Comprehensive Analysis of the Translatome Reveals the Relationship Between the Translational and Transcriptional Control in High Fat Diet-induced Liver Steatosis

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2020 Sep 24

PMID 32967529

Citations 8

Authors

Zupeng Luo

Hailong Hu

Siqi Liu

Zhiwang Zhang

Yixing Li

Lei Zhou

Affiliations

Soon will be listed here.

Abstract

Translational regulation plays a critical role in gene expression. However, there are few genome-wide studies on translational regulation in non-alcoholic fatty liver disease (NAFLD), which is a severe non-communicable epidemic worldwide. In this study, we performed RNC-mRNA (mRNAs bound to ribosome-nascent chain complex) sequencing and mRNA sequencing to probe the translation status of high-fat-diet (HFD) induced mouse fatty liver. Generally, in the HFD group compared to the control group, changes of translation ratios and changes in mRNA abundance had a negative correlation. The relative abundance of RNC-mRNAs and mRNAs were positively correlated, yet the former changed more slowly than the latter. However, the rate of change became more balanced when it came to the livers of mice that were fed the HFD plus lycopene, an antioxidant. This indicated relatively independent roles of translational modulation and transcriptional regulation. Furthermore, many genes were differentially regulated at the transcriptional or translational levels, suggesting a new screening strategy for functional genes. In conclusion, our analysis revealed the different and correlated role of translational control with transcriptional regulation in the HFD-induced mouse fatty liver relative to the control, which indicates critical roles of translational control for liver steatosis; thus, adding a new dimension towards a better understanding and improvement of treatment for NAFLD.

Citing Articles

Immunogenic peptides putatively from intratumor microbes: Opportunities for colorectal cancer treatment.

Guan X, Bu F, Fu Y, Zhang H, Xiang H, Chen X iScience. 2024; 27(12):111338.

PMID: 39640572 PMC: 11617993. DOI: 10.1016/j.isci.2024.111338.

Translatomics reveals the role of dietary calcium addition in regulating muscle fat deposition in pigs.

Yu J, Li X, Qi X, Ding Z, Su S, Yu L Sci Rep. 2024; 14(1):12295.

PMID: 38811812 PMC: 11136974. DOI: 10.1038/s41598-024-62986-0.

Identification and Functional Analysis of Drought-Responsive Long Noncoding RNAs in Maize Roots.

Tang X, Li Q, Feng X, Yang B, Zhong X, Zhou Y Int J Mol Sci. 2023; 24(20).

PMID: 37894720 PMC: 10606207. DOI: 10.3390/ijms242015039.

BATF relieves hepatic steatosis by inhibiting PD1 and promoting energy metabolism.

Zhang Z, Liao Q, Pan T, Yu L, Luo Z, Su S Elife. 2023; 12.

PMID: 37712938 PMC: 10503959. DOI: 10.7554/eLife.88521.

An integrative approach to assessing effects of a short-term Western diet on gene expression in rat liver.

Welles J, Lacko H, Kawasawa Y, Dennis M, Jefferson L, Kimball S Front Endocrinol (Lausanne). 2022; 13:1032293.

PMID: 36387860 PMC: 9643360. DOI: 10.3389/fendo.2022.1032293.

References

Ryaboshapkina M, Hammar M . Human hepatic gene expression signature of non-alcoholic fatty liver disease progression, a meta-analysis. Sci Rep. 2017; 7(1):12361. PMC: 5617840. DOI: 10.1038/s41598-017-10930-w. View

Sonenberg N, Hinnebusch A . Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009; 136(4):731-45. PMC: 3610329. DOI: 10.1016/j.cell.2009.01.042. View

Woolstenhulme C, Guydosh N, Green R, Buskirk A . High-precision analysis of translational pausing by ribosome profiling in bacteria lacking EFP. Cell Rep. 2015; 11(1):13-21. PMC: 4835038. DOI: 10.1016/j.celrep.2015.03.014. View

Barrera F, George J . The role of diet and nutritional intervention for the management of patients with NAFLD. Clin Liver Dis. 2013; 18(1):91-112. DOI: 10.1016/j.cld.2013.09.009. View

Gerashchenko M, Lobanov A, Gladyshev V . Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proc Natl Acad Sci U S A. 2012; 109(43):17394-9. PMC: 3491468. DOI: 10.1073/pnas.1120799109. View

Zhang M, Zhao K, Xu X, Yang Y, Yan S, Wei P . A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma. Nat Commun. 2018; 9(1):4475. PMC: 6203777. DOI: 10.1038/s41467-018-06862-2. View

Liu M, Ge R, Liu W, Liu Q, Xia X, Lai M . Differential proteomics profiling identifies LDPs and biological functions in high-fat diet-induced fatty livers. J Lipid Res. 2017; 58(4):681-694. PMC: 5392744. DOI: 10.1194/jlr.M071407. View

Zhang L, Qi Y, Aluo Z, Liu S, Zhang Z, Zhou L . Betaine increases mitochondrial content and improves hepatic lipid metabolism. Food Funct. 2018; 10(1):216-223. DOI: 10.1039/c8fo02004c. View

Kozak M . An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987; 15(20):8125-48. PMC: 306349. DOI: 10.1093/nar/15.20.8125. View

10.

Ferretti M, Ghalei H, Ward E, Potts E, Karbstein K . Rps26 directs mRNA-specific translation by recognition of Kozak sequence elements. Nat Struct Mol Biol. 2017; 24(9):700-707. PMC: 5777333. DOI: 10.1038/nsmb.3442. View

11.

Luo Z, Zhang Z, Tai L, Zhang L, Sun Z, Zhou L . Comprehensive analysis of differences of N-methyladenosine RNA methylomes between high-fat-fed and normal mouse livers. Epigenomics. 2019; 11(11):1267-1282. DOI: 10.2217/epi-2019-0009. View

12.

Pacana T, Sanyal A . Vitamin E and nonalcoholic fatty liver disease. Curr Opin Clin Nutr Metab Care. 2012; 15(6):641-8. PMC: 4984672. DOI: 10.1097/MCO.0b013e328357f747. View

13.

Mancina R, Dongiovanni P, Petta S, Pingitore P, Meroni M, Rametta R . The MBOAT7-TMC4 Variant rs641738 Increases Risk of Nonalcoholic Fatty Liver Disease in Individuals of European Descent. Gastroenterology. 2016; 150(5):1219-1230.e6. PMC: 4844071. DOI: 10.1053/j.gastro.2016.01.032. View

14.

Qi Y, Zhang Z, Liu S, Aluo Z, Zhang L, Yu L . Zinc Supplementation Alleviates Lipid and Glucose Metabolic Disorders Induced by a High-Fat Diet. J Agric Food Chem. 2020; 68(18):5189-5200. DOI: 10.1021/acs.jafc.0c01103. View

15.

Sookoian S, Pirola C . Genetic predisposition in nonalcoholic fatty liver disease. Clin Mol Hepatol. 2017; 23(1):1-12. PMC: 5381829. DOI: 10.3350/cmh.2016.0109. View

16.

Michel A, Andreev D, Baranov P . Computational approach for calculating the probability of eukaryotic translation initiation from ribo-seq data that takes into account leaky scanning. BMC Bioinformatics. 2014; 15:380. PMC: 4245810. DOI: 10.1186/s12859-014-0380-4. View

17.

Lian X, Guo J, Gu W, Cui Y, Zhong J, Jin J . Genome-Wide and Experimental Resolution of Relative Translation Elongation Speed at Individual Gene Level in Human Cells. PLoS Genet. 2016; 12(2):e1005901. PMC: 4771717. DOI: 10.1371/journal.pgen.1005901. View

18.

Zhong X, Yu J, Frazier K, Weng X, Li Y, Cham C . Circadian Clock Regulation of Hepatic Lipid Metabolism by Modulation of mA mRNA Methylation. Cell Rep. 2018; 25(7):1816-1828.e4. PMC: 6532766. DOI: 10.1016/j.celrep.2018.10.068. View

19.

Han Y, Hu Z, Cui A, Liu Z, Ma F, Xue Y . Post-translational regulation of lipogenesis via AMPK-dependent phosphorylation of insulin-induced gene. Nat Commun. 2019; 10(1):623. PMC: 6367348. DOI: 10.1038/s41467-019-08585-4. View

20.

Lu N, Li X, Yu J, Li Y, Wang C, Zhang L . Curcumin Attenuates Lipopolysaccharide-Induced Hepatic Lipid Metabolism Disorder by Modification of m A RNA Methylation in Piglets. Lipids. 2018; 53(1):53-63. DOI: 10.1002/lipd.12023. View