Benefits of co-translational complex assembly for cellular fitness

doi:10.1002/bies.202300024

. 2023 Mar 14;e2300024.

doi: 10.1002/bies.202300024. Online ahead of print.

Benefits of co-translational complex assembly for cellular fitness

Krishnendu Khan¹, Paul L Fox¹

Affiliations

PMID: 36916749
DOI: 10.1002/bies.202300024

Benefits of co-translational complex assembly for cellular fitness

Krishnendu Khan et al. Bioessays. 2023.

. 2023 Mar 14;e2300024.

doi: 10.1002/bies.202300024. Online ahead of print.

Authors

Krishnendu Khan¹, Paul L Fox¹

Affiliation

¹ Department of Cardiovascular and Metabolic Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio, USA.

PMID: 36916749
DOI: 10.1002/bies.202300024

Abstract

Complexes of two or more proteins form many, if not most, of the intracellular "machines" that execute physical and chemical work, and transmit information. Complexes can form from stochastic post-translational interactions of fully formed proteins, but recent attention has shifted to co-translational interactions in which the most common mechanism involves binding of a mature constituent to an incomplete polypeptide emerging from a translating ribosome. Studies in yeast have revealed co-translational interactions during formation of multiple major complexes, and together with recent mammalian cell studies, suggest widespread utilization of the mechanism. These translation-dependent interactions can involve a single or multiple mRNA templates, can be uni- or bi-directional, and can use multi-protein sub-complexes as a binding component. Here, we discuss benefits of co-translational complex assembly including accuracy and efficiency, overcoming hidden interfaces, localized and hierarchical assembly, and reduction of orphan protein degradation, toxicity, and dominant-negative pathogenesis, all serving to improve cell fitness.

Keywords: co-translational interaction; complex assembly; mRNA translation; multiprotein complex; protein-protein interaction; ribosome.

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References

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Grant support

[1] Natan, E., Wells, J. N., Teichmann, S. A., & Marsh, J. A. (2017). Regulation, evolution and consequences of cotranslational protein complex assembly. Current Opinion in Structural Biology, 42, 90-97.

[2] Natan, E., Wells, J. N., Teichmann, S. A., & Marsh, J. A. (2017). Regulation, evolution and consequences of cotranslational protein complex assembly. Current Opinion in Structural Biology, 42, 90-97.

[3] Khan, K., Long, B., Baleanu-Gogonea, C., Gogonea, V., Deshpande, G. M., Vasu, K., & Fox, P. L. (2022). Cotranslational interaction of human EBP50 and ezrin overcomes masked binding site during complex assembly. Proceedings of the National Academy of Sciences of the United States of America, 119, e2115799119.

[4] Khan, K., Long, B., Baleanu-Gogonea, C., Gogonea, V., Deshpande, G. M., Vasu, K., & Fox, P. L. (2022). Cotranslational interaction of human EBP50 and ezrin overcomes masked binding site during complex assembly. Proceedings of the National Academy of Sciences of the United States of America, 119, e2115799119.

[5] Shiber, A., Doring, K., Friedrich, U., Klann, K., Merker, D., Zedan, M., Tippmann, F., Kramer, G., & Bukau, B. (2018). Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling. Nature, 561, 268-272.

[6] Shiber, A., Doring, K., Friedrich, U., Klann, K., Merker, D., Zedan, M., Tippmann, F., Kramer, G., & Bukau, B. (2018). Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling. Nature, 561, 268-272.

[7] Duncan, C. D., & Mata, J. (2011). Widespread cotranslational formation of protein complexes. PLoS Genetics, 7, e1002398.

[8] Duncan, C. D., & Mata, J. (2011). Widespread cotranslational formation of protein complexes. PLoS Genetics, 7, e1002398.

[9] Badonyi, M., & Marsh, J. A. (2022). Large protein complex interfaces have evolved to promote cotranslational assembly. eLife, 11, e79602.

[10] Badonyi, M., & Marsh, J. A. (2022). Large protein complex interfaces have evolved to promote cotranslational assembly. eLife, 11, e79602.