Listeria monocytogenes: Towards a complete picture of its physiology and pathogenesis

Nature Reviews Microbiology

Volumn 16, Issue 1, 2018, Pages 32-46

  Radoshevich, Lilliana ^a,b,c,d   Cossart, Pascale ^a,b,c  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CEMAGREF   (France)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; SMALL UNTRANSLATED RNA; VIRULENCE FACTOR;

BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL VIRULENCE; CELL INVASION; CELL MOTILITY; CELL VACUOLE; CYTOLOGY; EPIGENETICS; HOST CELL; HUMAN; LISTERIA MONOCYTOGENES; LISTERIOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RIBOSWITCH; STRESS; TRANSCRIPTION REGULATION; ANIMAL; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; LISTERIA MONOCYTOGENES; LISTERIOSIS; VIRULENCE; VIRULENCE FACTORS;

EID: 85038235007     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro.2017.126     Document Type: Review

References (130)

1. Murray, E. G. D., Webb, M. A. & Swann, M. B. R. A. Disease of rabbits characterised by a large mononuclear leucocytosis, caused by a hitherto undescribed bacillus Bacterium monocytogenes (n.sp.). J. Pathol. 29, 407-439 (1926).
2. Schlech, W. F. III, Lavigne, P. M., Bortolussi, R. A., Allen, A. C., Haldane, E. V. et al. Epidemic listeriosis - evidence for transmission by food. N. Engl. J. Med. 308, 203-206 (1983).
3. de Noordhout, C. M. et al. The global burden of listeriosis: A systematic review and meta-Analysis. Lancet Infect. Dis. 14, 1073-1082 (2014).
4. McLauchlin, J. Human listeriosis in Britain, 1967-1985, a summary of 722 cases. 1. Listeriosis during pregnancy and in the newborn. Epidemiol. Infect. 104, 181-189 (1990).
5. McLauchlin, J. Human listeriosis in Britain, 1967-1985, a summary of 722 cases. 2. Listeriosis in non-pregnant individuals, a changing pattern of infection and seasonal incidence. Epidemiol. Infect. 104, 191-201 (1990).
6. Weller, D., Andrus, A., Wiedmann, M. & den Bakker, H. C. Listeria booriae sp. nov. and Listeria newyorkensis sp. nov., from food processing environments in the USA. Int. J. Syst. Evol. Microbiol. 65, 286-292 (2015).
7. Gandhi, M. & Chikindas, M. L. Listeria: A foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 113, 1-15 (2007).
8. Tasara, T. & Stephan, R. Cold stress tolerance of Listeria monocytogenes: A review of molecular adaptive mechanisms and food safety implications. J. Food Prot. 69, 1473-1484 (2006).
9. de las Heras, A., Cain, R. J., Bielecka, M. K. & Vazquez-Boland, J. A. Regulation of Listeria virulence: PrfA master and commander. Curr. Opin. Microbiol. 14, 118-127 (2011).
10. Cossart, P. Illuminating the landscape of host- pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl Acad. Sci. USA 108, 19484-19491 (2011).
11. Bakardjiev, A. I., Theriot, J. A. & Portnoy, D. A. Listeria monocytogenes traffics from maternal organs to the placenta and back. PLoS Pathog. 2, e66 (2006).
12. Pizarro-Cerdá, J., Kühbacher, A. & Cossart, P. Entry of Listeria monocytogenes in mammalian epithelial cells: An updated view. Cold Spring Harbor Persp. Med. 2, a010009 (2012).
13. Lambrechts, A., Gevaert, K., Cossart, P., Vandekerckhove, J. & Van Troys, M. Listeria comet tails: The actin-based motility machinery at work. Trends Cell Biol. 18, 220-227 (2008).
14. Bierne, H. & Cossart, P. When bacteria target the nucleus: The emerging family of nucleomodulins. Cell. Microbiol. 14, 622-633 (2012).
15. Cossart, P. & Helenius, A. Endocytosis of viruses and bacteria. Cold Spring Harbor Persp. Biol. 6, a016972 (2014).
16. Bierne, H., Sabet, C., Personnic, N. & Cossart, P. Internalins: A complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect. 9, 1156-1166 (2007).
17. Sabet, C., Lecuit, M., Cabanes, D., Cossart, P. & Bierne, H. LPXTG protein InlJ, a newly identified internalin involved in Listeria monocytogenes virulence. Infect. Immun. 73, 6912-6922 (2005).
18. Kühbacher, A. et al. Genome-wide siRNA screen identifies complementary signaling pathways involved in Listeria infection and reveals different actin nucleation mechanisms during Listeria cell invasion and actin comet tail formation. mBio 6, e00598 15 (2015).
19. Agaisse, H. et al. Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309, 1248-1251 (2005).
20. Kirchner, M. & Higgins, D. E. Inhibition of ROCK activity allows InlF-mediated invasion and increased virulence of Listeria monocytogenes. Mol. Microbiol. 68, 749-767 (2008).
21. Perelman, S. S. et al. Cell-based screen identifies human interferon-stimulated regulators of Listeria monocytogenes infection. PLoS Pathog. 12, e1006102 (2016).
22. Xayarath, B., Alonzo, F. 3 rd & Freitag, N. E. Identification of a peptide-pheromone that enhances Listeria monocytogenes escape from host cell vacuoles. PLoS Pathog. 11, e1004707 (2015).
23. Rabinovich, L., Sigal, N., Borovok, I., Nir-Paz, R. & Herskovits, A. A. Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150, 792-802 (2012).
24. Feiner, R. et al. A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat. Rev. Microbiol. 13, 641-650 (2015).
25. Birmingham, C. L. et al. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451, 350-354 (2008).
26. Lam, G. Y., Cemma, M., Muise, A. M., Higgins, D. E. & Brumell, J. H. Host and bacterial factors that regulate LC3 recruitment to Listeria monocytogenes during the early stages of macrophage infection. Autophagy 9, 985-995 (2013).
27. Nikitas, G. et al. Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E cadherin. J. Exp. Med. 208, 2263-2277 (2011).
28. Hamon, M. A., Ribet, D., Stavru, F. & Cossart, P. Listeriolysin O: The Swiss army knife of Listeria. Trends Microbiol. 20, 360-368 (2012).
29. Stavru, F., Bouillaud, F., Sartori, A., Ricquier, D. & Cossart, P. Listeria monocytogenes transiently alters mitochondrial dynamics during infection. Proc. Natl Acad. Sci. USA 108, 3612-3617 (2011).
30. Stavru, F., Palmer, A. E., Wang, C. X., Youle, R. J. & Cossart, P. Atypical mitochondrial fission upon bacterial infection. Proc. Natl Acad. Sci. USA 110, 16003-16008 (2013).
31. Pillich, H., Loose, M., Zimmer, K. P. & Chakraborty, T. Activation of the unfolded protein response by Listeria monocytogenes. Cell. Microbiol. 14, 949-964 (2012).
32. Kaser, A. et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134, 743-756 (2008).
33. Malet, J. K., Cossart, P. & Ribet, D. Alteration of epithelial cell lysosomal integrity induced by bacterial cholesterol-dependent cytolysins. Cell. Microbiol. 19, e12682 (2017).
34. Lebreton, A. et al. A bacterial protein targets the BAHD1 Chromatin complex to stimulate type III interferon response. Science 331, 1319-1321 (2011).
35. Lebreton, A. et al. Structural basis for the inhibition of the chromatin repressor BAHD1 by the bacterial nucleomodulin LntA. mBio 5, e00775 13 (2014).
36. Lebreton, A. et al. A direct interaction between the bacterial nucleomodulin LntA and the chromatin repressor BAHD1 modulates interferon responses to infection. FEBS J. 281, 726-727 (2014).
37. Radoshevich, L. & Dussurget, O. Cytosolic innate immune sensing and signaling upon infection. Front. Microbiol. 7, 313 (2016).
38. Dussurget, O., Bierne, H. & Cossart, P. The bacterial pathogen Listeria monocytogenes and the interferon family: Type I, type II and type III interferons. Front. Cell. Infect. Microbiol. 4, 50 (2014).
39. Theisen, E. & Sauer, J. D. Listeria monocytogenes and the inflammasome: from cytosolic bacteriolysis to tumor immunotherapy. Curr. Top. Microbiol. Immunol. 397, 133-160 (2016).
40. Hamon, M. A. et al. Histone modifications induced by a family of bacterial toxins. Proc. Natl Acad. Sci. USA 104, 13467-13472 (2007).
41. Hamon, M. A. & Cossart, P. K+ efflux is required for histone H3 dephosphorylation by Listeria monocytogenes listeriolysin O and other pore-forming toxins. Infection Immun. 79, 2839-2846 (2011).
42. Eskandarian, H. A. et al. A role for SIRT2 dependent histone H3K18 deacetylation in bacterial infection. Science 341, 1238858 (2013).
43. Samba-Louaka, A., Stavru, F. & Cossart, P. Role for telomerase in Listeria monocytogenes infection. Infect. Immun. 80, 4257-4263 (2012).
44. Samba-Louaka, A. et al. Listeria monocytogenes dampens the DNA damage response. PLoS Pathog. 10, e1004470 (2014).
45. Leitao, E. et al. Listeria monocytogenes induces host DNA damage and delays the host cell cycle to promote infection. Cell Cycle 13, 928-940 (2014).
46. Veiga, E. & Cossart, P. Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat. Cell Biol. 7, 894-900 (2005).
47. Bonazzi, M., Veiga, E., Pizarro-Cerda, J. & Cossart, P. Successive post-Translational modifications of E cadherin are required for InlA-mediated internalization of Listeria monocytogenes. Cell. Microbiol. 10, 2208-2222 (2008).
48. Bonazzi, M. et al. Clathrin phosphorylation is required for actin recruitment at sites of bacterial adhesion and internalization. J. Cell Biol. 195, 525-536 (2011).
49. Bonazzi, M. et al. A common clathrin-mediated machinery co ordinates cell-cell adhesion and bacterial internalization. Traffic 13, 1653-1666 (2012).
50. Ribet, D. et al. Listeria monocytogenes impairs SUMOylation for efficient infection. Nature 464, 1192-1195 (2010).
51. Impens, F., Radoshevich, L., Cossart, P. & Ribet, D. Mapping of SUMO sites and analysis of SUMOylation changes induced by external stimuli. Proc. Natl Acad. Sci. USA 111, 12432-12437 (2014).
52. Ribet, D. et al. Promyelocytic leukemia protein (PML) controls Listeria monocytogenes infection. mBio 8, e02179 16 (2017).
53. Boujemaa-Paterski, R. et al. Listeria protein ActA mimics WASP family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40, 11390-11404 (2001).
54. Jasnin, M. et al. Three-dimensional architecture of actin filaments in Listeria monocytogenes comet tails. Proc. Natl Acad. Sci. USA 110, 20521-20526 (2013).
55. Truong, D., Copeland, J. W. & Brumell, J. H. Bacterial subversion of host cytoskeletal machinery: hijacking formins and the Arp2/3 complex. Bioessays 36, 687-696 (2014).
56. Fattouh, R. et al. The diaphanous-related Formins promote protrusion formation and cell to cell spread of Listeria monocytogenes. J. Infect. Dis. 211, 1185-1195 (2015).
57. Rigano, L. A., Dowd, G. C., Wang, Y. & Ireton, K. Listeria monocytogenes antagonizes the human GTPase Cdc42 to promote bacterial spread. Cell. Microbiol. 16, 1068-1079 (2014).
58. Rajabian, T. et al. The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell to cell spread of Listeria. Nat. Cell Biol. 11, 1212-1218 (2009).
59. Czuczman, M. A. et al. Listeria monocytogenes exploits efferocytosis to promote cell to cell spread. Nature 509, 230-234 (2014).
60. Auerbuch, V., Brockstedt, D. G., Meyer-Morse, N., O'Riordan, M. & Portnoy, D. A. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200, 527-533 (2004).
61. Carrero, J. A., Calderon, B. & Unanue, E. R. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 200, 535-540 (2004).
62. O'Connell, R. M. et al. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 200, 437-445 (2004).
63. Stockinger, S. et al. IFN regulatory factor 3 dependent induction of type I IFNs by intracellular bacteria is mediated by a TLR-And Nod2 independent mechanism. J. Immunol. 173, 7416-7425 (2004).
64. Osborne, S. E. et al. Type I interferon promotes cell to cell spread of Listeria monocytogenes. Cell. Microbiol. 19, e12660 (2017).
65. Gutierrez, M. G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766 (2004).
66. Yoshikawa, Y. et al. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11, 1233-1240 (2009).
67. Mostowy, S. et al. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J. Biol. Chem. 286, 26987-26995 (2011).
68. Mitchell, G. et al. Avoidance of autophagy mediated by PlcA or ActA is required for Listeria monocytogenes growth in macrophages. Infect. Immun. 83, 2175-2184 (2015).
69. Lecuit, M. et al. A single amino acid in E cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18, 3956-3963 (1999).
70. Lecuit, M. et al. A transgenic model for listeriosis: Role of internalin in crossing the intestinal barrier. Science 292, 1722-1725 (2001).
71. Pentecost, M., Kumaran, J., Ghosh, P. & Amieva, M. R. Listeria monocytogenes Internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog. 6, e1000900 (2010).
72. Gessain, G. et al. PI3 kinase activation is critical for host barrier permissiveness to Listeria monocytogenes. J. Exp. Med. 212, 165-183 (2015).
73. Khelef, N., Lecuit, M., Bierne, H. & Cossart, P. Species specificity of the Listeria monocytogenes InlB protein. Cell. Microbiol. 8, 457-470 (2006).
74. Wollert, T., Heinz, D. W. & Schubert, W. D. Thermodynamically reengineering the listerial invasion complex InlA/E cadherin. Proc. Natl Acad. Sci. USA 104, 13960-13965 (2007).
75. Wollert, T. et al. Extending the host range of Listeria monocytogenes by rational protein design. Cell 129, 891-902 (2007).
76. Tsai, Y. H., Disson, O., Bierne, H. & Lecuit, M. Murinization of Internalin extends its receptor repertoire, altering Listeria monocytogenes cell tropism and host responses. PLoS Pathog. 9, e1003381 (2013).
77. Jones, G. S. et al. Intracellular Listeria monocytogenes comprises a minimal but vital fraction of the intestinal burden following foodborne infection. Infect. Immun. 83, 3146-3156 (2015).
78. Jones, G. S. & D'Orazio, S. E. Monocytes are the predominant cell type associated with Listeria monocytogenes in the gut, but they do not serve as an intracellular growth niche. J. Immunol. 198, 2796-2804 (2017).
79. Bleriot, C. et al. Liver-resident macrophage necroptosis orchestrates type 1 microbicidal inflammation and type 2 mediated tissue repair during bacterial infection. Immunity 42, 145-158 (2015).
80. Charlier, C. et al. Clinical features and prognostic factors of listeriosis: The MONALISA national prospective cohort study. Lancet Infect. Dis. 17, 510-519 (2017).
81. Bakardjiev, A. I., Stacy, B. A. & Portnoy, D. A. Growth of Listeria monocytogenes in the guinea pig placenta and role of cell to cell spread in fetal infection. J. Infect. Dis. 191, 1889-1897 (2005).
82. Disson, O. et al. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455, 1114-1118 (2008).
83. Lecuit, M. et al. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: Role of internalin interaction with trophoblast E cadherin. Proc. Natl Acad. Sci. USA 101, 6152-6157 (2004).
84. Zeldovich, V. B., Robbins, J. R., Kapidzic, M., Lauer, P. & Bakardjiev, A. I. Invasive extravillous trophoblasts restrict intracellular growth and spread of Listeria monocytogenes. PLoS Pathog. 7, e1002005 (2011).
85. Zeldovich, V. B. et al. Placental syncytium forms a biophysical barrier against pathogen invasion. PLoS Pathog. 9, e1003821 (2013).
86. Faralla, C. et al. InlP, a new virulence factor with strong placental tropism. Infect. Immun. 84, 3584-3596 (2016).
87. Rolhion, N. & Chassaing, B. When pathogenic bacteria meet the intestinal microbiota. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150504 (2016).
88. Archambaud, C. et al. Impact of lactobacilli on orally acquired listeriosis. Proc. Natl Acad. Sci. USA 109, 16684-16689 (2012).
89. Archambaud, C. et al. The intestinal microbiota interferes with the microRNA response upon oral Listeria infection. mBio 4, e00707 13 (2013).
90. Becattini, S. et al. Commensal microbes provide first line defense against Listeria monocytogenes infection. J. Exp. Med. 214, 1973-1989 (2017).
91. Becavin, C. et al. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD e highlights genomic variations underlying differences in pathogenicity. mBio 5, e00969 14 (2014).
92. Cotter, P. D. et al. Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog. 4, e1000144 (2008).
93. Quereda, J. J. et al. Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. Proc. Natl Acad. Sci. USA 113, 5706-5711 (2016).
94. Dussurget, O. et al. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 45, 1095-1106 (2002).
95. Begley, M., Sleator, R. D., Gahan, C. G. & Hill, C. Contribution of three bile-Associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73, 894-904 (2005).
96. Dowd, G. C., Joyce, S. A., Hill, C. & Gahan, C. G. Investigation of the mechanisms by which Listeria monocytogenes grows in porcine gallbladder bile. Infect. Immun. 79, 369-379 (2011).
97. Toledo-Arana, A. et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459, 950-956 (2009).
98. Mraheil, M. A. et al. The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res. 39, 4235-4248 (2011).
99. Wurtzel, O. et al. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol. Syst. Biol. 8, 583 (2012).
100. Dar, D. et al. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352, aad9822 (2016).
101. Lebreton, A. & Cossart, P. RNA-And protein-mediated control of Listeria monocytogenes virulence gene expression. RNA Biol. 14, 460-470 (2016).
102. Reniere, M. L. et al. Glutathione activates virulence gene expression of an intracellular pathogen. Nature 517, 170-173 (2015).
103. Hall, M. et al. Structural basis for glutathione-mediated activation of the virulence regulatory protein PrfA in Listeria. Proc. Natl Acad. Sci. USA 113, 14733-14738 (2016).
104. Mandin, P. et al. VirR, a response regulator critical for Listeria monocytogenes virulence. Mol. Microbiol. 57, 1367-1380 (2005).
105. Kang, J., Wiedmann, M., Boor, K. J. & Bergholz, T. M. VirR-mediated resistance of Listeria monocytogenes against food antimicrobials and cross-protection induced by exposure to organic acid salts. Appl. Environ. Microbiol. 81, 4553-4562 (2015).
106. Abachin, E. et al. Formation of D alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43, 1-14 (2002).
107. Thedieck, K. et al. The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol. Microbiol. 62, 1325-1339 (2006).
108. Behrens, S. et al. Ultra deep sequencing of Listeria monocytogenes sRNA transcriptome revealed new antisense RNAs. PloS ONE 9, e83979 (2014).
109. Burke, T. P. et al. Listeria monocytogenes is resistant to lysozyme through the regulation, not the acquisition, of cell wall-modifying enzymes. J. Bacteriol. 196, 3756-3767 (2014).
110. Boneca, I. G. et al. A critical role for peptidoglycan N deacetylation in Listeria evasion from the host innate immune system. Proc. Natl Acad. Sci. USA 104, 997-1002 (2007).
111. Burke, T. P. & Portnoy, D. A. SpoVG is a conserved RNA-binding protein that regulates Listeria monocytogenes lysozyme resistance, virulence, and swarming motility. mBio 7, e00240 16 (2016).
112. Quereda, J. J., Ortega, A. D., Pucciarelli, M. G. & Garcia-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. 10, e1004765 (2014).
113. Mellin, J. R. et al. A riboswitch-regulated antisense RNA in Listeria monocytogenes. Proc. Natl Acad. Sci. USA 110, 13132-13137 (2013).
114. Mellin, J. R. et al. Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA. Science 345, 940-943 (2014).
115. Aubry, C. et al. OatA, a peptidoglycan O acetyltransferase involved in Listeria monocytogenes immune escape, is critical for virulence. J. Infect. Dis. 204, 731-740 (2011).
116. Pensinger, D. A. et al. The Listeria monocytogenes PASTA kinase PrkA and its substrate YvcK are required for cell wall homeostasis, metabolism, and virulence. PLoS Pathog. 12, e1006001 (2016).
117. Marles-Wright, J. et al. Molecular architecture of the "stressosome, " a signal integration and transduction hub. Science 322, 92-96 (2008).
118. Impens, F. et al. N terminomics identifies Prli42 as a membrane miniprotein conserved in Firmicutes and critical for stressosome activation in Listeria monocytogenes. Nat. Microbiol. 2, 17005 (2017).
119. Orsi, R. H. & Wiedmann, M. Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Appl. Microbiol. Biotechnol. 100, 5273-5287 (2016).
120. Maury, M. M. et al. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat. Genet. 48, 308-313 (2016).
121. Moura, A. et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat. Microbiol. 2, 16185 (2016).
122. Ragon, M. et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 4, e1000146 (2008).
123. Abdullah, Z. et al. RIG I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 31, 4153-4164 (2012).
124. Hagmann, C. A. et al. RIG I detects triphosphorylated RNA of Listeria monocytogenes during Infection in non-immune cells. PloS ONE 8, e62872 (2013).
125. Radoshevich, L. et al. ISG15 counteracts Listeria monocytogenes infection. eLife 4, e06848 (2015).
126. Woodward, J. J., Iavarone, A. T. & Portnoy, D. A. c Di AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328, 1703-1705 (2010).
127. Archer, K. A., Durack, J. & Portnoy, D. A. STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog. 10, e1003861 (2014).
128. McFarland, A. P. et al. Sensing of bacterial cyclic dinucleotides by the oxidoreductase RECON promotes NF κB activation and shapes a proinflammatory antibacterial state. Immunity 46, 433-445 (2017).
129. Ribet, D. & Cossart, P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect. 17, 173-183 (2015).
130. Quereda, J. J. & Cossart, P. Regulating bacterial virulence with RNA. Annu. Rev. Microbiol. 71, 263-280 (2017).