Critical Roles of Translation Initiation and RNA Uridylation in Endogenous Retroviral Expression and Neural Differentiation in Pluripotent Stem Cells

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2020 Jun 4

PMID 32492424

Citations 15

Authors

Kazutoshi Takahashi

Daeun Jeong

Songnan Wang

Megumi Narita

Xuemei Jin

Mio Iwasaki

Samuel D Perli

Bruce R Conklin

Shinya Yamanaka

Affiliations

Soon will be listed here.

Abstract

Previous studies have suggested that the loss of the translation initiation factor eIF4G1 homolog NAT1 induces excessive self-renewability of naive pluripotent stem cells (PSCs); yet the role of NAT1 in the self-renewal and differentiation of primed PSCs is still unclear. Here, we generate a conditional knockout of NAT1 in primed PSCs and use the cells for the functional analyses of NAT1. Our results show that NAT1 is required for the self-renewal and neural differentiation of primed PSCs. In contrast, NAT1 deficiency in naive pluripotency attenuates the differentiation to all cell types. We also find that NAT1 is involved in efficient protein expression of an RNA uridyltransferase, TUT7. TUT7 is involved in the neural differentiation of primed PSCs via the regulation of human endogenous retrovirus accumulation. These data demonstrate the essential roles of NAT1 and TUT7 in the precise transition of stem cell fate.

Citing Articles

SARS-CoV-2 Nsp1 cooperates with initiation factors EIF1 and 1A to selectively enhance translation of viral RNA.

Aviner R, Lidsky P, Xiao Y, Tassetto M, Kim D, Zhang L PLoS Pathog. 2024; 20(2):e1011535.

PMID: 38335237 PMC: 10903962. DOI: 10.1371/journal.ppat.1011535.

Neurogenesis in primates versus rodents and the value of non-human primate models.

Zhang R, Quan H, Wang Y, Luo F Natl Sci Rev. 2023; 10(11):nwad248.

PMID: 38025664 PMC: 10659238. DOI: 10.1093/nsr/nwad248.

HERVs and Cancer-A Comprehensive Review of the Relationship of Human Endogenous Retroviruses and Human Cancers.

Stricker E, Peckham-Gregory E, Scheurer M Biomedicines. 2023; 11(3).

PMID: 36979914 PMC: 10046157. DOI: 10.3390/biomedicines11030936.

Eukaryotic translation initiation factor eIF4G2 opens novel paths for protein synthesis in development, apoptosis and cell differentiation.

Liu Y, Cui J, Hoffman A, Hu J Cell Prolif. 2022; 56(3):e13367.

PMID: 36547008 PMC: 9977666. DOI: 10.1111/cpr.13367.

Exocyst complex component 2 is a potential host factor for SARS-CoV-2 infection.

Yi R, Hashimoto R, Sakamoto A, Matsumura Y, Nagao M, Takahashi K iScience. 2022; 25(11):105427.

PMID: 36310645 PMC: 9595492. DOI: 10.1016/j.isci.2022.105427.

References

Meiner V, Cases S, MYERS H, Sande E, Bellosta S, Schambelan M . Disruption of the acyl-CoA:cholesterol acyltransferase gene in mice: evidence suggesting multiple cholesterol esterification enzymes in mammals. Proc Natl Acad Sci U S A. 1996; 93(24):14041-6. PMC: 19491. DOI: 10.1073/pnas.93.24.14041. View

McMahon A, Bradley A . The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell. 1990; 62(6):1073-85. DOI: 10.1016/0092-8674(90)90385-r. View

Pirouz M, Du P, Munafo M, Gregory R . Dis3l2-Mediated Decay Is a Quality Control Pathway for Noncoding RNAs. Cell Rep. 2016; 16(7):1861-73. PMC: 4998061. DOI: 10.1016/j.celrep.2016.07.025. View

Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K . Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007; 131(5):861-72. DOI: 10.1016/j.cell.2007.11.019. View

Yoshikane N, Nakamura N, Ueda R, Ueno N, Yamanaka S, Nakamura M . Drosophila NAT1, a homolog of the vertebrate translational regulator NAT1/DAP5/p97, is required for embryonic germband extension and metamorphosis. Dev Growth Differ. 2007; 49(7):623-34. DOI: 10.1111/j.1440-169X.2007.00956.x. View

Chambers S, Fasano C, Papapetrou E, Tomishima M, Sadelain M, Studer L . Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol. 2009; 27(3):275-80. PMC: 2756723. DOI: 10.1038/nbt.1529. View

Liberman N, Gandin V, Svitkin Y, David M, Virgili G, Jaramillo M . DAP5 associates with eIF2β and eIF4AI to promote Internal Ribosome Entry Site driven translation. Nucleic Acids Res. 2015; 43(7):3764-75. PMC: 4402527. DOI: 10.1093/nar/gkv205. View

Weingarten-Gabbay S, Khan D, Liberman N, Yoffe Y, Bialik S, Das S . The translation initiation factor DAP5 promotes IRES-driven translation of p53 mRNA. Oncogene. 2013; 33(5):611-8. DOI: 10.1038/onc.2012.626. View

Deiss L, Berissi H, Kimchi A . DAP-5, a novel homolog of eukaryotic translation initiation factor 4G isolated as a putative modulator of gamma interferon-induced programmed cell death. Mol Cell Biol. 1997; 17(3):1615-25. PMC: 231887. DOI: 10.1128/MCB.17.3.1615. View

10.

Uhlen M, Fagerberg L, Hallstrom B, Lindskog C, Oksvold P, Mardinoglu A . Proteomics. Tissue-based map of the human proteome. Science. 2015; 347(6220):1260419. DOI: 10.1126/science.1260419. View

11.

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

12.

Bukhari S, Truesdell S, Lee S, Kollu S, Classon A, Boukhali M . A Specialized Mechanism of Translation Mediated by FXR1a-Associated MicroRNP in Cellular Quiescence. Mol Cell. 2016; 61(5):760-773. PMC: 4811377. DOI: 10.1016/j.molcel.2016.02.013. View

13.

Shaughnessy Jr J, Jenkins N, Copeland N . cDNA cloning, expression analysis, and chromosomal localization of a gene with high homology to wheat eIF-(iso)4F and mammalian eIF-4G. Genomics. 1997; 39(2):192-7. DOI: 10.1006/geno.1996.4502. View

14.

Nakagawa M, Taniguchi Y, Senda S, Takizawa N, Ichisaka T, Asano K . A novel efficient feeder-free culture system for the derivation of human induced pluripotent stem cells. Sci Rep. 2014; 4:3594. PMC: 3884228. DOI: 10.1038/srep03594. View

15.

Huang D, Sherman B, Lempicki R . Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4(1):44-57. DOI: 10.1038/nprot.2008.211. View

16.

Yamanaka S, Zhang X, Maeda M, Miura K, Wang S, Farese Jr R . Essential role of NAT1/p97/DAP5 in embryonic differentiation and the retinoic acid pathway. EMBO J. 2000; 19(20):5533-41. PMC: 314019. DOI: 10.1093/emboj/19.20.5533. View

17.

Nichols J, Smith A . Naive and primed pluripotent states. Cell Stem Cell. 2009; 4(6):487-92. DOI: 10.1016/j.stem.2009.05.015. View

18.

Mandegar M, Huebsch N, Frolov E, Shin E, Truong A, Olvera M . CRISPR Interference Efficiently Induces Specific and Reversible Gene Silencing in Human iPSCs. Cell Stem Cell. 2016; 18(4):541-53. PMC: 4830697. DOI: 10.1016/j.stem.2016.01.022. View

19.

Miyazaki T, Futaki S, Suemori H, Taniguchi Y, Yamada M, Kawasaki M . Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells. Nat Commun. 2012; 3:1236. PMC: 3535336. DOI: 10.1038/ncomms2231. View

20.

Sugiyama H, Takahashi K, Yamamoto T, Iwasaki M, Narita M, Nakamura M . Nat1 promotes translation of specific proteins that induce differentiation of mouse embryonic stem cells. Proc Natl Acad Sci U S A. 2016; 114(2):340-345. PMC: 5240712. DOI: 10.1073/pnas.1617234114. View