Iron-responsive chromatin remodelling and MAPK signalling enhance adhesion in Candida albicans

Molecular Microbiology

Volumn 93, Issue 2, 2014, Pages 291-305

  Puri, Sumant ^a   Lai, William K M ^b   Rizzo, Jason M ^b   Buck, Michael J ^b   Edgerton, Mira ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEK1 PROTEIN; IRON; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CPH1; UNCLASSIFIED DRUG; FUNGAL PROTEIN; MICROCOCCAL NUCLEASE;

ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL ADHESION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; FUNGAL GENE; GENE EXPRESSION; GENE REPRESSION; IRON BALANCE; IRON TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; HOMEOSTASIS; METABOLISM; MULTIGENE FAMILY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CANDIDA ALBICANS; FUNGI;

BIOFILMS; CANDIDA ALBICANS; CELL ADHESION; CHROMATIN ASSEMBLY AND DISASSEMBLY; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMEOSTASIS; IRON; MAP KINASE SIGNALING SYSTEM; MICROCOCCAL NUCLEASE; MULTIGENE FAMILY; PHOSPHORYLATION; TRANSCRIPTION FACTORS;

EID: 84904036446     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12659     Document Type: Article

References (49)

1. Bastidas, R.J., Heitman, J., and Cardenas, M.E. (2009) The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog 5: e1000294.
2. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Met 57: 289-300.
3. Braun, B.R., and Johnson, A.D. (1997) Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277: 105-109.
4. Buck, M.J., and Lieb, J.D. (2006) A chromatin-mediated mechanism for specification of conditional transcription factor targets. Nat Genet 38: 1446-1451.
5. Cantero, P.D., and Ernst, J.F. (2011) Damage to the glycoshield activates PMT-directed O-mannosylation via the Msb2-Cek1 pathway in Candida albicans. Mol Microbiol 80: 715-725.
6. Chen, C., Pande, K., French, S.D., Tuch, B.B., and Noble, S.M. (2011) An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe 10: 118-135.
7. Csank, C., Makris, C., Meloche, S., Schroppel, K., Rollinghoff, M., Dignard, D., etal. (1997) Derepressed hyphal growth and reduced virulence in a VH1 family-related protein phosphatase mutant of the human pathogen Candida albicans. Mol Biol Cell 8: 2539-2551.
8. Dieterich, C., Schandar, M., Noll, M., Johannes, F.J., Brunner, H., Graeve, T., and Rupp, S. (2002) In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148: 497-506.
9. Finkel, J.S., Xu, W., Huang, D., Hill, E.M., Desai, J.V., Woolford, C.A., etal. (2012) Portrait of Candida albicans adherence regulators. PLoS Pathog 8: e1002525.
10. Galan-Diez, M., Arana, D.M., Serrano-Gomez, D., Kremer, L., Casasnovas, J.M., Ortega, M., etal. (2010) Candida albicans beta-glucan exposure is controlled by the fungal CEK1-mediated mitogen-activated protein kinase pathway that modulates immune responses triggered through dectin-1. Infect Immun 78: 1426-1436.
11. Garhammer, P., Hiller, K.A., Reitinger, T., and Schmalz, G. (2004) Metal content of saliva of patients with and without metal restorations. Clin Oral Investig 8: 238-242.
12. Gelis, S., de Groot, P.W., Castillo, L., Moragues, M.D., Sentandreu, R., Gomez, M.M., and Valentin, E. (2012) Pga13 in Candida albicans is localized in the cell wall and influences cell surface properties, morphogenesis and virulence. Fungal Genet Biol 49: 322-331.
13. de Groot, P.W., Hellingwerf, K.J., and Klis, F.M. (2003) Genome-wide identification of fungal GPI proteins. Yeast 20: 781-796.
14. de Groot, P.W., Bader, O., de Boer, A.D., Weig, M., and Chauhan, N. (2013) Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot Cell 12: 470-481.
15. Hameed, S., Prasad, T., Banerjee, D., Chandra, A., Mukhopadhyay, C.K., Goswami, S.K., etal. (2008) Iron deprivation induces EFG1-mediated hyphal development in Candida albicans without affecting biofilm formation. FEMS Yeast Res 8: 744-755.
16. Hameed, S., Dhamgaye, S., Singh, A., Goswami, S.K., and Prasad, R. (2011) Calcineurin signaling and membrane lipid homeostasis regulates iron mediated multidrug resistance mechanisms in Candida albicans. PLoS ONE 6: e18684.
17. Hentze, M.W., Muckenthaler, M.U., and Andrews, N.C. (2004) Balancing acts: molecular control of mammalian iron metabolism. Cell 117: 285-297.
18. Hsu, P.C., Yang, C.Y., and Lan, C.Y. (2011) Candida albicans Hap43 is a repressor induced under low-iron conditions and is essential for iron-responsive transcriptional regulation and virulence. Eukaryot Cell 10: 207-225.
19. Hsu, P.C., Chao, C.C., Yang, C.Y., Ye, Y.L., Liu, F.C., Chuang, Y.J., and Lan, C.Y. (2013) Diverse Hap43-independent functions of the Candida albicans CCAAT-binding complex. Eukaryot Cell 12: 804-815.
20. Jung, W.H., Sham, A., White, R., and Kronstad, J.W. (2006) Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans. PLoS Biol 4: e410.
21. Kaba, H.E., Nimtz, M., Muller, P.P., and Bilitewski, U. (2013) Involvement of the mitogen activated protein kinase Hog1p in the response of Candida albicans to iron availability. BMC Microbiol 13: 16.
22. Knight, S.A., Lesuisse, E., Stearman, R., Klausner, R.D., and Dancis, A. (2002) Reductive iron uptake by Candida albicans: role of copper, iron and the TUP1 regulator. Microbiology 148: 29-40.
23. Lai, W.K., Bard, J.E., and Buck, M.J. (2012) ArchTEx: accurate extraction and visualization of next-generation sequence data. Bioinformatics 28: 1021-1023.
24. Lan, C.Y., Rodarte, G., Murillo, L.A., Jones, T., Davis, R.W., Dungan, J., etal. (2004) Regulatory networks affected by iron availability in Candida albicans. Mol Microbiol 53: 1451-1469.
25. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
26. Li, D., Williams, D., Lowman, D., Monteiro, M.A., Tan, X., Kruppa, M., etal. (2009) The Candida albicans histidine kinase Chk1p: signaling and cell wall mannan. Fungal Genet Biol 46: 731-741.
27. Liu, H., Kohler, J., and Fink, G.R. (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
28. McCance, R.A., and Widdowson, E.M. (1938) The absorption and excretion of iron following oral and intravenous administration. J Physiol 94: 148-154.
29. Mao, X., Cao, F., Nie, X., Liu, H., and Chen, J. (2006) The Swi/Snf chromatin remodeling complex is essential for hyphal development in Candida albicans. FEBS Lett 580: 2615-2622.
30. Martens, J.A., and Winston, F. (2002) Evidence that Swi/Snf directly represses transcription in S. cerevisiae. Genes Dev 16: 2231-2236.
31. Miret, S., Simpson, R.J., and McKie, A.T. (2003) Physiology and molecular biology of dietary iron absorption. Annu Rev Nutr 23: 283-301.
32. Moreno-Ruiz, E., Ortu, G., de Groot, P.W., Cottier, F., Loussert, C., Prevost, M.C., etal. (2009) The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. Microbiology 155: 2004-2020.
33. Mukherjee, S., Crawford, J.M., McClear, N., and Tsang, A. (1997) A longitudinal study of unsaturated iron-binding capacity and lactoferrin in unstimulated parotid saliva. Biol Trace Elem Res 57: 1-8.
34. Pande, K., Chen, C., and Noble, S.M. (2013) Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat Genet 45: 1088-1091.
35. Pelletier, B., Mercier, A., Durand, M., Peter, C., Jbel, M., Beaudoin, J., and Labbe, S. (2007) Expression of Candida albicans Sfu1 in fission yeast complements the loss of the iron-regulatory transcription factor Fep1 and requires Tup co-repressors. Yeast 24: 883-900.
36. Pierce, J.V., Dignard, D., Whiteway, M., and Kumamoto, C.A. (2013) Normal adaptation of Candida albicans to the murine gastrointestinal tract requires Efg1p-dependent regulation of metabolic and host defense genes. Eukaryot Cell 12: 37-49.
37. Plaine, A., Walker, L., Da Costa, G., Mora-Montes, H.M., McKinnon, A., Gow, N.A., etal. (2008) Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45: 1404-1414.
38. Puri, S., Hohle, T.H., and O'Brian, M.R. (2010) Control of bacterial iron homeostasis by manganese. Proc Natl Acad Sci USA 107: 10691-10695.
39. Puri, S., Kumar, R., Chadha, S., Tati, S., Conti, H.R., Hube, B., etal. (2012) Secreted aspartic protease cleavage of Candida albicans Msb2 activates Cek1 MAPK signaling affecting biofilm formation and oropharyngeal candidiasis. PLoS ONE 7: e46020.
40. Rizzo, J.M., Mieczkowski, P.A., and Buck, M.J. (2011) Tup1 stabilizes promoter nucleosome positioning and occupancy at transcriptionally plastic genes. Nucleic Acids Res 39: 8803-8819.
41. Rizzo, J.M., Bard, J.E., and Buck, M.J. (2012) Standardized collection of MNase-seq experiments enables unbiased dataset comparisons. BMC Mol Biol 13: 15.
42. Rosenbach, A., Dignard, D., Pierce, J.V., Whiteway, M., and Kumamoto, C.A. (2010) Adaptations of Candida albicans for growth in the mammalian intestinal tract. Eukaryot Cell 9: 1075-1086.
43. Sandini, S., Stringaro, A., Arancia, S., Colone, M., Mondello, F., Murtas, S., etal. (2011) The MP65 gene is required for cell wall integrity, adherence to epithelial cells and biofilm formation in Candida albicans. BMC Microbiol 11: 106.
44. Singh, R.P., Prasad, H.K., Sinha, I., Agarwal, N., and Natarajan, K. (2011) Cap2-HAP complex is a critical transcriptional regulator that has dual but contrasting roles in regulation of iron homeostasis in Candida albicans. J Biol Chem 286: 25154-25170.
45. Sorgo, A.G., Heilmann, C.J., Brul, S., de Koster, C.G., and Klis, F.M. (2013) Beyond the wall: Candida albicans secret(e)s to survive. FEMS Microbiol Lett 338: 10-17.
46. Sutak, R., Lesuisse, E., Tachezy, J., and Richardson, D.R. (2008) Crusade for iron: iron uptake in unicellular eukaryotes and its significance for virulence. Trends Microbiol 16: 261-268.
47. Tolstorukov, M.Y., Sansam, C.G., Lu, P., Koellhoffer, E.C., Helming, K.C., Alver, B.H., etal. (2013) Swi/Snf chromatin remodeling/tumor suppressor complex establishes nucleosome occupancy at target promoters. Proc Natl Acad Sci USA 110: 10165-10170.
48. Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., etal. (2014) The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol 32: 381-386.
49. White, S.J., Rosenbach, A., Lephart, P., Nguyen, D., Benjamin, A., Tzipori, S., etal. (2007) Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog 3: e184.