The pore-forming toxin listeriolysin o mediates a novel entry pathway of L. monocytogenes into human hepatocytes

PLoS Pathogens

Volumn 7, Issue 11, 2011, Pages

  Vadia, Stephen ^a   Arnett, Eusondia ^a   Haghighat, Anne Cécile ^a   Wilson Kubalek, Elisabeth M ^b   Tweten, Rodney K ^c   Seveau, Stephanie ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; F ACTIN; INLA PROTEIN; INLB PROTEIN; LISTERIOLYSIN O; POLYSTYRENE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL TOXIN; CLATHRIN; CYTOTOXIN; DYNAMIN; HEAT SHOCK PROTEIN; HEMOLYSIN; HLYA PROTEIN, LISTERIA MONOCYTOGENES; MICROSPHERE; POLYSTYRENE DERIVATIVE; PORE FORMING CYTOTOXIC PROTEIN; PROTEIN TYROSINE KINASE;

ARTICLE; BACTERIAL VIRULENCE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM VESICLE; DOSE RESPONSE; FLUORESCENCE MICROSCOPY; HOST CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LISTERIA MONOCYTOGENES; LIVER CELL; MEMBRANE FORMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ASSEMBLY; PROTEIN POLYMERIZATION; SCANNING ELECTRON MICROSCOPY; CELL STRAIN HEPG2; HELA CELL; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); LISTERIA INNOCUA; LISTERIA MONOCYTOGENES;

ACTINS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE; CLATHRIN; CYTOTOXINS; DYNAMINS; HEAT-SHOCK PROTEINS; HELA CELLS; HEMOLYSIN PROTEINS; HEP G2 CELLS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; LISTERIA MONOCYTOGENES; MICROSPHERES; POLYSTYRENES; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN-TYROSINE KINASES;

EID: 81755183022     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002356     Document Type: Article

References (102)

1. Cossart P, Sansonetti PJ, (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304: 242-248.
2. Pizarro-Cerda J, Cossart P, (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727.
3. Valdez Y, Ferreira RB, Finlay BB, (2009) Molecular mechanisms of Salmonella virulence and host resistance. Curr Top Microbiol Immunol 337: 93-127.
4. Lara-Tejero M, Kato J, Wagner S, Liu X, Galan JE, (2011) A Sorting Platform Determines the Order of Protein Secretion in Bacterial Type III Systems. Science 331: 1188-1191.
5. Galan JE, (2009) Common themes in the design and function of bacterial effectors. Cell Host Microbe 5: 571-579.
6. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
7. Gellin BG, Broome CV, Bibb WF, Weaver RE, Gaventa S, et al. (1991) The epidemiology of listeriosis in the United States-1986. Listeriosis Study Group. Am J Epidemiol 133: 392-401.
8. Jackson KA, Iwamoto M, Swerdlow D, (2010) Pregnancy-associated listeriosis. Epidemiol Infect 138: 1503-1509.
9. 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.
10. Pentecost M, Otto G, Theriot JA, Amieva MR, (2006) Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2: e3.
11. 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.
12. Gaillard JL, Jaubert F, Berche P, (1996) The inlAB locus mediates the entry of Listeria monocytogenes into hepatocytes in vivo. J Exp Med 183: 359-369.
13. Stavru F, Archambaud C, Cossart P, (2011) Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol Rev 240: 160-184.
14. Seveau S, Pizarro-Cerda J, Cossart P, (2007) Molecular mechanisms exploited by Listeria monocytogenes during host cell invasion. Microbes Infect 9: 1167-1175.
15. Pizarro-Cerda J, Cossart P, (2009) Listeria monocytogenes membrane trafficking and lifestyle: the exception or the rule? Annu Rev Cell Dev Biol 25: 649-670.
16. Ireton K, (2007) Entry of the bacterial pathogen Listeria monocytogenes into mammalian cells. Cell Microbiol 9: 1365-1375.
17. 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.
18. Vazquez-Boland JA, Dominguez-Bernal G, Gonzalez-Zorn B, Kreft J, Goebel W, (2001) Pathogenicity islands and virulence evolution in Listeria. Microbes Infect 3: 571-584.
19. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P, (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84: 923-932.
20. Shen Y, Naujokas M, Park M, Ireton K, (2000) InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103: 501-510.
21. Pentecost M, Kumaran J, Ghosh P, Amieva MR, (2010) Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog 6: e1000900.
22. Dramsi S, Biswas I, Maguin E, Braun L, Mastroeni P, et al. (1995) Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 16: 251-261.
23. Seveau S, Bierne H, Giroux S, Prevost MC, Cossart P, (2004) Role of lipid rafts in E-cadherin- and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J Cell Biol 166: 743-753.
24. Seveau S, Tham TN, Payrastre B, Hoppe AD, Swanson JA, et al. (2007) A FRET analysis to unravel the role of cholesterol in Rac1 and PI 3-kinase activation in the InlB/Met signalling pathway. Cell Microbiol 9: 790-803.
25. Veiga E, Guttman JA, Bonazzi M, Boucrot E, Toledo-Arana A, et al. (2007) Invasive and adherent bacterial pathogens co-Opt host clathrin for infection. Cell Host Microbe 2: 340-351.
26. Pizarro-Cerda J, Bonazzi M, Cossart P, (2010) Clathrin-mediated endocytosis: what works for small, also works for big. Bioessays 32: 496-504.
27. Schnupf P, Portnoy DA, (2007) Listeriolysin O: a phagosome-specific lysin. Microbes Infect 9: 1176-1187.
28. Tilney LG, Portnoy DA, (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109: 1597-1608.
29. Henry R, Shaughnessy L, Loessner MJ, Alberti-Segui C, Higgins DE, et al. (2006) Cytolysin-dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cell Microbiol 8: 107-119.
30. Braun L, Ohayon H, Cossart P, (1998) The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol 27: 1077-1087.
31. Alvarez-Dominguez C, Vazquez-Boland JA, Carrasco-Marin E, Lopez-Mato P, Leyva-Cobian F, (1997) Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect Immun 65: 78-88.
32. Suarez M, Gonzalez-Zorn B, Vega Y, Chico-Calero I, Vazquez-Boland JA, (2001) A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cell Microbiol 3: 853-864.
33. Bergmann B, Raffelsbauer D, Kuhn M, Goetz M, Hom S, et al. (2002) InlA- but not InlB-mediated internalization of Listeria monocytogenes by non-phagocytic mammalian cells needs the support of other internalins. Mol Microbiol 43: 557-570.
34. Reis O, Sousa S, Camejo A, Villiers V, Gouin E, et al. (2010) LapB, a Novel Listeria monocytogenes LPXTG Surface Adhesin, Required for Entry into Eukaryotic Cells and Virulence. J Infect Dis 202: 551-62.
35. Dramsi S, Cossart P, (2003) Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect Immun 71: 3614-3618.
36. Gaillard JL, Berche P, Sansonetti P, (1986) Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun 52: 50-55.
37. Tweten RK, (2005) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 73: 6199-6209.
38. Billington SJ, Jost BH, Songer JG, (2000) Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol Lett 182: 197-205.
39. Mitchell TJ, Andrew PW, (1997) Biological properties of pneumolysin. Microb Drug Resist 3: 19-26.
40. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK, (2010) Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci U S A 107: 4341-4346.
41. Giddings KS, Zhao J, Sims PJ, Tweten RK, (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat Struct Mol Biol 11: 1173-1178.
42. Gelber SE, Aguilar JL, Lewis KL, Ratner AJ, (2008) Functional and phylogenetic characterization of Vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J Bacteriol 190: 3896-3903.
43. Wickham SE, Hotze EM, Farrand AJ, Polekhina G, Nero TL, et al. (2011) Mapping the intermedilysin-human CD59 receptor interface reveals a deep correspondence with the binding site on CD59 for complement binding proteins C8alpha and C9. J Biol Chem 286: 20952-20962.
44. Shepard LA, Shatursky O, Johnson AE, Tweten RK, (2000) The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. Biochemistry 39: 10284-10293.
45. Idone V, Tam C, Goss JW, Toomre D, Pypaert M, et al. (2008) Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J Cell Biol 180: 905-914.
46. Los FC, Kao CY, Smitham J, McDonald KL, Ha C, et al. (2011) RAB-5- and RAB-11-Dependent Vesicle-Trafficking Pathways Are Required for Plasma Membrane Repair after Attack by Bacterial Pore-Forming Toxin. Cell Host Microbe 9: 147-157.
47. Thiery J, Keefe D, Saffarian S, Martinvalet D, Walch M, et al. (2010) Perforin activates clathrin- and dynamin-dependent endocytosis, which is required for plasma membrane repair and delivery of granzyme B for granzyme-mediated apoptosis. Blood 115: 1582-1593.
48. Haghighat AC, Seveau S, (2010) Quantification of host-microbe interactions by automated fluorescence microscopy. J Immunol Methods 352: 186-191.
49. Gedde MM, Higgins DE, Tilney LG, Portnoy DA, (2000) Role of listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 68: 999-1003.
50. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science 294: 849-852.
51. Schuerch DW, Wilson-Kubalek EM, Tweten RK, (2005) Molecular basis of listeriolysin O pH dependence. Proc Natl Acad Sci U S A 102: 12537-12542.
52. Hotze EM, Wilson-Kubalek EM, Rossjohn J, Parker MW, Johnson AE, et al. (2001) Arresting pore formation of a cholesterol-dependent cytolysin by disulfide trapping synchronizes the insertion of the transmembrane beta-sheet from a prepore intermediate. J Biol Chem 276: 8261-8268.
53. Ramachandran R, Tweten RK, Johnson AE, (2004) Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit beta-strand alignment. Nat Struct Mol Biol 11: 697-705.
54. Nato F, Reich K, Lhopital S, Rouyre S, Geoffroy C, et al. (1991) Production and characterization of neutralizing and nonneutralizing monoclonal antibodies against listeriolysin O. Infect Immun 59: 4641-4646.
55. Giddings KS, Johnson AE, Tweten RK, (2003) Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins. Proc Natl Acad Sci U S A 100: 11315-11320.
56. Marriott HM, Mitchell TJ, Dockrell DH, (2008) Pneumolysin: a double-edged sword during the host-pathogen interaction. Curr Mol Med 8: 497-509.
57. Kumari S, Mg S, Mayor S, (2010) Endocytosis unplugged: multiple ways to enter the cell. Cell Res 20: 256-275.
58. Grundling A, Gonzalez MD, Higgins DE, (2003) Requirement of the Listeria monocytogenes broad-range phospholipase PC-PLC during infection of human epithelial cells. J Bacteriol 185: 6295-6307.
59. Burkholder KM, Bhunia AK, (2010) Listeria monocytogenes uses Listeria adhesion protein (LAP) to promote bacterial transepithelial translocation and induces expression of LAP receptor Hsp60. Infect Immun 78: 5062-5073.
60. Dramsi S, Bourdichon F, Cabanes D, Lecuit M, Fsihi H, et al. (2004) FbpA, a novel multifunctional Listeria monocytogenes virulence factor. Mol Microbiol 53: 639-649.
61. Reis O, Sousa S, Camejo A, Villiers V, Gouin E, et al. (2010) LapB, a novel Listeria monocytogenes LPXTG surface adhesin, required for entry into eukaryotic cells and virulence. J Infect Dis 202: 551-562.
62. Sabet C, Toledo-Arana A, Personnic N, Lecuit M, Dubrac S, et al. (2008) The Listeria monocytogenes virulence factor InlJ is specifically expressed in vivo and behaves as an adhesin. Infect Immun 76: 1368-1378.
63. Milohanic E, Jonquieres R, Cossart P, Berche P, Gaillard JL, (2001) The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor. Mol Microbiol 39: 1212-1224.
64. Linden SK, Bierne H, Sabet C, Png CW, Florin TH, et al. (2008) Listeria monocytogenes internalins bind to the human intestinal mucin MUC2. Arch Microbiol 190: 101-104.
65. Cabanes D, Sousa S, Cebria A, Lecuit M, Garcia-del Portillo F, et al. (2005) Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. EMBO J 24: 2827-2838.
66. Krawczyk-Balska A, Bielecki J, (2005) Listeria monocytogenes listeriolysin O and phosphatidylinositol-specific phospholipase C affect adherence to epithelial cells. Can J Microbiol 51: 745-751.
67. Bielecki J, (1994) Association of listeriolysin O with the cell surface of Listeria monocytogenes. Acta Microbiol Pol 43: 279-289.
68. Price KE, Camilli A, (2009) Pneumolysin localizes to the cell wall of Streptococcus pneumoniae. J Bacteriol 191: 2163-2168.
69. Bavdek A, Gekara NO, Priselac D, Gutierrez Aguirre I, Darji A, et al. (2007) Sterol and pH interdependence in the binding, oligomerization, and pore formation of Listeriolysin O. Biochemistry 46: 4425-4437.
70. Rottner K, Stradal TE, Wehland J, (2005) Bacteria-host-cell interactions at the plasma membrane: stories on actin cytoskeleton subversion. Dev Cell 9: 3-17.
71. Madden JC, Ruiz N, Caparon M, (2001) Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell 104: 143-152.
72. Magassa N, Chandrasekaran S, Caparon MG, (2010) Streptococcus pyogenes cytolysin-mediated translocation does not require pore formation by streptolysin O. EMBO Rep 11: 400-405.
73. Mayor S, Pagano RE, (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8: 603-612.
74. Gekara NO, Jacobs T, Chakraborty T, Weiss S, (2005) The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell Microbiol 7: 1345-1356.
75. Iliev AI, Djannatian JR, Nau R, Mitchell TJ, Wouters FS, (2007) Cholesterol-dependent actin remodeling via RhoA and Rac1 activation by the Streptococcus pneumoniae toxin pneumolysin. Proc Natl Acad Sci U S A 104: 2897-2902.
76. Joseph B, Przybilla K, Stuhler C, Schauer K, Slaghuis J, et al. (2006) Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol 188: 556-568.
77. Camejo A, Buchrieser C, Couve E, Carvalho F, Reis O, et al. (2009) In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 5: e1000449.
78. Sahu SC, Gaines DW, Williams KM, Raybourne RB, (2007) A synthetic polypeptide based on human E-cadherin inhibits invasion of human intestinal and liver cell lines by Listeria monocytogenes. J Med Microbiol 56: 1011-1016.
79. Nagai T, Arao T, Furuta K, Sakai K, Kudo K, et al. (2011) Sorafenib inhibits the hepatocyte growth factor-mediated epithelial mesenchymal transition in hepatocellular carcinoma. Mol Cancer Ther 10: 169-177.
80. Cossart P, Pizarro-Cerda J, Lecuit M, (2003) Invasion of mammalian cells by Listeria monocytogenes: functional mimicry to subvert cellular functions. Trends Cell Biol 13: 23-31.
81. Ibarra JA, Steele-Mortimer O, (2009) Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11: 1579-1586.
82. Parsot C, (2009) Shigella type III secretion effectors: how, where, when, for what purposes? Curr Opin Microbiol 12: 110-116.
83. Cossart P, Veiga E, (2008) Non-classical use of clathrin during bacterial infections. J Microsc 231: 524-528.
84. Iacovache I, Bischofberger M, van der Goot FG, (2010) Structure and assembly of pore-forming proteins. Curr Opin Struct Biol 20: 241-246.
85. Gonzalez MR, Bischofberger M, Pernot L, van der Goot FG, Freche B, (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci 65: 493-507.
86. Fernandes MC, Cortez M, Flannery AR, Tam C, Mortara RA, et al. (2011) Trypanosoma cruzi subverts the sphingomyelinase-mediated plasma membrane repair pathway for cell invasion. J Exp Med 208: 909-921.
87. Talbot UM, Paton AW, Paton JC, (1996) Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect Immun 64: 3772-3777.
88. Sukeno A, Nagamune H, Whiley RA, Jafar SI, Aduse-Opoku J, et al. (2005) Intermedilysin is essential for the invasion of hepatoma HepG2 cells by Streptococcus intermedius. Microbiol Immunol 49: 681-694.
89. Zhang JR, Mostov KE, Lamm ME, Nanno M, Shimida S, et al. (2000) The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102: 827-837.
90. Ammendolia MG, Superti F, Bertuccini L, Chiarini F, Conte MP, et al. (2007) Invasive pathway of Listeria ivanovii in human amnion-derived WISH cells. Int J Immunopathol Pharmacol 20: 509-518.
91. Russell BH, Vasan R, Keene DR, Xu Y, (2007) Bacillus anthracis internalization by human fibroblasts and epithelial cells. Cell Microbiol 9: 1262-1274.
92. Jost BH, Billington SJ, (2005) Arcanobacterium pyogenes: molecular pathogenesis of an animal opportunist. Antonie Van Leeuwenhoek 88: 87-102.
93. Logsdon LK, Hakansson AP, Cortes G, Wessels MR, (2011) Streptolysin O inhibits clathrin-dependent internalization of group a streptococcus. MBio 2: e00332-10.
94. Portnoy DA, Jacks PS, Hinrichs DJ, (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
95. Bakardjiev AI, Stacy BA, Fisher SJ, Portnoy DA, (2004) Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect Immun 72: 489-497.
96. Jones S, Portnoy DA, (1994) Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect Immun 62: 5608-5613.
97. Smith K, Youngman P, (1992) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74: 705-711.
98. Camilli A, Tilney LG, Portnoy DA, (1993) Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol Microbiol 8: 143-157.
99. 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. Infect Immun 57: 3629-3636.
100. Pushkareva VI, Ermolaeva SA, (2010) Listeria monocytogenes virulence factor Listeriolysin O favors bacterial growth in co-culture with the ciliate Tetrahymena pyriformis, causes protozoan encystment and promotes bacterial survival inside cysts. BMC Microbiol 10: 26.
101. Glomski IJ, Gedde MM, Tsang AW, Swanson JA, Portnoy DA, (2002) The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J Cell Biol 156: 1029-1038.
102. Arnett E, Lehrer RI, Pratikhya P, Lu W, Seveau S, (2010) Defensins enable macrophages to inhibit the intracellular proliferation of Listeria monocytogenes. Cell Microbiol 13: 635-51.