Variability of Listeria monocytogenes virulence: A result of the evolution between saprophytism and virulence?

Future Microbiology

Volumn 5, Issue 12, 2010, Pages 1799-1821

  Velge, Philippe ^a,b   Roche, Sylvie Marie ^a,b  

^a UR1282   (France)

^b UNIVERSITÉ DE TOURS   (France)

Author keywords

Evolution; Hostpathogen interaction; Infection model; Invasion; Listeria monocytogenes; Regulation; Saprophytism; Virulence

Indexed keywords

BACTERIAL RNA; BILE SALT; GLUTAMATE DECARBOXYLASE; HEMOLYSIN; MESSENGER RNA; MUCIN; PHOSPHATIDYLCHOLINE PHOSPHOLIPASE C; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PHOSPHOLIPID; RNA BINDING PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ABORTION; BACTEREMIA; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL REPRODUCTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BIOFILM; BLOOD BRAIN BARRIER; BLOOD PLACENTA BARRIER; CATTLE DISEASE; CELL ADHESION; CELL CULTURE; CELL INVASION; CENTRAL NERVOUS SYSTEM INFECTION; ENCEPHALITIS; EVOLUTION; EVOLUTIONARY ADAPTATION; FLAGELLUM; GASTROINTESTINAL TRACT; GUINEA PIG; HUMAN; IMMUNOCOMPROMISED PATIENT; IN VITRO STUDY; IN VIVO STUDY; INTRAUTERINE INFECTION; KARYOTYPE EVOLUTION; LISTERIA GRAYI; LISTERIA INNOCUA; LISTERIA IVANOVI; LISTERIA IVANOVII; LISTERIA MARTHII; LISTERIA MONOCYTOGENES; LISTERIA ROCOURTIAE; LISTERIA SEELIGERI; LISTERIA WELSHIMERI; LISTERIOSIS; LIVER CELL; MENINGITIS; MOUSE; NEWBORN INFECTION; NONHUMAN; OPERON; OSMOLARITY; PATHOGENICITY; PERISTALSIS; PH; PREGNANT WOMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; REGULON; REVIEW; RISK ASSESSMENT; SAPROTROPH; SEROTYPE; SEWAGE; SHEEP DISEASE; SLUDGE; SMALL INTESTINE; STILLBIRTH; STOMACH; VIRULENCE; WATER CONTAMINATION;

ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; LISTERIA MONOCYTOGENES; LISTERIOSIS; VIRULENCE; VIRULENCE FACTORS;

ANIMALIA; LISTERIA; LISTERIA MONOCYTOGENES;

EID: 78650457810     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.10.134     Document Type: Review

References (191)

1. Leclercq A, Clermont D, Bizet C et al.: Listeria rocourtiae sp. nov. Int. J. Syst. Evol. Microbiol. 60(Pt 9), 2210-2214 (2010).
2. Graves LM, Helsel LO, Steigerwalt AG et al.: Listeria marthii sp. nov., isolated from the natural environment, Finger Lakes National Forest. Int. J. Syst. Evol. Microbiol. 60(pt 6), 1280-1288 (2010).
3. Czuprynski CJ: Listeria monocytogenes: silage, sandwiches and science. Anim. Health Res. Rev. 6(2), 211-217 (2005).
4. Rocourt J, Hof H, Schrettenbrunner A, Malinverni R, Bille J: Acute purulent Listeria seelingeri meningitis in an immunocompetent adult. Schw. Med. Woch. 116(8), 248-251 (1986).
5. Cummins AJ, Fielding AK, Mclauchlin J: Listeria ivanovii infection in a patient with AIDS. J. Infect. 28, 89-91 (1994).
6. Perrin M, Bemer M, Delamare C: Fatal case of Listeria innocua bacteremia. J. Clin. Microbiol. 41(11), 5308-5309 (2003).
7. Guillet C, Join-Lambert O, Le Monnier A et al.: Human listeriosis caused by Listeria ivanovii. Emerg. Infect. Dis. 16(1), 136-138 (2010).
8. Roche SM, Gracieux P, Albert I et al.: Experimental validation of low virulence in field strains of Listeria monocytogenes. Infect. Immun. 71(6), 3429-3436 (2003).
9. Roche SM, Velge P, Bottreau E, Durier C, Marquet-van der Mee N, Pardon P: Assessment of the virulence of Listeria monocytogenes: agreement between a plaque-forming assay with HT-29 cells and infection of immunocompetent mice. Int. J. Food Microbiol. 68(1-2), 33-44. (2001).
10. Tabouret M, De Rycke J, Audurier A, Poutrel B: Pathogenicity of Listeria monocytogenes isolates in immunocompromised mice in relation to listeriolysin production. J. Med. Microbiol 34(1), 13-18 (1991).
11. Dunn KA, Bielawski JP, Ward TJ, Urquhart C, Gu H: Reconciling ecological and genomic divergence among lineages of Listeria under an "extended mosaic genome concept". Mol. Biol. Evol. 26(11), 2605-2615 (2009).
12. Phan-Thanh L, Jansch L: Elucidation of mechanisms of acid stress in Listeria monocytogenes by proteomic analysis. Meth. Biochem. Anal. 49, 75-88 (2006).
13. Phan-Thanh L, Gormon T: Analysis of heat and cold shock proteins in Listeria by two-dimensional electrophoresis. Electrophoresis 16, 444 (1995).
14. Seeliger HPR, Jones D: Genus Listeria Pirie. In: Bergeys Manual of Systematic Bacteriology. Sneath PHA, Mair SN, Sharpe ME, Holt JG (Ed.). Williams & Wilkins, Baltimore, USA, 1235 (1986).
15. Chambel L, Sol M, Fernandes I et al.: Occurrence and persistence of Listeria spp. in the environment of ewe and cows milk cheese dairies in Portugal unveiled by an integrated analysis of identification, typing and spatial-temporal mapping along production cycle. Int. J. Food Microbiol. 116(1), 52-63 (2007).
16. Hofer E, Ribeiro R, Feitosa DP: Species and serovars of the genus Listeria isolated from different sources in Brazil from 1971 to 1997. Mem. Inst. Oswaldo Cruz 95(5), 615-620 (2000).
17. Rocourt J: Listeriosis 1985-1995: microbiologic and epidemiologic aspects. Bull. Acad. Natl Med. 179, 1613-1624 (1995).
18. Liu D: Epidemiology. In: Handbook of Listeria monocytogenes. Liu D (Ed.). CRC Press, Boca Raton, FL, USA, 27-54 (2008).
19. Swaminathan B, Gerner-Smidt P: The epidemiology of human listeriosis. Microbes Infect. 9(10), 1236-1243 (2007).
20. EFSA: Rapport annuel de lEFSA-ECDC sur les infections transmissibles de lanimal à lhomme. EFSA J. 97, 1-2 (2007).
21. Vazquez-Boland JA, Kuhn M, Berche P et al.: Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14(3), 584-640 (2001).
22. Lecuit M: Understanding how Listeria monocytogenes targets and crosses host barriers. Clin. Microbiol. Infect. 11(6), 430-436 (2005).
23. Zundel E, Bernard S: Listeria monocytogenes translocates throughout the digestive tract in asymptomatic sheep. J. Med. Microbiol. 55(Pt 12), 1717-1723 (2006).
24. Unnerstad H, Romell A, Ericsson H, Danielsson-Tham ML, Tham W: Listeria monocytogenes in faeces from clinically healthy dairy cows in Sweden. Acta Vet. Scand. 41(2), 167-171 (2000).
25. Alexander AV, Walker RL, Johnson BJ, Charlton BR, Woods LW: Bovine abortions attributable to Listeria ivanovii: four cases (1988-1990). J. Am. Vet. Med. Assoc. 200(5), 711-714 (1992).
26. Gahan CG, Hill C: Gastrointestinal phase of Listeria monocytogenes infection. J. Appl. Microbiol. 98(6), 1345-1353 (2005).
27. Glaser P, Frangeul L, Buchrieser C et al.: Comparative genomics of Listeria species. Science 294(5543), 849-852 (2001).
28. Buchrieser C: Biodiversity of the species Listeria monocytogenes and the genus Listeria. Microbes Infect. 9(10), 1147-1155 (2007).
29. Chaturongakul S, Raengpradub S, Wiedmann M, Boor KJ: Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol. 16(8), 388-396 (2008).
30. Rea RB, Gahan CG, Hill C: Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect. Immun. 72(2), 717-727 (2004).
31. Chatterjee SS, Hossain H, Otten S et al.: Intracellular gene expression profile of Listeria monocytogenes. Infect. Immun. 74(2), 1323-1338 (2006).
32. Chan YC, Hu Y, Chaturongakul S et al.: Contributions of two-component regulatory systems, alternative s factors, and negative regulators to Listeria monocytogenes cold adaptation and cold growth. J. Food Protect. 71(2), 420-425 (2008).
33. Zhang C, Nietfeldt J, Zhang M, Benson AK: Functional consequences of genome evolution in Listeria monocytogenes: the lmo0423 and lmo0422 genes encode sC and LstR, a lineage II-specific heat shock system. J. Bacteriol. 187(21), 7243-7253 (2005).
34. Garner MR, Njaa BL, Wiedmann M, Boor KJ: s B contributes to Listeria monocytogenes gastrointestinal infection but not to systemic spread in the guinea pig infection model. Infect. Immun. 74(2), 876-886 (2006).
35. Hain T, Hossain H, Chatterjee SS et al.: Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e sB regulon. BMC Microbiol. 8, 20-32 (2008).
36. Toledo-Arana A, Dussurget O, Nikitas G et al.: The Listeria transcriptional landscape from saprophytism to virulence. Nature 459(7249), 950-956 (2009).
37. Ollinger J, Bowen B, Wiedmann M, Boor KJ, Bergholz TM: Listeria monocytogenes sB modulates PrfA-mediated virulence factor expression. Infect. Immun. 77(5), 2113-2124 (2009).
38. Scortti M, Monzo HJ, Lacharme-Lora L, Lewis DA, Vazquez-Boland JA: The PrfA virulence regulon. Microbes Infect. 9(10), 1196-1207 (2007).
39. Milohanic E, Glaser P, Coppee JY et al.: Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol. 47(6), 1613-1625 (2003).
40. Mertins S, Joseph B, Goetz M et al.: Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes. J. Bacteriol. 189(2), 473-490 (2007).
41. 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 (2002).
42. 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).
43. Autret N, Raynaud C, Dubail I, Berche P, Charbit A: Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect. Immun. 71(8), 4463-4471 (2003).
44. Mandin P, Fsihi H, Dussurget O et al.: VirR, a response regulator critical for Listeria monocytogenes virulence. Mol. Microbiol. 57(5), 1367-1380 (2005).
45. Thedieck K, Hain T, Mohamed W 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(5), 1325-1339 (2006).
46. Abachin E, Poyart C, Pellegrini E et al.: Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43(1), 1-14 (2002).
47. 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).
48. Cotter PD, Gahan CG, Hill C: A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol. Microbiol. 40(2), 465-475 (2001).
49. Begley M, Sleator RD, Gahan CG, Hill C: Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73(2), 894-904 (2005).
50. Dussurget O, Cabanes D, Dehoux P 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(4), 1095-1106 (2002).
51. Sleator RD, Wemekamp-Kamphuis HH, Gahan CG, Abee T, Hill C: A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol. Microbiol. 55(4), 1183-1195 (2005).
52. Dussurget O: New insights into determinants of Listeria monocytogenes virulence. Int. Rev. Cell. Mol. Biol. 270, 1-38 (2008).
53. ONeil 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).
54. Linden SK, Bierne H, Sabet C et al.: Listeria monocytogenes internalins bind to the human intestinal mucin MUC2. Arch. Microbiol. 190(1), 101-104 (2008).
55. Lievin-Le Moal V, Servin AL, Coconnier- Polter MH: The increase in mucin exocytosis and the upregulation of MUC genes encoding for membrane-bound mucins induced by the thiol-activated exotoxin listeriolysin O is a host cell defence response that inhibits the cell-entry of Listeria monocytogenes. Cell. Microbiol. 7(7), 1035-1048 (2005).
56. Dramsi S, Bourdichon F, Cabanes D, Lecuit M, Fsihi H, Cossart P: FbpA, a novel multifunctional Listeria monocytogenes virulence factor. Mol. Microbiol. 53(2), 639-649 (2004).
57. Wampler JL, Kim KP, Jaradat Z, Bhunia AK: Heat shock protein 60 acts as a receptor for the Listeria adhesion protein in Caco-2 cells. Infect. Immun. 72(2), 931-936 (2004).
58. Sabet C, Toledo-Arana A, Personnic N et al.: The Listeria monocytogenes virulence factor InlJ is specifically expressed in vivo and behaves as an adhesin. Infect. Immun. 76(4), 1368-1378 (2008).
59. Milohanic E, Jonquieres R, Cossart P, Berche P, Gaillard JL: The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol. Microbiol. 39(5), 1212-1224 (2001).
60. Milohanic E, Jonquieres R, Glaser P et al.: Sequence and binding activity of the autolysin-adhesin Ami from epidemic Listeria monocytogenes 4b. Infect. Immun. 72(8), 4401-4409 (2004).
61. Hamon MA, Batsche E, Regnault B et al.: Histone modifications induced by a family of bacterial toxins. Proc. Natl Acad. Sci. USA 104(33), 13467-13472 (2007).
62. Portnoy DA, Jacks PS, Hinrichs DJ: Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 167, 1459 (1988).
63. Cossart P, Toledo-Arana A: Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 10(9), 1041-1050 (2008).
64. Rosselin M, Virlogeux-Payant I, Roy C et al.: Rck of Salmonella enterica, subspecies enterica serovar Enteritidis, mediates a Zipper-like internalization. Cell Res. 20(6), 647 (2010).
65. Birmingham CL, Canadien V, Gouin E et al.: Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3(5), 442-451 (2007).
66. Lecuit M: Human listeriosis and animal models. Microbes Infect. 9(10), 1216-1225 (2007).
67. Disson O, Grayo S, Huillet E et al.: Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455(7216), 1114-1118 (2008).
68. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P: E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84, 923-932 (1996). (Pubitemid 26106861)
69. Schubert WD, Urbanke C, Ziehm T et al.: Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111(6), 825-836 (2002).
70. Lecuit M, Dramsi S, Gottardi C, Fedorchaiken M, Gumbiner B, Cossart P: A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18(14), 3956-3963 (1999).
71. Olier M, Pierre F, Rousseaux S et al.: Expression of truncated internalin A is involved in impaired internalization of some Listeria monocytogenes isolates carried asymptomatically by humans. Infect. Immun. 71(3), 1217-1224 (2003).
72. Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P: 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 (1991).
73. Khelef N, Lecuit M, Bierne H, Cossart P: Species specificity of the Listeria monocytogenes InlB protein. Cell. Microbiol. 8(3), 457-470 (2006).
74. Shen Y, Naujokas M, Park M, Ireton K: InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103(3), 501-510 (2000).
75. Niemann HH, Jager V, Butler PJ et al.: Structure of the human receptor tyrosine kinase met in complex with the Listeria invasion protein InlB. Cell 130(2), 235-246 (2007).
76. Engelbrecht F, Chun SK, Ochs C et al.: A new prfa-regulated gene of Listeria monocytogenes encoding a small, secreted protein which belongs to the family of internalins. Mol. Microbiol. 21, 823-837 (1996).
77. Rajabian T, Gavicherla B, Heisig M et al.: The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat. Cell. Biol. 11(10), 1212-1218 (2009).
78. Cabanes D, Sousa S, Cebria A, Lecuit M, Garcia-del Portillo F, Cossart P: Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. EMBO J. 24(15), 2827-2838 (2005).
79. Yang Y, Liu B, Dai J et al.: Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26(2), 215-226 (2007).
80. Reis O, Sousa S, Camejo A et al.: LapB, a Novel Listeria monocytogenes LPXTG surface adhesin, required for entry into eukaryotic cells and virulence. J. Infect. Dis. 202(4), 551-562 (2010).
81. Archambaud C, Nahori MA, Pizarro-Cerda J, Cossart P, Dussurget O: Control of Listeria superoxide dismutase by phosphorylation. J. Biol. Chem. 281(42), 31812-31822 (2006).
82. Boneca IG, Dussurget O, Cabanes D et al.: A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl Acad. Sci. USA 104(3), 997-1002 (2007).
83. Smith GA, Portnoy DA: The role of two phospholipases in the pathogenicity of Listeria monocytogenes. Infect. Agents Dis. 2, 183 (1993).
84. Singh R, Jamieson A, Cresswell P: GILT is a critical host factor for Listeria monocytogenes infection. Nature 455(7217), 1244-1247 (2008).
85. Leimeister-Wachter M, Domann E, Chakraborty T: Detection of a gene encoding a phosphatidylinositol-specific phospholipase-C that is coordinately expressed with listeriolysin in Listeria monocytogenes. Mol. Microbiol. 5, 361-366 (1991).
86. Geoffroy C, Raveneau J, Beretti JL et al.: Purification and characterization of an extracellular 29-kilodalton phospholipase-C from Listeria monocytogenes. Infect. Immun. 59, 2382-2388 (1991).
87. Domann E, Leimeisterwachter M, Goebel W, Chakraborty T: Molecular cloning, sequencing, and identification of a metalloprotease gene from Listeria monocytogenes that is species specific and physically linked to the listeriolysin gene. Infect. Immun. 59, 65-72 (1991).
88. Van Langendonck N, Bottreau E, Bailly S et al.: Tissue culture assays using caco-2 cell line differentiate virulent from non-virulent Listeria monocytogenes strains. J. Appl. Microbiol. 85, 337 (1998).
89. Marquis H, Doshi V, Portnoy DA: The broad-range phospholipase c and a metalloprotease mediate listeriolysin o-independent escape of Listeria monocytogenes from a primary vacuole in human epithelial cells. Infect. Immun. 63, 4531-4534 (1995).
90. Marquis H, Bouwer HG, Hinrichs DJ, Portnoy DA: Intracytoplasmic growth and virulence of Listeria monocytogenes auxotrophic mutants. Infect. Immunity 61(9), 3756-3760 (1993).
91. Klarsfeld AD, Goossens PL, Cossart P: Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells: plca, purh, purd, pyre and an arginine ABC transporter gene, arpJ. Mol. Microbiol. 13, 585 (1994).
92. Keeney KM, Stuckey JA, ORiordan MX: LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence. Mol. Microbiol. 66(3), 758-770 (2007).
93. Chico-Calero I, Suarez M, Gonzalez-Zorn B et al.: Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc. Natl Acad. Sci. USA 99(1), 431-436 (2002).
94. Bennett HJ, Pearce DM, Glenn S et al.: Characterization of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol. Microbiol. 63(5), 1453-1467 (2007).
95. Baumgartner M, Karst U, Gerstel B, Loessner M, Wehland J, Jansch L: Inactivation of Lgt allows systematic characterization of lipoproteins from Listeria monocytogenes. J. Bacteriol. 189(2), 313-324 (2007).
96. Joseph B, Mertins S, Stoll R et al.: Glycerol metabolism and PrfA activity in Listeria monocytogenes. J. Bacteriol. 190(15), 5412-5430 (2008).
97. 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).
98. Eisenreich W, Dandekar T, Heesemann J, Goebel W: Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat. Rev. 8(6), 401-412 (2010).
99. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P: L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68(3), 521-531 (1992).
100. Conner DE, Scott VN, Summer SS, Bernard DT: Pathogenicity of foodborne, environmental and clinical isolates of Listeria monocytogenes in mice. J. Food Sci. 54(6), 1553-1556 (1989).
101. Selander RK, Caugant DA, Ochman H, Musser JM, Gilmour MN, Whittam TS: Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Env. Microbiol. 51(5), 873-884 (1986).
102. Carriere C, Allardet-Servent A, Bourg G, Audurier A, Ramuz M: DNA polymorphism in strains of Listeria monocytogenes. J. Clin. Microbiol. 29(7), 1351-1355 (1991).
103. Mazurier SI, Audurier A, Marquetvandermee N, Notermans S, Wernars K: A comparative study of randomly amplified polymorphic DNA analysis and conventional phage typing for epidemiological studies of Listeria monocytogenes isolates. Res. Microbiol. 143, 507-512 (1992).
104. Murphy M, Corcoran D, Buckley JF, OMahony M, Whyte P, Fanning S: Development and application of multiple-locus variable number of tandem repeat analysis (MLVA) to subtype a collection of Listeria monocytogenes. Int. J. Food Microbiol. 115(2), 187-194 (2007).
105. Wiedmann M, Bruce JL, Knorr R et al.: Ribotype diversity of Listeria monocytogenes strains associated with outbreaks of listeriosis in ruminants. J. Clin. Microbiol. 34, 1086-1090 (1996).
106. Ragon M, Wirth T, Hollandt F et al.: A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 4(9), E1000146 (2008).
107. Goulet V, Jacquet C, Martin P, Vaillant V, Laurent E, De Valk H: Surveillance of human listeriosis in France, 2001-2003. Euro Surveillance 11(6), 79-81 (2006).
108. Czuprynski CJ, Faith NG, Steinberg H: Ability of the Listeria monocytogenes strain Scott A to cause systemic infection in mice infected by the intragastric route. Appl. Env. Microbiol. 68(6), 2893-2900 (2002).
109. Wiedmann M, Bruce JL, Keating C, Johnson AE, McDonough PL, Batt CA: Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect. Immun. 65(7), 2707-2716 (1997).
110. Ward TJ, Ducey TF, Usgaard T, Dunn KA, Bielawski JP: Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Appl. Env. Microbiol. 74(24), 7629-7642 (2008).
111. Gray MJ, Zadoks RN, Fortes ED et al.: Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl. Env. Microbiol. 70(10), 5833-5841 (2004).
112. Jeffers GT, Bruce JL, McDonough PL, Scarlett J, Boor KJ, Wiedmann M: Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 147(Pt 5), 1095-1104 (2001). (Pubitemid 32454628)
113. Roberts A, Nightingale K, Jeffers G, Fortes E, Kongo JM, Wiedmann M: Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology 152(Pt 3), 685-693 (2006).
114. Orsi RH, Sun Q, Wiedmann M: Genome-wide analyses reveal lineage specific contributions of positive selection and recombination to the evolution of Listeria monocytogenes. BMC Evol. Biol. 8(1), 233-235 (2008).
115. Graves LM, Swaminathan B: PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis. Int. J. Food Microbiol. 65(1-2), 55-62 (2001).
116. Martin P, Jacquet C, Goulet V, Vaillant V, De Valk H: Pulsed-field gel electrophoresis of Listeria monocytogenes strains: the PulseNet Europe Feasibility Study. Foodborne Pathog. Dis. 3(3), 303-308 (2006).
117. Borucki MK, Reynolds J, Gay CC et al.: Dairy farm reservoir of Listeria monocytogenes sporadic and epidemic strains. J. Food Protect. 67(11), 2496-2499 (2004).
118. Roche SM, Gracieux P, Milohanic E et al.: Investigation of specific substitutions in virulence genes characterizing phenotypic groups of low-virulence field strains of Listeria monocytogenes. Appl. Env. Microbiol. 71(10), 6039-6048 (2005).
119. Borucki MK, Kim SH, Call DR, Smole SC, Pagotto F: Selective discrimination of Listeria monocytogenes epidemic strains by a mixed-genome DNA microarray compared to discrimination by pulsed-field gel electrophoresis, ribotyping, and multilocus sequence typing. J. Clin. Microbiol. 42(11), 5270-5276 (2004).
120. Cheers C, McKenzie IFC, Pavlov H, Waid C, York J: Resistance and susceptibility of mice to bacterial infection: course of listeriosis in resistant or susceptible mice. Infect. Immun. 19(3), 763-768 (1978).
121. Stelma GN, Reyes AL, Peter JT et al.: Pathogenicity test for Listeria monocytogenes using immunocompromised mice. J. Clin. Microbiol. 25, 2085-2089 (1987).
122. Mandel TE, Cheers C: Resistance and susceptibility of mice to bacterial infection: histopathology of listeriosis in resistant and susceptible strains. Infect. Immun. 30(3), 851-861 (1980).
123. Liu D: Listeria monocytogenes: comparative interpretation of mouse virulence assay. FEMS Microbiol. Lett. 233(1), 159-164 (2004).
124. Pine L, Malcolm GB, Plikaytis BD: Listeria monocytogenes intragastric and intraperitoneal approximate 50% lethal doses for mice are comparable, but death occurs earlier by intragastric feeding. Infect. Immun. 58(9), 2940-2945 (1990).
125. Lecuit M, Vandormael-Pournin S, Lefort J et al.: A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292(5522), 1722-1725 (2001).
126. Wollert T, Pasche B, Rochon M et al.: Extending the host range of Listeria monocytogenes by rational protein design. Cell 129(5), 891-902 (2007).
127. Stams A: [Studies in cases of experimental eye infections with Listeria monocytogenes]. Graefes Arch. Clin. Exp. Ophthalmol. 173(1), 1-20 (1967).
128. Schluter D, Chahoud S, Lassmann H, Schumann A, Hof H, Deckertschluter M: Intracerebral targets and immunomodulation of murine Listeria monocytogenes meningoencephalitis. J. Neuropath. Exp. Neur. 55(1), 14-24 (1996).
129. Nishikawa S, Hirasue M, Miura T, Yamada K, Sasaki S, Nakane A: Systemic dissemination by intrarectal infection with Listeria monocytogenes in mice. Microbiol. Immunol. 42(4), 325-327 (1998).
130. Paterson JS: Experimental infection of the chick embryo with organisms of the genus Listerella. J. Pathol. Bacteriol. 51, 437-440 (1940).
131. Basher HA, Fowler DR, Rodgers FG, Seaman A, Woodbine M: Pathogenesis and growth of Listeria monocytogenes in fertile hens eggs. Zentralbl. Bakteriol. Mikrobiol. Hyg. [A] 256(4), 477-509 (1984).
132. Avery SM, Buncic S: Differences in pathogenicity for chick embryos and growth kinetics at 37 degrees C between clinical and meat isolates of Listeria monocytogenes previously stored at 4 degrees C. Int. J. Food Microbiol. 34(3), 319-327 (1997).
133. Olier M, Pierre F, Lemaitre JP, Divies C, Rousset A, Guzzo J: Assessment of the pathogenic potential of two Listeria monocytogenes human faecal carriage isolates. Microbiol. 148(Pt 6), 1855-1862 (2002).
134. Cappelier JM, Besnard V, Roche SM, Velge P, Federighi M: Avirulent viable but non culturable cells of Listeria monocytogenes need the presence of an embryo to be recovered in egg yolk and regain virulence after recovery. Vet. Res. 38(4), 573-583 (2007).
135. Mansfield BE, Dionne MS, Schneider DS, Freitag NE: Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell. Microbiol. 5(12), 901-911 (2003).
136. Thomsen LE, Slutz SS, Tan MW, Ingmer H: Caenorhabditis elegans is a model host for Listeria monocytogenes. Appl. Env. Microbiol. 72(2), 1700-1701 (2006).
137. Mukherjee K, Altincicek B, Hain T, Domann E, Vilcinskas A, Chakraborty T: Galleria mellonella as a model system for studying Listeria pathogenesis. Appl. Env. Microbiol. 76(1), 310-317 (2010).
138. Pine L, Kathariou S, Quinn F, George V, Wenger JD, Weaver RE: Cytopathogenic effects in enterocytelike Caco-2 cells differentiate virulent from avirulent Listeria strains. J. Clin. Microbiol. 29, 990-996 (1991).
139. Cheng LW, Viala JP, Stuurman N, Wiedemann U, Vale RD, Portnoy DA: Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen. Proc. Natl Acad. Sci. USA 102(38), 13646-13651 (2005).
140. Agaisse H, Burrack LS, Philips JA, Rubin EJ, Perrimon N, Higgins DE: Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309(5738), 1248-1251 (2005).
141. Liu D, Lawrence ML, Ainsworth AJ, Austin FW: Toward an improved laboratory definition of Listeria monocytogenes virulence. Int. J. Food Microbiol. 118(2), 101-115 (2007).
142. Jacquet C, Doumith M, Gordon JI, Martin PM, Cossart P, Lecuit M: A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J. Infect. Dis. 189(11), 2094-2100 (2004).
143. Jacquet C, Gouin E, Jeannel D, Cossart P, Rocourt J: Expression of ActA, Ami, InlB, and listeriolysin O in Listeria monocytogenes of human and food origin. Appl. Env. Microbiol. 68(2), 616-622 (2002).
144. Kathariou S: Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J. Food Protect. 65(11), 1811-1829 (2002).
145. Velge P, Herler M, Johansson J et al.: A naturally occurring mutation K220T in the pleiotropic activator PrfA of Listeria monocytogenes results in a loss of virulence due to decreasing DNA-binding affinity. Microbiology 153(Pt 4), 995-1005 (2007).
146. Roche SM, Grepinet O, Corde Y et al.: A Listeria monocytogenes strain is still virulent despite nonfunctional major virulence genes. J. Infect. Dis. 200(12), 1944-1948 (2009).
147. Jonquieres R, Bierne H, Mengaud J, Cossart P: The inlA gene of Listeria monocytogenes L028 harbors a nonsense mutation resulting in release of internalin. Infect. Immun. 66(7), 3420-3422 (1998).
148. Nightingale KK, Ivy RA, Ho AJ et al.: inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. Appl. Env. Microbiol. 74(21), 6570-6583 (2008).
149. Temoin S, Roche SM, Grepinet O, Fardini Y, Velge P: Multiple point mutations in virulence genes explain the low virulence of Listeria monocytogenes field strains. Microbiology 154(Pt 3), 939-948 (2008).
150. Smith GA, Theriot JA, Portnoy DA: The tandem repeat domain in the Listeria monocytogenes acta protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator- stimulated phosphoprotein and profilin. J. Cell Biol. 135(3), 647-650 (1996).
151. Chakraborty T, Ebel F, Wehland J, Dufrenne J, Notermans S: Naturally occurring virulence-attenuated isolates of Listeria monocytogenes capable of inducing long term protection against infection by virulent strains of homologous and heterologous serotypes. FEMS Immunol. Med. Microbiol. 10(1), 1-9 (1994).
152. Sokolovic Z, Schuller S, Bohne J et al.: Differences in virulence and in expression of Prfa and Prfa-regulated virulence genes of Listeria monocytogenes strains belonging to serogroup 4. Infect. Immun. 64(10), 4008-4019 (1996).
153. Moriishi K, Terao M, Koura M, Inoue S: Sequence analysis of the actA gene of Listeria monocytogenes isolated from human. Microbiol. Immunol. 42(2), 129-132 (1998).
154. Roberts AJ, Wiedmann M: Allelic exchange and site-directed mutagenesis probe the contribution of ActA amino-acid variability to phosphorylation and virulence-associated phenotypes among Listeria monocytogenes strains. FEMS Microbiol. Lett. 254(2), 300-307 (2006).
155. Barry RA, Bouwer HGA, Portnoy DA, Hinrichs DJ: Pathogenicity and immunogenicity of Listeria-monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect. Immun. 60, 1625-1632 (1992).
156. Liu D, Ainsworth AJ, Austin FW, Lawrence ML: Characterization of virulent and avirulent Listeria monocytogenes strains by PCR amplification of putative transcriptional regulator and internalin genes. J. Med. Microbiol. 52(Pt 12), 1065-1070 (2003).
157. 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(10), 6912-6922 (2005).
158. Yildirim S, Lin W, Hitchins AD et al.: Epidemic clone I-specific genetic markers in strains of Listeria monocytogenes serotype 4b from foods. Appl. Env. Microbiol. 70(7), 4158-4164 (2004).
159. Evans MR, Swaminathan B, Graves LM et al.: Genetic markers unique to Listeria monocytogenes serotype 4b differentiate epidemic clone II (hot dog outbreak strains) from other lineages. Appl. Env. Microbiol. 70(4), 2383-2390 (2004).
160. Cotter PD, Draper LA, Lawton EM et al.: Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog. 4(9), E1000144 (2008).
161. Mueller KJ, Freitag NE: Pleiotropic enhancement of bacterial pathogenesis resulting from the constitutive activation of the Listeria monocytogenes regulatory factor PrfA. Infect. Immun. 73(4), 1917-1926 (2005).
162. Shetron-Rama LM, Mueller K, Bravo JM, Bouwer HG, Way SS, Freitag NE: Isolation of Listeria monocytogenes mutants with high-level in vitro expression of host cytosol-induced gene products. Mol. Microbiol. 48(6), 1537-1551 (2003).
163. Ripio MT, Dominguezbernal G, Lara M, Suarez M, Vazquezboland JA: A gly145ser substitution in the transcriptional activator prfa causes constitutive overexpression of virulence factors in Listeria monocytogenes. J. Bacteriol. 179(5), 1533-1540 (1997).
164. Freitag NE, Port GC, Miner MD: Listeria monocytogenes - from saprophyte to intracellular pathogen. Nature Rev. 7(9), 623-628 (2009).
165. Gracieux P, Roche SM, Pardon P, Velge P: Hypovirulent Listeria monocytogenes strains are less frequently recovered than virulent strains on PALCAM and Rapid L. mono media. Int. J. Food Microbiol. 83(2), 133-145 (2003).
166. Vlaemynck G, Lafarge V, Scotter S: Improvement of the detection of listeria monocytogenes by the application of ALOA, a diagnostic, chromogenic isolation medium. J. Appl. Microbiol. 88, 430-441 (2000).
167. Scotter SL, Langton S, Lombard B et al.: Validation of ISO method 11290 part 1-detection of Listeria monocytogenes in foods. Int. J. Food Microbiol. 64(3), 295-306 (2001). (Pubitemid 32186395)
168. Roche SM, Gracieux P, Velge P: Poor detection of low-virulence field strains of L. monocytogenes is related to selective agents in selective media and is unrelated to PrfA. Food Microbiol. 26(1), 21-26 (2009).
169. Toro JC, Hoffner S, Linde C, Andersson M, Andersson J, Grundstrom S: Enhanced susceptibility of multidrug resistant strains of Mycobacterium tuberculosis to granulysin peptides correlates with a reduced fitness phenotype. Microbes Infect. 8(8), 1985-1993 (2006).
170. Duriez P, Zhang Y, Lu Z, Scott A, Topp E: Loss of virulence genes in Escherichia coli populations during manure storage on a commercial swine farm. Appl. Env. Microbiol. 74(13), 3935-3942 (2008).
171. Andersson DI, Levin BR: The biological cost of antibiotic resistance. Curr. Opin. Microbiol. 2(5), 489-493 (1999).
172. Van Stelten A, Simpson JM, Ward TJ, Nightingale KK: Revelation by single-nucleotide polymorphism genotyping that mutations leading to a premature stop codon in inlA are common among Listeria monocytogenes isolates from ready-to-eat foods but not human listeriosis cases. Appl. Env. Microbiol. 76(9), 2783-2790 (2010).
173. Ward TJ, Evans P, Wiedmann M et al.: Molecular and phenotypic characterization of Listeria monocytogenes from U.S. Department of Agriculture Food Safety and Inspection Service surveillance of ready-to-eat foods and processing facilities. J. Food Protect. 73(5), 861-869 (2010).
174. Allerberger F, Dierich M, Petranyi G, Lalic M, Bubert A: Nonhemolytic strains of Listeria monocytogenes detected in milk products using VIDAS immunoassay kit. Zentralbl. Hyg. Umweltmed. 200, 189-195 (1997).
175. Roche SM, Kerouanton A, Minet J, Le Monnier A, Brisabois A, Velge P: Prevalence of low-virulence Listeria monocytogenes strains from different foods and environments. Int. J. Food Microbiol. 130(2), 151-155 (2009).
176. Varnam AH, Evans MG: Listeria monocytogenes. In: Foodborne Pathogens, An Illustrated Text Vol. Wolfe Publishing Ltd., Aylesbury, UK, 327-355 (1991).
177. Bruhn KW, Craft N, Miller JF: Listeria as a vaccine vector. Microbes Infect. 9(10), 1226-1235 (2007).
178. Angelakopoulos H, Loock K, Sisul DM, Jensen ER, Miller JF, Hohmann EL: Safety and shedding of an attenuated strain of Listeria monocytogenes with a deletion of actA/plcB in adult volunteers: a dose escalation study of oral inoculation. Infect. Immun. 70(7), 3592-3601 (2002).
179. Brockstedt DG, Giedlin MA, Leong ML et al.: Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc. Natl Acad. Sci. USA 101(38), 13832-13837 (2004).
180. Yan L, Qiu J, Chen J et al.: Selected prfA mutations in recombinant attenuated Listeria monocytogenes strains augment expression of foreign immunogens and enhance vaccine-elicited humoral and cellular immune responses. Infect. Immun. 76(8), 3439-3450 (2008).
181. Hain T, Chatterjee SS, Ghai R et al.: Pathogenomics of Listeria spp. Int. J. Med. Microbiol.297(7-8), 541-557 (2007).
182. Salcedo C, Arreaza L, Alcala B, de la Fuente L, Vazquez JA: Development of a multilocus sequence typing method for analysis of Listeria monocytogenes clones. J. Clin. Microbiol. 41(2), 757-762 (2003).
183. Thomson NR, Clayton DJ, Windhorst D et al.: Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18(10), 1624-1637 (2008).
184. Schmid MW, Ng EY, Lampidis R et al.: Evolutionary history of the genus Listeria and its virulence genes. Syst. Appl. Microbiol. 28(1), 1-18 (2005).
185. Hain T, Steinweg C, Kuenne CT et al.: Whole-genome sequence of Listeria welshimeri reveals common steps in genome reduction with Listeria innocua as compared to Listeria monocytogenes. J. Bacteriol. 188(21), 7405-7415 (2006).
186. Sleator RD, Watson D, Hill C, Gahan CG: The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology 155(Pt 8), 2463-2475 (2009).
187. Volokhov DV, Duperrier S, Neverov AA, George J, Buchrieser C, Hitchins AD: The presence of the internalin gene in natural atypically hemolytic Listeria innocua strains suggests descent from L. monocytogenes. Appl. Environ. Microbiol. 73(6), 1928-1939 (2007).
188. Chen J, Chen Q, Jiang L et al.: Internalin profiling and multilocus sequence typing suggest four Listeria innocua subgroups with different evolutionary distances from Listeria monocytogenes. BMC Microbiol. 10, 97 (2010).
189. Doumith M, Cazalet C, Simoes N et al.: New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect. Immun. 72(2), 1072-1083 (2004).
190. Ducey TF, Page B, Usgaard T, Borucki MK, Pupedis K, Ward TJ: A single-nucleotide-polymorphism-based multilocus genotyping assay for subtyping lineage I isolates of Listeria monocytogenes. Appl. Env. Microbiol. 73(1), 133-147 (2007).
191. Retchless AC, Lawrence JG: Temporal fragmentation of speciation in bacteria. Science 317(5841), 1093-1096 (2007).