The H/ACA RNP assembly factor SHQ1 functions as an RNA mimic

Genes and Development

Volumn 25, Issue 22, 2011, Pages 23982408-

  Walbott, Hélène ^a,f   Machado Pinilla, Rosario ^b   Liger, Dominique ^a   Blaud, Magali ^c   Réty, Stéphane ^c   Grozdanov, Petar N ^b,g   Godin, Kate ^d,e,h   van Tilbeurgh, Herman ^a   Varani, Gabriele ^d,e   Thomas Meier, U ^b   Leulliot, Nicolas ^c  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^g TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^h MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

H ACA RNPs; Ribonucleoprotein assembly; Telomerase; X linked dyskeratosis congenita

Indexed keywords

BINDING PROTEIN; DYSKERIN; PEPTIDES AND PROTEINS; PROTEIN CBF5P; PROTEIN SHQ1; RIBONUCLEOPROTEIN; RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL VIABILITY; CRYSTAL STRUCTURE; DYSKERATOSIS CONGENITA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; YEAST;

EID: 81255142796     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.176834.111     Document Type: Article

References (60)

1. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci 98: 10037-10041.
2. Blaha G, Stanley RE, Steitz TA. 2009. Formation of the first peptide bond: The structure of EF-P bound to the 70S ribosome. Science 325: 966-970.
3. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, Bricogne G. 2004. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60: 2210-2221.
4. Brodersen DE, Ramakrishnan V. 2003. Shape can be seductive. Nat Struct Mol Biol 10: 78-80.
5. Bullinger L, KrÖnke J, SchÖn C, Radtke I, Urlbauer K, Botzenhardt U, Gaidzik V, Carió A, Senger C, Schlenk RF, et al. 2010. Identification of acquired copy number alterations and uniparental disomies in cytogenetically normal acute myeloid leukemia using high-resolution single-nucleotide polymorphism analysis. Leukemia 24: 438-449.
6. Chadwick N, Zeef L, Portillo V, Fennessy C, Warrander F, Hoyle S, Buckle A-M. 2009. Identification of novel Notch target genes in T cell leukaemia. Mol Cancer 8: 35. doi: 10.1186/ 1476-4598-8-35.
7. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
8. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011.
9. Darzacq X, Kittur N, Roy S, Shav-Tal Y, Singer RH, Meier UT. 2006. Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J Cell Biol 173: 207-218.
10. Dez C, Henras A, Faucon B, Lafontaine D, Caizergues-Ferrer M, Henry Y. 2001. Stable expression in yeast of the mature form of human telomerase RNA depends on its association with the box H/ACA small nucleolar RNP proteins Cbf5p, Nhp2p and Nop10p. Nucleic Acids Res 29: 598-603.
11. Dez C, Noaillac-Depeyre J, Caizergues-Ferrer M, Henry Y. 2002. Naf1p, an essential nucleoplasmic factor specifically required for accumulation of box H/ACA small nucleolar RNPs. Mol Cell Biol 22: 7053-7065.
12. Duan J, Li L, Lu J, Wang W, Ye K. 2009. Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase. Mol Cell 34: 427-439.
13. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
14. Eswar N, Eramian D, Webb B, Shen M-Y, Sali A. 2008. Protein structure modeling with MODELLER. Methods Mol Biol 426: 145-159.
15. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
16. Fatica A, Dlakić M, Tollervey D. 2002. Naf1p is a box H/ACA snoRNP assembly factor. RNA 8: 1502-1514.
17. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz H-R, Ceric G, Forslund K, Eddy SR, Sonnhammer ELL, et al. 2008. The Pfam protein families database. Nucleic Acids Res 36: D281-D288. doi: 10.1093/nar/gkm960.
18. Gao Y-G, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V. 2009. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326: 694-699.
19. Godin KS, Walbott H, Leulliot N, van Tilbeurgh H, Varani G. 2009. The box H/ACA snoRNP assembly factor Shq1p is a chaperone protein homologous to Hsp90 cochaperones that binds to the Cbf5p enzyme. J Mol Biol 390: 231-244.
20. Graille M, Mora L, Buckingham RH, van Tilbeurgh H, de Zamaroczy M. 2004. Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO J 23: 1474-1482.
21. Grozdanov PN, Roy S, Kittur N, Meier UT. 2009a. SHQ1 is required prior to NAF1 for assembly of H/ACA small nucleolar and telomerase RNPs. RNA 15: 1188-1197.
22. Grozdanov PN, Fernandez-Fuentes N, Fiser A, Meier UT. 2009b. Pathogenic NAP57 mutations decrease ribonucleoprotein assembly in dyskeratosis congenita. Hum Mol Genet 18: 4546-4551.
23. Heiss NS, Knight SW, Vulliamy TJ, Klauck SM, Wiemann S, Mason PJ, Poustka A, Dokal I. 1998. X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat Genet 19: 32-38.
24. Henras A, Henry Y, Bousquet-Antonelli C, Noaillac-Depeyre J, Gélugne JP, Caizergues-Ferrer M. 1998. Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J 17: 7078-7090.
25. Hoareau-Aveilla C, Bonoli M, Caizergues-Ferrer M, Henry Y. 2006. hNaf1 is required for accumulation of human box H/ACA snoRNPs, scaRNPs, and telomerase. RNA 12: 832-840.
26. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, et al. 2009. InterPro: The integrative protein signature database. Nucleic Acids Res 37: D211-D215. doi: 10.1093/nar/gkn785.
27. Jin H, Loria JP, Moore PB. 2007. Solution structure of an rRNA substrate bound to the pseudouridylation pocket of a box H/ACA snoRNA. Mol Cell 26: 205-215.
28. King TH, Liu B, McCully RR, Fournier MJ. 2003. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell 11: 425-435.
29. Kirwan M, Dokal I. 2008. Dyskeratosis congenita: A genetic disorder of many faces. Clin Genet 73: 103-112.
30. Kiss T. 2004. Biogenesis of small nuclear RNPs. J Cell Sci 117: 5949-5951.
31. Kiss T, Fayet-Lebaron E, Jády BE. 2010. Box H/ACA small ribonucleoproteins. Mol Cell 37: 597-606.
32. Kobayashi K, Kikuno I, Kuroha K, Saito K, Ito K, Ishitani R, Inada T, Nureki O. 2010. Structural basis for mRNA surveillance by archaeal Pelota and GTP-bound EF1a complex. Proc Natl Acad Sci 107: 17575-17579.
33. Lafontaine DLJ, Bousquet-Antonelli C, Henry Y, Caizergues-Ferrer M, Tollervey D. 1998. The box H+ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase. Genes Dev 12: 527-537.
34. Leslie AGW. 1992. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESFEAMCB Newsletter on Protein Crystallography 26.
35. Leulliot N, Godin KS, Hoareau-Aveilla C, Quevillon-Cheruel S, Varani G, Henry Y, van Tilbeurgh H. 2007. The box H/ACA RNP assembly factor Naf1p contains a domain homologous to Gar1p mediating its interaction with Cbf5p. J Mol Biol 371: 1338-1353.
36. Li H. 2008. Unveiling substrate RNA binding to H/ACA RNPs: One side fits all. Curr Opin Struct Biol 18: 78-85.
37. Li L, Ye K. 2006. Crystal structure of an H/ACA box ribonucleoprotein particle. Nature 443: 302-307.
38. Liang B, Zhou J, Kahen E, Terns RM, Terns MP, Li H. 2009. Structure of a functional ribonucleoprotein pseudouridine synthase bound to a substrate RNA. Nat Struct Mol Biol 16: 740-746.
39. Lukowiak AA, Narayanan A, Li ZH, Terns RM, Terns MP. 2001. The snoRNA domain of vertebrate telomerase RNA functions to localize the RNA within the nucleus. RNA 7: 1833-1844.
40. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
41. Meier UT. 2005. The many facets of H/ACA ribonucleoproteins. Chromosoma 114: 1-14.
42. Mitchell JR, Cheng J, Collins K. 1999. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 39 end. Mol Cell Biol 19: 567-576.
43. Muller S, Fourmann J-B, Loegler C, Charpentier B, Branlant C. 2007. Identification of determinants in the protein partners aCBF5 and aNOP10 necessary for the tRNA:C55-synthase and RNA-guided RNA:C-synthase activities. Nucleic Acids Res 35: 5610-5624.
44. Nakamura Y, Ito K. 2003. Making sense of mimic in translation termination. Trends Biochem Sci 28: 99-105.
45. Normand C, Capeyrou R, Quevillon-Cheruel S, Mougin A, Henry Y, Caizergues-Ferrer M. 2006. Analysis of the binding of the N-terminal conserved domain of yeast Cbf5p to a box H/ACA snoRNA. RNA 12: 1868-1882.
46. Rashid R, Liang B, Baker DL, Youssef OA, He Y, Phipps K, Terns RM, Terns MP, Li H. 2006. Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol Cell 21: 249-260.
47. Schneider TR, Sheldrick GM. 2002. Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58: 1772-1779.
48. Singh M, Gonzales FA, Cascio D, Heckmann N, Chanfreau G, Feigon J. 2009. Structure and functional studies of the CS domain of the essential H/ACA ribonucleoparticle assembly protein SHQ1. J Biol Chem 284: 1906-1916.
49. Song H, Mugnier P, Das AK, Webb HM, Evans DR, Tuite MF, Hemmings BA, Barford D. 2000. The crystal structure of human eukaryotic release factor eRF1-Mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100: 311-321.
50. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, et al. 2010. Integrative genomic profiling of human prostate cancer. Cancer Cell 18: 11-22.
51. van den Elzen AMG, Henri J, Lazar N, Gas ME, Durand D, Lacroute F, Nicaise M, van Tilbeurgh H, Séraphin B, Graille M. 2010. Dissection of Dom34-Hbs1 reveals independent functions in two RNA quality control pathways. Nat Struct Mol Biol 17: 1446-1452.
52. Vulliamy TJ, Marrone A, Knight SW, Walne A, Mason PJ, Dokal I. 2006. Mutations in dyskeratosis congenita: Their impact on telomere length and the diversity of clinical presentation. Blood 107: 2680-2685.
53. Weixlbaumer A, Jin H, Neubauer C, Voorhees RM, Petry S, Kelley AC, Ramakrishnan V. 2008. Insights into translational termination from the structure of RF2 bound to the ribosome. Science 322: 953-956.
54. Yang Y, Isaac C, Wang C, Dragon F, Pogacic V, Meier UT. 2000. Conserved composition of mammalian box H/ACA and box C/D small nucleolar ribonucleoprotein particles and their interaction with the common factor Nopp140. Mol Biol Cell 11: 567-577.
55. Yang PK, Rotondo G, Porras T, Legrain P, Chanfreau G. 2002. The Shq1p.Naf1p complex is required for box H/ACA small nucleolar ribonucleoprotein particle biogenesis. J Biol Chem 277: 45235-45242.
56. Ye K. 2007. H/ACA guide RNAs, proteins and complexes. Curr Opin Struct Biol 17: 287-292.
57. Yu YT, Shu MD, Steitz JA. 1998. Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J 17: 5783-5795.
58. Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, Costanzo M, Brost RL, Boone C, Hughes TR, et al. 2008. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol 180: 563-578.
59. Zhou J, Liang B, Li H. 2011. Structural and functional evidence of high specificity of Cbf5 for ACA trinucleotide. RNA 17: 244-250.
60. Zhu Y, Tomlinson RL, Lukowiak AA, Terns RM, Terns MP. 2004. Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol Biol Cell 15: 81-90.