#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Secondary Structure across the Bacterial Transcriptome Reveals Versatile Roles in mRNA Regulation and Function


Messenger RNA (mRNA) is intrinsically prone to form higher order structures which is optimized for mRNA stability in the cell. We took advantage of recent developments in high throughput sequencing technologies and coupled them with RNA structure-probing approaches to provide a high resolution view of the mRNA secondary structure of Escherichia coli on a global, transcriptome-wide scale. Our data highlight the contribution of mRNA secondary structure as a direct effector of a variety of processes, including translation initiation and termination, mRNA abundance and degradation. This goes beyond the primary function of mRNA as an information entity in the transfer of the genetic information and places it more centrally in regulating fidelity of translation.


Vyšlo v časopise: Secondary Structure across the Bacterial Transcriptome Reveals Versatile Roles in mRNA Regulation and Function. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005613
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005613

Souhrn

Messenger RNA (mRNA) is intrinsically prone to form higher order structures which is optimized for mRNA stability in the cell. We took advantage of recent developments in high throughput sequencing technologies and coupled them with RNA structure-probing approaches to provide a high resolution view of the mRNA secondary structure of Escherichia coli on a global, transcriptome-wide scale. Our data highlight the contribution of mRNA secondary structure as a direct effector of a variety of processes, including translation initiation and termination, mRNA abundance and degradation. This goes beyond the primary function of mRNA as an information entity in the transfer of the genetic information and places it more centrally in regulating fidelity of translation.


Zdroje

1. Kramer G, Boehringer D, Ban N, Bukau B (2009) The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat Struct Mol Biol 16: 589–597. doi: 10.1038/nsmb.1614 19491936

2. Pechmann S, Chartron JW, Frydman J (2014) Local slowdown of translation by nonoptimal codons promotes nascent-chain recognition by SRP in vivo. Nat Struct Mol Biol 21: 1100–1105. doi: 10.1038/nsmb.2919 25420103

3. Zhang G, Ignatova Z (2011) Folding at the birth of the nascent chain: coordinating translation with co-translational folding. Curr Opin Struct Biol 21: 25–31. doi: 10.1016/j.sbi.2010.10.008 21111607

4. Porschke D (1973) The dynamics of nucleic-acid single-strand conformation changes. Oligo- and polyriboadenylic acids. European journal of biochemistry / FEBS 39: 117–126. 4770785

5. Ding Y, Tang Y, Kwok CK, Zhang Y, Bevilacqua PC, et al. (2014) In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 505: 696–700. doi: 10.1038/nature12756 24270811

6. Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, et al. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature 467: 103–107. doi: 10.1038/nature09322 20811459

7. Li F, Zheng Q, Vandivier LE, Willmann MR, Chen Y, et al. (2012) Regulatory impact of RNA secondary structure across the Arabidopsis transcriptome. Plant Cell 24: 4346–4359. doi: 10.1105/tpc.112.104232 23150631

8. Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman JS (2014) Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505: 701–705. doi: 10.1038/nature12894 24336214

9. Spitale RC, Flynn RA, Zhang QC, Crisalli P, Lee B, et al. (2015) Structural imprints in vivo decode RNA regulatory mechanisms. Nature 519: 486–490. doi: 10.1038/nature14263 25799993

10. Sugimoto Y, Vigilante A, Darbo E, Zirra A, Militti C, et al. (2015) hiCLIP reveals the in vivo atlas of mRNA secondary structures recognized by Staufen 1. Nature 519: 491–494. doi: 10.1038/nature14280 25799984

11. Wan Y, Qu K, Zhang QC, Flynn RA, Manor O, et al. (2014) Landscape and variation of RNA secondary structure across the human transcriptome. Nature 505: 706–709. doi: 10.1038/nature12946 24476892

12. Kwok CK, Tang Y, Assmann SM, Bevilacqua PC (2015) The RNA structurome: transcriptome-wide structure probing with next-generation sequencing. Trends Biochem Sci 40: 221–232. doi: 10.1016/j.tibs.2015.02.005 25797096

13. Parsyan A, Svitkin Y, Shahbazian D, Gkogkas C, Lasko P, et al. (2011) mRNA helicases: the tacticians of translational control. Nat Rev Mol Cell Biol 12: 235–245. doi: 10.1038/nrm3083 21427765

14. Takyar S, Hickerson RP, Noller HF (2005) mRNA helicase activity of the ribosome. Cell 120: 49–58. 15652481

15. Burgess DJ (2015) RNA: Detailed probing of RNA structure in vivo. Nature reviews Genetics 16: 255. doi: 10.1038/nrg3939 25854184

16. Mahen EM, Watson PY, Cottrell JW, Fedor MJ (2010) mRNA secondary structures fold sequentially but exchange rapidly in vivo. PLoS Biol 8: e1000307. doi: 10.1371/journal.pbio.1000307 20161716

17. Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S, Cohen SN (2002) Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci U S A 99: 9697–9702. 12119387

18. Chen C, Zhang H, Broitman SL, Reiche M, Farrell I, et al. (2013) Dynamics of translation by single ribosomes through mRNA secondary structures. Nat Struct Mol Biol 20: 582–588. doi: 10.1038/nsmb.2544 23542154

19. Wen JD, Lancaster L, Hodges C, Zeri AC, Yoshimura SH, et al. (2008) Following translation by single ribosomes one codon at a time. Nature 452: 598–603. doi: 10.1038/nature06716 18327250

20. Zhang G, Hubalewska M, Ignatova Z (2009) Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat Struct Mol Biol 16: 274–280. doi: 10.1038/nsmb.1554 19198590

21. Gorochowski TE, Ignatova Z, Bovenberg RA, Roubos JA (2015) Trade-offs between tRNA abundance and mRNA secondary structure support smoothing of translation elongation rate. Nucleic Acids Res 43: 3022–3032. doi: 10.1093/nar/gkv199 25765653

22. Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129: 897–907. 1752426

23. Pop C, Rouskin S, Ingolia NT, Han L, Phizicky EM, et al. (2014) Causal signals between codon bias, mRNA structure, and the efficiency of translation and elongation. Mol Syst Biol 10: 770. doi: 10.15252/msb.20145524 25538139

24. Bentele K, Saffert P, Rauscher R, Ignatova Z, Bluthgen N (2013) Efficient translation initiation dictates codon usage at gene start. Mol Syst Biol 9: 675. doi: 10.1038/msb.2013.32 23774758

25. Goodman DB, Church GM, Kosuri S (2013) Causes and effects of N-terminal codon bias in bacterial genes. Science 342: 475–479. doi: 10.1126/science.1241934 24072823

26. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218–223. doi: 10.1126/science.1168978 19213877

27. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628. doi: 10.1038/nmeth.1226 18516045

28. Ehretsmann CP, Carpousis AJ, Krisch HM (1992) Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev 6: 149–159. 1730408

29. McDowall KJ, Lin-Chao S, Cohen SN (1994) A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269: 10790–10796. 7511606

30. Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Blasi U (2003) Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9: 1308–1314. 14561880

31. Li F, Zheng Q, Ryvkin P, Dragomir I, Desai Y, et al. (2012) Global analysis of RNA secondary structure in two metazoans. Cell Rep 1: 69–82. doi: 10.1016/j.celrep.2011.10.002 22832108

32. Incarnato D, Neri F, Anselmi F, Oliviero S (2014) Genome-wide profiling of mouse RNA secondary structures reveals key features of the mammalian transcriptome. Genome Biol 15: 491. 25323333

33. Shabalina SA, Ogurtsov AY, Spiridonov NA (2006) A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res 34: 2428–2437. 16682450

34. Iost I, Dreyfus M (2006) DEAD-box RNA helicases in Escherichia coli. Nucleic Acids Res 34: 4189–4197. 16935881

35. Resch A, Vecerek B, Palavra K, Blasi U (2010) Requirement of the CsdA DEAD-box helicase for low temperature riboregulation of rpoS mRNA. RNA Biol 7: 796–802. 21045550

36. Vakulskas CA, Pannuri A, Cortes-Selva D, Zere TR, Ahmer BM, et al. (2014) Global effects of the DEAD-box RNA helicase DeaD (CsdA) on gene expression over a broad range of temperatures. Mol Microbiol 92: 945–958. doi: 10.1111/mmi.12606 24708042

37. Fluman N, Navon S, Bibi E, Pilpel Y (2014) mRNA-programmed translation pauses in the targeting of E. coli membrane proteins. Elife 3.

38. Woolhead CA, McCormick PJ, Johnson AE (2004) Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116: 725–736. 15006354

39. Carrier TA, Keasling JD (1997) Controlling messenger RNA stability in bacteria: strategies for engineering gene expression. Biotechnol Prog 13: 699–708. 9413129

40. Mackie GA (2013) RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol 11: 45–57. doi: 10.1038/nrmicro2930 23241849

41. Clarke JE, Kime L, Romero AD, McDowall KJ (2015) Direct entry by RNase E is a major pathway for the degradation and processing of RNA in Escherichia coli. Nucleic Acids Res 42: 11733–11751.

42. Ma J, Campbell A, Karlin S (2002) Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. J Bacteriol 184: 5733–5745. 12270832

43. Wood CR, Boss MA, Patel TP, Emtage JS (1984) The influence of messenger RNA secondary structure on expression of an immunoglobulin heavy chain in Escherichia coli. Nucleic Acids Res 12: 3937–3950. 6328446

44. Osterman IA, Evfratov SA, Sergiev PV, Dontsova OA (2013) Comparison of mRNA features affecting translation initiation and reinitiation. Nucleic Acids Res 41: 474–486. doi: 10.1093/nar/gks989 23093605

45. Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, et al. (1992) Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol Microbiol 6: 1219–1229. 1375310

46. Studer SM, Joseph S (2006) Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol Cell 22: 105–115. 16600874

47. de Smit MH, van Duin J (2003) Translational standby sites: how ribosomes may deal with the rapid folding kinetics of mRNA. J Mol Biol 331: 737–743. 12909006

48. Salis HM, Mirsky EA, Voigt CA (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27: 946–950. doi: 10.1038/nbt.1568 19801975

49. Duval M, Korepanov A, Fuchsbauer O, Fechter P, Haller A, et al. (2013) Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. PLoS Biol 11: e1001731. doi: 10.1371/journal.pbio.1001731 24339747

50. Sengupta J, Agrawal RK, Frank J (2001) Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc Natl Acad Sci U S A 98: 11991–11996. 11593008

51. Bonetti B, Fu L, Moon J, Bedwell DM (1995) The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol 251: 334–345. 7650736

52. Bjornsson A, Mottagui-Tabar S, Isaksson LA (1996) Structure of the C-terminal end of the nascent peptide influences translation termination. The EMBO journal 15: 1696–1704. 8612594

53. Tork S, Hatin I, Rousset JP, Fabret C (2004) The major 5' determinant in stop codon read-through involves two adjacent adenines. Nucleic Acids Res 32: 415–421. 14736996

54. Callaghan AJ, Marcaida MJ, Stead JA, McDowall KJ, Scott WG, et al. (2005) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437: 1187–1191. 16237448

55. Koslover DJ, Callaghan AJ, Marcaida MJ, Garman EF, Martick M, et al. (2008) The crystal structure of the Escherichia coli RNase E apoprotein and a mechanism for RNA degradation. Structure 16: 1238–1244. doi: 10.1016/j.str.2008.04.017 18682225

56. Tripathy DR, Dinda AK, Dasgupta S (2013) A simple assay for the ribonuclease activity of ribonucleases in the presence of ethidium bromide. Anal Biochem 437: 126–129. doi: 10.1016/j.ab.2013.03.005 23499964

57. Green MR, Sambrook J (2012) Molecular Cloning: A Laboratory Manual New York: Cold Spring Haror Laboratory Press.

58. Cozzone AJ, Stent GS (1973) Movement of ribosomes over messenger RNA in polysomes of rel + and rel—Escherichia coli strains. J Mol Biol 76: 163–179. 4578097

59. Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835–840. doi: 10.1038/nature09267 20703300

60. Peters JE, Thate TE, Craig NL (2003) Definition of the Escherichia coli MC4100 genome by use of a DNA array. J Bacteriol 185: 2017–2021. 12618467

61. Zhang Y, Mooney RA, Grass JA, Sivaramakrishnan P, Herman C, et al. (2014) DksA guards elongating RNA polymerase against ribosome-stalling-induced arrest. Mol Cell 53: 766–778. doi: 10.1016/j.molcel.2014.02.005 24606919

62. Lorenz R, Bernhart SH, Honer Zu Siederdissen C, Tafer H, Flamm C, et al. (2011) ViennaRNA Package 2.0. Algorithms Mol Biol 6: 26. doi: 10.1186/1748-7188-6-26 22115189

63. Li GW, Oh E, Weissman JS (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484: 538–541. doi: 10.1038/nature10965 22456704

64. Soper TJ, Woodson SA (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14: 1907–1917. doi: 10.1261/rna.1110608 18658123

65. Schmidt M, Zheng P, Delihas N (1995) Secondary structures of Escherichia coli antisense micF RNA, the 5'-end of the target ompF mRNA, and the RNA/RNA duplex. Biochemistry 34: 3621–3631. 7534474

66. Woese CR, Magrum LJ, Gupta R, Siegel RB, Stahl DA, et al. (1980) Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res 8: 2275–2293. 6159576

67. Gutell RR, Lee JC, Cannone JJ (2002) The accuracy of ribosomal RNA comparative structure models. Curr Opin Struct Biol 12: 301–310. 12127448

68. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, et al. (2001) Crystal structure of the ribosome at 5.5 A resolution. Science 292: 883–896. 11283358

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#