saotome I, Curto M, McClatchey AI. 2011. Ezrin-mediated apical integrity is required for intestinal homeostasis. Proc. Natl. Acad. Sci. U. S. A. 108:11924–11929. http://dx.doi.org/10.1073/pnas.1103418108.
   PubMedGoogle Scholar
• Tanentzapf G, Tepass U. 2003. Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5:46–52. http://dx.doi.org/10.1038/ncb896.
   PubMed Web of Science ®Google Scholar
• Franz A, Riechmann V. 2010. Stepwise polarisation of the Drosophila follicular epithelium. Dev. Biol. 338:136–147. http://dx.doi.org/10.1016/j.ydbio.2009.11.027.
   PubMedGoogle Scholar
• McKinley RF, Yu CG, Harris TJ. 2012. Assembly of Bazooka polarity landmarks through a multifaceted membrane-association mechanism. J. Cell Sci. 125:1177–1190. http://dx.doi.org/10.1242/jcs.091884.
   PubMedGoogle Scholar
• Wodarz A, Ramrath A, Grimm A, Knust E. 2000. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150:1361–1374. http://dx.doi.org/10.1083/jcb.150.6.1361.
   PubMed Web of Science ®Google Scholar
• Sotillos S, Diaz-Meco MT, Caminero E, Moscat J, Campuzano S. 2004. DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J. Cell Biol. 166:549–557. http://dx.doi.org/10.1083/jcb.200311031.
   PubMed Web of Science ®Google Scholar
• Fletcher GC, Lucas EP, Brain R, Tournier A, Thompson BJ. 2012. Positive feedback and mutual antagonism combine to polarize Crumbs in the Drosophila follicle cell epithelium. Curr. Biol. 22:1116–1122. http://dx.doi.org/10.1016/j.cub.2012.04.020.
   PubMedGoogle Scholar
• Carey B, Trapnell BC. 2010. The molecular basis of pulmonary alveolar proteinosis. Clin. Immunol. 135:223–235. http://dx.doi.org/10.1016/j.clim.2010.02.017.
   PubMed Web of Science ®Google Scholar
• Fan S, Hurd TW, Liu CJ, Straight SW, Weimbs T, Hurd EA, Domino SE, Margolis B. 2004. Polarity proteins control ciliogenesis via kinesin motor interactions. Curr. Biol. 14:1451–1461. http://dx.doi.org/10.1016/j.cub.2004.08.025.
   PubMed Web of Science ®Google Scholar
• Chao J, Wood JG, Gonzalez NC. 2011. Alveolar macrophages initiate the systemic microvascular inflammatory response to alveolar hypoxia. Respir. Physiol. Neurobiol. 178:439–448. http://dx.doi.org/10.1016/j.resp.2011.03.008.
   PubMedGoogle Scholar
• Cardenas-Rodriguez M, Badano JL. 2009. Ciliary biology: understanding the cellular and genetic basis of human ciliopathies. Am. J. Med. Genet. C Semin. Med. Genet. 151C:263–280. http://dx.doi.org/10.1002/ajmg.c.30227.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/j.cub.2006.03.058.
   PubMedGoogle Scholar
• Fedeles S, Gallagher AR. 16 November 2012. Cell polarity and cystic kidney disease. Pediatr. Nephrol. [Epub ahead of print.] http://dx.doi.org/10.1007/s00467-012-2337-z.
   Google Scholar
• Carroll TJ, Yu J. 2012. The kidney and planar cell polarity. Curr. Top. Dev. Biol. 101:185–212. http://dx.doi.org/10.1016/B978-0-12-394592-1.00011-9.
   PubMedGoogle Scholar
• Olsen O, Funke L, Long JF, Fukata M, Kazuta T, Trinidad JC, Moore KA, Misawa H, Welling PA, Burlingame AL, Zhang M, Bredt DS. 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. http://dx.doi.org/10.1083/jcb.200702054.
   PubMedGoogle Scholar
• Fehon RG, McClatchey AI, Bretscher A. 2010. Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11:276–287. http://dx.doi.org/10.1038/nrm2866.
   PubMed Web of Science ®Google Scholar
• Fogg VC, Liu CJ, Margolis B. 2005. Multiple regions of Crumbs3 are required for tight junction formation in MCF10A cells. J. Cell Sci. 118:2859–2869. http://dx.doi.org/10.1242/jcs.02412.
   PubMed Web of Science ®Google Scholar
• Charras GT, Hu CK, Coughlin M, Mitchison TJ. 2006. Reassembly of contractile actin cortex in cell blebs. J. Cell Biol. 175:477–490. http://dx.doi.org/10.1083/jcb.200602085.
   PubMed Web of Science ®Google Scholar