Comparative Study between Transcriptionally- and Translationally-Acting Adenine Riboswitches Reveals Key Differences in Riboswitch Regulatory Mechanisms

English version České info

Many bacterial mRNAs are regulated at the transcriptional or translational level by ligand-binding elements called riboswitches. Although they both bind adenine, the adenine riboswitches of Bacillus subtilis and Vibrio vulnificus differ by controlling transcription and translation, respectively. Here, we demonstrate that, beyond the obvious difference in transcriptional and translational modulation, both adenine riboswitches exhibit different ligand binding properties and appear to operate under different regulation regimes (kinetic versus thermodynamic). While the B. subtilis pbuE riboswitch fully depends on co-transcriptional binding of adenine to function, the V. vulnificus add riboswitch can bind to adenine after transcription is completed and still perform translation regulation. Further investigation demonstrates that the rate of transcription is critical for the B. subtilis pbuE riboswitch to perform efficiently, which is in agreement with a co-transcriptional regulation. Our results suggest that the nature of gene regulation control, that is transcription or translation, may have a high importance in riboswitch regulatory mechanisms.

Vyšlo v časopise: Comparative Study between Transcriptionally- and Translationally-Acting Adenine Riboswitches Reveals Key Differences in Riboswitch Regulatory Mechanisms. PLoS Genet 7(1): e32767. doi:10.1371/journal.pgen.1001278
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001278

Souhrn

Zdroje

1. WatersLS

StorzG

2009 Regulatory RNAs in bacteria. Cell 136 615 628

2. KeeneJD

2007 RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8 533 543

3. SerganovA

PatelDJ

2007 Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat Rev Genet 8 776 790

4. RothA

BreakerRR

2009 The structural and functional diversity of metabolite-binding riboswitches. Annu Rev Biochem 78 305 334

5. BlouinS

MulhbacherJ

PenedoJC

LafontaineDA

2009 Riboswitches: ancient and promising genetic regulators. Chembiochem 10 400 416

6. CromieMJ

ShiY

LatifiT

GroismanEA

2006 An RNA sensor for intracellular Mg(2+). Cell 125 71 84

7. DannCE3rd

WakemanCA

SielingCL

BakerSC

IrnovI

2007 Structure and mechanism of a metal-sensing regulatory RNA. Cell 130 878 892

8. MoritaMT

TanakaY

KodamaTS

KyogokuY

YanagiH

1999 Translational induction of heat shock transcription factor sigma32: evidence for a built-in RNA thermosensor. Genes Dev 13 655 665

9. MoritaM

KanemoriM

YanagiH

YuraT

1999 Heat-induced synthesis of sigma32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J Bacteriol 181 401 410

10. SerganovA

2009 The long and the short of riboswitches. Curr Opin Struct Biol 19 251 259

11. DambachMD

WinklerWC

2009 Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12 161 169

12. HenkinTM

2008 Riboswitch RNAs: using RNA to sense cellular metabolism. Genes Dev 22 3383 3390

13. HenkinTM

2009 RNA-dependent RNA switches in bacteria. Methods Mol Biol 540 207 214

14. GrundyFJ

HenkinTM

1993 tRNA as a positive regulator of transcription antitermination in B. subtilis. Cell 74 475 482

15. LohE

DussurgetO

GripenlandJ

VaitkeviciusK

TiensuuT

2009 A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139 770 779

16. BateyRT

GilbertSD

MontangeRK

2004 Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432 411 415

17. SerganovA

YuanYR

PikovskayaO

PolonskaiaA

MalininaL

2004 Structural Basis for Discriminative Regulation of Gene Expression by Adenine- and Guanine-Sensing mRNAs. Chem Biol 11 1729 1741

18. MandalM

BoeseB

BarrickJE

WinklerWC

BreakerRR

2003 Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113 577 586

19. MandalM

BreakerRR

2004 Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat Struct Mol Biol 11 29 35

20. RiederR

LangK

GraberD

MicuraR

2007 Ligand-Induced Folding of the Adenosine Deaminase A-Riboswitch and Implications on Riboswitch Translational Control. Chembiochem 8 896 902

21. WickiserJK

CheahMT

BreakerRR

CrothersDM

2005 The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44 13404 13414

22. LemayJF

PenedoJC

TremblayR

LilleyDM

LafontaineDA

2006 Folding of the adenine riboswitch. Chem Biol 13 857 868

23. PanT

ArtsimovitchI

FangXW

LandickR

SosnickTR

1999 Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proc Natl Acad Sci U S A 96 9545 9550

24. WongTN

SosnickTR

PanT

2007 Folding of noncoding RNAs during transcription facilitated by pausing-induced nonnative structures. Proc Natl Acad Sci U S A 104 17995 18000

25. BrehmSL

CechTR

1983 Fate of an intervening sequence ribonucleic acid: excision and cyclization of the Tetrahymena ribosomal ribonucleic acid intervening sequence in vivo. Biochemistry 22 2390 2397

26. ZarrinkarPP

WilliamsonJR

1994 Kinetic intermediates in RNA folding. Science 265 918 924

27. ZhangF

RamsayES

WoodsonSA

1995 In vivo facilitation of Tetrahymena group I intron splicing in Escherichia coli pre-ribosomal RNA. RNA 1 284 292

28. WickiserJK

WinklerWC

BreakerRR

CrothersDM

2005 The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol Cell 18 49 60

29. LobanovKV

Korol'kovaNV

EreminaS

Errais LopesL

ProshkinSA

2007 [Mutations altering the specificity of the sensor RNA encoded by the Bacillus subtilis pbuE gene]. Genetika 43 859 864

30. LemayJF

LafontaineDA

2007 Core requirements of the adenine riboswitch aptamer for ligand binding. RNA 13 339 350

31. MulhbacherJ

LafontaineDA

2007 Ligand recognition determinants of guanine riboswitches. Nucleic Acids Res 35 5568 5580

32. GilbertSD

StoddardCD

WiseSJ

BateyRT

2006 Thermodynamic and Kinetic Characterization of Ligand Binding to the Purine Riboswitch Aptamer Domain. J Mol Biol 359 754 768

33. EskandariS

PrychynaO

LeungJ

AvdicD

O'NeillMA

2007 Ligand-Directed Dynamics of Adenine Riboswitch Conformers. J Am Chem Soc

34. PrychynaO

DahabiehMS

ChaoJ

O'NeillMA

2009 Sequence-dependent folding and unfolding of ligand-bound purine riboswitches. Biopolymers 91 953 965

35. WardDC

ReichE

StryerL

1969 Fluorescence studies of nucleotides and polynucleotides. I. Formycin, 2-aminopurine riboside, 2,6-diaminopurine riboside, and their derivatives. J Biol Chem 244 1228 1237

36. StiversJT

1998 2-Aminopurine fluorescence studies of base stacking interactions at abasic sites in DNA: metal-ion and base sequence effects. Nucleic Acids Res 26 3837 3844

37. JeanJM

HallKB

2001 2-Aminopurine fluorescence quenching and lifetimes: role of base stacking. Proc Natl Acad Sci U S A 98 37 41

38. MerinoEJ

WilkinsonKA

CoughlanJL

WeeksKM

2005 RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc 127 4223 4231

39. BennettBD

KimballEH

GaoM

OsterhoutR

Van DienSJ

2009 Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5 593 599

40. WinklerWC

NahviA

SudarsanN

BarrickJE

BreakerRR

2003 An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat Struct Biol 10 701 707

41. SudarsanN

WickiserJK

NakamuraS

EbertMS

BreakerRR

2003 An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev 17 2688 2697

42. GrundyFJ

LehmanSC

HenkinTM

2003 The L box regulon: lysine sensing by leader RNAs of bacterial lysine biosynthesis genes. Proc Natl Acad Sci U S A 100 12057 12062

43. MironovAS

GusarovI

RafikovR

LopezLE

ShatalinK

2002 Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111 747 756

44. WinklerWC

Cohen-ChalamishS

BreakerRR

2002 An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A 99 15908 15913

45. WinklerW

NahviA

BreakerRR

2002 Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419 952 956

46. BlouinS

LafontaineDA

2007 A loop-loop interaction and a K-turn motif located in the lysine aptamer domain are important for the riboswitch gene regulation control. RNA 13 1256 1267

47. SchaakJE

BabitzkeP

BevilacquaPC

2003 Phylogenetic conservation of RNA secondary and tertiary structure in the trpEDCFBA operon leader transcript in Bacillus. Rna 9 1502 1515

48. GreenleafWJ

FriedaKL

FosterDA

WoodsideMT

BlockSM

2008 Direct observation of hierarchical folding in single riboswitch aptamers. Science 319 630 633

49. McDowellJC

RobertsJW

JinDJ

GrossC

1994 Determination of intrinsic transcription termination efficiency by RNA polymerase elongation rate. Science 266 822 825

50. NechooshtanG

Elgrably-WeissM

SheafferA

WesthofE

AltuviaS

2009 A pH-responsive riboregulator. Genes Dev 23 2650 2662

51. FarnhamPJ

GreenblattJ

PlattT

1982 Effects of NusA protein on transcription termination in the tryptophan operon of Escherichia coli. Cell 29 945 951

52. VerhounigA

KarcherD

BockR

2010 Inducible gene expression from the plastid genome by a synthetic riboswitch. Proc Natl Acad Sci U S A 107 6204 6209

53. NygaardP

SaxildHH

2005 The purine efflux pump PbuE in Bacillus subtilis modulates expression of the PurR and G-box (XptR) regulons by adjusting the purine base pool size. J Bacteriol 187 791 794

54. NouX

KadnerRJ

2000 Adenosylcobalamin inhibits ribosome binding to btuB RNA. Proc Natl Acad Sci U S A 97 7190 7195

55. NahviA

SudarsanN

EbertMS

ZouX

BrownKL

2002 Genetic control by a metabolite binding mRNA. Chem Biol 9 1043

56. FuchsRT

GrundyFJ

HenkinTM

2006 The S(MK) box is a new SAM-binding RNA for translational regulation of SAM synthetase. Nat Struct Mol Biol 13 226 233

57. BairdNJ

Ferre-D'AmareAR

Idiosyncratically tuned switching behavior of riboswitch aptamer domains revealed by comparative small-angle X-ray scattering analysis. RNA 16 598 609

58. LangK

RiederR

MicuraR

2007 Ligand-induced folding of the thiM TPP riboswitch investigated by a structure-based fluorescence spectroscopic approach. Nucleic Acids Res 35 5370 5378

59. RentmeisterA

MayerG

KuhnN

FamulokM

2007 Conformational changes in the expression domain of the Escherichia coli thiM riboswitch. Nucleic Acids Res 35 3713 3722

60. BurmannBM

SchweimerK

LuoX

WahlMC

StittBL

2010 A NusE:NusG complex links transcription and translation. Science 328 501 504

61. RiederU

KreutzC

MicuraR

2010 Folding of a transcriptionally acting preQ1 riboswitch. Proc Natl Acad Sci U S A 107 10804 10809

62. KulshinaN

BairdNJ

Ferre-D'AmareAR

2009 Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat Struct Mol Biol 16 1212 1217

63. SmithKD

LipchockSV

AmesTD

WangJ

BreakerRR

2009 Structural basis of ligand binding by a c-di-GMP riboswitch. Nat Struct Mol Biol 16 1218 1223

64. PanT

SosnickT

2006 RNA folding during transcription. Annu Rev Biophys Biomol Struct 35 161 175

65. JohansenLE

NygaardP

LassenC

AgersoY

SaxildHH

2003 Definition of a second Bacillus subtilis pur regulon comprising the pur and xpt-pbuX operons plus pbuG, nupG (yxjA), and pbuE (ydhL). J Bacteriol 185 5200 5209

66. RepoilaF

MajdalaniN

GottesmanS

2003 Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 48 855 861

67. SimonsRW

HoumanF

KlecknerN

1987 Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53 85 96

68. DesnoyersG

MorissetteA

PrevostK

MasseE

2009 Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J 28 1551 1561

69. MasseE

GottesmanS

2002 A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99 4620 4625

70. PowellBS

RivasMP

CourtDL

NakamuraY

TurnboughCLJr

1994 Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res 22 5765 5766

71. PleissJA

DerrickML

UhlenbeckOC

1998 T7 RNA polymerase produces 5′ end heterogeneity during in vitro transcription from certain templates. Rna 4 1313 1317

72. FlanneryBP

TeukolskySA

VetterlingWT

1992 Numerical Recipes in Fortran, 2nd Edn Cambridge Cambridge University Press, UK

73. RistM

MarinoJ

2001 Association of an RNA kissing complex analyzed using 2-aminopurine fluorescence. Nucleic Acids Res 29 2401 2408

74. PrevostK

SalvailH

DesnoyersG

JacquesJF

PhaneufE

2007 The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol Microbiol 64 1260 1273

75. QiY

HulettFM

1998 PhoP-P and RNA polymerase sigmaA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: PhoP-P activator sites within the coding region stimulate transcription in vitro. Mol Microbiol 28 1187 1197

76. HelmannJD

2003 Purification of Bacillus subtilis RNA polymerase and associated factors. Methods Enzymol 370 10 24

77. MandalM

LeeM

BarrickJE

WeinbergZ

EmilssonGM

2004 A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306 275 279

78. GrundyFJ

WinklerWC

HenkinTM

2002 tRNA-mediated transcription antitermination in vitro: codon-anticodon pairing independent of the ribosome. Proc Natl Acad Sci U S A 99 11121 11126

79. PuglisiJD

TinocoIJr

1989 Absorbance melting curves of RNA. Methods Enzymol 180 304 325

80. AlbergoDD

MarkyLA

BreslauerKJ

TurnerDH

1981 Thermodynamics of (dG–dC)3 double-helix formation in water and deuterium oxide. Biochemistry 20 1409 1413