PI3-kinase activation is critical for host barrier permissiveness to Listeria monocytogenes

Journal of Experimental Medicine

Volumn 212, Issue 2, 2015, Pages 165-183

  Gessain, Grégoire ^a,b,c   Tsai, Yu Huan ^a,b,c   Travier, Laetitia ^a,b   Bonazzi, Matteo ^a,b,d,f   Grayo, Solène ^a,b   Cossart, Pascale ^a,b,d   Charlier, Caroline ^a,b,c,e   Disson, Olivier ^a,b,f   Lecuit, Marc ^a,b,c,e  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d CEMAGREF   (France)

^e WORLD HEALTH ORGANIZATION   (Switzerland)

^f CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; SCATTER FACTOR RECEPTOR; UVOMORULIN; BACTERIAL PROTEIN; CADHERIN; PROTEIN BINDING; PROTEIN KINASE B;

ARTICLE; BLOOD PLACENTA BARRIER; CELL INVASION; COLONY FORMING UNIT; CONFOCAL MICROSCOPY; ENZYME ACTIVATION; ENZYME ACTIVITY; HOST; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTESTINE CELL; LISTERIA MONOCYTOGENES; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RNA ISOLATION; SIGNAL TRANSDUCTION; TARGET CELL; TROPHOBLAST; WESTERN BLOTTING; WHOLE CELL; ANIMAL; CELL LINE; CHORION VILLUS; FEMALE; GOBLET CELL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE; INTESTINE MUCOSA; LISTERIOSIS; METABOLISM; MICROBIOLOGY; MOUSE; PEYER PATCH; PHOSPHORYLATION; PLACENTA; PREGNANCY; TRANSGENIC MOUSE;

ANIMALS; BACTERIAL PROTEINS; CADHERINS; CELL LINE; CHORIONIC VILLI; ENZYME ACTIVATION; FEMALE; GOBLET CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINAL MUCOSA; INTESTINES; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, TRANSGENIC; PEYER'S PATCHES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PLACENTA; PREGNANCY; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TROPHOBLASTS;

EID: 84922729111     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20141406     Document Type: Article

References (59)

1. Bécavin, C., C. Bouchier, P. Lechat, C. Archambaud, S. Creno, E. Gouin, Z. Wu, A. Kühbacher, S. Brisse, M.G. Pucciarelli, et al. 2014. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying differences in pathogenicity. MBio. 5:e00969-e14. http://dx.doi.org/10.1128/mBio.00969-14
2. Biggs, W.H. III, J. Meisenhelder, T. Hunter, W.K. Cavenee, and K.C. Arden. 1999. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. USA. 96:7421-7426. http://dx.doi.org/10.1073/pnas.96.13.7421
3. Braun, L., B. Ghebrehiwet, and P. Cossart. 2000. gC1q-R/p32, a C1qbinding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J. 19:1458-1466. http://dx.doi.org/10.1093/ emboj/19.7.1458
4. Bucior, I., J.F. Pielage, and J.N. Engel. 2012. Pseudomonas aeruginosa pili and flagella mediate distinct binding and signaling events at the apical and basolateral surface of airway epithelium. PLoS Pathog. 8:e1002616. http://dx.doi.org/10.1371/journal.ppat.1002616
5. Chiba, S., T. Nagai, T. Hayashi, Y. Baba, S. Nagai, and S. Koyasu. 2011. Listerial invasion protein internalin B promotes entry into ileal Peyer's patches in vivo. Microbiol. Immunol. 55:123-129. http://dx.doi.org/10.1111/j.1348-0421.2010.00292.x
6. Cossart, P., J. Pizarro-Cerdá, and M. Lecuit. 2003. Invasion of mammalian cells by Listeria monocytogenes: functional mimicry to subvert cellular functions. Trends Cell Biol. 13:23-31. http://dx.doi.org/10.1016/ S0962-8924(02)00006-5
7. Cummings, H.E., J. Barbi, P. Reville, S. Oghumu, N. Zorko, A. Sarkar, T.L. Keiser, B. Lu, T. Rückle, S. Varikuti, et al. 2012. Critical role for phosphoinositide 3-kinase gamma in parasite invasion and disease progression of cutaneous leishmaniasis. Proc. Natl. Acad. Sci. USA. 109:1251-1256. http://dx.doi.org/10.1073/pnas.1110339109
8. Disson, O., and M. Lecuit. 2013. In vitro and in vivo models to study human listeriosis: mind the gap. Microbes Infect. 15:971-980. http://dx.doi.org/ 10.1016/j.micinf.2013.09.012
9. Disson, O., S. Grayo, E. Huillet, G. Nikitas, F. Langa-Vives, O. Dussurget, M. Ragon, A. Le Monnier, C. Babinet, P. Cossart, and M. Lecuit. 2008. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature. 455:1114-1118. http://dx.doi.org/10.1038/ nature07303
10. Disson, O., G. Nikitas, S. Grayo, O. Dussurget, P. Cossart, and M. Lecuit. Modeling human listeriosis in natural and genetically engineered animals. Nat. Protoc. 4:799-810. http://dx.doi.org/10.1038/nprot.2009.66
11. Doran, K.S., A. Banerjee, O. Disson, and M. Lecuit. 2013. Concepts and mechanisms: crossing host barriers. Cold Spring Harb Perspect Med. 3:1. http://dx.doi.org/10.1101/cshperspect.a010090
12. Dramsi, S., I. Biswas, E. Maguin, L. Braun, P. Mastroeni, and P. Cossart. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol. Microbiol. 16:251-261. http://dx.doi.org/10.1111/j.1365-2958.1995. tb02297.x
13. Dramsi, S., S. Lévi, A. Triller, and P. Cossart. 1998. Entry of Listeria monocytogenes into neurons occurs by cell-to-cell spread: an in vitro study. Infect. Immun. 66:4461-4468.
14. Durual, S., C. Blanchard, M. Estienne, M.F. Jacquier, J.C. Cuber, V. Perrot, C. Laboisse, and J.C. Cuber. 2005. Expression of human TFF3 in relation to growth of HT-29 cell subpopulations: involvement of PI3-K but not STAT6. Differentiation. 73:36-44. http://dx.doi.org/10.1111/ j.1432-0436.2005.07301006.x
15. Engelman, J.A., J. Luo, and L.C. Cantley. 2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7:606-619. http://dx.doi.org/10.1038/nrg1879
16. Gaillard, J.L., P. Berche, C. Frehel, E. Gouin, and P. Cossart. 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. http://dx.doi.org/10.1016/0092-8674(91)90009-N
17. Girard, D., A. Leclercq, E. Laurent, M. Lecuit, H. de Valk, and V. Goulet. Pregnancy-related listeriosis in France, 1984 to 2011, with a focus on 606 cases from 1999 to 2011. Euro Surveill. 19:19.
18. Guo, J.P., D. Coppola, and J.Q. Cheng. 2011. IKBKE protein activates Akt independent of phosphatidylinositol 3-kinase/PDK1/mTORC2 and the pleckstrin homology domain to sustain malignant transformation. J. Biol. Chem. 286:37389-37398. http://dx.doi.org/10.1074/jbc.M111.287433
19. Hull, B.E., and L.A. Staehelin. 1976. Functional significance of the variations in the geometrical organization of tight junction networks. J. Cell Biol. 68:688-704. http://dx.doi.org/10.1083/jcb.68.3.688
20. Ireton, K., B. Payrastre, H. Chap, W. Ogawa, H. Sakaue, M. Kasuga, and P. Cossart. 1996. A role for phosphoinositide 3-kinase in bacterial invasion. Science. 274:780-782. http://dx.doi.org/10.1126/science.274.5288.780
21. Ireton, K., B. Payrastre, and P. Cossart. 1999. The Listeria monocytogenes protein InlB is an agonist of mammalian phosphoinositide 3-kinase. J. Biol. Chem. 274:17025-17032. http://dx.doi.org/10.1074/jbc.274.24.17025
22. Jacquet, C., M. Doumith, J.I. Gordon, P.M. Martin, P. Cossart, and M. Lecuit. 2004. A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J. Infect. Dis. 189:2094-2100. http://dx.doi.org/10.1086/420853
23. Jang, M.H., M.N. Kweon, K. Iwatani, M. Yamamoto, K. Terahara, C. Sasakawa, T. Suzuki, T. Nochi, Y. Yokota, P.D. Rennert, et al. 2004. Intestinal villous M cells: an antigen entry site in the mucosal epithelium. Proc. Natl. Acad. Sci. USA. 101:6110-6115. http://dx.doi.org/10.1073/ pnas.0400969101
24. Jiwani, S., Y. Wang, G.C. Dowd, A. Gianfelice, P. Pichestapong, B. Gavicherla, N. Vanbennekom, and K. Ireton. 2012. Identification of components of the host type IA phosphoinositide 3-kinase pathway that promote internalization of Listeria monocytogenes. Infect. Immun. 80:1252-1266. http://dx.doi.org/10.1128/IAI.06082-11
25. Jonquières, R., J. Pizarro-Cerdá, and P. Cossart. 2001. Synergy between the N- and C-terminal domains of InlB for efficient invasion of nonphagocytic cells by Listeria monocytogenes. Mol. Microbiol. 42:955-965. http://dx.doi.org/10.1046/j.1365-2958.2001.02704.x
26. Khelef, N., M. Lecuit, H. Bierne, and P. Cossart. 2006. Species specificity of the Listeria monocytogenes InlB protein. Cell. Microbiol. 8:457-470. http://dx.doi.org/10.1111/j.1462-5822.2005.00634.x
27. Kölsch, V., T. Seher, G.J. Fernandez-Ballester, L. Serrano, and M. Leptin. Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science. 315:384-386. http://dx.doi.org/10.1126/science.1134833
28. Kourtis, A.P., J.S. Read, and D.J. Jamieson. 2014. Pregnancy and infection. N. Engl. J. Med. 370:2211-2218. http://dx.doi.org/10.1056/NEJMra1213566
29. Lecuit, M. 2007. Human listeriosis and animal models. Microbes Infect. 9:1216-1225. http://dx.doi.org/10.1016/j.micinf.2007.05.009
30. Lecuit, M., H. Ohayon, L. Braun, J. Mengaud, and P. Cossart. 1997. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect. Immun. 65:5309-5319.
31. Lecuit, M., S. Dramsi, C. Gottardi, M. Fedor-Chaiken, B. Gumbiner, and P. Cossart. 1999. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18:3956-3963. http://dx.doi.org/10.1093/emboj/18.14.3956
32. Lecuit, M., S. Vandormael-Pournin, J. Lefort, M. Huerre, P. Gounon, C. Dupuy, C. Babinet, and P. Cossart. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science. 292:1722-1725. http://dx.doi.org/10.1126/science.1059852
33. Lecuit, M., D.M. Nelson, S.D. Smith, H. Khun, M. Huerre, M.C. Vacher- Lavenu, J.I. Gordon, and P. Cossart. 2004. 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. http://dx.doi.org/10.1073/pnas.0401434101
34. Madara, J.L., and J.S. Trier. 1982. Structure and permeability of goblet cell tight junctions in rat small intestine. J. Membr. Biol. 66:145-157. http:// dx.doi.org/10.1007/BF01868490
35. Madara, J.L., J.S. Trier, and M.R. Neutra. 1980. Structural changes in the plasma membrane accompanying differentiation of epithelial cells in human and monkey small intestine. Gastroenterology. 78:963-975.
36. Maehama, T., and J.E. Dixon. 1998. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5- trisphosphate. J. Biol. Chem. 273:13375-13378. http://dx.doi.org/10.1074/jbc.273.22.13375
37. Mahajan, K., and N.P. Mahajan. 2012. PI3K-independent AKT activation in cancers: a treasure trove for novel therapeutics. J. Cell. Physiol. 227:3178-3184. http://dx.doi.org/10.1002/jcp.24065
38. Marchiando, A.M., L. Shen, W.V. Graham, K.L. Edelblum, C.A. Duckworth, Y. Guan, M.H. Montrose, J.R. Turner, and A.J. Watson. The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology. 140:1208-1218. http://dx.doi.org/10.1053/j.gastro.2011.01.004
39. McDole, J.R., L.W. Wheeler, K.G. McDonald, B. Wang, V. Konjufca, K.A. Knoop, R.D. Newberry, and M.J. Miller. 2012. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature. 483:345-349. http://dx.doi.org/10.1038/nature10863
40. McGuckin, M.A., S.K. Lindén, P. Sutton, and T.H. Florin. 2011. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9:265-278. http:// dx.doi.org/10.1038/nrmicro2538
41. Mengaud, J., H. Ohayon, P. Gounon, P. Cossart, and P. CossartMege R-M. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell. 84:923-932. http://dx.doi.org/10.1016/S0092-8674(00)81070-3
42. Neutra, M.R., A. Frey, and J.P. Kraehenbuhl. 1996. Epithelial M cells: gateways for mucosal infection and immunization. Cell. 86:345-348. http://dx.doi.org/10.1016/S0092-8674(00)80106-3
43. Nikitas, G., C. Deschamps, O. Disson, T. Niault, P. Cossart, and M. Lecuit. 2011. Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J. Exp. Med. 208:2263-2277. http://dx.doi.org/10.1084/jem.20110560
44. Pattillo, R.A., G.O. Gey, E. Delfs, W.Y. Huang, L. Hause, D.J. Garancis, M. Knoth, J. Amatruda, J. Bertino, H.G. Friesen, and R.F. Mattingly. The hormone-synthesizing trophoblastic cell in vitro: a model for cancer research and placental hormone synthesis. Ann. N. Y. Acad. Sci. 172(10 Physiology a):288-298. http://dx.doi.org/10.1111/j.1749-6632.1971.tb34942.x
45. Pentecost, M., J. Kumaran, P. Ghosh, and M.R. Amieva. 2010. Listeria monocytogenes internalin B activates junctional endocytosis to accelerate intestinal invasion. PLoS Pathog. 6:e1000900. http://dx.doi.org/10.1371/journal.ppat.1000900
46. Perez, T.D., M. Tamada, M.P. Sheetz, and W.J. Nelson. 2008. Immediateearly signaling induced by E-cadherin engagement and adhesion. J. Biol. Chem. 283:5014-5022. http://dx.doi.org/10.1074/jbc.M705209200
47. Phan, Q.T., C.L. Myers, Y. Fu, D.C. Sheppard, M.R. Yeaman, W.H. Welch, A.S. Ibrahim, J.E. Edwards Jr., and S.G. Filler. 2007. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5:e64. http://dx.doi.org/10.1371/journal. pbio.0050064
48. Porvaznik, M., W. Baker, and R.I. Walker. 1983. Disruption of the goblet cell intercellular junction following histamine infusion of the rabbit ileum. Experientia. 39:514-518. http://dx.doi.org/10.1007/BF01965183
49. Robbins, J.R., and A.I. Bakardjiev. 2012. Pathogens and the placental fortress. Curr. Opin. Microbiol. 15:36-43. http://dx.doi.org/10.1016/j.mib.2011.11.006
50. Robbins, J.R., K.M. Skrzypczynska, V.B. Zeldovich, M. Kapidzic, and A.I. Bakardjiev. 2010. Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes. PLoS Pathog. 6:e1000732. http://dx.doi.org/10.1371/journal.ppat.1000732
51. Saeed, M.F., A.A. Kolokoltsov, A.N. Freiberg, M.R. Holbrook, and R.A. Davey. 2008. Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog. 4:e1000141. http://dx.doi.org/10.1371/journal.ppat.1000141
52. Shen, Y., M. Naujokas, M. Park, and K. Ireton. 2000. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell. 103:501-510. http://dx.doi.org/10.1016/S0092-8674(00)00141-0
53. Swaminathan, B., and P. Gerner-Smidt. 2007. The epidemiology of human listeriosis. Microbes Infect. 9:1236-1243. http://dx.doi.org/10.1016/j.micinf.2007.05.011
54. Tom, B.H., L.P. Rutzky, M.M. Jakstys, R. Oyasu, C.I. Kaye, and B.D. Kahan. 1976. Human colonic adenocarcinoma cells. I. Establishment and description of a new line. In Vitro. 12:180-191. http://dx.doi.org/ 10.1007/BF02796440
55. Tsai, Y.H., O. Disson, H. Bierne, and M. Lecuit. 2013. Murinization of internalin extends its receptor repertoire, altering Listeria monocytogenes cell tropism and host responses. PLoS Pathog. 9:e1003381. http://dx.doi.org/10.1371/journal.ppat.1003381
56. Vanhaesebroeck, B., L. Stephens, and P. Hawkins. 2012. PI3K signalling: the path to discovery and understanding. Nat. Rev. Mol. Cell Biol. 13:195-203. http://dx.doi.org/10.1038/nrm3290
57. Wang, M.L., S.A. Keilbaugh, T. Cash-Mason, X.C. He, L. Li, and G.D. Wu. 2008. Immune-mediated signaling in intestinal goblet cells via PI3-kinase- and AKT-dependent pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 295:G1122-G1130. http://dx.doi.org/10.1152/ajpgi.90430.2008
58. Wollert, T., B. Pasche, M. Rochon, S. Deppenmeier, J. van den Heuvel, A.D. Gruber, D.W. Heinz, A. Lengeling, and W.-D. Schubert. 2007. Extending the host range of Listeria monocytogenes by rational protein design. Cell. 129:891-902. http://dx.doi.org/10.1016/j.cell.2007.03.049
59. Yusta, B., D. Holland, J.A. Koehler, M. Maziarz, J.L. Estall, R. Higgins, and D.J. Drucker. 2009. ErbB signaling is required for the proliferative actions of GLP-2 in the murine gut. Gastroenterology. 137:986-996. http://dx.doi.org/10.1053/j.gastro.2009.05.057