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PMID: 15692568 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins.

The EMBO journal ·Vol. 24 ·No. 3 ·2005-02-09 ·Pages 533-42

Rudra D, Zhao Y, Warner JR

Abstract

The 138 genes encoding the 79 ribosomal proteins (RPs) of Saccharomyces cerevisiae form the tightest cluster of coordinately regulated genes in nearly all transcriptome experiments. The basis for this observation remains unknown. We now provide evidence that two factors, Fhl1p and Ifh1p, are key players in the transcription of RP genes. Both are found at transcribing RP genes in vivo. Ifh1p, but not Fhl1p, leaves the RP genes when transcription is repressed. The occupancy of the RP genes by Ifh1p depends on its interaction with the phospho-peptide recognizing forkhead-associated domain of Fhl1p. Disruption of this interaction is severely deleterious to ribosome synthesis and cell growth. Loss of functional Fhl1p leads to cells that have only 20% the normal amount of RNA and that synthesize ribosomes at only 5-10% the normal rate. Homeostatic mechanisms within the cell respond by reducing the transcription of rRNA to match the output of RPs, and by reducing the global transcription of mRNA to match the capacity of the translational apparatus.

MeSH Terms
Cell Division DNA, Fungal/genetics,metabolism Forkhead Transcription Factors Genes, Fungal Mutagenesis, Site-Directed Oligonucleotide Array Sequence Analysis Promoter Regions, Genetic Protein Binding Protein Structure, Tertiary RNA, Fungal/genetics,metabolism RNA, Messenger/genetics,metabolism Recombinant Proteins/chemistry,genetics,metabolism Ribosomal Proteins/biosynthesis,genetics Saccharomyces cerevisiae/genetics,growth & development,metabolism Saccharomyces cerevisiae Proteins/biosynthesis,chemistry,genetics,metabolism Trans-Activators/chemistry,genetics,metabolism Transcription Factors/chemistry,genetics,metabolism Transcription, Genetic
Chemicals
DNA, Fungal FHL1 protein, S cerevisiae Forkhead Transcription Factors IFH1 protein, S cerevisiae RNA, Fungal RNA, Messenger Recombinant Proteins Ribosomal Proteins Saccharomyces cerevisiae Proteins Trans-Activators Transcription Factors
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Rudra Dipayan
Department of Cell Biology, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
Zhao Yu
Warner Jonathan R
References (54)
54 references, click to expand
  1. Transcriptional elements of the yeast ribosomal protein gene CYH2.
    J Biol Chem. 1987 Apr 25;262(12):5690-5 PMID: 3553182
  2. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  3. Elevated recombination rates in transcriptionally active DNA.
    Cell. 1989 Feb 24;56(4):619-30 PMID: 2645056
  4. Mutational analysis of the upstream activation site of yeast ribosomal protein genes.
    Curr Genet. 1989 Apr;15(4):247-51 PMID: 2752447
  5. The economics of ribosome biosynthesis in yeast.
    Trends Biochem Sci. 1999 Nov;24(11):437-40 PMID: 10542411
  6. The TOR signaling cascade regulates gene expression in response to nutrients.
    Genes Dev. 1999 Dec 15;13(24):3271-9 PMID: 10617575
  7. RAP, RAP, open up! New wrinkles for RAP1 in yeast.
    Trends Genet. 2000 Feb;16(2):51-3 PMID: 10652526
  8. Forkhead transcription factors, Fkh1p and Fkh2p, collaborate with Mcm1p to control transcription required for M-phase.
    Curr Biol. 2000 Jul 27-Aug 10;10(15):896-906 PMID: 10959837
  9. Genomic expression programs in the response of yeast cells to environmental changes.
    Mol Biol Cell. 2000 Dec;11(12):4241-57 PMID: 11102521
  10. Remodeling of yeast genome expression in response to environmental changes.
    Mol Biol Cell. 2001 Feb;12(2):323-37 PMID: 11179418
  11. Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase.
    Mol Cell. 2000 Dec;6(6):1297-307 PMID: 11163204
  12. A Rsc3/Rsc30 zinc cluster dimer reveals novel roles for the chromatin remodeler RSC in gene expression and cell cycle control.
    Mol Cell. 2001 Apr;7(4):741-51 PMID: 11336698
  13. The tandem affinity purification (TAP) method: a general procedure of protein complex purification.
    Methods. 2001 Jul;24(3):218-29 PMID: 11403571
  14. Mechanisms controlling differential promoter-occupancy by the yeast forkhead proteins Fkh1p and Fkh2p: implications for regulating the cell cycle and differentiation.
    Genes Dev. 2001 Sep 15;15(18):2445-56 PMID: 11562353
  15. The FHA domain.
    FEBS Lett. 2002 Feb 20;513(1):58-66 PMID: 11911881
  16. Activator-specific recruitment of TFIID and regulation of ribosomal protein genes in yeast.
    Mol Cell. 2002 Apr;9(4):823-33 PMID: 11983173
  17. Transcriptional regulatory networks in Saccharomyces cerevisiae.
    Science. 2002 Oct 25;298(5594):799-804 PMID: 12399584
  18. The different (sur)faces of Rap1p.
    Mol Genet Genomics. 2003 Mar;268(6):791-8 PMID: 12655405
  19. Exploration, normalization, and summaries of high density oligonucleotide array probe level data.
    Biostatistics. 2003 Apr;4(2):249-64 PMID: 12925520
  20. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast.
    Mol Cell Biol. 2004 Jan;24(1):338-51 PMID: 14673167
  21. Transcriptome profiling of a Saccharomyces cerevisiae mutant with a constitutively activated Ras/cAMP pathway.
    Physiol Genomics. 2003 Dec 16;16(1):107-18 PMID: 14570984
  22. High-definition macromolecular composition of yeast RNA-processing complexes.
    Mol Cell. 2004 Jan 30;13(2):225-39 PMID: 14759368
  23. Predicting gene expression from sequence.
    Cell. 2004 Apr 16;117(2):185-98 PMID: 15084257
  24. Mapping global histone acetylation patterns to gene expression.
    Cell. 2004 Jun 11;117(6):721-33 PMID: 15186774
  25. Evidence for nucleosome depletion at active regulatory regions genome-wide.
    Nat Genet. 2004 Aug;36(8):900-5 PMID: 15247917
  26. Global nucleosome occupancy in yeast.
    Genome Biol. 2004;5(9):R62 PMID: 15345046
  27. Comparison of ABF1 and RAP1 in chromatin opening and transactivator potentiation in the budding yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 2004 Oct;24(20):9152-64 PMID: 15456886
  28. Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression.
    Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14315-22 PMID: 15353587
  29. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size.
    Genes Dev. 2004 Oct 15;18(20):2491-505 PMID: 15466158
  30. What better measure than ribosome synthesis?
    Genes Dev. 2004 Oct 15;18(20):2431-6 PMID: 15489289
  31. Messenger RNA for ribosomal proteins in yeast.
    J Mol Biol. 1983 Mar 25;165(1):79-89 PMID: 6341608
  32. Tripartite upstream promoter element essential for expression of Saccharomyces cerevisiae ribosomal protein genes.
    Mol Cell Biol. 1986 Feb;6(2):674-87 PMID: 3023862
  33. The extended promoter of the gene encoding ribosomal protein S33 in yeast consists of multiple protein binding elements.
    Nucleic Acids Res. 1989 Sep 25;17(18):7427-39 PMID: 2677998
  34. Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6958-62 PMID: 1495986
  35. GCR1, a transcriptional activator in Saccharomyces cerevisiae, complexes with RAP1 and can function without its DNA binding domain.
    EMBO J. 1993 Jun;12(6):2431-7 PMID: 8508768
  36. Distortion of the DNA double helix by RAP1 at silencers and multiple telomeric binding sites.
    J Mol Biol. 1993 May 20;231(2):293-310 PMID: 8510148
  37. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5.
    Nature. 1993 Jul 29;364(6436):412-20 PMID: 8332212
  38. Protein kinase A mediates growth-regulated expression of yeast ribosomal protein genes by modulating RAP1 transcriptional activity.
    Mol Cell Biol. 1994 Mar;14(3):1920-8 PMID: 8114723
  39. Suppression of yeast RNA polymerase III mutations by FHL1, a gene coding for a fork head protein involved in rRNA processing.
    Mol Cell Biol. 1994 May;14(5):2905-13 PMID: 8164651
  40. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1.
    Genes Dev. 1994 Oct 1;8(19):2257-69 PMID: 7958893
  41. Nutrient availability and the RAS/cyclic AMP pathway both induce expression of ribosomal protein genes in Saccharomyces cerevisiae but by different mechanisms.
    Mol Cell Biol. 1995 Jun;15(6):3187-96 PMID: 7760815
  42. The IFH1 gene product interacts with a fork head protein in Saccharomyces cerevisiae.
    Yeast. 1995 Mar;11(3):261-70 PMID: 7785326
  43. The multifunctional transcription factors Abf1p, Rap1p and Reb1p are required for full transcriptional activation of the chromosomal PGK gene in Saccharomyces cerevisiae.
    Mol Gen Genet. 1996 Feb 25;250(3):348-56 PMID: 8602150
  44. The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA.
    Cell. 1996 Apr 5;85(1):125-36 PMID: 8620531
  45. Characterization of the yeast transcriptome.
    Cell. 1997 Jan 24;88(2):243-51 PMID: 9008165
  46. Dissecting the regulatory circuitry of a eukaryotic genome.
    Cell. 1998 Nov 25;95(5):717-28 PMID: 9845373
  47. Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae.
    Mol Biol Cell. 1999 Apr;10(4):987-1000 PMID: 10198052
  48. Protein kinase C enables the regulatory circuit that connects membrane synthesis to ribosome synthesis in Saccharomyces cerevisiae.
    J Biol Chem. 1999 May 7;274(19):13235-41 PMID: 10224082
  49. DNA-binding requirements of the yeast protein Rap1p as selected in silico from ribosomal protein gene promoter sequences.
    Bioinformatics. 1999 Apr;15(4):267-77 PMID: 10320394
  50. Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme.
    Nature. 1999 Jun 10;399(6736):609-13 PMID: 10376605
  51. Chromatin opening and transactivator potentiation by RAP1 in Saccharomyces cerevisiae.
    Mol Cell Biol. 1999 Aug;19(8):5279-88 PMID: 10409719
  52. Direct analysis of protein complexes using mass spectrometry.
    Nat Biotechnol. 1999 Jul;17(7):676-82 PMID: 10404161
  53. Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1.
    Nature. 2004 Dec 23;432(7020):1058-61 PMID: 15616569
  54. Constitutive transcription of yeast ribosomal protein gene TCM1 is promoted by uncommon cis- and trans-acting elements.
    Mol Cell Biol. 1988 Oct;8(10):4328-41 PMID: 3054514
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1038/sj.emboj.7600553
Published
2005-02-09
Epub
2005-00-03
Pages
533-42
Language
English
Region
England
NLM ID
8208664
PMCID
PMC548658
Subset
IM
Grants
NIGMS NIH HHS · R01 GM025532 · United States
NCI NIH HHS · CA-13330 · United States
NIGMS NIH HHS · GM-25532 · United States
External Links
PubMed source DOI: 10.1038/sj.emboj.7600553 PMC Full Text View journal details
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