A sticky situation: Untangling the transcriptional network controlling biofilm development in Candida albicans

Transcription

Volumn 3, Issue 6, 2012, Pages

  Fox, Emily P ^a,b   Nobile, Clarissa J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biofilm development; Candida albicans; Transcription networks; Transcriptional regulation

Indexed keywords

ARGININE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCR1; TRANSCRIPTION FACTOR BRG1; TRANSCRIPTION FACTOR EFG1; TRANSCRIPTION FACTOR NDT80; TRANSCRIPTION FACTOR ROB1; TRANSCRIPTION FACTOR TEC1; UNCLASSIFIED DRUG;

BINDING AFFINITY; BIOFILM; CANDIDA ALBICANS; DELETION MUTANT; FATTY ACID SYNTHESIS; GENE EXPRESSION; GENE FUNCTION; GENE REGULATORY NETWORK; GENE TARGETING; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN SYNTHESIS; PROTEIN TARGETING; REVIEW; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; BIOFILM DEVELOPMENT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; TRANSCRIPTION NETWORKS; TRANSCRIPTIONAL REGULATION;

CANDIDA ALBICANS;

BIOFILM DEVELOPMENT; CANDIDA ALBICANS; TRANSCRIPTION NETWORKS; TRANSCRIPTIONAL REGULATION;

BIOFILMS; CANDIDA ALBICANS; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84872193074     PISSN: 21541264     EISSN: 21541272     Source Type: Journal    
DOI: 10.4161/trans.22281     Document Type: Review

References (59)

1. Pappas PG, Rex JH, Sobel JD, Filler SG, Dismukes WE, Walsh TJ, et al.; Infectious Diseases Society of America. Guidelines for treatment of candidiasis. Clin Infect Dis 2004; 38:161-89; PMID:14699449; http://dx.doi.org/10.1086/380796.
2. Calderone RA, Fonzi WA. Virulence factors of Candida albicans. Trends Microbiol 2001; 9:327-35; PMID:11435107; http://dx.doi.org/10.1016/S0966-842X(01)02094-7.
3. Kullberg BJ, Oude Lashof AM. Epidemiology of opportunistic invasive mycoses. Eur J Med Res 2002; 7:183-91; PMID:12069910.
4. Weig M, Gross U, Mühlschlegel F. Clinical aspects and pathogenesis of Candida infection. Trends Microbiol 1998; 6:468-70; PMID:10036723; http://dx.doi.org/10.1016/S0966-842X(98)01407-3.
5. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284:1318-22; PMID:10334980; http://dx.doi.org/10.1126/science.284.5418.1318.
6. Donlan RM. Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis 2001; 33:1387-92; PMID:11565080; http://dx.doi.org/10.1086/322972.
7. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15:167-93; PMID:11932229; http://dx.doi.org/10.1128/CMR.15.2.167-193.2002.
8. Kojic EM, Darouiche RO. Candida infections of medical devices. Clin Microbiol Rev 2004; 17:255-67; PMID:15084500; http://dx.doi.org/10.1128/CMR.17.2.255-267.2004.
9. Douglas LJ. Medical importance of biofilms in Candida infections. Rev Iberoam Micol 2002; 19:139-43; PMID:12825991.
10. Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol 2003; 11:30-6; PMID:12526852; http://dx.doi.org/10.1016/S0966-842X(02)00002-1.
11. Wenzel RP. Nosocomial candidemia: risk factors and attributable mortality. Clin Infect Dis 1995; 20:1531-4; PMID:7548504; http://dx.doi.org/10.1093/clinids/20.6.1531.
12. Hawser SP, Douglas LJ. Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 1994; 62:915-21; PMID:8112864.
13. Baillie GS, Douglas LJ. Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol 1999; 48:671-9; PMID:10403418; http://dx.doi.org/10.1099/00222615-48-7-671.
14. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 2001; 183:5385-94; PMID:11514524; http://dx.doi.org/10.1128/JB.183.18.5385-5394.2001.
15. Nobile CJ, Mitchell AP. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 2005; 15:1150-5; PMID:15964282; http://dx.doi.org/10.1016/j.cub.2005.05.047.
16. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Köhler JR, et al. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 2010; 6:e1000828; PMID:20360962; http://dx.doi.org/10.1371/journal.ppat.1000828.
17. Ramage G, Tomsett K, Wickes BL, López-Ribot JL, Redding SW. Denture stomatitis: a role for Candida biofilms. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004; 98:53-9; PMID:15243471; http://dx.doi.org/10.1016/j.tripleo.2003.04.002.
18. Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, Pitula A. Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 2004; 72:6023-31; PMID:15385506; http://dx.doi.org/10.1128/IAI.72.10.6023-6031.2004.
19. Schinabeck MK, Long LA, Hossain MA, Chandra J, Mukherjee PK, Mohamed S, et al. Rabbit model of Candida albicans biofilm infection: liposomal amphotericin B antifungal lock therapy. Antimicrob Agents Chemother 2004; 48:1727-32; PMID:15105127; http://dx.doi.org/10.1128/AAC.48.5.1727-1732.2004.
20. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, et al. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 2012; 148:126-38; PMID:22265407; http://dx.doi.org/10.1016/j.cell.2011.10.048.
21. Homann OR, Dea J, Noble SM, Johnson AD. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 2009; 5:e1000783; PMID:20041210; http://dx.doi.org/10.1371/journal.pgen.1000783.
22. Bonhomme J, Chauvel M, Goyard S, Roux P, Rossignol T, d'Enfert C. Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans. Mol Microbiol 2011; 80:995-1013; PMID:21414038; http://dx.doi.org/10.1111/j.1365-2958.2011.07626.x.
23. Finkel JS, Xu W, Huang D, Hill EM, Desai JV, Woolford CA, et al. Portrait of Candida albicans adherence regulators. PLoS Pathog 2012; 8:e1002525; PMID:22359502; http://dx.doi.org/10.1371/journal.ppat.1002525.
24. García-Sánchez S, Aubert S, Iraqui I, Janbon G, Ghigo JM, d'Enfert C. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 2004; 3:536-45; PMID:15075282; http://dx.doi.org/10.1128/EC.3.2.536-545.2004.
25. Kelly MT, MacCallum DM, Clancy SD, Odds FC, Brown AJ, Butler G. The Candida albicans CaACE2 gene affects morphogenesis, adherence and virulence. Mol Microbiol 2004; 53:969-83; PMID:15255906; http://dx.doi.org/10.1111/j.1365-2958.2004.04185.x.
26. Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, Nantel A, et al. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 2009; 7:e1000133; PMID:19529758; http://dx.doi.org/10.1371/journal.pbio.1000133.
27. Askew C, Sellam A, Epp E, Mallick J, Hogues H, Mullick A, et al. The zinc cluster transcription factor Ahr1p directs Mcm1p regulation of Candida albicans adhesion. Mol Microbiol 2011; 79:940-53; PMID:21299649; http://dx.doi.org/10.1111/j.1365-2958.2010.07504.x.
28. Charos AE, Reed BD, Raha D, Szekely AM, Weissman SM, Snyder M. A highly integrated and complex PPARGC1A transcription factor binding network in HepG2 cells. Genome Res 2012; 22:1668-79; PMID:22955979; http://dx.doi.org/10.1101/gr.127761.111.
29. Wilson NK, Foster SD, Wang X, Knezevic K, Schütte J, Kaimakis P, et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 2010; 7:532-44; PMID:20887958; http://dx.doi.org/10.1016/j.stem.2010.07.016.
30. Young RA. Control of the embryonic stem cell state. Cell 2011; 144:940-54; PMID:21414485; http://dx.doi.org/10.1016/j.cell.2011.01.032.
31. Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 2001; 293:880-3; PMID:11486091; http://dx.doi.org/10.1126/science.1061320.
32. Locke, J. C. et al. Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1, 2005 0013 (2005).
33. Borneman AR, Leigh-Bell JA, Yu H, Bertone P, Gerstein M, Snyder M. Target hub proteins serve as master regulators of development in yeast. Genes Dev 2006; 20:435-48; PMID:16449570; http://dx.doi.org/10.1101/gad.1389306.
34. Ni L, Bruce C, Hart C, Leigh-Bell J, Gelperin D, Umansky L, et al. Dynamic and complex transcription factor binding during an inducible response in yeast. Genes Dev 2009; 23:1351-63; PMID:19487574; http://dx.doi.org/10.1101/gad.1781909.
35. Schweizer A, Rupp S, Taylor BN, Röllinghoff M, Schröppel K. The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol Microbiol 2000; 38:435-45; PMID:11069668; http://dx.doi.org/10.1046/j.1365-2958.2000.02132.x.
36. Müller D, Stelling J. Precise regulation of gene expression dynamics favors complex promoter architectures. PLoS Comput Biol 2009; 5:e1000279; PMID:19180182; http://dx.doi.org/10.1371/journal.pcbi.1000279.
37. Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, Andes DR, et al. Complementary adhesin function in C. albicans biofilm formation. Curr Biol 2008; 18:1017-24; PMID:18635358; http://dx.doi.org/10.1016/j.cub.2008.06.034.
38. Nobile CJ, Nett JE, Andes DR, Mitchell AP. Function of Candida albicans adhesin Hwp1 in biofilm formation. Eukaryot Cell 2006; 5:1604-10; PMID:17030992; http://dx.doi.org/10.1128/EC.00194-06.
39. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, et al. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2006; 2:e63; PMID:16839200; http://dx.doi.org/10.1371/journal.ppat.0020063.
40. Coleman DA, Oh SH, Zhao X, Hoyer LL. Heterogeneous distribution of Candida albicans cell-surface antigens demonstrated with an Als1-specific monoclonal antibody. Microbiology 2010; 156:3645-59; PMID:20705663; http://dx.doi.org/10.1099/mic.0.043851-0.
41. Green CB, Zhao X, Yeater KM, Hoyer LL. Construction and real-time RT-PCR validation of Candida albicans PALS-GFP reporter strains and their use in flow cytometry analysis of ALS gene expression in budding and filamenting cells. Microbiology 2005; 151:1051-60; PMID:15817774; http://dx.doi.org/10.1099/mic.0.27696-0.
42. Staab JF, Ferrer CA, Sundstrom P. Developmental expression of a tandemly repeated, proline-and glutamine-rich amino acid motif on hyphal surfaces on Candida albicans. J Biol Chem 1996; 271:6298-305; PMID:8626424; http://dx.doi.org/10.1074/jbc.271.11.6298.
43. Hundal HS, Taylor PM. Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am J Physiol Endocrinol Metab 2009; 296:E603-13; PMID:19158318; http://dx.doi.org/10.1152/ajpendo.91002.2008.
44. Sophianopoulou V, Diallinas G. Amino acid transporters of lower eukaryotes: regulation, structure and topogenesis. FEMS Microbiol Rev 1995; 16:53-75; PMID:7888172; http://dx.doi.org/10.1111/j.1574-6976.1995.tb00155.x.
45. Ghosh S, Navarathna DH, Roberts DD, Cooper JT, Atkin AL, Petro TM, et al. Arginine-induced germ tube formation in Candida albicans is essential for escape from murine macrophage line RAW 264.7. Infect Immun 2009; 77:1596-605; PMID:19188358; http://dx.doi.org/10.1128/IAI.01452-08.
46. Nett JE, Lepak AJ, Marchillo K, Andes DR. Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis 2009; 200:307-13; PMID:19527170; http://dx.doi.org/10.1086/599838.
47. Tripathi G, Wiltshire C, Macaskill S, Tournu H, Budge S, Brown AJ. Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J 2002; 21:5448-56; PMID:12374745; http://dx.doi.org/10.1093/emboj/cdf507.
48. Igarashi K, Kashiwagi K. Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 2010; 48:506-12; PMID:20159658; http://dx.doi.org/10.1016/j.plaphy.2010.01.017.
49. Igarashi K, Kashiwagi K. Modulation of cellular function by polyamines. Int J Biochem Cell Biol 2010; 42:39-51; PMID:19643201; http://dx.doi.org/10.1016/j.biocel.2009.07.009.
50. Ramage G, Saville SP, Wickes BL, López-Ribot JL. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 2002; 68:5459-63; PMID:12406738; http://dx.doi.org/10.1128/AEM.68.11.5459-5463.2002.
51. Deveau A, Hogan DA. Linking quorum sensing regulation and biofilm formation by Candida albicans. Methods Mol Biol 2011; 692:219-33; PMID:21031315; http://dx.doi.org/10.1007/978-1-60761-971-0_16.
52. Athenstaedt K, Zweytick D, Jandrositz A, Kohlwein SD, Daum G. Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J Bacteriol 1999; 181:6441-8; PMID:10515935.
53. Bennett RJ, Johnson AD. The role of nutrient regulation and the Gpa2 protein in the mating pheromone response of C. albicans. Mol Microbiol 2006; 62:100-19; PMID:16987174; http://dx.doi.org/10.1111/j.1365-2958.2006.05367.x.
54. Horak CE, Luscombe NM, Qian J, Bertone P, Piccirrillo S, Gerstein M, et al. Complex transcriptional circuitry at the G1/S transition in Saccharomyces cerevisiae. Genes Dev 2002; 16:3017-33; PMID:12464632; http://dx.doi.org/10.1101/gad.1039602.
55. Liu TT, Znaidi S, Barker KS, Xu L, Homayouni R, Saidane S, et al. Genome-wide expression and location analyses of the Candida albicans Tac1p regulon. Eukaryot Cell 2007; 6:2122-38; PMID:17905926; http://dx.doi.org/10.1128/EC.00327-07.
56. Lo MC, Peterson LF, Yan M, Cong X, Jin F, Shia WJ, et al. Combined gene expression and DNA occupancy profiling identifies potential therapeutic targets of t(8;21) AML. Blood 2012; 120:1473-84; PMID:22740448; http://dx.doi.org/10.1182/blood-2011-12-395335.
57. MacQuarrie KL, Fong AP, Morse RH, Tapscott SJ. Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet 2011; 27:141-8; PMID:21295369; http://dx.doi.org/10.1016/j.tig.2011.01.001.
58. Ramage G, VandeWalle K, López-Ribot JL, Wickes BL. The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 2002; 214:95-100; PMID:12204378; http://dx.doi.org/10.1111/j.1574-6968.2002.tb11330.x.
59. Uppuluri P, Pierce CG, Thomas DP, Bubeck SS, Saville SP, Lopez-Ribot JL. The transcriptional regulator Nrg1p controls Candida albicans biofilm formation and dispersion. Eukaryot Cell 2010; 9:1531-7; PMID:20709787; http://dx.doi.org/10.1128/EC.00111-10.