Novel insights into iron metabolism by integrating deletome and transcriptome analysis in an iron deficiency model of the yeast Saccharomyces cerevisiae

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Jo, William J ^a   Hyoun, Jeung Hyoun ^a   Oh, Eric ^a   Jaramillo, Daniel ^b   Holman, Patricia ^a   Loguinov, Alex V ^a   Arkin, Adam P ^c,d   Nislow, Corey ^e,f   Giaever, Guri ^e,f   Vulpe, Chris D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of California at Berkeley   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DELETOME; GENE PRODUCT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CT16; TRANSCRIPTION FACTOR DAP1; TRANSCRIPTION FACTOR MRS4; TRANSCRIPTION FACTOR YHR045W; TRANSCRIPTOME; UNCLASSIFIED DRUG; FUNGAL DNA; IRON; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE INTERACTION; GENE MUTATION; GENE REGULATORY NETWORK; GENETIC ANALYSIS; GENETIC IDENTIFICATION; GENETIC TRANSCRIPTION; HOMOZYGOSITY; IRON DEFICIENCY; IRON METABOLISM; IRON TRANSPORT; NONHUMAN; PEROXISOME; SACCHAROMYCES CEREVISIAE; CLUSTER ANALYSIS; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

SACCHAROMYCES CEREVISIAE;

CLUSTER ANALYSIS; DNA, FUNGAL; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENOME, FUNGAL; IRON; PEROXISOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 64849099555     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-130     Document Type: Article

References (51)

1. Yip R Iron deficiency: Contemporary scientific issues and international programmatic approaches The Journal of nutrition 1994, 124(8 Suppl):1479S-1490S 8064407
2. De Freitas J Wintz H Kim JH Poynton H Fox T Vulpe C Yeast, a model organism for iron and copper metabolism studies Biometals 2003, 16(1):185-197 10.1023/A:1020771000746 12572678
3. Kaplan J McVey Ward D Crisp RJ Philpott CC Iron-dependent metabolic remodeling in S. cerevisiae Biochimica et biophysica acta 2006, 1763(7):646-651 16697062
4. Yamaguchi-Iwai Y Dancis A Klausner RD AFT1: A mediator of iron regulated transcriptional control in Saccharomyces cerevisiae Embo Journal 1995, 14(6):1231-1239 398200 7720713
5. Yamaguchi-Iwai Y Ueta R Fukunaka A Sasaki R Subcellular localization of Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae J Biol Chem 2002, 277(21):18914-18918 10.1074/jbc.M200949200 11877447
6. Shakoury-Elizeh M Tiedeman J Rashford J Ferea T Demeter J Garcia E Rolfes R Brown PO Botstein D Philpott CC Transcriptional remodeling in response to iron deprivation in Saccharomyces cerevisiae Mol Biol Cell 2004, 15(3):1233-1243 363115 14668481 10.1091/mbc.E03-09-0642
7. Blaiseau PL Lesuisse E Camadro JM Aft2p, a novel iron-regulated transcription activator that modulates, with Aft1p, intracellular iron use and resistance to oxidative stress in yeast Journal of Biological Chemistry 2001, 276(36):34221-34226 10.1074/jbc.M104987200 11448968
8. Rutherford JC Jaron S Ray E Brown PO Winge DR A second iron-regulatory system in yeast independent of Aft1p Proceedings of the National Academy of Sciences of the United States of America 2001, 98(25):14322-14327 64680 11734641 10.1073/pnas.261381198
9. Rutherford JC Ojeda L Balk J Muhlenhoff U Lill R Winge DR Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis J Biol Chem 2005, 280(11):10135-10140 10.1074/jbc.M413731200 15649888
10. Puig S Askeland E Thiele DJ Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation Cell 2005, 120(1):99-110 10.1016/j.cell.2004.11.032 15652485
11. Puig S Vergara SV Thiele DJ Cooperation of two mRNA-binding proteins drives metabolic adaptation to iron deficiency Cell metabolism 2008, 7(6):555-564 10.1016/j.cmet.2008.04.010 18522836
12. Felice MR De Domenico I Li L Ward DM Bartok B Musci G Kaplan J Post-transcriptional regulation of the yeast high affinity iron transport system The Journal of biological chemistry 2005, 280(23):22181-22190 10.1074/jbc.M414663200 15817488
13. Winzeler EA Shoemaker DD Astromoff A Liang H Anderson K Andre B Bangham R Benito R Boeke JD Bussey H et al Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis Science 1999, 285(5429):901-906 10.1126/science.285.5429.901 10436161
14. Davis-Kaplan SR Ward DM Shiflett SL Kaplan J Genome-wide analysis of iron-dependent growth reveals a novel yeast gene required for vacuolar acidification J Biol Chem 2004, 279(6):4322-4329 10.1074/jbc.M310680200 14594803
15. Dudley AM Janse DM Tanay A Shamir R Church GM A global view of pleiotropy and phenotypically derived gene function in yeast Mol Syst Biol 2005, 1(1):mSb4100004 E4100001 10.1038/msb4100004
16. Lesuisse E Knight SA Courel M Santos R Camadro JM Dancis A Genome-wide screen for genes with effects on distinct iron uptake activities in Saccharomyces cerevisiae Genetics 2005, 169(1):107-122 1448889 15489514 10.1534/genetics.104.035873
17. Shoemaker DD Lashkari DA Morris D Mittmann M Davis RW Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar-coding strategy Nat Genet 1996, 14(4):450-456 10.1038/ ng1296-450 8944025
18. Giaever G Chu AM Ni L Connelly C Riles L Veronneau S Dow S Lucau-Danila A Anderson K Andre B et al Functional profiling of the Saccharomyces cerevisiae genome Nature 2002, 418(6896):387-391 10.1038/nature00935 12140549
19. Jo WJ Loguinov A Chang M Wintz H Nislow C Arkin AP Giaever G Vulpe CD Identification of genes involved in the toxic response of Saccharomyces cerevisiae against iron and copper overload by parallel analysis of deletion mutants Toxicol Sci 2008, 101(1):140-151 10.1093/toxsci/kfm226 17785683
20. Loguinov AV Mian IS Vulpe CD Exploratory differential gene expression analysis in microarray experiments with no or limited replication Genome Biol 2004, 5(3):R18 395768 15003121 10.1186/gb-2004-5-3-r18
21. Eason RG Pourmand N Tongprasit W Herman ZS Anthony K Jejelowo O Davis RW Stolc V Characterization of synthetic DNA bar codes in Saccharomyces cerevisiae gene-deletion strains Proc Natl Acad Sci USA 2004, 101(30):11046-11051 491991 15258289 10.1073/pnas.0403672101
22. Jo WJ Loguinov A Chang M Wintz H Nislow C Arkin AP Giaever G Vulpe CD Identification of Genes Involved in the Toxic Response of Saccharomyces cerevisiae against Iron and Copper Overload by Parallel Analysis of Deletion Mutants Toxicol Sci 2007, 17785683
23. Kiemer L Costa S Ueffing M Cesareni G WI-PHI: A weighted yeast interactome enriched for direct physical interactions Proteomics 2007, 7(6):932-943 10.1002/pmic.200600448 17285561
24. Teixeira MC Monteiro P Jain P Tenreiro S Fernandes AR Mira NP Alenquer M Freitas AT Oliveira AL Sa-Correia I The YEASTRACT database: A tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae Nucleic acids research 2006, 34 Database D446-451 1347376 16381908 10.1093/nar/gkj013
25. Ideker T Ozier O Schwikowski B Siegel AF Discovering regulatory and signalling circuits in molecular interaction networks Bioinformatics (Oxford, England) 2002, 18(Suppl 1):S233-240 12169552
26. Philpott CC Protchenko O Kim YW Boretsky Y Shakoury-Elizeh M The response to iron deprivation in Saccharomyces cerevisiae: Expression of siderophore-based systems of iron uptake Biochem Soc Trans 2002, 30(4):698-702 10.1042/BST0300698 12196168
27. Protchenko O Ferea T Rashford J Tiedeman J Brown PO Botstein D Philpott CC Three cell wall mannoproteins facilitate the uptake of iron in Saccharomyces cerevisiae J Biol Chem 2001, 276(52):49244-49250 10.1074/ jbc.M109220200 11673473
28. Yun CW Tiedeman JS Moore RE Philpott CC Siderophore-iron uptake in Saccharomyces cerevisiae - Identification of ferrichrome and fusarinine transporters Journal of Biological Chemistry 2000, 275(21):16354-16359 10.1074/jbc.M001456200 10748025
29. De Freitas JM Kim JH Poynton H Su T Wintz H Fox T Holman P Loguinov A Keles S Laan van der M et al Exploratory and confirmatory gene expression profiling of mac1Delta J Biol Chem 2004, 279(6):4450-4458 10.1074/jbc.M212308200 14534306
30. Raguzzi F Lesuisse E Crichton RR Iron storage in Saccharomyces cerevisiae FEBS Lett 1988, 231(1):253-258 10.1016/0014-5793(88)80742-7 3282922
31. Radisky DC Snyder WB Emr SD Kaplan J Characterization of VPS41, a gene required for vacuolar trafficking and high-affinity iron transport in yeast Proc Natl Acad Sci USA 1997, 94(11):5662-5666 20835 9159129 10.1073/pnas.94.11.5662
32. Szczypka MS Zhu Z Silar P Thiele DJ Saccharomyces cerevisiae mutants altered in vacuole function are defective in copper detoxification and iron-responsive gene transcription Yeast 1997, 13(15):1423-1435 10.1002/ (SICI)1097-0061(199712)13:15<1423::AID-YEA190>3.0.CO;2-C 9434348
33. Bode HP Dumschat M Garotti S Fuhrmann GF Iron sequestration by the yeast vacuole. A study with vacuolar mutants of Saccharomyces cerevisiae Eur J Biochem 1995, 228(2):337-342 10.1111/j.1432-1033.1995.00337.x 7705347
34. Eide DJ Bridgham JT Zhao Z Mattoon JR The vacuolar H(+)-ATPase of Saccharomyces cerevisiae is required for efficient copper detoxification, mitochondrial function, and iron metabolism Mol Gen Genet 1993, 241(3-4):447-456 8246899
35. Lesuisse E Labbe P Effects of cadmium and of YAP1 and CAD1/YAP2 genes on iron metabolism in the yeast Saccharomyces cerevisiae Microbiology (Reading, England) 1995, 141(Pt 11):2937-2943 8535522
36. Wu A Wemmie JA Edgington NP Goebl M Guevara JL Moye-Rowley WS Yeast bZip proteins mediate pleiotropic drug and metal resistance The Journal of biological chemistry 1993, 268(25):18850-18858 8360174
37. Ruotolo R Marchini G Ottonello S Membrane transporters and protein traffic networks differentially affecting metal tolerance: A genomic phenotyping study in yeast Genome biology 2008, 9(4):R67 2643938 18394190 10.1186/gb-2008-9-4-r67
38. Hasan MR Koikawa S Kotani S Miyamoto S Nakagawa H Ferritin forms dynamic oligomers to associate with microtubules in vivo: Implication for the role of microtubules in iron metabolism Experimental cell research 2006, 312(11):1950-1960 10.1016/j.yexcr.2006.02.023 16603154
39. Birrell GW Brown JA Wu HI Giaever G Chu AM Davis RW Brown JM Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents Proc Natl Acad Sci USA 2002, 99(13):8778-8783 124375 12077312 10.1073/ pnas.132275199
40. Haugen AC Kelley R Collins JB Tucker CJ Deng C Afshari CA Brown JM Ideker T Van Houten B Integrating phenotypic and expression profiles to map arsenic-response networks Genome biology 2004, 5(12):R95 545798 15575969 10.1186/gb-2004-5-12-r95
41. Berry DB Gasch AP Stress-activated genomic expression changes serve a preparative role for impending stress in yeast Molecular biology of the cell 2008, 19(11):4580-4587 2575158 18753408 10.1091/mbc.E07-07-0680
42. Puig S Lau M Thiele DJ Cti6 is an Rpd3-Sin3 histone deacetylase-associated protein required for growth under iron-limiting conditions in Saccharomyces cerevisiae J Biol Chem 2004, 279(29):30298-30306 10.1074/jbc.M313463200 15133041
43. Papamichos-Chronakis M Petrakis T Ktistaki E Topalidou I Tzamarias D Cti6, a PHD domain protein, bridges the Cyc8-Tup1 corepressor and the SAGA coactivator to overcome repression at GAL1 Molecular cell 2002, 9(6):1297-1305 10.1016/S1097-2765(02)00545-2 12086626
44. Crisp RJ Adkins EM Kimmel E Kaplan J Recruitment of Tup1p and Cti6p regulates heme-deficient expression of Aft1p target genes The EMBO journal 2006, 25(3):512-521 1383541 16437160 10.1038/sj.emboj.7600961
45. Spiropoulos A Bisson LF MET17 and Hydrogen Sulfide Formation in Saccharomyces cerevisiae Appl Environ Microbiol 2000, 66(10):4421-4426 92319 11010893 10.1128/AEM.66.10.4421-4426.2000
46. Hand RA Jia N Bard M Craven RJ Saccharomyces cerevisiae Dap1p, a novel DNA damage response protein related to the mammalian membrane-associated progesterone receptor Eukaryotic cell 2003, 2(2):306-317 154842 12684380 10.1128/EC.2.2.306-317.2003
47. Craven RJ Mallory JC Hand RA Regulation of iron homeostasis mediated by the heme-binding protein Dap1 (damage resistance protein 1) via the P450 protein Erg11/Cyp51 The Journal of biological chemistry 2007, 282(50):36543-36551 10.1074/jbc.M706770200 17954932
48. Muhlenhoff U Stadler JA Richhardt N Seubert A Eickhorst T Schweyen RJ Lill R Wiesenberger G A specific role of the yeast mitochondrial carriers MRS3/4p in mitochondrial iron acquisition under iron-limiting conditions The Journal of biological chemistry 2003, 278(42):40612-40620 10.1074/jbc.M307847200 12902335
49. Zhang Y Lyver ER Knight SA Lesuisse E Dancis A Frataxin and mitochondrial carrier proteins, Mrs3p and Mrs4p, cooperate in providing iron for heme synthesis The Journal of biological chemistry 2005, 280(20):19794-19807 10.1074/jbc.M500397200 15767258
50. Zhang Y Lyver ER Knight SA Pain D Lesuisse E Dancis A Mrs3p, Mrs4p, and frataxin provide iron for Fe-S cluster synthesis in mitochondria The Journal of biological chemistry 2006, 281(32):22493-22502 10.1074/ jbc.M604246200 16769722
51. Hughes TR Yeast and drug discovery Functional & integrative genomics 2002, 2(4-5):199-211 10.1007/s10142-002-0059-1 12192593