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Same but not alike: Structure, flexibility and energetics of domains in multi-domain proteins are influenced by the presence of other domains

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  • Sneha Vishwanath
  • Alexandre G de Brevern
  • Narayanaswamy Srinivasan

Abstract

The majority of the proteins encoded in the genomes of eukaryotes contain more than one domain. Reasons for high prevalence of multi-domain proteins in various organisms have been attributed to higher stability and functional and folding advantages over single-domain proteins. Despite these advantages, many proteins are composed of only one domain while their homologous domains are part of multi-domain proteins. In the study presented here, differences in the properties of protein domains in single-domain and multi-domain systems and their influence on functions are discussed. We studied 20 pairs of identical protein domains, which were crystallized in two forms (a) tethered to other proteins domains and (b) tethered to fewer protein domains than (a) or not tethered to any protein domain. Results suggest that tethering of domains in multi-domain proteins influences the structural, dynamic and energetic properties of the constituent protein domains. 50% of the protein domain pairs show significant structural deviations while 90% of the protein domain pairs show differences in dynamics and 12% of the residues show differences in the energetics. To gain further insights on the influence of tethering on the function of the domains, 4 pairs of homologous protein domains, where one of them is a full-length single-domain protein and the other protein domain is a part of a multi-domain protein, were studied. Analyses showed that identical and structurally equivalent functional residues show differential dynamics in homologous protein domains; though comparable dynamics between in-silico generated chimera protein and multi-domain proteins were observed. From these observations, the differences observed in the functions of homologous proteins could be attributed to the presence of tethered domain. Overall, we conclude that tethered domains in multi-domain proteins not only provide stability or folding advantages but also influence pathways resulting in differences in function or regulatory properties.Author summary: High prevalence of multi-domain proteins in proteomes has been attributed to higher stability and functional and folding advantages of the multi-domain proteins. Influence of tethering of domains on the overall properties of proteins has been well studied but its influence on the properties of the constituent domains is largely unaddressed. Here, we investigate the influence of tethering of domains in multi-domain proteins on the structural, dynamics and energetics properties of the constituent domains and its implications on the functions of proteins. To this end, comparative analyses were carried out for identical protein domains crystallized in tethered and untethered forms. Also, comparative analyses of single-domain proteins and their homologous multi-domain proteins were performed. The analyses suggest that tethering influences the structural, dynamic and energetic properties of constituent protein domains. Our observations hint at regulation of protein domains by tethered domains in multi-domain systems, which may manifest at the differential function observed between single-domain and homologous multi-domain proteins.

Suggested Citation

  • Sneha Vishwanath & Alexandre G de Brevern & Narayanaswamy Srinivasan, 2018. "Same but not alike: Structure, flexibility and energetics of domains in multi-domain proteins are influenced by the presence of other domains," PLOS Computational Biology, Public Library of Science, vol. 14(2), pages 1-26, February.
  • Handle: RePEc:plo:pcbi00:1006008
    DOI: 10.1371/journal.pcbi.1006008
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    1. Bin Qian & Srivatsan Raman & Rhiju Das & Philip Bradley & Airlie J. McCoy & Randy J. Read & David Baker, 2007. "High-resolution structure prediction and the crystallographic phase problem," Nature, Nature, vol. 450(7167), pages 259-264, November.
    2. P. Robert & Y. Escoufier, 1976. "A Unifying Tool for Linear Multivariate Statistical Methods: The RV‐Coefficient," Journal of the Royal Statistical Society Series C, Royal Statistical Society, vol. 25(3), pages 257-265, November.
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    1. Willow Coyote-Maestas & David Nedrud & Antonio Suma & Yungui He & Kenneth A. Matreyek & Douglas M. Fowler & Vincenzo Carnevale & Chad L. Myers & Daniel Schmidt, 2021. "Probing ion channel functional architecture and domain recombination compatibility by massively parallel domain insertion profiling," Nature Communications, Nature, vol. 12(1), pages 1-16, December.

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