1,727
Views
9
CrossRef citations to date
0
Altmetric
Research Paper

Multiple Puf proteins regulate the stability of ribosome biogenesis transcripts

&
Pages 1228-1243 | Received 03 Jul 2018, Accepted 24 Aug 2018, Published online: 25 Sep 2018

References

  • Woolford JL Jr., Baserga SJ. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics. 2013 Nov;195(3):643–681. PubMed PMID: 24190922; PubMed Central PMCID: PMC3813855.
  • Osheim YN, French SL, Keck KM, et al. Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol Cell. 2004 Dec 22;16(6):943–954. PubMed PMID: 15610737.
  • Steffen KK, McCormick MA, Pham KM, et al. Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics. 2012 May;191(1):107–118. PubMed PMID: 22377630; PubMed Central PMCID: PMC3338253.
  • Warner JR. The economics of ribosome biosynthesis in yeast. Trends Biochem Sci. 1999 Nov;24(11):437–440. PubMed PMID: 10542411.
  • Gerber AP, Herschlag D, Brown PO. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2004 Mar;2(3):E79. PubMed PMID: 15024427; PubMed Central PMCID: PMCPmc368173. Eng.
  • Jackson JS Jr., Houshmandi SS, Lopez Leban F, et al. Recruitment of the Puf3 protein to its mRNA target for regulation of mRNA decay in yeast. Rna. 2004 Oct;10(10):1625–1636. PubMed PMID: 15337848; PubMed Central PMCID: PMC1370648.
  • Murata Y, Wharton RP. Binding of pumilio to maternal hunchback messenger-Rna is required for posterior patterning in drosophila embryos. Cell. 1995 Mar 10;80(5):747–756. PubMed PMID: WOS:A1995QM39900011; English.
  • Nakahata S, Katsu Y, Mita K, et al. Biochemical identification of Xenopus pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J Biol Chem. 2001 Jun 15;276(24):20945–20953. PubMed PMID: WOS:000169297900021; English.
  • Souza GM, Da Silva AM, Kuspa A. Starvation promotes dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development. 1999 Jul;126(14):3263–3274. PubMed PMID: WOS:000081818800020; English.
  • Tadauchi T, Matsumoto K, Herskowitz I, et al. Post-transcriptional regulation through the HO 3 ‘-UTR by Mpt5, a yeast homolog of Pumilio and FBF. Embo J. 2001 Feb 1;20(3):552–561. PubMed PMID: WOS:000166848400024; English.
  • Wang X, McLachlan J, Zamore PD, et al. Modular recognition of RNA by a human pumilio-homology domain. Cell. 2002 Aug 23;110(4):501–512. PubMed PMID: 12202039.
  • Wang X, Zamore PD, Hall TM. Crystal structure of a Pumilio homology domain. Mol Cell. 2001 Apr;7(4):855–865. PubMed PMID: 11336708.
  • Wreden C, Verrotti AC, Schisa JA, et al. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development. 1997 Aug;124(15):3015–3023. PubMed PMID: WOS:A1997XP68800015; English.
  • Zamore PD, Bartel DP, Lehmann R, et al. The PUMILIO-RNA interaction: a single RNA-binding domain monomer recognizes a bipartite target sequence. Biochemistry. 1999 Jan 12;38(2):596–604. PubMed PMID: 9888799.
  • Zamore PD, Williamson JR, Lehmann R. The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. Rna-A Publ Rna Soc. 1997 Dec;3(12):1421–1433. PubMed PMID: WOS:000071255700006; English.
  • Wilinski D, Qiu C, Lapointe CP, et al. RNA regulatory networks diversified through curvature of the PUF protein scaffold. Nat Commun. 2015;6:8213. PubMed PMID: 26364903; PubMed Central PMCID: PMC4570272.
  • Qiu C, McCann KL, Wine RN, et al. A divergent Pumilio repeat protein family for pre-rRNA processing and mRNA localization. Proc Natl Acad Sci USA. 2014 Dec 30;111(52):18554–18559. PubMed PMID: 25512524; PubMed Central PMCID: PMC4284587.
  • Zhu D, Stumpf CR, Krahn JM, et al. A 5ʹ cytosine binding pocket in Puf3p specifies regulation of mitochondrial mRNAs. Proc Natl Acad Sci USA. 2009 Dec 1;106(48):20192–20197. PubMed PMID: 19918084; PubMed Central PMCID: PMC2787145.
  • Wang Y, Opperman L, Wickens M, et al. Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein. Proc Natl Acad Sci USA. 2009 Dec 01;106(48):20186–20191. PubMed PMID: 19901328; PubMed Central PMCID: PMC2787170.
  • Miller MT, Higgin JJ, Hall TM. Basis of altered RNA-binding specificity by PUF proteins revealed by crystal structures of yeast Puf4p. Nat Struct Mol Biol. 2008 Apr;15(4):397–402. PubMed PMID: 18327269; PubMed Central PMCID: PMC2802072.
  • Koh YY, Wang Y, Qiu C, et al. Stacking interactions in PUF-RNA complexes. Rna. 2011 Apr;17(4):718–727. PubMed PMID: 21372189; PubMed Central PMCID: PMC3062182.
  • Edwards TA, Pyle SE, Wharton RP, et al. Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell. 2001 Apr 20;105(2):281–289. PubMed PMID: 11336677.
  • Goldstrohm AC, Hook BA, Seay DJ, et al. PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol. 2006 Jun;13(6):533–539. PubMed PMID: WOS:000238122500018; English.
  • Goldstrohm AC, Seay DJ, Hook BA, et al. PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem. 2007 Jan 5;282(1):109–114. PubMed PMID: WOS:000243166500013; English.
  • Lee D, Ohn T, Chiang YC, et al. PUF3 acceleration of deadenylation in vivo can operate independently of CCR4 activity, possibly involving effects on the PAB1-mRNP structure. J Mol Biol. 2010 Jun 18;399(4):562–575. PubMed PMID: WOS:000279138700003; English.
  • Miller MA, Olivas WM. Roles of Puf proteins in mRNA degradation and translation. Wiley Interdiscip Rev RNA. 2011 Jul-Aug;2(4):471–492. PubMed PMID: 21957038.
  • Blewett NH, Goldstrohm AC. A eukaryotic translation initiation factor 4E-binding protein promotes mRNA decapping and is required for PUF repression. Mol Cell Biol. 2012 Oct;32(20):4181–4194. PubMed PMID: 22890846; PubMed Central PMCID: PMC3457345.
  • Russo J, Olivas WM. Conditional regulation of Puf1p, Puf4p, and Puf5p activity alters YHB1 mRNA stability for a rapid response to toxic nitric oxide stress in yeast. Mol Biol Cell. 2015 Mar 15;26(6):1015–1029. PubMed PMID: 25631823; PubMed Central PMCID: PMC4357503.
  • Ulbricht RJ, Olivas WM. Puf1p acts in combination with other yeast Puf proteins to control mRNA stability. Rna. 2008 Feb;14(2):246–262. PubMed PMID: 18094119; PubMed Central PMCID: PMC2212245.
  • Olivas W, Parker R. The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. Embo J. 2000 Dec 1;19(23):6602–6611. PubMed PMID: 11101532; PubMed Central PMCID: PMC305854.
  • Foat BC, Houshmandi SS, Olivas WM, et al. Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc Natl Acad Sci USA. 2005 Dec 6;102(49):17675–17680. PubMed PMID: 16317069; PubMed Central PMCID: PMC1295595.
  • Lapointe CP, Preston MA, Wilinski D, et al. Architecture and dynamics of overlapped RNA regulatory networks. Rna. 2017 Aug 02;23:1636–1647. PubMed PMID: 28768715.
  • Miller MA, Russo J, Fischer AD, et al. Carbon source-dependent alteration of Puf3p activity mediates rapid changes in the stabilities of mRNAs involved in mitochondrial function. Nucleic Acids Res. 2014 Apr;42(6):3954–3970. PubMed PMID: 24371272; PubMed Central PMCID: PMC3973295.
  • Thomson E, Rappsilber J, Tollervey D. Nop9 is an RNA binding protein present in pre-40S ribosomes and required for 18S rRNA synthesis in yeast. Rna. 2007 Dec;13(12):2165–2174. PubMed PMID: 17956976; PubMed Central PMCID: PMC2080597.
  • Wang B, Ye K. Nop9 binds the central pseudoknot region of 18S rRNA. Nucleic Acids Res. 2017 Apr 07;45(6):3559–3567. PubMed PMID: 28053123; PubMed Central PMCID: PMC5389560.
  • Li Z, Lee I, Moradi E, et al. Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol. 2009 Oct;7(10):e1000213. PubMed PMID: 19806183; PubMed Central PMCID: PMC2749941.
  • Yi YH, Ma TH, Lee LW, et al. A genetic cascade of let-7-ncl-1-fib-1 modulates nucleolar size and rRNA pool in caenorhabditis elegans. PLoS Genet. 2015 Oct;11(10):e1005580. PubMed PMID: 26492166; PubMed Central PMCID: PMC4619655.
  • Droll D, Archer S, Fenn K, et al. The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett. 2010 Mar 19;584(6):1156–1162. PubMed PMID: 20153321; PubMed Central PMCID: PMC2855960.
  • Schumann Burkard G, Kaser S, de Araujo PR, et al. Nucleolar proteins regulate stage-specific gene expression and ribosomal RNA maturation in Trypanosoma brucei. Mol Microbiol. 2013 May;88(4):827–840. PubMed PMID: 23617823.
  • Abbasi N, Kim HB, Park NI, et al. APUM23, a nucleolar Puf domain protein, is involved in pre-ribosomal RNA processing and normal growth patterning in Arabidopsis. Plant J. 2010 Dec;64(6):960–976. PubMed PMID: 21143677.
  • Scott RE, White-Grindley E, Ruley HE, et al. P2P-R expression is genetically coregulated with components of the translation machinery and with PUM2, a translational repressor that associates with the P2P-R mRNA. J Cell Physiol. 2005 Jul;204(1):99–105. PubMed PMID: 15617101.
  • Opperman L, Hook B, DeFino M, et al. A single spacer nucleotide determines the specificities of two mRNA regulatory proteins. Nat Struct Mol Biol. 2005 Nov;12(11):945–951. PubMed PMID: 16244662.
  • Koh YY, Opperman L, Stumpf C, et al. A single C. elegans PUF protein binds RNA in multiple modes. Rna. 2009 Jun;15(6):1090–1099. PubMed PMID: 19369425; PubMed Central PMCID: PMC2685523.
  • Valley CT, Porter DF, Qiu C, et al. Patterns and plasticity in RNA-protein interactions enable recruitment of multiple proteins through a single site. Proc Natl Acad Sci USA. 2012 Apr 17;109(16):6054–6059. PubMed PMID: 22467831; PubMed Central PMCID: PMC3341033.
  • Hook BA, Goldstrohm AC, Seay DJ, et al. Two yeast PUF proteins negatively regulate a single mRNA. J Biol Chem. 2007 May 25;282(21):15430–15438. PubMed PMID: 17389596.
  • Munchel SE, Shultzaberger RK, Takizawa N, et al. Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell. 2011 Aug 1;22(15):2787–2795. PubMed PMID: 21680716; PubMed Central PMCID: PMC3145553.
  • Deng Y, Singer RH, Gu W. Translation of ASH1 mRNA is repressed by Puf6p-Fun12p/eIF5B interaction and released by CK2 phosphorylation. Genes Dev. 2008 Apr 15;22(8):1037–1050. PubMed PMID: 18413716; PubMed Central PMCID: PMC2335325.
  • Kedde M, van Kouwenhove M, Zwart W, et al. A Pumilio-induced RNA structure switch in p27-3ʹ UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol. 2010 Oct;12(10):1014–1020. PubMed PMID: 20818387.
  • Lee CD, Tu BP. Glucose-regulated phosphorylation of the PUF protein Puf3 regulates the translational fate of its bound mRNAs and association with RNA granules. Cell Rep. 2015 Jun 16;11(10):1638–1650. PubMed PMID: 26051939; PubMed Central PMCID: PMC4472502.
  • Archer SK, Luu VD, de Queiroz RA, et al. Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathog. 2009 Aug;5(8):e1000565. PubMed PMID: 19714224; PubMed Central PMCID: PMC2727004.
  • Suh N, Crittenden SL, Goldstrohm A, et al. FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline. Genetics. 2009 Apr;181(4):1249–1260. PubMed PMID: 19221201; PubMed Central PMCID: PMC2666496.
  • Huber MD, Dworet JH, Shire K, et al. The budding yeast homolog of the human EBNA1-binding protein 2 (Ebp2p) is an essential nucleolar protein required for pre-rRNA processing. J Biol Chem. 2000 Sep 15;275(37):28764–28773. PubMed PMID: WOS:000089330700058; English.
  • Tsuno A, Miyoshi K, Tsujii R, et al. RRS1, a conserved essential gene, encodes a novel regulatory protein required for ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol. 2000 Mar;20(6):2066–2074. PubMed PMID: 10688653; PubMed Central PMCID: PMC110823.
  • de la Cruz J, Kressler D, Tollervey D, et al. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3ʹ end formation of 5.8S rRNA in Saccharomyces cerevisiae. Embo J. 1998 Feb 16;17(4):1128–1140. PubMed PMID: 9463390; PubMed Central PMCID: PMC1170461.
  • White J, Li Z, Sardana R, et al. Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol Cell Biol. 2008 May;28(10):3151–3161. PubMed PMID: 18332120; PubMed Central PMCID: PMC2423152.
  • Decatur WA, Fournier MJ. rRNA modifications and ribosome function. Trends Biochem Sci. 2002 Jul;27(7):344–351. PubMed PMID: 12114023.
  • Lebreton A, Saveanu C, Decourty L, et al. A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J Cell Biol. 2006 May 8;173(3):349–360. PubMed PMID: 16651379; PubMed Central PMCID: PMC2063836.
  • Miyoshi K, Shirai C, Horigome C, et al. Rrs1p, a ribosomal protein L11-binding protein, is required for nuclear export of the 60S pre-ribosomal subunit in Saccharomyces cerevisiae. FEBS Lett. 2004 May 7;565(1–3):106–110. PubMed PMID: 15135061.
  • Kamentsky L, Jones TR, Fraser A, et al. Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Bioinformatics. 2011 Apr 15;27(8):1179–1180. PubMed PMID: WOS:000289301600028; English.
  • Freeberg MA, Han T, Moresco JJ, et al. Pervasive and dynamic protein binding sites of the mRNA transcriptome in Saccharomyces cerevisiae. Genome Biol. 2013 Feb 14;14;14(2):R13. PubMed PMID: 23409723; PubMed Central PMCID: PMC4053964.
  • Kershaw CJ, Costello JL, Talavera D, et al. Integrated multi-omics analyses reveal the pleiotropic nature of the control of gene expression by Puf3p. Sci Rep. 2015 Oct 23;5:15518. PubMed PMID: 26493364; PubMed Central PMCID: PMC4616039.
  • Duttagupta R, Tian B, Wilusz CJ, et al. Global analysis of Pub1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol Cell Biol. 2005 Jul;25(13):5499–5513. PubMed PMID: 15964806; PubMed Central PMCID: PMC1156976.
  • Yosefzon Y, Koh YY, Chritton JJ, et al. Divergent RNA binding specificity of yeast Puf2p. Rna. 2011 Aug;17(8):1479–1488. PubMed PMID: 21685478; PubMed Central PMCID: PMC3153972.
  • Gu W, Deng Y, Zenklusen D, et al. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev. 2004 Jun 15;18(12):1452–1465. PubMed PMID: 15198983; PubMed Central PMCID: PMC423195.
  • Yang YT, Ting YH, Liang KJ, et al. The roles of Puf6 and Loc1 in 60S biogenesis are interdependent, and both are required for efficient accommodation of Rpl43. J Biol Chem. 2016 Sep 9;291(37):19312–19323. PubMed PMID: 27458021; PubMed Central PMCID: PMC5016672.
  • Aviv T, Lin Z, Ben-Ari G, et al. Sequence-specific recognition of RNA hairpins by the SAM domain of Vts1p. Nat Struct Mol Biol. 2006 Feb;13(2):168–176. PubMed PMID: 16429151.
  • Rendl LM, Bieman MA, Smibert CA. S. cerevisiae Vts1p induces deadenylation-dependent transcript degradation and interacts with the Ccr4p-Pop2p-Not deadenylase complex. Rna. 2008 Jul;14(7):1328–1336. PubMed PMID: 18469165; PubMed Central PMCID: PMC2441989.
  • Pedro-Segura E, Vergara SV, Rodriguez-Navarro S, et al. The Cth2 ARE-binding protein recruits the Dhh1 helicase to promote the decay of succinate dehydrogenase SDH4 mRNA in response to iron deficiency. J Biol Chem. 2008 Oct 17;283(42):28527–28535. PubMed PMID: 18715869; PubMed Central PMCID: PMC2568921.
  • Cai Y, Futcher B. Effects of the yeast RNA-binding protein Whi3 on the half-life and abundance of CLN3 mRNA and other targets. PLoS One. 2013;8(12):e84630. PubMed PMID: 24386402; PubMed Central PMCID: PMC3875557.
  • Holmes KJ, Klass DM, Guiney EL, et al. Whi3, an S. cerevisiae RNA-binding protein, is a component of stress granules that regulates levels of its target mRNAs. PLoS One. 2013;8(12):e84060. PubMed PMID: 24386330; PubMed Central PMCID: PMC3873981.
  • Vasudevan S, Peltz SW. Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol Cell. 2001 Jun;7(6):1191–1200. PubMed PMID: 11430822.
  • Huber A, French SL, Tekotte H, et al. Sch9 regulates ribosome biogenesis via Stb3, Dot6 and Tod6 and the histone deacetylase complex RPD3L. Embo J. 2011 Jul 05;30(15):3052–3064. PubMed PMID: 21730963; PubMed Central PMCID: PMC3160192.
  • Urban J, Soulard A, Huber A, et al. Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell. 2007 Jun 8;26(5):663–674. PubMed PMID: 17560372.
  • Lahr RM, Fonseca BD, Ciotti GE, et al. La-related protein 1 (LARP1) binds the mRNA cap, blocking eIF4F assembly on TOP mRNAs. Elife. 2017 Apr 7;6. PubMed PMID: 28379136; PubMed Central PMCID: PMC5419741. DOI:10.7554/eLife.24146
  • Hong S, Freeberg MA, Han T, et al. LARP1 functions as a molecular switch for mTORC1-mediated translation of an essential class of mRNAs. Elife. 2017 Jun 26;6. PubMed PMID: 28650797; PubMed Central PMCID: PMC5484620. DOI:10.7554/eLife.25237
  • Codon AC, Gasent-Ramirez JM, Benitez T. Factors Which Affect the Frequency of Sporulation and Tetrad Formation in Saccharomyces cerevisiae Baker’s Yeasts. Appl Environ Microbiol. 1995 Apr;61(4):1677. PubMed PMID: 16535013; PubMed Central PMCID: PMC1388431.
  • Gietz RD, Schiestl RH, Willems AR, et al. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast. 1995 Apr 15;11(4):355–360. PubMed PMID: 7785336.
  • Goldstein AL, McCusker JH. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 1999 Oct;15(14):1541–1553. PubMed PMID: 10514571.
  • Caponigro G, Muhlrad D, Parker R. A small segment of the MAT alpha 1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons. Mol Cell Biol. 1993 Sep;13(9):5141–5148. PubMed PMID: 8355674; PubMed Central PMCID: PMC360202.
  • Wei Y, Tsang CK, Zheng XF. Mechanisms of regulation of RNA polymerase III-dependent transcription by TORC1. Embo J. 2009 Aug 5;28(15):2220–2230. PubMed PMID: 19574957; PubMed Central PMCID: PMC2726700.
  • Atkin AL. Preparation of yeast cells for confocal microscopy. Methods Mol Biol. 1999;122:131–139. PubMed PMID: 10231788.
  • Voth WP, Jiang YW, Stillman DJ. New ‘marker swap’ plasmids for converting selectable markers on budding yeast gene disruptions and plasmids. Yeast. 2003 Aug;20(11):985–993. PubMed PMID: 12898713.