Ciliary Phosphoinositide Regulates Ciliary Protein Trafficking in Drosophila

Cell Reports

Volumn 13, Issue 12, 2015, Pages 2808-2816

  Park, Jina ^a   Lee, Nayoung ^a   Kavoussi, Adriana ^b   Seo, Jeong Taeg ^a   Kim, Chul Hoon ^b   Moon, Seok Jun ^a  

^a Yonsei University College of Dentistry   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL;

ANIMAL; CELL MOTION; CILIUM; DROSOPHILA; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CILIA; DROSOPHILA; PHOSPHATIDYLINOSITOLS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84979975362     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.12.009     Document Type: Article

References (42)

1. Bae, Y.K., Kim, E., L'hernault, S.W., Barr, M.M., The CIL-1 PI 5-phosphatase localizes TRP Polycystins to cilia and activates sperm in C. elegans. Curr. Biol. 19 (2009), 1599–1607.
2. Belzile, O., Hernandez-Lara, C.I., Wang, Q., Snell, W.J., Regulated membrane protein entry into flagella is facilitated by cytoplasmic microtubules and does not require IFT. Curr. Biol. 23 (2013), 1460–1465.
3. Berbari, N.F., Lewis, J.S., Bishop, G.A., Askwith, C.C., Mykytyn, K., Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc. Natl. Acad. Sci. USA 105 (2008), 4242–4246.
4. Bielas, S.L., Silhavy, J.L., Brancati, F., Kisseleva, M.V., Al-Gazali, L., Sztriha, L., Bayoumi, R.A., Zaki, M.S., Abdel-Aleem, A., Rosti, R.O., et al. Mutations in INPP5E, encoding inositol polyphosphate-5-phosphatase E, link phosphatidyl inositol signaling to the ciliopathies. Nat. Genet. 41 (2009), 1032–1036.
5. Chávez, M., Ena, S., Van Sande, J., de Kerchove d'Exaerde, A., Schurmans, S., Schiffmann, S.N., Modulation of Ciliary Phosphoinositide Content Regulates Trafficking and Sonic Hedgehog Signaling Output. Dev. Cell 34 (2015), 338–350.
6. Chih, B., Liu, P., Chinn, Y., Chalouni, C., Komuves, L.G., Hass, P.E., Sandoval, W., Peterson, A.S., A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat. Cell Biol. 14 (2012), 61–72.
7. Colbert, H.A., Smith, T.L., Bargmann, C.I., OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17 (1997), 8259–8269.
8. Conduit, S.E., Dyson, J.M., Mitchell, C.A., Inositol polyphosphate 5-phosphatases; new players in the regulation of cilia and ciliopathies. FEBS Lett. 586 (2012), 2846–2857.
9. Cook, B., Hardy, R.W., McConnaughey, W.B., Zuker, C.S., Preserving cell shape under environmental stress. Nature 452 (2008), 361–364.
10. Corbit, K.C., Aanstad, P., Singla, V., Norman, A.R., Stainier, D.Y., Reiter, J.F., Vertebrate Smoothened functions at the primary cilium. Nature 437 (2005), 1018–1021.
11. Crouse, J.A., Lopes, V.S., Sanagustin, J.T., Keady, B.T., Williams, D.S., Pazour, G.J., Distinct functions for IFT140 and IFT20 in opsin transport. Cytoskeleton (Hoboken) 71 (2014), 302–310.
12. Deretic, D., Williams, A.H., Ransom, N., Morel, V., Hargrave, P.A., Arendt, A., Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc. Natl. Acad. Sci. USA 102 (2005), 3301–3306.
13. Drummond, I.A., Cilia functions in development. Curr. Opin. Cell Biol. 24 (2012), 24–30.
14. Eberl, D.F., Hardy, R.W., Kernan, M.J., Genetically similar transduction mechanisms for touch and hearing in Drosophila. J. Neurosci. 20 (2000), 5981–5988.
15. Ezratty, E.J., Stokes, N., Chai, S., Shah, A.S., Williams, S.E., Fuchs, E., A role for the primary cilium in Notch signaling and epidermal differentiation during skin development. Cell 145 (2011), 1129–1141.
16. Fliegauf, M., Benzing, T., Omran, H., When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8 (2007), 880–893.
17. Garcia-Gonzalo, F.R., Phua, S.C., Roberson, E.C., Garcia, G. 3rd, Abedin, M., Schurmans, S., Inoue, T., Reiter, J.F., Phosphoinositides Regulate Ciliary Protein Trafficking to Modulate Hedgehog Signaling. Dev. Cell 34 (2015), 400–409.
18. Gong, Z., Son, W., Chung, Y.D., Kim, J., Shin, D.W., McClung, C.A., Lee, Y., Lee, H.W., Chang, D.J., Kaang, B.K., et al. Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J. Neurosci. 24 (2004), 9059–9066.
19. Gratz, S.J., Cummings, A.M., Nguyen, J.N., Hamm, D.C., Donohue, L.K., Harrison, M.M., Wildonger, J., O'Connor-Giles, K.M., Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194 (2013), 1029–1035.
20. Green, J.S., Parfrey, P.S., Harnett, J.D., Farid, N.R., Cramer, B.C., Johnson, G., Heath, O., McManamon, P.J., O'Leary, E., Pryse-Phillips, W., The cardinal manifestations of Bardet-Biedl syndrome, a form of Laurence-Moon-Biedl syndrome. N. Engl. J. Med. 321 (1989), 1002–1009.
21. Han, Y.G., Kwok, B.H., Kernan, M.J., Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr. Biol. 13 (2003), 1679–1686.
22. Hassan, B.A., Prokopenko, S.N., Breuer, S., Zhang, B., Paululat, A., Bellen, H.J., skittles, a Drosophila phosphatidylinositol 4-phosphate 5-kinase, is required for cell viability, germline development and bristle morphology, but not for neurotransmitter release. Genetics 150 (1998), 1527–1537.
23. Hu, Q., Milenkovic, L., Jin, H., Scott, M.P., Nachury, M.V., Spiliotis, E.T., Nelson, W.J., A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329 (2010), 436–439.
24. Jacoby, M., Cox, J.J., Gayral, S., Hampshire, D.J., Ayub, M., Blockmans, M., Pernot, E., Kisseleva, M.V., Compère, P., Schiffmann, S.N., et al. INPP5E mutations cause primary cilium signaling defects, ciliary instability and ciliopathies in human and mouse. Nat. Genet. 41 (2009), 1027–1031.
25. Keady, B.T., Le, Y.Z., Pazour, G.J., IFT20 is required for opsin trafficking and photoreceptor outer segment development. Mol. Biol. Cell 22 (2011), 921–930.
26. Kim, J., Chung, Y.D., Park, D.Y., Choi, S., Shin, D.W., Soh, H., Lee, H.W., Son, W., Yim, J., Park, C.S., et al. A TRPV family ion channel required for hearing in Drosophila. Nature 424 (2003), 81–84.
27. Lee, E., Sivan-Loukianova, E., Eberl, D.F., Kernan, M.J., An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr. Biol. 18 (2008), 1899–1906.
28. Lee, J., Moon, S., Cha, Y., Chung, Y.D., Drosophila TRPN(=NOMPC) channel localizes to the distal end of mechanosensory cilia. PLoS ONE, 5, 2010, e11012.
29. Lehnert, B.P., Baker, A.E., Gaudry, Q., Chiang, A.S., Wilson, R.I., Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. Neuron 77 (2013), 115–128.
30. Liu, Q., Zhou, J., Daiger, S.P., Farber, D.B., Heckenlively, J.R., Smith, J.E., Sullivan, L.S., Zuo, J., Milam, A.H., Pierce, E.A., Identification and subcellular localization of the RP1 protein in human and mouse photoreceptors. Invest. Ophthalmol. Vis. Sci. 43 (2002), 22–32.
31. Mukhopadhyay, S., Wen, X., Chih, B., Nelson, C.D., Lane, W.S., Scales, S.J., Jackson, P.K., TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev. 24 (2010), 2180–2193.
32. Nachury, M.V., Loktev, A.V., Zhang, Q., Westlake, C.J., Peränen, J., Merdes, A., Slusarski, D.C., Scheller, R.H., Bazan, J.F., Sheffield, V.C., Jackson, P.K., A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129 (2007), 1201–1213.
33. Nachury, M.V., Seeley, E.S., Jin, H., Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier?. Annu. Rev. Cell Dev. Biol. 26 (2010), 59–87.
34. Park, J., Lee, J., Shim, J., Han, W., Lee, J., Bae, Y.C., Chung, Y.D., Kim, C.H., Moon, S.J., dTULP, the Drosophila melanogaster homolog of tubby, regulates transient receptor potential channel localization in cilia. PLoS Genet., 9, 2013, e1003814.
35. Pazour, G.J., Dickert, B.L., Vucica, Y., Seeley, E.S., Rosenbaum, J.L., Witman, G.B., Cole, D.G., Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151 (2000), 709–718.
36. Plotnikova, O.V., Seo, S., Cottle, D.L., Conduit, S., Hakim, S., Dyson, J.M., Mitchell, C.A., Smyth, I.M., INPP5E interacts with AURKA, linking phosphoinositide signaling to primary cilium stability. J. Cell Sci. 128 (2015), 364–372.
37. Rohatgi, R., Milenkovic, L., Scott, M.P., Patched1 regulates hedgehog signaling at the primary cilium. Science 317 (2007), 372–376.
38. Rosenbaum, J.L., Witman, G.B., Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3 (2002), 813–825.
39. Santagata, S., Boggon, T.J., Baird, C.L., Gomez, C.A., Zhao, J., Shan, W.S., Myszka, D.G., Shapiro, L., G-protein signaling through tubby proteins. Science 292 (2001), 2041–2050.
40. Valente, E.M., Silhavy, J.L., Brancati, F., Barrano, G., Krishnaswami, S.R., Castori, M., Lancaster, M.A., Boltshauser, E., Boccone, L., Al-Gazali, L., et al., International Joubert Syndrome Related Disorders Study Group. Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome. Nat. Genet. 38 (2006), 623–625.
41. Wang, J., Morita, Y., Mazelova, J., Deretic, D., The Arf GAP ASAP1 provides a platform to regulate Arf4- and Rab11-Rab8-mediated ciliary receptor targeting. EMBO J. 31 (2012), 4057–4071.
42. Williams, C.L., Li, C., Kida, K., Inglis, P.N., Mohan, S., Semenec, L., Bialas, N.J., Stupay, R.M., Chen, N., Blacque, O.E., et al. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J. Cell Biol. 192 (2011), 1023–1041.