The centrosome is an actin-organizing centre

Nature Cell Biology

Volumn 18, Issue 1, 2016, Pages 65-75

  Farina, Francesca ^a   Gaillard, Jérémie ^a   Guérin, Christophe ^a   Couté, Yohann ^a   Sillibourne, James ^a,b   Blanchoin, Laurent ^a   Théry, Manuel ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; CELL PROTEIN; PERICENTRIOLAR MATERIAL 1 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WASH PROTEIN; ACTIN;

ACTIN FILAMENT; ARTICLE; CELL FUNCTION; CELL ISOLATION; CELL NUCLEUS; CENTROSOME; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MICROTUBULE ORGANIZING CENTER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; CELL CULTURE; CELL POLARITY; CYTOSKELETON; METABOLISM; MICROTUBULE; PHYSIOLOGY;

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; CELL POLARITY; CELLS, CULTURED; CENTROSOME; CYTOSKELETON; HUMANS; MICROTUBULES;

EID: 84952639793     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3285     Document Type: Article

References (70)

1. Bornens, M. Organelle positioning and cell polarity. Nat. Rev. Mol. Cell Biol. 9, 874-886 (2008).
2. Etienne-Manneville, S. Actin and microtubules in cell motility: which one is in control Traffic 5, 470-477 (2004).
3. Rodriguez, O. C. et al. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5, 599-609 (2003).
4. Coles, C. H., Bradke, F. Coordinating neuronal actin-microtubule dynamics. Curr. Biol. 25, R677-R691 (2015).
5. Chesarone, M. A., DuPage, A. G., Goode, B. L. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat. Rev. Mol. Cell Biol. 11, 62-74 (2010).
6. Vaughan, S., Dawe, H. R. Common themes in centriole and centrosome movements. Trends Cell Biol. 21, 57-66 (2011).
7. Tang, N., Marshall, W. F. Centrosome positioning in vertebrate development. J. Cell Sci. 125, 4951-4961 (2012).
8. Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L., Bornens, M. The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317-329 (2000).
9. Chevrier, V. The Rho-associated protein kinase p160ROCK is required for centrosome positioning. J. Cell Biol. 157, 807-817 (2002).
10. Euteneuer, U., Schliwa, M. Evidence for an involvement of actin in the positioning and motility of centrosomes. J. Cell Biol. 101, 96-103 (1985).
11. Cao, J., Crest, J., Fasulo, B., Sullivan, W. Cortical actin dynamics facilitate earlystage centrosome separation. Curr. Biol. 20, 770-776 (2010).
12. Wang, W., Chen, L., Ding, Y., Jin, J., Liao, K. Centrosome separation driven by actin-microfilaments during mitosis is mediated by centrosome-associated tyrosinephosphorylated cortactin. J. Cell Sci. 121, 1334-1343 (2008).
13. Rosenblatt, J., Cramer, L. P., Baum, B., Mcgee, K. M. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 117, 361-372 (2004).
14. Kunda, P., Pelling, A. E., Liu, T., Baum, B. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18, 91-101 (2008).
15. Antoniades, I., Stylianou, P., Skourides, P. A. Making the connection: ciliary adhesion complexes anchor basal bodies to the actin cytoskeleton. Dev. Cell 28, 70-80 (2014).
16. 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).
17. Kleve, M. G., Clark, W. H. Association of actin with sperm centrioles: isolation of centriolar complexes and immunofluorescent localization of actin. J. Cell Biol. 86, 87-95 (1980).
18. 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).
19. Hong, H., Kim, J., Kim, J. Myosin heavy chain 10 (MYH10) is required for centriole migration during the biogenesis of primary cilia. Biochem. Biophys. Res. Commun. 461, 180-185 (2015).
20. Dawe, H. R. et al. Nesprin-2 interacts with meckelin and mediates ciliogenesis via remodelling of the actin cytoskeleton. J. Cell Sci. 122, 2716-2726 (2009).
21. Gomez, T. S. et al. Formins regulate the actin-related protein 2/3 complexindependent polarization of the centrosome to the immunological synapse. Immunity 26, 177-190 (2007).
22. Chodagam, S., Royou, A., Whitfield, W., Karess, R., Raff, J. W. The centrosomal protein CP190 regulates myosin function during early Drosophila development. Curr. Biol. 15, 1308-1313 (2005).
23. Stevenson, V. A., Kramer, J., Kuhn, J., Theurkauf, W. E. Centrosomes and the Scrambled protein coordinate microtubule-independent actin reorganization. Nat. Cell Biol. 3, 68-75 (2001).
24. Munro, E., Nance, J., Priess, J. R. Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 7, 413-424 (2004).
25. Cowan, C. R., Hyman, A. a. Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 431, 92-96 (2004).
26. Woolner, S., O'Brien, L. L., Wiese, C., Bement, W. M. Myosin-10 and actin filaments are essential for mitotic spindle function. J. Cell Biol. 182, 77-88 (2008).
27. Mitsushima, M. et al. Revolving movement of a dynamic cluster of actin filaments during mitosis. J. Cell Biol. 191, 453-462 (2010).
28. Fink, J. et al. External forces control mitotic spindle positioning. Nat. Cell Biol. 13, 771-778 (2011).
29. Stinchcombe, J. C., Majorovits, E., Bossi, G., Fuller, S., Griffiths, G. M. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443, 462-465 (2006).
30. Bornens, M. Is the centriole bound to the nuclear membrane Nature 270, 80-82 (1977).
31. Burakov, A. V., Nadezhdina, E. S. Association of nucleus and centrosome: magnet or velcro Cell Biol. Int. 37, 95-104 (2013).
32. Bornens, M., Moudjou, M. Studying the composition and function of centrosomes in vertebrates. Methods Cell Biol. 61, 13-34 (1999).
33. Andersen, J. S. et al. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574 (2003).
34. Jakobsen, L. et al. Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J. 30, 1520-1535 (2011).
35. Firat-Karalar, E. N., Sante, J., Elliott, S., Stearns, T. Proteomic analysis of mammalian sperm cells identifies new components of the centrosome. J. Cell Sci. 127, 4128-4133 (2014).
36. Bornens, M., Paintrand, M., Berges, J., Marty, M. C., Karsenti, E. Structural and chemical characterization of isolated centrosomes. Cell Motil. Cytoskeleton 8, 238-249 (1987).
37. Miranda, A. F., Godman, G. C., Tanenbaum, S. W. Action of cytochalasin D on cells of established lines. II. Cortex and microfilaments. J. Cell Biol. 62, 406-423 (1974).
38. Chesarone, M. A., Goode, B. L. Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28-37 (2009).
39. Hubert, T., Vandekerckhove, J., Gettemans, J. Actin and Arp2/3 localize at the centrosome of interphase cells. Biochem. Biophys. Res. Commun. 404, 153-158 (2011).
40. Welch, M. D., DePace, A. H., Verma, S., Iwamatsu, A., Mitchison, T. J. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell Biol. 138, 375-384 (1997).
41. Nolen, B. J. et al. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034 (2009).
42. Monfregola, J., Napolitano, G., D'Urso, M., Lappalainen, P., Ursini, M. V. Functional characterization of Wiskott-Aldrich syndrome protein and scar homolog (WASH), a bi-modular nucleation-promoting factor able to interact with biogenesis of lysosome-related organelle subunit 2 (BLOS2) and gamma-tubulin. J. Biol. Chem. 285, 16951-16957 (2010).
43. Derivery, E. et al. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev. Cell 17, 712-723 (2009).
44. Bärenz, F., Mayilo, D., Gruss, O. J. Centriolar satellites: busy orbits around the centrosome. Eur. J. Cell Biol. 90, 983-989 (2011).
45. Dammermann, A., Merdes, A. Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159, 255-266 (2002).
46. Sillibourne, J. E. et al. Primary ciliogenesis requires the distal appendage component Cep123. Biol. Open 2, 535-545 (2013).
47. Kubo, A., Sasaki, H., Yuba-Kubo, A., Tsukita, S., Shiina, N. Centriolar satellites: molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis. J. Cell Biol. 147, 969-980 (1999).
48. Clark, I. B., Meyer, D. I. Overexpression of normal and mutant Arp1-(centractin) differentially affects microtubule organization during mitosis and interphase. J. Cell Sci. 112, 3507-3518 (1999).
49. Patel, H. et al. Kindlin-1 regulates mitotic spindle formation by interacting with integrins and Plk-1. Nat. Commun. 4, 2056 (2013).
50. Pugacheva, E. N., Golemis, E. A. The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome. Nat. Cell Biol. 7, 937-946 (2005).
51. Fielding, A. B., Dobreva, I., McDonald, P. C., Foster, L. J., Dedhar, S. Integrin-linked kinase localizes to the centrosome and regulates mitotic spindle organization. J. Cell Biol. 180, 681-689 (2008).
52. Hubert, T., Van Impe, K., Vandekerckhove, J., Gettemans, J. The actin-capping protein CapG localizes to microtubule-dependent organelles during the cell cycle. Biochem. Biophys. Res. Commun. 380, 166-170 (2009).
53. 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).
54. Epting, D. et al. The Rac1 regulator ELMO controls basal body migration and docking in multiciliated cells through interaction with Ezrin. Development 142, 174-184 (2015).
55. Sabino, D. et al. Moesin is a major regulator of centrosome behavior in epithelial cells with extra centrosomes. Curr. Biol. 25, 879-889 (2015).
56. Kaplan, D. D., Meigs, T. E., Kelly, P., Casey, P. J. Identification of a role for-catenin in the establishment of a bipolar mitotic spindle. J. Biol. Chem. 279, 10829-10832 (2004).
57. Ritchey, L., Ottman, R., Roumanos, M., Chakrabarti, R. A functional cooperativity between Aurora A kinase and LIM kinase1: Implication in the mitotic process. Cell Cycle 11, 296-309 (2012).
58. Lemullois, M., Klotz, C., Sandoz, D. Immunocytochemical localization of myosin during ciliogenesis of quail oviduct. Eur. J. Cell Biol. 43, 429-437 (1987).
59. Espreafico, E. M. et al. Localization of myosin-V in the centrosome. Proc. Natl Acad. Sci. USA 95, 8636-8641 (1998).
60. Lawo, S., Hasegan, M., Gupta, G. D., Pelletier, L. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat. Cell Biol. 14, 1-13 (2012).
61. Mennella, V. et al. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 14, 1159-1168 (2012).
62. Burke, T. A. et al. Homeostatic actin cytoskeleton networks are regulated by assembly factor competition for monomers. Curr. Biol. 24, 579-585 (2014).
63. Sillibourne, J. E. et al. Autophosphorylation of polo-like kinase 4 and its role in centriole duplication. Mol. Biol. Cell 21, 547-561 (2010).
64. Dubois, T. et al. Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics. Nat. Cell Biol. 7, 353-364 (2005).
65. Moudjou, M., Bornens, M. in Cell Biology: A Laboratory Handbook (ed. Celis, J.) 111-119 (Academic Press, 1998).
66. Shelanski, M. Chemistry of the filaments and tubules of brain. J. Histochem. Cytochem. 21, 529-539 (1973).
67. Hyman, A. et al. Preparation of modified tubulins. Methods Enzymol. 196, 478-485 (1991).
68. Michelot, A. et al. Actin-filament stochastic dynamics mediated by ADF/cofilin. Curr. Biol. 17, 825-833 (2007).
69. Achard, V. et al. A 'primer'-based mechanism underlies branched actin filament network formation and motility. Curr. Biol. 20, 423-428 (2010).
70. Casabona, M. G., Vandenbrouck, Y., Attree, I., Couté, Y. Proteomic characterization of Pseudomonas aeruginosa PAO1 inner membrane. Proteomics 13, 2419-2423 (2013).