The Small RNA Rli27 Regulates a Cell Wall Protein inside Eukaryotic Cells by Targeting a Long 5′-UTR Variant

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Listeria monocytogenes has evolved to adapt to numerous environments, including the intracellular niche of eukaryotic cells. Small RNAs (sRNA) play important regulatory roles in changing environments, and are thus predicted to modulate L. monocytogenes adaption to the intracellular lifestyle. This study shows how the regulatory activity of an sRNA on a defined target is restricted to bacteria in the intracellular infection phase. This regulation relies on a long (234-nucleotide) 5′-UTR that bears the sRNA-binding site present in a transcript variant that is upregulated by intracellular L. monocytogenes. The concomitant increase in both the target transcript containing the long 5′-UTR and the sRNA, which is postulated to facilitate opening of the Shine-Dalgarno site, culminates in markedly higher protein levels in intracellular bacteria. The limited amounts of both the target and the regulator in extracellular bacteria ensure that production of this bacterial protein is confined mainly to the host rather than the non-host environment.

Vyšlo v časopise: The Small RNA Rli27 Regulates a Cell Wall Protein inside Eukaryotic Cells by Targeting a Long 5′-UTR Variant. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004765
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004765

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Zdroje

1. CossartP, Toledo-AranaA (2008) Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10 : 1041–1050.

2. HamonM, BierneH, CossartP (2006) Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4 : 423–434.

3. Vazquez-BolandJA, KuhnM, BercheP, ChakrabortyT, Dominguez-BernalG, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14 : 584–640.

4. CossartP (2011) Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc Natl Acad Sci U S A 108 : 19484–19491.

5. DoumithM, CazaletC, SimoesN, FrangeulL, JacquetC, et al. (2004) New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect Immun 72 : 1072–1083.

6. GaillardJL, BercheP, FrehelC, GouinE, CossartP (1991) Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65 : 1127–1141.

7. BuchrieserC (2007) Biodiversity of the species Listeria monocytogenes and the genus Listeria. Microbes Infect 9 : 1147–1155.

8. ReisO, SousaS, CamejoA, VilliersV, GouinE, et al. (2010) LapB, a novel Listeria monocytogenes LPXTG surface adhesin, required for entry into eukaryotic cells and virulence. J Infect Dis 202 : 551–562.

9. MariscottiJF, QueredaJJ, Garcia-Del PortilloF, PucciarelliMG (2014) The Listeria monocytogenes LPXTG surface protein Lmo1413 is an invasin with capacity to bind mucin. Int J Med Microbiol 304 : 393–404.

10. PucciarelliMG, CalvoE, SabetC, BierneH, CossartP, et al. (2005) Identification of substrates of the Listeria monocytogenes sortases A and B by a non-gel proteomic analysis. Proteomics 5 : 4808–4817.

11. MariscottiJF, QueredaJJ, PucciarelliMG (2012) Contribution of sortase A to the regulation of Listeria monocytogenes LPXTG surface proteins. International Microbiology 15 : 43–51.

12. Garcia-del PortilloF, CalvoE, D'OrazioV, PucciarelliMG (2011) Association of ActA to peptidoglycan revealed by cell wall proteomics of intracellular Listeria monocytogenes. J Biol Chem 286 : 34675–34689.

13. Valentin-HansenP, JohansenJ, RasmussenAA (2007) Small RNAs controlling outer membrane porins. Curr Opin Microbiol 10 : 152–155.

14. MraheilMA, BillionA, MohamedW, MukherjeeK, KuenneC, et al. (2011) The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res 39 : 4235–4248.

15. Toledo-AranaA, RepoilaF, CossartP (2007) Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10 : 182–188.

16. PapenfortK, VogelJ (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8 : 116–127.

17. Toledo-AranaA, DussurgetO, NikitasG, SestoN, Guet-RevilletH, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459 : 950–956.

18. WurtzelO, SestoN, MellinJR, KarunkerI, EdelheitS, et al. (2012) Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8 : 583.

19. MellinJR, CossartP (2012) The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA Biol 9 : 372–378.

20. MujahidS, BergholzTM, OliverHF, BoorKJ, WiedmannM (2012) Exploration of the role of the non-coding RNA SbrE in L. monocytogenes stress response. Int J Mol Sci 14 : 378–393.

21. NielsenJS, OlsenAS, BondeM, Valentin-HansenP, KallipolitisBH (2008) Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J Bacteriol 190 : 6264–6270.

22. NielsenJS, LarsenMH, LillebaekEM, BergholzTM, ChristiansenMH, et al. (2011) A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS One 6: e19019.

23. SieversS, LillebaekEM, JacobsenK, LundA, MollerupMS, et al. (2014) A multicopy sRNA of Listeria monocytogenes regulates expression of the virulence adhesin LapB. Nucleic Acids Res doi:10.1093/nar/gku630

24. ChatterjeeSS, HossainH, OttenS, KuenneC, KuchminaK, et al. (2006) Intracellular gene expression profile of Listeria monocytogenes. Infect Immun 74 : 1323–1338.

25. LohE, GripenlandJ, JohanssonJ (2006) Control of Listeria monocytogenes virulence by 5′-untranslated RNA. Trends Microbiol 14 : 294–298.

26. Seifart GomesC, IzarB, PazanF, MohamedW, MraheilMA, et al. (2011) Universal Stress Proteins Are Important for Oxidative and Acid Stress Resistance and Growth of Listeria monocytogenes EGD-e In Vitro and In Vivo. PLoS One 6: e24965.

27. GlaserP, FrangeulL, BuchrieserC, RusniokC, AmendA, et al. (2001) Comparative genomics of Listeria species. Science 294 : 849–852.

28. TjadenB (2008) TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 36: W109–113.

29. Padalon-BrauchG, HershbergR, Elgrably-WeissM, BaruchK, RosenshineI, et al. (2008) Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36 : 1913–1927.

30. QueredaJJ, PucciarelliMG (2014) Deletion of the membrane protein Lmo0412 increases the virulence of Listeria monocytogenes. Microbes Infect doi 10.1016/j.micinf.2014.07.002

31. MarraffiniLA, DedentAC, SchneewindO (2006) Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol Mol Biol Rev 70 : 192–221.

32. BierneH, CossartP (2007) Listeria monocytogenes surface proteins: from genome predictions to function. Microbiol Mol Biol Rev 71 : 377–397.

33. DreisbachA, HempelK, BuistG, HeckerM, BecherD, et al. (2010) Profiling the surfacome of Staphylococcus aureus. Proteomics 10 : 3082–3096.

34. MilohanicE, GlaserP, CoppeeJY, FrangeulL, VegaY, et al. (2003) Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 47 : 1613–1625.

35. IrnovI, SharmaCM, VogelJ, WinklerWC (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38 : 6637–6651.

36. FrohlichKS, PapenfortK, FeketeA, VogelJ (2013) A small RNA activates CFA synthase by isoform-specific mRNA stabilization. EMBO J 32 : 2963–2979.

37. SharmaCM, HoffmannS, DarfeuilleF, ReignierJ, FindeissS, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464 : 250–255.

38. SoperT, MandinP, MajdalaniN, GottesmanS, WoodsonSA (2010) Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci U S A 107 : 9602–9607.

39. WongKK, BouwerHG, FreitagNE (2004) Evidence implicating the 5′ untranslated region of Listeria monocytogenes actA in the regulation of bacterial actin-based motility. Cell Microbiol 6 : 155–166.

40. JohanssonJ, MandinP, RenzoniA, ChiaruttiniC, SpringerM, et al. (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110 : 551–561.

41. ShenA, HigginsDE (2005) The 5′ untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Mol Microbiol 57 : 1460–1473.

42. DramsiS, BiswasI, MaguinE, BraunL, MastroeniP, et al. (1995) Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 16 : 251–261.

43. ArnaudM, ChastanetA, DebarbouilleM (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70 : 6887–6891.

44. TasaraT, StephanR (2007) Evaluation of housekeeping genes in Listeria monocytogenes as potential internal control references for normalizing mRNA expression levels in stress adaptation models using real-time PCR. FEMS Microbiol Lett 269 : 265–272.

45. UntergasserA, CutcutacheI, KoressaarT, YeJ, FairclothBC, et al. (2012) Primer3–new capabilities and interfaces. Nucleic Acids Res 40: e115.

46. OrtegaAD, Gonzalo-AsensioJ, Garcia-del PortilloF (2012) Dynamics of Salmonella small RNA expression in non-growing bacteria located inside eukaryotic cells. RNA Biol 9 : 469–488.

47. ArgamanL, HershbergR, VogelJ, BejeranoG, WagnerEG, et al. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11 : 941–950.