The C. Elegans F-box proteins LIN-23 and SEL-10 antagonize centrosome duplication by regulating ZYG-1 levels

Journal of Cell Science

Volumn 125, Issue 15, 2012, Pages 3535-3544

  Peel, Nina ^a   Dougherty, Michael ^b   Goeres, Jacqueline ^b   Liu, Yan ^b   O'Connell, Kevin F ^b  

^a The College of New Jersey   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Centrosome; F box; ZYG 1

Indexed keywords

F BOX PROTEIN; LIN 23 PROTEIN; MEMBRANE PROTEIN; PLK4 KINASE; PROTEASOME; SCF UBIQUITIN LIGASE; SEL 10 PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; ZYG 1 PROTEIN;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CARCINOGENESIS; CELL DIVISION; CENTROSOME; CONTROLLED STUDY; DROSOPHILA; ENZYME DEGRADATION; HUMAN; HUMAN CELL; MITOSIS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CENTRIOLES; CENTROSOME; CULLIN PROTEINS; F-BOX PROTEINS; HEK293 CELLS; HUMANS; MALE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SKP CULLIN F-BOX PROTEIN LIGASES;

CAENORHABDITIS ELEGANS;

EID: 84868578981     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.097105     Document Type: Article

References (53)

1. Basto, R., Lau, J., Vinogradova, T., Gardiol, A., Woods, C. G., Khodjakov, A. and Raff, J. W. (2006). Flies without centrioles. Cell 125, 1375-1386.
2. Basto, R., Brunk, K., Vinadogrova, T., Peel, N., Franz, A., Khodjakov, A. and Raff, J. W. (2008). Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042.
3. Brownlee, C. W., Klebba, J. E., Buster, D. W. and Rogers, G. C. (2011). The Protein Phosphatase 2A regulatory subunit Twins stabilizes Plk4 to induce centriole amplification. J. Cell Biol. 195, 231-243.
4. Carvalho-Santos, Z., Machado, P., Branco, P., Tavares-Cadete, F., Rodrigues- Martins, A., Pereira-Leal, J. B. and Bettencourt-Dias, M. (2010). Stepwise evolution of the centriole-assembly pathway. J. Cell Sci. 123, 1414-1426.
5. Cizmecioglu, O., Krause, A., Bahtz, R., Ehret, L., Malek, N. and Hoffmann, I. (2012). Plk2 regulates centriole duplication through phosphorylation-mediated degradation of Fbxw7 (human Cdc4). J. Cell. Sci. 125, 981-992.
6. Cowan, C. R. and Hyman, A. A. (2006). Cyclin E-Cdk2 temporally regulates centrosome assembly and establishment of polarity in Caenorhabditis elegans embryos. Nat. Cell Biol. 8, 1441-1447.
7. Cunha-Ferreira, I., Rodrigues-Martins, A., Bento, I., Riparbelli, M., Zhang, W., Laue, E., Callaini, G., Glover, D. and Bettencourt-Dias, M. (2008). The SCF/Slimb Ubiquitin Ligase Limits Centrosome Amplification through Degradation of SAK/ PLK4. Curr. Biol. 19, 43-49.
8. D'Angiolella, V., Donato, V., Vijayakumar, S., Saraf, A., Florens, L., Washburn, M. P., Dynlacht, B. and Pagano, M. (2010). SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 466, 138-142.
9. Dammermann, A., Maddox, P. S., Desai, A. and Oegema, K. (2008). SAS-4 is recruited to a dynamic structure in newly forming centrioles that is stabilized by the gamma-tubulin-mediated addition of centriolar microtubules. J. Cell Biol. 180, 771-785.
10. Delattre, M., Leidel, S., Wani, K., Baumer, K., Bamat, J., Schnabel, H., Feichtinger, R., Schnabel, R. and Gönczy, P. (2004). Centriolar SAS-5 is required for centrosome duplication in C. elegans. Nat. Cell Biol. 6, 656-664.
11. Delattre, M., Canard, C. and Gönczy, P. (2006). Sequential protein recruitment in C. elegans centriole formation. Curr. Biol. 16, 1844-1849.
12. Ding, M., Chao, D., Wang, G. and Shen, K. (2007). Spatial regulation of an E3 ubiquitin ligase directs selective synapse elimination. Science 317, 947-951.
13. Ganem, N. J., Godinho, S. A. and Pellman, D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282.
14. Greenan, G., Brangwynne, C. P., Jaensch, S., Gharakhani, J., Jülicher, F. and Hyman, A. A. (2010). Centrosome size sets mitotic spindle length in Caenorhabditis elegans embryos. Curr. Biol. 20, 353-358.
15. Guderian, G., Westendorf, J., Uldschmid, A. and Nigg, E. A. (2010). Plk4 trans- autophosphorylation regulates centriole number by controlling betaTrCP-mediated degradation. J. Cell Sci. 123, 2163-2169.
16. Habedanck, R., Stierhof, Y.-D., Wilkinson, C. J. and Nigg, E. A. (2005). The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7, 1140-1146.
17. Hebeisen, M. and Roy, R. (2008). CDC-25.1 stability is regulated by distinct domains to restrict cell division during embryogenesis in C. elegans. Development 135, 1259- 1269.
18. Hodges, M. E., Scheumann, N., Wickstead, B., Langdale, J. A. and Gull, K. (2010). Reconstructing the evolutionary history of the centriole from protein components. J. Cell Sci. 123, 1407-1413.
19. Holland, A. J., Lan, W., Niessen, S., Hoover, H. and Cleveland, D. W. (2010). Polo- like kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J. Cell Biol. 188, 191-198.
20. Hubbard, E. J., Wu, G., Kitajewski, J. and Greenwald, I. (1997). sel-10, a negative regulator of lin-12 activity in Caenorhabditis elegans, encodes a member of the CDC4 family of proteins. Genes Dev. 11, 3182-3193.
21. Jäger, S., Schwartz, H. T., Horvitz, H. R. and Conradt, B. (2004). The Caenorhabditis elegans F-box protein SEL-10 promotes female development and may target FEM-1 and FEM-3 for degradation by the proteasome. Proc. Natl. Acad. Sci. USA 101, 12549-12554.
22. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
23. Kemp, C. A., Song, M. H., Addepalli, M. K., Hunter, G. and O'Connell, K. (2007). Suppressors of zyg-1 define regulators of centrosome duplication and nuclear association in Caenorhabditis elegans. Genetics 176, 95-113.
24. Kipreos, E. T. and Pagano, M. (2000). The F-box protein family. Genome Biol 1. doi:10.1186/gb-2000-1-5-reviews3002.
25. Kitagawa, D., Busso, C., Flückiger, I. and Gönczy, P. (2009). Phosphorylation of SAS-6 by ZYG-1 is critical for centriole formation in C. elegans embryos. Dev. Cell 17, 900-907.
26. Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y.-D. and Nigg, E. A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
27. Koepp, D. M., Schaefer, L. K., Ye, X., Keyomarsi, K., Chu, C., Harper, J. W. and Elledge, S. J. (2001). Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294, 173-177.
28. Korzeniewski, N., Spardy, N., Duensing, A. and Duensing, S. (2011). Genomic instability and cancer: lessons learned from human papillomaviruses. Cancer Lett. 305, 113-122.
29. Leidel, S., Delattre, M., Cerutti, L., Baumer, K. and Gönczy, P. (2005). SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat. Cell Biol. 7, 115-125.
30. Moberg, K. H., Bell, D. W., Wahrer, D. C. R., Haber, D. A. and Hariharan, I. K. (2001). Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413, 311-316.
31. Moberg, K. H., Mukherjee, A., Veraksa, A., Artavanis-Tsakonas, S. and Hariharan, I. K. (2004). The Drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr. Biol. 14, 965-974.
32. Murphy, T. D. (2003). Drosophila skpA, a component of SCF ubiquitin ligases, regulates centrosome duplication independently of cyclin E accumulation. J. Cell Sci. 116, 2321-2332.
33. Nash, P., Tang, X., Orlicky, S., Chen, Q., Gertler, F. B., Mendenhall, M. D., Sicheri, F., Pawson, T. and Tyers, M. (2001). Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414, 514-521.
34. Nayak, S., Santiago, F. E., Jin, H., Lin, D., Schedl, T. and Kipreos, E. T. (2002). The Caenorhabditis elegans Skp1-related gene family: diverse functions in cell proliferation, morphogenesis, and meiosis. Curr. Biol. 12, 277-287.
35. Nigg, E. A. and Raff, J. W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678.
36. O'Connell, K. F., Caron, C., Kopish, K. R., Hurd, D. D., Kemphues, K. J., Li, Y. and White, J. G. (2001). The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105, 547-558.
37. Peel, N., Stevens, N. R., Basto, R. and Raff, J. W. (2007). Overexpressing centriole- replication proteins in vivo induces centriole overduplication and de novo formation. Curr. Biol. 17, 834-843.
38. Pelletier, L., O'Toole, E., Schwager, A., Hyman, A. A. and Müller-Reichert, T. (2006). Centriole assembly in Caenorhabditis elegans. Nature 444, 619-623.
39. Peters, N., Perez, D. E., Song, M. H., Liu, Y., Müller-Reichert, T., Caron, C., Kemphues, K. J. and O'Connell, K. F. (2010). Control of mitotic and meiotic centriole duplication by the Plk4-related kinase ZYG-1. J. Cell Sci. 123, 795-805.
40. Puklowski, A., Homsi, Y., Keller, D., May, M., Chauhan, S., Kossatz, U., Grünwald, V., Kubicka, S., Pich, A., Manns, M. P. et al. (2011). The SCF-FBXW5 E3- ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nat. Cell Biol. 13, 1004-1009.
41. Rajagopalan, H., Jallepalli, P. V., Rago, C., Velculescu, V. E., Kinzler, K. W., Vogelstein, B. and Lengauer, C. (2004). Inactivation of hCDC4 can cause chromosomal instability. Nature 428, 77-81.
42. Reinke, V., Gil, I. S., Ward, S. and Kazmer, K. (2004). Genome-wide germline- enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131, 311-323.
43. Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M. and Rogers, S. L. (2009). The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 184, 225-239.
44. Sillibourne,J.E.,Tack,F.,Vloemans,N.,Boeckx,A.,Thambirajah,S., Bonnet, P., Ramaekers, F. C. S., Bornens, M. and Grand-Perret, T. (2010). Autophosphorylation of polo-like kinase 4 and its role in centriole duplication. Mol. Biol. Cell 21, 547-561.
45. Song, M. H., Aravind, L., Müller-Reichert, T. and O'Connell, K. F. (2008). The conserved protein SZY-20 opposes the Plk4-related kinase ZYG-1 to limit centrosome size. Dev. Cell 15, 901-912.
46. Song, M. H., Liu, Y., Anderson, D. E., Jahng, W. J. and O'Connell, K. F. (2011). Protein phosphatase 2A-SUR-6/B55 regulates centriole duplication in C. elegans by controlling the levels of centriole assembly factors. Dev. Cell 20, 563-571.
47. Strnad, P. and Gönczy, P. (2008). Mechanisms of procentriole formation. Trends Cell Biol. 18, 389-396.
48. Torres, J. Z., Summers, M. K., Peterson, D., Brauer, M. J., Lee, J., Senese, S., Gholkar, A. A., Lo, Y.-C., Lei, X., Jung, K. et al. (2011). The STARD9/Kif16a kinesin associates with mitotic microtubules and regulates spindle pole assembly. Cell 147, 1309-1323.
49. Tsou, M.-F. B. and Stearns, T. (2006). Mechanism limiting centrosome duplication to once per cell cycle. Nature 442, 947-951.
50. Welcker, M. and Clurman, B. E. (2008). FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8, 83- 93.
51. Wu, G., Hubbard, E. J., Kitajewski, J. K. and Greenwald, I. (1998). Evidence for functional and physical association between Caenorhabditis elegans SEL-10, a Cdc4p-related protein, and SEL-12 presenilin. Proc. Natl. Acad. Sci. USA 95, 15787- 15791.
52. Yamanaka, A., Yada, M., Imaki, H., Koga, M., Ohshima, Y. and Nakayama, K.-I. (2002). Multiple Skp1-related proteins in Caenorhabditis elegans: diverse patterns of interaction with Cullins and F-box proteins. Curr. Biol. 12, 267-275.
53. Zhu, F., Lawo, S., Bird, A., Pinchev, D., Ralph, A., Richter, C., Müller-Reichert, T., Kittler, R., Hyman, A. A. and Pelletier, L. (2008). The mammalian SPD-2 ortholog Cep192 regulates centrosome biogenesis. Curr. Biol. 18, 136-141.