The connections of Wnt pathway components with cell cycle and centrosome: side effects or a hidden logic?
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
166533
Swiss National Science Foundation - Switzerland
PubMed
28741966
PubMed Central
PMC6047740
DOI
10.1080/10409238.2017.1350135
Knihovny.cz E-zdroje
- Klíčová slova
- Wnt, cell cycle, centrosome, cilium, crosstalk, planar cell polarity,
- MeSH
- buněčný cyklus * MeSH
- centrozom metabolismus MeSH
- lidé MeSH
- mezibuněčná komunikace MeSH
- polarita buněk MeSH
- signální dráha Wnt * MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Wnt signaling cascade has developed together with multicellularity to orchestrate the development and homeostasis of complex structures. Wnt pathway components - such as β-catenin, Dishevelled (DVL), Lrp6, and Axin-- are often dedicated proteins that emerged in evolution together with the Wnt signaling cascade and are believed to function primarily in the Wnt cascade. It is interesting to see that in recent literature many of these proteins are connected with cellular functions that are more ancient and not limited to multicellular organisms - such as cell cycle regulation, centrosome biology, or cell division. In this review, we summarize the recent literature describing this crosstalk. Specifically, we attempt to find the answers to the following questions: Is the response to Wnt ligands regulated by the cell cycle? Is the centrosome and/or cilium required to activate the Wnt pathway? How do Wnt pathway components regulate the centrosomal cycle and cilia formation and function? We critically review the evidence that describes how these connections are regulated and how they help to integrate cell-to-cell communication with the cell and the centrosomal cycle in order to achieve a fine-tuned, physiological response.
c Department of Histology and Embryology Faculty of Medicine Masaryk University Brno Czech Republic
Department of Experimental Biology Faculty of Science Masaryk University Brno Czech Republic
Zobrazit více v PubMed
Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 1982;31:99–109. PubMed
Nusslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980;287:795–801. PubMed
Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet. 1998;19:379–83. PubMed
ten Berge D, Kurek D, Blauwkamp T, Koole W, Maas A, Eroglu E, Siu RK, Nusse R. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nature cell biology. 2011;13:1070–5. PubMed PMC
Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 1999;398:422–6. PubMed
He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science. 1998;281:1509–12. PubMed
Schulte G, Bryja V. The Frizzled family of unconventional G-protein-coupled receptors. Trends Pharmacol Sci. 2007;28:518–25. PubMed
Tamai K, Zeng X, Liu C, Zhang X, Harada Y, Chang Z, He X. A mechanism for Wnt coreceptor activation. Mol Cell. 2004;13:149–56. PubMed
Schwarz-Romond T, Fiedler M, Shibata N, Butler PJ, Kikuchi A, Higuchi Y, Bienz M. The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat Struct Mol Biol. 2007;14:484–92. PubMed
Fagotto F, Jho E, Zeng L, Kurth T, Joos T, Kaufmann C, Costantini F. Domains of axin involved in protein-protein interactions, Wnt pathway inhibition, and intracellular localization. The Journal of cell biology. 1999;145:741–56. PubMed PMC
Li L, Yuan H, Weaver CD, Mao J, Farr GH, 3rd, Sussman DJ, Jonkers J, Kimelman D, Wu D. Axin and Frat1 interact with dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1. Embo J. 1999;18:4233–40. PubMed PMC
Smalley MJ, Sara E, Paterson H, Naylor S, Cook D, Jayatilake H, Fryer LG, Hutchinson L, Fry MJ, Dale TC. Interaction of axin and Dvl-2 proteins regulates Dvl-2-stimulated TCF-dependent transcription. Embo J. 1999;18:2823–35. PubMed PMC
Wallingford JB, Habas R. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development. 2005;132:4421–36. PubMed
Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes & development. 1998;12:2610–22. PubMed PMC
Gammons MV, Rutherford TJ, Steinhart Z, Angers S, Bienz M. Essential role of the Dishevelled DEP domain in a Wnt-dependent human-cell-based complementation assay. Journal of cell science. 2016;129:3892–902. PubMed PMC
Paclikova P, Bernatik O, Radaszkiewicz TW, Bryja V. N-terminal part of Dishevelled DEP domain is required for Wnt/beta-catenin signaling in mammalian cells. Molecular and Cellular Biology. 2017 PubMed PMC
Pan WJ, Pang SZ, Huang T, Guo HY, Wu D, Li L. Characterization of function of three domains in dishevelled-1: DEP domain is responsible for membrane translocation of dishevelled-1. Cell Res. 2004;14:324–30. PubMed
Tauriello DV, Jordens I, Kirchner K, Slootstra JW, Kruitwagen T, Bouwman BA, Noutsou M, Rudiger SG, Schwamborn K, Schambony A, Maurice MM. Wnt/beta-catenin signaling requires interaction of the Dishevelled DEP domain and C terminus with a discontinuous motif in Frizzled. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:E812–20. PubMed PMC
Bryja V, Bernatik O. Dishevelled at the crossroad of pathways. In: Hoppler S, Moon RT, editors. Wnt signaling in Development and Disease: Molecular Mechanisms and Biological Functions. Willey Publishers; 2014.
Bernatik O, Ganji RS, Dijksterhuis JP, Konik P, Cervenka I, Polonio T, Krejci P, Schulte G, Bryja V. Sequential activation and inactivation of Dishevelled in the Wnt/beta-catenin pathway by casein kinases. The Journal of biological chemistry. 2011;286:10396–410. PubMed PMC
Bernatik O, Sedova K, Schille C, Ganji RS, Cervenka I, Trantirek L, Schambony A, Zdrahal Z, Bryja V. Functional analysis of dishevelled-3 phosphorylation identifies distinct mechanisms driven by casein kinase 1 and frizzled5. The Journal of biological chemistry. 2014;289:23520–33. PubMed PMC
Bienz M. Signalosome assembly by domains undergoing dynamic head-to-tail polymerization. Trends Biochem Sci. 2014;39:487–95. PubMed
Zeng X, Huang H, Tamai K, Zhang X, Harada Y, Yokota C, Almeida K, Wang J, Doble B, Woodgett J, Wynshaw-Boris A, et al. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development. 2008;135:367–75. PubMed PMC
Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, Niehrs C. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science. 2007;316:1619–22. PubMed
Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J. 1998;17:1371–84. PubMed PMC
Kishida S, Yamamoto H, Ikeda S, Kishida M, Sakamoto I, Koyama S, Kikuchi A. Axin, a negative regulator of the wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of beta-catenin. The Journal of biological chemistry. 1998;273:10823–6. PubMed
Sakanaka C, Weiss JB, Williams LT. Bridging of beta-catenin and glycogen synthase kinase-3beta by axin and inhibition of beta-catenin-mediated transcription. Proceedings of the National Academy of Sciences of the United States of America. 1998;95:3020–3. PubMed PMC
Henderson BR, Fagotto F. The ins and outs of APC and beta-catenin nuclear transport. EMBO Rep. 2002;3:834–9. PubMed PMC
Stadeli R, Hoffmans R, Basler K. Transcription under the control of nuclear Arm/beta-catenin. Curr Biol. 2006;16:R378–85. PubMed
Daniels DL, Weis WI. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol. 2005;12:364–71. PubMed
Axelrod JD. Progress and challenges in understanding planar cell polarity signaling. Semin Cell Dev Biol. 2009;20:964–71. PubMed
Zallen JA. Planar polarity and tissue morphogenesis. Cell. 2007;129:1051–63. PubMed
Habas R, Kato Y, He X. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daaml. Cell. 2001;107:843–54. PubMed
Butler MT, Wallingford JB. Planar cell polarity in development and disease. Nature reviews Molecular cell biology. 2017 PubMed PMC
Kohn AD, Moon RT. Wnt and calcium signaling: beta-catenin-independent pathways. Cell calcium. 2005;38:439–46. PubMed
Slusarski DC, Pelegri F. Calcium signaling in vertebrate embryonic patterning and morphogenesis. Developmental biology. 2007;307:1–13. PubMed PMC
Nurse P. Regulation of the eukaryotic cell cycle. European journal of cancer. 1997;33:1002–4. PubMed
Khodjakov A, Rieder CL. The nature of cell-cycle checkpoints: facts and fallacies. Journal of biology. 2009;8:88. PubMed PMC
Boveri T. Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris. Journal of cell science. 2008;121(Suppl 1):1–84. PubMed
Klotz C, Dabauvalle MC, Paintrand M, Weber T, Bornens M, Karsenti E. Parthenogenesis in Xenopus eggs requires centrosomal integrity. The Journal of cell biology. 1990;110:405–15. PubMed PMC
Picard A, Karsenti E, Dabauvalle MC, Doree M. Release of mature starfish oocytes from interphase arrest by microinjection of human centrosomes. Nature. 1987;327:170–2. PubMed
Bornens M, Gonczy P. Centrosomes back in the limelight. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 2014;369 PubMed PMC
Kalab P, Heald R. The RanGTP gradient - a GPS for the mitotic spindle. Journal of cell science. 2008;121:1577–86. PubMed PMC
Louvet-Vallee S, Vinot S, Maro B. Mitotic spindles and cleavage planes are oriented randomly in the two-cell mouse embryo. Curr Biol. 2005;15:464–9. PubMed
Khodjakov A, Rieder CL. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. The Journal of cell biology. 2001;153:237–42. PubMed PMC
Piel M, Nordberg J, Euteneuer U, Bornens M. Centrosome-dependent exit of cytokinesis in animal cells. Science. 2001;291:1550–3. PubMed
Oliferenko S, Chew TG, Balasubramanian MK. Positioning cytokinesis. Genes & development. 2009;23:660–74. PubMed
Doe CQ. Neural stem cells: balancing self-renewal with differentiation. Development. 2008;135:1575–87. PubMed
Knoblich JA. Mechanisms of asymmetric stem cell division. Cell. 2008;132:583–97. PubMed
Lancaster MA, Knoblich JA. Spindle orientation in mammalian cerebral cortical development. Current opinion in neurobiology. 2012;22:737–46. PubMed PMC
Arquint C, Gabryjonczyk AM, Nigg EA. Centrosomes as signalling centres. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 2014;369 PubMed PMC
Jackman M, Lindon C, Nigg EA, Pines J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nature cell biology. 2003;5:143–8. PubMed
Wakefield JG, Huang JY, Raff JW. Centrosomes have a role in regulating the destruction of cyclin B in early Drosophila embryos. Curr Biol. 2000;10:1367–70. PubMed
Luders J, Stearns T. Microtubule-organizing centres: a re-evaluation. Nature reviews Molecular cell biology. 2007;8:161–7. PubMed
Mennella V, Agard DA, Huang B, Pelletier L. Amorphous no more: subdiffraction view of the pericentriolar material architecture. Trends in cell biology. 2014;24:188–97. PubMed PMC
Conduit PT, Wainman A, Raff JW. Centrosome function and assembly in animal cells. Nature reviews Molecular cell biology. 2015;16:611–24. PubMed
Tollenaere MA, Mailand N, Bekker-Jensen S. Centriolar satellites: key mediators of centrosome functions. Cellular and molecular life sciences : CMLS. 2014 PubMed PMC
Bornens M, Azimzadeh J. Origin and evolution of the centrosome. Advances in experimental medicine and biology. 2007;607:119–29. PubMed
Bornens M. The centrosome in cells and organisms. Science. 2012;335:422–6. PubMed
Cunha-Ferreira I, Bento I, Bettencourt-Dias M. From zero to many: control of centriole number in development and disease. Traffic. 2009;10:482–98. PubMed
Holland AJ, Fachinetti D, Zhu Q, Bauer M, Verma IM, Nigg EA, Cleveland DW. The autoregulated instability of Polo-like kinase 4 limits centrosome duplication to once per cell cycle. Genes & development. 2012;26:2684–9. PubMed PMC
Fava LL, Schuler F, Sladky V, Haschka MD, Soratroi C, Eiterer L, Demetz E, Weiss G, Geley S, Nigg EA, Villunger A. The PIDDosome activates p53 in response to supernumerary centrosomes. Genes & development. 2017;31:34–45. PubMed PMC
Wong YL, Anzola JV, Davis RL, Yoon M, Motamedi A, Kroll A, Seo CP, Hsia JE, Kim SK, Mitchell JW, Mitchell BJ, et al. Reversible centriole depletion with an inhibitor of Polo-like kinase 4. Science. 2015;348:1155–60. PubMed PMC
Bazzi H, Anderson KV. Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo. Proceedings of the National Academy of Sciences of the United States of America. 2014;111:E1491–500. PubMed PMC
Gonczy P. Centrosomes and cancer: revisiting a long-standing relationship. Nature reviews Cancer. 2015;15:639–52. PubMed
Nigg EA, Cajanek L, Arquint C. The centrosome duplication cycle in health and disease. FEBS letters. 2014;588:2366–72. PubMed
Godinho SA, Pellman D. Causes and consequences of centrosome abnormalities in cancer. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 2014;369 PubMed PMC
Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA. Centrosomes and cilia in human disease. Trends Genet. 2011;27:307–15. PubMed PMC
Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature. 2009;460:278–82. PubMed PMC
Levine MS, Bakker B, Boeckx B, Moyett J, Lu J, Vitre B, Spierings DC, Lansdorp PM, Cleveland DW, Lambrechts D, Foijer F, et al. Centrosome Amplification Is Sufficient to Promote Spontaneous Tumorigenesis in Mammals. Developmental cell. 2017 PubMed PMC
Serein O, Larsimont JC, Karambelas AE, Marthiens V, Moers V, Boeckx B, Le Mercier M, Lambrechts D, Basto R, Blanpain C. Transient PLK4 overexpression accelerates tumorigenesis in p53-deficient epidermis. Nature cell biology. 2016;18:100–10. PubMed
Basto R, Brunk K, Vinadogrova T, Peel N, Franz A, Khodjakov A, Raff JW. Centrosome amplification can initiate tumorigenesis in flies. Cell. 2008;133:1032–42. PubMed PMC
Marthiens V, Rujano MA, Pennetier C, Tessier S, Paul-Gilloteaux P, Basto R. Centrosome amplification causes microcephaly. Nature cell biology. 2013;15:731–40. PubMed
Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA. Centrosomes and cilia in human disease. Trends in genetics : TIG. 2011;27:307–15. PubMed PMC
Goetz SC, Anderson KV. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet. 2010;11:331–44. PubMed PMC
Singla V, Reiter JF. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science. 2006;313:629–33. PubMed
Yoshiba S, Hamada H. Roles of cilia, fluid flow, and Ca2+ signaling in breaking of left-right symmetry. Trends in genetics : TIG. 2014;30:10–7. PubMed
Mitchison HM, Valente EM. Motile and non-motile cilia in human pathology: from function to phenotypes. The Journal of pathology. 2017;241:294–309. PubMed
Braun DA, Hildebrandt F. Ciliopathies. Cold Spring Harbor perspectives in biology. 2017;9 PubMed PMC
Brooks ER, Wallingford JB. Multiciliated cells. Current biology : CB. 2014;24:R973–82. PubMed PMC
Meunier A, Azimzadeh J. Multiciliated Cells in Animals. Cold Spring Harbor perspectives in biology. 2016;8 PubMed PMC
Sorokin S. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. The Journal of cell biology. 1962;15:363–77. PubMed PMC
Schmidt TI, Kleylein-Sohn J, Westendorf J, Le Clech M, Lavoie SB, Stierhof YD, Nigg EA. Control of centriole length by CPAP and CP110. Current biology : CB. 2009;19:1005–11. PubMed
Spektor A, Tsang WY, Khoo D, Dynlacht BD. Cep97 and CP110 suppress a cilia assembly program. Cell. 2007;130:678–90. PubMed
Goetz SC, Liem KF, Jr, Anderson KV. The spinocerebellar ataxia-associated gene Tau tubulin kinase 2 controls the initiation of ciliogenesis. Cell. 2012;151:847–58. PubMed PMC
Cajanek L, Nigg EA. Cepl64 triggers ciliogenesis by recruiting Tau tubulin kinase 2 to the mother centriole. Proceedings of the National Academy of Sciences of the United States of America. 2014;111:E2841–50. PubMed PMC
Lu Q, Insinna C, Ott C, Stauffer J, Pintado PA, Rahajeng J, Baxa U, Walia V, Cuenca A, Hwang YS, Daar IO, et al. Early steps in primary cilium assembly require EHDl/EHD3-dependent ciliary vesicle formation. Nature cell biology. 2015 PubMed
Rosenbaum JL, Witman GB. Intraflagellar transport. Nature reviews Molecular cell biology. 2002;3:813–25. PubMed
Bhogaraju S, Cajanek L, Fort C, Blisnick T, Weber K, Taschner M, Mizuno N, Lamla S, Bastin P, Nigg EA, Lorentzen E. Molecular Basis of Tubulin Transport Within the Cilium by IFT74 and IFT81. Science. 2013;341:1009–12. PubMed PMC
Sanchez I, Dynlacht BD. Cilium assembly and disassembly. Nature cell biology. 2016;18:711–7. PubMed PMC
Nachury MV, Seeley ES. The perennial organelle: assembly and disassembly of the primary cilium. Journal of cell science. 2010;123:511–18. PubMed PMC
Jakobsen L, Vanselow K, Skogs M, Toyoda Y, Lundberg E, Poser I, Falkenby LG, Bennetzen M, Westendorf J, Nigg EA, Uhlen M, et al. Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J. 2011;30:1520–35. PubMed PMC
Gupta GD, Coyaud E, Goncalves J, Mojarad BA, Liu Y, Wu Q, Gheiratmand L, Comartin D, Tkach JM, Cheung SW, Bashkurov M, et al. A Dynamic Protein Interaction Landscape of the Human Centrosome-Cilium Interface. Cell. 2015;163:1484–99. PubMed PMC
May-Simera HL, Kelley MW. Cilia, Wnt signaling, and the cytoskeleton. Cilia. 2012;1:7. PubMed PMC
Wallingford JB, Mitchell B. Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes & development. 2011;25:201–13. PubMed PMC
Otto EA, Schermer B, Obara T, O'Toole JF, Hiller KS, Mueller AM, Ruf RG, Hoefele J, Beekmann F, Landau D, Foreman JW, et al. Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat Genet. 2003;34:413–20. PubMed PMC
Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Kronig C, Schermer B, Benzing T, Cabello OA, Jenny A, Mlodzik M, et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet. 2005;37:537–43. PubMed PMC
Veland IR, Montjean R, Eley L, Pedersen LB, Schwab A, Goodship J, Kristiansen K, Pedersen SF, Saunier S, Christensen ST. Inversin/Nephrocystin-2 is required for fibroblast polarity and directional cell migration. PLoS One. 2013;8:e60193. PubMed PMC
Sugiyama N, Tsukiyama T, Yamaguchi TP, Yokoyama T. The canonical Wnt signaling pathway is not involved in renal cyst development in the kidneys of inv mutant mice. Kidney international. 2011;79:957–65. PubMed PMC
Gerdes JM, Liu Y, Zaghloul NA, Leitch CC, Lawson SS, Kato M, Beachy PA, Beales PL, DeMartino GN, Fisher S, Badano JL, et al. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat Genet. 2007;39:1350–60. PubMed
Corbit KC, Shyer AE, Dowdle WE, Gaulden J, Singla V, Chen MH, Chuang PT, Reiter JF. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nature cell biology. 2008;10:70–6. PubMed
McDermott KM, Liu BY, Tlsty TD, Pazour GJ. Primary cilia regulate branching morphogenesis during mammary gland development. Curr Biol. 2010;20:731–7. PubMed PMC
Lin F, Hiesberger T, Cordes K, Sinclair AM, Goldstein LS, Somlo S, Igarashi P. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proceedings of the National Academy of Sciences of the United States of America. 2003;100:5286–91. PubMed PMC
Liu B, Chen S, Cheng D, Jing W, Helms JA. Primary cilia integrate hedgehog and Wnt signaling during tooth development. Journal of dental research. 2014;93:475–82. PubMed PMC
Ocbina PJ, Tuson M, Anderson KV. Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS One. 2009;4:e6839. PubMed PMC
Huang P, Schier AF. Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development. 2009;136:3089–98. PubMed PMC
Sipe CW, Lu X. Kif3a regulates planar polarization of auditory hair cells through both ciliary and non-ciliary mechanisms. Development. 2011;138:3441–9. PubMed PMC
Kim M, Suh YA, Oh JH, Lee BR, Kim J, Jang SJ. KIF3A binds to beta-arrestin for suppressing Wnt/beta-catenin signalling independently of primary cilia in lung cancer. Scientific reports. 2016;6:32770. PubMed PMC
Balmer S, Dussert A, Collu GM, Benitez E, Iomini C, Mlodzik M. Components of Intraflagellar Transport Complex A Function Independently of the Cilium to Regulate Canonical Wnt Signaling in Drosophila. Developmental cell. 2015;34:705–18. PubMed PMC
Wigley WC, Fabunmi RP, Lee MG, Marino CR, Muallem S, DeMartino GN, Thomas PJ. Dynamic association of proteasomal machinery with the centrosome. The Journal of cell biology. 1999;145:481–90. PubMed PMC
Fabunmi RP, Wigley WC, Thomas PJ, DeMartino GN. Activity and Regulation of the Centrosome-associated Proteasome. Journal of Biological Chemistry. 2000;275:409–13. PubMed
Gerhardt C, Lier JM, Burmuhl S, Struchtrup A, Deutschmann K, Vetter M, Leu T, Reeg S, Grune T, Ruther U. The transition zone protein Rpgrip1l regulates proteasomal activity at the primary cilium. The Journal of cell biology. 2015;210:115–33. PubMed PMC
Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, Pera EM, De Robertis EM. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell. 2007;131:980–93. PubMed PMC
Vora S, Phillips BT. Centrosome-Associated Degradation Limits beta-Catenin Inheritance by Daughter Cells after Asymmetric Division. Current biology : CB. 2015;25:1005–16. PubMed
Chitalia VC, Foy RL, Bachschmid MM, Zeng L, Panchenko MV, Zhou MI, Bharti A, Seldin DC, Lecker SH, Dominguez I, Cohen HT. Jade-1 inhibits Wnt signalling by ubiquitylating beta-catenin and mediates Wnt pathway inhibition by pVHL. Nature cell biology. 2008;10:1208–16. PubMed PMC
Borgal L, Rinschen MM, Dafinger C, Hoff S, Reinert MJ, Lamkemeyer T, Lienkamp SS, Benzing T, Schermer B. Casein Kinase 1 Alpha Phosphorylates the Wnt-Regulator Jade-1 and Modulates its Activity. The Journal of biological chemistry. 2014 PubMed PMC
Mollet G, Silbermann F, Delous M, Salomon R, Antignac C, Saunier S. Characterization of the nephrocystin/nephrocystin-4 complex and subcellular localization of nephrocystin-4 to primary cilia and centrosomes. Hum Mol Genet. 2005;14:645–56. PubMed
Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW. Flies without centrioles. Cell. 2006;125:1375–86. PubMed
Bazzi H, Anderson KV. Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo. Proceedings of the National Academy of Sciences of the United States of America. 2014;111:E1491–500. PubMed PMC
Insolera R, Bazzi H, Shao W, Anderson KV, Shi SH. Cortical neurogenesis in the absence of centrioles. Nature neuroscience. 2014;17:1528–35. PubMed PMC
Niehrs C, Acebron SP. Mitotic and mitogenic Wnt signalling. EMBO J. 2012;31:2705–13. PubMed PMC
Acebron SP, Niehrs C. beta-Catenin-Independent Roles of Wnt/LRP6 Signaling. Trends in cell biology. 2016;26:956–67. PubMed
Davidson G, Shen J, Huang Y-L, Su Y, Karaulanov E, Bartscherer K, Hassler C, Stannek P, Boutros M, Niehrs C. Cell Cycle Control of Wnt Receptor Activation. Developmental cell. 2009;17:788–99. PubMed
Lee G, White LS, Hurov KE, Stappenbeck TS, Piwnica-Worms H. Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:4701–6. PubMed PMC
Acebron SP, Karaulanov E, Berger BS, Huang YL, Niehrs C. Mitotic wnt signaling promotes protein stabilization and regulates cell size. Mol Cell. 2014;54:663–74. PubMed
Chen M, Philipp M, Wang J, Premont RT, Garrison TR, Caron MG, Lefkowitz RJ, Chen W. G Protein-coupled receptor kinases phosphorylate LRP6 in the Wnt pathway. The Journal of biological chemistry. 2009;284:35040–8. PubMed PMC
Cervenka I, Wolf J, Masek J, Krejci P, Wilcox WR, Kozubik A, Schulte G, Gutkind JS, Bryja V. Mitogen-activated protein kinases promote WNT/beta-catenin signaling via phosphorylation of LRP6. Mol Cell Biol. 2011;31:179–89. PubMed PMC
Krejci P, Aklian A, Kaucka M, Sevcikova E, Prochazkova J, Masek JK, Mikolka P, Pospisilova T, Spoustova T, Weis M, Paznekas WA, et al. Receptor tyrosine kinases activate canonical WNT/beta-catenin signaling via MAP kinase/LRP6 pathway and direct beta-catenin phosphorylation. PLoS One. 2012;7:e35826. PubMed PMC
Olmeda D, Castel S, Vilaro S, Cano A. Beta-catenin regulation during the cell cycle: implications in G2/M and apoptosis. Mol Biol Cell. 2003;14:2844–60. PubMed PMC
Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH, Jr, O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI. beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes & development. 2008;22:91–105. PubMed PMC
Kikuchi K, Niikura Y, Kitagawa K, Kikuchi A. Dishevelled, a Wnt signalling component, is involved in mitotic progression in cooperation with Plk1. EMBO J. 2010;29:3470–83. PubMed PMC
Cervenka I, Valnohova J, Bernatik O, Harnos J, Radsetoulal M, Sedova K, Hanakova K, Potesil D, Sedlackova M, Salasova A, Steinhart Z, et al. Dishevelled is a NEK2 kinase substrate controlling dynamics of centrosomal linker proteins. Proceedings of the National Academy of Sciences of the United States of America. 2016;113:9304–9. PubMed PMC
Fumoto K, Kadono M, Izumi N, Kikuchi A. Axin localizes to the centrosome and is involved in microtubule nucleation. EMBO reports. 2009;10:606–13. PubMed PMC
Kim SM, Choi EJ, Song KJ, Kim S, Seo E, Jho EH, Kee SH. Axin localizes to mitotic spindles and centrosomes in mitotic cells. Exp Cell Res. 2009;315:943–54. PubMed
Hadjihannas MV, Bruckner M, Behrens J. Conductin/axin2 and Wnt signalling regulates centrosome cohesion. EMBO Rep. 2010;11:317–24. PubMed PMC
Ruan K, Ye F, Li C, Liou YC, Lin SC, Lin SY. PLK1 interacts and phosphorylates Axin that is essential for proper centrosome formation. PLoS One. 2012;7:e49184. PubMed PMC
Poulton JS, Mu FW, Roberts DM, Peifer M. APC2 and Axin promote mitotic fidelity by facilitating centrosome separation and cytoskeletal regulation. Development. 2013;140:4226–36. PubMed PMC
Greer YE, Rubin JS. Casein kinase 1 delta functions at the centrosome to mediate Wnt-3a-dependent neurite outgrowth. The Journal of cell biology. 2011;192:993–1004. PubMed PMC
Greer YE, Westlake CJ, Gao B, Bharti K, Shiba Y, Xavier CP, Pazour GJ, Yang Y, Rubin JS. Casein kinase 1 delta functions at the centrosome and Golgi to promote ciliogenesis. Molecular biology of the cell. 2014;25:1629–40. PubMed PMC
Chaki M, Airik R, Ghosh AK, Giles RH, Chen R, Slaats GG, Wang H, Hurd TW, Zhou W, Cluckey A, Gee HY, et al. Exome Capture Reveals ZNF423 and CEP164 Mutations, Linking Renal Ciliopathies to DNA Damage Response Signaling. Cell. 2012;150:533–48. PubMed PMC
Hadjihannas MV, Bernkopf DB, Bruckner M, Behrens J. Cell cycle control of Wnt/beta-catenin signalling by conductin/axin2 through CDC20. EMBO Rep. 2012;13:347–54. PubMed PMC
Kafri P, Hasenson SE, Kanter I, Sheinberger J, Kinor N, Yunger S, Shav-Tal Y. Quantifying beta-catenin subcellular dynamics and cyclin D1 mRNA transcription during Wnt signaling in single living cells. eLife. 2016;5 PubMed PMC
Lui C, Mok MT, Henderson BR. Characterization of Adenomatous Polyposis Coli Protein Dynamics and Localization at the Centrosome. Cancers. 2016;8 PubMed PMC
Schertel C, Huang D, Bjorklund M, Bischof J, Yin D, Li R, Wu Y, Zeng R, Wu J, Taipale J, Song H, et al. Systematic screening of a Drosophila ORF library in vivo uncovers Wnt/Wg pathway components. Dev Cell. 2013;25:207–19. PubMed
Weber U, Mlodzik M. APC/CFzr/Cdh1-Dependent Regulation of Planar Cell Polarity Establishment via Nek2 Kinase Acting on Dishevelled. Developmental cell. 2017;40:53–66. PubMed PMC
Hardy T, Lee M, Hames RS, Prosser SL, Cheary DM, Samant MD, Schultz F, Baxter JE, Rhee K, Fry AM. Multisite phosphorylation of C-Nap1 releases it from Cep135 to trigger centrosome disjunction. Journal of cell science. 2014;127:2493–506. PubMed PMC
Faragher AJ, Fry AM. Nek2A kinase stimulates centrosome disjunction and is required for formation of bipolar mitotic spindles. Mol Biol Cell. 2003;14:2876–89. PubMed PMC
Martins T, Meghini F, Florio F, Kimata Y. The APC/C Coordinates Retinal Differentiation with G1 Arrest through the Nek2-Dependent Modulation of Wingless Signaling. Developmental cell. 2017;40:67–80. PubMed PMC
Schlesinger A, Shelton CA, Maloof JN, Meneghini M, Bowerman B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes & development. 1999;13:2028–38. PubMed PMC
McCartney BM, McEwen DG, Grevengoed E, Maddox P, Bejsovec A, Peifer M. Drosophila APC2 and Armadillo participate in tethering mitotic spindles to cortical actin. Nature cell biology. 2001;3:933–8. PubMed
Zipperlen P, Fraser AG, Kamath RS, Martinez-Campos M, Ahringer J. Roles for 147 embryonic lethal genes on C.elegans chromosome I identified by RNA interference and video microscopy. The EMBO journal. 2001;20:3984–92. PubMed PMC
Walston T, Tuskey C, Edgar L, Hawkins N, Ellis G, Bowerman B, Wood W, Hardin J. Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev Cell. 2004;7:831–41. PubMed
Sawa H. Control of cell polarity and asymmetric division in C. elegans. Current topics in developmental biology. 2012;101:55–76. PubMed
Wallingford JB. Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annual review of cell and developmental biology. 2012;28:627–53. PubMed
Morin X, Bellaiche Y. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Developmental cell. 2011;21:102–19. PubMed
Miller RK, Rose MD. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. The Journal of cell biology. 1998;140:377–90. PubMed PMC
Bloom K. It's a kar9ochore to capture microtubules. Nature cell biology. 2000;2:E96–8. PubMed
Bahmanyar S, Nelson WJ, Barth AI. Role of APC and its binding partners in regulating microtubules in mitosis. Advances in experimental medicine and biology. 2009;656:65–74. PubMed PMC
Caldwell CM, Kaplan KB. The role of APC in mitosis and in chromosome instability. Advances in experimental medicine and biology. 2009;656:51–64. PubMed
Zhang L, Shay JW. Multiple Roles of APC and its Therapeutic Implications in Colorectal Cancer. Journal of the National Cancer Institute. 2017;109 PubMed PMC
Kaplan DD, Meigs TE, Kelly P, Casey PJ. Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. The Journal of biological chemistry. 2004;279:10829–32. PubMed
Thorpe CJ, Schlesinger A, Carter JC, Bowerman B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell. 1997;90:695–705. PubMed
Banziger C, Soldini D, Schutt C, Zipperlen P, Hausmann G, Basler K. Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell. 2006;125:509–22. PubMed
Habib SJ, Chen BC, Tsai FC, Anastassiadis K, Meyer T, Betzig E, Nusse R. A localized Wnt signal orients asymmetric stem cell division in vitro. Science. 2013;339:1445–8. PubMed PMC
Stolz A, Neufeld K, Ertych N, Bastians H. Wnt-mediated protein stabilization ensures proper mitotic microtubule assembly and chromosome segregation. EMBO reports. 2015;16:490–9. PubMed PMC
Carvajal-Gonzalez JM, Mulero-Navarro S, Mlodzik M. Centriole positioning in epithelial cells and its intimate relationship with planar cell polarity. BioEssays : news and reviews in molecular, cellular and developmental biology. 2016;38:1234–45. PubMed PMC
Antic D, Stubbs JL, Suyama K, Kintner C, Scott MP, Axelrod JD. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PloS one. 2010;5:e8999. PubMed PMC
Borovina A, Superina S, Voskas D, Ciruna B. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nature cell biology. 2010;12:407–12. PubMed
Oishi I, Kawakami Y, Raya A, Callol-Massot C, Izpisua Belmonte JC. Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nature genetics. 2006;38:1316–22. PubMed
Park TJ, Mitchell BJ, Abitua PB, Kintner C, Wallingford JB. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nature genetics. 2008;40:871–9. PubMed PMC
Park TJ, Haigo SL, Wallingford JB. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nature genetics. 2006;38:303–11. PubMed
Gray RS, Abitua PB, Wlodarczyk BJ, Szabo-Rogers HL, Blanchard O, Lee I, Weiss GS, Liu KJ, Marcotte EM, Wallingford JB, Finnell RH. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nature cell biology. 2009;11:1225–32. PubMed PMC
Carvajal-Gonzalez JM, Roman AC, Mlodzik M. Positioning of centrioles is a conserved readout of Frizzled planar cell polarity signalling. Nature communications. 2016;7 11135. PubMed PMC
Caron A, Xu X, Lin X. Wnt/beta-catenin signaling directly regulates Foxj1 expression and ciliogenesis in zebrafish Kupffer's vesicle. Development. 2012;139:514–24. PubMed PMC
Stubbs JL, Oishi I, Izpisua Belmonte JC, Kintner C. The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat Genet. 2008;40:1454–60. PubMed PMC
Walentek P, Beyer T, Thumberger T, Schweickert A, Blum M. ATP4a is required for Wnt-dependent Foxj1 expression and leftward flow in Xenopus left-right development. Cell Rep. 2012;1:516–27. PubMed
Walentek P, Schneider I, Schweickert A, Blum M. Wnt11b is involved in cilia-mediated symmetry breakage during Xenoplus left-right development. PLoS One. 2013;8:e73646. PubMed PMC
Hashimoto M, Shinohara K, Wang J, Ikeuchi S, Yoshiba S, Meno C, Nonaka S, Takada S, Hatta K, Wynshaw-Boris A, Hamada H. Planar polarization of node cells determines the rotational axis of node cilia. Nature cell biology. 2010;12:170–6. PubMed
Ohata S, Nakatani J, Herranz-Perez V, Cheng J, Belinson H, Inubushi T, Snider WD, Garcia-Verdugo JM, Wynshaw-Boris A, Alvarez-Buylla A. Loss of Dishevelleds disrupts planar polarity in ependymal motile cilia and results in hydrocephalus. Neuron. 2014;83:558–71. PubMed PMC
Mitchell B, Stubbs JL, Huisman F, Taborek P, Yu C, Kintner C. The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr Biol. 2009;19:924–9. PubMed PMC
Ganner A, Lienkamp S, Schafer T, Romaker D, Wegierski T, Park TJ, Spreitzer S, Simons M, Gloy J, Kim E, Wallingford JB, et al. Regulation of ciliary polarity by the APC/C. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:17799–804. PubMed PMC
Mahuzier A, Gaude HM, Grampa V, Anselme I, Silbermann F, Leroux-Berger M, Delacour D, Ezan J, Montcouquiol M, Saunier S, Schneider-Maunoury S, et al. Dishevelled stabilization by the ciliopathy protein Rpgrip1l is essential for planar cell polarity. The Journal of cell biology. 2012;198:927–40. PubMed PMC
Lee KH, Johmura Y, Yu LR, Park JE, Gao Y, Bang JK, Zhou M, Veenstra TD, Yeon Kim B, Lee KS. Identification of a novel Wnt5a-CK1 epsilon-Dvl2-Plk1-mediated primary cilia disassembly pathway. The EMBO journal. 2012 PubMed PMC
Gao C, Chen YG. Dishevelled: The hub of Wnt signaling. Cellular signalling. 2010;22:717–27. PubMed
Zhang B, Zhang T, Wang G, Wang G, Chi W, Jiang Q, Zhang C. GSK3beta-Dzip1-Rab8 Cascade Regulates Ciliogenesis after Mitosis. PLoS biology. 2015;13:e1002129. PubMed PMC
Thoma CR, Frew IJ, Hoerner CR, Montani M, Moch H, Krek W. pVHL and GSK3beta are components of a primary cilium-maintenance signalling network. Nature cell biology. 2007;9:588–95. PubMed
Wakefield JG, Stephens DJ, M TJ. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J Cell Sci. 2003;116(Pt 4):637–46. PubMed
Itoh K, Jenny A, Mlodzik M, Sokol SY. Centrosomal localization of Diversin and its relevance to Wnt signaling. J Cell Sci. 2009;122:3791–98. PubMed PMC
Alexandrova EM, Sokol SY. Xenopus axin-related protein: a link between its centrosomal localization and function in the Wnt/beta-catenin pathway. Dev Dyn. 2010;239:261–70. PubMed
Sillibourne JE, Milne DM, Takahashi M, Ono Y, Meek DW. Centrosomal Anchoring of the Protein Kinase CK1δ Mediated by Attachment to the Large, Coiled-coil Scaffolding Protein CG-NAP/AKAP450. Journal of Molecular Biology. 2002;322:785–97. PubMed
Zyss D, Ebrahimi H, Gergely F. Casein kinase I delta controls centrosome positioning during T cell activation. The Journal of cell biology. 2011;195:781–97. PubMed PMC
Firat-Karalar EN, Rauniyar N, Yates JR, 3rd, Stearns T. Proximity interactions among centrosome components identify regulators of centriole duplication. Current biology : CB. 2014;24:664–70. PubMed PMC
Mick DU, Rodrigues RB, Leib RD, Adams CM, Chien AS, Gygi SP, Nachury MV. Proteomics of Primary Cilia by Proximity Labeling. Developmental cell. 2015;35:497–512. PubMed PMC
Andersen JS, Wilkinson CJ, Mayor T, Mortensen P. Proteomic characterization of the human centrosome by protein correlation profiling. Nature. 2003;426:570–74. PubMed
Mbom BC, Siemers KA, Ostrowski MA, Nelson WJ, Barth AI. Nek2 phosphorylates and stabilizes beta-catenin at mitotic centrosomes downstream of Plk1. Mol Biol Cell. 2014;25:977–91. PubMed PMC
He XQ, Song YQ, Liu R, Liu Y, Zhang F, Zhang Z, Shen YT, Xu L, Chen MH, Wang YL, Xu BH, et al. Axin-1 Regulates Meiotic Spindle Organization in Mouse Oocytes. PloS one. 2016;11:e0157197. PubMed PMC
Dikovskaya D, Newton IP, Nathke IS. The adenomatous polyposis coli protein is required for the formation of robust spindles formed in CSF Xenopus extracts. Molecular biology of the cell. 2004;15:2978–91. PubMed PMC
Lui C, Ashton C, Sharma M, Brocardo MG, Henderson BR. APC functions at the centrosome to stimulate microtubule growth. The international journal of biochemistry & cell biology. 2016;70:39–47. PubMed
Yamashita YM, Jones DL, Fuller MT. Orientation of Asymmetric Stem Cell Division by the APC Tumor Suppressor and Centrosome. Science. 2003;301:1547–50. PubMed
Fumoto K, Kikuchi K, Gon H, Kikuchi A. Wnt5a signaling controls cytokinesis by correctly positioning ESCRT-III at the midbody. J Cell Sci. 2012;125:4822–32. PubMed
Yang Y, Liu M, Li D, Ran J, Gao J, Suo S, Sun SC, Zhou J. CYLD regulates spindle orientation by stabilizing astral microtubules and promoting dishevelled-NuMA-dynein/dynactin complex formation. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(6):2158–63. PubMed PMC
Brockman JL, Gross SG, Sussman MR, Anderson RA. Cell cycle-dependent localization of casein kinase I to mitotic spindles. Proceedings of the National Academy of Sciences of the United States of America. 1992;89:9454–58. PubMed PMC
Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nature cell biology. 2001;3:426–32. PubMed
Linking planar polarity signalling to actomyosin contractility during vertebrate neurulation
Primary Cilia Formation Does Not Rely on WNT/β-Catenin Signaling
KIF14 controls ciliogenesis via regulation of Aurora A and is important for Hedgehog signaling
Phosphorylation of multiple proteins involved in ciliogenesis by Tau Tubulin kinase 2
Comparative phosphorylation map of Dishevelled 3 links phospho-signatures to biological outputs