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Expansion of eIF4E and 4E-BP Family Members in Deuterostomes

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Evolution of the Protein Synthesis Machinery and Its Regulation

Abstract

Analysis of eIF4E sequences from the more than twenty fish genomes currently available, as well as those of select tetrapods, echinoderm (Strongylocentrotus purpuratus), tunicate (Ciona intestinalis), and cephalocordate (Branchiostoma lanceolatum), has allowed a glimpse of the origins and evolution of the eIF4E and 4E-BP families in vertebrates. Metazoan eIF4E family members group into three classes, with Class I containing the canonical cap-binding translational initiation factor, eIF4E-1. Class II and III eIF4E family members have distinct characteristics and have been shown to regulate the translation of particular mRNAs. All deuterostomes have at least one representative from each of the three classes of eIF4E. Outgroup deuterostomes such as sea urchins, tunicates, and lancelets have only one eIF4E from each class: eIF4E-1, eIF4E-2, and eIF4E-3. Evidence of the duplication of Class I eIF4Es can be seen in elephant shark (Callorhinchus milii), coelacanth (Latimeria chalumnae), and the basal ray-finned fish, spotted gar (Lepisosteus oculatus), which all have three eIF4E-1 subclasses: eIF4E-1A, -1B, and -1C. The emergence of eIF4E-1 subclasses is consistent with the duplication of Class I prior to the teleost-specific whole genome duplication (TGD), probably at one of the vertebrate genome duplications that occurred at ~550 Ma (VGD1) and 500 Ma (VGD2). eIF4E-1C has maintained the function of a prototypical initiation factor. It has been retained in all teleosts, but lost in tetrapods; eIF4E-1B has neofunctionalized to become a tissue-specific regulator of mRNA recruitment. It has been retained in tetrapods and most teleosts, but lost in the Tetraodontiforms such as Tetroadon and Takifugu species. Some percomorphs have acquired new cognates of eIF4E-1A and eIF4E-3 to give eIF4E-1A1 and -1A2 and eIF4E-3A and -3B. A duplication of class II eIF4Es occurred prior to the emergence of the tetrapod branch to give eIF4E-2A and -2B. eIF4E-2B is retained by amphibians and teleosts, but has been lost in coelacanth and amniotes. Overall, duplication within the different classes of eIF4E occurred early in vertebrate evolution with some neofunctionalization. Further duplication within teleosts of eIF4E-1A and eIF4E-3 occurred and has been retained in some teleost lineages. Asymmetric losses in different vertebrate classes also occurred. Similarly, expansion of the 4E-BPs took place in vertebrates to give three classes, 4E-BP1, -BP2, and -BP3, with further duplication in select teleosts to give six 4E-BP cognates, with asymmetric loss in more recently emerging teleosts.

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Acknowledgments

RJ and TB are supported by NIH R01ES021949-01 and NSF OCE1313888 to RJ and Allen R. Place. KG was supported by a graduate fellowship from the NOAA-EPP-funded Living Marine Sciences Cooperative Science Center (LMRCSC), NA11SEC4810002. Thanks are extended to Dr. Helen Dooley and Anthony Redmond from the University of Aberdeen for providing transcriptomic sequences of eIF4Es and 4E-BPs from spotted cat shark, Scyliorhinus canicula. This work was begun and inspired by Dr. Bhavesh Joshi, currently chief scientific officer, BridgePath Scientific.

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  1. 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

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    Greco Hernández

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Gillespie, K.M., Bachvaroff, T.R., Jagus, R. (2016). Expansion of eIF4E and 4E-BP Family Members in Deuterostomes. 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_8

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