Nutritional status modulates box C/D snoRNP biogenesis by regulated subcellular relocalization of the R2TP complex

Genome Biology

Volumn 15, Issue 7, 2014, Pages

  Kakihara, Yoshito ^a   Makhnevych, Taras ^a   Zhao, Liang ^a   Tang, Weiwen ^a   Houry, Walid A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; MULTIPROTEIN COMPLEX; NOP 1 PROTEIN; NOP 56 PROTEIN; NOP 58 PROTEIN; PIH1 PROTEIN; R2TP COMPLEX PROTEIN; RVB1 PROTEIN; RVB2 PROTEIN; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; SMALL NUCLEOLAR RIBONUCLEOPROTEIN BOX C D; SNU 13 PROTEIN; TAH1 PROTEIN; UNCLASSIFIED DRUG; NOP58 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; PIH1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL GROWTH; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; NONHUMAN; NUTRITIONAL STATUS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION, FUNGAL; NUCLEAR PROTEINS; PROTEIN STABILITY; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84919384495     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-014-0404-4     Document Type: Article

References (58)

1. Venema J, Tollervey D: Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 1999, 33:261-311.
2. Warner JR: The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 1999, 24:437-440.
3. Kressler D, Doere M, Rojo M, Linder P: Synthetic lethality with conditional dbp6 alleles identifies rsa1p, a nucleoplasmic protein involved in the assembly of 60S ribosomal subunits. Mol Cell Biol 1999, 19:8633-8645.
4. Butler JS: The yin and yang of the exosome. Trends Cell Biol 2002, 12:90-96.
5. Cordin O, Banroques J, Tanner NK, Linder P: The DEAD-box protein family of RNA helicases. Gene 2006, 367:17-37.
6. Bertrand E, Bordonne R: Assembly and traffic of small nuclear RNPs. Prog Mol Subcell Biol 2004, 35:79-97.
7. Cavaille J, Nicoloso M, Bachellerie JP: Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature 1996, 383:732-735.
8. Kiss-Laszlo Z, Henry Y, Kiss T: Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J 1998, 17:797-807.
9. Tollervey D, Lehtonen H, Jansen R, Kern H, Hurt EC: Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 1993, 72:443-457.
10. Omer AD, Ziesche S, Ebhardt H, Dennis PP: In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex. Proc Natl Acad Sci U S A 2002, 99:5289-5294.
11. Watkins NJ, Dickmanns A, Luhrmann R: Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5 K protein, for the hierarchical assembly of the box C/D snoRNP. Mol Cell Biol 2002, 22:8342-8352.
12. Yang Y, Isaac C, Wang C, Dragon F, Pogacic V, Meier UT: 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 2000, 11:567-577.
13. Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, Jady BE, Rothe B, Pescia C, Robert MC, Kiss T, Bardoni B, Krol A, Branlant C, Allmang C, Bertrand E, Charpentier B: The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 2008, 180:579-595.
14. Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, Costanzo M, Brost RL, Boone C, Hughes TR, Yip CM, Houry WA: Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol 2008, 180:563-578.
15. Peng WT, Robinson MD, Mnaimneh S, Krogan NJ, Cagney G, Morris Q, Davierwala AP, Grigull J, Yang X, Zhang W, Mitsakakis N, Ryan OW, Datta N, Jojic V, Pal C, Canadien V, Richards D, Beattie B, Wu LF, Altschuler SJ, Roweis S, Frey BJ, Emili A, Greenblatt JF, Hughes TR: A panoramic view of yeast noncoding RNA processing. Cell 2003, 113:919-933.
16. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, Ospina JK, Kiss T, Matera AG, Bordonne R, Bertrand E: PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 2004, 16:777-787.
17. Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, Luhrmann R: Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 2004, 16:789-798.
18. McKeegan KS, Debieux CM, Boulon S, Bertrand E, Watkins NJ: A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly. Mol Cell Biol 2007, 27:6782-6793.
19. Watkins NJ, Lemm I, Luhrmann R: Involvement of nuclear import and export factors in U8 box C/D snoRNP biogenesis. Mol Cell Biol 2007, 27:7018-7027.
20. Pradet-Balade B, Girard C, Boulon S, Paul C, Azzag K, Bordonne R, Bertrand E, Verheggen C: CRM1 controls the composition of nucleoplasmic presnoRNA complexes to licence them for nucleolar transport. EMBO J 2011, 30:2205-2218.
21. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J, Boone C, Emili A, Houry WA: Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005, 120:715-727.
22. Kakihara Y, Houry WA: The R2TP complex: discovery and functions. Biochim Biophys Acta 2012, 1823:101-107.
23. Jha S, Dutta A: RVB1/RVB2: running rings around molecular biology. Mol Cell 2009, 34:521-533.
24. Huen J, Kakihara Y, Ugwu F, Cheung KL, Ortega J, Houry WA: Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes. Biochem Cell Biol 2010, 88:29-40.
25. Gonzales FA, Zanchin NI, Luz JS, Oliveira CC: Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58p-interacting protein that is involved in Pre-rRNA processing. J Mol Biol 2005, 346:437-455.
26. Jimenez B, Ugwu F, Zhao R, Orti L, Makhnevych T, Pineda-Lucena A, Houry WA: Structure of minimal tetratricopeptide repeat domain protein Tah1 reveals mechanism of its interaction with Pih1 and Hsp90. J Biol Chem 2012, 287:5698-5709.
27. Jeronimo C, Forget D, Bouchard A, Li Q, Chua G, Poitras C, Therien C, Bergeron D, Bourassa S, Greenblatt J, Chabot B, Poirier GG, Hughes TR, Blanchette M, Price DH, Coulombe B: Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol Cell 2007, 27:262-274.
28. Boulon S, Pradet-Balade B, Verheggen C, Molle D, Boireau S, Georgieva M, Azzag K, Robert MC, Ahmad Y, Neel H, Lamond AI, Bertrand E: HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 2010, 39:912-924.
29. Horejsi Z, Takai H, Adelman CA, Collis SJ, Flynn H, Maslen S, Skehel JM, de Lange T, Boulton SJ: CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol Cell 2010, 39:839-850.
30. Inoue M, Saeki M, Egusa H, Niwa H, Kamisaki Y: PIH1D1, a subunit of R2TP complex, inhibits doxorubicin-induced apoptosis. Biochem Biophys Res Commun 2010, 403:340-344.
31. Kamano Y, Saeki M, Egusa H, Kakihara Y, Houry WA, Yatani H, Kamisaki Y: PIH1D1 interacts with mTOR complex 1 and enhances ribosome RNA transcription. FEBS Lett 2013, 587:3303-3308.
32. Saeki M, Egusa H, Kamano Y, Kakihara Y, Houry WA, Yatani H, Noguchi S, Kamisaki Y: Exosome-bound WD repeat protein Monad inhibits breast cancer cell invasion by degrading amphiregulin mRNA. PLoS One 2013, 8:e67326.
33. Ye K, Jia R, Lin J, Ju M, Peng J, Xu A, Zhang L: Structural organization of box C/D RNA-guided RNA methyltransferase. Proc Natl Acad Sci U S A 2009, 106:13808-13813.
34. Lin J, Lai S, Jia R, Xu A, Zhang L, Lu J, Ye K: Structural basis for site-specific ribose methylation by box C/D RNA protein complexes. Nature 2011, 469:559-563.
35. Paci A, Liu XH, Huang H, Lim A, Houry WA, Zhao R: The stability of the small nucleolar ribonucleoprotein (snoRNP) assembly protein Pih1 in Saccharomyces cerevisiae is modulated by its C terminus. J Biol Chem 2012, 287:43205-43214.
36. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, Punna T, Ihmels J, Andrews B, Boone C, Greenblatt JF, Weissman JS, Krogan NJ: Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 2005, 123:507-519.
37. Gribun A, Cheung KL, Huen J, Ortega J, Houry WA: Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex. J Mol Biol 2008, 376:1320-1333.
38. King TH, Decatur WA, Bertrand E, Maxwell ES, Fournier MJ: A wellconnected and conserved nucleoplasmic helicase is required for production of box C/D and H/ACA snoRNAs and localization of snoRNP proteins. Mol Cell Biol 2001, 21:7731-7746.
39. Zaman S, Lippman SI, Zhao X, Broach JR: How Saccharomyces responds to nutrients. Annu Rev Genet 2008, 42:27-81.
40. Rohde JR, Bastidas R, Puria R, Cardenas ME: Nutritional control via Tor signaling in Saccharomyces cerevisiae. Curr Opin Microbiol 2008, 11:153-160.
41. Rout MP, Blobel G, Aitchison JD: A distinct nuclear import pathway used by ribosomal proteins. Cell 1997, 89:715-725.
42. Makhnevych T, Lusk CP, Anderson AM, Aitchison JD, Wozniak RW: Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 2003, 115:813-823.
43. Gadal O, Strauss D, Kessl J, Trumpower B, Tollervey D, Hurt E: Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol Cell Biol 2001, 21:3405-3415.
44. Johnson AW, Lund E, Dahlberg J: Nuclear export of ribosomal subunits. Trends Biochem Sci 2002, 27:580-585.
45. Neville M, Rosbash M: The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae. EMBO J 1999, 18:3746-3756.
46. Arevalo-Rodriguez M, Heitman J: Cyclophilin A is localized to the nucleus and controls meiosis in Saccharomyces cerevisiae. Eukaryot Cell 2005, 4:17-29.
47. Gautier T, Berges T, Tollervey D, Hurt E: Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol Cell Biol 1997, 17:7088-7098.
48. Lafontaine DL, Tollervey D: Synthesis and assembly of the box C + D small nucleolar RNPs. Mol Cell Biol 2000, 20:2650-2659.
49. Colau G, Thiry M, Leduc V, Bordonne R, Lafontaine DL: The small nucle(ol) ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol Cell Biol 2004, 24:7976-7986.
50. Mouaikel J, Verheggen C, Bertrand E, Tazi J, Bordonne R: Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus. Mol Cell 2002, 9:891-901.
51. Rothe B, Back R, Quinternet M, Bizarro J, Robert MC, Blaud M, Romier C, Manival X, Charpentier B, Bertrand E, Branlant C: Characterization of the interaction between protein Snu13p/15.5 K and the Rsa1p/NUFIP factor and demonstration of its functional importance for snoRNP assembly. Nucleic Acids Res 2014, 42:2015-2036.
52. Stavreva DA, Kawasaki M, Dundr M, Koberna K, Muller WG, Tsujimura-Takahashi T, Komatsu W, Hayano T, Isobe T, Raska I, Misteli T, Takahashi N, McNally JG: Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol Cell Biol 2006, 26:5131-5145.
53. Matic I, Schimmel J, Hendriks IA, van Santen MA, van de Rijke F, van Dam H, Gnad F, Mann M, Vertegaal AC: Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif. Mol Cell 2010, 39:641-652.
54. Westman BJ, Verheggen C, Hutten S, Lam YW, Bertrand E, Lamond AI: A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol Cell 2010, 39:618-631.
55. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR: Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
56. Burke D, Dawson D, Stearns T: Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 2000.
57. Shen X: Preparation and analysis of the INO80 complex. Methods Enzymol 2004, 377:401-412.
58. Kushnirov VV: Rapid and reliable protein extraction from yeast. Yeast 2000, 16:857-860.