Home LiteratureArticle Details
PMID: 20582318 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

MicroRNA-122 modulates the rhythmic expression profile of the circadian deadenylase Nocturnin in mouse liver.

PloS one ·Vol. 5 ·No. 6 ·2010-06-22 ·Pages e11264

Kojima S, Gatfield D, Esau CC, Green CB

Abstract

Nocturnin is a circadian clock-regulated deadenylase thought to control mRNA expression post-transcriptionally through poly(A) tail removal. The expression of Nocturnin is robustly rhythmic in liver at both the mRNA and protein levels, and mice lacking Nocturnin are resistant to diet-induced obesity and hepatic steatosis. Here we report that Nocturnin expression is regulated by microRNA-122 (miR-122), a liver specific miRNA. We found that the 3'-untranslated region (3'-UTR) of Nocturnin mRNA harbors one putative recognition site for miR-122, and this site is conserved among mammals. Using a luciferase reporter construct with wild-type or mutant Nocturnin 3'-UTR sequence, we demonstrated that overexpression of miR-122 can down-regulate luciferase activity levels and that this effect is dependent on the presence of the putative miR-122 recognition site. Additionally, the use of an antisense oligonucleotide to knock down miR-122 in vivo resulted in significant up-regulation of both Nocturnin mRNA and protein expression in mouse liver during the night, resulting in Nocturnin rhythms with increased amplitude. Together, these data demonstrate that the normal rhythmic profile of Nocturnin expression in liver is shaped in part by miR-122. Previous studies have implicated Nocturnin and miR-122 as important post-transcriptional regulators of both lipid metabolism and circadian clock controlled gene expression in the liver. Therefore, the demonstration that miR-122 plays a role in regulating Nocturnin expression suggests that this may be an important intersection between hepatic metabolic and circadian control.

MeSH Terms
3' Untranslated Regions Animals Base Sequence Blotting, Northern Cell Line Circadian Rhythm Gene Expression Profiling Humans Liver/enzymology Male Mice Mice, Inbred C57BL MicroRNAs/physiology NIH 3T3 Cells Nuclear Proteins/genetics Polymerase Chain Reaction RNA, Messenger/genetics Transcription Factors/genetics
Chemicals
3' Untranslated Regions MicroRNAs Nuclear Proteins RNA, Messenger Transcription Factors nocturnin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kojima Shihoko
Department of Neuroscience, University of Texas Southwestern Medical Center, Dallas, Texas, United States of America.
Gatfield David
Esau Christine C
Green Carla B
References (37)
37 references, click to expand
  1. MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster.
    J Biol Chem. 2007 Aug 24;282(34):25053-66 PMID: 17597072
  2. Origins and Mechanisms of miRNAs and siRNAs.
    Cell. 2009 Feb 20;136(4):642-55 PMID: 19239886
  3. Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity.
    Proc Natl Acad Sci U S A. 2007 Jun 5;104(23):9888-93 PMID: 17517647
  4. microRNA modulation of circadian-clock period and entrainment.
    Neuron. 2007 Jun 7;54(5):813-29 PMID: 17553428
  5. Integration of microRNA miR-122 in hepatic circadian gene expression.
    Genes Dev. 2009 Jun 1;23(11):1313-26 PMID: 19487572
  6. Silencing of microRNAs in vivo with 'antagomirs'.
    Nature. 2005 Dec 1;438(7068):685-9 PMID: 16258535
  7. Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver.
    Nucleic Acids Res. 2008 Mar;36(4):1153-62 PMID: 18158304
  8. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation.
    Mol Cell. 2009 Sep 24;35(6):868-80 PMID: 19716330
  9. Relief of microRNA-mediated translational repression in human cells subjected to stress.
    Cell. 2006 Jun 16;125(6):1111-24 PMID: 16777601
  10. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression.
    Hepatology. 2008 Dec;48(6):1810-20 PMID: 19030170
  11. The miRNA-192/194 cluster regulates the Period gene family and the circadian clock.
    FEBS J. 2009 Oct;276(19):5447-55 PMID: 19682069
  12. Nocturnin, a deadenylase in Xenopus laevis retina: a mechanism for posttranscriptional control of circadian-related mRNA.
    Curr Biol. 2003 Feb 4;13(3):189-98 PMID: 12573214
  13. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells.
    Curr Opin Cell Biol. 2009 Jun;21(3):452-60 PMID: 19450959
  14. Rhythmic expression of Nocturnin mRNA in multiple tissues of the mouse.
    BMC Dev Biol. 2001;1:9 PMID: 11394964
  15. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing.
    Mol Cell. 2007 Aug 3;27(3):435-48 PMID: 17679093
  16. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1.
    RNA Biol. 2004 Jul;1(2):106-13 PMID: 17179747
  17. miR-519d overexpression is associated with human obesity.
    Obesity (Silver Spring). 2010 Nov;18(11):2170-6 PMID: 20057369
  18. Probing microRNAs with microarrays: tissue specificity and functional inference.
    RNA. 2004 Nov;10(11):1813-9 PMID: 15496526
  19. A role for microRNAs in the Drosophila circadian clock.
    Genes Dev. 2009 Sep 15;23(18):2179-91 PMID: 19696147
  20. microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma.
    Biochem Biophys Res Commun. 2009 Dec 11;390(2):247-51 PMID: 19800867
  21. Structural and functional analysis of 3' untranslated region of mouse Period1 mRNA.
    Biochem Biophys Res Commun. 2003 Jan 31;301(1):1-7 PMID: 12535631
  22. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma.
    Cancer Res. 2007 Jul 1;67(13):6092-9 PMID: 17616664
  23. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection.
    Science. 2010 Jan 8;327(5962):198-201 PMID: 19965718
  24. A role of miR-27 in the regulation of adipogenesis.
    FEBS J. 2009 Apr;276(8):2348-58 PMID: 19348006
  25. Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells.
    Mol Cell Biol. 2005 Nov;25(21):9198-208 PMID: 16227573
  26. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting.
    Cell Metab. 2006 Feb;3(2):87-98 PMID: 16459310
  27. Current tools for the identification of miRNA genes and their targets.
    Nucleic Acids Res. 2009 May;37(8):2419-33 PMID: 19295136
  28. Up-regulated expression of microRNA-143 in association with obesity in adipose tissue of mice fed high-fat diet.
    Biochem Biophys Res Commun. 2008 Nov 28;376(4):728-32 PMID: 18809385
  29. MicroRNAs direct rapid deadenylation of mRNA.
    Proc Natl Acad Sci U S A. 2006 Mar 14;103(11):4034-9 PMID: 16495412
  30. Immediate early response of the circadian polyA ribonuclease nocturnin to two extracellular stimuli.
    RNA. 2007 May;13(5):745-55 PMID: 17400819
  31. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas.
    J Cell Biochem. 2006 Oct 15;99(3):671-8 PMID: 16924677
  32. The up-regulation of microRNA-335 is associated with lipid metabolism in liver and white adipose tissue of genetically obese mice.
    Biochem Biophys Res Commun. 2009 Aug 7;385(4):492-6 PMID: 19460359
  33. LNA-mediated microRNA silencing in non-human primates.
    Nature. 2008 Apr 17;452(7189):896-9 PMID: 18368051
  34. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines.
    Gastroenterology. 2006 Jun;130(7):2113-29 PMID: 16762633
  35. Messenger RNA regulation: to translate or to degrade.
    EMBO J. 2008 Feb 6;27(3):471-81 PMID: 18256698
  36. MicroRNA assassins: factors that regulate the disappearance of miRNAs.
    Nat Struct Mol Biol. 2010 Jan;17(1):5-10 PMID: 20051982
  37. miR-122, a paradigm for the role of microRNAs in the liver.
    J Hepatol. 2008 Apr;48(4):648-56 PMID: 18291553
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2010-06-22
Epub
2010-00-22
Pages
e11264
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC2889834
Subset
IM
Grants
NIGMS NIH HHS · R01 GM076626 · United States
NIGMS NIH HHS · GM076626 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com