Mrhl Long Noncoding RNA Mediates Meiotic Commitment of Mouse Spermatogonial Cells by Regulating Sox8 Expression

REFERENCES

• Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, Draper BW, Ketting RF. 2007. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129:69–82. https://doi.org/10.1016/j.cell.2007.03.026.
   PubMed Web of Science ®Google Scholar
• Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T. 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203–207.
   PubMed Web of Science ®Google Scholar
• Rinn JL, Chang HY. 2012. Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166. https://doi.org/10.1146/annurev-biochem-051410-092902.
   PubMed Web of Science ®Google Scholar
• Gilbert SL, Pehrson JR, Sharp PA. 2000. XIST RNA associates with specific regions of the inactive X chromatin. J Biol Chem 275:36491–36494. https://doi.org/10.1074/jbc.C000409200.
   PubMed Web of Science ®Google Scholar
• Park Y, Kelley RL, Hyangyee O, Kuroda MI, Meller VH. 2002. Extent of chromatin spreading determined by roX RNA recruitment of MSL proteins. Science 298:1620–1623. https://doi.org/10.1126/science.1076686.
   PubMed Web of Science ®Google Scholar
• Sleutels F, Zwart R, Barlow DP. 2002. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810–813. https://doi.org/10.1038/415810a.
   PubMed Web of Science ®Google Scholar
• Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C. 2008. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32:232–246. https://doi.org/10.1016/j.molcel.2008.08.022.
   PubMed Web of Science ®Google Scholar
• Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, Sunkin SM, Crowe ML, Grimmond SM, Perkins AC, Mattick JS. 2008. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 18:1433–1445. https://doi.org/10.1101/gr.078378.108.
   PubMed Web of Science ®Google Scholar
• Fatica A, Bozzoni I. 2014. Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15:7–21. https://doi.org/10.1038/nri3777.
   PubMed Web of Science ®Google Scholar
• Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A, Lawrence JB. 2009. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 33:717–726. https://doi.org/10.1016/j.molcel.2009.01.026.
   PubMed Web of Science ®Google Scholar
• Marchese FP, Grossi E, Marin-Bejar O, Bharti SK, Raimondi I, Gonzalez J, Martinez-Herrera DJ, Athie A, Amadoz A, Brosh RM, Jr, Huarte M. 2016. A long noncoding RNA regulates sister chromatid cohesion. Mol Cell 63:397–407. https://doi.org/10.1016/j.molcel.2016.06.031.
   PubMed Web of Science ®Google Scholar
• Atianand MK, Hu W, Satpathy AT, Shen Y, Ricci EP, Alvarez-Dominguez JR, Bhatta A, Schattgen SA, McGowan JD, Blin J, Braun JE, Gandhi P, Moore MJ, Chang HY, Lodish HF, Caffrey DR, Fitzgerald KA. 2016. A long noncoding RNA lincRNA-EPS acts as a transcriptional brake to restrain inflammation. Cell 165:1672–1685. https://doi.org/10.1016/j.cell.2016.05.075.
   PubMed Web of Science ®Google Scholar
• Carnero E, Barriocanal M, Prior C, Pablo Unfried J, Segura V, Guruceaga E, Enguita M, Smerdou C, Gastaminza P, Fortes P. 2016. Long noncoding RNA EGOT negatively affects the antiviral response and favors HCV replication. EMBO Rep 17:1013–1028. https://doi.org/10.15252/embr.201541763.
   PubMed Web of Science ®Google Scholar
• Yoon JH, Abdelmohsen K, Srikantan S, Yang X, Martindale JL, De S, Huarte M, Zhan M, Becker KG, Gorospe M. 2012. LincRNA-p21 suppresses target mRNA translation. Mol Cell 47:648–655. https://doi.org/10.1016/j.molcel.2012.06.027.
   PubMed Web of Science ®Google Scholar
• Gong C, Maquat LE. 2011. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470:284–288. https://doi.org/10.1038/nature09701.
   PubMed Web of Science ®Google Scholar
• Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP. 2February2010. Noncoding RNA Gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal https://doi.org/10.1126/scisignal.2000568.
   Google Scholar
• Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, Wysocka J, Lei M, Dekker J, Helms JA, Chang HY. 2011. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–124. https://doi.org/10.1038/nature09819.
   PubMed Web of Science ®Google Scholar
• Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT. 2014. Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell 55:171–185. https://doi.org/10.1016/j.molcel.2014.05.009.
   PubMed Web of Science ®Google Scholar
• Feng J, Bi C, Clark BS, Mady R, Shah P, Kohtz JD. 2006. The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev 20:1470–1484. https://doi.org/10.1101/gad.1416106.
   PubMed Web of Science ®Google Scholar
• Rapicavoli NA, Qu K, Zhang J, Mikhail M, Laberge RM, Chang HY. 2013. A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife 2:e00762. https://doi.org/10.7554/eLife.00762.
   PubMed Web of Science ®Google Scholar
• Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I. 2011. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147:358–369. https://doi.org/10.1016/j.cell.2011.09.028.
   PubMed Web of Science ®Google Scholar
• Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, Blencowe BJ, Prasanth SG, Prasanth KV. 2010. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39:925–938. https://doi.org/10.1016/j.molcel.2010.08.011.
   PubMed Web of Science ®Google Scholar
• Li J, Chen C, Ma X, Geng G, Liu B, Zhang Y, Zhang S, Zhong F, Liu C, Yin Y, Cai W, Zhang H. 2016. Long noncoding RNA NRON contributes to HIV-1 latency by specifically inducing tat protein degradation. Nat Commun 7:11730. https://doi.org/10.1038/ncomms11730.
   PubMed Web of Science ®Google Scholar
• Fatima R, Akhade VS, Pal D, Rao SM. 2015. Long noncoding RNAs in development and cancer: potential biomarkers and therapeutic targets. Mol Cell Ther 3:5. https://doi.org/10.1186/s40591-015-0042-6.
   PubMedGoogle Scholar
• Nishant KT, Ravishankar H, Rao MR. 2004. Characterization of a mouse recombination hot spot locus encoding a novel non-protein-coding RNA. Mol Cell Biol 24:5620–5634. https://doi.org/10.1128/MCB.24.12.5620-5634.2004.
   PubMed Web of Science ®Google Scholar
• Ganesan G, Rao SM. 2008. A novel noncoding RNA processed by Drosha is restricted to nucleus in mouse. RNA 14:1399–1410. https://doi.org/10.1261/rna.838308.
   PubMed Web of Science ®Google Scholar
• Arun G, Akhade VS, Donakonda S, Rao MR. 2012. mrhl RNA, a long noncoding RNA, negatively regulates Wnt signaling through its protein partner Ddx5/p68 in mouse spermatogonial cells. Mol Cell Biol 32:3140–3152. https://doi.org/10.1128/MCB.00006-12.
   PubMed Web of Science ®Google Scholar
• Akhade VS, Arun G, Donakonda S, Rao MR. 2014. Genome wide chromatin occupancy of mrhl RNA and its role in gene regulation in mouse spermatogonial cells. RNA Biol 11:1262–1279. https://doi.org/10.1080/15476286.2014.996070.
   PubMed Web of Science ®Google Scholar
• Akhade VS, Dighe SN, Kataruka S, Rao MR. 2016. Mechanism of Wnt signaling induced down regulation of mrhl long non-coding RNA in mouse spermatogonial cells. Nucleic Acids Res 44:387–401. https://doi.org/10.1093/nar/gkv1023.
   PubMed Web of Science ®Google Scholar
• Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, van de Kant HJ, Wegner M, de Rooij DG, Behringer RR, Schedl A. 2004. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131:1891–1901. https://doi.org/10.1242/dev.01087.
   PubMedGoogle Scholar
• O'Bryan MK, Takada S, Kennedy CL, Scott G, Harada S, Ray MK, Dai Q, Wilhelm D, de Kretser DM, Eddy EM, Koopman P, Mishina Y. 2008. Sox8 is a critical regulator of adult Sertoli cell function and male fertility. Dev Biol 316:359–370. https://doi.org/10.1016/j.ydbio.2008.01.042.
   PubMed Web of Science ®Google Scholar
• Golestaneh N, Beauchamp E, Fallen S, Kokkinaki M, Uren A, Dym M. 2009. Wnt signaling promotes proliferation and stemness regulation of spermatogonial stem/progenitor cells. Reproduction 138:151–162. https://doi.org/10.1530/REP-08-0510.
   PubMed Web of Science ®Google Scholar
• Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810. https://doi.org/10.1146/annurev.cellbio.20.010403.113126.
   PubMed Web of Science ®Google Scholar
• MacDonald BT, Tamai K, He X. 2009. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9–26. https://doi.org/10.1016/j.devcel.2009.06.016.
   PubMed Web of Science ®Google Scholar
• McMahon SB, Wood MA, Cole MD. 2000. The essential cofactor TRRAP recruits the histone acetyltransferase hGCN5 to c-Myc. Mol Cell Biol 20:556–562. https://doi.org/10.1128/MCB.20.2.556-562.2000.
   PubMed Web of Science ®Google Scholar
• Lüscher B. 2001. Function and regulation of the transcription factors of the Myc/Max/Mad network. Gene 277:1–14. https://doi.org/10.1016/S0378-1119(01)00697-7.
   PubMedGoogle Scholar
• Eilers AL, Billin AN, Liu J, Ayer DE. 1999. A 13-amino acid amphipathic alpha-helix is required for the functional interaction between the transcriptional repressor Mad1 and mSin3A. J Biol Chem 274:32750–32756. https://doi.org/10.1074/jbc.274.46.32750.
   PubMed Web of Science ®Google Scholar
• Brubaker K, Cowley SM, Huang K, Loo L, Yochum GS, Ayer DE, Eisenman RN, Radhakrishnan I. 2000. Solution structure of the interacting domains of the Mad-Sin3 complex: implications for recruitment of a chromatin-modifying complex. Cell 103:655–665. https://doi.org/10.1016/S0092-8674(00)00168-9.
   PubMed Web of Science ®Google Scholar
• Feng CW, Bowles J, Koopman P. 2014. Control of mammalian germ cell entry into meiosis. Mol Cell Endocrinol 382:488–497. https://doi.org/10.1016/j.mce.2013.09.026.
   PubMed Web of Science ®Google Scholar
• Mondal T, Subhash S, Vaid R, Enroth S, Uday S, Reinius B, Mitra S, Mohammed A, James AR, Hoberg E, Moustakas A, Gyllensten U, Jones SJ, Gustafsson CM, Sims AH, Westerlund F, Gorab E, Kanduri C. 2015. MEG3 long noncoding RNA regulates the TGF-β pathway genes through formation of RNA-DNA triplex structures. Nat Commun 6:7743. https://doi.org/10.1038/ncomms8743.
   PubMed Web of Science ®Google Scholar
• Bao J, Wu J, Schuster AS, Hennig GW, Yan W. 2013. Expression profiling reveals developmentally regulated lncRNA repertoire in the mouse male germline. Biol Reprod 89:107. https://doi.org/10.1095/biolreprod.113.113308.
   PubMed Web of Science ®Google Scholar
• Liang M, Li W, Tian H, Hu T, Wang L, Lin Y, Li Y, Huang H, Sun F. 2014. Sequential expression of long noncoding RNA as mRNA gene expression in specific stages of mouse spermatogenesis. Sci Rep 4:5966. https://doi.org/10.1038/srep05966.
   PubMed Web of Science ®Google Scholar
• Ran M, Chen B, Li Z, Wu M, Liu X, He C, Zhang S, Li Z. 2016. Systematic identification of long noncoding RNAs in immature and mature porcine testes. Biol Reprod 94:77. https://doi.org/10.1095/biolreprod.115.136911.
   PubMed Web of Science ®Google Scholar
• Wen K, Yang L, Xiong T, Di C, Ma D, Wu M, Xue Z, Zhang X, Long L, Zhang W, Zhang J, Bi X, Dai J, Zhang Q, Lu ZJ, Gao G. 2016. Critical roles of long noncoding RNAs in Drosophila spermatogenesis. Genome Res 26:1233–1244. https://doi.org/10.1101/gr.199547.115.
   PubMed Web of Science ®Google Scholar
• Yoneda R, Satoh Y, Yoshida I, Kawamura S, Kotani T, Kimura AP. 2016. A genomic region transcribed into a long noncoding RNA interacts with the Prss42/Tessp-2 promoter in spermatocytes during mouse spermatogenesis, and its flanking sequences can function as enhancers. Mol Reprod Dev 83:541–557. https://doi.org/10.1002/mrd.22650.
   PubMed Web of Science ®Google Scholar
• Li L, Wang M, Wang M, Wu X, Geng L, Xue Y, Wei X, Jia Y, Wu X. 2016. A long non-coding RNA interacts with Gfra1 and maintains survival of mouse spermatogonial stem cells. Cell Death Dis 7:e2140. https://doi.org/10.1038/cddis.2016.24.
   PubMed Web of Science ®Google Scholar