Actin remodelling factors control ciliogenesis by regulating YAP/TAZ activity and vesicle trafficking

Nature Communications

Volumn 6, Issue , 2015, Pages

  Kim, Jongshin ^a   Jo, Haiin ^a   Hong, Hyowon ^a   Kim, Min Hwan ^a   Kim, Jin Man ^a   Lee, June Koo ^a   Heo, Won Do ^a,b   Kim, Joon ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Institute for Basic Science   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; PROTEIN LIMK2; PROTEIN TESK1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TAZ; TRANSCRIPTION FACTOR YAP; UNCLASSIFIED DRUG; LIM KINASE; LIMK2 PROTEIN, HUMAN; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAZ PROTEIN, HUMAN; TESTIS-SPECIFIC PROTEIN KINASE 1; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; GENE EXPRESSION; SIGNALING;

ACTIN FILAMENT; ARTICLE; CELL CYCLE PROGRESSION; CILIOGENESIS; CONTROLLED STUDY; CYTOPLASM; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; REGULATORY MECHANISM; TRANSPORT VESICLE; CELL LINE; CLATHRIN-COATED VESICLE; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; HEK293 CELL LINE; METABOLISM; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BLOTTING, WESTERN; CELL LINE; CILIA; CLATHRIN-COATED VESICLES; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; LIM KINASES; MICROSCOPY, FLUORESCENCE; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84926642096     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7781     Document Type: Article

References (62)

1. Gerdes, J. M., Davis, E. E. & Katsanis, N. The vertebrate primary cilium in development, homeostasis, and disease. Cell 137, 32-45 (2009).
2. Goetz, S. C. & Anderson, K. V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331-344 (2010).
3. Kim, S. et al. Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat. Cell Biol. 13, 351-360 (2011).
4. Li, A. et al. Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat. Cell Biol. 13, 402-411 (2011).
5. Pugacheva, E. N., Jablonski, S. A., Hartman, T. R., Henske, E. P. & Golemis, E. A. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129, 1351-1363 (2007).
6. Rieder, C. L., Jensen, C. G. & Jensen, L. C. The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J. Ultrastruc. Res. 68, 173-185 (1979).
7. Santos, N. & Reiter, J. F. Building it up and taking it down: the regulation of vertebrate ciliogenesis. Dev. Dyn. 237, 1972-1981 (2008).
8. Tucker, R. W., Pardee, A. B. & Fujiwara, K. Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells. Cell 17, 527-535 (1979).
9. Mori, Y., Akedo, H., Tanigaki, Y., Tanaka, K. & Okada, M. Ciliogenesis in tissue-cultured cells by the increased density of cell population. Exp. Cell Res. 120, 435-439 (1979).
10. Huangfu, D. et al. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426, 83-87 (2003).
11. Ishikawa, H. & Marshall, W. F. Mechanobiology of Ciliogenesis. Bio Science 64, 1084-1091 (2014).
12. Pitaval, A., Tseng, Q., Bornens, M. & Théry, M. Cell shape and contractility regulate ciliogenesis in cell cycle-arrested cells. J. Cell Biol. 191, 303-312 (2010).
13. Kim, J. et al. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464, 1048-1051 (2010).
14. Bershteyn, M., Atwood, S. X., Woo, W.-M., Li, M. & Oro, A. E. MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev. Cell 19, 270-283 (2010).
15. Cao, J. et al. miR-129-3p controls cilia assembly by regulating CP110 and actin dynamics. Nat. Cell Biol. 14, 697-706 (2012).
16. Hernandez-Hernandez, V. et al. Bardet-Biedl syndrome proteins control the cilia length through regulation of actin polymerization. Hum. Mol. Genet. 22, 3858-3868 (2013).
17. Halder, G. & Johnson, R. L. Hippo signaling: growth control and beyond. Development 138, 9-22 (2011).
18. Zhao, B., Tumaneng, K. & Guan, K.-L. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13, 877-883 (2011).
19. Halder, G., Dupont, S. & Piccolo, S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13, 591-600 (2012).
20. Aragona, M. et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059 (2013).
21. Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011).
22. Habbig, S. et al. NPHP4, a cilia-associated protein, negatively regulates the Hippo pathway. J. Cell Biol. 193, 633-642 (2011).
23. Habbig, S. et al. The ciliopathy disease protein NPHP9 promotes nuclear delivery and activation of the oncogenic transcriptional regulator TAZ. Hum. Mol. Genet. 21, 5528-5538 (2012).
24. Kim, M., Kim, M., Lee, M.-S., Kim, C.-H. & Lim, D.-S. The MST1/2-SAV1 complex of the Hippo pathway promotes ciliogenesis. Nat. Commun. 5, 5370 (2014).
25. Knödler, A. et al. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl Acad. Sci. USA 107, 6346-6351 (2010).
26. Westlake, C. J. et al. Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc. Natl Acad. Sci. USA 108, 2759-2764 (2011).
27. Wada, K.-I., Itoga, K., Okano, T., Yonemura, S. & Sasaki, H. Hippo pathway regulation by cell morphology and stress fibers. Development 138, 3907-3914 (2011).
28. Zhao, B. et al. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 26, 54-68 (2012).
29. Choi, J. W. et al. LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50, 157-186 (2010).
30. Yu, F.-X. et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791 (2012).
31. Zhao, B. et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747-2761 (2007).
32. Zhao, B. et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962-1971 (2008).
33. von Gise, A. et al. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc. Natl Acad. Sci. USA 109, 2394-2399 (2012).
34. Lee, K. H. et al. Identification of a novel Wnt5a-CK1e-Dvl2-Plk1-mediated primary cilia disassembly pathway. EMBO J. 31, 3104-3117 (2012).
35. Inoko, A. et al. Trichoplein and Aurora A block aberrant primary cilia assembly in proliferating cells. J. Cell Biol. 197, 391-405 (2012).
36. Gerstein, M. B. et al. Architecture of the human regulatory network derived from ENCODE data. Nature 489, 91-100 (2012).
37. Mizuno, K. Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal. 25, 457-469 (2013).
38. Ross-Macdonald, P. et al. Identification of a nonkinase target mediating cytotoxicity of novel kinase inhibitors. Mol. Cancer Ther. 7, 3490-3498 (2008).
39. Piccolo, S., Dupont, S. & Cordenonsi, M. The biology of YAP/TAZ: Hippo signaling and beyond. Physiol. Rev. 94, 1287-1312 (2014).
40. Schmidt, K. N. et al. Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis. J. Cell Biol. 199, 1083-1101 (2012).
41. Ridley, A. J. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529 (2006).
42. Pan, J., You, Y., Huang, T. & Brody, S. L. RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1. J. Cell Sci. 120, 1868-1876 (2007).
43. Park, T. J., Haigo, S. L. & Wallingford, J. B. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nature Genet. 38, 303-311 (2006).
44. Park, T. J., Mitchell, B. J., Abitua, P. B., Kintner, C. & Wallingford, J. B. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nature Genet. 40, 871-879 (2008).
45. Adams, M. et al. A meckelin-filamin A interaction mediates ciliogenesis. Hum. Mol. Genet. 21, 1272-1286 (2012).
46. Hossain, Z. et al. Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1. Proc. Natl Acad. Sci. USA 104, 1631-1636 (2007).
47. Makita, R. et al. Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am. J. Physiol. Renal. Physiol. 294, F542-F553 (2008).
48. Tian, Y. et al. TAZ promotes PC2 degradation through a SCFb-Trcp E3 ligase complex. Mol. Cell Biol. 27, 6383-6395 (2007).
49. Yim, H., Sung, C. K., You, J., Tian, Y. & Benjamin, T. Nek1 and TAZ interact to maintain normal levels of polycystin 2. J. Am. Soc. Nephrol. 22, 832-837 (2011).
50. Kim, I. et al. Conditional mutation of Pkd2 causes cystogenesis and upregulates β-catenin. J. Am. Soc. Nephrol. 20, 2556-2569 (2009).
51. Shalom, O., Shalva, N., Altschuler, Y. & Motro, B. The mammalian Nek1 kinase is involved in primary cilium formation. FEBS Lett. 582, 1465-1470 (2008).
52. White, M. C. & Quarmby, L. M. The NIMA-family kinase, Nek1 affects the stability of centrosomes and ciliogenesis. BMC Cell Biol. 9, 29 (2008).
53. Evangelista, M. et al. Kinome siRNA screen identifies regulators of ciliogenesis and hedgehog signal transduction. Sci. Signal. 1, ra7 (2008).
54. Thiel, C. et al. NEK1 mutations cause short-rib polydactyly syndrome type majewski. Am. J. Hum. Genet. 88, 106-114 (2011).
55. Pollard, T. D. & Cooper, J. A. Actin, a central player in cell shape and movement. Science 326, 1208-1212 (2009).
56. Rottner, K., Hänisch, J. & Campellone, K. G. WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends. Cell. Biol. 20, 650-661 (2010).
57. Hattula, K. et al. Characterization of the Rab8-specific membrane traffic route linked to protrusion formation. J. Cell Sci. 119, 4866-4877 (2006).
58. Yoshizaki, H. et al. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 162, 223-232 (2003).
59. Ye, J. et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134 (2012).
60. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108 (2008).
61. Carpenter, A. E. et al. Cell Profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100 (2006).
62. Valcu, M. & Valcu, C.-M. Data transformation practices in biomedical sciences. Nat. Methods 8, 104-105 (2011).