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Research Article

Bimodal protein solubility distribution revealed by an aggregation analysis of the entire ensemble of Escherichia coli proteins

Tatsuya Niwa, Bei-Wen Ying, Katsuyo Saito, WenZhen Jin, Shoji Takada, Takuya Ueda, and Hideki Taguchi
PNAS March 17, 2009 106 (11) 4201-4206; https://doi.org/10.1073/pnas.0811922106
Tatsuya Niwa
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Bei-Wen Ying
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Katsuyo Saito
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WenZhen Jin
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Shoji Takada
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Takuya Ueda
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  • For correspondence: taguchi@k.u-tokyo.ac.jp ueda@k.u-tokyo.ac.jp
Hideki Taguchi
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  • For correspondence: taguchi@k.u-tokyo.ac.jp ueda@k.u-tokyo.ac.jp
  1. Edited by George H. Lorimer, University of Maryland, College Park, MD, and approved January 26, 2009 (received for review November 23, 2008)

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Abstract

Protein folding often competes with intermolecular aggregation, which in most cases irreversibly impairs protein function, as exemplified by the formation of inclusion bodies. Although it has been empirically determined that some proteins tend to aggregate, the relationship between the protein aggregation propensities and the primary sequences remains poorly understood. Here, we individually synthesized the entire ensemble of Escherichia coli proteins by using an in vitro reconstituted translation system and analyzed the aggregation propensities. Because the reconstituted translation system is chaperone-free, we could evaluate the inherent aggregation propensities of thousands of proteins in a translation-coupled manner. A histogram of the solubilities, based on data from 3,173 translated proteins, revealed a clear bimodal distribution, indicating that the aggregation propensities are not evenly distributed across a continuum. Instead, the proteins can be categorized into 2 groups, soluble and aggregation-prone proteins. The aggregation propensity is most prominently correlated with the structural classification of proteins, implying that the prediction of aggregation propensity requires structural information about the protein.

Keywords:
  • cell-free translation
  • protein aggregation
  • protein folding

Footnotes

  • 1To whom correspondence may be addressed at:
    University of Tokyo, Bioscience Building 401, Kashiwanoha 5-1-5, Kashiwa 277-8562, Japan.
    E-mail: taguchi{at}k.u-tokyo.ac.jp or ueda{at}k.u-tokyo.ac.jp
  • Author contributions: T.N., B.-W.Y., T.U., and H.T. designed research; T.N., B.-W.Y., and K.S. performed research; T.N. and H.T. contributed new reagents/analytic tools; T.N., B.-W.Y., W.J., S.T., T.U., and H.T. analyzed data; and T.N., S.T., T.U., and H.T. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0811922106/DCSupplemental.

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Bimodal protein solubility distribution revealed by an aggregation analysis of the entire ensemble of Escherichia coli proteins
Tatsuya Niwa, Bei-Wen Ying, Katsuyo Saito, WenZhen Jin, Shoji Takada, Takuya Ueda, Hideki Taguchi
Proceedings of the National Academy of Sciences Mar 2009, 106 (11) 4201-4206; DOI: 10.1073/pnas.0811922106

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Bimodal protein solubility distribution revealed by an aggregation analysis of the entire ensemble of Escherichia coli proteins
Tatsuya Niwa, Bei-Wen Ying, Katsuyo Saito, WenZhen Jin, Shoji Takada, Takuya Ueda, Hideki Taguchi
Proceedings of the National Academy of Sciences Mar 2009, 106 (11) 4201-4206; DOI: 10.1073/pnas.0811922106
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Proceedings of the National Academy of Sciences: 106 (11)
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