Dynamic Remodeling of membrane composition drives cell cycle through primary cilia excision

Phua, Siew Cheng; Chiba, Shuhei; Suzuki, Masako; Su, Emily; Roberson, Elle C.; Pusapati, Ganesh V.; Schurmans, Stéphane; Setou, Mitsutoshi; Rohatgi, Rajat; Reiter, Jeremy F.; Ikegami, Koji; Inoue, Takanari

doi:10.1016/j.cell.2016.12.032

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Dynamic Remodeling of membrane composition drives cell cycle through primary cilia excision

Phua, Siew Cheng; Chiba, Shuhei; Suzuki, Masako et al.

2017 • In Cell, 168, p. 264-279

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/236869

DOI
10.1016/j.cell.2016.12.032

PubMed
28086093

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Inpp5e Cell 2017 2019.pdf

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Keywords :

primary cilia; Inpp5e; phosphoinositides

Abstract :

[en] The life cycle of a primary cilium begins in quiescence and ends prior to mitosis. In quiescent cells, the primary cilium insulates itself from contiguous dynamic membrane processes on the cell surface to function as a stable signaling apparatus. Here, we demonstrate that basal restriction of ciliary structure dynamics is established by the cilia-enriched phosphoinositide 5-phosphatase, Inpp5e. Growth induction displaces ciliary Inpp5e and accumulates phosphatidylinositol 4,5-bisphosphate in distal cilia. This change triggers otherwise-forbidden actin polymerization in primary cilia, which excises cilia tips in a process we call cilia decapitation. While cilia disassembly is traditionally thought to occur solely through resorption, we show that an acute loss of IFT-B through cilia decapitation precedes resorption. Finally, we propose that cilia decapitation induces mitogenic signaling and constitutes a molecular link between the cilia life cycle and cell-division cycle. This newly defined ciliary mechanism may find significance in cell proliferation control during normal development and cancer.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Phua, Siew Cheng

Chiba, Shuhei

Suzuki, Masako

Su, Emily

Roberson, Elle C.

Pusapati, Ganesh V.

Schurmans, Stéphane ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Biochimie métabolique vétérinaire

Setou, Mitsutoshi

Rohatgi, Rajat

Reiter, Jeremy F.

Ikegami, Koji

Inoue, Takanari

Language :

English

Title :

Dynamic Remodeling of membrane composition drives cell cycle through primary cilia excision

Publication date :

2017

Journal title :

Cell

ISSN :

0092-8674

eISSN :

1097-4172

Publisher :

Cell Press, United States - Massachusetts

Volume :

168

Pages :

264-279

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 14 June 2019

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104 (5 by ULiège)

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Scopus citations^®

230

Scopus citations^®
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217

OpenCitations

237

Bibliography

Basten, S.G., Giles, R.H., Functional aspects of primary cilia in signaling, cell cycle and tumorigenesis. Cilia, 2, 2013, 6.
Bergman, K., Goodenough, U.W., Goodenough, D.A., Jawitz, J., Martin, H., Gametic differentiation in Chlamydomonas reinhardtii. II. Flagellar membranes and the agglutination reaction. J. Cell Biol. 67 (1975), 606–622.
Bhogaraju, S., Cajanek, L., Fort, C., Blisnick, T., Weber, K., Taschner, M., Mizuno, N., Lamla, S., Bastin, P., Nigg, E.A., Lorentzen, E., Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science 341 (2013), 1009–1012.
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.
Boehlke, C., Kotsis, F., Patel, V., Braeg, S., Voelker, H., Bredt, S., Beyer, T., Janusch, H., Hamann, C., Gödel, M., et al. Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat. Cell Biol. 12 (2010), 1115–1122.
Breslow, D.K., Koslover, E.F., Seydel, F., Spakowitz, A.J., Nachury, M.V., An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier. J. Cell Biol. 203 (2013), 129–147.
Cao, M., Ning, J., Hernandez-Lara, C.I., Belzile, O., Wang, Q., Dutcher, S.K., Liu, Y., Snell, W.J., Uni-directional ciliary membrane protein trafficking by a cytoplasmic retrograde IFT motor and ciliary ectosome shedding. eLife, 4, 2015, e05242.
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.
Chaya, T., Omori, Y., Kuwahara, R., Furukawa, T., ICK is essential for cell type-specific ciliogenesis and the regulation of ciliary transport. EMBO J. 33 (2014), 1227–1242.
Christensen, S.T., Clement, C.A., Satir, P., Pedersen, L.B., Primary cilia and coordination of receptor tyrosine kinase (RTK) signalling. J. Pathol. 226 (2012), 172–184.
Das, R.M., Storey, K.G., Apical abscission alters cell polarity and dismantles the primary cilium during neurogenesis. Science 343 (2014), 200–204.
Dubreuil, V., Marzesco, A.M., Corbeil, D., Huttner, W.B., Wilsch-Bräuninger, M., Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J. Cell Biol. 176 (2007), 483–495.
Elias, J.E., Gygi, S.P., Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4 (2007), 207–214.
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.
Francis, S.S., Sfakianos, J., Lo, B., Mellman, I., A hierarchy of signals regulates entry of membrane proteins into the ciliary membrane domain in epithelial cells. J. Cell Biol. 193 (2011), 219–233.
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.
Han, Y.-G., Kim, H.J., Dlugosz, A.A., Ellison, D.W., Gilbertson, R.J., Alvarez-Buylla, A., Dual and opposing roles of primary cilia in medulloblastoma development. Nat. Med. 15 (2009), 1062–1065.
He, M., Subramanian, R., Bangs, F., Omelchenko, T., Liem, K.F., Kapoor, T.M., Anderson, K.V., The kinesin-4 protein Kif7 regulates mammalian Hedgehog signalling by organizing the cilium tip compartment. Nat. Cell Biol. 16 (2014), 663–672.
Hogan, M.C., Manganelli, L., Woollard, J.R., Masyuk, A.I., Masyuk, T.V., Tammachote, R., Huang, B.Q., Leontovich, A.A., Beito, T.G., Madden, B.J., et al. Characterization of PKD protein-positive exosome-like vesicles. J. Am. Soc. Nephrol. 20 (2009), 278–288.
Hui, C.C., Angers, S., Gli proteins in development and disease. Annu. Rev. Cell Dev. Biol. 27 (2011), 513–537.
Humbert, M.C., Weihbrecht, K., Searby, C.C., Li, Y., Pope, R.M., Sheffield, V.C., Seo, S., ARL13B, PDE6D, and CEP164 form a functional network for INPP5E ciliary targeting. Proc. Natl. Acad. Sci. USA 109 (2012), 19691–19696.
Humke, E.W., Dorn, K.V., Milenkovic, L., Scott, M.P., Rohatgi, R., The output of Hedgehog signaling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins. Genes Dev. 24 (2010), 670–682.
Inoki, K., Ouyang, H., Zhu, T., Lindvall, C., Wang, Y., Zhang, X., Yang, Q., Bennett, C., Harada, Y., Stankunas, K., et al. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126 (2006), 955–968.
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.
Käll, L., Canterbury, J.D., Weston, J., Noble, W.S., MacCoss, M.J., Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 4 (2007), 923–925.
Kim, S., Zaghloul, N.A., Bubenshchikova, E., Oh, E.C., Rankin, S., Katsanis, N., Obara, T., Tsiokas, L., Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat. Cell Biol. 13 (2011), 351–360.
Lancaster, M.A., Schroth, J., Gleeson, J.G., Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nat. Cell Biol. 13 (2011), 700–707.
Lin, Y.-C., Niewiadomski, P., Lin, B., Nakamura, H., Phua, S.C., Jiao, J., Levchenko, A., Inoue, T., Rohatgi, R., Inoue, T., Chemically inducible diffusion trap at cilia reveals molecular sieve-like barrier. Nat. Chem. Biol. 9 (2013), 437–443.
Mattila, P.K., Lappalainen, P., Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9 (2008), 446–454.
Monje, M., Mitra, S.S., Freret, M.E., Raveh, T.B., Kim, J., Masek, M., Attema, J.L., Li, G., Haddix, T., Edwards, M.S.B., et al. Hedgehog-responsive candidate cell of origin for diffuse intrinsic pontine glioma. Proc. Natl. Acad. Sci. USA 108 (2011), 4453–4458.
Nauli, S.M., Alenghat, F.J., Luo, Y., Williams, E., Vassilev, P., Li, X., Elia, A.E.H., Lu, W., Brown, E.M., Quinn, S.J., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33 (2003), 129–137.
Oki, T., Nishimura, K., Kitaura, J., Togami, K., Maehara, A., Izawa, K., Sakaue-Sawano, A., Niida, A., Miyano, S., Aburatani, H., et al. A novel cell-cycle-indicator, mVenus-p27K-, identifies quiescent cells and visualizes G0-G1 transition. Sci. Rep., 4, 2014, 4012.
Orhon, I., Dupont, N., Zaidan, M., Boitez, V., Burtin, M., Schmitt, A., Capiod, T., Viau, A., Beau, I., Kuehn, E.W., et al. Primary-cilium-dependent autophagy controls epithelial cell volume in response to fluid flow. Nat. Cell Biol. 18 (2016), 657–667.
Pan, J., Wang, Q., Snell, W.J., An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev. Cell 6 (2004), 445–451.
Paridaen, J.T.M.L., Wilsch-Bräuninger, M., Huttner, W.B., Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155 (2013), 333–344.
Phua, S.C., Lin, Y.C., Inoue, T., An intelligent nano-antenna: Primary cilium harnesses TRP channels to decode polymodal stimuli. Cell Calcium 58 (2015), 415–422.
Plotnikova, O.V., Golemis, E.A., Pugacheva, E.N., Cell cycle-dependent ciliogenesis and cancer. Cancer Res. 68 (2008), 2058–2061.
Plotnikova, O.V., Pugacheva, E.N., Golemis, E.A., Primary cilia and the cell cycle. Methods Cell Biol. 94 (2009), 137–160.
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.
Posor, Y., Eichhorn-Gruenig, M., Puchkov, D., Schöneberg, J., Ullrich, A., Lampe, A., Müller, R., Zarbakhsh, S., Gulluni, F., Hirsch, E., et al. Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499 (2013), 233–237.
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 (2007), 1351–1363.
Regl, G., Kasper, M., Schnidar, H., Eichberger, T., Neill, G.W., Ikram, M.S., Quinn, A.G., Philpott, M.P., Frischauf, A.-M., Aberger, F., The zinc-finger transcription factor GLI2 antagonizes contact inhibition and differentiation of human epidermal cells. Oncogene 23 (2004), 1263–1274.
Rohatgi, R., Milenkovic, L., Scott, M.P., Patched1 regulates hedgehog signaling at the primary cilium. Science 317 (2007), 372–376.
Roy, S., Ingham, P.W., Hedgehogs tryst with the cell cycle. J. Cell Sci. 115 (2002), 4393–4397.
Saarikangas, J., Zhao, H., Lappalainen, P., Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol. Rev. 90 (2010), 259–289.
Sasaki, H., Hui, C., Nakafuku, M., Kondoh, H., A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124 (1997), 1313–1322.
Singla, V., Reiter, J.F., The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313 (2006), 629–633.
Stamataki, D., Ulloa, F., Tsoni, S.V., Mynett, A., Briscoe, J., A gradient of Gli activity mediates graded Sonic Hedgehog signaling in the neural tube. Genes Dev. 19 (2005), 626–641.
Suh, B.C., Inoue, T., Meyer, T., Hille, B., Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science 314 (2006), 1454–1457.
Susaki, E., Nakayama, K., Nakayama, K.I., Cyclin D2 translocates p27 out of the nucleus and promotes its degradation at the G0-G1 transition. Mol. Cell. Biol. 27 (2007), 4626–4640.
Van Troys, M., Dewitte, D., Goethals, M., Carlier, M.F., Vandekerckhove, J., Ampe, C., The actin binding site of thymosin beta 4 mapped by mutational analysis. EMBO J. 15 (1996), 201–210.
Wang, Y., Ding, Q., Yen, C.J., Xia, W., Izzo, J.G., Lang, J.Y., Li, C.W., Hsu, J.L., Miller, S.A., Wang, X., et al. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 21 (2012), 374–387.
Wang, W.-J., Tay, H.G., Soni, R., Perumal, G.S., Goll, M.G., Macaluso, F.P., Asara, J.M., Amack, J.D., Tsou, M.-F.B., CEP162 is an axoneme-recognition protein promoting ciliary transition zone assembly at the cilia base. Nat. Cell Biol. 15 (2013), 591–601.
Wang, J., Silva, M., Haas, L.A., Morsci, N.S., Nguyen, K.C.Q., Hall, D.H., Barr, M.M., C. elegans ciliated sensory neurons release extracellular vesicles that function in animal communication. Curr. Biol. 24 (2014), 519–525.
Wang, J., Kaletsky, R., Silva, M., Williams, A., Haas, L.A., Androwski, R.J., Landis, J.N., Patrick, C., Rashid, A., Santiago-Martinez, D., et al. Cell-Specific Transcriptional Profiling of Ciliated Sensory Neurons Reveals Regulators of Behavior and Extracellular Vesicle Biogenesis. Curr. Biol. 25 (2015), 3232–3238.
Wong, S.Y., Seol, A.D., So, P.-L., Ermilov, A.N., Bichakjian, C.K., Epstein, E.H. Jr., Dlugosz, A.A., Reiter, J.F., Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat. Med. 15 (2009), 1055–1061.
Wood, C.R., Rosenbaum, J.L., Ciliary ectosomes: transmissions from the cell's antenna. Trends Cell Biol. 25 (2015), 276–285.
Wood, C.R., Huang, K., Diener, D.R., Rosenbaum, J.L., The cilium secretes bioactive ectosomes. Curr. Biol. 23 (2013), 906–911.
Yarar, D., Waterman-Storer, C.M., Schmid, S.L., SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell 13 (2007), 43–56.
Yeh, C., Li, A., Chuang, J.Z., Saito, M., Cáceres, A., Sung, C.H., IGF-1 activates a cilium-localized noncanonical Gβγ signaling pathway that regulates cell-cycle progression. Dev. Cell 26 (2013), 358–368.
Yoon, J.W., Kita, Y., Frank, D.J., Majewski, R.R., Konicek, B.A., Nobrega, M.A., Jacob, H., Walterhouse, D., Iannaccone, P., Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J. Biol. Chem. 277 (2002), 5548–5555.