Biogeneza rzęski pierwotnej

• Authors: Martyna Poprzeczko , Ewa Joachimiak , Dorota Włoga , Hanna Fabczak

Title variants

EN

Biogenesis of the primary cilium

• Languages of publication: PL EN

Abstracts

PL

Rzęski pierwotne, struktury zbudowane na bazie cytoszkieletu mikrotubularnego, występują na powierzchni niemal wszystkich komórek ssaczych. Dzięki licznym receptorom błonowym, rzęski pierwotne pośredniczą w odbieraniu i przekazywaniu bodźców ze środowiska do wnętrza komórki, i tym samym odgrywają niezwykle ważną rolę w prawidłowym rozwoju i funkcjonowaniu większości tkanek i narządów. Tworzenie rzęski (ciliogeneza) to złożony, wieloetapowy i wielopoziomowo regulowany proces ściśle związany z cyklem komórkowym. Mutacje w genach kodujących białka strukturalne lub odpowiedzialne za prawidłowe funkcjonowanie rzęsek, jak również, regulujące przebieg ciliogenezy są przyczyną ich dysfunkcji, prowadzącej w efekcie do wielonarządowych chorób zwanych ciliopatiami.

EN

Cilia are highly specialized, microtubule-based protrusions, extended on cell surface in almost all mammalian cell types. They function as cell antennae that receive and transmit signals from the environment to the cell body. Cilia formation, so-called ciliogenesis is strictly controlled at multiple levels by a number of proteins, and correlated with the cell cycle progression. Cilia dysfunctions cause a wide range of human diseases, called ciliopathies. Moreover, ciliary defects may lead to obesity and cancer. In this article, we summarize current knowledge concerning cilia function and structure, regulation of ciliogenesis, and the most important signaling pathways and diseases affected by cilia dysfunction.

Keywords

PL

ciliogeneza; ciliopatie; cykl komórkowy; rzęska pierwotna

EN

cell cycle; ciliogenesis; ciliopathies; primary cilium

• Journal: Kosmos
• Year: 2018
• Volume: 67
• Issue: 1
• Pages: 179-193

Dates

published

2018

Contributors

author

Martyna Poprzeczko

• Pracownia Cytoszkieletu i Biologii Rzęsek, Zakład Biologii Komórki, Instytut Biologii Doświadczalnej im. M. Nenckiego PAN, Pasteura 3, 02-093 Warszawa, Polska
• Laboratory of Cytoskeleton and Cilia Biology, Department of Cell Biology, Nencki Institute of Experimental Biology PAS, 3Pasteur Str., 02-093 Warsaw, Poland

author

Ewa Joachimiak

• Pracownia Cytoszkieletu i Biologii Rzęsek, Zakład Biologii Komórki, Instytut Biologii Doświadczalnej im. M. Nenckiego PAN, Pasteura 3, 02-093 Warszawa, Polska
• Laboratory of Cytoskeleton and Cilia Biology, Department of Cell Biology, Nencki Institute of Experimental Biology PAS, 3Pasteur Str., 02-093 Warsaw, Poland

author

Dorota Włoga

• Pracownia Cytoszkieletu i Biologii Rzęsek, Zakład Biologii Komórki, Instytut Biologii Doświadczalnej im. M. Nenckiego PAN, Pasteura 3, 02-093 Warszawa, Polska
• Laboratory of Cytoskeleton and Cilia Biology, Department of Cell Biology, Nencki Institute of Experimental Biology PAS, 3Pasteur Str., 02-093 Warsaw, Poland

author

Hanna Fabczak

• Pracownia Cytoszkieletu i Biologii Rzęsek, Zakład Biologii Komórki, Instytut Biologii Doświadczalnej im. M. Nenckiego PAN, Pasteura 3, 02-093 Warszawa, Polska
• Laboratory of Cytoskeleton and Cilia Biology, Department of Cell Biology, Nencki Institute of Experimental Biology PAS, 3Pasteur Str., 02-093 Warsaw, Poland

References

• Aragona M., Panciera T., Manfrin A., Giulitti S., Michielin F., Elvassore N., Dupont S., Piccolo S., 2013. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059.
• Benmerah A., 2013. The ciliary pocket. Curr. Opin. Cell Biol. 25, 78-84.
• Berbari N. F., O'connor A. K., Haycraft C. J., Yoder B. K., 2009. The primary cilium as a complex signaling center. Curr. Biol. 19, 526-535.
• Bershteyn M., Atwood S. X., Woo W. M., Li M., Oro A. E., 2010. MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev. Cell 19, 270-283.
• Besschetnova T. Y., Kolpakova-Hart E., Guan Y., Zhou J., Olsen B. R., Shah J. V., 2010. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr. Biol. 20,182-187.
• Bhogaraju S., Cajanek L., Fort C., Blisnick T., Weber K., Taschner M., Mizuno N, Lamla S., Bastin P., Nigg E. A., Lorentzen E., 2013. Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science 341, 1009-1012.
• Cardenas-Rodriguez M., Badano J. L., 2009. Ciliary biology: understanding the cellular and genetic basis of human ciliopathies. Am. J. Med. Genet. C. Semin. Med. Genet. 151C, 263-280.
• Chang J., Lee K., Nagashima K., Bang J., Kim B., Erikson R. L., Lee K., Lee H., Park J., Lee K. S., 2013. Essential role of Cenexin1, but not Odf2, in ciliogenesis. Cell Cycle 12, 655-662.
• Chen Z., Indjeian V. B., Mcmanus M., Wang L., Dynlacht, B. D., 2002. CP110, a cell cycle-dependent CDK substrate, regulates centrosome duplication in human cells. Dev. Cell 3, 339-350.
• D'angiolella V., Donato V., Vijayakumar S., Saraf A., Florens L., Washburn M. P., Dynlacht B., Pagano M., 2010. SCFCyclin F controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 466, 138-142.
• Delaval B., Bright A., Lawson N. D., Doxsey S., 2011. The cilia protein IFT88 is required for spindle orientation in mitosis. Nat. Cell Biol. 13, 461-468.
• Fabczak H., 2001. Rodzina białek Rho a cytoszkielet. Kosmos 50, 283-293.
• Fliegauf M., Benzing T., Omran H., 2007. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893.
• Funabashi T., Katoh Y., Michisaka S., Terada M., Sugawa M., Nakayama K.,
• 2017. Ciliary entry of KIF17 is dependent on its binding to the IFT-B complex via IFT46-IFT56 as well as on its nuclear localization signal. Mol. Biol. Cell 28, 624-633.
• Garcia-Gonzalo F. R., Reiter J. F., 2012. Scoring a backstage pass: Mechanisms of ciliogenesis and ciliary access. J. Cell Biol. 197, 697-709.
• Garcia-Gonzalo F. R., Reiter J. F., 2017. Open sesame: How transition fibers and the transition zone control ciliary. Cold Spring Harb. Perspect. Biol. 9, doi: 10.1101/cshperspect.a028134.
• Gherman A., Davis E. E., Katsanis N., 2006. The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat. Gen. 38, 961-962.
• Goetz S. C., Liem K. F. Jr., Anderson K. V., 2012. The spinocerebellar ataxia-associated gene Tau tubulin kinase 2 controls the initiation of ciliogenesis. Cell 151, 847-858.
• Huet D., Blisnick T., Perrot S., Bastin P., 2014. The GTPase IFT27 is involved in both anterograde and retrograde intraflagellar transport. Elife 3, e02419.
• Ibi M., Zou P., Inoko A., Shiromizu T., Matsuyama M., Hayashi Y., Enomoto M., Mori D., Hirotsune S., Kiyono T., Tsukita S., Goto H., Inagaki M., 2011. Trichoplein controls microtubule anchoring at the centrosome by binding to Odf2 and ninein. J. Cell Sci. 124, 857-864.
• Inaba H., Goto H., Kasahara K., Kumamoto K., Yonemura S., Inoko A., Yamano S., Wanibuchi H., He D., Goshima N., Kiyono T., Hirotsune S., Inagaki M., 2016. Ndel1 suppresses ciliogenesis in proliferating cells by regulating the trichoplei-Aurora A pathway. J. Cell Biol. 212, 409-423.
• Inoko A., Matsuyama M., Goto H., Ohmuro-Matsuyama Y., Hayashi Y., Enomoto M., Ibi M., Urano T., Yonemura S., Kiyono T., Izawa I., Inagaki M., 2012. Trichoplein and Aurora A block aberrant primary cilia assembly in proliferating cells. J. Cell Biol. 197, 391-405.
• Ishikawa H., Marshall W. F., 2011. Ciliogenesis: building the cell's antenna. Nature Rev. Mol. Cell Biol. 12, 222-234.
• Ishikawa H., Kubo A., Tsukita S., 2005. Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat. Cell Biol. 7, 517-524.
• Izawa I., Goto H., Kasahara K., Inagaki M., 2015. Current topics of functional links between primary cilia and cell cycle. Cilia 4, 12.
• Kasahara K., Kawakami Y., Kiyono T., Yonemura S., Kawamura Y., Era S., Matsuzaki F., Goshima N., Inagaki M., 2014. Ubiquitin-proteasome system controls ciliogenesis at the initial step of axoneme extension. Nat. Commun. 5, 5081.
• Ke Y. N., Yang W. X., 2014. Primary cilium: an elaborate structure that blocks cell division? Gene 547, 175-185.
• Kim J., Lee J. E., Heynen-Genel S., Suyama E., Ono K., Lee K., Ideker T., Aza-Blanc P., Gleeson J.G. 2010. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464, 1048-1051.
• Kim J., Jo H., Hong H., Kim M. H., Kim J. M., Lee J. K., Heo W. D., Kim J., 2015. Actin remodelling factors control ciliogenesis by regulating YAP/TAZ activity and vesicle trafficking. Nat. Commun. 6, 6781.
• Kim M., Kim M., Lee M. S., Kim C. H., Lim D. S., 2014. The MST1/2-SAV1 complex of the Hippo pathway promotes ciliogenesis. Nat. Commun. 5, 5370.
• Kim S., Tsiokas L., 2011. Cilia and cell cycle re-entry. More than a coincidence. Cell Cycle 10, 2683-2690.
• Kim S., Dynlacht B. D., 2013. Assembling a primary cilium. Curr. Opin. Cell Biol. 25, 506-511.
• Kim S., Zaghloul N. A., Bubenshchikova E., Oh E. C., Rankin S., Katsanis N., Obara T., Tsiokas L., 2011. Nde1-mediated inhibition of ciliogenesis affects cell cycle reentry. Nat. Cell Biol. 13, 351-360.
• Kinzel D., Boldt K., Davis E. E., Burtscher I., Trümbach D., Diplas, B., Attié-Bitach T., Wurst W., Katsanis N., Ueffing M., Lickert H., 2010. Pitchfork regulates primary cilia disassembly and left-right asymmetry. Dev. Cell 19, 66-77.
• Kleylein-Sohn J., Westendorf J., Le Clech M., Habedanck R., Stierhof Y. D., Nigg E. A. 2007. Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
• Kobayashi T., Dynlacht B. D., 2011. Regulating the transition from centriole to basal body. J. Cell Biol. 193, 435-444.
• Kobayashi T., Tsang W. Y., Li J., Lane W., Dynlacht B. D., 2011. Centriolar kinesin Kif24 interacts with CP110 to remodel microtubules and regulate ciliogenesis. Cell 145, 914-925.
• Korobeynikov V., Deneka A. Y., Golemis E. A. 2017. Mechanisms for nonmitotic activation of Aurora-A at cilia. Biochem. Soc. Trans. 45, 37-49.
• Kozminski K. G., Johnson K. A., Forscher P., Rosenbaum J. L., 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA 90, 5519-5523.
• Kuhns S., Schmidt K. N., Reymann J., Gilbert D. F., Neuner A., Hub B., Carvalho R., Wiedemann P., Zentgraf H., Erfle H., Klingmüller U., Boutros M., Pereira G., 2013. The microtubule affinity regulating kinase MARK4 promotes axoneme extension during early ciliogenesis. J. Cell Biol. 200, 505-522.
• Lefebvre P. A., Rosenbaum J. L., 1986. Regulation of the synthesis and assembly of ciliary and flagellar proteins during regeneration. Annu. Rev. Cell Biol. 2, 517-546.
• Li A., Saito M., Chuang J. Z., Tseng Y. Y., Dedesma C., Tomizawa K., Kaitsuka T., Sung C. H., 2011. Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorp- tion, S-phase entry and fate of neural progenitors. Nat. Cell Biol. 13, 402-411.
• Liang Y., Meng D., Zhu B., Pan J., 2016. Mechanism of ciliary disassembly. Cell. Mol. Life Sci. 73, 1787-1802.
• Madhivanan K., Aguilar R. C., 2014. Ciliopathies: The trafficking connection. Traffic 15, 1031-1056.
• Mahaffey J., Grego-Bessa J., Liem K. F., Anderson K. V. Jr., 2013. Cofilin and Vangl2 cooperate in the initiation of planar cell polarity in the mouse embryo. Development 140, 1262-1271.
• Malicki J. J., Avidor-Reiss T., 2014. From the cytoplasm into the cilium: Bon voyage. Organogenesis 10, 138-157.
• Malicki J., Johnson C. A., 2017. The cilium: Cellular antenna and central processing unit. Trends Cell Biol. 27, 126-140.
• Maskey D., Marlin M. C., Kim S., Kim S., Ong E. C., Li G., Tsiokas L., 2015. Cell cycle-dependent ubiquitylation and destruction of NDE1 by CDK5-FBW7 regulates ciliary length. EMBO J. 34, 2424-2440.
• Miyamoto T., Hosoba K., Ochiai H., Royba E., Izumi H., Sakuma T., Yamamoto T., Dynlacht B. D., Matsuura S., 2015. The microtubule-depolymerizing activity of a mitotic kinesin protein KIF2AKIF2A drives primary cilia disassembly coupled with cell proliferation. Cell Rep. doi: 10.1016/j.celrep.2015.01.003.
• 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., 2007. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213.
• Nachury M. V., Seeley E. S., Jin H., 2010. Trafficking to the ciliary membrane: How to Get across the periciliary diffusion barrier? Annu. Rev. Cell Dev. Biol. 26, 59-87.
• Oda T., Chiba S., Nagai T., Mizuno K., 2014. Binding to Cep164, but not EB1, is essential for centriolar localization of TTBK2 and its function in ciliogenesis. Genes Cells 19, 927-940.
• Ou Y., Ruan Y., Cheng M., Moser J. J., Rattner J. B., Van Der Hoorn F. A., 2009. Adenylate cyclase regulates elongation of mammalian primary cilia. Exp. Cell Res. 315, 2802-2817.
• Pedersen L. B., Veland I. R., Schroder J. M., Christensen S. T., 2008. Assembly of primary cilia. Dev. Dynam.. 237, 1993-2006.
• Prevo B., Scholey J. M., Peterman E. J. G., 2017. Intraflagellar transport: mechanisms of motor action, cooperation, and cargo delivery. FEBS J., doi: 10.1111/febs.14068.
• Pugacheva E. N., Jablonski S. A., Hartman T. R., Henske E. P., Golemis E. A., 2007. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129, 1351-1363.
• Qin H., Wang Z., Diener D., Rosenbaum J., 2007. Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr. Biol. 17, 193-202.
• Ran J., Yang Y., Li D., Liu M., Zhou J., 2015. Deacetylation of α-tubulin and cortactin is required for HDAC6 to trigger ciliary disassembly. Sci. Rep. 5, 12917.
• Rieder C. L., Jensen C. G., Jensen L. C. W., 1979. The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J. Ultrast. Res. 68, 173-185.
• Sacher M., Kim Y.-G., Lavie A., Oh B.-H., Segev N., 2008. The TRAPP complex: insights into its architecture and function. Traffic 9, 2032-2042.
• Sánchez I., Dynlacht B. D., 2016. Cilium assembly and disassembly. Nat. Cell Biol. 18, 711-717.
• Sánchez de Diego A., Alonso Guerrero A., Martínez A. C., van Wely K. H., 2014. Dido3-dependent HDAC6 targeting controls cilium size. Nat. Commun. 5, 3500.
• Santos N., Reiter J. F., 2014 A central region of Gli2 regulates its localization to the primary cilium and transcriptional activity. J. Cell Sci. 127, 1500-1510.
• Schmidt K. N., Kuhns S., Neuner A., Hub B., Zentgraf H., Pereira G., 2012. Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis. J. Cell Biol. 199, 1083-1101.
• Singla V., Reiter J. F., 2006. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633.
• Sorokin S., 1962. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363-377.
• Sorokin S., 1968. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3, 207-230.
• Spektor A., Tsang W. Y., Khoo D., Dynlacht B. D., 2007. Cep97 and CP110 suppress a cilia assembly program. Cell 130, 678-690.
• Stepanek L., Pigino G., 2016. Microtubule doublets are double-track railways for intraflagellar transport trains. Science 352, 721-724.
• Sung C. H., Li A., 2011. Ciliary resorption modulates G1 length and cell cycle progression. Cell Cycle 10, 2825-2826.
• Tanos B. E., Yang H.-J., Soni R. Wang W.-J., Macaluso F.P., Asara J. M., Tsou M.-F. B., 2013. Centriole distal appendages promote membrane docking, leading to cilia initiation, Genes Dev. 27, 163-168.
• Tateishi K., Yamazaki Y., Nishida T., Watanabe S., Kunimoto K., Ishikawa H., Tsukita S., 2013. Two appendages homologous between basal bodies and centrioles are formed using distinct Odf2 domains. J. Cell Biol. 203, 417-425.
• Tucker R. W., Pardee A. B., 1979. Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells. Cell 17, 527-535.
• Wacławek E., Włoga D., 2016. Microtubule severing proteins - structure and regulation of activity. Post. Biochem. 62, 46-51.
• Westlake C. J., Baye L. M., Nachury M. V., Wright K. J., Ervin K. E., Phu L., Chalouni C., Beck J. S., Kirkpatrick D. S., Slusarski D. C., Sheffield V. C., Scheller R. H., Jackson P. K., 2011. 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.
• Wheatley D. N., Wang A. M., Strugnell G. E., 1996. Expression of primary cilia in mammalian cells. Cell Biol. Inter. 20, 73-81.
• Wloga D., Joachimiak E., Louka P., Gaertig J., 2017. Posttranslational modifications of tubulin and cilia. Cold Spring Harb Perspect Biol. 9. doi: 10.1101/cshperspect.a028159.
• Xu Q., Zhang Y., Wei Q., Huang Y., Hu J., Ling K., 2016. Phosphatidylinositol phosphate kinase PIPKIγ and phosphatase INPP5E coordinate initiation of ciliogenesis. Nat. Commun. 7, 10777.
• Yan X., Zhu X., 2013. Branched F-actin as a negative regulator of cilia formation. Exp. Cell Res. 319, 147-151.
• Zhao X., Jin M., Wang M., Sun L., Hong X., Cao Y., Wang C., 2016. Fidgetin-like 1 is a ciliogenesis-inhibitory centrosome protein. Cell Cycle 15, 2367-2375.
• Zhou X., Fan L.X., Li K., Ramchandran R., Calvet J.P., Li X., 2014. SIRT2 regulates ciliogenesis and contributes to abnormal centrosome amplification caused by loss of polycystin-1. Hum, Mol, Genet. 23, 1644-1655.