ActA Promotes Listeria monocytogenes Aggregation, Intestinal Colonization and Carriage

PLoS Pathogens

Volumn 9, Issue 1, 2013, Pages

  Travier, Laetitia ^a,b   Guadagnini, Stéphanie ^a   Gouin, Edith ^a,b   Dufour, Alexandre ^a,c   Chenal Francisque, Viviane ^a   Cossart, Pascale ^a,b   Olivo Marin, Jean Christophe ^a,c   Ghigo, Jean Marc ^a,c   Disson, Olivier ^a,b   Lecuit, Marc ^a,b,d  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACT A PROTEIN; BACTERIAL PROTEIN; UNCLASSIFIED DRUG;

ACT A GENE; ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOFILM; BRIGHT FIELD MICROSCOPY; CELL AGGREGATION; DENSITOMETRY; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; ISOELECTRIC POINT; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; NONHUMAN; PROTEIN INTERACTION; SCANNING ELECTRON MICROSCOPY;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CECUM; CELL LINE; COLON; DISEASE MODELS, ANIMAL; FECES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINAL MUCOSA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMBRANE PROTEINS; MICE; VIRULENCE FACTORS;

EID: 84875069366     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003131     Document Type: Article

References (74)

1. 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.
2. 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. Molecular Microbiology 16: 251-261.
3. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, et al. (2001) A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292: 1722-1725.
4. Disson O, Grayo S, Huillet E, Nikitas G, Langa-Vives F, et al. (2008) Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455: 1114-1118.
5. Lecuit M, Nelson D, Smith S, Khun H, Huerre M, et al. (2004) Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proceedings of the National Academy of Sciences 101: 6152.
6. Nikitas G, Deschamps C, Disson O, Niault T, Cossart P, et al. (2011) Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J Exp Med 208: 2263-2277.
7. Cossart P, Vicente MF, Mengaud J, Baquero F, Perez-Diaz JC, et al. (1989) Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infection and Immunity 57: 3629-3636.
8. Goebel W, Kathariou S, Kuhn M, Sokolovic Z, Kreft J, et al. (1988) Hemolysin from Listeria-biochemistry, genetics and function in pathogenesis. Infection 16: S149-156.
9. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, et al. (1992) L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-531.
10. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, et al. (2009) Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nature Cell Biology 11: 1233-1240.
11. Leimeister-Wächter M, Domann E, Chakraborty T, (1992) The expression of virulence genes in Listeria monocytogenes is thermoregulated. J Bacteriol 174: 947-952.
12. Mengaud J, Dramsi S, Gouin E, Vazquez-Boland JA, Milon G, et al. (1991) Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated. Molecular Microbiology 5: 2273-2283.
13. de Las Heras A, Cain RJ, Bielecka MK, Vázquez-Boland JA, (2011) Regulation of Listeria virulence: PrfA master and commander. Current Opinion in Microbiology 14: 118-127.
14. 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.
15. MacGowan AP, Marshall RJ, MacKay IM, Reeves DS, (1991) Listeria faecal carriage by renal transplant recipients, haemodialysis patients and patients in general practice: its relation to season, drug therapy, foreign travel, animal exposure and diet. Epidemiol Infect 106: 157-166.
16. Grif K, Patscheider G, Dierich MP, Allerberger F, (2003) Incidence of fecal carriage of Listeria monocytogenes in three healthy volunteers: a one-year prospective stool survey. Eur J Clin Microbiol Infect Dis 22: 16-20.
17. Ivanek R, Gröhn YT, Wiedmann M, (2007) Listeria monocytogenes in multiple habitats and host populations: review of available data for mathematical modeling. Foodborne Pathog Dis 3: 319-336.
18. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM, (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
19. Carpentier B, Cerf O, (2011) Review-Persistence of Listeria monocytogenes in food industry equipment and premises. International Journal of Food Microbiology 145: 1-8.
20. Rieu A, Weidmann S, Garmyn D, Piveteau P, Guzzo J, (2007) Agr system of Listeria monocytogenes EGD-e: role in adherence and differential expression pattern. Appl Environ Microbiol 73: 6125-6133.
21. Challan Belval S, Gal L, Margiewes S, Garmyn D, Piveteau P, et al. (2006) Assessment of the roles of LuxS, S-ribosyl homocysteine, and autoinducer 2 in cell attachment during biofilm formation by Listeria monocytogenes EGD-e. Appl Environ Microbiol 72: 2644-2650.
22. Taylor CM, Beresford M, Epton HAS, Sigee DC, Shama G, et al. (2002) Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol 184: 621-628.
23. Wilson RL, Brown LL, Kirkwood-Watts D, Warren TK, Lund SA, et al. (2006) Listeria monocytogenes 10403S HtrA is necessary for resistance to cellular stress and virulence. Infect Immun 74: 765-768.
24. van der Veen S, Abee T, (2010) HrcA and DnaK are important for static and continuous-flow biofilm formation and disinfectant resistance in Listeria monocytogenes. Microbiology 156: 3782-3790.
25. van der Veen S, Abee T, (2010) Dependence of continuous-flow biofilm formation by Listeria monocytogenes EGD-e on SOS response factor YneA. Appl Environ Microbiol 76: 1992-1995.
26. van der Veen S, Abee T, (2010) Importance of SigB for Listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Appl Environ Microbiol 76: 7854-7860.
27. Lemon KP, Freitag NE, Kolter R, (2010) The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. Journal of Bacteriology 192: 3969-3976.
28. Zhou Q, Feng F, Wang L, Feng X, Yin X, et al. (2011) Virulence Regulator PrfA is Essential for Biofilm Formation in Listeria monocytogenes but not in Listeria innocua. Curr Microbiol 63: 186-192.
29. Kjaergaard K, Schembri MA, Hasman H, Klemm P, (2000) Antigen 43 from Escherichia coli induces inter- and intraspecies cell aggregation and changes in colony morphology of Pseudomonas fluorescens. Journal of Bacteriology 182: 4789-4796.
30. Wells TJ, Tree JJ, Ulett GC, Schembri MA, (2007) Autotransporter proteins: novel targets at the bacterial cell surface. FEMS Microbiology Letters 274: 163-172.
31. Bohne J, Sokolovic Z, Goebel W, (1994) Transcriptional regulation of prfA and PrfA-regulated virulence genes in Listeria monocytogenes. Molecular Microbiology 11: 1141-1150.
32. Welch MD, Rosenblatt J, Skoble J, Portnoy DA, Mitchison TJ, (1998) Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281: 105-108.
33. Meng G, Spahich N, Kenjale R, Waksman G, St Geme JW, (2011) Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation. The EMBO Journal 30: 3864-3874.
34. Braun L, Dramsi S, Dehoux P, Bierne H, Lindahl G, et al. (1997) InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Molecular Microbiology 25: 285-294.
35. Lasa I, David V, Gouin E, Marchand JB, Cossart P, (1995) The amino-terminal part of ActA is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Molecular Microbiology 18: 425-436.
36. Lasa I, Gouin E, Goethals M, Vancompernolle K, David V, et al. (1997) Identification of two regions in the N-terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes. EMBO J 16: 1531-1540.
37. Pistor S, Chakraborty T, Walter U, Wehland J, (1995) The bacterial actin nucleator protein ActA of Listeria monocytogenes contains multiple binding sites for host microfilament proteins. Curr Biol 5: 517-525.
38. Smith GA, Theriot JA, Portnoy DA, (1996) 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: 647-660.
39. Pistor S, Gröbe L, Sechi AS, Domann E, Gerstel B, et al. (2000) Mutations of arginine residues within the 146-KKRRK-150 motif of the ActA protein of Listeria monocytogenes abolish intracellular motility by interfering with the recruitment of the Arp2/3 complex. J Cell Sci 113: 3277-3287.
40. Theriot JA, Rosenblatt J, Portnoy DA, Goldschmidt-Clermont PJ, Mitchison TJ, (1994) Involvement of profilin in the actin-based motility of L. monocytogenes in cells and in cell-free extracts. Cell 76: 505-517.
41. Chakraborty T, Ebel F, Domann E, Niebuhr K, Gerstel B, et al. (1995) A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells. EMBO J 14: 1314-1321.
42. Skoble J, Portnoy DA, Welch MD, (2000) Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J Cell Biol 150: 527-538.
43. Boujemaa-Paterski R, Gouin E, Hansen G, Samarin S, Le Clainche C, et al. (2001) Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40: 11390-11404.
44. Melton-Witt JA, Rafelski SM, Portnoy DA, Bakardjiev AI, (2011) Oral infection with signature-tagged Listeria monocytogenes reveals organ-specific growth and dissemination routes in guinea pigs. Infection and Immunity 80: 730-732.
45. Hardy J, Margolis JJ, Contag CH, (2006) Induced biliary excretion of Listeria monocytogenes. Infection and Immunity 74: 1819-1827.
46. Pentecost M, Otto G, Theriot JA, Amieva MR, (2006) Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2: e3.
47. Franciosa G, Maugliani A, Scalfaro C, Floridi F, Aureli P, (2009) Expression of internalin A and biofilm formation among Listeria monocytogenes clinical isolates. Int J Immunopathol Pharmacol 22: 183-193.
48. Cossart P, (2011) Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc Natl Acad Sci USA 108: 19484-19491.
49. Kocks C, Hellio R, Gounon P, Ohayon H, Cossart P, (1993) Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J Cell Sci 105: 699-710.
50. Mourrain P, Lasa I, Gautreau A, Gouin E, Pugsley A, et al. (1997) ActA is a dimer. Proc Natl Acad Sci USA 94: 10034-10039.
51. Cicchetti G, Maurer P, Wagener P, Kocks C, (1999) Actin and phosphoinositide binding by the ActA protein of the bacterial pathogen Listeria monocytogenes. J Biol Chem 274: 33616-33626.
52. Gouin E, Dehoux P, Mengaud J, Kocks C, Cossart P, (1995) iactA of Listeria ivanovii, although distantly related to Listeria monocytogenes actA, restores actin tail formation in an L. monocytogenes actA mutant. Infection and Immunity 63: 2729-2737.
53. Conter M, Vergara A, Di Ciccio P, Zanardi E, Ghidini S, et al. (2010) Polymorphism of actA gene is not related to in vitro virulence of Listeria monocytogenes. International Journal of Food Microbiology 137: 100-105.
54. Suárez M, González-Zorn B, Vega Y, Chico-Calero I, Vázquez-Boland JA, (2001) A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cellular Microbiology 3: 853-864.
55. Holch A, Gottlieb CT, Larsen MH, Ingmer H, Gram L, (2010) Poor invasion of trophoblastic cells but normal plaque formation in fibroblastic cells despite actA deletion in a group of Listeria monocytogenes strains persisting in some food processing environments. Appl Environ Microbiol 76: 3391-3397.
56. Stevens MP, Humphrey TJ, Maskell DJ, (2009) Molecular insights into farm animal and zoonotic Salmonella infections. Philos Trans R Soc Lond, B, Biol Sci 364: 2709-2723.
57. Mundy R, Macdonald TT, Dougan G, Frankel G, Wiles S, (2005) Citrobacter rodentium of mice and man. Cell Microbiol 7: 1697-1706.
58. Ferens WA, Hovde CJ, (2011) Escherichia coli O157:H7: animal reservoir and sources of human infection. Foodborne Pathog Dis 8: 465-487.
59. Hermans D, Pasmans F, Heyndrickx M, Van Immerseel F, Martel A, et al. (2012) A tolerogenic mucosal immune response leads to persistent Campylobacter jejuni colonization in the chicken gut. Crit Rev Microbiol 38: 17-29.
60. Lecuit M, Sonnenburg J, Cossart P, Gordon J, (2007) Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model. Journal of Biological Chemistry 282: 15065.
61. Doyle MP, Erickson MC, (2006) Reducing the carriage of foodborne pathogens in livestock and poultry. Poult Sci 85: 960-973.
62. Chase-Topping M, Gally D, Low C, Matthews L, Woolhouse M, (2008) Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat Rev Micro 6: 904-912.
63. Wernars K, Heuvelman K, Notermans S, Domann E, Leimeister-Wächter M, et al. (1992) Suitability of the prfA gene, which encodes a regulator of virulence genes in Listeria monocytogenes, in the identification of pathogenic Listeria spp. Appl Environ Microbiol 58: 765-768.
64. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science 294: 849-852.
65. Gouin E, Adib-Conquy M, Balestrino D, Nahori M-A, Villiers V, et al. (2010) The Listeria monocytogenes InlC protein interferes with innate immune responses by targeting the I{kappa}B kinase subunit IKK{alpha}. Proc Natl Acad Sci USA 107: 17333-17338.
66. Balestrino D, Hamon MA, Dortet L, Nahori M-A, Pizarro-Cerda J, et al. (2010) Single-cell techniques using chromosomally tagged fluorescent bacteria to study Listeria monocytogenes infection processes. Applied and Environmental Microbiology 76: 3625-3636.
67. Lauer P, Chow MYN, Loessner MJ, Portnoy DA, Calendar R, (2002) Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. Journal of Bacteriology 184: 4177-4186.
68. Arnaud M, Chastanet A, Débarbouillé M, (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
69. Kocks C, Marchand JB, Gouin E, d'Hauteville H, Sansonetti PJ, et al. (1995) The unrelated surface proteins ActA of Listeria monocytogenes and IcsA of Shigella flexneri are sufficient to confer actin-based motility on Listeria innocua and Escherichia coli respectively. Molecular Microbiology 18: 413-423.
70. Disson O, Nikitas G, Grayo S, Dussurget O, Cossart P, et al. (2009) Modeling human listeriosis in natural and genetically engineered animals. Nat Protoc 4: 799-810.
71. Archambaud C, Nahori M-A, Soubigou G, Bécavin C, Laval L, et al. (2012) Impact of lactobacilli on orally acquired listeriosis. Proceedings of the National Academy of Sciences 109: 16684-16689.
72. Dramsi S, Lévi S, Triller A, Cossart P, (1998) Entry of Listeria monocytogenes into neurons occurs by cell-to-cell spread: an in vitro study. Infection and Immunity 66: 4461-4468.
73. Friederich E, Gouin E, Hellio R, Kocks C, Cossart P, et al. (1995) Targeting of Listeria monocytogenes ActA protein to the plasma membrane as a tool to dissect both actin-based cell morphogenesis and ActA function. EMBO J 14: 2731-2744.
74. Archambaud C, Gouin E, Pizarro-Cerda J, Cossart P, Dussurget O, (2005) Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Molecular Microbiology 56: 383-396.