Transcriptional Response of Candida albicans to Hypoxia: Linkage of Oxygen Sensing and Efg1p-regulatory Networks

Journal of Molecular Biology

Volumn 361, Issue 3, 2006, Pages 399-411

  Setiadi, Eleonora R ^a   Doedt, Thomas ^a   Cottier, Fabien ^a   Noffz, Christine ^a   Ernst, Joachim F ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Candida albicans; EFG1; hypoxia; lipids; transcriptome

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EFG1P; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CULTURE MEDIUM; DNA MICROARRAY; DOWN REGULATION; FATTY ACID SYNTHESIS; FERMENTATION; FUNGUS HYPHAE; FUNGUS MUTANT; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; GLYCOLYSIS; HYPOXIA; MORPHOGENESIS; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; TRANSCRIPTION REGULATION; UPREGULATION;

CANDIDA ALBICANS; SACCHAROMYCETALES;

EID: 33746363517     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.06.040     Document Type: Article

References (52)

1. Tsai A.G., Friesenecker B., Mazzoni M.C., Kerger H., Buerk D.G., Johnson P.C., and Intaglietta M. Microvascular and tissue oxygen gradients in the rat mesentery. Proc. Natl Acad. Sci. USA 95 (1998) 6590-6595
2. O2 profiles to describe the oxygen pressure field within the tissue. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 132 (2002) 75-85
3. Odds F.C. Pathogenesis of Candida infections. J. Am. Acad. Dermatol. 31 (1994) S2-S5
4. Kullberg B.J., and Oude Lashof A.M.L. Epidemiology of opportunistic invasive mycoses. Eur. J. Med. Res. 7 (2002) 183-191
5. Zhang L., and Hach A. Molecular mechanism of heme signaling in yeast: the transcriptional activator Hap1 serves as the key mediator. Cell. Mol. Life Sci. 56 (1999) 415-426
6. Zitomer R.S., Carrico P., and Deckert J. Regulation of hypoxic gene expression in yeast. Kidney Int. 51 (1997) 507-513
7. Kastaniotis A.J., and Zitomer R.S. Rox1 mediated repression. Oxygen dependent repression in yeast. Advan. Exp. Med. Biol. 475 (2000) 185-195
8. Kwast K.E., Burke P.V., Staahl B.T., and Poyton R.O. Oxygen sensing in yeast: evidence for the involvement of the respiratory chain in regulating the transcription of a subset of hypoxic genes. Proc. Natl Acad. Sci. USA 96 (1999) 5446-5451
9. Bourdineaud J.P., De Sampaïo G., and Lauquin G.J. A Rox1-independent hypoxic pathway in yeast. Antagonistic action of the repressor Ord1 and activator Yap1 for hypoxic expression of the SRP1/TIR1 gene. Mol. Microbiol. 38 (2000) 879-890
10. Passoth V., Cohn M., Schäfer B., Hahn-Hägerdal, and Klinner U. Analysis of the hypoxia-induced ADH2 promoter of the respiratory yeast Pichia stipitis reveals a new mechanism for sensing of oxygen limitation in yeast. Yeast 20 (2003) 39-51
11. Balasubramanian B., Lowry C.V., and Zitomer R.S. The Rox1 repressor of the Saccharomyces cerevisiae hypoxic genes is a specific DNA-binding protein with a high-mobility-group motif. Mol. Cell. Biol. 13 (1993) 6071-6078
12. Vasconcelles M.J., Jiang Y., McDaid K., Gilooly L., Wretzel S., Porter D.L., et al. Identification and characterization of a low oxygen response element involved in the hypoxic induction of a family of Saccharomyces cerevisiae genes. Implications for the conservation of oxygen sensing in eukaryotes. J. Biol. Chem. 276 (2001) 14374-14384
13. Mennella T.A., Klinkenberg L.G., and Zitomer R.S. Recruitment of Tup1-Ssn6 by yeast hypoxic genes and chromatin-independent exclusion of TATA binding protein. Eukar. Cell 2 (2003) 1288-1303
14. Ter Linde J.J., Liang H., Davis R.W., Steensma H.Y., van Dijken J.P., and Pronk J.T. Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae. J. Bacteriol. 181 (1999) 7409-7413
15. Becerra M., Lombadía-Ferreira L.J., Hauser N.C., Hoheisel J.D., Tizon B., and Cerdán M.E. The yeast transcriptome in aerobic and hypoxic conditions: effects of hap1, rox1, rox3 and srb10 deletions. Mol. Microbiol. 43 (2002) 545-555 (Erratum in: Mol Microbiol., (2002) 45, 265)
16. Firth J.D., Ebert B.L., Pugh C.W., and Ratcliffe P.J. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc. Natl Acad. Sci. USA 91 (1994) 6496-6500
17. Gancedo J.M. Carbon catabolite repression in yeast. Eur. J. Biochem. 206 (1992) 297-313
18. Kadosh D., and Johnson A.D. Rfg1, a protein related to the Saccharomyces cerevisiae hypoxic regulator Rox1, controls filamentous growth and virulence in Candida albicans. Mol. Cell. Biol. 21 (2001) 2496-2505
19. Khalaf R.A., and Zitomer R.S. The DNA binding protein Rfg1 is a repressor of filamentation in Candida albicans. Genetics 157 (2001) 1503-1512
20. Brown Jr. D.H., Giusani A.D., Chen X., and Kumamoto C.A. Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol. Microbiol. 34 (1999) 651-662
21. Sonneborn A., Bockmühl D.P., and Ernst J.F. Chlamydospore formation in Candida albicans requires the Efg1p morphogenetic regulator. Infect. Immun. 67 (1999) 5514-5517
22. Hornby J.M., Jensen E.C., Lisec A.D., Tasto J.J., Jahnke B., Shoemaker R., et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67 (2001) 2982-2992
23. Chen H., Fujita M., Feng Q., Clardy J., and Fink G.R. Tyrosol is a quorum-sensing molecule in Candida albicans. Proc. Natl Acad. Sci. USA 101 (2004) 5048-5052
24. Davis D. Adaptation to environmental pH in Candida albicans and its relation to pathogenesis. Curr. Genet. 44 (2003) 1-7 (Erratum: Curr. Genet. (2003)44, 58)
25. Maidan M.M., De Rop L., Serneels J., Exler S., Rupp S., Tournu H., et al. The G protein-coupled receptor Gpr1 and the Galpha protein Gpa2 act through the cAMP-protein kinase A pathway to induce morphogenesis in Candida albicans. Mol. Biol. Cell 16 (2005) 1971-1986
26. Abramova N.E., Cohen B.D., Sertil O., Kapoor R., Davies K.J., and Lowry C.V. Regulatory mechanisms controlling expression of the DAN/TIR mannoprotein genes during anaerobic remodeling of the cell wall in Saccharomyces cerevisiae. Genetics 157 (2001) 1169-1177
27. Abramova N., Sertil O., Mehta S., and Lowry C.V. Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J. Bacteriol. 183 (2001) 2881-2887
28. Stoldt V.R., Sonneborn A., Leuker C.E., and Ernst J.F. Efg1p, an essential regulator of morphogenesis of the human fungal pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J. 16 (1997) 1982-1991
29. Lo H.J., Köhler J.R., DiDomenico B., Loebenberg D., Cacciapuoti A., and Fink G.R. Nonfilamentous C. albicans mutants are avirulent. Cell 90 (1997) 939-949
30. Doedt T., Krishnamurthy S., Bockmühl D.P., Tebarth B., Stempel C., Russell C.L., et al. APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15 (2004) 3167-3180
31. Sohn K., Urban C., Brunner H., and Rupp S. EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol. Microbiol. 47 (2003) 89-102
32. Roemer T., Jiang B., Davison J., Ketela T., Veillette K., Breton A., et al. Large-scale essential gene identification in Candida albicans and applications to antifungal drug discovery. Mol. Microbiol. 50 (2003) 167-181
33. Duttagupta R., Vasudevan S., Wilusz C.J., and Peltz S.W. A yeast homologue of Hsp70, Ssa1p, regulates turnover of the MFA2 transcript through its AU-rich 3′ untranslated region. Mol. Cell. Biol. 23 (2003) 2623-2632
34. Krishnahmurthy S., Plaine A., Albert J., Prasad T., Prasad R., and Ernst J.F. Dosage-dependent functions of fatty acid desaturase Ole1p in growth and morphogenesis of Candida albicans. Microbiology 150 (2004) 1991-2003
35. Murayama S.Y., Negishi Y., Umeyama T., Kaneko A., Oura T., Niimi M., et al. Construction and functional analysis of the fatty acid desaturase gene disruptants in Candida albicans. Microbiology 152 (2006) 1551-1558
36. Klengel T., Liang W.J., Chaloupka J., Ruoff C., Schroeppel K., Naglik J.R., et al. Fungal adenolyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr. Biol. 15 (2005) 2021-2026
37. Semenza G.L., Jiang B.-H., Leung S.W., Passantino R., Concordet J.P., Maire P., and Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem. 271 (1996) 32529-32537
38. Hochachka P.W., Buck L.T., Doll C.J., and Land S.C. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl Acad. Sci. USA 93 (1996) 9493-9498
39. Kadosh D., and Johnson A.D. Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16 (2005) 2903-2912
40. García-Sánchez S., Mavor A.L., Russell C.L., Argimon S., Dennison P., Enjalbert B., and Brown A.J.P. Global roles of Ssn6 in Tup1- and Nrg1-dependent gene regulation in the fungal pathogen, Candida albicans. Mol. Biol. Cell 16 (2005) 2913-2925
41. Lott T.J., Fundyga R.E., Kuykendall R.J., and Arnold J. The human commensal yeast, Candida albicans, has an ancient origin. Fungal Genet. Biol. 42 (2005) 444-451
42. Oh C.S., and Martin C.E. Candida albicans Spt23p controls the expression of the Ole1p Delta9 fatty acid desaturase and regulates unsaturated fatty acid biosynthesis. J. Biol. Chem. 17 (2006) 7030-7039
43. Nakagawa Y., Sugioka S., Keneko Y., and Harashima S. O2R, a novel regulatory element mediating Rox1p-independent O(2) and unsaturated fatty acid repression of OLE1 in Saccharomyces cerevisiae. J. Bacteriol. 183 (2001) 745-751
44. Fantino E., Marguet D., and Lauquin G.J. Downstream activating sequence within the coding region of a yeast gene: specific binding in vitro of RAP1 protein. Mol. Gen. Genet. 236 (1992) 65-75
45. Greger I.H., and Proudfoot N.J. Poly(A) signals control both transcriptional termination and initiation between the tandem GAL10 and GAL7 genes of Saccharomyces cerevisiae. EMBO J. 17 (1998) 4771-4779
46. Vemula M., Kandasamy P., Oh C.S., Chellappa R., Gonzalez C.I., and Martin C.E. Maintenance and regulation of mRNA stability of the Saccharomyces cerevisiae OLE1 gene requires multiple elements within the transcript that act through translation-independent mechanisms. J. Biol. Chem. 278 (2003) 45269-45279
47. Kim A.S., Garni R.M., Henry-Stanley M.J., Bendel C.M., Erlandsen S.L., and Wells C.L. Hypoxia and extraintestinal dissemination of Candida albicans yeast forms. Shock 19 (2003) 257-262
48. Fonzi W.A., and Irwin M.Y. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134 (1993) 717-728
49. Prill S.K.-H., Klinkert B., Timpel C., Gale C.A., Schröppel K., and Ernst J.F. PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol. Microbiol. 55 (2005) 546-560
50. Tebarth B., Doedt T., Krishnamurthy S., Weide M., Monterola F., Dominguez A., and Ernst J.F. Adaptation of the Efg1p morphogenetic pathway in Candida albicans by negative autoregulation and PKA-dependent repression of the EFG1 gene. J. Mol. Biol. 329 (2003) 949-962
51. Sherman F., Fink G., and Hicks J. Methods in Yeast Genetics (1986), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
52. Mishra P., and Prasad R. Alterations in fatty acyl composition can selectively affect amino acid transport in Saccharomyces cerevisiae. Biochem. Int. 15 (1987) 499-508