Loss of miR-83 extends lifespan and affects target gene expression in an age-dependent manner in Caenorhabditis elegans

Emmanuel Enoch Dzakah; Ahmed Waqas; Shuai Wei; Bin Yu; Xiaolin Wang; Tao Fu; Lei Liu; Ge Shan

doi:10.1016/j.jgg.2018.11.003

Volume 45 Issue 12

Dec. 2018

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Article Navigation > Journal of Genetics and Genomics > 2018 > 45(12): 651-662

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Loss of miR-83 extends lifespan and affects target gene expression in an age-dependent manner in Caenorhabditis elegans

doi: 10.1016/j.jgg.2018.11.003

Emmanuel Enoch Dzakah^{a, b, #},
Ahmed Waqas^{a, #},
Shuai Wei^a,
Bin Yu^{a, #},
Xiaolin Wang^a,
Tao Fu^a,
Lei Liu^a,
Ge Shan^{a, c}

a
Division of Molecular Medicine, Hefei National Laboratory for Physical Sciences at Microscale, the CAS Key Laboratory of Innate Immunity and Chronic Disease, School of Life Sciences, University of Science and Technology of China, Hefei 230027, China
b
Department of Molecular Biology and Biotechnology, School of Biological Sciences, College of Agriculture and Natural Sciences, University of Cape Coast, Cape Coast 03321, Ghana
c
CAS Centre for Excellence in Molecular Cell Science, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China

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Corresponding author: E-mail address: shange@ustc.edu.cn (Ge Shan)
Received Date: 2018-05-24
Accepted Date: 2018-11-06
Rev Recd Date: 2018-10-11

Available Online: 2018-12-09

Publish Date: 2018-12-20

Abstract

Abstract

MicroRNAs (miRNAs) are short non-coding RNAs that are involved in the post-transcriptional regulation of protein-coding genes. miRNAs modulate lifespan and the aging process in a variety of organisms. In this study, we identified a role of miR-83 in regulating lifespan of Caenorhabditis elegans. mir-83 mutants exhibited extended lifespan, and the overexpression of miR-83 was sufficient to decrease the prolonged lifespan of the mutants. We observed upregulation of the expression levels of a set of miR-83 target genes in young mir-83 mutant adults; while different sets of genes were upregulated in older mir-83 mutant adults. In vivo assays showed that miR-83 regulated expression of target genes including din-1, spp-9 and col-178, and we demonstrated that daf-16 and din-1 were required for the extension of lifespan in the mir-83 mutants. The regulation of din-1 by miR-83 during aging resulted in the differential expression of din-1 targets such as gst-4 and gst-10. In daf-2 mutants, the expression level of miR-83 was significantly reduced compared to wild-type animals. We identified a role for miR-83 in modulating lifespan in C. elegans and provided molecular insights into its functional mechanism.
- miR-83,
- Longevity

Current address: Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309, USA.

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References(73)

References

[1]	Agarwal, V., Bell, G.W., Nam, J. et al. Predicting effective microRNA target sites in mammalian mRNAs eLife, 4 (2015)
[2]	Ambros, V. The functions of animal microRNAs Nature, 431 (2004),pp. 350-355
[3]	Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function Cell, 116 (2004),pp. 281-297
[4]	Bartel, D.P. MicroRNAs: target recognition and regulatory functions Cell, 136 (2009),pp. 215-233
[5]	Boehm, M., Slack, F. Science, 310 (2005),pp. 1954-1957
[6]	Boulias, K., Horvitz, H.R. Cell Metabol., 15 (2012),pp. 439-450
[7]	Bowen, R.L., Atwood, C.S. Living and dying for sex Gerontology, 50 (2004),pp. 265-290
[8]	Broughton, J.P., Lovci, M.T., Huang, J.L. et al. Pairing beyond the seed supports microRNA targeting specificity Mol. Cell, 64 (2016),pp. 320-333
[9]	Budovskaya, Y.V., Wu, K., Southworth, L.K. et al. Cell, 134 (2008),pp. 291-303
[10]	Burke, S.L., Hammell, M., Ambros, V. Genetics, 200 (2015),pp. 1201-1218
[11]	Campisi, J. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors Cell, 120 (2005),pp. 513-522
[12]	Cecchetelli, A.D., Cram, E.J. Regulating distal tip cell migration in space and time Mech. Dev., 148 (2017),pp. 11-17
[13]	de Lencastre, A., Pincus, Z., Zhou, K. et al. Curr. Biol., 20 (2010),pp. 2159-2168
[14]	Ebert, M.S., Sharp, P.A. Roles for micrornas in conferring robustness to biological processes Cell, 149 (2012),pp. 515-524
[15]	Eran, E., Roy, N., Israel, S. et al. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists BMC Bioinf., 10 (2009),p. 48
[16]	Griffiths-Jones, S., Saini, H.K., van Dongen, S. et al. miRBase: tools for microRNA genomics Nucleic Acids Res., 36 (2008),pp. D154-D158
[17]	Guo, H., Ingolia, N.T., Weissman, J.S. et al. Mammalian microRNAs predominantly act to decrease target mRNA levels Nature, 466 (2010),pp. 835-840
[18]	Halaschek-Wiener, J., Khattra, J.S., McKay, S. et al. Genome Res., 15 (2005),pp. 603-615
[19]	Hammell, M., Long, D., Zhang, L. et al. mirWIP: microRNA target prediction based on microRNA-containing ribonucleoprotein-enriched transcripts Nat. Methods, 5 (2008),pp. 813-819
[20]	He, F. Bio-protocol, Bio., 101 (2011),p. e47
[21]	Heid, J., Cencioni, C., Ripa, R. et al. Age-dependent increase of oxidative stress regulates microRNA-29 family preserving cardiachealth Sci. Rep., 7 (2017),p. 16839
[22]	Herndon, L.A., Schmeissner, P.J., Dudaronek, J.M. et al. Nature, 419 (2002),pp. 808-814
[23]	Hieronymus, H., Silver, P.A. A systems view of mRNP biology Genes Dev., 18 (2004),pp. 2845-2860
[24]	Hooten, N.N., Abdelmohsen, K., Gorospe, M. et al. MicroRNA expression patterns reveal differential expression of target genes with age PLoS One, 5 (2010)
[25]	Hooten, N.N., Fitzpatrick, M., , De, S. et al. Age-related changes in microRNA levels in serum Aging, 5 (2013),pp. 725-740
[26]	Horn, T., Boutros, M. E-RNAi: a web application for the multi-species design of RNAi reagents--2010 update Nucleic Acids Res., 38 (2010),pp. W332-W339
[27]	Hsu, A.L., Murphy, C.T., Kenyon, C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor Science, 300 (2003),pp. 1142-1145
[28]	Huntzinger, E., Izaurralde, E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay Nat. Rev. Genet., 12 (2011),pp. 99-110
[29]	Ibañez-Ventoso, C., Yang, M., Guo, S. et al. Aging Cell, 5 (2006),pp. 235-246
[30]	Inukai, S., Pincus, Z., de Lencastre, A. et al. A microRNA feedback loop regulates global microRNA abundance during aging RNA, 24 (2018),pp. 159-172
[31]	Johnson, D.W., Llop, J.R., Farrell, S.F. et al. PLoS Genet., 10 (2014),p. e1004278
[32]	Jung, H.J., Suh, Y. MicroRNA in aging: from discovery to biology Curr. Genomics, 13 (2012),pp. 548-557
[33]	Kadandale, P., Chatterjee, I., Singson, A. Germline transformation of Caenorhabditis elegans by injection Methods Mol. Biol., 518 (2009),pp. 123-133
[34]	Kaletsky, R., Lakhina, V., Arey, R. et al. Nature, 529 (2015),pp. 92-96
[35]	Kaul, T.K., Reis, R.P., Ogungbe, I.V. et al. PLoS One, 9 (2014)
[36]	Keene, J.D., Lager, P.J. Post-transcriptional operons and regulons co-ordinating gene expression Chromosome Res., 13 (2005),pp. 327-337
[37]	Krek, A., Grün, D., Poy, M.N. et al. Combinatorial microRNA target predictions Nat. Genet., 37 (2005),pp. 495-500
[38]	Li, T., Yan, X., Jiang, M. et al. The comparison of microRNA profile of the dermis between the young and elderly J. Dermatol. Sci., 82 (2016),pp. 75-83
[39]	Liu, H., Wang, X., Wang, H.D. et al. Nat. Commun., 3 (2012),p. 1073
[40]	Lu, T., Pan, Y., Kao, S.Y. et al. Gene regulation and DNA damage in the ageing human brain Nature, 429 (2004),pp. 883-891
[41]	Lucanic, M., Graham, J., Scott, G. et al. Aging, 5 (2013),pp. 394-411
[42]	Ludewig, A.H., Kober-Eisermann, C., Weitzel, C. et al. Genes Dev., 18 (2004),pp. 2120-2133
[43]	Lund, J., Tedesco, P., Duke, K. et al. Curr. Biol., 12 (2002),pp. 1566-1573
[44]	Mann, F.G., Van Nostrand, E.L., Friedland, A.E. et al. PLoS Genet., 12 (2016)
[45]	Martinez, N.J., Ow, M.C., Barrasa, I.M. et al. Genes Dev., 22 (2008),pp. 2535-2549
[46]	Martinez, N.J., Ow, M.C., Reece-Hoyes, J.S. et al. Genome Res., 18 (2008),pp. 2005-2015
[47]	McGeer, P.L., McGeer, E.G. Inflammation and the degenerative diseases of aging Ann. N. Y. Acad. Sci., 1035 (2004),pp. 104-116
[48]	Meng, L., Chen, L., Li, Z. et al. J. Genet. Genomics, 40 (2013),pp. 445-452
[49]	Miska, E.A., Alvarez-Saavedra, E., Abbott, A.L. et al. PLoS Genet., 3 (2007),p. e215
[50]	Mukherji, S., Ebert, M.S., Zheng, G.X. et al. MicroRNAs can generate thresholds in target gene expression Nat. Genet., 43 (2011),pp. 854-859
[51]	Narayan, N., Morenos, L., Phipson, B. et al. Functionally distinct roles for different miR-155 expression levels through contrasting effects on gene expression, in acute myeloid leukaemia Leukemia, 31 (2017),pp. 808-820
[52]	Ogg, S., Paradis, S., Gottlieb, S. et al. Nature, 389 (1997),pp. 994-999
[53]	Paraskevopoulou, M.D., Georgakilas, G., Kostoulas, N. et al. DIANA-microT web server v5.0: service integration into miRNA functional analysis workflows Nucleic Acids Res., 41 (2013),pp. W169-W173
[54]	Pasquinelli, A.E. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship Nat. Rev. Genet., 13 (2012),pp. 271-282
[55]	Petersen, C.P., Bordeleau, M.E., Pelletier, J. et al. Short RNAs repress translation after initiation in mammalian cells Mol. Cell, 21 (2006),pp. 533-542
[56]	Pincus, Z., Slack, F.J. Genome Biol., 9 (2008),p. 233
[57]	Pincus, Z., Smith-Vikos, T., Slack, F.J. PLoS Genet., 7 (2011)
[58]	Rangaraju, S., Solis, G.M., Thompson, R.C. et al. eLife, 4 (2015)
[59]	Seggerson, K., Tang, L., Moss, E.G. Dev. Biol., 243 (2002),pp. 215-225
[60]	Seo, K., Choi, E., Lee, D. et al. Aging Cell, 12 (2013),pp. 1073-1081
[61]	Shan, G. RNA interference as a gene knockdown technique Int. J. Biochem. Cell Biol., 42 (2010),pp. 1243-1251
[62]	Shu, J., Xia, Z., Li, L. et al. Dose-dependent differential mRNA target selection and regulation by let-7a-7f and miR-17-92 cluster microRNAs RNA Biol., 9 (2012),pp. 1275-1287
[63]	Smith-Vikos, T., Slack, F.J. MicroRNAs and their roles in aging J. Cell Sci., 125 (2012),pp. 7-17
[64]	Son, H.G., Seo, M., Ham, S. et al. Nat. Commun., 8 (2017),p. 14749
[65]	Takeda, T., Tanabe, H. Lifespan and reproduction in brain-specific miR-29-knockdown mouse Biochem. Biophys. Res. Commun., 471 (2016),pp. 454-458
[66]	Tao, J., Wu, Q.Y., Ma, Y.C. et al. Sci. Rep., 7 (2017),p. 43547
[67]	Van Wynsberghe, P.M., Chan, S.P., Slack, F.J. et al. Analysis of microRNA expression and function Methods Cell Biol., 106 (2011),pp. 219-252
[68]	Walhout, A.J.M. Unraveling transcription regulatory networks by protein-DNA and protein–protein interaction mapping Genome Res., 16 (2006),pp. 1445-1454
[69]	Whyte, W.A., Orlando, D.A., Hnisz, D. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell, 153 (2013),pp. 307-319
[70]	Wilkinson, D.S., Taylor, R.C., Dillin, A.
[71]	Wu, L., Fan, J., Belasco, J.G. MicroRNAs direct rapid deadenylation of mRNA Proc. Natl. Acad. Sci. U. S. A., 103 (2006),pp. 4034-4039
[72]	Yu, B., Wang, X., Wei, S. et al. Dev. Cell, 43 (2017),pp. 212-226
[73]	Zanotti, S., Gibertini, S., Curcio, M. et al. Opposing roles of miR-21 and miR-29 in the progression of fibrosis in Duchenne muscular dystrophy Biochim. Biophys. Acta, 1852 (2015),pp. 1451-1464