Dominant Rio1 kinase/ATPase catalytic mutant induces trapping of late pre-40S biogenesis factors in 80S-like ribosomes

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8635-8647

  Ferreira Cerca, Sébastien ^a,b   Kiburu, Irene ^c,d   Thomson, Emma ^a   Laronde, Nicole ^c,d   Hurt, Ed ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c Bldg 142   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (MAGNESIUM); HYDROXYLAMINE; MUTANT PROTEIN; PHOSPHATE P 32; PROTEIN SERINE THREONINE KINASE; RECOMBINANT PROTEIN; RIBOSOME RNA; RIO1 KINASE; RNA 40S; RNA 80S; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME REGULATION; GEL ELECTROPHORESIS; GENE OVEREXPRESSION; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; RIBOSOME; RIBOSOME SUBUNIT; SACCHAROMYCES CEREVISIAE; STRUCTURE ANALYSIS; THIN LAYER CHROMATOGRAPHY; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; ASPARTIC ACID; CATALYTIC DOMAIN; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RIBOSOMES;

EID: 84905563228     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku542     Document Type: Article

References (40)

1. Kressler, D., Hurt, E. and Bassler, J. (2009) Driving ribosome assembly. Biochim. Biophys. Acta, 1803, 673-683.
2. Thomson, E., Ferreira-Cerca, S. and Hurt, E. (2013) Eukaryotic ribosome biogenesis at a glance. J. Cell Sci., 126, 4815-4821.
3. Woolford, J.L. Jr and Baserga, S.J. (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics, 195, 643-681.
4. Esser, D. and Siebers, B. (2013) Atypical protein kinases of the RIO family in archaea. Biochem. Soc. Trans., 41, 399-404.
5. LaRonde-LeBlanc, N. and Wlodawer, A. (2005) A family portrait of the RIO kinases. J. Biol. Chem., 280, 37297-37300.
6. LaRonde-LeBlanc, N. and Wlodawer, A. (2005) The RIO kinases: an atypical protein kinase family required for ribosome biogenesis and cell cycle progression. Biochim. Biophys. Acta, 1754, 14-24.
7. Laronde, N.A. (2014) The Ancient Microbial RIO Kinases. J. Biol. Chem., 289, 9488-9492.
8. Angermayr, M., Roidl, A. and Bandlow, W. (2002) Yeast Rio1p is the founding member of a novel subfamily of protein serine kinases involved in the control of cell cycle progression. Mol. Microbiol., 44, 309-324.
9. Baumas, K., Soudet, J., Caizergues-Ferrer, M., Faubladier, M., Henry, Y. andMougin, A. (2012) Human RioK3 is a novel component of cytoplasmic pre-40S pre-ribosomal particles. RNA Biol., 9, 162-174.
10. Geerlings, T.H., Faber, A.W., Bister, M.D., Vos, J.C. and Raue, H.A. (2003) Rio2p, an evolutionarily conserved, low abundant protein kinase essential for processing of 20 S Pre-rRNA in Saccharomyces cerevisiae. J. Biol. Chem., 278, 22537-22545.
11. Vanrobays, E., Gelugne, J.P., Gleizes, P.E. and Caizergues-Ferrer, M. (2003) Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol. Cell. Biol., 23, 2083-2095.
12. Vanrobays, E., Gleizes, P.E., Bousquet-Antonelli, C., Noaillac-Depeyre, J., Caizergues-Ferrer, M. and Gelugne, J.P. (2001) Processing of 20S pre-rRNA to 18S ribosomal RNA in yeast requires Rrp10p, an essential non-ribosomal cytoplasmic protein. EMBO J., 20, 4204-4213.
13. Widmann, B., Wandrey, F., Badertscher, L., Wyler, E., Pfannstiel, J., Zemp, I. and Kutay, U. (2011) The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Mol. Biol. Cell, 23, 22-35.
14. 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.
15. Read, R.D., Fenton, T.R., Gomez, G.G., Wykosky, J., Vandenberg, S.R., Babic, I., Iwanami, A., Yang, H., Cavenee, W.K., Mischel, P.S. et al. (2013) A kinome-wide RNAi screen in Drosophila Glia reveals that the RIO kinases mediate cell proliferation and survival through TORC2-Akt signaling in glioblastoma. PLoS Genet., 9, e1003253.
16. Wyler, E., Zimmermann, M., Widmann, B., Gstaiger, M., Pfannstiel, J., Kutay, U. and Zemp, I. (2010) Tandem affinity purification combined with inducible shRNA expression as a tool to study the maturation of macromolecular assemblies. RNA, 17, 189-200.
17. Ferreira-Cerca, S., Sagar, V., Schafer, 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.
18. 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.
19. Kuhlbrandt, W. (2004) Biology, structure and mechanism of P-type ATPases. Nat. Rev. Mol. Cell Biol., 5, 282-295.
20. Amlacher, S., Sarges, P., Flemming, D., van Noort, V., Kunze, R., Devos, D.P., Arumugam, M., Bork, P. and Hurt, E. (2011) Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell, 146, 277-289.
21. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
22. McCoy, A.J. (2006) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr., 63, 32-41.
23. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
24. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
25. Choi, S.K., Olsen, D.S., Roll-Mecak, A., Martung, A., Remo, K.L., Burley, S.K., Hinnebusch, A.G. and Dever, T.E. (2000) Physical and functional interaction between the eukaryotic orthologs of prokaryotic translation initiation factors IF1 and IF2. Mol. Cell. Biol., 20, 7183-7191.
26. Vilella, M.D., Remacha, M., Ortiz, B.L., Mendez, E. and Ballesta, J.P. (1991) Characterization of the yeast acidic ribosomal phosphoproteins using monoclonal antibodies. Proteins L44/L45 and L44' have different functional roles. Eur. J. Biochem., 196, 407-414.
27. 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.
28. Ferreira-Cerca, S., Poll, G., Gleizes, P.E., Tschochner, H. and Milkereit, P. (2005) Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell, 20, 263-275.
29. Pertschy, B., Schneider, C., Gnadig, M., Schafer, T., Tollervey, D. and Hurt, E. (2009) RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem., 284, 35079-35091.
30. Laronde-Leblanc, N., Guszczynski, T., Copeland, T. and Wlodawer, A. (2005) Structure and activity of the atypical serine kinase Rio1. FEBS J., 272, 3698-3713.
31. Soudet, J., Gelugne, J.P., Belhabich-Baumas, K., Caizergues-Ferrer, M. and Mougin, A. (2009) Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae. EMBO J., 29, 80-92.
32. de la Cruz, J., Iost, I., Kressler, D. and Linder, P. (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A., 94, 5201-5206.
33. Deloche, O., de la Cruz, J., Kressler, D., Doere, M. and Linder, P. (2004) A membrane transport defect leads to a rapid attenuation of translation initiation in Saccharomyces cerevisiae. Mol. Cell, 13, 357-366.
34. Dong, J., Lai, R., Nielsen, K., Fekete, C.A., Qiu, H. and Hinnebusch, A.G. (2004) The essential ATP-binding cassette protein RLI1 functions in translation by promoting preinitiation complex assembly. J. Biol. Chem., 279, 42157-42168.
35. Valasek, L., Nielsen, K.H. and Hinnebusch, A.G. (2002) Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo. EMBO J., 21, 5886-5898.
36. Lebaron, S., Schneider, C., van Nues, R.W., Swiatkowska, A., Walsh, D., Bottcher, 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.
37. Ferreira-Cerca, S., Poll, G., Kuhn, H., Neueder, A., Jakob, S., Tschochner, H. and Milkereit, P. (2007) Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol. Cell, 28, 446-457.
38. Kappel, L., Loibl, M., Zisser, G., Klein, I., Fruhmann, G., Gruber, C., Unterweger, S., Rechberger, G., Pertschy, B. and Bergler, H. (2012) Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J. Cell Biol., 199, 771-782.
39. Matsuo, Y., Granneman, S., Thoms, M., Manikas, R.G., Tollervey, D. and Hurt, E. (2013) Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature, 505, 112-116.
40. Granneman, S., Petfalski, E., Swiatkowska, A. and Tollervey, D. (2010) Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J., 29, 2026-2036.