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Relationship between regulatory pattern of gene expression level and gene function

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  • Masayo Inoue
  • Katsuhisa Horimoto

Abstract

Regulation of gene expression levels is essential for all living systems and transcription factors (TFs) are the main regulators of gene expression through their ability to repress or induce transcription. A balance between synthesis and degradation rates controls gene expression levels. To determine which rate is dominant, we analyzed the correlation between expression levels of a TF and its regulated gene based on a mathematical model. We selected about 280,000 expression patterns of 355 TFs and 647 regulated genes using DNA microarray data from the Gene Expression Omnibus (GEO) data repository. Based on our model, correlation between the expressions of TF–regulated gene pairs corresponds to tuning of the synthesis rate, whereas no correlation indicates excessive synthesis and requires tuning of the degradation rate. The gene expression relationships between TF–regulated gene pairs were classified into four types that correspond to different gene regulatory mechanisms. It was surprising that fewer than 20% of these genes were governed by the familiar regulatory mechanism, i.e., through the synthesis rate. Moreover, we performed pathway analysis and found that each classification type corresponded to distinct gene functions: cellular regulation pathways were dominant in the type with synthesis rate regulation and terms associated with diseases such as cancer, Parkinson’s disease, and Alzheimer’s disease were dominant in the type with degradation rate regulation. Interestingly, these diseases are caused by the accumulation of proteins. These results indicated that gene expression is regulated structurally, not arbitrarily, according to the gene function. This funding is indicative of a systematic control of transcription processes at the whole-cell level.

Suggested Citation

  • Masayo Inoue & Katsuhisa Horimoto, 2017. "Relationship between regulatory pattern of gene expression level and gene function," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-14, May.
  • Handle: RePEc:plo:pone00:0177430
    DOI: 10.1371/journal.pone.0177430
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    References listed on IDEAS

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    1. Michael H. G. Kubbutat & Stephen N. Jones & Karen H. Vousden, 1997. "Regulation of p53 stability by Mdm2," Nature, Nature, vol. 387(6630), pages 299-303, May.
    2. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    3. Jeffrey A. Lefstin & Keith R. Yamamoto, 1998. "Allosteric effects of DNA on transcriptional regulators," Nature, Nature, vol. 392(6679), pages 885-888, April.
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