Bacterial and cellular RNAs at work during Listeria infection

Future Microbiology

Volumn 9, Issue 9, 2014, Pages 1025-1037

  Sesto, Nina ^a,b,c   Koutero, Mikael ^a,b,c   Cossart, Pascale ^a,b,c  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c USC 2020   (France)

Author keywords

asRNA; CRISPR; excludon; immune response; miRNA; riboswitch; RNA secretion; sRNA; thermosensor; virulence

Indexed keywords

BACTERIAL RNA; COMPLEMENTARY RNA; CYANOCOBALAMIN; LONG UNTRANSLATED RNA; MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE III; RNA; TRANSFER RNA; MICRORNA; VIRULENCE FACTOR;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIAL VIRULENCE; BACTERIOPHAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA STRAND; EPITHELIUM CELL; FLAGELLUM; HELICOBACTER PYLORI; HERPES VIRUS SAIMIRI; IMMUNE RESPONSE; LISTERIA INNOCUA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MYCOBACTERIUM AVIUM; NEISSERIA GONORRHOEAE; NONHUMAN; PHENOTYPE; PROTEIN SECONDARY STRUCTURE; REGULATORY MECHANISM; TYPE IV SECRETION SYSTEM; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA;

BACTERIA (MICROORGANISMS); LISTERIA;

GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICROBIOTA; MICRORNAS; RNA, BACTERIAL; VIRULENCE FACTORS;

EID: 84908123897     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.14.79     Document Type: Article

References (81)

1. Cossart P. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl Acad. Sci. USA 108(49), 19484-19491 (2011).
2. Mostowy S, Cossart P. Virulence factors that modulate the cell biology of Listeria infection and the host response. Adv. Immunol. 113, 19-32 (2012).
3. Lebreton A, Cossart P, Bierne H. Bacteria tune interferon responses by playing with chromatin. Virulence 3(1), 87-91 (2012).
4. Stavru F, Archambaud C, Cossart P. Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol. Rev. 240(1), 160-184 (2011).
5. Caldelari I, Chao Y, Romby P, Vogel J. RNA-mediated regulation in pathogenic bacteria. Cold Spring Harb. Perspect. Med. 3(9), a010298 (2013).
6. Storz G, Vogel J, Wassarman KM. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 43(6), 880-891 (2011).
7. Christiansen JK, Nielsen JS, Ebersbach T, Valentin-Hansen P, Sogaard-Andersen L, Kallipolitis BH. Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12(7), 1383-1396 (2006).
8. Mandin P, Repoila F, Vergassola M, Geissmann T, Cossart P. Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res. 35(3), 962-974 (2007).
9. Behrens S, Widder S, Mannala GK, et al. Ultra deep sequencing of Listeria monocytogenes sRNA transcriptome revealed new antisense RNAs. PLoS ONE 9(2), e83979 (2014).
10. Mraheil MA, Billion A, Mohamed W, et al. The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res. 39(10), 4235-4248 (2011).
11. Oliver HF, Orsi RH, Ponnala L, et al. Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs. BMC Genomics 10, 641 (2009).
12. Toledo-Arana A, Dussurget O, Nikitas G, et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459(7249), 950-956 (2009).
13. Wurtzel O, Sesto N, Mellin JR, et al. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol. Syst. Biol. 8, 583 (2012).
14. Mellin JR, Cossart P. The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA Biol. 9(4), 372-378 (2012).
15. O'connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10(2), 111-122 (2010).
16. Sun K, Lai EC. Adult-specific functions of animal microRNAs. Nat. Rev. Genet. 14(8), 535-548 (2013).
17. Rottiers V, Naar AM. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 13(4), 239-250 (2012).
18. Geisler S, Coller J. RNA in unexpected places: long non-coding RNA functions in Diverse cellular contexts. Nat. Rev. Mol. Cell Biol. 14(11), 699-712 (2013).
19. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19(1), 92-105 (2009).
20. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, Cossart P. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110(5), 551-561 (2002).
21. Loh E, Dussurget O, Gripenland J, et al. A trans-Acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139(4), 770-779 (2009).
22. Sesto N, Wurtzel O, Archambaud C, Sorek R, Cossart P. The excludon: a new concept in bacterial antisense RNA-mediated gene regulation. Nat. Rev. Microbiol. 11(2), 75-82 (2013).
23. Mellin JR, Tiensuu T, Becavin C, Gouin E, Johansson J, Cossart P. A riboswitch-regulated antisense RNA in Listeria monocytogenes. Proc. Natl Acad. Sci. USA 110(32), 13132-13137 (2013).
24. Sesto N, Touchon M, Andrade JM, et al. A PNPase dependent CRISPR system in Listeria. PLoS Genet. 10(1), e1004065 (2014).
25. Serganov A, Nudler E. A decade of riboswitches. Cell 152(1-2), 17-24 (2013).
26. O'Neil HS, Marquis H. Listeria monocytogenes flagella are used for motility, not as adhesins, to increase host cell invasion. Infect. Immun. 74(12), 6675-6681 (2006).
27. Ramos HC, Rumbo M, Sirard JC. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12(11), 509-517 (2004).
28. Buchrieser C, Rusniok C, Kunst F, Cossart P, Glaser P. Comparison of the genome sequences of Listeria monocytogenes and Listeria innocua: clues for evolution and pathogenicity. FEMS Immunol. Med. Microbiol. 35(3), 207-213 (2003).
29. Thiennimitr P, Winter SE, Winter MG, et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl Acad. Sci. USA 108(42), 17480-17485 (2011).
30. Joseph B, Przybilla K, Stuhler C, et al. Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J. Bacteriol. 188(2), 556-568 (2006).
31. Archambaud C, Nahori MA, Soubigou G, et al. Impact of lactobacilli on orally acquired listeriosis. Proc. Natl Acad. Sci. USA 109(41), 16684-16689 (2012).
32. Cossart P, Toledo-Arana A. Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 10(9), 1041-1050 (2008).
33. Garcia-Del Portillo F, Calvo E, D'Orazio V, Pucciarelli MG. Association of ActA to peptidoglycan revealed by cell wall proteomics of intracellular Listeria monocytogenes. J. Biol. Chem. 286(40), 34675-34689 (2011).
34. Quereda JJ, Álvaro D, Ortega, M, Pucciarelli G, García-del Portillo F. The Listeria small RNA Rli27 regulates a cell wall protein inside eukaryotic cells by targeting a long 5'-UTR variant. PLOS Genet. (2014) (In Press).
35. Nielsen JS, Lei LK, Ebersbach T, et al. Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes. Nucleic Acids Res. 38(3), 907-919 (2010).
36. Nielsen JS, Larsen MH, Lillebaek EM, et al. A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS ONE 6(4), e19019 (2011).
37. Chaudhuri S, Gantner BN, Ye RD, Cianciotto NP, Freitag NE. The Listeria monocytogenes ChiA chitinase enhances virulence through suppression of host innate immunity. MBio 4(2), e00617-12 (2013).
38. Nielsen JS, Christiansen MH, Bonde M, et al. Searching for small sigmaB-regulated genes in Staphylococcus aureus. Arch. Microbiol. 193(1), 23-34 (2011).
39. Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2(11), a012427 (2012).
40. Storz G, Wolf YI, Ramamurthi KS. Small proteins can no longer be ignored. Annu. Rev. Biochem. 83,753-777 (2014).
41. Sorek R, Lawrence CM, Wiedenheft B. CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82, 237-266 (2013).
42. Hain T, Ghai R, Billion A, et al. Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes. BMC Genomics 13, 144 (2012).
43. Kuenne C, Billion A, Mraheil MA, et al. Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics 14, 47 (2013).
44. Cardenas PP, Carrasco B, Sanchez H, Deikus G, Bechhofer DH, Alonso JC. Bacillus subtilis polynucleotide phosphorylase 3-To-5 DNase activity is involved in DNA repair. Nucleic Acids Res. 37(12), 4157-4169 (2009).
45. Mick E, Stern A, Sorek R. Holding a grudge: persisting anti-phage CRISPR immunity in multiple human gut microbiomes. RNA Biol. 10(5), 900-906 (2013).
46. Rho M, Wu YW, Tang H, Doak TG, Ye Y. Diverse CRISPRs evolving in human microbiomes. PLoS Genet. 8(6), e1002441 (2012).
47. Rabinovich L, Sigal N, Borovok I, Nir-Paz R, Herskovits AA. Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150(4), 792-802 (2012).
48. Wurtzel O, Sesto N, Mellin JR, et al. Comparative Transcriptomics of Pathogenic and Non-pathogenic Listeria Species (2012). Www.weizmann.ac.il/molgen/Sorek/ Listeria-browser
49. Gripenland J, Netterling S, Loh E, Tiensuu T, Toledo-Arana A, Johansson J. RNAs: regulators of bacterial virulence. Nat. Rev. Microbiol. 8(12), 857-866 (2010).
50. Papenfort K, Vogel J. Regulatory RNA in bacterial pathogens. Cell Host Microbe 8(1), 116-127 (2010).
51. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10(2), 126-139 (2009).
52. Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 19(6), 586-593 (2012).
53. Xiao B, Liu Z, Li BS, et al. Induction of microRNA-155 during Helicobacter pylori infection and its negative regulatory role in the inflammatory response. J. Infect. Dis. 200(6), 916-925 (2009).
54. Schulte LN, Eulalio A, Mollenkopf HJ, Reinhardt R, Vogel J. Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. EMBO J. 30(10), 1977-1989 (2011).
55. Sharbati J, Lewin A, Kutz-Lohroff B, Kamal E, Einspanier R, Sharbati S. Integrated microRNA-mRNA-Analysis of human monocyte derived macrophages upon Mycobacterium avium subsp. hominissuis infection. PLoS ONE 6(5), e20258 (2011).
56. Schnitger AK, Machova A, Mueller RU, et al. Listeria monocytogenes infection in macrophages induces vacuolar-dependent host miRNA response. PLoS ONE 6(11), e27435 (2011).
57. Izar B, Mannala GK, Mraheil MA, Chakraborty T, Hain T. MicroRNA response to Listeria monocytogenes infection in epithelial cells. Int. J. Mol. Sci. 13(1), 1173-1185 (2012).
58. Ma F, Xu S, Liu X, et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat. Immunol. 12(9), 861-869 (2011).
59. Archambaud C, Sismeiro O, Toedling J, et al. The intestinal microbiota interferes with the microRNA response upon oral Listeria infection. MBio 4(6), e00707-13 (2013).
60. Kurashige J, Kamohara H, Watanabe M, et al. MicroRNA-200b regulates cell proliferation, invasion, and migration by directly targeting ZEB2 in gastric carcinoma. Ann. Surg. Oncol. 19(Suppl. 3), S656-S664 (2012).
61. Baud J, Varon C, Chabas S, Chambonnier L, Darfeuille F, Staedel C. Helicobacter pylori initiates a mesenchymal transition through ZEB1 in gastric epithelial cells. PLoS ONE 8(4), e60315 (2013).
62. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl Acad. Sci. USA 103(33), 12481-12486 (2006).
63. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl Acad. Sci. USA 104(5), 1604-1609 (2007).
64. Pamer EG. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4(10), 812-823 (2004).
65. Lind EF, Elford AR, Ohashi PS. Micro-RNA 155 is required for optimal CD8+ T cell responses to acute viral and intracellular bacterial challenges. J. Immunol. 190(3), 1210-1216 (2013).
66. Ma X, Becker Buscaglia LE, Barker JR, Li Y. MicroRNAs in NF-kappaB signaling. J. Mol. Cell Biol. 3(3), 159-166 (2011).
67. Liu Z, Xiao B, Tang B, et al. Up-regulated microRNA-146a negatively modulate Helicobacter pylori-induced inflammatory response in human gastric epithelial cells. Microbes Infect. 12(11), 854-863 (2010).
68. Monk CE, Hutvagner G, Arthur JS. Regulation of miRNA transcription in macrophages in response to Candida albicans. PLoS ONE 5(10), e13669 (2010).
69. Mrazek J, Kreutmayer SB, Grasser FA, Polacek N, Huttenhofer A. Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res. 35(10), e73 (2007).
70. Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT, Dillard JP. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55(6), 1704-1721 (2005).
71. Woodward JJ, Iavarone AT, Portnoy DA. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328(5986), 1703-1705 (2010).
72. Abdullah Z, Schlee M, Roth S, et al. RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 31(21), 4153-4164 (2012).
73. Cazalla D, Yario T, Steitz JA. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 328(5985), 1563-1566 (2010).
74. Libri V, Helwak A, Miesen P, et al. Murine cytomegalovirus encodes a miR-27 inhibitor disguised as a target. Proc. Natl Acad. Sci. USA 109(1), 279-284 (2012).
75. Marcinowski L, Tanguy M, Krmpotic A, et al. Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog. 8(2), e1002510 (2012).
76. Weiberg A, Wang M, Lin FM, et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342(6154), 118-123 (2013).
77. Sander LE, Davis MJ, Boekschoten MV, et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474(7351), 385-389 (2011).
78. Hagmann CA, Herzner AM, Abdullah Z, et al. RIG-I detects triphosphorylated RNA of Listeria monocytogenes during infection in non-immune cells. PLoS ONE 8(4), e62872 (2013).
79. Lenz LL, Mohammadi S, Geissler A, Portnoy DA. SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl Acad. Sci. USA 100(21), 12432-12437 (2003).
80. Machata S, Hain T, Rohde M, Chakraborty T. Simultaneous deficiency of both MurA and p60 proteins generates a rough phenotype in Listeria monocytogenes. J. Bacteriol. 187(24), 8385-8394 (2005).
81. Mellin JR, Koutero M, Dar D, Nahori MA, Sorek R, Cossart P. Riboswitches. Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA. Science 345(6199), 940-943 (2014).