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Evolution of eIF4E-Interacting Proteins

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Evolution of the Protein Synthesis Machinery and Its Regulation

Abstract

Most eukaryotic mRNAs are translated by a cap-dependent mechanism, which requires recognition of the 5′ cap structure of the mRNA by eIF4E. Due to its crucial role in translation, eIF4E is a major target of regulation. One of the most prominent mechanisms regulating eIF4E activity is through its interaction with numerous proteins termed eIF4E-interacting proteins (4E-IPs). By competing with eIF4G for eIF4E binding, 4E-IPs act in general as translational repressors, although additional functions have been described. In this chapter, we discuss recent functional, phylogenetic and structural evidence that throws light on the evolution of 4E-IPs and evolutionary recurring themes. Phylogenetic analysis suggests that the first identified 4E-IPs, the mammalian 4E-binding proteins (4E-BPs), appeared as a single-copy gene in the last common ancestor of Amoebozoa, Glaucocystophyta, Fungi and Metazoa. 4E-BP is found in all Metazoans except Nematoda. It is found in glaucocystophytes, but has been lost in Viridiplantae. It is lost in most fungi, although it can be found in basidiomycetes as well as some glomeromycetes and zygomycetes. 4E-BP has been duplicated in vertebrates with up to six cognates found. 4E-BP seems to be absent, not lost, in most protist lineages since it has not been found in lineages thought to be at the root of the eukaryotes. Additional 4E-IPs, unrelated to 4E-BP, evolved independently in a lineage-specific manner, perhaps by a process of molecular tinkering, i.e., by gene duplication of preexisting proteins from different cellular processes and later in evolution incorporated into translation. Multiple duplications of eIF4E during eukaryotic radiation might have contributed, to some extent, to 4E-IP’s evolution. Some 4E-IPs are shared by different taxa, such as the eIF4E transporter, neuroguidin and Maskin, which are present in Amoebozoa, some/all fungi and the metazoan lineages. Unique lineage-specific 4E-IPs have evolved independently in some taxonomic groups such as Eap1p and p20 in yeasts, SPN-2 in C. elegans and Bicoid in higher Dipterans. Neuroguidin is the only 4E-IP represented in all eukaryotic lineages. Despite the diversity in function, sequence and origin, recent studies have revealed that 4E-IPs exhibit common binding principles when complexed with eIF4E.

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Acknowledgments

G.H. thanks the National Institute of Cancer (INCan), Mexico, and the National Council of Science and Technology (CONACyT, Mexico, grant no. 168154) for funding this work. B.C and M.B. acknowledge Université Sorbonne Paris Cité (USPC) for the Research Project 2014 grant and 2015 International Fellowship. R.J and T.B are supported by NIH R01ES021949-01 and NSF OCE1313888 to R.J. and Allen R. Place. K.G. was supported by a graduate fellowship from the NOAA-EPP-funded Living Marine Sciences Cooperative Science Center (LMRCSC), NA11SEC4810002.

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Authors and Affiliations

  1. Division of Basic Research, National Institute of Cancer (INCan), 22 San Fernando Avenue, Tlalpan, 14080, Mexico City, Mexico

    Greco Hernández

  2. Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, 701 E. Pratt Street, Baltimore, MD, 21202, USA

    Kathleen M. Gillespie, Tsvetan R. Bachvaroff & Rosemary Jagus

  3. Department of Biochemistry, Max Planck Institute for Developmental Biology, Spemannstrasse 35, 72076, Tübingen, Germany

    Cátia Igreja & Daniel Peter

  4. Université Paris Diderot, Sorbonne Paris Cité, Epigenetics and Cell Fate, UMR7216, CNRS, 75013, Paris, France

    Manuel Bulfoni & Bertrand Cosson

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Correspondence to Greco Hernández .

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  1. Division of Basic Research, National Institute for Cancer, Mexico City, Distrito Federal, Mexico

    Greco Hernández

  2. Institute of Marine and Environmental Te, Univ. of Maryland Center for Environment, Baltimore, Maryland, USA

    Rosemary Jagus

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Hernández, G. et al. (2016). Evolution of eIF4E-Interacting Proteins. In: Hernández, G., Jagus, R. (eds) Evolution of the Protein Synthesis Machinery and Its Regulation. Springer, Cham. https://doi.org/10.1007/978-3-319-39468-8_10

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