Ccdc13 is a novel human centriolar satellite protein required for ciliogenesis and genome stability

Journal of Cell Science

Volumn 127, Issue 13, 2014, Pages 2910-2919

  Staples, Christopher J ^a   Myers, Katie N ^a   Beveridge, Ryan D D ^a   Patil, Abhijit A ^a   Howard, Anna E ^a   Barone, Giancarlo ^a   Lee, Alvin J X ^b   Swanton, Charles ^b   Howell, Michael ^c   Maslen, Sarah ^d   Skehel, J Mark ^d   Boulton, Simon J ^e   Collis, Spencer J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c CRUK London Research Institute   (United Kingdom)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^e London Research Institute   (United Kingdom)

Author keywords

Ccdc13; Centriolar satellites; Ciliogenesis; Genome stability

Indexed keywords

ALPHA TUBULIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; COILED COIL DOMAIN CONTAINING PROTEIN 13; GAMMA TUBULIN; HISTONE H2AX; MESSENGER RNA; PERICENTRIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN;

ANAPHASE; ARTICLE; CENTRIOLE; DNA DAMAGE; DNA END JOINING REPAIR; EUKARYOTIC FLAGELLUM; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENOMIC INSTABILITY; INTERPHASE; KINETOSOME; M PHASE CELL CYCLE CHECKPOINT; METAPHASE; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; MITOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; GENETIC TRANSFECTION; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY;

CELL CYCLE PROTEINS; CENTRIOLES; CILIA; GENOMIC INSTABILITY; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HUMANS; TRANSFECTION;

EID: 84903789507     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.147785     Document Type: Article

References (36)

1. Balczon, R., Bao, L. and Zimmer, W. E. (1994). PCM-1, A 228-kD centrosome autoantigen with a distinct cell cycle distribution. J. Cell Biol. 124, 783-793.
2. Bärenz, F., Mayilo, D. and Gruss, O. J. (2011). Centriolar satellites: busy orbits around the centrosome. Eur. J. Cell Biol. 90, 983-989.
3. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M. B., Bartek, J. and Lukas, J. (2006). Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173, 195-206.
4. Bonner, W. M., Redon, C. E., Dickey, J. S., Nakamura, A. J., Sedelnikova, O. A., Solier, S. and Pommier, Y. (2008). GammaH2AX and cancer. Nat. Rev. Cancer 8, 957-967.
5. Chaki, M., Airik, R., Ghosh, A. K., Giles, R. H., Chen, R., Slaats, G. G., Wang, H., Hurd, T. W., Zhou, W., Cluckey, A. et al. (2012). Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling. Cell 150, 533-548.
6. Chapman, J. R., Taylor, M. R. and Boulton, S. J. (2012). Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47, 497-510.
7. Chavali, P. L. and Gergely, F. (2013). Cilia born out of shock and stress. EMBO J. 32, 3011-3013.
8. Choi, H. J., Lin, J. R., Vannier, J. B., Slaats, G. G., Kile, A. C., Paulsen, R. D., Manning, D. K., Beier, D. R., Giles, R. H., Boulton, S. J. et al. (2013). NEK8 links the ATR-regulated replication stress response and S phase CDK activity to renal ciliopathies. Mol. Cell 51, 423-439.
9. Dammermann, A. and Merdes, A. (2002). Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159, 255-266.
10. Dictenberg, J. B., Zimmerman, W., Sparks, C. A., Young, A., Vidair, C., Zheng, Y., Carrington, W., Fay, F. S. and Doxsey, S. J. (1998). Pericentrin and gamma-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J. Cell Biol. 141, 163-174.
11. Giunta, S., Belotserkovskaya, R. and Jackson, S. P. (2010). DNA damage signaling in response to double-strand breaks during mitosis. J. Cell Biol. 190, 197-207.
12. Griffith, E., Walker, S., Martin, C. A., Vagnarelli, P., Stiff, T., Vernay, B., Al Sanna, N., Saggar, A., Hamel, B., Earnshaw, W. C. et al. (2008). Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat. Genet. 40, 232-236.
13. Janssen, A., van der Burg, M., Szuhai, K., Kops, G. J. and Medema, R. H. (2011). Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333, 1895-1898.
14. Kalay, E., Yigit, G., Aslan, Y., Brown, K. E., Pohl, E., Bicknell, L. S., Kayserili, H., Li, Y., Tüysüz, B., Nürnberg, G. et al. (2011). CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat. Genet. 43, 23-26.
15. Kim, K. and Rhee, K. (2011). The pericentriolar satellite protein CEP90 is crucial for integrity of the mitotic spindle pole. J. Cell Sci. 124, 338-347.
16. Kim, J. C., Badano, J. L., Sibold, S., Esmail, M. A., Hill, J., Hoskins, B. E., Leitch, C. C., Venner, K., Ansley, S. J., Ross, A. J. et al. (2004). The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet. 36, 462-470.
17. Kim, J., Krishnaswami, S. R. and Gleeson, J. G. (2008). CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet. 17, 3796-3805.
18. Kim, K., Lee, K. and Rhee, K. (2012). CEP90 is required for the assembly and centrosomal accumulation of centriolar satellites, which is essential for primary cilia formation. PLoS ONE 7, e48196.
19. Kodani, A., Tonthat, V., Wu, B. and Sütterlin, C. (2010). Par6 alpha interacts with the dynactin subunit p150 Glued and is a critical regulator of centrosomal protein recruitment. Mol. Biol. Cell 21, 3376-3385.
20. Lee, S. and Rhee, K. (2010). CEP215 is involved in the dynein-dependent accumulation of pericentriolar matrix proteins for spindle pole formation. Cell Cycle 9, 775-784.
21. Logan, C. V., Abdel-Hamed, Z. and Johnson, C. A. (2011). Molecular genetics and pathogenic mechanisms for the severe ciliopathies: insights into neurodevelopment and pathogenesis of neural tube defects. Mol. Neurobiol. 43, 12-26.
22. Lopes, C. A., Prosser, S. L., Romio, L., Hirst, R. A., O'Callaghan, C., Woolf, A. S. and Fry, A. M. (2011). Centriolar satellites are assembly points for proteins implicated in human ciliopathies, including oral-facial-digital syndrome 1. J. Cell Sci. 124, 600-612.
23. Ma, L. and Jarman, A. P. (2011). Dilatory is a Drosophila protein related to AZI1 (CEP131) that is located at the ciliary base and required for cilium formation. J. Cell Sci. 124, 2622-2630.
24. Malicki, J., Avanesov, A., Li, J., Yuan, S. and Sun, Z. (2011). Analysis of cilia structure and function in zebrafish. Methods Cell Biol. 101, 39-74.
25. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R., III, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007). ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166.
26. Mogensen, M. M., Malik, A., Piel, M., Bouckson-Castaing, V. and Bornens, M. (2000). Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J. Cell Sci. 113, 3013-3023.
27. Nachury, M. V. (2008). Tandem affinity purification of the BBSome, a critical regulator of Rab8 in ciliogenesis. Methods Enzymol. 439, 501-513.
28. Prosser, S. L., Straatman, K. R. and Fry, A. M. (2009). Molecular dissection of the centrosome overduplication pathway in S-phase-arrested cells. Mol. Cell. Biol. 29, 1760-1773.
29. Sivasubramaniam, S., Sun, X., Pan, Y. R., Wang, S. and Lee, E. Y. (2008). Cep164 is a mediator protein required for the maintenance of genomic stability through modulation of MDC1, RPA, and CHK1. Genes Dev. 22, 587-600.
30. Smith, E., Dejsuphong, D., Balestrini, A., Hampel, M., Lenz, C., Takeda, S., Vindigni, A. and Costanzo, V. (2009). An ATM-and ATR-dependent checkpoint inactivates spindle assembly by targeting CEP63. Nat. Cell Biol. 11, 278-285.
31. Staples, C. J., Myers, K. N., Beveridge, R. D., Patil, A. A., Lee, A. J., Swanton, C., Howell, M., Boulton, S. J. and Collis, S. J. (2012). The centriolar satellite protein Cep131 is important for genome stability. J. Cell Sci. 125, 4770-4779.
32. Stiff, T., Alagoz, M., Alcantara, D., Outwin, E., Brunner, H. G., Bongers, E. M., O'Driscoll, M. and Jeggo, P. A. (2013). Deficiency in origin licensing proteins impairs cilia formation: implications for the aetiology of Meier-Gorlin syndrome. PLoS Genet. 9, e1003360.
33. Stowe, T. R., Wilkinson, C. J., Iqbal, A. and Stearns, T. (2012). The centriolar satellite proteins Cep72 and Cep290 interact and are required for recruitment of BBS proteins to the cilium. Mol. Biol. Cell 23, 3322-3335.
34. Valdés-Sánchez, L., De la Cerda, B., Diaz-Corrales, F. J., Massalini, S., Chakarova, C. F., Wright, A. F. and Bhattacharya, S. S. (2013). ATR localizes to the photoreceptor connecting cilium and deficiency leads to severe photoreceptor degeneration in mice. Hum. Mol. Genet. 22, 1507-1515.
35. Yan, X., Habedanck, R. and Nigg, E. A. (2006). A complex of two centrosomal proteins, CAP350 and FOP, cooperates with EB1 in microtubule anchoring. Mol. Biol. Cell 17, 634-644.
36. Zhou, W., Otto, E. A., Cluckey, A., Airik, R., Hurd, T. W., Chaki, M., Diaz, K., Lach, F. P., Bennett, G. R., Gee, H. Y. et al. (2012). FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 44, 910-915.