Candida albicans is able to use M cells as a portal of entry across the intestinal barrier in vitro

Cellular Microbiology

Volumn 18, Issue 2, 2016, Pages 195-210

  Albac, Sandrine ^a   Schmitz, Antonin ^a   Lopez Alayon, Carolina ^a   d'Enfert, Christophe ^b,c   Sautour, Marc ^a,d   Ducreux, Amandine ^a   Labruère Chazal, Catherine ^e   Laue, Michael ^f   Holland, Gudrun ^f   Bonnin, Alain ^a,d   Dalle, Frederic ^a,d  

^a UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^b INSTITUT PASTEUR   (France)

^c USC 2019   (France)

^d DIJON UNIVERSITY HOSPITAL   (France)

^e UNIVERSITÉ BOURGOGNE FRANCHE COMTÉ   (France)

^f ROBERT KOCH INSTITUTE   (Germany)

Author keywords

Adhesion; Endocytosis; Infection; Invasion; Mucosal immunity; Transcytosis

Indexed keywords

ALS3 PROTEIN; F ACTIN; INVASIN; SSA1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL ADHESION; CELL INVASION; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; FUNGUS MUTANT; IN VITRO STUDY; INTERNALIZATION; INTESTINE CELL; MICROFOLD CELL; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; B LYMPHOCYTE; CANDIDEMIA; CELL LINE; COCULTURE; EPITHELIUM CELL; GASTROINTESTINAL TRACT; HOST PATHOGEN INTERACTION; HUMAN; MICROBIOLOGY; PEYER PATCH; PHYSIOLOGY;

B-LYMPHOCYTES; CANDIDA ALBICANS; CANDIDEMIA; CELL ADHESION; CELL LINE; COCULTURE TECHNIQUES; ENDOCYTOSIS; EPITHELIAL CELLS; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; PEYER'S PATCHES;

EID: 84955204607     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12495     Document Type: Article

References (66)

1. Castro-Sanchez, P., and Martin-Villa, J.M. (2013) Gut immune system and oral tolerance. Br J Nutr 109 (Suppl 2): S3-S11.
2. Clark, M.A., Hirst, B.H., and Jepson, M.A. (1998) M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer's patch M cells. Infect Immun 66: 1237-1243.
3. Clark, M.A., and Jepson, M.A. (2003) Intestinal M cells and their role in bacterial infection. Int J Med Microbiol 293: 17-39.
4. Dalle, F., Jouault, T., Trinel, P.A., Esnault, J., Mallet, J.M., and d'Athis, P., et al. (2003) Beta-1, 2- and alpha-1, 2-linked oligomannosides mediate adherence of Candida albicans blastospores to human enterocytes in vitro. Infect Immun 71: 7061-7068.
5. Dalle, F., Wachtler, B., L'Ollivier, C., Holland, G., Bannert, N., and Wilson, D., et al. (2010) Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol 12: 248-271.
6. Daniels, J.J., Autenrieth, I.B., and Goebel, W. (2000) Interaction of Listeria monocytogenes with the intestinal epithelium. FEMS Microbiol Lett 190: 323-328.
7. Dennison, P.M., Ramsdale, M., Manson, C.L., and Brown, A.J. (2005) Gene disruption in Candida albicans using a synthetic, codon-optimised Cre-loxP system. Fungal Genet Biol 42: 737-748.
8. des Rieux, A., Fievez, V., Theate, I., Mast, J., Preat, V., and Schneider, Y.J. (2007) An improved in vitro model of human intestinal follicle-associated epithelium to study nanoparticle transport by M cells. Eur J Pharm Sci 30: 380-391.
9. Filler, S.G., and Sheppard, D.C. (2006). Fungal invasion of normally non-phagocytic host cells. PLoS Pathog 2: e129.
10. Gabor, F., Stangl, M., and Wirth, M. (1998) Lectin-mediated bioadhesion: binding characteristics of plant lectins on the enterocyte-like cell lines Caco-2, HT-29 and HCT-8. J Control Release 55: 131-142.
11. Gebert, A., Rothkotter, H.J., and Pabst, R. (1996) M cells in Peyer's patches of the intestine. Int Rev Cytol 167: 91-159.
12. Gillum, A.M., Tsay, E.Y., and Kirsch, D.R. (1984) Isolation of the Candida albicans gene for orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179-182.
13. Grubb, S.E., Murdoch, C., Sudbery, P.E., Saville, S.P., Lopez-Ribot, J.L., and Thornhill, M.H. (2008) Candida albicans-endothelial cell interactions: a key step in the pathogenesis of systemic candidiasis. Infect Immun 76: 4370-4377.
14. Gullberg, E. (2005) Particle transcytosis accross the human intestinal epithelium: model development and target identification for improved drug delivery. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Pharmacy 3, 62.
15. Gullberg, E., Leonard, M., Karlsson, J., Hopkins, A.M., Brayden, D., Baird, A.W., and Artursson, P. (2000) Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochem Biophys Res Commun 279: 808-813.
16. Hase, K., Kawano, K., Nochi, T., Pontes, G.S., Fukuda, S., Ebisawa, M., et al. (2009) Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 462: 226-230.
17. Hnisz, D., Tscherner, M., and Kuchler, K. (2011) Morphological and molecular genetic analysis of epigenetic switching of the human fungal pathogen Candida albicans. Methods Mol Biol 734: 303-315.
18. Hoschuetzky, H., Aberle, H., and Kemler, R. (1994) Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J Cell Biol 127: 1375-1380.
19. Kalischuk, L.D., Leggett, F., and Inglis, G.D. (2010) Campylobacter jejuni induces transcytosis of commensal bacteria across the intestinal epithelium through M-like cells. Gut Pathog 2: 14.
20. Kerneis, S., Bogdanova, A., Kraehenbuhl, J.P., and Pringault, E. (1997) Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277: 949-952.
21. Kim, S.H., Jung, D.I., Yang, I.Y., Kim, J., Lee, K.Y., Nochi, T., et al. (2011) M cells expressing the complement C5a receptor are efficient targets for mucosal vaccine delivery. Eur J Immunol 41: 3219-3229.
22. Kraehenbuhl, J.P., and Neutra, M.R. (2000) Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 16: 301-332.
23. Lamaze, C., Fujimoto, L.M., Yin, H.L., and Schmid, S.L. (1997) The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J Biol Chem 272: 20332-20335.
24. Lapthorne, S., Macsharry, J., Scully, P., Nally, K., and Shanahan, F. (2012) Differential intestinal M-cell gene expression response to gut commensals. Immunology 136: 312-324. doi: 10.1111/j.1365-2567.2012.03581.x.
25. Lefevre, M.E., Joel, D.D., and Schidlovsky, G. (1985) Retention of ingested latex particles in Peyer's patches of germfree and conventional mice. Proc Soc Exp Biol Med 179: 522-528.
26. Lelouard, H., Reggio, H., Roy, C., Sahuquet, A., Mangeat, P., and Montcourrier, P. (2001) Glycocalyx on rabbit intestinal M cells displays carbohydrate epitopes from Muc2. Infect Immun 69: 1061-1071.
27. Lim, J.S., Na, H.S., Lee, H.C., Choy, H.E., Park, S.C., Han, J.M., and Cho, K.A. (2009) Caveolae-mediated entry of Salmonella typhimurium in a human M-cell model. Biochem Biophys Res Commun 390: 1322-1327.
28. Macpherson, A.J., and Harris, N.L. (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4: 478-485.
29. Mantis, N.J., Frey, A., and Neutra, M.R. (2000) Accessibility of glycolipid and oligosaccharide epitopes on rabbit villus and follicle-associated epithelium. Am J Physiol Gastrointest Liver Physiol 278: G915-G923.
30. Maresca, M., Dumay, E., Fantini, J., and Caporiccio, B. (2007) Selective transport of staphylococcal enterotoxin A through in vitro generated human M cells. Microbes Infect 9: 1507-1510.
31. Martinez-Argudo, I., Sands, C., and Jepson, M.A. (2007) Translocation of enteropathogenic Escherichia coli across an in vitro M cell model is regulated by its type III secretion system. Cell Microbiol 9: 1538-1546.
32. Mavor, A.L., Thewes, S., and Hube, B. (2005) Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr Drug Targets 6: 863-874.
33. Naglik, J.R., Moyes, D.L., Wachtler, B., and Hube, B. (2011) Candida albicans interactions with epithelial cells and mucosal immunity. Microbes Infect 13: 963-976.
34. Neutra, M.R. (1999) M cells in antigen sampling in mucosal tissues. Curr Top Microbiol Immunol 236: 17-32.
35. Neutra, M.R., Frey, A., and Kraehenbuhl, J.P. (1996) Epithelial M cells: gateways for mucosal infection and immunization. Cell 86: 345-348.
36. Neutra, M.R., Phillips, T.L., Mayer, E.L., and Fishkind, D.J. (1987) Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer's patch. Cell Tissue Res 247: 537-546.
37. Nobile, C.J., Andes, D.R., Nett, J.E., Smith, F.J., Yue, F., Phan, Q.T., et al. (2006) Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2, e63.
38. Nucci, M., Anaissie, E. (2001) Revisiting the source of candidemia: skin or gut? Clin Infect Dis 33: 1659-1667. Epub 2001 Nov 8.
39. Owen, R.L. (1977) Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 72: 440-451.
40. Park, H., Myers, C.L., Sheppard, D.C., Phan, Q.T., Sanchez, A.A., Edwards, JE, Jr, and Filler, S.G. (2005) Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell Microbiol 7: 499-510.
41. Phan, Q.T., Myers, C.L., Fu, Y., Sheppard, D.C., Yeaman, M.R., Welch, W.H., et al. (2007) Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5, e64.
42. Pinto, M., Robine-Leon, S., Appay, M.D., Kedinger, M., Triadou, N., Dussaulx, E., et al. (1983) Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell 47: 323-330.
43. Porta, A., Ramon, A.M., and Fonzi, W.A. (1999) PRR1, a homolog of Aspergillus nidulans palF, controls pH-dependent gene expression and filamentation in Candida albicans. J Bacteriol 181: 7516-7523.
44. Reis, R.S., and Horn, F. (2010) Enteropathogenic Escherichia coli, Samonella, Shigella and Yersinia: cellular aspects of host-bacteria interactions in enteric diseases. Gut Pathog 2: 8.
45. Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., et al. (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2: 361-367.
46. Rochereau, N., Drocourt, D., Perouzel, E., Pavot, V., Redelinghuys, P., Brown, G.D., et al. (2013) Dectin-1 is essential for reverse transcytosis of glycosylated SIgA-antigen complexes by intestinal M cells. PLoS Biol 11, e1001658.
47. Sansonetti, P.J., Arondel, J., Cantey, J.R., Prevost, M.C., and Huerre, M. (1996) Infection of rabbit Peyer's patches by Shigella flexneri: effect of adhesive or invasive bacterial phenotypes on follicle-associated epithelium. Infect Immun 64: 2752-2764.
48. Schulte, R., Kerneis, S., Klinke, S., Bartels, H., Preger, S., Kraehenbuhl, J.P., et al. (2000) Translocation of Yersinia entrocolitica across reconstituted intestinal epithelial monolayers is triggered by Yersinia invasin binding to beta1 integrins apically expressed on M-like cells. Cell Microbiol 2: 173-185.
49. Siebers, A., and Finlay, B.B. (1996) M cells and the pathogenesis of mucosal and systemic infections. Trends Microbiol 4: 22-29.
50. Sohn, K., Senyurek, I., Fertey, J., Konigsdorfer, A., Joffroy, C., Hauser, N., et al. (2006) An in vitro assay to study the transcriptional response during adherence of Candida albicans to different human epithelia. FEMS Yeast Res 6: 1085-1093.
51. Sun, J.N., Solis, N.V., Phan, Q.T., Bajwa, J.S., Kashleva, H., Thompson, A., et al. (2010) Host cell invasion and virulence mediated by Candida albicans Ssa1. PLoS Pathog 6, e1001181.
52. Vautier, S., Drummond, R.A., Chen, K., Murray, G.I., Kadosh, D., Brown, A.J., et al. (2015) Candida albicans colonization and dissemination from the murine gastrointestinal tract: the influence of morphology and Th17 immunity. Cell Microbiol 17: 445-450.
53. Voss, A., Hollis, R.J., Pfaller, M.A., Wenzel, R.P., and Doebbeling, B.N. (1994) Investigation of the sequence of colonization and candidemia in nonneutropenic patients. J Clin Microbiol 32: 975-980.
54. Wächtler, B., Citiulo, F., Jablonowski, N., Forster, S., Dalle, F., Schaller, M., et al. (2012) Candida albicans-epithelial interactions: dissecting the roles of active penetration, induced endocytosis and host factors on the infection process. PLoS One 7, e36952.
55. Wächtler, B., Wilson, D., Haedicke, K., Dalle, F., and Hube, B. (2011) From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS One 6, e17046.
56. Walther, A., and Wendland, J. (2003) An improved transformation protocol for the human fungal pathogen Candida albicans. Curr Genet 42: 339-343.
57. Westphal, S., Lugering, A., von Wedel, J., von Eiff, C., Maaser, C., Spahn, T., et al. (2008) Resistance of chemokine receptor 6-deficient mice to Yersinia enterocolitica infection: evidence of defective M-cell formation in vivo. Am J Pathol 172: 671-680.
58. Wiesner, S.M., Bendel, C.M., Hess, D.J., Erlandsen, S.L., and Wells, C.L. (2002) Adherence of yeast and filamentous forms of Candida albicans to cultured enterocytes. Crit Care Med 30: 677-683.
59. Wilson, R.B., Davis, D., and Mitchell, A.P. (1999) Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J Bacteriol 181: 1868-1874.
60. Wong, N.A., Herriot, M., and Rae, F. (2003) An immunohistochemical study and review of potential markers of human intestinal M cells. Eur J Histochem 47: 143-150.
61. Zakikhany, K., Naglik, J.R., Schmidt-Westhausen, A., Holland, G., Schaller, M., and Hube, B. (2007) In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell Microbiol 9: 2938-2954.
62. Zhao, X., Oh, S.H., Cheng, G., Green, C.B., Nuessen, J.A., Yeater, K., et al. (2004) ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 150: 2415-2428.
63. Zheng, X., and Wang, Y. (2004) Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J 23: 1845-1856.
64. Zhu, W., and Filler, S.G. (2009) Interactions of Candida albicans with epithelial cells. Cell Microbiol 12: 273-282.
65. Zhu, W., Phan, Q.T., Boontheung, P., Solis, N.V., Loo, J.A., and Filler, S.G. (2012) EGFR and HER2 receptor kinase signaling mediate epithelial cell invasion by Candida albicans during oropharyngeal infection. Proc Natl Acad Sci U S A 109: 14194-14199.
66. Zink, S., Nass, T., Rosen, P., and Ernst, J.F. (1996) Migration of the fungal pathogen Candida albicans across endothelial monolayers. Infect Immun 64: 5085-5091.