A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of candida albicans in epithelial cells

Cell Host and Microbe

Volumn 8, Issue 3, 2010, Pages 225-235

  Moyes, David L ^a   Runglall, Manohursingh ^a   Murciano, Celia ^a   Shen, Chengguo ^a   Nayar, Deepa ^a   Thavaraj, Selvam ^a   Kohli, Arinder ^a   Islam, Ayesha ^a   Mora Montes, Hector ^b   Challacombe, Stephen J ^a   Naglik, Julian R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PROTEIN C FOS; PROTEIN C JUN; RNA; SYNAPTOTAGMIN I;

ARTICLE; CANDIDA ALBICANS; COMMENSAL; DNA BINDING; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FUNGAL STRAIN; FUNGUS HYPHAE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MORPHOLOGY; MOUTH FLORA; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RNA EXTRACTION; RNA INTERFERENCE; YEAST;

CANDIDA ALBICANS; CANDIDIASIS, ORAL; CELL LINE, TUMOR; CELL WALL; CYTOKINES; DUAL SPECIFICITY PHOSPHATASE 1; EPITHELIAL CELLS; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYPHAE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; MOUTH MUCOSA; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-FOS; SIGNAL TRANSDUCTION; VIRULENCE; YEASTS;

CANDIDA ALBICANS;

EID: 77956583415     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2010.08.002     Document Type: Article

References (42)

1. M.T. Abreu, M. Fukata, and M. Arditi TLR signaling in the gut in health and disease J. Immunol. 174 2005 4453 4460
2. S. Agrawal, A. Agrawal, B. Doughty, A. Gerwitz, J. Blenis, T. Van Dyke, and B. Pulendran Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos J. Immunol. 171 2003 4984 4989
3. B.R. Braun, and A.D. Johnson Control of filament formation in Candida albicans by the transcriptional repressor TUP1 Science 277 1997 105 109
4. J.M. Brondello, J. Pouysségur, and F.R. McKenzie Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation Science 286 1999 2514 2517
5. A. Chambellan, R. Leahy, W. Xu, P.J. Cruickshank, A. Janocha, K. Szabo, S.B. Cannady, S.A. Comhair, and S.C. Erzurum Pivotal role of c-Fos in nitric oxide synthase 2 expression in airway epithelial cells Nitric Oxide 20 2009 143 149
6. H. Chi, and R.A. Flavell Acetylation of MKP-1 and the control of inflammation Sci. Signal. 1 2008 e44
7. S. Dillon, A. Agrawal, T. Van Dyke, G. Landreth, L. McCauley, A. Koh, C. Maliszewski, S. Akira, and B. Pulendran A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells J. Immunol. 172 2004 4733 4743
8. S. Dillon, S. Agrawal, K. Banerjee, J. Letterio, T.L. Denning, K. Oswald-Richter, D.J. Kasprowicz, K. Kellar, J. Pare, and T. van Dyke Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance J. Clin. Invest. 116 2006 916 928
9. A.M. Gillum, E.Y. Tsay, and D.R. Kirsch 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 1984 179 182
10. N.A.R. Gow, G.W. Gooday, R.J. Newsam, and K. Gull Ultrastructure of the septum in Candida albicans Curr. Microbiol. 4 1980 357 359
11. A.D. Kennedy, J.A. Willment, D.W. Dorward, D.L. Williams, G.D. Brown, and F.R. DeLeo Dectin-1 promotes fungicidal activity of human neutrophils Eur. J. Immunol. 37 2007 467 478
12. C.M. Kinney, U.M. Chandrasekharan, L. Mavrakis, and P.E. DiCorleto VEGF and thrombin induce MKP-1 through distinct signaling pathways: role for MKP-1 in endothelial cell migration Am. J. Physiol. Cell Physiol. 294 2008 C241 C250
13. H.C. Korting, B. Hube, S. Oberbauer, E. Januschke, G. Hamm, A. Albrecht, C. Borelli, and M. Schaller Reduced expression of the hyphal-independent Candida albicans proteinase genes SAP1 and SAP3 in the efg1 mutant is associated with attenuated virulence during infection of oral epithelium J. Med. Microbiol. 52 2003 623 632
14. Y. Kumagai, O. Takeuchi, and S. Akira Pathogen recognition by innate receptors J. Infect. Chemother. 14 2008 86 92
15. M.S. Lee, and Y.J. Kim Signaling pathways downstream of pattern-recognition receptors and their cross talk Annu. Rev. Biochem. 76 2007 447 480
16. L. Li, and A. Dongari-Bagtzoglou Epithelial GM-CSF induction by Candida glabrata J. Dent. Res. 88 2009 746 751
17. Y. Liu, E.G. Shepherd, and L.D. Nelin MAPK phosphatases - regulating the immune response Nat. Rev. Immunol. 7 2007 202 212
18. H.J. Lo, J.R. Köhler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G.R. Fink Nonfilamentous C. albicans mutants are avirulent Cell 90 1997 939 949
19. R. Medzhitov Recognition of microorganisms and activation of the immune response Nature 449 2007 819 826
20. H.M. Mora-Montes, S. Bates, M.G. Netea, D.F. Díaz-Jiménez, E. López-Romero, S. Zinker, P. Ponce-Noyola, B.J. Kullberg, A.J. Brown, and F.C. Odds Endoplasmic reticulum alpha-glycosidases of Candida albicans are required for N glycosylation, cell wall integrity, and normal host-fungus interaction Eukaryot. Cell 6 2007 2184 2193
21. A.M. Murad, C. d'Enfert, C. Gaillardin, H. Tournu, F. Tekaia, D. Talibi, D. Marechal, V. Marchais, J. Cottin, and A.J. Brown Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1 Mol. Microbiol. 42 2001 981 993
22. A.M. Murad, P. Leng, M. Straffon, J. Wishart, S. Macaskill, D. MacCallum, N. Schnell, D. Talibi, D. Marechal, and F. Tekaia NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans EMBO J. 20 2001 4742 4752
23. J.R. Naglik, G. Newport, T.C. White, L.L. Fernandes-Naglik, J.S. Greenspan, D. Greenspan, S.P. Sweet, S.J. Challacombe, and N. Agabian In vivo analysis of secreted aspartyl proteinase expression in human oral candidiasis Infect. Immun. 67 1999 2482 2490
24. J.R. Naglik, C.A. Rodgers, P.J. Shirlaw, J.L. Dobbie, L.L. Fernandes-Naglik, D. Greenspan, N. Agabian, and S.J. Challacombe Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections J. Infect. Dis. 188 2003 469 479
25. J.R. Naglik, F. Fostira, J. Ruprai, J.F. Staab, S.J. Challacombe, and P. Sundstrom Candida albicans HWP1 gene expression and host antibody responses in colonization and disease J. Med. Microbiol. 55 2006 1323 1327
26. J.R. Naglik, D. Moyes, J. Makwana, P. Kanzaria, E. Tsichlaki, G. Weindl, A.R. Tappuni, C.A. Rodgers, A.J. Woodman, and S.J. Challacombe Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis Microbiology 154 2008 3266 3280
27. M.G. Netea, N.A. Gow, C.A. Munro, S. Bates, C. Collins, G. Ferwerda, R.P. Hobson, G. Bertram, H.B. Hughes, and T. Jansen Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors J. Clin. Invest. 116 2006 1642 1650
28. M.G. Netea, G.D. Brown, B.J. Kullberg, and N.A.R. Gow An integrated model of the recognition of Candida albicans by the innate immune system Nat. Rev. Microbiol. 6 2008 67 78
29. C.J. Nobile, N. Solis, C.L. Myers, A.J. Fay, J.S. Deneault, A. Nantel, A.P. Mitchell, and S.G. Filler Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions Cell. Microbiol. 10 2008 2180 2196
30. F.C. Odds Candida and Candidosis 1988 Bailliere Tindall Philadelphia
31. B. Opitz, A. Püschel, W. Beermann, A.C. Hocke, S. Förster, B. Schmeck, V. van Laak, T. Chakraborty, N. Suttorp, and S. Hippenstiel Listeria monocytogenes activated p38 MAPK and induced IL-8 secretion in a nucleotide-binding oligomerization domain 1-dependent manner in endothelial cells J. Immunol. 176 2006 484 490
32. A. Plaine, L. Walker, G. Da Costa, H.M. Mora-Montes, A. McKinnon, N.A.R. Gow, C. Gaillardin, C.A. Munro, and M.L. Richard Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity Fungal Genet. Biol. 45 2008 1404 1414
33. D. Rahman, M. Mistry, S. Thavaraj, S.J. Challacombe, and J.R. Naglik Murine model of concurrent oral and vaginal Candida albicans colonization to study epithelial host-pathogen interactions Microbes Infect. 9 2007 615 622
34. A. Roeder, C.J. Kirschning, M. Schaller, G. Weindl, H. Wagner, H.C. Korting, and R.A. Rupec Induction of nuclear factor- kappa B and c-Jun/activator protein-1 via toll-like receptor 2 in macrophages by antimycotic-treated Candida albicans J. Infect. Dis. 190 2004 1318 1326
35. M. Schaller, K. Zakikhany, J.R. Naglik, G. Weindl, and B. Hube Models of oral and vaginal candidiasis based on in vitro reconstituted human epithelia Nat. Protoc. 1 2006 2767 2773
36. A.J. Shaywitz, and M.E. Greenberg CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals Annu. Rev. Biochem. 68 1999 821 861
37. X. Wang, and B. Seed A PCR primer bank for quantitative gene expression analysis Nucleic Acids Res. 31 2003 e154
38. X. Wang, and Y. Liu Regulation of innate immune response by MAP kinase phosphatase-1 Cell. Signal. 19 2007 1372 1382
39. G. Weindl, J.R. Naglik, S. Kaesler, T. Biedermann, B. Hube, H.C. Korting, and M. Schaller Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling J. Clin. Invest. 117 2007 3664 3672
40. R. Wisdom AP-1: one switch for many signals Exp. Cell Res. 253 1999 180 185
41. K. Zakikhany, J.R. Naglik, A. Schmidt-Westhausen, G. Holland, M. Schaller, and B. Hube In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination Cell. Microbiol. 9 2007 2938 2954
42. Q. Zhao, X. Wang, L.D. Nelin, Y. Yao, R. Matta, M.E. Manson, R.S. Baliga, X. Meng, C.V. Smith, and J.A. Bauer MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock J. Exp. Med. 203 2006 131 140