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PMID: 25060708 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

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

Genome biology ·Vol. 15 ·No. 7 ·2014-07-25 ·Pages 404

Kakihara Y, Makhnevych T, Zhao L, Tang W, Houry WA

Abstract

Box C/D snoRNPs, which are typically composed of box C/D snoRNA and the four core protein components Nop1, Nop56, Nop58, and Snu13, play an essential role in the modification and processing of pre-ribosomal RNA. The highly conserved R2TP complex, comprising the proteins Rvb1, Rvb2, Tah1, and Pih1, has been shown to be required for box C/D snoRNP biogenesis and assembly; however, the molecular basis of R2TP chaperone-like activity is not yet known. Here, we describe an unexpected finding in which the activity of the R2TP complex is required for Nop58 protein stability and is controlled by the dynamic subcellular redistribution of the complex in response to growth conditions and nutrient availability. In growing cells, the complex localizes to the nucleus and interacts with box C/D snoRNPs. This interaction is significantly reduced in poorly growing cells as R2TP predominantly relocalizes to the cytoplasm. The R2TP-snoRNP interaction is mainly mediated by Pih1. The R2TP complex exerts a novel regulation on box C/D snoRNP biogenesis that affects their assembly and consequently pre-rRNA maturation in response to different growth conditions.

MeSH Terms
Cell Nucleus/metabolism Cytoplasm/metabolism Gene Expression Regulation, Fungal Nuclear Proteins/genetics,metabolism Protein Stability Ribonucleoproteins, Small Nucleolar/genetics,metabolism Saccharomyces cerevisiae/physiology Saccharomyces cerevisiae Proteins/genetics,metabolism Stress, Physiological
Chemicals
NOP58 protein, S cerevisiae Nuclear Proteins PIH1 protein, S cerevisiae Ribonucleoproteins, Small Nucleolar Saccharomyces cerevisiae Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kakihara Yoshito
Makhnevych Taras
Zhao Liang
Tang Weiwen
Houry Walid A
References (57)
57 references, click to expand
  1. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile.
    Cell. 2005 Nov 4;123(3):507-19 PMID: 16269340
  2. Assembly and traffic of small nuclear RNPs.
    Prog Mol Subcell Biol. 2004;35:79-97 PMID: 15113080
  3. Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex.
    J Mol Biol. 2008 Mar 7;376(5):1320-33 PMID: 18234224
  4. Cyclophilin A is localized to the nucleus and controls meiosis in Saccharomyces cerevisiae.
    Eukaryot Cell. 2005 Jan;4(1):17-29 PMID: 15643056
  5. In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5289-94 PMID: 11959980
  6. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis.
    Mol Cell Biol. 1997 Dec;17(12):7088-98 PMID: 9372940
  7. The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology.
    Mol Cell Biol. 2004 Sep;24(18):7976-86 PMID: 15340060
  8. Ribosome synthesis in Saccharomyces cerevisiae.
    Annu Rev Genet. 1999;33:261-311 PMID: 10690410
  9. The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae.
    EMBO J. 1999 Jul 1;18(13):3746-56 PMID: 10393189
  10. Synthetic lethality with conditional dbp6 alleles identifies rsa1p, a nucleoplasmic protein involved in the assembly of 60S ribosomal subunits.
    Mol Cell Biol. 1999 Dec;19(12):8633-45 PMID: 10567587
  11. Rapid and reliable protein extraction from yeast.
    Yeast. 2000 Jun 30;16(9):857-60 PMID: 10861908
  12. Nutritional control via Tor signaling in Saccharomyces cerevisiae.
    Curr Opin Microbiol. 2008 Apr;11(2):153-60 PMID: 18396450
  13. The yin and yang of the exosome.
    Trends Cell Biol. 2002 Feb;12(2):90-6 PMID: 11849973
  14. Exosome-bound WD repeat protein Monad inhibits breast cancer cell invasion by degrading amphiregulin mRNA.
    PLoS One. 2013 Jul 03;8(7):e67326 PMID: 23844004
  15. A well-connected 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 Nov;21(22):7731-46 PMID: 11604509
  16. Potential roles for ubiquitin and the proteasome during ribosome biogenesis.
    Mol Cell Biol. 2006 Jul;26(13):5131-45 PMID: 16782897
  17. Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes.
    Biochem Cell Biol. 2010 Feb;88(1):29-40 PMID: 20130677
  18. PIH1D1, a subunit of R2TP complex, inhibits doxorubicin-induced apoptosis.
    Biochem Biophys Res Commun. 2010 Dec 17;403(3-4):340-4 PMID: 21078300
  19. 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 May;21(10):3405-15 PMID: 11313466
  20. Characterization of the interaction between protein Snu13p/15.5K and the Rsa1p/NUFIP factor and demonstration of its functional importance for snoRNP assembly.
    Nucleic Acids Res. 2014 Feb;42(3):2015-36 PMID: 24234454
  21. A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly.
    Mol Cell Biol. 2007 Oct;27(19):6782-93 PMID: 17636026
  22. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  23. Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly.
    Cell. 1993 Feb 12;72(3):443-57 PMID: 8431947
  24. RVB1/RVB2: running rings around molecular biology.
    Mol Cell. 2009 Jun 12;34(5):521-33 PMID: 19524533
  25. 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 Feb;11(2):567-77 PMID: 10679015
  26. How Saccharomyces responds to nutrients.
    Annu Rev Genet. 2008;42:27-81 PMID: 18303986
  27. The R2TP complex: discovery and functions.
    Biochim Biophys Acta. 2012 Jan;1823(1):101-7 PMID: 21925213
  28. Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58p-interacting protein that is involved in Pre-rRNA processing.
    J Mol Biol. 2005 Feb 18;346(2):437-55 PMID: 15670595
  29. Preparation and analysis of the INO80 complex.
    Methods Enzymol. 2004;377:401-12 PMID: 14979041
  30. Structure of minimal tetratricopeptide repeat domain protein Tah1 reveals mechanism of its interaction with Pih1 and Hsp90.
    J Biol Chem. 2012 Feb 17;287(8):5698-709 PMID: 22179618
  31. Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP.
    Mol Cell Biol. 2002 Dec;22(23):8342-52 PMID: 12417735
  32. Hypermethylation of the cap structure of both yeast snRNAs and snoRNAs requires a conserved methyltransferase that is localized to the nucleolus.
    Mol Cell. 2002 Apr;9(4):891-901 PMID: 11983179
  33. A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58.
    Mol Cell. 2010 Aug 27;39(4):618-31 PMID: 20797632
  34. A panoramic view of yeast noncoding RNA processing.
    Cell. 2003 Jun 27;113(7):919-33 PMID: 12837249
  35. Nuclear export of ribosomal subunits.
    Trends Biochem Sci. 2002 Nov;27(11):580-5 PMID: 12417134
  36. Cell cycle regulated transport controlled by alterations in the nuclear pore complex.
    Cell. 2003 Dec 26;115(7):813-23 PMID: 14697200
  37. Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA.
    EMBO J. 1998 Feb 2;17(3):797-807 PMID: 9451004
  38. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation.
    J Cell Biol. 2008 Feb 11;180(3):563-78 PMID: 18268103
  39. Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif.
    Mol Cell. 2010 Aug 27;39(4):641-52 PMID: 20797634
  40. Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex.
    Mol Cell. 2004 Dec 3;16(5):789-98 PMID: 15574333
  41. PIH1D1 interacts with mTOR complex 1 and enhances ribosome RNA transcription.
    FEBS Lett. 2013 Oct 11;587(20):3303-8 PMID: 24036451
  42. Structural basis for site-specific ribose methylation by box C/D RNA protein complexes.
    Nature. 2011 Jan 27;469(7331):559-63 PMID: 21270896
  43. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme.
    Mol Cell. 2007 Jul 20;27(2):262-74 PMID: 17643375
  44. The stability of the small nucleolar ribonucleoprotein (snoRNP) assembly protein Pih1 in Saccharomyces cerevisiae is modulated by its C terminus.
    J Biol Chem. 2012 Dec 21;287(52):43205-14 PMID: 23139418
  45. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery.
    J Cell Biol. 2008 Feb 11;180(3):579-95 PMID: 18268104
  46. HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II.
    Mol Cell. 2010 Sep 24;39(6):912-924 PMID: 20864038
  47. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli.
    Mol Cell. 2004 Dec 3;16(5):777-87 PMID: 15574332
  48. Involvement of nuclear import and export factors in U8 box C/D snoRNP biogenesis.
    Mol Cell Biol. 2007 Oct;27(20):7018-27 PMID: 17709390
  49. A distinct nuclear import pathway used by ribosomal proteins.
    Cell. 1997 May 30;89(5):715-25 PMID: 9182759
  50. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone.
    Cell. 2005 Mar 11;120(5):715-27 PMID: 15766533
  51. The economics of ribosome biosynthesis in yeast.
    Trends Biochem Sci. 1999 Nov;24(11):437-40 PMID: 10542411
  52. CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability.
    Mol Cell. 2010 Sep 24;39(6):839-50 PMID: 20864032
  53. Structural organization of box C/D RNA-guided RNA methyltransferase.
    Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13808-13 PMID: 19666563
  54. The DEAD-box protein family of RNA helicases.
    Gene. 2006 Feb 15;367:17-37 PMID: 16337753
  55. Synthesis and assembly of the box C+D small nucleolar RNPs.
    Mol Cell Biol. 2000 Apr;20(8):2650-9 PMID: 10733567
  56. CRM1 controls the composition of nucleoplasmic pre-snoRNA complexes to licence them for nucleolar transport.
    EMBO J. 2011 Jun 1;30(11):2205-18 PMID: 21522132
  57. Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides.
    Nature. 1996 Oct 24;383(6602):732-5 PMID: 8878486
Article Info
Journal
Genome biology
Abbr.
Genome Biol
ISSN
1474-760X
DOI
10.1186/s13059-014-0404-4
Published
2014-07-25
Epub
2014-00-25
Pages
404
Language
English
Region
England
NLM ID
100960660
PMCID
PMC4165372
Subset
IM
Grants
Canadian Institutes of Health Research · MOP-93778 · Canada
Canadian Institutes of Health Research · TGF-53910 · Canada
External Links
PubMed source DOI: 10.1186/s13059-014-0404-4 PMC Full Text View journal details
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