Vitamin E Deficiency Disrupts Gene Expression Networks During Zebrafish Development

Overview

Journal Nutrients

Date 2021 Feb 12

PMID 33573233

Citations 4

Authors

Brian Head

Stephen A Ramsey

Chrissa Kioussi

Robyn L Tanguay

Maret G Traber

Affiliations

Soon will be listed here.

Abstract

Vitamin E (VitE) is essential for vertebrate embryogenesis, but the mechanisms involved remain unknown. To study embryonic development, we fed zebrafish adults (>55 days) either VitE sufficient (E+) or deficient (E-) diets for >80 days, then the fish were spawned to generate E+ and E- embryos. To evaluate the transcriptional basis of the metabolic and phenotypic outcomes, E+ and E- embryos at 12, 18 and 24 h post-fertilization (hpf) were subjected to gene expression profiling by RNASeq. Hierarchical clustering, over-representation analyses and gene set enrichment analyses were performed with differentially expressed genes. E- embryos experienced overall disruption to gene expression associated with gene transcription, carbohydrate and energy metabolism, intracellular signaling and the formation of embryonic structures. mTOR was apparently a major controller of these changes. Thus, embryonic VitE deficiency results in genetic and transcriptional dysregulation as early as 12 hpf, leading to metabolic dysfunction and ultimately lethal outcomes.

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References

Packer J, Slater T, Willson R . Direct observation of a free radical interaction between vitamin E and vitamin C. Nature. 1979; 278(5706):737-8. DOI: 10.1038/278737a0. View

Lebold K, Jump D, Miller G, Wright C, Labut E, Barton C . Vitamin E deficiency decreases long-chain PUFA in zebrafish (Danio rerio). J Nutr. 2011; 141(12):2113-8. PMC: 3223870. DOI: 10.3945/jn.111.144279. View

Head B, La Du J, Tanguay R, Kioussi C, Traber M . Vitamin E is necessary for zebrafish nervous system development. Sci Rep. 2020; 10(1):15028. PMC: 7506018. DOI: 10.1038/s41598-020-71760-x. View

Moazzami A, Andersson R, Kamal-Eldin A . Changes in the metabolic profile of rat liver after α-tocopherol deficiency as revealed by metabolomics analysis. NMR Biomed. 2011; 24(5):499-505. DOI: 10.1002/nbm.1615. View

White R, Collins J, Sealy I, Wali N, Dooley C, Digby Z . A high-resolution mRNA expression time course of embryonic development in zebrafish. Elife. 2017; 6. PMC: 5690287. DOI: 10.7554/eLife.30860. View

Finno C, Peterson J, Kang M, Park S, Bordbari M, Durbin-Johnson B . Single-Cell RNA-seq Reveals Profound Alterations in Mechanosensitive Dorsal Root Ganglion Neurons with Vitamin E Deficiency. iScience. 2019; 21:720-735. PMC: 6864320. DOI: 10.1016/j.isci.2019.10.064. View

Lee M, Bonner J, Bernard D, Sanchez E, Sause E, Prentice R . Disruption of the folate pathway in zebrafish causes developmental defects. BMC Dev Biol. 2012; 12:12. PMC: 3410756. DOI: 10.1186/1471-213X-12-12. View

Gohil K, Schock B, Chakraborty A, Terasawa Y, Raber J, Farese Jr R . Gene expression profile of oxidant stress and neurodegeneration in transgenic mice deficient in alpha-tocopherol transfer protein. Free Radic Biol Med. 2003; 35(11):1343-54. DOI: 10.1016/s0891-5849(03)00509-4. View

Evans H, Bishop K . ON THE EXISTENCE OF A HITHERTO UNRECOGNIZED DIETARY FACTOR ESSENTIAL FOR REPRODUCTION. Science. 1922; 56(1458):650-1. DOI: 10.1126/science.56.1458.650. View

10.

Barraud P, Seferiadis A, Tyson L, Zwart M, Szabo-Rogers H, Ruhrberg C . Neural crest origin of olfactory ensheathing glia. Proc Natl Acad Sci U S A. 2010; 107(49):21040-5. PMC: 3000254. DOI: 10.1073/pnas.1012248107. View

11.

Shimobayashi M, Hall M . Multiple amino acid sensing inputs to mTORC1. Cell Res. 2015; 26(1):7-20. PMC: 4816134. DOI: 10.1038/cr.2015.146. View

12.

Iwasa K, Shima K, Komai K, Nishida Y, Yokota T, Yamada M . Retinitis pigmentosa and macular degeneration in a patient with ataxia with isolated vitamin E deficiency with a novel c.717 del C mutation in the TTPA gene. J Neurol Sci. 2014; 345(1-2):228-30. DOI: 10.1016/j.jns.2014.07.001. View

13.

McDougall M, Choi J, Kim H, Bobe G, Stevens J, Cadenas E . Lethal dysregulation of energy metabolism during embryonic vitamin E deficiency. Free Radic Biol Med. 2017; 104:324-332. PMC: 5344700. DOI: 10.1016/j.freeradbiomed.2017.01.020. View

14.

Zhang J, Head B, Leonard S, Choi J, Tanguay R, Traber M . Vitamin E deficiency dysregulates thiols, amino acids and related molecules during zebrafish embryogenesis. Redox Biol. 2020; 38:101784. PMC: 7658488. DOI: 10.1016/j.redox.2020.101784. View

15.

Fishwick K, Li R, Halley P, Deng P, Storey K . Initiation of neuronal differentiation requires PI3-kinase/TOR signalling in the vertebrate neural tube. Dev Biol. 2009; 338(2):215-25. DOI: 10.1016/j.ydbio.2009.12.001. View

16.

Tixier V, Bataille L, Etard C, Jagla T, Weger M, Daponte J . Glycolysis supports embryonic muscle growth by promoting myoblast fusion. Proc Natl Acad Sci U S A. 2013; 110(47):18982-7. PMC: 3839714. DOI: 10.1073/pnas.1301262110. View

17.

Tanimura T, Shepard T . Glucose metabolism by rat embryos in vitro. Proc Soc Exp Biol Med. 1970; 135(1):51-4. DOI: 10.3181/00379727-135-34985. View

18.

Finno C, Bordbari M, Gianino G, Ming-Whitfield B, Burns E, Merkel J . An innate immune response and altered nuclear receptor activation defines the spinal cord transcriptome during alpha-tocopherol deficiency in Ttpa-null mice. Free Radic Biol Med. 2018; 120:289-302. PMC: 5940542. DOI: 10.1016/j.freeradbiomed.2018.02.037. View

19.

Tveden-Nyborg P, Vogt L, Schjoldager J, Jeannet N, Hasselholt S, Paidi M . Maternal vitamin C deficiency during pregnancy persistently impairs hippocampal neurogenesis in offspring of guinea pigs. PLoS One. 2012; 7(10):e48488. PMC: 3485340. DOI: 10.1371/journal.pone.0048488. View

20.

Scheldeman C, Mills J, Siekierska A, Serra I, Copmans D, Iyer A . mTOR-related neuropathology in mutant tsc2 zebrafish: Phenotypic, transcriptomic and pharmacological analysis. Neurobiol Dis. 2017; 108:225-237. DOI: 10.1016/j.nbd.2017.09.004. View