Abstract
Why is it important to understand mRNA degradation in a cell? First, RNA degradation has a clearing function and removes RNAs arising from transcription, splicing, export, or translation “accidents” to ensure robust gene expression (see Chap. 8). Second, while regulation of gene expression has a very important transcription component, mRNAs must be turned over rapidly for fast changes in transcriptome composition. Coordinated destabilization of an entire class of mRNAs can promote major physiological changes in a cell. Third, specific mechanisms of mRNA decay can serve to regulate gene expression through feedback control. Research on these topics has been frequently done first with yeasts and led to a better understanding of gene expression in eukaryotes. We start with an overview of the methods for measuring mRNA decay on a large scale with an emphasis on how technical issues affect the current picture of global mRNA decay in yeast. Next, we describe the importance of nuclear degradation in shaping the stable transcriptome. Once in the cytoplasm, mRNAs are exposed to translation and we provide an overview of the complexes and individual enzymes that ensure progressive deadenylation, mRNA decapping, and 5′ to 3′ or 3′ to 5′ exonucleolytic RNA degradation. Finally, how organelle transcripts are degraded in mitochondria is briefly exposed.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Albrecht M, Lengauer T (2004) Novel Sm-like proteins with long C-terminal tails and associated methyltransferases. FEBS Lett 569:18–26
Amberg DC, Goldstein AL, Cole CN (1992) Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev 6:1173–1189
Amrani N, Ghosh S, Mangus DA, Jacobson A (2008) Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453:1276–1280
Anderson JT, Wilson SM, Datar KV, Swanson MS (1993) NAB2: a yeast nuclear polyadenylated RNA-binding protein essential for cell viability. Mol Cell Biol 13:2730–2741
Araki Y, Takahashi S, Kobayashi T, Kajiho H, Hoshino S, Katada T (2001) Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J 20:4684–4693
Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D (2003) Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100:3889–3894
Arigo JT, Carroll KL, Ames JM, Corden JL (2006) Regulation of yeast NRD1 expression by premature transcription termination. Mol Cell 21:641–651
Arraiano CM, Mauxion F, Viegas SC, Matos RG, Séraphin B (2013) Intracellular ribonucleases involved in transcript processing and decay: precision tools for RNA. Biochim Biophys Acta 1829:491–513
Badis G, Saveanu C, Fromont-Racine M, Jacquier A (2004) Targeted mRNA degradation by deadenylation-independent decapping. Mol Cell 15:5–15
Baer BW, Kornberg RD (1980) Repeating structure of cytoplasmic poly(A)-ribonucleoprotein. Proc Natl Acad Sci USA 77:1890–1892
Baer BW, Kornberg RD (1983) The protein responsible for the repeating structure of cytoplasmic poly(A)-ribonucleoprotein. J Cell Biol 96:717–721
Bandyra KJ, Bouvier M, Carpousis AJ, Luisi BF (2013) The social fabric of the RNA degradosome. Biochim Biophys Acta 1829:514–522
Bashkirov VI, Scherthan H, Solinger JA, Buerstedde JM, Heyer WD (1997) A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J Cell Biol 136:761–773
Basquin J, Roudko VV, Rode M, Basquin C, Séraphin B, Conti E (2012) Architecture of the nuclease module of the yeast Ccr4-not complex: the Not1-Caf1-Ccr4 interaction. Mol Cell 48:207–218
Beelman CA, Stevens A, Caponigro G, LaGrandeur TE, Hatfield L, Fortner DM, Parker R (1996) An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 382:642–646
Boeck R, Tarun S Jr, Rieger M, Deardorff JA, Müller-Auer S, Sachs AB (1996) The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J Biol Chem 271:432–438
Boeck R, Lapeyre B, Brown CE, Sachs AB (1998) Capped mRNA degradation intermediates accumulate in the yeast spb8-2 mutant. Mol Cell Biol 18:5062–5072
Borja MS, Piotukh K, Freund C, Gross JD (2011) Dcp1 links coactivators of mRNA decapping to Dcp2 by proline recognition. RNA 17:278–290
Bousquet-Antonelli C, Presutti C, Tollervey D (2000) Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102:765–775
Bouveret E, Rigaut G, Shevchenko A, Wilm M, Séraphin B (2000) A Sm-like protein complex that participates in mRNA degradation. EMBO J 19:1661–1671
Bregman A, Avraham-Kelbert M, Barkai O, Duek L, Guterman A, Choder M (2011) Promoter elements regulate cytoplasmic mRNA Decay. Cell 147:1473–1483
Brown CE, Sachs AB (1998) Poly(A) tail length control in Saccharomyces cerevisiae occurs by message-specific deadenylation. Mol Cell Biol 18:6548–6559
Brown CE, Tarun SZ Jr, Boeck R, Sachs AB (1996) PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol Cell Biol 16:5744–5753
Buchan JR, Muhlrad D, Parker R (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183:441–455
Burger K, Mühl B, Kellner M, Rohrmoser M, Gruber-Eber A, Windhager L, Friedel CC, Dölken L, Eick D (2013) 4-thiouridine inhibits rRNA synthesis and causes a nucleolar stress response. RNA Biol 10
Butler JS, Mitchell P (2011) Rrp6, rrp47 and cofactors of the nuclear exosome. Adv Exp Med Biol 702:91–104
Callahan KP, Butler JS (2010) TRAMP complex enhances RNA degradation by the nuclear exosome component Rrp6. J Biol Chem 285:3540–3547
Chang JH, Jiao X, Chiba K, Oh C, Martin CE, Kiledjian M, Tong L (2012) Dxo1 is a new type of eukaryotic enzyme with both decapping and 5′-3′ exoribonuclease activity. Nat Struct Mol Biol 19:1011–1017
Chowdhury A, Mukhopadhyay J, Tharun S (2007) The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs. RNA 13:998–1016
Cleary MD, Meiering CD, Jan E, Guymon R, Boothroyd JC (2005) Biosynthetic labeling of RNA with uracil phosphoribosyltransferase allows cell-specific microarray analysis of mRNA synthesis and decay. Nat Biotechnol 23:232–237
Collart MA, Panasenko OO (2012) The Ccr4–not complex. Gene 492:42–53
Coller J, Parker R (2005) General translational repression by activators of mRNA decapping. Cell 122:875–886
Coller JM, Tucker M, Sheth U, Valencia-Sanchez MA, Parker R (2001) The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 7:1717–1727
Costello JL, Stead JA, Feigenbutz M, Jones RM, Mitchell P (2011) The C-terminal region of the exosome-associated protein Rrp47 is specifically required for box C/D small nucleolar RNA 3′-maturation. J Biol Chem 286:4535–4543
Cougot N, Babajko S, Séraphin B (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165:31–40
Daugeron MC, Mauxion F, Séraphin B (2001) The yeast POP2 gene encodes a nuclease involved in mRNA deadenylation. Nucleic Acids Res 29:2448–2455
Decker CJ, Teixeira D, Parker R (2007) Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J Cell Biol 179:437–449
Decourty L, Saveanu C, Zemam K, Hantraye F, Frachon E, Rousselle J-C, Fromont-Racine M, Jacquier A (2008) Linking functionally related genes by sensitive and quantitative characterization of genetic interaction profiles. Proc Natl Acad Sci USA 105:5821–5826
Deshmukh MV, Jones BN, Quang-Dang D-U, Flinders J, Floor SN, Kim C, Jemielity J, Kalek M, Darzynkiewicz E, Gross JD (2008) mRNA decapping is promoted by an RNA-binding channel in Dcp2. Mol Cell 29:324–336
Dichtl B, Stevens A, Tollervey D (1997) Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J 16:7184–7195
Van Dijk E, Cougot N, Meyer S, Babajko S, Wahle E, Séraphin B (2002) Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 21:6915–6924
Van Dijk EL, Chen CL, d′ Aubenton-Carafa Y, Gourvennec S, Kwapisz M, Roche V, Bertrand C, Silvain M, Legoix-Né P, Loeillet S et al (2011) XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475:114–117
Dmochowska A, Golik P, Stepien PP (1995) The novel nuclear gene DSS-1 of Saccharomyces cerevisiae is necessary for mitochondrial biogenesis. Curr Genet 28:108–112
Dölken L, Ruzsics Z, Rädle B, Friedel CC, Zimmer R, Mages J, Hoffmann R, Dickinson P, Forster T, Ghazal P et al (2008) High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14:1959–1972
Dong S, Li C, Zenklusen D, Singer RH, Jacobson A, He F (2007) YRA1 autoregulation requires nuclear export and cytoplasmic Edc3p-mediated degradation of its pre-mRNA. Mol Cell 25:559–573
Dori-Bachash M, Shalem O, Manor YS, Pilpel Y, Tirosh I (2012) Widespread promoter-mediated coordination of transcription and mRNA degradation. Genome Biol 13:R114
Drinnenberg IA, Fink GR, Bartel DP (2011) Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333:1592
Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, De Montigny J, Marck C, Neuvéglise C, Talla E et al (2004) Genome evolution in yeasts. Nature 430:35–44
Dunckley T, Parker R (1999) The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 18:5411–5422
Dunckley T, Tucker M, Parker R (2001) Two related proteins, Edc1p and Edc2p, stimulate mRNA decapping in Saccharomyces cerevisiae. Genetics 157:27–37
Dziembowski A, Lorentzen E, Conti E, Séraphin B (2007) A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14:15–22
Engel SR, Cherry JM (2013) The new modern era of yeast genomics: community sequencing and the resulting annotation of multiple Saccharomyces cerevisiae strains at the Saccharomyces Genome Database. Database J Biol, Databases Curation 2013
Ensinger MJ, Martin SA, Paoletti E, Moss B (1975) Modification of the 5′-terminus of mRNA by soluble guanylyl and methyl transferases from vaccinia virus. Proc Natl Acad Sci USA 72:2525–2529
Eulalio A, Behm-Ansmant I, Izaurralde E (2007a) P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 8:9–22
Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E (2007b) P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 27:3970–3981
Fleischer TC, Weaver CM, McAfee KJ, Jennings JL, Link AJ (2006) Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev 20:1294–1307
Foat BC, Houshmandi SS, Olivas WM, Bussemaker HJ (2005) Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc Natl Acad Sci USA 102:17675–17680
Fromm SA, Truffault V, Kamenz J, Braun JE, Hoffmann NA, Izaurralde E, Sprangers R (2012) The structural basis of Edc3- and Scd6-mediated activation of the Dcp1:Dcp2 mRNA decapping complex. EMBO J 31:279–290
Fromont-Racine M, Rain JC, Legrain P (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet 16:277–282
Fromont-Racine M, Mayes AE, Brunet-Simon A, Rain JC, Colley A, Dix I, Decourty L, Joly N, Ricard F, Beggs JD et al (2000) Genome-wide protein interaction screens reveal functional networks involving Sm-like proteins. Yeast 17:95–110
Furuichi Y, LaFiandra A, Shatkin AJ (1977) 5′-Terminal structure and mRNA stability. Nature 266:235–239
Garland W, Feigenbutz M, Turner M, Mitchell P (2013) Rrp47 functions in RNA surveillance and stable RNA processing when divorced from the exoribonuclease and exosome-binding domains of Rrp6. RNA 19(12):1659–1668
Gerber AP, Herschlag D, Brown PO (2004) Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2:e79
Goebels C, Thonn A, Gonzalez-Hilarion S, Rolland O, Moyrand F, Beilharz TH, Janbon G (2013) Introns Regulate Gene Expression in Cryptococcus neoformans in a Pab2p Dependent Pathway. PLoS Genet 9:e1003686
Goldstrohm AC, Hook BA, Seay DJ, Wickens M (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13:533–539
Goldstrohm AC, Seay DJ, Hook BA, Wickens M (2007) PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem 282:109–114
Granneman S, Kudla G, Petfalski E, Tollervey D (2009) Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proc Natl Acad Sci USA 106:9613–9618
Green DM, Marfatia KA, Crafton EB, Zhang X, Cheng X, Corbett AH (2002) Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J Biol Chem 277:7752–7760
Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR (2004) Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol Cell Biol 24:5534–5547
Gu M, Rajashankar KR, Lima CD (2010) Structure of the Saccharomyces cerevisiae Cet1-Ceg1 mRNA capping apparatus. Struct Lond Engl 1993(18):216–227
Gudipati RK, Neil H, Feuerbach F, Malabat C, Jacquier A (2012) The yeast RPL9B gene is regulated by modulation between two modes of transcription termination. EMBO J 31:2427–2437
Halbach F, Reichelt P, Rode M, Conti E (2013) The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell 154:814–826
Halbeisen RE, Scherrer T, Gerber AP (2009) Affinity purification of ribosomes to access the translatome. Methods San Diego Calif 48:306–310
Harigaya Y, Jones BN, Muhlrad D, Gross JD, Parker R (2010) Identification and analysis of the interaction between Edc3 and Dcp2 in Saccharomyces cerevisiae. Mol Cell Biol 30:1446–1456
He W, Parker R (2001) The yeast cytoplasmic LsmI/Pat1p complex protects mRNA 3′ termini from partial degradation. Genetics 158:1445–1455
Hector RE, Nykamp KR, Dheur S, Anderson JT, Non PJ, Urbinati CR, Wilson SM, Minvielle-Sebastia L, Swanson MS (2002) Dual requirement for yeast hnRNP Nab2p in mRNA poly(A) tail length control and nuclear export. EMBO J 21:1800–1810
Hirayama T, Matsuura T, Ushiyama S, Narusaka M, Kurihara Y, Yasuda M, Ohtani M, Seki M, Demura T, Nakashita H et al (2013) A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis. Nat Commun 4:2247
Hoffmann B, Nickel J, Speer F, Schafer B (2008) The 3′ ends of mature transcripts are generated by a processosome complex in fission yeast mitochondria. J Mol Biol 377:1024–1037
Hofmann TJ, Min J, Zassenhaus HP (1993) Formation of the 3′ end of yeast mitochondrial mRNAs occurs by site-specific cleavage two bases downstream of a conserved dodecamer sequence. Yeast 9:1319–1330
Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO (2008) Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 6:e255
Holub P, Lalakova J, Cerna H, Pasulka J, Sarazova M, Hrazdilova K, Arce MS, Hobor F, Stefl R, Vanacova S (2012) Air2p is critical for the assembly and RNA-binding of the TRAMP complex and the KOW domain of Mtr4p is crucial for exosome activation. Nucleic Acids Res 40:5679–5693
Houseley J, LaCava J, Tollervey D (2006) RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7:529–539
Hsu CL, Stevens A (1993) Yeast cells lacking 5′–>3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol Cell Biol 13:4826–4835
Hu W, Sweet TJ, Chamnongpol S, Baker KE, Coller J (2009) Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 461:225–229
Iglesias N, Tutucci E, Gwizdek C, Vinciguerra P, Von Dach E, Corbett AH, Dargemont C, Stutz F (2010) Ubiquitin-mediated mRNP dynamics and surveillance prior to budding yeast mRNA export. Genes Dev 24:1927–1938
Ingelfinger D, Arndt-Jovin DJ, Lührmann R, Achsel T (2002) The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8:1489–1501
Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218–223
Jackson JS Jr, Houshmandi SS, Lopez Leban F, Olivas WM (2004) Recruitment of the Puf3 protein to its mRNA target for regulation of mRNA decay in yeast. RNA 10:1625–1636
Jain S, Parker R (2013) The discovery and analysis of P Bodies. Adv Exp Med Biol 768:23–43
Jensen TH, Jacquier A, Libri D (2013) Dealing with pervasive transcription. Mol Cell 52:473–484
Jiao X, Xiang S, Oh C, Martin CE, Tong L, Kiledjian M (2010) Identification of a quality-control mechanism for mRNA 5′-end capping. Nature 467:608–611
Jimenez A, Tipper DJ, Davies J (1973) Mode of Action of Thiolutin, an Inhibitor of Macromolecular Synthesis in Saccharomyces cerevisiae. Antimicrob Agents Chemother 3:729–738
Johnson AW (1997) Rat1p and Xrn1p are functionally interchangeable exoribonucleases that are restricted to and required in the nucleus and cytoplasm, respectively. Mol Cell Biol 17:6122–6130
Keene JD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8:533–543
Keene JD, Tenenbaum SA (2002) Eukaryotic mRNPs may represent posttranscriptional operons. Mol Cell 9:1161–1167
Kim Guisbert K, Duncan K, Li H, Guthrie C (2005) Functional specificity of shuttling hnRNPs revealed by genome-wide analysis of their RNA binding profiles. RNA 11:383–393
Klass DM, Scheibe M, Butter F, Hogan GJ, Mann M, Brown PO (2013) Quantitative proteomic analysis reveals concurrent RNA-protein interactions and identifies new RNA-binding proteins in Saccharomyces cerevisiae. Genome Res 23:1028–1038
Kshirsagar M, Parker R (2004) Identification of Edc3p as an enhancer of mRNA decapping in Saccharomyces cerevisiae. Genetics 166:729–739
LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121:713–724
Larimer FW, Stevens A (1990) Disruption of the gene XRN1, coding for a 5′—3′ exoribonuclease, restricts yeast cell growth. Gene 95:85–90
De Lay N, Schu DJ, Gottesman S (2013) Bacterial small RNA-based negative regulation: Hfq and its accomplices. J Biol Chem 288:7996–8003
Lebreton A, Tomecki R, Dziembowski A, Séraphin B (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456:993–996
Legrain P, Rosbash M (1989) Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell 57:573–583
Lemieux C, Bachand F (2009) Cotranscriptional recruitment of the nuclear poly(A)-binding protein Pab2 to nascent transcripts and association with translating mRNPs. Nucleic Acids Res 37:3418–3430
Lidschreiber M, Leike K, Cramer P (2013) Cap completion and C-terminal repeat domain kinase recruitment underlie the initiation-elongation transition of RNA polymerase II. Mol Cell Biol 33:3805–3816
Liu H, Kiledjian M (2005) Scavenger Decapping Activity Facilitates 5′ to 3′ mRNA Decay. Mol Cell Biol 25:9764–9772
Liu H, Rodgers ND, Jiao X, Kiledjian M (2002) The scavenger mRNA decapping enzyme DcpS is a member of the HIT family of pyrophosphatases. EMBO J 21:4699–4708
Liu Q, Greimann JC, Lima CD (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127:1223–1237
Lo TL, Qu Y, Uwamahoro N, Quenault T, Beilharz TH, Traven A (2012) The mRNA decay pathway regulates the expression of the Flo11 adhesin and biofilm formation in Saccharomyces cerevisiae. Genetics 191:1387–1391
Lowell JE, Rudner DZ, Sachs AB (1992) 3′-UTR-dependent deadenylation by the yeast poly(A) nuclease. Genes Dev 6:2088–2099
Luo G, Costanzo M, Boone C, Dickson RC (2011) Nutrients and the Pkh1/2 and Pkc1 protein kinases control mRNA decay and P-body assembly in yeast. J Biol Chem 286:8759–8770
Luo W, Johnson AW, Bentley DL (2006) The role of Rat1 in coupling mRNA 3?-end processing to transcription termination: implications for a unified allosteric-torpedo model. Genes Dev 20:954–965
Makino DL, Baumgärtner M, Conti E (2013a) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495:70–75
Makino DL, Halbach F, Conti E (2013b) The RNA exosome and proteasome: common principles of degradation control. Nat Rev Mol Cell Biol 14:654–660
Malecki M, Viegas SC, Carneiro T, Golik P, Dressaire C, Ferreira MG, Arraiano CM (2013) The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J 32:1842–1854
Malys N, Carroll K, Miyan J, Tollervey D, McCarthy JEG (2004) The “scavenger” m7G pppX pyrophosphatase activity of Dcs1 modulates nutrient-induced responses in yeast. Nucleic Acids Res 32:3590–3600
Mangus DA, Amrani N, Jacobson A (1998) Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol Cell Biol 18:7383–7396
Mangus DA, Smith MM, McSweeney JM, Jacobson A (2004a) Identification of factors regulating poly(A) tail synthesis and maturation. Mol Cell Biol 24:4196–4206
Mangus DA, Evans MC, Agrin NS, Smith M, Gongidi P, Jacobson A (2004b) Positive and negative regulation of poly(A) nuclease. Mol Cell Biol 24:5521–5533
Marshall AN, Montealegre MC, Jiménez-López C, Lorenz MC, van Hoof A (2013) Alternative splicing and subfunctionalization generates functional diversity in fungal proteomes. PLoS Genet 9:e1003376
Matunis MJ, Matunis EL, Dreyfuss G (1993) PUB1: a major yeast poly(A)+RNA-binding protein. Mol Cell Biol 13:6114–6123
Menschaert G, Van Criekinge W, Notelaers T, Koch A, Crappé J, Gevaert K, Van Damme P (2013) Deep proteome coverage based on ribosome profiling aids mass spectrometry-based protein and peptide discovery and provides evidence of alternative translation products and near-cognate translation initiation events. Mol. Cell. Proteomics MCP 12:1780–1790
Miller C, Schwalb B, Maier K, Schulz D, Dümcke S, Zacher B, Mayer A, Sydow J, Marcinowski L, Dölken L et al (2011) Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast. Mol Syst Biol 7:458
Milligan L, Decourty L, Saveanu C, Rappsilber J, Ceulemans H, Jacquier A, Tollervey D (2008) A yeast exosome cofactor, Mpp6, functions in RNA surveillance and in the degradation of noncoding RNA transcripts. Mol Cell Biol 28:5446–5457
Min J, Heuertz RM, Zassenhaus HP (1993) Isolation and characterization of an NTP-dependent 3′-exoribonuclease from mitochondria of Saccharomyces cerevisiae. J Biol Chem 268:7350–7357
Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′–>5′ exoribonucleases. Cell 91:457–466
Mitchell SF, Jain S, She M, Parker R (2013) Global analysis of yeast mRNPs. Nat Struct Mol Biol 20:127–133
Moteki S, Price D (2002) Functional coupling of capping and transcription of mRNA. Mol Cell 10:599–609
Muhlrad D, Decker CJ, Parker R (1994) Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′–>3′ digestion of the transcript. Genes Dev 8:855–866
Munchel SE, Shultzaberger RK, Takizawa N, Weis K (2011) Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell 22:2787–2795
Narayanaswamy R, Levy M, Tsechansky M, Stovall GM, O’Connell JD, Mirrielees J, Ellington AD, Marcotte EM (2009) Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc Natl Acad Sci USA 106:10147–10152
Nissan T, Rajyaguru P, She M, Song H, Parker R (2010) Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol Cell 39:773–783
Nonet M, Scafe C, Sexton J, Young R (1987) Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol 7:1602–1611
Noree C, Sato BK, Broyer RM, Wilhelm JE (2010) Identification of novel filament-forming proteins in Saccharomyces cerevisiae and Drosophila melanogaster. J Cell Biol 190:541–551
OʹConnell JD, Zhao A, Ellington AD, Marcotte EM (2012) Dynamic reorganization of metabolic enzymes into intracellular bodies. Annu Rev Cell Dev Biol 28:89–111
Olivas W, Parker R (2000) The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. EMBO J 19:6602–6611
Osinga KA, De Vries E, Van der Horst G, Tabak HF (1984) Processing of yeast mitochondrial messenger RNAs at a conserved dodecamer sequence. EMBO J 3:829–834
Parker R (2012) RNA degradation in Saccharomyces cerevisae. Genetics 191:671–702
Pearson EL, Moore CL (2013) Dismantling promoter-driven RNA polymerase II transcription complexes in vitro by the termination factor Rat1. J Biol Chem 288:19750–19759
Pelechano V, Pérez-Ortín JE (2008) The transcriptional inhibitor thiolutin blocks mRNA degradation in yeast. Yeast 25:85–92
Pelechano V, Chávez S, Pérez-Ortín JE (2010) A complete set of nascent transcription rates for yeast genes. PLoS ONE 5:e15442
Perez-Ortin JE, de Miguel-Jimenez L, Chavez S (2012) Genome-wide studies of mRNA synthesis and degradation in eukaryotes. Biochim Biophys Acta-Gene Regul Mech 1819:604–615
Porrua O, Hobor F, Boulay J, Kubicek K, DʹAubenton-Carafa Y, Gudipati RK, Stefl R, Libri D (2012) In vivo SELEX reveals novel sequence and structural determinants of Nrd1-Nab3-Sen1-dependent transcription termination. EMBO J 31:3935–3948
Qiu C, Kershner A, Wang Y, Holley CP, Wilinski D, Keles S, Kimble J, Wickens M, Hall TMT (2012) Divergence of Pumilio/fem-3 mRNA binding factor (PUF) protein specificity through variations in an RNA-binding pocket. J Biol Chem 287:6949–6957
Quenault T, Lithgow T, Traven A (2011) PUF proteins: repression, activation and mRNA localization. Trends Cell Biol 21:104–112
Ramachandran V, Shah KH, Herman PK (2011) The cAMP-dependent protein kinase signaling pathway is a key regulator of P body foci formation. Mol Cell 43:973–981
Read RL, Martinho RG, Wang S-W, Carr AM, Norbury CJ (2002) Cytoplasmic poly(A) polymerases mediate cellular responses to S phase arrest. Proc Natl Acad Sci USA 99:12079–12084
Rissland OS, Norbury CJ (2009) Decapping is preceded by 3′ uridylation in a novel pathway of bulk mRNA turnover. Nat Struct Mol Biol 16:616–623
Rogowska AT, Puchta O, Czarnecka AM, Kaniak A, Stepien PP, Golik P (2006) Balance between transcription and RNA degradation is vital for Saccharomyces cerevisiae mitochondria: reduced transcription rescues the phenotype of deficient RNA degradation. Mol Biol Cell 17:1184–1193
Roth KM, Wolf MK, Rossi M, Butler JS (2005) The nuclear exosome contributes to autogenous control of NAB2 mRNA levels. Mol Cell Biol 25:1577–1585
Roth KM, Byam J, Fang F, Butler JS (2009) Regulation of NAB2 mRNA 3′-end formation requires the core exosome and the Trf4p component of the TRAMP complex. RNA 15:1045–1058
Sachs AB, Davis RW (1989) The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58:857–867
Sachs AB, Deardorff JA (1992) Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell 70:961–973
Sachs AB, Bond MW, Kornberg RD (1986) A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45:827–835
Sachs AB, Davis RW, Kornberg RD (1987) A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol Cell Biol 7:3268–3276
Saint-Georges Y, Garcia M, Delaveau T, Jourdren L, Le Crom S, Lemoine S, Tanty V, Devaux F, Jacq C (2008) Yeast mitochondrial biogenesis: a role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS ONE 3:e2293
Salgado-Garrido J, Bragado-Nilsson E, Kandels-Lewis S, Séraphin B (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J 18:3451–3462
San Paolo S, Vanacova S, Schenk L, Scherrer T, Blank D, Keller W, Gerber AP (2009) Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genet 5:e1000555
Santiveri CM, Mirassou Y, Rico-Lastres P, Martínez-Lumbreras S, Pérez-Cañadillas JM (2011) Pub1p C-terminal RRM domain interacts with Tif4631p through a conserved region neighbouring the Pab1p binding site. PLoS ONE 6:e24481
Sayani S, Chanfreau GF (2012) Sequential RNA degradation pathways provide a fail-safe mechanism to limit the accumulation of unspliced transcripts in Saccharomyces cerevisiae. RNA 18:1563–1572
Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A (2009) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16:56–62
Schmidt K, Xu Z, Mathews DH, Butler JS (2012) Air proteins control differential TRAMP substrate specificity for nuclear RNA surveillance. RNA 18:1934–1945
Schneider C, Anderson JT, Tollervey D (2007) The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol Cell 27:324–331
Schneider C, Leung E, Brown J, Tollervey D (2009) The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37:1127–1140
Schulz D, Schwalb B, Kiesel A, Baejen C, Torkler P, Gagneur J, Soeding J, Cramer P (2013) Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell 155:1075–1087
Schwartz D, Decker CJ, Parker R (2003) The enhancer of decapping proteins, Edc1p and Edc2p, bind RNA and stimulate the activity of the decapping enzyme. RNA 9:239–251
Shah KH, Zhang B, Ramachandran V, Herman PK (2013) Processing body and stress granule assembly occur by independent and differentially regulated pathways in Saccharomyces cerevisiae. Genetics 193:109–123
Shalem O, Dahan O, Levo M, Martinez MR, Furman I, Segal E, Pilpel Y (2008) Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Mol Syst Biol 4:223
Sharif H, Conti E (2013) Architecture of the Lsm1-7-Pat1 complex: a conserved assembly in eukaryotic mRNA turnover. Cell Rep 5:283–291
Sharif H, Ozgur S, Sharma K, Basquin C, Urlaub H, Conti E (2013) Structural analysis of the yeast Dhh1-Pat1 complex reveals how Dhh1 engages Pat1, Edc3 and RNA in mutually exclusive interactions. Nucleic Acids Res 41:8377–8390
Shatkin AJ, Manley JL (2000) The ends of the affair: capping and polyadenylation. Nat Struct Biol 7:838–842
Sheiness D, Puckett L, Darnell JE (1975) Possible relationship of poly(A) shortening to mRNA turnover. Proc Natl Acad Sci USA 72:1077–1081
Sheth U, Parker R (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300:805–808
Sinturel F, Bréchemier-Baey D, Kiledjian M, Condon C, Bénard L (2012) Activation of 5′-3′ exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast. Proc Natl Acad Sci USA 109:8264–8269
Sripati CE, Groner Y, Warner JR (1976) Methylated, blocked 5′ termini of yeast mRNA. J Biol Chem 251:2898–2904
Stead JA, Costello JL, Livingstone MJ, Mitchell P (2007) The PMC2NT domain of the catalytic exosome subunit Rrp6p provides the interface for binding with its cofactor Rrp47p, a nucleic acid-binding protein. Nucleic Acids Res 35:5556–5567
Steiger M, Carr-Schmid A, Schwartz DC, Kiledjian M, Parker R (2003) Analysis of recombinant yeast decapping enzyme. RNA 9:231–238
Stepien PP, Margossian SP, Landsman D, Butow RA (1992) The yeast nuclear gene suv3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc Natl Acad Sci USA 89:6813–6817
Stevens A (1978) An exoribonuclease from Saccharomyces cerevisiae: effect of modifications of 5′ end groups on the hydrolysis of substrates to 5′ mononucleotides. Biochem Biophys Res Commun 81:656–661
Stevens A (1980) An mRNA decapping enzyme from ribosomes of Saccharomyces cerevisiae. Biochem Biophys Res Commun 96:1150–1155
Stevens A (1988) mRNA-decapping enzyme from Saccharomyces cerevisiae: purification and unique specificity for long RNA chains. Mol Cell Biol 8:2005–2010
Sun M, Schwalb B, Schulz D, Pirkl N, Etzold S, Lariviere L, Maier KC, Seizl M, Tresch A, Cramer P (2012) Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res 22:1350–1359
Sun M, Schwalb B, Pirkl N, Maier KC, Schenk A, Failmezger H, Tresch A, Cramer P (2013) Global analysis of Eukaryotic mRNA degradation reveals Xrn1-dependent buffering of transcript levels. Mol Cell 52:52–62
Sweet T, Kovalak C, Coller J (2012) The DEAD-box protein Dhh1 promotes decapping by slowing ribosome movement. PLoS Biol 10:e1001342
Sweet TJ, Boyer B, Hu W, Baker KE, Coller J (2007) Microtubule disruption stimulates P-body formation. RNA 13:493–502
Swisher KD, Parker R (2010) Localization to, and effects of Pbp1, Pbp4, Lsm12, Dhh1, and Pab1 on stress granules in Saccharomyces cerevisiae. PLoS ONE 5:e10006
Synowsky SA, Heck AJR (2008) The yeast Ski complex is a hetero-tetramer. Protein Sci 17:119–125
Synowsky SA, van Wijk M, Raijmakers R, Heck AJR (2009) Comparative multiplexed mass spectrometric analyses of endogenously expressed yeast nuclear and cytoplasmic exosomes. J Mol Biol 385:1300–1313
Tenenbaum SA, Carson CC, Lager PJ, Keene JD (2000) Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc Natl Acad Sci USA 97:14085–14090
Tharun S, Parker R (2001) Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs. Mol Cell 8:1075–1083
Tharun S, He W, Mayes AE, Lennertz P, Beggs JD, Parker R (2000) Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404:515–518
Toh-E A, Guerry P, Wickner RB (1978) Chromosomal superkiller mutants of Saccharomyces cerevisiae. J Bacteriol 136:1002–1007
Trapman J, Retèl J, Planta RJ (1975) Ribosomal precursor particles from yeast. Exp Cell Res 90:95–104
Trcek T, Larson DR, Moldón A, Query CC, Singer RH (2011) Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell 147:1484–1497
Tuck AC, Tollervey D (2013) A Transcriptome-wide Atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 154:996–1009
Tucker M, Staples RR, Valencia-Sanchez MA, Muhlrad D, Parker R (2002) Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J 21:1427–1436
Turk EM, Das V, Seibert RD, Andrulis ED (2013) The mitochondrial RNA landscape of Saccharomyces cerevisiae. PLoS ONE 8:e78105
Udem SA, Kaufman K, Warner JR (1971) Small ribosomal ribonucleic acid species of Saccharomyces cerevisiae. J Bacteriol 105:101–106
Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302:1212–1215
Vanácová S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, Langen H, Keith G, Keller W (2005) A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 3:e189
Wang Z, Kiledjian M (2001) Functional link between the mammalian exosome and mRNA decapping. Cell 107:751–762
Wang L, Lewis MS, Johnson AW (2005) Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p. RNA 11:1291–1302
Wang SW, Toda T, MacCallum R, Harris AL, Norbury C (2000) Cid1, a fission yeast protein required for S-M checkpoint control when DNA polymerase delta or epsilon is inactivated. Mol Cell Biol 20:3234–3244
Wasmuth EV, Lima CD (2012) Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Mol Cell 48:133–144
Wegierski T, Dmochowska A, Jabłonowska A, Dziembowski A, Bartnik E, Stepień PP (1998) Yeast nuclear PET127 gene can suppress deletions of the SUV3 or DSS1 genes: an indication of a functional interaction between 3′ and 5′ ends of mitochondrial mRNAs. Acta Biochim Pol 45:935–940
Wery M, Ruidant S, Schillewaert S, Lepore N, Lafontaine DLJ (2009) The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 15:406–419
Wickens M, Bernstein DS, Kimble J, Parker R (2002) A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet TIG 18:150–157
Widner WR, Wickner RB (1993) Evidence that the SKI antiviral system of Saccharomyces cerevisiae acts by blocking expression of viral mRNA. Mol Cell Biol 13:4331–4341
Wiesenberger G, Fox TD (1997) Pet127p, a membrane-associated protein involved in stability and processing of Saccharomyces cerevisiae mitochondrial RNAs. Mol Cell Biol 17:2816–2824
Wlotzka W, Kudla G, Granneman S, Tollervey D (2011) The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 30:1790–1803
Wu D, Muhlrad D, Bowler MW, Liu Z, Parker R, Song H (2013) Lsm2 and Lsm3 bridge the interaction of the Lsm1-7 complex with Pat1 for decapping activation. Cell Res 24(2):233–246
Wyers F, Rougemaille M, Badis G, Rousselle J-C, Dufour M-E, Boulay J, Régnault B, Devaux F, Namane A, Séraphin B et al (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121:725–737
Xiang S, Cooper-Morgan A, Jiao X, Kiledjian M, Manley JL, Tong L (2009) Structure and function of the 5′–>3′ exoribonuclease Rat1 and its activating partner Rai1. Nature 458:784–788
Xue Y, Bai X, Lee I, Kallstrom G, Ho J, Brown J, Stevens A, Johnson AW (2000) Saccharomyces cerevisiae RAI1 (YGL246c) is homologous to human DOM3Z and encodes a protein that binds the nuclear exoribonuclease Rat1p. Mol Cell Biol 20:4006–4015
Yamasaki S, Anderson P (2008) Reprogramming mRNA translation during stress. Curr Opin Cell Biol 20:222–226
Zaman S, Lippman SI, Schneper L, Slonim N, Broach JR (2009) Glucose regulates transcription in yeast through a network of signaling pathways. Mol Syst Biol 5(245)
Acknowledgments
We thank Alain Jacquier and Frank Feuerbach for criticism of the manuscript. Funding was provided by the Institut Pasteur, the CNRS, and the French Agence Nationale de la Recherche (ANR-2011-BSV6-011-02 and ANR-2008-JCJC-0019-01/GENO-GIM).
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Fromont-Racine, M., Saveanu, C. (2014). mRNA Degradation and Decay. In: Sesma, A., von der Haar, T. (eds) Fungal RNA Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-05687-6_7
Download citation
DOI: https://doi.org/10.1007/978-3-319-05687-6_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-05686-9
Online ISBN: 978-3-319-05687-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)