Deep sequencing shows multiple oligouridylations are required for 3' to 5' degradation of histone mRNAs on polyribosomes

Molecular Cell

Volumn 53, Issue 6, 2014, Pages 1020-1030

  Slevin, Michael K ^a,b   Meaux, Stacie ^a,b   Welch, Joshua D ^c   Bigler, Rebecca ^b   Miliani de Marval, PaulaL ^b   Su, Wei ^d   Rhoads, Robert E ^d   Prins, Jan F ^c   Marzluff, William F ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c Brooks Computer Science Building   (United States)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYCLOHEXIMIDE; EXONUCLEASE; HISTONE; HISTONE H2A; HISTONE MESSENGER RNA; MESSENGER RNA; UNCLASSIFIED DRUG; CAPPED RNA; DIS3L2 EXONUCLEASE; PM EXONUCLEASE; RIBOSOME RNA; SCL 100 EXONUCLEASE; SMALL INTERFERING RNA;

ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; EXOSOME; HELA CELL; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN GENOME; OLIGOURIDYLATION; POLYSOME; RNA DEGRADATION; RNA SEQUENCE; STOP CODON; TRANSLATION INITIATION; 3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; FEMALE; GENE SILENCING; HISTONE CODE; NUCLEOTIDE SEQUENCE; RNA TRANSLATION; SIGNAL TRANSDUCTION;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; CODON; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; HELA CELLS; HISTONES; HUMANS; JURKAT CELLS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; POLYRIBOSOMES; RNA STABILITY; S PHASE; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; URIDINE;

EID: 84896327838     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.02.027     Document Type: Article

References (39)

1. Anderson J.S., Parker R.P. The 3' to 5' degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3' to 5' exonucleases of the exosome complex. EMBO J. 1998, 17:1497-1506.
2. Caponigro G., Parker R. Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol. Rev. 1996, 60:233-249.
3. Caruccio N., Ross J. Purification of a human polyribosome-associated 3' to 5' exoribonuclease. J.Biol. Chem. 1994, 269:31814-31821.
4. Chang H.M., Triboulet R., Thornton J.E., Gregory R.I. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 2013, 497:244-248.
5. Decker C.J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 1993, 7:1632-1643.
6. Dobin A., Davis C.A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., Gingeras T.R. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29:15-21.
7. Garneau N.L., Wilusz J., Wilusz C.J. The highways and byways ofmRNA decay. Nat. Rev. Mol. Cell Biol. 2007, 8:113-126.
8. Graves R.A., Marzluff W.F. Rapid reversible changes in the rate of histone gene transcription and histone mRNA levels in mouse myeloma cells. Mol. Cell. Biol. 1984, 4:351-357.
9. Graves R.A., Pandey N.B., Chodchoy N., Marzluff W.F. Translation is required for regulation of histone mRNA degradation. Cell 1987, 48:615-626.
10. Harris M.E., Böhni R., Schneiderman M.H., Ramamurthy L., Schümperli D., Marzluff W.F. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol. Cell. Biol. 1991, 11:2416-2424.
11. Heo I., Joo C., Kim Y.K., Ha M., Yoon M.J., Cho J., Yeom K.H., Han J., Kim V.N. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009, 138:696-708.
12. Hoefig K.P., Rath N., Heinz G.A., Wolf C., Dameris J., Schepers A., Kremmer E., Ansel K.M., Heissmeyer V. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nat. Struct. Mol. Biol. 2013, 20:73-81.
13. Kappen L.S., Goldberg I.H. Analysis of the two steps in polypeptide chain initiation inhibited by pactamycin. Biochemistry 1976, 15:811-818.
14. Kaygun H., Marzluff W.F. Translation termination is involved in histone mRNA degradation when DNA replication is inhibited. Mol. Cell. Biol. 2005, 25:6879-6888.
15. Li J., Yang Z., Yu B., Liu J., Chen X. Methylation protects miRNAs and siRNAs from a 3'-end uridylation activity in Arabidopsis. Curr. Biol. 2005, 15:1501-1507.
16. Lyons S.M., Ricciardi A.S., Guo A.Y., Kambach C., Marzluff W.F. The C-terminal extension of Lsm4 interacts directly with the 3' end of the histone mRNP and is required for efficient histone mRNA degradation. RNA 2014, 20:88-102.
17. Malecki M., Viegas S.C., Carneiro T., Golik P., Dressaire C., Ferreira M.G., Arraiano C.M. The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J. 2013, 32:1842-1854.
18. Marzluff W.F., Gongidi P., Woods K.R., Jin J.P., Maltais L.J. Thehuman and mouse replication-dependent histone genes. Genomics 2002, 80:487-498.
19. Marzluff W.F., Wagner E.J., Duronio R.J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 2008, 9:843-854.
20. Mitchell P., Tollervey D. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3'->5' degradation. Mol. Cell 2003, 11:1405-1413.
21. Mullen T.E., Marzluff W.F. Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5' to 3' and 3' to 5'. Genes Dev. 2008, 22:50-65.
22. Munns T.W., Liszewski M.K., Sims H.F. Characterization of antibodies specific for N6-methyladenosine and for 7-methylguanosine. Biochemistry 1977, 16:2163-2168.
23. Newman M.A., Mani V., Hammond S.M. Deep sequencing of microRNA precursors reveals extensive 3' end modification. RNA 2011, 17:1795-1803.
24. Parker R., Song H. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 2004, 11:121-127.
25. Passos D.O., Doma M.K., Shoemaker C.J., Muhlrad D., Green R., Weissman J., Hollien J., Parker R. Analysis of Dom34 and its function in no-go decay. Mol. Biol. Cell 2009, 20:3025-3032.
26. Ross J., Peltz S.W., Kobs G., Brewer G. Histone mRNA degradation invivo: the first detectable step occurs at or near the 3' terminus. Mol. Cell. Biol. 1986, 6:4362-4371.
27. Ross J., Kobs G., Brewer G., Peltz S.W. Properties of the exonuclease activity that degrades H4 histone mRNA. J.Biol. Chem. 1987, 262:9374-9381.
28. Saito S., Hosoda N., Hoshino S. The Hbs1-Dom34 protein complex functions in non-stop mRNA decay in mammalian cells. J.Biol. Chem. 2013, 288:17832-17843.
29. Scharl E.C., Steitz J.A. The site of 3' end formation of histone messenger RNA is a fixed distance from the downstream element recognized by the U7 snRNP. EMBO J. 1994, 13:2432-2440.
30. Shen B., Goodman H.M. Uridine addition after microRNA-directed cleavage. Science 2004, 306:997.
31. Song M.G., Kiledjian M. 3' Terminal oligo U-tract-mediated stimulation of decapping. RNA 2007, 13:2356-2365.
32. Stimac E., Groppi V.E., Coffino P. Inhibition of protein synthesis stabilizes histone mRNA. Mol. Cell. Biol. 1984, 4:2082-2090.
33. Su W., Slepenkov S.V., Slevin M.K., Lyons S.M., Ziemniak M., Kowalska J., Darzynkiewicz E., Jemielity J., Marzluff W.F., Rhoads R.E. mRNAs containing the histone 3' stem-loop are degraded primarily by decapping mediated by oligouridylation of the 3' end. RNA 2013, 19:1-16.
34. Tan D., Marzluff W.F., Dominski Z., Tong L. Structure of histone mRNA stem-loop, human stem-loop binding protein, and 3'hExo ternary complex. Science 2013, 339:318-321.
35. Thornton J.E., Chang H.M., Piskounova E., Gregory R.I. Lin28-mediated control of let-7 microRNA expression by alternative TUTases Zcchc11 (TUT4) and Zcchc6 (TUT7). RNA 2012, 18:1875-1885.
36. Tomecki R., Kristiansen M.S., Lykke-Andersen S., Chlebowski A., Larsen K.M., Szczesny R.J., Drazkowska K., Pastula A., Andersen J.S., Stepien P.P., et al. The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J. 2010, 29:2342-2357.
37. Wilusz J.E., JnBaptiste C.K., Lu L.Y., Kuhn C.D., Joshua-Tor L., Sharp P.A. A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 2012, 26:2392-2407.
38. Yang X.C., Purdy M., Marzluff W.F., Dominski Z. Characterization of 3'hExo, a 3' exonuclease specifically interacting with the 3' end of histone mRNA. J.Biol. Chem. 2006, 281:30447-30454.
39. Zhao Y., Mo B., Chen X. Mechanisms that impact microRNA stability in plants. RNA Biol. 2012, 9:1218-1223.