The Rbf1, Hfl1 and Dbp4 of Candida albicans regulate common as well as transcription factor-specific mitochondrial and other cell activities

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Khamooshi, Kasra ^a   Sikorski, Patricia ^a   Sun, Nuo ^a   Calderone, Richard ^a   Li, Dongmei ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Candida albicans; Lipid oxidation; Metabolic regulation; Mitochondria; Non glucose carbon metabolism; Transcription factor

Indexed keywords

CARBON; CELL NUCLEUS DNA; FUNGAL PROTEIN; GLYCEROL; MITOCHONDRIAL DNA; PHOSPHOLIPID; PROTEIN DBP4; PROTEIN DPN4P; PROTEIN GOA1; PROTEIN HFL1; PROTEIN RBF1; RIBOSOME RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CARBON METABOLISM; CELL ACTIVITY; CELL STRESS; CONTROLLED STUDY; DNA REPLICATION; FUNGAL CELL WALL; FUNGAL GENOME; FUNGAL METABOLISM; FUNGUS GROWTH; FUNGUS MUTANT; GENE FUNCTION; GENE INACTIVATION; GENE LIBRARY; MICROARRAY ANALYSIS; MITOCHONDRIAL RESPIRATION; NONHUMAN; PEROXISOME; PHOSPHOLIPID SYNTHESIS; RNA PROCESSING; TRANSCRIPTION REGULATION;

CANDIDA ALBICANS;

ANTIFUNGAL AGENTS; CAENORHABDITIS ELEGANS PROTEINS; CANDIDA ALBICANS; CARBON; CELL RESPIRATION; CELL WALL; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE KNOCKOUT TECHNIQUES; GENE LIBRARY; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; LIPID PEROXIDATION; MITOCHONDRIA; NUCLEAR PROTEINS; PHENOTYPE; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84892629093     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-56     Document Type: Article

References (48)

1. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med 2012, 4:165rv13.
2. Calderone R, Gay-Andrieu F, Li D, Alex D, Sun N. Antifungals and antifungal discovery, chapter 17. Antimicrobial Drug Discovery 2012, UK: CABI, Tegos G, Mylonakis E.
3. Arnold HM, Micek ST, Shorr AF, Zilberberg MD, Labelle AJ, Kothari S, Kollef MH. Hospital resource utilization and costs of inappropriate treatment of candidemia. Pharmacotherapy 2010, 30:361-368. 10.1592/phco.30.4.361, 20334456.
4. Gauwerky K, Borelli C, Korting HC. Targeting virulence. A new paradigm for antifungals. Drug Discov Today 2009, 14:214-222. 10.1016/j.drudis.2008.11.013, 19152839.
5. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche HU, Quan SP, Horn D. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance®) registry, 2004-2008. Diagn Microbiol Infect Dis 2012, 74:323-31. 10.1016/j.diagmicrobio.2012.10.003, 23102556.
6. Blumberg HM, Jarvis WR, Soucie JM, Edwards JE, Patterson JE, Pfaller MA, Rangel-Frausto MS, Rinaldi MG, Saiman L, Wiblin RT, Wenzel RP, National Epidemiology of Mycoses Survey(NEMIS) Study Group Risk factors for Candida blood stream infections in surgical intensive care unit patients. Clin Infect Dis 2001, 33:177-186. 10.1086/321811, 11418877, National Epidemiology of Mycoses Survey(NEMIS) Study Group.
7. Thompson GR, Patel PK, Kirkpatrick WR, Westbrook SD, Berg D, Erlandsen J, Redding SW, Patterson TF. Oropharyngeal candidiasis in the era of anti-retroviral therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endo 2010, 109:488-495.
8. Gagne J, Goldfarb N. Candidemia in the in-patient setting: treatment options and economics. Expert Opin Pharmacother 2007, 8:1643-1650. 10.1517/14656566.8.11.1643, 17685882.
9. Grumaz C, Lorenz S, Stevens P, Lindemann E, Schöck U, Retey J, Rupp S, Sohn K. Species and condition specific adaptation of the transcriptional landscapes in Candida albicans and Candida dubliniensis. BMC Genomics 2013, 14:212. 10.1186/1471-2164-14-212, 3626586, 23547856.
10. Shahi P, Moye-Rowley WS. Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim Biophys Acta 2009, 1794:852-859. 10.1016/j.bbapap.2008.12.012, 2671576, 19150512.
11. Sandai D, Yin Z, Selway L, Stead D, Walker J, Leach MD, Bohovych I, Ene IV, Kastora S, Budge S, Munro CA, Odds FC, Gow NA, Brown AJ. The evolutionary rewiring of ubiquitination targets has reprogrammed the regulation of carbon assimilation in the pathogenic yeast Candida albicans. MBio 2012, 3:e00495-12. doi: 10.1128, 3520108, 23232717.
12. Niimi M, Kamiyama A, Tokunaga M. Respiration of medically important Candida species and Saccharomyces cerevisiae in relation to glucose effect. J Med Vet Mycol 1988, 26:195-198. 10.1080/02681218880000271, 3050010.
13. Ramírez MA, Lorenz MC. Mutations in alternative carbon utilization pathways in Candida albicans attenuate virulence and confer pleiotropic phenotypes. Eukaryot Cell 2007, 6:280-290. 10.1128/EC.00372-06, 1797957, 17158734.
14. Barelle CJ, Priest CL, Maccallum DM, Gow NA, Odds FC, Brown AJ. Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 2006, 8:961-971. 10.1111/j.1462-5822.2005.00676.x, 1472618, 16681837.
15. Lorenz M, Bender J, Fink G. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 2004, 3:1076-1087. 10.1128/EC.3.5.1076-1087.2004, 522606, 15470236.
16. Bambach A, Fernandes MP, Ghosh A, Kruppa M, Alex D, Li D, Fonzi WA, Chauhan N, Sun N, Agrellos OA, Vercesi AE, Rolfes RJ, Calderone R. Goa1p of Candida albicans localizes to the mitochondria during stress and is required for mitochondrial function and virulence. Eukaryot Cell 2009, 8:1706-1720. 10.1128/EC.00066-09, 2772395, 19717740.
17. Chen H, Calderone R, Sun N, Wang Y, Li D. Caloric restriction restores the chronological life span of the Goa1 null mutant of Candida albicans in spite of high cell levels of ROS. Fungal Genet Biol 2012, 49:1023-32. 10.1016/j.fgb.2012.09.007, 23063955.
18. Li D, Chen H, Florentino A, Alex D, Sikorski P, Fonzi WA, Calderone R. Enzymatic dysfunction of mitochondrial complex I of the Candida albicans goa1 mutant is associated with increased reactive oxidants and cell death. Eukaryot Cell 2011, 10:672-682. 10.1128/EC.00303-10, 3127659, 21398508.
19. Sun N, Fonzi W, Chen H, She X, Zhang L, Zhang L, Calderone R. Azole susceptibility and transcriptome profiling in Candida albicans mitochondrial electron transport chain complex I mutants. Antimicrob Agents Chemother 2013, 57:532-542. 10.1128/AAC.01520-12, 3535965, 23147730.
20. She X, Zhang L, Chen H, Calderone R, Li D. Cell surface changes in the Candida albicans mitochondrial mutant goa1Δ are associated with reduced recognition by innate immune cells. Cell Microbiol 2013, 12. doi:10.1111/cmi.12135.
21. Homann OR, Dea J, Noble SM, Johnson AD. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 2009, 5:e1000783. 10.1371/journal.pgen.1000783, 2790342, 20041210.
22. Aoki Y, Ishii N, Watanabe M, Yoshihara F, Arisawa M. Rbf1 (RPG-box binding factor), a transcription factor involved in yeast-hyphal transition of Candida albicans. Nippon Ishinkin Gakkai Zasshi 1998, 39:67-71.
23. Levitin A, Whiteway M. The effect of prostaglandin E2 on transcriptional responses of Candida albicans. Microbiol Res 2007, 162:201-210. 10.1016/j.micres.2007.02.001, 17433645.
24. Chamilos G, Lewis RE, Kontoyiannis DP. Inhibition of Candida parapsilosis mitochondrial respiratory pathways enhances susceptibility to caspofungin. Antimicrob Agents Chemother 2006, 50:744-747. 10.1128/AAC.50.2.744-747.2006, 1366909, 16436735.
25. Joseph-Horne T, Hollomon DW, Wood PM. Fungal respiration: a fusion of standard and alternative components. Biochim Biophys Acta 2001, 1504:179-195. 10.1016/S0005-2728(00)00251-6, 11245784.
26. Nohturfft A, Zhang SC. Coordination of lipid metabolism in membrane biogenesis. Annu Rev Cell Dev Biol 2009, 25:539-566. 10.1146/annurev.cellbio.24.110707.175344, 19575637.
27. Shingu-Vazquez M, Traven A. Mitochondria and fungal pathogenesis: drug tolerance, virulence, and potential for antifungal therapy. Eukaryot Cell 2011, 10:1376-1383. 10.1128/EC.05184-11, 3209048, 21926328.
28. Zhou H, Lorenz M. Carnitine acetyltransferases are required for growth on non-fermentable carbon sources but not for pathogenesis in Candida albicans. Microbiology 2008, 154:500-509. 10.1099/mic.0.2007/014555-0, 18227254.
29. Carman A, Vylkova S, Lorenz M. Role of acetyl coenzyme A synthesis and breakdown in alternative carbon source utilization in Candida albicans. Eukaryot Cell 2008, 7:1733-1741. 10.1128/EC.00253-08, 2568070, 18689527.
30. Lorenz M, Fink G. The glyoxylate cycle is required for fungal virulence. Nature 2001, 412:83-86. 10.1038/35083594, 11452311.
31. Hazelwood LA, Daran JM, van Maris AJ, Pronk JT, Dickinson JR. The ehulich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 2008, 74:2259-2266. 10.1128/AEM.02625-07, 2293160, 18281432.
32. Barz T, Ackermann K, Pyerin W. Control of methionine biosynthesis genes by protein kinase CK2-mediated phosphorylation of Cdc34. Cell Mol Life Sci 2006, 63:2183-2190. 10.1007/s00018-006-6213-5, 16952051.
33. Malanovic N, Streith I, Wolinski H, Rechberger G, Kohlwein SD, Tehlivets O. S-adenosyl-L-homocysteine hydrolase, key enzyme of methylation metabolism, regulates phosphatidylcholine synthesis and triacylglycerol homeostasis in yeast: implications for homocysteine as a risk factor of atherosclerosis. J Biol Chem 2008, 283:23989-2399. 10.1074/jbc.M800830200, 3259781, 18591246.
34. Eisman B, Alonso-Monge R, Román E, Arana D, Nombela C, Pla J. The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryot Cell 2006, 2:347-358.
35. Li D, Williams D, Lowman D, Monteiro MA, Tan X, Kruppa M, Fonzi W, Roman E, Pla J, Calderone R. The Candida albicans histidine kinase Chk1p: signaling and cell wall mannan. Fungal Genet Biol 2009, 46:731-41. 10.1016/j.fgb.2009.06.008, 2731578, 19563901.
36. Maesaki S, Marichal P, Vanden Bossche H, Sanglard D, Kohno S. Rhodamine 6G efflux for the detection of CDR1-overexpressing azole-resistant Candida albicans strains. J Antimicrob Chemother 1999, 44:27-31. 10.1093/jac/44.1.27, 10459807.
37. Saengkhae C, Loetchutinat C, Garnier-Suillerot A. Kinetic analysis of rhodamines efflux mediated by the multidrug resistance protein (MRP1). Biophys J 2003, 85:2006-2014. 10.1016/S0006-3495(03)74628-1, 1303372, 12944313.
38. Zhao F, Song CP, He J, Zhu H. Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root Ion channel activities. Plant Physiol 2007, 145:1061-1072. 10.1104/pp.107.105882, 2048800, 17905858.
39. Brandt ME, Vickery LE. Charge pair interactions stabilizing ferredoxin-ferredoxin reductase complexes. Identification by complementary site-specific mutations. J Biol Chem 1993, 268:17126-30.
40. van Steensel B. Mapping of genetic and epigenetic regulatory networks using microarrays. Nat Genet 2005, 37(Suppl):S18-24.
41. Vandeputte P, Ischer F, Sanglard D, Coste AT. In vivo systematic analysis of Candida albicans Zn2-Cys6 transcription factors mutants for mice organ colonization. PLoS ONE 2011, 6:e26962. 10.1371/journal.pone.0026962, 3205040, 22073120.
42. Hao B, Clancy CJ, Cheng S, Raman SB, Iczkowski KA, Nguyen MH. Candida albicans RFX2 encodes a DNA binding protein involved in DNA damage responses, morphogenesis, and virulence. Eukaryot Cell 2009, 8:627-639. 10.1128/EC.00246-08, 2669197, 19252121.
43. Talibi D, Raymond M. Isolation of a putative Candida albicans transcriptional regulator involved in pleiotropic drug resistance by functional complementation of a pdr1 pdr3 mutation in Saccharomyces cerevisiae. J Bacteriol 1999, 181:231-240. 103554, 9864335.
44. Kumme J, Dietz M, Wagner C, Schüller HJ. Dimerization of yeast transcription factors Ino2 and Ino4 is regulated by precursors of phospholipid biosynthesis mediated by Opi1 repressor. Curr Genet 2008, 54:35-45. 10.1007/s00294-008-0197-7, 18542964.
45. Henry SA, Kohlwein SD, Carman GM. Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics 2012, 190:317-349. 10.1534/genetics.111.130286, 3276621, 22345606.
46. Hirst J, King MS, Pryde KR. The production of reactive oxygen species by complex I. Biochem Soc Trans 2008, 36:976-80. 10.1042/BST0360976, 18793173.
47. Bai RK, Perng CL, Hsu CH, Wong LJC. Quantitative PCR analysis of mitochondrial DNA content in patients with mitochondrial disease. Ann N Y Acad Sci 2004, 41011:304-309.
48. Kelly RDW, Mahmud A, McKenzie M, Trounce IA, St Joh JC. Mitochondrial DNA copy number is regulated in a tissue specific manner by DNA methylation of the nuclear-encoded DNA polymerase gamma A. Nucleic Acids Res 2012, 40:10124-10138. 10.1093/nar/gks770, 3488228, 22941637.