CK1δ and CK1ε are components of human 40S subunit precursors required for cytoplasmic 40S maturation

Journal of Cell Science

Volumn 127, Issue 6, 2014, Pages 1242-1253

  Zemp, Ivo ^a   Wandrey, Franziska ^a,b   Rao, Sanjana ^a   Ashiono, Caroline ^a   Wyler, Emanuel ^a,b,c   Montellese, Christian ^a,b   Kutay, Ulrike ^a  

^a ETH ZURICH   (Switzerland)

^b Zurich PhD Program in Molecular Life Sciences   (Switzerland)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

CK1 ; CK1 ; Pre 40S maturation; Protein kinase; Ribosome biogenesis

Indexed keywords

CASEIN KINASE IDELTA; CASEIN KINASE IEPSILON; DACTINOMYCIN; EXPORTIN 1; NUCLEAR PROTEIN; RNA 18S; RNA PRECURSOR; SMALL INTERFERING RNA; TRANS ACTING FACTOR; BYSL PROTEIN, HUMAN; CELL ADHESION MOLECULE; PROTEIN PRECURSOR; PROTEIN SUBUNIT; RIBOSOME RNA; TRANSACTIVATOR PROTEIN;

ARTICLE; AUTOPHOSPHORYLATION; BIOGENESIS; CELL MATURATION; CONTROLLED STUDY; CYTOPLASM; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RIBOSOME SUBUNIT; RNA INTERFERENCE; RNA PROCESSING; RNA TRANSLATION; STEADY STATE; SUCROSE GRADIENT; WESTERN BLOTTING; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SUBUNIT; PROTEIN TRANSPORT; SMALL RIBOSOMAL SUBUNIT;

CASEIN KINASE IDELTA; CASEIN KINASE IEPSILON; CELL ADHESION MOLECULES; CYTOPLASM; HEK293 CELLS; HELA CELLS; HUMANS; PHOSPHORYLATION; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA, RIBOSOMAL; TRANS-ACTIVATORS;

EID: 84903367072     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.138719     Document Type: Article

References (42)

1. Badura, L., Swanson, T., Adamowicz, W., Adams, J., Cianfrogna, J., Fisher, K., Holland, J., Kleiman, R., Nelson, F., Reynolds, L. et al. (2007). An inhibitor of casein kinase I epsilon induces phase delays in circadian rhythms under freerunning and entrained conditions. J. Pharmacol. Exp. Ther. 322, 730-738.
2. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R. and Cohen, P. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315.
3. Basu, U., Si, K., Warner, J. R. and Maitra, U. (2001). The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 21, 1453-1462.
4. Baumas, K., Soudet, J., Caizergues-Ferrer, M., Faubladier, M., Henry, Y. and Mougin, A. (2012). Human RioK3 is a novel component of cytoplasmic pre-40S pre-ribosomal particles. RNA Biol. 9, 162-174.
5. Behrend, L., Milne, D. M., Stöter, M., Deppert, W., Campbell, L. E., Meek, D. W. and Knippschild, U. (2000). IC261, a specific inhibitor of the protein kinases casein kinase 1-delta and-epsilon, triggers the mitotic checkpoint and induces p53-dependent postmitotic effects. Oncogene 19, 5303-5313.
6. Biswas, A., Mukherjee, S., Das, S., Shields, D., Chow, C. W. and Maitra, U. (2011). Opposing action of casein kinase 1 and calcineurin in nucleocytoplasmic shuttling of mammalian translation initiation factor eIF6. J. Biol. Chem. 286, 3129-3138.
7. Bryja, V., Schulte, G. and Arenas, E. (2007). Wnt-3a utilizes a novel low dose and rapid pathway that does not require casein kinase 1-mediated phosphorylation of Dvl to activate beta-catenin. Cell. Signal. 19, 610-616.
8. Carron, C., O'Donohue, M. F., Choesmel, V., Faubladier, M. and Gleizes, P. E. (2011). Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals. Nucleic Acids Res. 39, 280-291.
9. Cheong, J. K. and Virshup, D. M. (2011). Casein kinase 1: Complexity in the family. Int. J. Biochem. Cell Biol. 43, 465-469.
10. Etchegaray, J. P., Machida, K. K., Noton, E., Constance, C. M., Dallmann, R., Di Napoli, M. N., DeBruyne, J. P., Lambert, C. M., Yu, E. A., Reppert, S. M. et al. (2009). Casein kinase 1 delta regulates the pace of the mammalian circadian clock. Mol. Cell. Biol. 29, 3853-3866.
11. Ferreira-Cerca, S., Sagar, V., Schäfer, T., Diop, M., Wesseling, A. M., Lu, H., Chai, E., Hurt, E. and LaRonde-LeBlanc, N. (2012). ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit. Nat. Struct. Mol. Biol. 19, 1316-1323.
12. Fish, K. J., Cegielska, A., Getman, M. E., Landes, G. M. and Virshup, D. M. (1995). Isolation and characterization of human casein kinase I epsilon (CKI), a novel member of the CKI gene family. J. Biol. Chem. 270, 14875-14883.
13. Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. (2003). Ribosome assembly in eukaryotes. Gene 313, 17-42.
14. Greer, Y. E. and Rubin, J. S. (2011). Casein kinase 1 delta functions at the centrosome to mediate Wnt-3a-dependent neurite outgrowth. J. Cell Biol. 192, 993-1004.
15. Gross, S. D. and Anderson, R. A. (1998). Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell. Signal. 10, 699-711.
16. Henras, A. K., Soudet, J., Gérus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008). The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65, 2334-2359.
17. Jouffe, C., Cretenet, G., Symul, L., Martin, E., Atger, F., Naef, F. and Gachon, F. (2013). The circadian clock coordinates ribosome biogenesis. PLoS Biol. 11, e1001455.
18. Knippschild, U., Milne, D. M., Campbell, L. E., DeMaggio, A. J., Christenson, E., Hoekstra, M. F. and Meek, D. W. (1997). p53 is phosphorylated in vitro and in vivo by the delta and epsilon isoforms of casein kinase 1 and enhances the level of casein kinase 1 delta in response to topoisomerase-directed drugs. Oncogene 15, 1727-1736.
19. Knippschild, U., Gocht, A., Wolff, S., Huber, N., Löhler, J. and Stöter, M. (2005). The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell. Signal. 17, 675-689.
20. Kressler, D., Hurt, E. and Bassler, J. (2010). Driving ribosome assembly. Biochim. Biophys. Acta 1803, 673-683.
21. Lamanna, A. C. and Karbstein, K. (2011). An RNA conformational switch regulates pre-18S rRNA cleavage. J. Mol. Biol. 405, 3-17.
22. Lebaron, S., Schneider, C., van Nues, R. W., Swiatkowska, A., Walsh, D., Böttcher, B., Granneman, S., Watkins, N. J. and Tollervey, D. (2012). Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol. 19, 744-753.
23. Lee, C., Etchegaray, J. P., Cagampang, F. R., Loudon, A. S. and Reppert, S. M. (2001). Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855-867.
24. Lee, J. W., Hirota, T., Peters, E. C., Garcia, M., Gonzalez, R., Cho, C. Y., Wu, X., Schultz, P. G. and Kay, S. A. (2011). A small molecule modulates circadian rhythms through phosphorylation of the period protein. Angew. Chem. Int. Ed. Engl. 50, 10608-10611.
25. Mashhoon, N., DeMaggio, A. J., Tereshko, V., Bergmeier, S. C., Egli, M., Hoekstra, M. F. and Kuret, J. (2000). Crystal structure of a conformationselective casein kinase-1 inhibitor. J. Biol. Chem. 275, 20052-20060.
26. Milne, D. M., Looby, P. and Meek, D. W. (2001). Catalytic activity of protein kinase CK1 delta (casein kinase 1delta) is essential for its normal subcellular localization. Exp. Cell Res. 263, 43-54.
27. Panse, V. G. and Johnson, A. W. (2010). Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci. 35, 260-266.
28. Peters, J. M., McKay, R. M., McKay, J. P. and Graff, J. M. (1999). Casein kinase I transduces Wnt signals. Nature 401, 345-350.
29. Rena, G., Bain, J., Elliott, M. and Cohen, P. (2004). D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Rep. 5, 60-65.
30. Rouquette, J., Choesmel, V. and Gleizes, P. E. (2005). Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J. 24, 2862-2872.
31. Schäfer, T., Maco, B., Petfalski, E., Tollervey, D., Böttcher, B., Aebi, U. and Hurt, E. (2006). Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441, 651-655.
32. Sloan, K. E., Mattijssen, S., Lebaron, S., Tollervey, D., Pruijn, G. J. andWatkins, N. J. (2013). Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell Biol. 200, 577-588.
33. Strunk, B. S., Loucks, C. R., Su, M., Vashisth, H., Cheng, S., Schilling, J., Brooks, C. L., III, Karbstein, K. and Skiniotis, G. (2011). Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333, 1449-1453.
34. Strunk, B. S., Novak, M. N., Young, C. L. and Karbstein, K. (2012). A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150, 111-121.
35. Tschochner, H. and Hurt, E. (2003). Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13, 255-263.
36. Walton, K. M., Fisher, K., Rubitski, D., Marconi, M., Meng, Q. J., Sládek, M., Adams, J., Bass, M., Chandrasekaran, R., Butler, T. et al. (2009). Selective inhibition of casein kinase 1 epsilon minimally alters circadian clock period. J. Pharmacol. Exp. Ther. 330, 430-439.
37. Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440.
38. Widmann, B., Wandrey, F., Badertscher, L., Wyler, E., Pfannstiel, J., Zemp, I. and Kutay, U. (2012). The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Mol. Biol. Cell 23, 22-35.
39. Wild, T., Horvath, P., Wyler, E., Widmann, B., Badertscher, L., Zemp, I., Kozak, K., Csucs, G., Lund, E. and Kutay, U. (2010). A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol. 8, e1000522.
40. Wyler, E., Zimmermann, M., Widmann, B., Gstaiger, M., Pfannstiel, J., Kutay, U. and Zemp, I. (2011). Tandem affinity purification combined with inducible shRNA expression as a tool to study the maturation of macromolecular assemblies. RNA 17, 189-200.
41. Zemp, I. and Kutay, U. (2007). Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 581, 2783-2793.
42. Zemp, I., Wild, T., O'Donohue, M. F., Wandrey, F., Widmann, B., Gleizes, P. E. and Kutay, U. (2009). Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 185, 1167-1180.