RNA polymerase I stability couples cellular growth to metal availability

Molecular Cell

Volumn 51, Issue 1, 2013, Pages 105-115

  Lee, Yueh Jung ^a   Lee, Chrissie Young ^a,c   Grzechnik, Agnieszka ^a,d   Gonzales Zubiate, Fernando ^a,e   Vashisht, Ajay A ^b   Lee, Albert ^a,f   Wohlschlegel, James ^b   Chanfreau, Guillaume F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Easel Biotechnologies LLC   (United States)

^d GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f AGILENT TECHNOLOGIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; EXPORTIN 1; PROTEIN; PROTEIN RPA190P; PROTEIN UBP2P; PROTEIN UBP4P; RNA POLYMERASE II; UNCLASSIFIED DRUG; ZINC; ZINC BINDING PROTEIN; PROTEINASE; RIBOSOME RNA; UBIQUITIN NALPHA PROTEIN HYDROLASE; UBIQUITIN-NALPHA-PROTEIN HYDROLASE;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME STABILITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VIVO STUDY; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SUBUNIT; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; UBIQUITINATION; ZINC DEFICIENCY; BIOSYNTHESIS; CYTOLOGY; DOWN REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

EUKARYOTA;

DOWN-REGULATION; ENDOPEPTIDASES; ENZYME STABILITY; RNA POLYMERASE I; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; UBIQUITINATION; VACUOLES; ZINC;

EID: 84891673687     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.05.005     Document Type: Article

References (45)

1. Amerik A.Y., Nowak J., Swaminathan S., Hochstrasser M. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 2000, 11:3365-3380.
2. Bird A.J., Gordon M., Eide D.J., Winge D.R. Repression of ADH1 and ADH3 during zinc deficiency by Zap1-induced intergenic RNA transcripts. EMBO J. 2006, 25:5726-5734.
3. Catala M., Tremblay M., Samson E., Conconi A., Abou Elela S. Deletion of Rnt1p alters the proportion of open versus closed rRNA gene repeats in yeast. Mol. Cell. Biol. 2008, 28:619-629.
4. Chen H.T., Hahn S. Mapping the location of TFIIB within the RNA polymerase II transcription preinitiation complex: a model for the structure of the PIC. Cell 2004, 119:169-180.
5. Claypool J.A., French S.L., Johzuka K., Eliason K., Vu L., Dodd J.A., Beyer A.L., Nomura M. Tor pathway regulates Rrn3p-dependent recruitment of yeast RNA polymerase I to the promoter but does not participate in alteration of the number of active genes. Mol. Biol. Cell 2004, 15:946-956.
6. Cramer P., Bushnell D.A., Kornberg R.D. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 2001, 292:1863-1876.
7. Donaldson I.M., Friesen J.D. Zinc stoichiometry of yeast RNA polymerase II and characterization of mutations in the zinc-binding domain of the largest subunit. J.Biol. Chem. 2000, 275:13780-13788.
8. Drygin D., Rice W.G., Grummt I. The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu. Rev. Pharmacol. Toxicol. 2010, 50:131-156.
9. Dupré S., Haguenauer-Tsapis R. Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol. Cell. Biol. 2001, 21:4482-4494.
10. Falchuk K.H., Mazus B., Ber E., Ulpino-Lobb L., Vallee B.L. Zinc deficiency and the Euglena gracilis chromatin: formation of an alpha-amanitin-resistant RNA polymerase II. Biochemistry 1985, 24:2576-2580.
11. Fath S., Milkereit P., Podtelejnikov A.V., Bischler N., Schultz P., Bier M., Mann M., Tschochner H. Association of yeast RNA polymerase I with a nucleolar substructure active in rRNA synthesis and processing. J.Cell Biol. 2000, 149:575-590.
12. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
13. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 2003, 17:1691-1702.
14. Hirsch H.H., Schiffer H.H., Wolf D.H. Biogenesis of the yeast vacuole (lysosome). Proteinase yscB contributes molecularly and kinetically to vacuolar hydrolase-precursor maturation. Eur. J. Biochem. 1992, 207:867-876.
15. Kraft C., Deplazes A., Sohrmann M., Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 2008, 10:602-610.
16. Kruhlak M., Crouch E.E., Orlov M., Montaño C., Gorski S.A., Nussenzweig A., Misteli T., Phair R.D., Casellas R. The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature 2007, 447:730-734.
17. Kvam E., Goldfarb D.S. Nucleus-vacuole junctions and piecemeal microautophagy of the nucleus in S. cerevisiae. Autophagy 2007, 3:85-92.
18. Lee A., Henras A.K., Chanfreau G. Multiple RNA surveillance pathways limit aberrant expression of iron uptake mRNAs and prevent iron toxicity in S. cerevisiae. Mol. Cell 2005, 19:39-51.
19. Lempiäinen H., Shore D. Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 2009, 21:855-863.
20. Li Y., Moir R.D., Sethy-Coraci I.K., Warner J.R., Willis I.M. Repression of ribosome and tRNA synthesis in secretion-defective cells is signaled by a novel branch of the cell integrity pathway. Mol. Cell. Biol. 2000, 20:3843-3851.
21. Lyons T.J., Gasch A.P., Gaither L.A., Botstein D., Brown P.O., Eide D.J. Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc. Natl. Acad. Sci. USA 2000, 97:7957-7962.
22. Mayer C., Grummt I. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 2006, 25:6384-6391.
23. Mayer C., Bierhoff H., Grummt I. The nucleolus as a stress sensor: JNK2 inactivates the transcription factor TIF-IA and down-regulates rRNA synthesis. Genes Dev. 2005, 19:933-941.
24. Merchant S., Bogorad L. Rapid degradation of apoplastocyanin in Cu(II)-deficient cells of Chlamydomonas reinhardtii. J.Biol. Chem. 1986, 261:15850-15853.
25. Moehle C.M., Dixon C.K., Jones E.W. Processing pathway for protease B of Saccharomyces cerevisiae. J.Cell Biol. 1989, 108:309-325.
26. Moss T. At the crossroads of growth control; making ribosomal RNA. Curr. Opin. Genet. Dev. 2004, 14:210-217.
27. Naryshkina T., Bruning A., Gadal O., Severinov K. Role of second-largest RNA polymerase I subunit Zn-binding domain in enzyme assembly. Eukaryot. Cell 2003, 2:1046-1052.
28. Neumann S., Petfalski E., Brügger B., Grosshans H., Wieland F., Tollervey D., Hurt E. Formation and nuclear export of tRNA, rRNA and mRNA is regulated by the ubiquitin ligase Rsp5p. EMBO Rep. 2003, 4:1156-1162.
29. Nierras C.R., Warner J.R. Protein kinase C enables the regulatory circuit that connects membrane synthesis to ribosome synthesis in Saccharomyces cerevisiae. J.Biol. Chem. 1999, 274:13235-13241.
30. North M., Steffen J., Loguinov A.V., Zimmerman G.R., Vulpe C.D., Eide D.J. Genome-wide functional profiling identifies genes and processes important for zinc-limited growth of Saccharomyces cerevisiae. PLoS Genet. 2012, 8:e1002699.
31. Philippi A., Steinbauer R., Reiter A., Fath S., Leger-Silvestre I., Milkereit P., Griesenbeck J., Tschochner H. TOR-dependent reduction in the expression level of Rrn3p lowers the activity of the yeast RNA Pol I machinery, but does not account for the strong inhibition of rRNA production. Nucleic Acids Res. 2010, 38:5315-5326.
32. Powers T., Walter P. Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 1999, 10:987-1000.
33. Puig S., Askeland E., Thiele D.J. Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 2005, 120:99-110.
34. Richardson L.A., Reed B.J., Charette J.M., Freed E.F., Fredrickson E.K., Locke M.N., Baserga S.J., Gardner R.G. A conserved deubiquitinating enzyme controls cell growth by regulating RNA polymerase I stability. Cell Rep 2012, 2:372-385.
35. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Séraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17:1030-1032.
36. Shcherbik N., Pestov D.G. The ubiquitin ligase Rsp5 is required for ribosome stability in Saccharomyces cerevisiae. RNA 2011, 17:1422-1428.
37. Simm C., Lahner B., Salt D., LeFurgey A., Ingram P., Yandell B., Eide D.J. Saccharomyces cerevisiae vacuole in zinc storage and intracellular zinc distribution. Eukaryot. Cell 2007, 6:1166-1177.
38. Stade K., Ford C.S., Guthrie C., Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 1997, 90:1041-1050.
39. Stefanovsky V., Langlois F., Gagnon-Kugler T., Rothblum L.I., Moss T. Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell 2006, 21:629-639.
40. Terhune M.W., Sandstead H.H. Decreased RNA polymerase activity in mammalian zinc deficiency. Science 1972, 177:68-69.
41. Toesca I., Nery C.R., Fernandez C.F., Sayani S., Chanfreau G.F. Cryptic transcription mediates repression of subtelomeric metal homeostasis genes. PLoS Genet. 2011, 7:e1002163.
42. Treich I., Riva M., Sentenac A. Zinc-binding subunits of yeast RNA polymerases. J.Biol. Chem. 1991, 266:21971-21976.
43. Vida T.A., Emr S.D. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J.Cell Biol. 1995, 128:779-792.
44. Warner J.R. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 1999, 24:437-440.
45. Zhao H., Eide D. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J.Biol. Chem. 1996, 271:23203-23210.