Transcription factor control of growth rate dependent genes in Saccharomyces cerevisiae: A three factor design

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Fazio, Alessandro ^a   Jewett, Michael C ^a,c   Daran Lapujade, Pascale ^b   Mustacchi, Roberta ^a   Usaite, Renata ^a   Pronk, Jack T ^b   Workman, Christopher T ^a   Nielsen, Jens ^a,d  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c HARVARD MEDICAL SCHOOL   (United States)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; OXYGEN; PROTEIN ACE2; PROTEIN FHL1; PROTEIN SFP1; PROTEIN SWI6; RAP1 PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR YAP1; CARBON; FUNGAL RNA; NITROGEN;

ARTICLE; CELL CYCLE REGULATION; CELL GROWTH; CHEMOSTAT; CONTROLLED STUDY; FUNGUS CULTURE; GENE EXPRESSION; GENE TARGETING; GENETIC IDENTIFICATION; GROWTH RATE; GROWTH REGULATION; NONHUMAN; NUTRIENT LIMITATION; RNA ANALYSIS; RNA METABOLISM; SACCHAROMYCES CEREVISIAE; STEADY STATE; TRANSCRIPTION REGULATION; UPREGULATION; AEROBIC METABOLISM; ANAEROBIC GROWTH; DNA MICROARRAY; FUNGAL GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

SACCHAROMYCES CEREVISIAE;

AEROBIOSIS; ANAEROBIOSIS; CARBON; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; NITROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 49049097132     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-341     Document Type: Article

References (59)

1. DeRisi JL Iyer VR Brown PO Exploring the metabolic and genetic control of gene expression on a genomic scale Science 1997, 278(5338):680-686. 9381177 10.1126/science.278.5338.680
2. Wodicka L Dong H Mittmann M Ho MH Lockhart DJ Genome-wide expression monitoring in Saccharomyces cerevisiae Nat Biotechnol 1997, 15(13):1359-1367. 10.1038/nbt1297-1359 9415887
3. Boer VM de Winde JH Pronk JT Piper MD The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur J Biol Chem 2003, 278(5):3265-3274. 10.1074/jbc.M209759200 12414795
4. Wu J Zhang N Hayes A Panoutsopoulou K Oliver SG Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth and starvation Proc Natl Acad Sci U S A 2004, 101(9):3148-3153. 10.1073/pnas.0308321100 14973188 365758
5. Usaite R Patil KR Grotkjaer T Nielsen J Regenberg B Global transcriptional and physiological responses of Saccharomyces cerevisiae to ammonium, L-alanine, or L-glutamine limitation Appl Environ Microbiol 2006, 72(9):6194-6203. 10.1128/AEM.00548-06 16957246 1563674
6. ter Linde JJ Liang H Davis RW Steensma HY van Dijken JP Pronk JT Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae J Bacteriol 1999, 181(24):7409-7413. 94195 10601195
7. Piper MD Daran-Lapujade P Bro C Regenberg B Knudsen S Nielsen J Pronk JT Reproducibility of oligonucleotide microarray transcriptome analyses. An interlaboratory comparison using chemostat cultures of Saccharomyces cerevisiae J Biol Chem 2002, 277(40):37001-37008. 10.1074/jbc.M204490200 12121991
8. Tai SL Boer VM Daran-Lapujade P Walsh MC de Winde JH Daran JM Pronk JT Two-dimensional transcriptome analysis in chemostat cultures. Combinatorial effects of oxygen availability and macronutrient limitation in Saccharomyces cerevisiae J Biol Chem 2005, 280(1):437-447. 15496405
9. Hayes A Zhang N Wu J Butler PR Hauser NC Hoheisel JD Lim FL Sharrocks AD Oliver SG Hybridization array technology coupled with chemostat culture: Tools to interrogate gene expression in Saccharomyces cerevisiae Methods 2002, 26(3):281-290. 10.1016/S1046-2023(02)00032-4 12054884
10. Daran-Lapujade P Jansen ML Daran JM van Gulik W de Winde JH Pronk JT Role of transcriptional regulation in controlling fluxes in central carbon metabolism of Saccharomyces cerevisiae. A chemostat culture study J Biol Chem 2004, 279(10):9125-9138. 10.1074/jbc.M309578200 14630934
11. Hoskisson PA Hobbs G Continuous culture - making a comeback? Microbiology 2005, 151(Pt 10):3153-3159. 16207900 10.1099/mic.0.27924-0
12. Regenberg B Grotkjaer T Winther O Fausboll A Akesson M Bro C Hansen LK Brunak S Nielsen J Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae Genome Biol 2006, 7(11):R107. 10.1186/gb-2006-7-11-r107 17105650 1794586
13. Castrillo JI Zeef LA Hoyle DC Zhang N Hayes A Gardner DC Cornell MJ Petty J Hakes L Wardleworth L Rash B Brown M Dunn WB Broadhurst D O'Donoghue K Hester SS Dunkley TP Hart SR Swainston N Li P Gaskell SJ Paton NW Lilley KS Kell DB Oliver SG Growth control of the eukaryote cell: A systems biology study in yeast J Biol 2007, 6(2):4. 17439666 10.1186/jbiol54 2373899
14. Brauer MJ Huttenhower C Airoldi EM Rosenstein R Matese JC Gresham D Boer VM Troyanskaya OG Botstein D Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast Mol Biol Cell 2008, 19(1):352-367. 17959824 10.1091/mbc.E07-08-0779 2174172
15. Pir P Kirdar B Hayes A Onsan ZY Ulgen KO Oliver SG Integrative investigation of metabolic and transcriptomic data BMC Bioinformatics 2006, 7:203. 16611354 10.1186/1471-2105-7-203 1481621
16. Xie Y Varshavsky A RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: A negative feedback circuit Proc Natl Acad Sci U S A 2001, 98(6):3056-3061. 11248031 10.1073/pnas.071022298 30606
17. Hanna J Finley D A proteasome for all occasions FEBS Lett 2007, 581(15):2854-2861. 17418826 10.1016/j.febslet.2007.03.053 1965587
18. Patil KR Nielsen J Uncovering transcriptional regulation of metabolism by using metabolic network topology Proc Natl Acad Sci U S A 2005, 102(8):2685-2689. 15710883 10.1073/pnas.0406811102 549453
19. Nielsen J Jewett MC Impact of systems biology on metabolic engineering of Saccharomyces cerevisiae FEMS Yeast Res 2008, 8(1):122-131. 17727659
20. Beyer A Workman C Hollunder J Radke D Moller U Wilhelm T Ideker T Integrated assessment and prediction of transcription factor binding PLoS Comput Biol 2006, 2(6):e70. 16789814 10.1371/journal.pcbi.0020070 1479087
21. Harbison CT Gordon DB Lee TI Rinaldi NJ Macisaac KD Danford TW Hannett NM Tagne JB Reynolds DB Yoo J Jennings EG Zeitlinger J Pokholok DK Kellis M Rolfe PA Takusagawa KT Lander ES Gifford DK Fraenkel E Young RA Transcriptional regulatory code of a eukaryotic genome Nature 2004, 431(7004):99-104. 15343339 10.1038/nature02800
22. Warner JR The economics of ribosome biosynthesis in yeast Trends Biochem Sci 1999, 24(11):437-440. 10542411 10.1016/S0968-0004(99)01460-7
23. Morse RH RAP, RAP, open up! New wrinkles for RAP1 in yeast Trends Genet 2000, 16(2):51-53. 10652526 10.1016/S0168-9525(99)01936-8
24. Lieb JD Liu X Botstein D Brown PO Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association Nat Genet 2001, 28(4):327-334. 11455386 10.1038/ng569
25. Kraakman LS Griffioen G Zerp S Groeneveld P Thevelein JM Mager WH Planta RJ Growth-related expression of ribosomal protein genes in Saccharomyces cerevisiae Mol Gen Genet 1993, 239(1-2):196-204. 8389977
26. Lee TI Rinaldi NJ Robert F Odom DT Bar-Joseph Z Gerber GK Hannett NM Harbison CT Thompson CM Simon I Zeitlinger J Jennings EG Murray HL Gordon DB Ren B Wyrick JJ Tagne JB Volkert TL Fraenkel E Gifford DK Young RA Transcriptional regulatory networks in Saccharomyces cerevisiae Science 2002, 298(5594):799-804. 10.1126/science.1075090 12399584
27. Schawalder SB Kabani M Howald I Choudhury U Werner M Shore D Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1 Nature 2004, 432(7020):1058-1061. 15616569 10.1038/ nature03200
28. Wade JT Hall DB Struhl K The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes Nature 2004, 432(7020):1054-1058. 15616568 10.1038/nature03175
29. Rudra D Zhao Y Warner JR Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins Embo J 2005, 24(3):533-542. 15692568 10.1038/sj.emboj.7600553 548658
30. Simon I Barnett J Hannett N Harbison CT Rinaldi NJ Volkert TL Wyrick JJ Zeitlinger J Gifford DK Jaakkola TS Young RA Serial regulation of transcriptional regulators in the yeast cell cycle Cell 2001, 106(6):697-708. 11572776 10.1016/S0092-8674(01)00494-9
31. Horak CE Luscombe NM Qian J Bertone P Piccirrillo S Gerstein M Snyder M Complex transcriptional circuitry at the G1/S transition in Saccharomyces cerevisiae Genes Dev 2002, 16(23):3017-3033. 10.1101/ gad.1039602 12464632 187492
32. Laabs TL Markwardt DD Slattery MG Newcomb LL Stillman DJ Heideman W ACE2 is required for daughter cell-specific G1 delay in Saccharomyces cerevisiae Proc Natl Acad Sci U S A 2003, 100(18):10275-10280. 10.1073/ pnas.1833999100 12937340 193551
33. Ho Y Gruhler A Heilbut A Bader GD Moore L Adams SL Millar A Taylor P Bennett K Boutilier K Yang L Wolting C Donaldson I Schandorff S Shewnarane J Vo M Taggart J Goudreault M Muskat B Alfarano C Dewar D Lin Z Michalickova K Willems AR Sassi H Nielsen PA Rasmussen KJ Andersen JR Johansen LE Hansen LH Jespersen H Podtelejnikov A Nielsen E Crawford J Poulsen V Sorensen BD Matthiesen J Hendrickson RC Gleeson F Pawson T Moran MF Durocher D Mann M Hogue CW Figeys D Tyers M Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry Nature 2002, 415(6868):180-183. 10.1038/415180a 11805837
34. Kasten MM Stillman DJ Identification of the Saccharomyces cerevisiae genes STB1-STB5 encoding Sin3p binding proteins Mol Gen Genet 1997, 256(4):376-386. 10.1007/s004380050581 9393435
35. Jorgensen P Rupes I Sharom JR Schneper L Broach JR Tyers M A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size Genes Dev 2004, 18(20):2491-2505. 15466158 10.1101/gad.1228804 529537
36. Marion RM Regev A Segal E Barash Y Koller D Friedman N O'Shea EK Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression Proc Natl Acad Sci U S A 2004, 101(40):14315-14322. 15353587 10.1073/pnas.0405353101 521938
37. Jorgensen P Nishikawa JL Breitkreutz BJ Tyers M Systematic identification of pathways that couple cell growth and division in yeast Science 2002, 297(5580):395-400. 12089449 10.1126/science.1070850
38. Cipollina C Alberghina L Porro D Vai M SFP1 is involved in cell size modulation in respiro-fermentative growth conditions Yeast 2005, 22(5):385-399. 15806610 10.1002/yea.1218
39. Jorgensen P Tyers M How cells coordinate growth and division Curr Biol 2004, 14(23):R1014-27. 15589139 10.1016/j.cub.2004.11.027
40. Temple MD Perrone GG Dawes IW Complex cellular responses to reactive oxygen species Trends Cell Biol 2005, 15(6):319-326. 15953550 10.1016/ j.tcb.2005.04.003
41. Chua G Morris QD Sopko R Robinson MD Ryan O Chan ET Frey BJ Andrews BJ Boone C Hughes TR Identifying transcription factor functions and targets by phenotypic activation Proc Natl Acad Sci U S A 2006, 103(32):12045-12050. 16880382 10.1073/pnas.0605140103 1567694
42. Mendizabal I Rios G Mulet JM Serrano R de Larrinoa IF Yeast putative transcription factors involved in salt tolerance FEBS Lett 1998, 425(2):323-328. 9559673 10.1016/S0014-5793(98)00249-X
43. Steinfeld I Shamir R Kupiec M A genome-wide analysis in Saccharomyces cerevisiae demonstrates the influence of chromatin modifiers on transcription Nat Genet 2007, 39(3):303-309. 10.1038/ng1965 17325681
44. DeRisi J van den Hazel B Marc P Balzi E Brown P Jacq C Goffeau A Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants FEBS Lett 2000, 470(2):156-160. 10734226 10.1016/S0014-5793(00)01294-1
45. Workman CT Mak HC McCuine S Tagne JB Agarwal M Ozier O Begley TJ Samson LD Ideker T A systems approach to mapping DNA damage response pathways Science 2006, 312(5776):1054-1059. 16709784 10.1126/science.1122088
46. Grotkjaer T Winther O Regenberg B Nielsen J Hansen LK Robust multi-scale clustering of large DNA microarray datasets with the consensus algorithm Bioinformatics 2006, 22(1):58-67. 16257984 10.1093/bioinformatics/bti746
47. van Dijken JP Bauer J Brambilla L Duboc P Francois JM Gancedo C Giuseppin ML Heijnen JJ Hoare M Lange HC Madden EA Niederberger P Nielsen J Parrou JL Petit T Porro D Reuss M van Riel N Rizzi M Steensma HY Verrips CT Vindelov J Pronk JT An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains Enzyme Microb Technol 2000, 26(9-10):706-714. 10.1016/ S0141-0229(00)00162-9 10862876
48. Affymetrix Affymetrix GeneChip Expression Analysis Technical Manual. Affymetrix, Santa Clara, CA
49. Gautier L Cope L Bolstad BM Irizarry RA Affy - analysis of Affymetrix GeneChip data at the probe level Bioinformatics 2004, 20(3):307-315. 14960456 10.1093/bioinformatics/btg405
50. Wu Z Irizarry RA Gentleman R Martínez-Murillo F Spencer F A model based background adjustment for oligonucleotide expression arrays Johns Hopkins University, Dept of Biostatistics Working Papers Working Paper 1 2004. http://www.bepress.com/cgi/viewcontent.cgi?article= 1001&context=jhubiostat
51. Workman C Jensen LJ Jarmer H Berka R Gautier L Nielser HB Saxild HH Nielsen C Brunak S Knudsen S A new non-linear normalization method for reducing variability in DNA microarray experiments Genome Biol 2002, 3(9):rEsearch0048. 12225587 10.1186/gb-2002-3-9-research0048 126873
52. Irizarry RA Hobbs B Collin F Beazer-Barclay YD Antonellis KJ Scherf U Speed TP Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 2003, 4(2):249-264. 12925520 10.1093/biostatistics/4.2.249
53. Churchill GA Using ANOVA to analyze microarray data Biotechniques 2004, 37(2):173- 5, 177. 15335204
54. Cui X Hwang JT Qiu J Blades NJ Churchill GA Improved statistical tests for differential gene expression by shrinking variance components estimates Biostatistics 2005, 6(1):59-75. 15618528 10.1093/biostatistics/ kxh018
55. Storey JD Tibshirani R Statistical significance for genomewide studies Proc Natl Acad Sci U S A 2003, 100(16):9440-9445. 12883005 10.1073/ pnas.1530509100 170937
56. Benjamini Y Hochberg Y Controlling the False Discovery Rate: A practical and powerful approach to multiple testing J R Statist Soc B 1995, 57(1):289-300. http://www.biostat.jhsph.edu/~yonchen/ Controlling%20the%20false%20discovery%20rate.pdf
57. Dwight SS Harris MA Dolinski K Ball CA Binkley G Christie KR Fisk DG Issel-Tarver L Schroeder M Sherlock G Sethuraman A Weng S Botstein D Cherry JM Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO) Nucleic Acids Res 2002, 30(1):69-72. 11752257 10.1093/nar/30.1.69 99086
58. Stark C Breitkreutz BJ Reguly T Boucher L Breitkreutz A Tyers M BioGRID: a general repository for interaction datasets Nucleic Acids Res 2006, 34(Database issue):D535-9. 16381927 10.1093/nar/gkj109 1347471
59. Shannon P Markiel A Ozier O Baliga NS Wang JT Ramage D Amin N Schwikowski B Ideker T Cytoscape: A software environment for integrated models of biomolecular interaction networks Genome Res 2003, 13(11):2498-2504. 14597658 10.1101/gr.1239303 403769