Functional and topological characterization of transcriptional cooperativity in yeast

BMC Research Notes

Baldo Oliva¹  Daniel Aguilar¹ 

[1] Structural Bioinformatics Group (GRIB/IMIM), Departament de Ciencies Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona Biomedical Research Park (PRBB), c/Dr. Aiguader 88, 08003, Barcelona, Spain

关键词: Transcriptional cooperativity;    Gene expression;    Gene regulation;    Transcription factor;    Regulatory network;   

Others  :  1166440
DOI  :  10.1186/1756-0500-5-227

 received in 2012-02-09, accepted in 2012-04-27,  发布年份 2012

【 摘 要 】

Background

Many cellular programs are regulated through the integration of specific transcriptional signals originated from external stimuli, being cooperation between transcription factors a key feature in this process. In this work, we studied how transcriptional cooperativity in yeast is aimed at integrating different regulatory inputs rather than controlling particular cellular functions from a organizational, evolutionary and functional point of view.

Findings

Our results showed that cooperative transcription factor pairs co-evolve and are essential for the life of the cell. When organized into a layered regulatory network, we observed that cooperative transcription factors were preferentially placed in the middle layers, which highlights a role in regulatory signal integration. We also observed significant co-activity and co-evolution between members of the same cooperative pairs, but a lack of common co-expression profile.

Conclusions

Our results suggest that transcriptional cooperativity has a specific role within the regulatory control scheme of the cell, focused in the amplification and integration of cellular signals rather than control of particular cellular functions. This information can be used for better characterization of regulatory interactions between transcription factors, aimed at determining the spatial and temporal control of gene expression.

【 授权许可】

   
2012 Aguilar and Oliva; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Miller JA, Widom J: Collaborative competition mechanism for gene activation in vivo. Mol Cell Biol 2003, 23:1623-1632.
• [2]Remenyi A, Scholer HR, Wilmanns M: Combinatorial control of gene expression. Nat Struct Mol Biol 2004, 11:812-815.
• [3]Chen L, Glover JN, Hogan PG, Rao A, Harrison SC: Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature 1998, 392:42-48.
• [4]Tan S, Richmond TJ: Eukaryotic transcription factors. Curr Opin Struct Biol 1998, 8:41-48.
• [5]Davidson EH: Genomic regulatory systems: development and evolution. San Diego, CA, USA: Academic; 2001.
• [6]Nagamine N, Kawada Y, Sakakibara Y: Identifying cooperative transcriptional regulations using protein-protein interactions. Nucleic Acids Res 2005, 33:4828-4837.
• [7]Banerjee N, Zhang MQ: Identifying cooperativity among transcription factors controlling the cell cycle in yeast. Nucleic Acids Res 2003, 31:7024-7031.
• [8]Chang YH, Wang YC, Chen BS: Identification of transcription factor cooperativity via stochastic system model. Bioinformatics 2006, 22:2276-2282.
• [9]Tsai HK, Lu HH, Li WH: Statistical methods for identifying yeast cell cycle transcription factors. Proc Natl Acad Sci USA 2005, 102:13532-13537.
• [10]Aguilar D, Oliva B: Topological comparison of methods for predicting transcriptional cooperativity in yeast. BMC Genomics 2008, 9:137. BioMed Central Full Text
• [11]Yu H, Gerstein M: Genomic analysis of the hierarchical structure of regulatory networks. Proc Natl Acad Sci U S A 2006, 103:14724-14731.
• [12]Jovelin R, Phillips PC: Evolutionary rates and centrality in the yeast gene regulatory network. Genome Biol 2009, 10:R35. BioMed Central Full Text
• [13]Goh C, Bogan A, Joachimiak M, Walther D, Cohen F: Co-evolution of proteins with their interaction partners. J Mol Biol 2000, 299:283-293.
• [14]Koretke K, Lupas A, Warren P, Rosenberg M, Brown J: Evolution of two-component signal transduction. Mol Biol Evol 2000, 17:1956-1970.
• [15]Amorim MJ, Cotobal C, Duncan C, Mata J: Global coordination of transcriptional control and mRNA decay during cellular differentiation. Mol Syst Biol 2010, 6:380.
• [16]Pál C, Papp B, Hurst LD: Highly expressed genes in yeast evolve slowly. Genetics 2001, 158:927-931.
• [17]Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH: Why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A 2005, 102:14338-14343.
• [18]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:e70.
• [19]Bhardwaj N, Kim PM, Gerstein M: Rewiring of transcriptional regulatory networks: hierarchy, rather than connectivity, better reflects the importance of regulators. Sci Signal 2010, 3:ra79.
• [20]DeRisi JL, Iyer VR, Brown PO: Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 1997, 278:680-686.
• [21]Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabrielian AE, Landsman D, Lockhart DJ, Davis RW: A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 1998, 2:65-73.
• [22]Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I: The transcriptional program of sporulation in budding yeast. Science 1998, 282:699-705.
• [23]Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA: Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 2001, 12:323-337.
• [24]Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA: Dissecting the regulatory circuitry of a eukaryotic genome. Cell 1998, 95:717-728.
• [25]Boorsma A, Lu XJ, Zakrzewska A, Klis FM, Bussemaker HJ: Inferring condition-specific modulation of transcription factor activity in yeast through regulon-based analysis of genomewide expression. PLoS One 2008, 3:e3112.
• [26]Quackenbush J: Computational analysis of microarray data. Nat Rev Genet 2001, 2:418-427. Review
• [27]Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, González JR, Gratacòs M, Huang J, Kalaitzopoulos D, Komura D, MacDonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, Zhang J, Zerjal T, Zhang J, Armengol L, Conrad DF, Estivill X, Tyler-Smith C, Carter NP, Aburatani H, Lee C, Jones KW, Scherer SW, Hurles ME: Global variation in copy number in the human genome. Nature 2006, 444:444-454.
• [28]Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, et al.: Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999, 285:901-906.
• [29]Stark C, Breitkreutz BJ, Chatr-Aryamontri A, Boucher L, Oughtred R, Livstone MS, Nixon J, Van Auken K, Wang X, Shi X, Reguly T, Rust JM, Winter A, Dolinski K, Tyers M: The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 2011, 39:D698-704.
• [30]Xia Y, Franzosa EA, Gerstein MB: Integrated assessment of genomic correlates of protein evolutionary rate. PLoS Comput Biol 2009, 5:e1000413.
• [31]Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW: The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 2004, 32:5539-5545.
• [32]Gene Ontology Consortium: The Gene Ontology: enhancements for 2011. Nucleic Acids Res 2012, 40:D559-D564.
• [33]R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2010.