ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit

Nature Structural and Molecular Biology

Volumn 19, Issue 12, 2012, Pages 1316-1323

  Ferreira Cerca, Sébastien ^a   Sagar, Vatsala ^b   Schäfer, Thorsten ^a,d   Diop, Momar ^b   Wesseling, Anne Maria ^a   Lu, Haiyun ^b   Chai, Eileen ^b   Hurt, Ed ^a   Laronde Leblanc, Nicole ^b,c  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Bldg 142   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM; MAGNESIUM; PHOSPHOTRANSFERASE; POTASSIUM; RIO2 KINASE; SODIUM; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; RIBOSOME;

ADENOSINE TRIPHOSPHATASES; HUMANS; MODELS, MOLECULAR; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMES;

EUKARYOTA;

EID: 84870839593     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2403     Document Type: Article

References (38)

1. Geerlings, T.H., Faber, A.W., Bister, M.D., Vos, J.C. & Raue, H.A. 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 (2003).
2. Vanrobays, E., Gelugne, J.P., Gleizes, P.E. & Caizergues-Ferrer, M. Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol. Cell Biol. 23, 2083-2095 (2003).
3. Schäfer, T., Strauss, D., Petfalski, E., Tollervey, D. & Hurt, E. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 22, 1370-1380 (2003).
4. Henras, A.K. et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol. Life Sci. 65, 2334-2359 (2008).
5. Fromont-Racine, M., Senger, B., Saveanu, C. & Fasiolo, F. Ribosome assembly in eukaryotes. Gene 313, 17-42 (2003).
6. Zemp, I. et al. Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 185, 1167-1180 (2009).
7. Granneman, S., Petfalski, E., Swiatkowska, A. & Tollervey, D. Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J. 29, 2026-2036 (2010).
8. Strunk, B.S. et al. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333, 1449-1453 (2011).
9. LaRonde-LeBlanc, N., Guszczynski, T., Copeland, T. & Wlodawer, A. Autophosphorylation of Archaeoglobus fulgidus Rio2 and crystal structures of its nucleotide-metal ion complexes. FEBS J. 272, 2800-2810 (2005).
10. LaRonde-LeBlanc, N. & Wlodawer, A. Crystal structure of A. fulgidus Rio2 defines a new family of serine protein kinases. Structure 12, 1585-1594 (2004).
11. Amlacher, S. et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146, 277-289 (2011).
12. Post, R.L. & Kume, S. Evidence for an aspartyl phosphate residue at the active site of sodium and potassium ion transport adenosine triphosphatase. J. Biol. Chem. 248, 6993-7000 (1973).
13. Kühlbrandt, W. Biology, structure and mechanism of P-type ATPases. Nat. Rev. Mol. Cell Biol. 5, 282-295 (2004).
14. Hanks, S.K., Quinn, A.M. & Hunter, T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52 (1988).
15. Taylor, S.S. & Kornev, A.P. Protein kinases: evolution of dynamic regulatory proteins. Trends Biochem. Sci. 36, 65-77 (2011).
16. Sanders, D.A., Gillece-Castro, B.L., Stock, A.M., Burlingame, A.L. & Koshland, D.E. Jr. Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J. Biol. Chem. 264, 21770-21778 (1989).
17. Collet, J.F., Stroobant, V., Pirard, M., Delpierre, G. & Van Schaftingen, E. A new class of phosphotransferases phosphorylated on an aspartate residue in an amino-terminal DXDX(T/V) motif. J. Biol. Chem. 273, 14107-14112 (1998).
18. Zheng, J. et al. Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry 32, 2154-2161 (1993).
19. Parang, K. & Cole, P.A. Designing bisubstrate analog inhibitors for protein kinases. Pharmacol. Ther. 93, 145-157 (2002).
20. Schäfer, T. et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441, 651-655 (2006).
21. Aaronson, R.P. & Blobel, G. On the attachment of the nuclear pore complex. J. Cell Biol. 62, 746-754 (1974).
22. Phillips, J.C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).
23. Trabuco, L.G., Villa, E., Mitra, K., Frank, J. & Schulten, K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673-683 (2008).
24. Bishop, A.C., Buzko, O. & Shokat, K.M. Magic bullets for protein kinases. Trends Cell Biol. 11, 167-172 (2001).
25. Palmgren, M.G. & Nissen, P. P-type ATPases. Annu. Rev. Biophys. 40, 243-266 (2011).
26. Ye, Q., Crawley, S.W., Yang, Y., Cote, G.P. & Jia, Z. Crystal structure of the alpha-kinase domain of Dictyostelium myosin heavy chain kinase A. Sci. Signal. 3, ra17 (2010).
27. Xu, W., Doshi, A., Lei, M., Eck, M.J. & Harrison, S.C. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638 (1999).
28. Nagar, B. et al. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112, 859-871 (2003).
29. Malakhova, M. et al. Structural basis for activation of the autoinhibitory C-terminal kinase domain of p90 RSK2. Nat. Struct. Mol. Biol. 15, 112-113 (2008).
30. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 334, 1524-1529 (2011).
31. Janke, C. et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962 (2004).
32. Longtine, M.S. et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (1998).
33. Puig, O. et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218-229 (2001).
34. Peluso, P., Shan, S.O., Nock, S., Herschlag, D. & Walter, P. Role of SRP RNA in the GTPase cycles of Ffh and FtsY. Biochemistry 40, 15224-15233 (2001).
35. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
36. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
37. Delano, W. The Pymol molecular graphics system (Delano Scientific, 2002).
38. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph 14, 33-38, 27-28 (1996).