The Drosophila F-box protein Fbxl7 binds to the protocadherin Fat and regulates Dachs localization and Hippo signaling

eLife

Volumn 3, Issue August2014, 2014, Pages 1-25

  Bosch, Justin A ^a   Sumabat, Taryn M ^a   Hafezi, Yassi ^a   Pellock, Brett J ^b   Gandhi, Kevin D ^a   Hariharan, Iswar K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PROVIDENCE COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; DACHS PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; F BOX PROTEIN; FAT PROTEIN, DROSOPHILA; FBXL7 PROTEIN, DROSOPHILA; HPO PROTEIN, DROSOPHILA; MYOSIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ANIMAL; BINDING SITE; CELL POLARITY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MORPHOGENESIS; MUTATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSPORT VESICLE;

ANIMALS; BINDING SITES; BODY PATTERNING; CELL ADHESION MOLECULES; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; F-BOX PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; MYOSINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSPORT VESICLES;

EID: 84922430062     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03383     Document Type: Article

References (74)

1. Ambegaonkar AA, Pan G, Mani M, Feng Y, Irvine KD. 2012. Propagation of Dachsous-Fat planar cell polarity. Current Biology 22:1302-1308. doi: 10.1016/j.cub.2012.05.049.
2. Bella J, Hindle KL, McEwan PA, Lovell SC. 2008. The leucine-rich repeat structure. Cellular and Molecular Life Sciences 65:2307-2333. doi: 10.1007/s00018-008-8019-0.
3. Bennett FC, Harvey KF. 2006. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Current Biology 16:2101-2110. doi: 10.1016/j.cub.2006.09.045.
4. Boedigheimer M, Laughon A. 1993. Expanded: a gene involved in the control of cell proliferation in imaginal discs. Development 118:1291-1301.
5. Bossuyt W, Chen CL, Chen Q, Sudol M, McNeill H, Pan D, Kopp A, Halder G. 2013. An evolutionary shift in the regulation of the Hippo pathway between mice and flies. Oncogene 33:1218-1228. doi: 10.1038/onc.2013.82.
6. Bosveld F, Bonnet I, Guirao B, Tlili S, Wang Z, Petitalot A, Marchand R, Bardet PL, Marcq P, Graner F, Bellaïche Y. 2012. Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 336:724-727. doi: 10.1126/science.1221071.
7. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. 2003. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113:25-36. doi: 10.1016/S0092-8674(03)00231-9.
8. Brittle A, Thomas C, Strutt D. 2012. Planar polarity specification through asymmetric subcellular localization of Fat and Dachsous. Current Biology 22:907-914. doi: 10.1016/j.cub.2012.03.053.
9. Brittle AL, Repiso A, Casal J, Lawrence PA, Strutt D. 2010. Four-jointed modulates growth and planar polarity by reducing the affinity of dachsous for fat. Current Biology 20:803-810. doi: 10.1016/j.cub.2010.03.056.
10. Bryant PJ, Huettner B, Held LI Jnr, Ryerse J, Szidonya J. 1988. Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila. Developmental Biology 129:541-554. doi: 10.1016/0012-1606(88)90399-5.
11. Carrano AC, Eytan E, Hershko A, Pagano M. 1999. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nature Cell Biology 1:193-199. doi: 10.1038/12013.
12. Cho E, Feng Y, Rauskolb C, Maitra S, Fehon R, Irvine KD. 2006. Delineation of a Fat tumor suppressor pathway. Nature Genetics 38:1142-1150. doi: 10.1038/ng1887.
13. Clark HF, Brentrup D, Schneitz K, Bieber A, Goodman C, Noll M. 1995. Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes & Development 9:1530-1542. doi: 10.1101/gad.9.12.1530.
14. Coon TA, Glasser JR, Mallampalli RK, Chen BB. 2012. Novel E3 ligase component FBXL7 ubiquitinates and degrades Aurora A, causing mitotic arrest. Cell Cycle 11:721-729. doi: 10.4161/cc.11.4.19171.
15. Dui W, Lu W, Ma J, Jiao R. 2012. A systematic phenotypic screen of F-box genes through a tissue-specific RNAi-based approach in Drosophila. Journal of Genetics and Genomics 39:397-413. doi: 10.1016/j.jgg.2012.05.009.
16. Fanto M, Clayton L, Meredith J, Hardiman K, Charroux B, Kerridge S, McNeill H. 2003. The tumor-suppressor and cell adhesion molecule Fat controls planar polarity via physical interactions with Atrophin, a transcriptional co-repressor. Development 130:763-774. doi: 10.1242/dev.00304.
17. Feng Y, Irvine KD. 2007. Fat and expanded act in parallel to regulate growth through warts. Proceedings of the National Academy of Sciences of USA 104:20362-20367. doi: 10.1073/pnas.0706722105.
18. Feng Y, Irvine KD. 2009. Processing and phosphorylation of the Fat receptor. Proceedings of the National Academy of Sciences of USA 106:11989-11994. doi: 10.1073/pnas.0811540106.
19. Galan JM, Peter M. 1999. Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. Proceedings of the National Academy of Sciences of USA 96:9124-9129. doi: 10.1073/pnas.96.16.9124.
20. Hafezi Y, Bosch JA, Hariharan IK. 2012. Differences in levels of the transmembrane protein Crumbs can influence cell survival at clonal boundaries. Developmental Biology 368:358-369. doi: 10.1016/j.ydbio.2012.06.001.
21. Haglund K, Shimokawa N, Szymkiewicz I, Dikic I. 2002. Cbl-directed monoubiquitination of CIN85 is involved in regulation of ligand-induced degradation of EGF receptors. Proceedings of the National Academy of Sciences of USA 99:12191-12196. doi: 10.1073/pnas.192462299.
22. Halder G, Johnson RL. 2011. Hippo signaling: growth control and beyond. Development 138:9-22. doi: 10.1242/dev.045500.
23. Hamaratoglu F, Willecke M, Kango-Singh M, Nolo R, Hyun E, Tao C, Jafar-Nejad H, Halder G. 2006. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nature Cell Biology 8:27-36. doi: 10.1038/ncb1339.
24. Hsiung YG, Chang HC, Pellequer JL, La Valle R, Lanker S, Wittenberg C. 2001. F-box protein Grr1 interacts with phosphorylated targets via the cationic surface of its leucine-rich repeat. Molecular and Cellular Biology 21:2506-2520. doi: 10.1128/MCB.21.7.2506-2520.2001.
25. Huang J, Wu S, Barrera J, Matthews K, Pan D. 2005. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122:421-434. doi: 10.1016/j.cell.2005.06.007.
26. Ishikawa HO, Takeuchi H, Haltiwanger RS, Irvine KD. 2008. Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 321:401-404. doi: 10.1126/science.1158159.
27. Johnson RI, Bao S, Cagan RL. 2012. Interactions between Drosophila IgCAM adhesion receptors and cindr, the Cd2ap/Cin85 ortholog. Developmental Dynamics 241:1933-1943. doi: 10.1002/dvdy.23879.
28. Johnson RI, Sedgwick A, D'Souza-Schorey C, Cagan RL. 2011. Role for a Cindr-Arf6 axis in patterning emerging epithelia. Molecular Biology of the Cell 22:4513-4526. doi: 10.1091/mbc.E11-04-0305.
29. Johnson RI, Seppa MJ, Cagan RL. 2008. The Drosophila CD2AP/CIN85 orthologue Cindr regulates junctions and cytoskeleton dynamics during tissue patterning. The Journal of Cell Biology 180:1191-1204. doi: 10.1083/jcb.200706108.
30. Jursnich VA, Fraser SE, Held LI Jnr, Ryerse J, Bryant PJ. 1990. Defective gap-junctional communication associated with imaginal disc overgrowth and degeneration caused by mutations of the dco gene in Drosophila. Developmental Biology 140:413-429. doi: 10.1016/0012-1606(90)90090-6.
31. Ko HW, Jiang J, Edery I. 2002. Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420:673-678. doi: 10.1038/nature01272.
32. Kobe B, Deisenhofer J. 1994. The leucine-rich repeat: a versatile binding motif. Trends in Biochemical Sciences 19:415-421. doi: 10.1016/0968-0004(94)90090-6.
33. Kwon Y, Vinayagam A, Sun X, Dephoure N, Gygi SP, Hong P, Perrimon N. 2013. The Hippo signaling pathway interactome. Science 342:737-740. doi: 10.1126/science.1243971.
34. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Research 40:D302-D305. doi: 10.1093/nar/gkr931.
35. Ma D, Yang CH, McNeill H, Simon MA, Axelrod JD. 2003. Fidelity in planar cell polarity signalling. Nature 421:543-547. doi: 10.1038/nature01366.
36. Mahoney PA, Weber U, Onofrechuk P, Biessmann H, Bryant PJ, Goodman CS. 1991. The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 67:853-868. doi: 10.1016/0092-8674(91)90359-7.
37. Mao Y, Kucuk B, Irvine KD. 2009. Drosophila lowfat, a novel modulator of Fat signaling. Development 136:3223-3233. doi: 10.1242/dev.036152.
38. Mao Y, Rauskolb C, Cho E, Hu WL, Hayter H, Minihan G, Katz FN, Irvine KD. 2006. Dachs: an unconventional myosin that functions downstream of Fat to regulate growth, affinity and gene expression in Drosophila. Development 133:2539-2551. doi: 10.1242/dev.02427.
39. Mao Y, Tournier AL, Bates PA, Gale JE, Tapon N, Thompson BJ. 2011. Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes & Development 25:131-136. doi: 10.1101/gad.610511.
40. Matakatsu H, Blair SS. 2004. Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 131:3785-3794. doi: 10.1242/dev.01254.
41. Matakatsu H, Blair SS. 2006. Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins. Development 133:2315-2324. doi: 10.1242/dev.02401.
42. Matakatsu H, Blair SS. 2008. The DHHC palmitoyltransferase approximated regulates Fat signaling and Dachs localization and activity. Current Biology 18:1390-1395. doi: 10.1016/j.cub.2008.07.067.
43. Matakatsu H, Blair SS. 2012. Separating planar cell polarity and Hippo pathway activities of the protocadherins Fat and Dachsous. Development 139:1498-1508. doi: 10.1242/dev.070367.
44. Nelson DE, Randle SJ, Laman H. 2013. Beyond ubiquitination: the atypical functions of Fbxo7 and other F-box proteins. Open Biology 3:130131. doi: 10.1098/rsob.130131.
45. Pan D. 2010. The hippo signaling pathway in development and cancer. Developmental Cell 19:491-505. doi: 10.1016/j.devcel.2010.09.011.
46. Pan G, Feng Y, Ambegaonkar AA, Sun G, Huff M, Rauskolb C, Irvine KD. 2013. Signal transduction by the Fat cytoplasmic domain. Development 140:831-842. doi: 10.1242/dev.088534.
47. Park HO, Chant J, Herskowitz I. 1993. BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature 365:269-274. doi: 10.1038/365269a0.
48. Petrelli A, Gilestro GF, Lanzardo S, Comoglio PM, Migone N, Giordano S. 2002. The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 416:187-190. doi: 10.1038/416187a.
49. Rauskolb C, Pan G, Reddy BV, Oh H, Irvine KD. 2011. Zyxin links fat signaling to the hippo pathway. PLOS Biology 9:e1000624. doi: 10.1371/journal.pbio.1000624.
50. Rogulja D, Rauskolb C, Irvine KD. 2008. Morphogen control of wing growth through the Fat signaling pathway. Developmental Cell 15:309-321. doi: 10.1016/j.devcel.2008.06.003.
51. Schmick M, Vartak N, Papke B, Kovacevic M, Truxius DC, Rossmannek L, Bastiaens PI. 2014. KRas localizes to the plasma membrane by spatial cycles of solubilization, trapping and vesicular transport. Cell 157:459-471. doi: 10.1016/j.cell.2014.02.051.
52. Sharma P, McNeill H. 2013. Fat and dachsous cadherins. Progress in Molecular Biology and Translational Science 116:215-235. doi: 10.1016/B978-0-12-394311-8.00010-8.
53. Silva E, Tsatskis Y, Gardano L, Tapon N, McNeill H. 2006. The tumor-suppressor gene fat controls tissue growth upstream of expanded in the hippo signaling pathway. Current Biology 16:2081-2089. doi: 10.1016/j.cub.2006.09.004.
54. Simon MA. 2004. Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression. Development 131:6175-6184. doi: 10.1242/dev.01550.
55. Simon MA, Xu A, Ishikawa HO, Irvine KD. 2010. Modulation of fat:dachsous binding by the cadherin domain kinase four-jointed. Current Biology 20:811-817. doi: 10.1016/j.cub.2010.04.016.
56. Skaar JR, Pagan JK, Pagano M. 2013. Mechanisms and function of substrate recruitment by F-box proteins. Nature Reviews Molecular Cell Biology 14:369-381. doi: 10.1038/nrm3582.
57. Sopko R, Silva E, Clayton L, Gardano L, Barrios-Rodiles M, Wrana J, Varelas X, Arbouzova NI, Shaw S, Saburi S, Matakatsu H, Blair S, McNeill H. 2009. Phosphorylation of the tumor suppressor fat is regulated by its ligand Dachsous and the kinase discs overgrown. Current Biology 19:1112-1117. doi: 10.1016/j.cub.2009.05.049.
58. Soubeyran P, Kowanetz K, Szymkiewicz I, Langdon WY, Dikic I. 2002. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416:183-187. doi: 10.1038/416183a.
59. Strutt H, Strutt D. 2002. Nonautonomous planar polarity patterning in Drosophila: dishevelled-independent functions of frizzled. Developmental Cell 3:851-863. doi: 10.1016/S1534-5807(02)00363-5.
60. Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U, Krek W. 1999. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nature Cell Biology 1:207-214. doi: 10.1038/12027.
61. Tapon N, Harvey KF. 2012. The Hippo pathway-from top to bottom and everything in between. Seminars in Cell & Developmental Biology 23:768-769. doi: 10.1016/j.semcdb.2012.08.007.
62. Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK. 2001. The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105:345-355. doi: 10.1016/S0092-8674(01)00332-4.
63. Thomas C, Strutt D. 2012. The roles of the cadherins Fat and Dachsous in planar polarity specification in Drosophila. Developmental Dynamics 241:27-39. doi: 10.1002/dvdy.22736.
64. Tyler DM, Li W, Zhuo N, Pellock B, Baker NE. 2007. Genes affecting cell competition in Drosophila. Genetics 175:643-657. doi: 10.1534/genetics.106.061929.
65. Venken KJ, Schulze KL, Haelterman NA, Pan H, He Y, Evans-Holm M, Carlson JW, Levis RW, Spradling AC, Hoskins RA, Bellen HJ. 2011. MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nature Methods 8:737-743. doi: 10.1038/nmeth.1662.
66. Villano JL, Katz FN. 1995. four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. Development 121:2767-2777.
67. Willecke M, Hamaratoglu F, Kango-Singh M, Udan R, Chen CL, Tao C, Zhang X, Halder G. 2006. The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Current Biology 16:2090-2100. doi: 10.1016/j.cub.2006.09.005.
68. Willecke M, Hamaratoglu F, Sansores-Garcia L, Tao C, Halder G. 2008. Boundaries of Dachsous Cadherin activity modulate the Hippo signaling pathway to induce cell proliferation. Proceedings of the National Academy of Sciences of USA 105:14897-14902. doi: 10.1073/pnas.0805201105.
69. Wu K, Fuchs SY, Chen A, Tan P, Gomez C, Ronai Z, Pan ZQ. 2000. The SCF(HOS/beta-TRCP)-ROC1 E3 ubiquitin ligase utilizes two distinct domains within CUL1 for substrate targeting and ubiquitin ligation. Molecular and Cellular Biology 20:1382-1393. doi: 10.1128/MCB.20.4.1382-1393.2000.
70. Xu T, Rubin GM. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117:1223-1237.
71. Yang CH, Axelrod JD, Simon MA. 2002. Regulation of Frizzled by fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108:675-688. doi: 10.1016/S0092-8674(02)00658-X.
72. Yen HC, Elledge SJ. 2008. Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 322:923-929. doi: 10.1126/science.1160462.
73. Zhang L, Ren F, Zhang Q, Chen Y, Wang B, Jiang J. 2008. The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Developmental Cell 14:377-387. doi: 10.1016/j.devcel.2008.01.006.
74. Zhao X, Yang CH, Simon MA. 2013. The Drosophila Cadherin Fat regulates tissue size and planar cell polarity through different domains. PLOS ONE 8:e62998. doi: 10.1371/journal.pone.0062998.