Efg1 directly regulates ACE2 expression to mediate cross talk between the cAMP/PKA and RAM pathways during candida albicans morphogenesis

Eukaryotic Cell

Volumn 13, Issue 9, 2014, Pages 1169-1180

  Saputo, Sarah ^a   Kumar, Anuj ^b   Krysan, Damian J ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANDIDA ALBICANS;

ANGIOTENSIN CONVERTING ENZYME 2; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIPEPTIDYL CARBOXYPEPTIDASE; DNA BINDING PROTEIN; EFG1 PROTEIN, CANDIDA ALBICANS; FUNGAL PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; BIOSYNTHESIS; CANDIDA ALBICANS; FUNGUS HYPHAE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MORPHOGENESIS; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

ANIMALS; CANDIDA ALBICANS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; MALE; MORPHOGENESIS; PEPTIDYL-DIPEPTIDASE A; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

EID: 84907473481     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00148-14     Document Type: Article

References (46)

1. Moran GP, Coleman D, Sullivan D. 2012. An introduction to the medically important Candida species, p 11-25. In Calderone R, Clancy CJ (ed), Candida and candidiasis, 2nd ed. ASM Press, Washington, DC.
2. Vazquez JA, Sobel JD. 2003. Candidiasis, p 143-187. In Dismukes WE, Pappas PG, Sobel JD (ed), Clinical mycology. Oxford University Press, Oxford, United Kingdom.
3. Sudbery PE. 2011. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9:737-748. http://dx.doi.org/10.1038/nrmicro2636.
4. Sudbery PE, Gow N, Sudbery PE. 2004. The distinct morphotypes of Candida albicans. Trends Microbiol. 12:317-324. http://dx.doi.org/10. 1016/j.tim.2004.05.008.
5. Guarner J, Brandt ME. 2011. Histopathologic diagnosis of fungal infections in the 21st century. Clin. Microbiol. Rev. 24:247-280. http://dx.doi. org/10.1128/CMR.00053-10.
6. Magee PT. 2010. Fungal pathogenesis and morphological switches. Nat. Genet. 42:560-561. http://dx.doi.org/10.1038/ng0710-560.
7. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cucciapuoti A, Fink GR. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939- 949. http://dx.doi.org/10.1016/S0092-8674(00)80358-X.
8. Braun BR, Head WS, Wang MX, Johnson AD. 2000. Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156:31-44.
9. Sarthy AN, McGonigal T, Coen M, Frost DJ, Meulbroek JA, Goldman RC. 1997. Phenotype in Candida albicans of a disruption of the BGL2 gene encoding a 1,3-beta-glucosyltransferase. Microbiology 143:367-376. http: //dx.doi.org/10.1099/00221287-143-2-367.
10. Lorenz MC, Fink GR. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412:83-86. http://dx.doi.org/10.1038/35083594.
11. Gow NAR, van de Veerdonk FL, Brown AJP, Netea MG. 2012. Candida albicans morphogenesis and host defense: discriminating invasion from colonization. Nat. Rev. Microbiol. 10:112-122. http://dx.doi.org/10.1038 /nrmicro2711.
12. Noble SM, French S, Kohn LA, Chen V, Johnson AD. 2010. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42:590-598. http: //dx.doi.org/10.1038/ng.605.
13. Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL. 2003. Engineered control of cell morphology in vivo reveals distinct role for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2:1053-1060. http://dx.doi.org/10.1128/EC.2.5.1053-1060.2003.
14. Bharucha N, Chabrier-Roselló Y, Xu T, Johnson C, Sobcynski S, Song SQ, Dobry CJ, Anderson CP, Benjamin AJ, Kumar A, Krysan DJ. 2011. A largescalecomplexhaploinsufficiency- based genetic interaction screen inCandida albicans: analysis of the RAM Network during morphogenesis. PLoS Genet. 7:e1002058. http://dx.doi.org/10.1371/journal.pgen.1002058.
15. Mazanka E, Weiss EL. 2010. Sequential counteracting kinases restrict an asymmetric gene expression program to early G1. Mol. Biol. Cell 21:2809- 2820. http://dx.doi.org/10.1091/mbc.E10-02-0174.
16. Kurischko C, Weiss G, Ottey M, Luca FC. 2005. A role for the Saccharomyces cerevisiae regulation of Ace2 and polarized morphogenesis signaling network in cell integrity. Genetics 171:443-455. http://dx.doi.org/10. 1534/genetics.105.042101.
17. Weiss EL. 2012. Mitotic exit and separation of mother and daughter cells. Genetics 192:1165-1202. http://dx.doi.org/10.1534/genetics.112.145516.
18. Sbia M, Parnell EJ, Yu Y, Olsen AE, Kretschmann KL, Voth WP, Stillman DJ. 2008. Regulation of the yeast Ace2 transcription factor during the cell cycle. J. Biol. Chem. 283:11135-11145. http://dx.doi.org/10. 1074/jbc.M800196200.
19. Kelly MT, MacCallum DM, Clancy SD, Odds FC, Brown AJP, Butler G. 2004. The Candida albicans CaACE2 gene affects morphogenesis, adherence, and virulence. Mol. Microbiol. 53:969-983. http://dx.doi.org/10. 1111/j.1365-2958.2004.04185.x.
20. McNemar MD, Fonzi WA. 2002. Conserved serine and threonine kinase encoded byCBK1regulates expression of several hypha-associated transcripts and genes encoding cell wall proteins in Candida albicans. J. Bacteriol. 184: 2058-2061. http://dx.doi.org/10.1128/JB.184.7.2058-2061.2002.
21. Song Y, Cheon SA, Lee KE, Lee S-Y, Lee B-K, Oh D-B, Kang HA, Kim J-Y. 2008. Role of the RAM network in cell polarity and hyphal morphogenesis in Candida albicans. Mol. Biol. Cell 19:5456-5477. http://dx.doi. org/10.1091/mbc.E08-03-0272.
22. Mulhern SM, Logue ME, Butler G. 2006. Candida albicans transcription factor Ace2 regulates metabolism and is required for filamentation in hypoxic conditions. Eukaryot. Cell 5:2001-2013. http://dx.doi.org/10.1128 /EC.00155-06.
23. Stoldt VR, Sonneborn A, Leuker CE, Ernst JF. 1997. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH protein regulating morphogenetic processes in fungi. EMBO J. 16:1982-1991. http://dx.doi.org/10.1093 /emboj/16.8.1982.
24. Doedt T, Krishnamurthy S, Bockmühl DP, Tebarth B, Stempel C, Russell CL, Brown AJ, Ernst JF. 2004. APES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15:3167- 3180. http://dx.doi.org/10.1091/mbc.E03-11-0782.
25. Schneper L, Krauss A, Miyamoto R, Fang S, Broach JR. 2004. The ras/protein kinaseApathway acts in parallel with the Mob2/Cbk1 pathway to effect cell cycle progression and proper bud site selection. Eukaryot. Cell 3:108-120. http://dx.doi.org/10.1128/EC.3.1.108-120.2004.
26. Wang A, Raniga PP, Lane S, Lu Y, Liu H. 2009. Hyphal chain formation in Candida albicans: Cdc28-Hgc1 phosphorylation of Efg1 represses cell separation genes. Mol. Cell. Biol. 29:4406-4416. http://dx.doi.org/10. 1128/MCB.01502-08.
27. Gutierrez-Escribano P, Gonzalez-Novo A, Belen Suarez M, Li C-R, Wang Y, Vazquez de Aldana CR, Correa-Bordes J. 2011. CDKdependent phosphorylation of Mob2 is essential for hyphal development in Candida albicans. Mol. Biol. Cell 22:2458-2469. http://dx.doi.org/10. 1091/mbc.E11-03-0205.
28. Burke DJ, Dawson D, Stearns T. 2000. Methods in yeast genetics. CSHL Press, Woodbury, NY.
29. Morales DK, Grahl N, Okegbe C, Dietrich LE, Jacobs NJ, Hogan DA. 2013. Control of Candida albicans metabolism and biofilm formation by Pseudomonas aeruginosa phenazines. mBio 4:e00526 -12. http://dx.doi. org/10.1128/mBio.00526-12.
30. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3:1101-1108. http://dx.doi.org/10. 1038/nprot.2008.73.
31. Hernday AD, Noble SM, Mitrovich QM, Johnson AD. 2010. Genetics and molecular biology of Candida albicans. Methods Enzymol. 470:737- 758. http://dx.doi.org/10.1016/S0076-6879(10)70031-8.
32. Pierce JV, Kumamoto CA. 2012. Variation in Candida albicans EFG1 expression enables host-dependent changes in colonizing fungal populations. mBio 3:e00117-12. http://dx.doi.org/10.1128/mBio.00117-12.
33. Tebarth B, Doedt T, Krishnamurthy S, Weide M, Monterola F, Domingues A, Ernst JF. 2003. Adaptation of the Efg1p morphogenetic pathway in Candida albicans by negative autoregulation and PKAdependent repression of the EFG1 gene. J. Mol. Biol. 329:949-962. http: //dx.doi.org/10.1016/S0022-2836(03)00505-9.
34. Lassak T, Schneider E, Bussmann M, Kurtz D, Manak JR, Srkantha T, Soll DR, Ernst JF. 2011. Target specificity of the Candida albicans Efg1 regulator. Mol. Microbiol. 82:602-618. http://dx.doi.org/10.1111/j.1365 -2958.2011.07837.x.
35. Bockmuhl DP, Ernst JF. 2001. A potential phosphorylation site for an A-kinase in the Efg1 regulator protein contributes to hyphal morphogenesis of Candida albicans. Genetics 157:1523-1530.
36. Bastidas RJ, Heitman J, Cardenas ME. 2009. The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog. 5:e1000294. http://dx.doi.org/10.1371/journal.ppat.1000294.
37. Hnisz D, Bardet AF, Nobile CJ, Petryshyn A, Glaser W, Schöck U, Stark A, Kuchler K. 2012. A histone deacetylase adjusts transcription kinetics at coding sequences during Candida albicans morphogenesis. PLoS Genet. 8:e1003118. http://dx.doi.org/10.1371/journal.pgen.1003118.
38. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148:126-138. http://dx.doi.org/10.1016/j.cell.2011.10.048.
39. Finkel JS, Xu W, Huang D, Hill EM, Desai JV, Woolford CA, Nett JE, Taff H, Norice CT, Andes DR, Lanni F, Mitchell AP. 2012. Portrait of Candida albicans adherence regulators. PLoS Pathog. 8:e1002525. http: //dx.doi.org/10.1371/journal.ppat.1002525.
40. Giusani AD, Vinces M, Kumamoto CA. 2002. Invasive filamentous growth of Candida albicans is promoted by Czf1p-dependent relief of Efg1p-mediated repression. Genetics 160:1749-1753.
41. Sellam A, Askew C, Epp E, Lavoie H, Whiteway M, Nantel A. 2009. Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans. Mol. Biol. Cell 20:2389-2400. http://dx.doi.org/10.1091/mbc.E08-11-1093.
42. Schweizer A, Rupp S, Taylor BN, Röllinghoff M, Schröppel K. 2000. The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol. Microbiol. 38:435-445. http://dx. doi.org/10.1046/j.1365-2958.2000.02132.x.
43. Lu Y, Su C, Liu H. 2012. A GATA transcription factor recruits Hda1 in response to reduced Tor1 signaling to establish a hyphal chromatin state in Candida albicans. PLoS Pathog. 8:e1002663. http://dx.doi.org/10.1371 /journal.ppat.1002663.
44. Lane S, Birse C, Zhou S, Matson R, Liu H. 2001. DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J. Biol. Chem. 276:48988-48996. http://dx. doi.org/10.1074/jbc.M104484200.
45. Saputo S, Chabrier-Rosello Y, Luca FC, Kumar A, Krysan DJ. 2012. The RAM network in pathogenic fungi. Eukaryot. Cell 11:708-717. http://dx. doi.org/10.1128/EC.00044-12.
46. Lindsay AK, Deveau A, Piispanen AE, Hogan DA. 2012. Farnesol and cyclic AMP signaling effects on the hypha-to-yeast transition in Candida albicans. Eukaryot. Cell 11:1219-1225. http://dx.doi.org/10.1128/EC. 00144-12.