The F-box protein Slmb restricts the activity of aPKC to polarize epithelial cells

Development (Cambridge)

Volumn 141, Issue 15, 2014, Pages 2978-2983

  Skwarek, Lara C ^a   Windler, Sarah L ^a   de Vreede, Geert ^a   Rogers, Gregory C ^b   Bilder, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Drosophila; Epithelia; Par; Polarity; Tumor; Ubiquitin ligase

Indexed keywords

ATYPICAL PROTEIN KINASE; F ACTIN; F BOX PROTEIN; INTERSTITIAL COLLAGENASE; MEMBRANE PROTEIN; PROTEIN KINASE; PROTEIN SLMB; REGULATOR PROTEIN; SCAFFOLD PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ADULT; ANIMAL TISSUE; ARTICLE; CELL POLARITY; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; DROSOPHILA; EPITHELIUM CELL; FEMALE; HETEROZYGOSITY; IMAGINAL DISC; MISSENSE MUTATION; MITOTIC RECOMBINATION; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN RESTRICTION; TUMOR SUPPRESSOR GENE; UPREGULATION;

DROSOPHILA; EPITHELIA; PAR; POLARITY; TUMOR; UBIQUITIN LIGASE;

ALLELES; ANIMALS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSOMES; EPITHELIAL CELLS; F-BOX PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LYSOSOMES; MUTATION; PHENOTYPE; PROTEIN KINASE C; PROTEIN TRANSPORT; UBIQUITIN-PROTEIN LIGASES;

EID: 84904681383     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.109694     Document Type: Article

References (38)

1. Bilder, D. (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 18, 1909-1925.
2. Bilder, D., Li, M. and Perrimon, N. (2000). Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289, 113-116.
3. Blaumueller, C. M. and Mlodzik, M. (2000). The Drosophila tumor suppressor expanded regulates growth, apoptosis, and patterning during development. Mech. Dev. 92, 251-262.
4. Buster, D. W., Daniel, S. G., Nguyen, H. Q., Windler, S. L., Skwarek, L. C., Peterson, M., Roberts, M., Meserve, J. H., Hartl, T., Klebba, J. E. et al. (2013). SCFSlimb ubiquitin ligase suppresses condensin II-mediated nuclear reorganization by degrading Cap-H2. J. Cell Biol. 201, 49-63.
5. Chartier, F. J.-M., Hardy, É. J.-L. and Laprise, P. (2011). Crumbs controls epithelial integrity by inhibiting Rac1 and PI3K. J. Cell Sci. 124, 3393-3398.
6. Colosimo, P. F., Liu, X., Kaplan, N. A. and Tolwinski, N. S. (2009). GSK3βaffects apical-basal polarity and cell-cell adhesion by regulating aPKC levels. Dev. Dyn. 239, 115-125.
7. de Vreede, G., Schoenfeld, J. D., Windler, S. L., Morrison, H., Lu, H. and Bilder, D. (2014). The Scribble module regulates retromer-dependent endocytic trafficking during epithelial polarization. Development 141, 2796-2802.
8. Doggett, K., Grusche, F. A., Richardson, H. E. and Brumby, A. M. (2011). Loss of the Drosophila cell polarity regulator Scribbled promotes epithelial tissue overgrowth and cooperation with oncogenic Ras-Raf through impaired Hippo pathway signaling. BMC Dev. Biol. 11, 57.
9. Eaton, S. (2008). Retromer retrieves Wntless. Dev. Cell 14, 4-6.
10. Eder, A. M., Sui, X., Rosen, D. G., Nolden, L. K., Cheng, K. W., Lahad, J. P., Kango-Singh, M., Lu, K. H., Warneke, C. L., Atkinson, E. N. et al. (2005). Atypical PKCiota contributes to poor prognosis through loss of apical-basal polarity and cyclin E overexpression in ovarian cancer. Proc. Natl. Acad. Sci. USA 102, 12519-12524.
11. Elsum, I., Yates, L., Humbert, P. O. and Richardson, H. E. (2012). The ScribbleDlg-Lgl polarity module in development and cancer: from flies to man. Essays Biochem. 53, 141-168.
12. Fernández, B. G., Gaspar, P., Brás-Pereira, C., Jezowska, B., Rebelo, S. R. and Janody, F. (2011). Actin-Capping Protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 138, 2337-2346.
13. Frescas, D. and Pagano, M. (2008). Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 8, 438-449.
14. Goldstein, B. and Macara, I. G. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622.
15. Haack, T., Bergstralh, D. T. and St Johnston, D. (2013). Damage to the Drosophila follicle cell epithelium produces"false clones"with apparent polarity phenotypes.
16. Halbsgut, N., Linnemannstöns, K., Zimmermann, L. I. and Wodarz, A. (2011). Apical-basal polarity in Drosophila neuroblasts is independent of vesicular trafficking. Mol. Biol. Cell 22, 4373-4379.
17. Jiang, J. and Struhl, G. (1998). Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391, 493-496.
18. Laprise, P. and Tepass, U. (2011). Novel insights into epithelial polarity proteins in Drosophila. Trends Cell Biol. 21, 401-408.
19. Lee, S., Wang, J.-W., Yu, W. and Lu, B. (2012). Phospho-dependent ubiquitination and degradation of PAR-1 regulates synaptic morphology and tau-mediated Aβ toxicity in Drosophila. Nat. Commun. 3, 1312.
20. Li, S., Wang, C., Sandanaraj, E., Aw, S. S. Y., Koe, C. T., Wong, J. J. L., Yu, F., Ang, B. T., Tang, C. and Wang, H. (2014). The SCF SlimbE3 ligase complex regulates asymmetric division to inhibit neuroblast overgrowth. EMBO Rep. 15, 619-729.
21. Menut, L., Vaccari, T., Dionne, H., Hill, J., Wu, G. and Bilder, D. (2007). A mosaic genetic screen for Drosophila neoplastic tumor suppressor genes based on defective pupation. Genetics177, 1667.
22. Milétich, I. and Limbourg-Bouchon, B. (2000). Drosophila null slimb clones transiently deregulate Hedgehog-independent transcription of wingless in all limb discs, and induce decapentaplegic transcription linked to imaginal disc regeneration. Mech. Dev. 93, 15-26.
23. Morais-de-Sá, E., Vega-Rioja, A., Trovisco, V. and St Johnston, D. (2013). Oskar is targeted for degradation by the sequential action of Par-1, GSK-3, and the SCFslimb ubiquitin ligase. Dev. Cell 26, 303-314.
24. Morrison, H. A., Dionne, H., Rusten, T. E., Brech, A., Fisher, W. W., Pfeiffer, B. D., Celniker, S. E., Stenmark, H. and Bilder, D. (2008). Regulation of early endosomal entry by the Drosophila tumor suppressors Rabenosyn and Vps45. Mol. Biol. Cell 19, 4167-4176.
25. Noureddine, M. A., Donaldson, T. D., Thacker, S. A. and Duronio, R. J. (2002). Drosophila Roc1a encodes a RING-H2 protein with a unique function in processing the Hh signal transducer Ci by the SCF E3 ubiquitin ligase. Dev. Cell 2, 757-770.
26. Partanen, J. I., Tervonen, T. A. and Klefström, J. (2013). Breaking the epithelial polarity barrier in cancer: the strange case of LKB1/PAR-4. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20130111.
27. Robinson, B. S. and Moberg, K. H. (2011). Drosophila endocytic neoplastic tumor suppressor genes regulate Sav/Wts/Hpo signaling and the c-Jun N-terminal kinase pathway. Cell Cycle 10, 4110-4118.
28. Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M. and Rogers, S. L. (2009). The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 184, 225-239.
29. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
30. Shivas, J. M., Morrison, H. A., Bilder, D. and Skop, A. R. (2010). Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 20, 445-452.
31. Sotillos, S., Di{dotless}́az-Meco, M. T., Caminero, E., Moscat, J. and Campuzano, S. (2004). DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J. Cell Biol. 166, 549-557.
32. St Johnston, D. and Ahringer, J. (2010). Cell polarity in eggs and epithelia: parallels and diversity. Cell 141, 757-774.
33. Sun, G. and Irvine, K. D. (2011). Regulation of Hippo signaling by Jun kinase signaling during compensatory cell proliferation and regeneration, and in neoplastic tumors. Dev. Biol. 350, 139-151.
34. Tanentzapf, G. and Tepass, U. (2003). Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5, 46-52.
35. 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.
36. Theodosiou, N. A., Zhang, S., Wang, W. Y. and Xu, T. (1998). slimb coordinates wg and dpp expression in the dorsal-ventral and anterior-posterior axes during limb development. Development 125, 3411-3416.
37. Windler, S. L. and Bilder, D. (2010). Endocytic internalization routes required for Delta/Notch signaling. Curr. Biol. 20, 538-543.
38. Zonies, S., Motegi, F., Hao, Y. and Seydoux, G. (2010). Symmetry breaking and polarization of the C. elegans zygote by the polarity protein PAR-2. Development 137, 1669-1677.