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

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Quereda, Juan J ^a,c   Ortega, Álvaro D ^a,d   Pucciarelli, M Graciela ^a,b   García del Portillo, Francisco ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; CELL MEMBRANE PROTEIN; PROTEIN LMO0514; RLI27; UNCLASSIFIED DRUG; 5' UNTRANSLATED REGION; MESSENGER RNA; SMALL UNTRANSLATED RNA;

5' UNTRANSLATED REGION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; BINDING SITE; BIOINFORMATICS; CHROMOSOME MUTATION; CONTROLLED STUDY; EUKARYOTIC CELL; FRACTIONATION; GEL MOBILITY SHIFT ASSAY; GENE AMPLIFICATION; GENE EXPRESSION; GENOMICS; LISTERIA; LISTERIA INNOCUA; LISTERIA MONOCYTOGENES; LISTERIA WELSHIMERI; MOLECULAR INTERACTION; NONHUMAN; NORTHERN BLOTTING; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; UPREGULATION; WESTERN BLOTTING; WILD TYPE; BIOSYNTHESIS; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOGENICITY; VIRULENCE;

5' UNTRANSLATED REGIONS; BACTERIAL PROTEINS; BASE SEQUENCE; CELL WALL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LISTERIA MONOCYTOGENES; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; VIRULENCE;

EID: 84908355671     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004765     Document Type: Article

References (47)

1. Cossart P, Toledo-Arana A, (2008) Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10: 1041–1050.
2. Hamon M, Bierne H, Cossart P, (2006) Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4: 423–434.
3. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584–640.
4. Cossart P, (2011) Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc Natl Acad Sci U S A 108: 19484–19491.
5. Doumith M, Cazalet C, Simoes N, Frangeul L, Jacquet C, 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. Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P, (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. Buchrieser C, (2007) Biodiversity of the species Listeria monocytogenes and the genus Listeria. Microbes Infect 9: 1147–1155.
8. Reis O, Sousa S, Camejo A, Villiers V, Gouin E, 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. Mariscotti JF, Quereda JJ, Garcia-Del Portillo F, Pucciarelli MG, (2014) The Listeria monocytogenes LPXTG surface protein Lmo1413 is an invasin with capacity to bind mucin. Int J Med Microbiol 304: 393–404.
10. Pucciarelli MG, Calvo E, Sabet C, Bierne H, Cossart P, 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. Mariscotti JF, Quereda JJ, Pucciarelli MG, (2012) Contribution of sortase A to the regulation of Listeria monocytogenes LPXTG surface proteins. International Microbiology 15: 43–51.
12. Garcia-del Portillo F, Calvo E, D'Orazio V, Pucciarelli MG, (2011) Association of ActA to peptidoglycan revealed by cell wall proteomics of intracellular Listeria monocytogenes. J Biol Chem 286: 34675–34689.
13. Valentin-Hansen P, Johansen J, Rasmussen AA, (2007) Small RNAs controlling outer membrane porins. Curr Opin Microbiol 10: 152–155.
14. Mraheil MA, Billion A, Mohamed W, Mukherjee K, Kuenne C, et al. (2011) The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res 39: 4235–4248.
15. Toledo-Arana A, Repoila F, Cossart P, (2007) Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10: 182–188.
16. Papenfort K, Vogel J, (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8: 116–127.
17. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950–956.
18. Wurtzel O, Sesto N, Mellin JR, Karunker I, Edelheit S, et al. (2012) Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8: 583.
19. Mellin JR, Cossart P, (2012) The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA Biol 9: 372–378.
20. Mujahid S, Bergholz TM, Oliver HF, Boor KJ, Wiedmann M, (2012) Exploration of the role of the non-coding RNA SbrE in L. monocytogenes stress response. Int J Mol Sci 14: 378–393.
21. Nielsen JS, Olsen AS, Bonde M, Valentin-Hansen P, Kallipolitis BH, (2008) Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J Bacteriol 190: 6264–6270.
22. Nielsen JS, Larsen MH, Lillebaek EM, Bergholz TM, Christiansen MH, et al. (2011) A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS One 6: e19019.
23. Sievers S, Lillebaek EM, Jacobsen K, Lund A, Mollerup MS, 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. Chatterjee SS, Hossain H, Otten S, Kuenne C, Kuchmina K, et al. (2006) Intracellular gene expression profile of Listeria monocytogenes. Infect Immun 74: 1323–1338.
25. Loh E, Gripenland J, Johansson J, (2006) Control of Listeria monocytogenes virulence by 5′-untranslated RNA. Trends Microbiol 14: 294–298.
26. Seifart Gomes C, Izar B, Pazan F, Mohamed W, Mraheil MA, 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. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science 294: 849–852.
28. Tjaden B, (2008) TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 36: W109–113.
29. Padalon-Brauch G, Hershberg R, Elgrably-Weiss M, Baruch K, Rosenshine I, 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. Quereda JJ, Pucciarelli MG, (2014) Deletion of the membrane protein Lmo0412 increases the virulence of Listeria monocytogenes. Microbes Infect doi 10.1016/j.micinf.2014.07.002
31. Marraffini LA, Dedent AC, Schneewind O, (2006) Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol Mol Biol Rev 70: 192–221.
32. Bierne H, Cossart P, (2007) Listeria monocytogenes surface proteins: from genome predictions to function. Microbiol Mol Biol Rev 71: 377–397.
33. Dreisbach A, Hempel K, Buist G, Hecker M, Becher D, et al. (2010) Profiling the surfacome of Staphylococcus aureus. Proteomics 10: 3082–3096.
34. Milohanic E, Glaser P, Coppee JY, Frangeul L, Vega Y, et al. (2003) Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 47: 1613–1625.
35. Irnov I, Sharma CM, Vogel J, Winkler WC, (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38: 6637–6651.
36. Frohlich KS, Papenfort K, Fekete A, Vogel J, (2013) A small RNA activates CFA synthase by isoform-specific mRNA stabilization. EMBO J 32: 2963–2979.
37. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250–255.
38. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA, (2010) Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci U S A 107: 9602–9607.
39. Wong KK, Bouwer HG, Freitag NE, (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. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, et al. (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110: 551–561.
41. Shen A, Higgins DE, (2005) The 5′ untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Mol Microbiol 57: 1460–1473.
42. Dramsi S, Biswas I, Maguin E, Braun L, Mastroeni P, 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. Arnaud M, Chastanet A, Debarbouille M, (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887–6891.
44. Tasara T, Stephan R, (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. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, et al. (2012) Primer3–new capabilities and interfaces. Nucleic Acids Res 40: e115.
46. Ortega AD, Gonzalo-Asensio J, Garcia-del Portillo F, (2012) Dynamics of Salmonella small RNA expression in non-growing bacteria located inside eukaryotic cells. RNA Biol 9: 469–488.
47. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, et al. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11: 941–950.