Invitro and invivo models to study human listeriosis: Mind the gap

Microbes and Infection

Volumn 15, Issue 14-15, 2013, Pages 971-980

  Disson, Olivier ^a,b   Lecuit, Marc ^a,b,c,d  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c WORLD HEALTH ORGANIZATION   (Switzerland)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Animal model; Invitro; Invivo; Listeria monocytogenes; Listeriosis

Indexed keywords

BACTERIAL PROTEIN; INTERNALIN A; INTERNALIN B; LISTERIOLYSIN O; PROTEIN ACTA; UNCLASSIFIED DRUG; INLB PROTEIN, LISTERIA MONOCYTOGENES; INTERNALIN PROTEIN, BACTERIA; MEMBRANE PROTEIN;

ARTICLE; BACTERIAL MENINGITIS; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; BACTERIUM CONTAMINATION; BLOOD BRAIN BARRIER; CELL SPREADING; CELL VACUOLE; DISEASE MODEL; ENCEPHALITIS; EPIDEMIOLOGICAL DATA; FOOD CONTAMINATION; GOBLET CELL; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; INTESTINE; INTRAUTERINE INFECTION; LIFE CYCLE; LISTERIA MONOCYTOGENES; LISTERIOSIS; NONHUMAN; PERMEABILITY BARRIER; PLACENTA; PRIORITY JOURNAL; SEPTICEMIA; SPECIES DIFFERENCE; TRANSCYTOSIS; ANIMAL; ANIMAL MODEL; IN VITRO; IN VIVO; INTRACELLULAR SPACE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; REVIEW;

ANIMALIA; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

ANIMAL MODEL; IN VITRO; IN VIVO; LISTERIA MONOCYTOGENES; LISTERIOSIS;

ANIMALS; BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SPACE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMBRANE PROTEINS;

EID: 84889099506     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2013.09.012     Document Type: Article

References (67)

1. Lecuit M. Human listeriosis and animal models. Microbes Infect. 2007, 9:1216-1225.
2. Pamer E.G. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 2004, 4:812-823.
3. Mackaness G.B. Cellular resistance to infection. J. Exp. Med. 1962, 116:381-406.
4. Hamon M., Bierne H., Cossart P. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 2006, 4:423-434.
5. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P., Chakraborty T., Charbit A., Chetouani F., Couve E., de Daruvar A., Dehoux P., Domann E., Dominguez-Bernal G., Duchaud E., Durant L., Dussurget O., Entian K.D., Fsihi H., Garcia-del Portillo F., Garrido P., Gautier L., Goebel W., Gomez-Lopez N., Hain T., Hauf J., Jackson D., Jones L.M., Kaerst U., Kreft J., Kuhn M., Kunst F., Kurapkat G., Madueno E., Maitournam A., Vicente J.M., Ng E., Nedjari H., Nordsiek G., Novella S., de Pablos B., Perez-Diaz J.C., Purcell R., Remmel B., Rose M., Schlueter T., Simoes N., Tierrez A., Vazquez-Boland J.A., Voss H., Wehland J., Cossart P. Comparative genomics of Listeria species. Science 2001, 294:849-852.
6. Dussurget O., Cabanes D., Dehoux P., Lecuit M., Buchrieser C., Glaser P., Cossart P. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 2002, 45:1095-1106.
7. Cabanes D., Dussurget O., Dehoux P., Cossart P. Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol. Microbiol. 2004, 51:1601-1614.
8. 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. 2005, 24:2827-2838.
9. Bierne H., Cossart P. Listeria monocytogenes surface proteins: from genome predictions to function. Microbiol. Mol. Biol. Rev. 2007, 71:377-397.
10. Cossart P., Toledo-Arana A. Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 2008, 10:1041-1050.
11. 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. 2011, 14:118-127.
12. Johansson J., Mandin P., Renzoni A., Chiaruttini C., Springer M., Cossart P. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 2002, 110:551-561.
13. Loh E., Dussurget O., Gripenland J., Vaitkevicius K., Tiensuu T., Mandin P., Repoila F., Buchrieser C., Cossart P., Johansson J. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 2009, 139:770-779.
14. Pizarro-Cerda J., Kuhbacher A., Cossart P. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harbor Perspect. Med. 2012, 2.
15. Mengaud J., Ohayon H., Gounon P., Mege R.M., Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 1996, 84:923-932.
16. Lecuit M., Hurme R., Pizarro-Cerda J., Ohayon H., Geiger B., Cossart P. A role for alpha-and beta-catenins in bacterial uptake. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:10008-10013.
17. Sousa S., Cabanes D., Archambaud C., Colland F., Lemichez E., Popoff M., Boisson-Dupuis S., Gouin E., Lecuit M., Legrain P., Cossart P. ARHGAP10 is necessary for alpha-catenin recruitment at adherens junctions and for Listeria invasion. Nat. Cell Biol. 2005, 7:954-960.
18. Sousa S., Cabanes D., Bougneres L., Lecuit M., Sansonetti P., Tran-Van-Nhieu G., Cossart P. Src, cortactin and Arp2/3 complex are required for E-cadherin-mediated internalization of Listeria into cells. Cell. Microbiol. 2007, 9:2629-2643.
19. Sousa S., Cabanes D., El-Amraoui A., Petit C., Lecuit M., Cossart P. Unconventional myosin VIIa and vezatin, two proteins crucial for Listeria entry into epithelial cells. J. Cell Sci. 2004, 117:2121-2130.
20. 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. 2008, 10:2208-2222.
21. Shen Y., Naujokas M., Park M., Ireton K. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 2000, 103:501-510.
22. Braun L., Ghebrehiwet B., Cossart P. gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J. 2000, 19:1458-1466.
23. Veiga E., Cossart P. Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat. Cell Biol. 2005, 7:894-900.
24. Gaillard J.L., Berche P., Mounier J., Richard S., Sansonetti P. Invitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect. Immun. 1987, 55:2822-2829.
25. Schnupf P., Portnoy D.A. Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 2007, 9:1176-1187.
26. Beauregard K.E., Lee K.D., Collier R.J., Swanson J.A. pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J. Exp. Med. 1997, 186:1159-1163.
27. Glomski I.J., Gedde M.M., Tsang A.W., Swanson J.A., Portnoy D.A. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 2002, 156:1029-1038.
28. Singh R., Jamieson A., Cresswell P. GILT is a critical host factor for Listeria monocytogenes infection. Nature 2008, 455:1244-1247.
29. Smith G.A., Marquis H., Jones S., Johnston N.C., Portnoy D.A., Goldfine H. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect. Immun. 1995, 63:4231-4237.
30. Chico-Calero I., Suarez M., Gonzalez-Zorn B., Scortti M., Slaghuis J., Goebel W., Vazquez-Boland J.A. Hpt, a bacterial homolog of the microsomal glucose- 6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:431-436.
31. Tilney L.G., Portnoy D.A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 1989, 109:1597-1608.
32. 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 1992, 68:521-531.
33. Rajabian T., Gavicherla B., Heisig M., Muller-Altrock S., Goebel W., Gray-Owen S.D., Ireton K. The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat. Cell Biol. 2009, 11:1212-1218.
34. Gouin E., Adib-Conquy M., Balestrino D., Nahori M.A., Villiers V., Colland F., Dramsi S., Dussurget O., Cossart P. The Listeria monocytogenes InlC protein interferes with innate immune responses by targeting the I{kappa}B kinase subunit IKK{alpha}. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17333-17338.
35. Disson O., Nikitas G., Grayo S., Dussurget O., Cossart P., Lecuit M. Modeling human listeriosis in natural and genetically engineered animals. Nat. Protoc. 2009, 4:799-810.
36. Lecuit M., Dramsi S., Gottardi C., Fedor-Chaiken M., Gumbiner B., Cossart P. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 1999, 18:3956-3963.
37. Khelef N., Lecuit M., Bierne H., Cossart P. Species specificity of the Listeria monocytogenes InlB protein. Cell. Microbiol. 2006, 8:457-470.
38. Pirie J.H.H. A new disease of veld rodents, "Tiger river disease". Publ. S. Afr. Inst. Med. Res. 1927, 3:163-186.
39. Lecuit M., Vandormael-Pournin S., Lefort J., Huerre M., Gounon P., Dupuy C., Babinet C., Cossart P. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 2001, 292:1722-1725.
40. Disson O., Grayo S., Huillet E., Nikitas G., Langa-Vives F., Dussurget O., Ragon M., Le Monnier A., Babinet C., Cossart P., Lecuit M. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 2008, 455:1114-1118.
41. Jacquet C., Doumith M., Gordon J.I., Martin P.M., Cossart P., Lecuit M. A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J. Infect. Dis. 2004, 189:2094-2100.
42. Wollert T., Pasche B., Rochon M., Deppenmeier S., van den Heuvel J., Gruber A.D., Heinz D.W., Lengeling A., Schubert W.-D. Extending the host range of Listeria monocytogenes by rational protein design. Cell 2007, 129:891-902.
43. Chiba S., Nagai T., Hayashi T., Baba Y., Nagai S., Koyasu S. Listerial invasion protein internalin B promotes entry into ileal Peyer's patches invivo. Microbiol. Immunol. 2011, 55:123-129.
44. Pentecost M., Kumaran J., Ghosh P., Amieva M.R. Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog. 2010, 6:e1000900.
45. Pentecost M., Otto G., Theriot J.A., Amieva M.R. Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog. 2006, 2:e3.
46. Nikitas G., Deschamps C., Disson O., Niault T., Cossart P., Lecuit M. Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J. Exp. Med. 2011, 208:2263-2277.
47. Tilney L.G., DeRosier D.J., Tilney M.S. How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement. J. Cell Biol. 1992, 118:71-81.
48. 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. 2013, 9:e1003381.
49. Monk I.R., Casey P.G., Hill C., Gahan C.G.M. Directed evolution and targeted mutagenesis to murinize Listeria monocytogenes internalin A for enhanced infectivity in the murine oral infection model. BMC Microbiol. 2010, 10:318.
50. Bou Ghanem E.N., Jones G.S., Myers-Morales T., Patil P.D., Hidayatullah A.N., D'Orazio S.E. InlA promotes dissemination of Listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice. PLoS Pathog. 2012, 8:e1003015.
51. Bergmann S., Beard P.M., Pasche B., Lienenklaus S., Weiss S., Gahan C.G., Schughart K., Lengeling A. Influence of internalin a murinisation on host resistance to orally acquired listeriosis in mice. BMC Microbiol. 2013, 13:90.
52. Lecuit M., Sonnenburg J.L., Cossart P., Gordon J.I. Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model. J. Biol. Chem. 2007, 282:15065-15072.
53. Mylonakis E., Paliou M., Hohmann E.L., Calderwood S.B., Wing E.J. Listeriosis during pregnancy: a case series and review of 222 cases. Medicine 2002, 81:260-269.
54. Lecuit M., Nelson D.M., Smith S.D., Khun H., Huerre M., Vacher-Lavenu M.C., Gordon J.I., Cossart P. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6152-6157.
55. Bakardjiev A.I., Stacy B.A., Fisher S.J., Portnoy D.A. Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect. Immun. 2004, 72:489-497.
56. Le Monnier A., Autret N., Join-Lambert O.F., Jaubert F., Charbit A., Berche P., Kayal S. ActA is required for crossing of the fetoplacental barrier by Listeria monocytogenes. Infect. Immun. 2007, 75:950-957.
57. Gaillard J.L., Berche P., Sansonetti P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect. Immun. 1986, 52:50-55.
58. Portnoy D.A., Jacks P.S., Hinrichs D.J. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 1988, 167:1459-1471.
59. Hamon M.A., Ribet D., Stavru F., Cossart P. Listeriolysin O: the Swiss army knife of Listeria. Trends Microbiol. 2012, 20:360-368.
60. Levraud J.P., Disson O., Kissa K., Bonne I., Cossart P., Herbomel P., Lecuit M. Real-time observation of Listeria monocytogenes-phagocyte interactions in living zebrafish larvae. Infect. Immun. 2009, 77:3651-3660.
61. Carpentier B., Cerf O. Review - persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 2011, 145:1-8.
62. Freitag N.E., Port G.C., Miner M.D. Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat. Rev. Microbiol. 2009, 7:623-628.
63. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T., Vaitkevicius K., Barthelemy M., Vergassola M., Nahori M.-A., Soubigou G., Régnault B., Coppée J.-Y., Lecuit M., Johansson J., Cossart P. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459:950-956.
64. Chaturongakul S., Raengpradub S., Wiedmann M., Boor K.J. Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol. 2008, 16:388-396.
65. Travier L., Guadagnini S., Gouin E., Dufour A., Chenal-Francisque V., Cossart P., Olivo-Marin J.C., Ghigo J.M., Disson O., Lecuit M. ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. PLoS Pathog. 2013, 9:e1003131.
66. Ragon M., Wirth T., Hollandt F., Lavenir R., Lecuit M., Le Monnier A., Brisse S. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 2008, 4:e1000146.
67. Doran K.S., Banerjee A., Disson O., Lecuit M. Concepts and mechanisms: crossing host barriers. Cold Spring Harbor Perspect. Med. 2013, 3. a010090.