Regulation of Sox8 through lncRNA Mrhl-Mediated Chromatin Looping in Mouse Spermatogonia

REFERENCES

• O'Bryan M, Takada S, Kennedy C, Scott G, Harada S, Ray M, Dai Q, Wilhelm D, de Kretser D, Eddy E, 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
• Barrionuevo F, Scherer G. 2010. SOX E genes: Sox9 and Sox8 in mammalian testis development. Int J Biochem Cell Biol 42:433–436. https://doi.org/10.1016/j.biocel.2009.07.015.
   PubMed Web of Science ®Google Scholar
• Barrionuevo F, Hurtado A, Kim G, Real F, Bakkali M, Kopp J, Sander M, Scherer G, Burgos M, Jiménez R. 2016. Sox9 and Sox8 protect the adult testis from male-to-female genetic reprogramming and complete degeneration. Elife 5:e15635. https://doi.org/10.7554/eLife.15635.
   Google Scholar
• Richardson N, Gillot I, Gregoire E, Youssef S, de Rooij D, de Bruin A, De Cian M, Chaboissier M. 2020. Sox8 and Sox9 act redundantly for ovarian-to-testicular fate reprogramming in the absence of R-spondin1 in mouse sex reversals. Elife 9:e53972. https://doi.org/10.7554/eLife.53972.
   Google Scholar
• Nishant K, Ravishankar H, Rao M. 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
• Akhade V, Arun G, Donakonda S, Satyanarayana Rao M. 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
• Kataruka S, Akhade V, Kayyar B, Rao M. 2017. Mrhl long noncoding RNA mediates meiotic commitment of mouse spermatogonial cells by regulating Sox8 expression. Mol Cell Biol 37:e00632-16. https://doi.org/10.1128/MCB.00632-16.
   Google Scholar
• Akhade V, Dighe S, Kataruka S, Rao M. 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
• Mondal T, Subhash S, Vaid R, Enroth S, Uday S, Reinius B, Mitra S, Mohammed A, James A, Hoberg E, Moustakas A, Gyllensten U, Jones S, Gustafsson C, Sims A, 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
• Postepska-Igielska A, Giwojna A, Gasri-Plotnitsky L, Schmitt N, Dold A, Ginsberg D, Grummt I. 2015. LncRNA Khps1 regulates expression of the proto-oncogene SPHK1 via triplex-mediated changes in chromatin structure. Mol Cell 60:626–636. https://doi.org/10.1016/j.molcel.2015.10.001.
   PubMed Web of Science ®Google Scholar
• O'Leary VB, Ovsepian SV, Carrascosa LG, Buske FA, Radulovic V, Niyazi M, Moertl S, Trau M, Atkinson MJ, Anastasov N. 2015. PARTICLE, a triplex-forming long ncRNA, regulates locus-specific methylation in response to low-dose irradiation. Cell Rep 11:474–485. https://doi.org/10.1016/j.celrep.2015.03.043.
   PubMed Web of Science ®Google Scholar
• Schmitz K, Mayer C, Postepska A, Grummt I. 2010. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24:2264–2269. https://doi.org/10.1101/gad.590910.
   PubMed Web of Science ®Google Scholar
• Grote P, Herrmann B. 2013. The long non-coding RNA Fendrr links epigenetic control mechanisms to gene regulatory networks in mammalian embryogenesis. RNA Biol 10:1579–1585. https://doi.org/10.4161/rna.26165.
   PubMed Web of Science ®Google Scholar
• Ong C, Corces V. 2014. CTCF: an architectural protein bridging genome topology and function. Nat Rev Genet 15:234–246. https://doi.org/10.1038/nrg3663.
   PubMed Web of Science ®Google Scholar
• Saldaña-Meyer R, González-Buendía E, Guerrero G, Narendra V, Bonasio R, Recillas-Targa F, Reinberg D. 2014. CTCF regulates the human p53 gene through direct interaction with its natural antisense transcript, Wrap53. Genes Dev 28:723–734. https://doi.org/10.1101/gad.236869.113.
   PubMed Web of Science ®Google Scholar
• Saldaña-Meyer R, Rodriguez-Hernaez J, Escobar T, Nishana M, Jácome-López K, Nora E, Bruneau B, Tsirigos A, Furlan-Magaril M, Skok J, Reinberg D. 2019. RNA interactions are essential for CTCF-mediated genome organization. Mol Cell 76:412–422. https://doi.org/10.1016/j.molcel.2019.08.015.
   PubMed Web of Science ®Google Scholar
• Xiang J, Yin Q, Chen T, Zhang Y, Zhang X, Wu Z, Zhang S, Wang H, Ge J, Lu X, Yang L, Chen L. 2014. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res 24:513–531. https://doi.org/10.1038/cr.2014.35.
   PubMed Web of Science ®Google Scholar
• Yao H, Brick K, Evrard Y, Xiao T, Camerini-Otero R, Felsenfeld G. 2010. Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev 24:2543–2555. https://doi.org/10.1101/gad.1967810.
   PubMed Web of Science ®Google Scholar
• Pal D, Neha C, Bhaduri U, Zenia Z, Dutta S, Chidambaram S, Rao M. 2021. LncRNA Mrhl orchestrates differentiation programs in mouse embryonic stem cells through chromatin mediated regulation. Stem Cell Res 53:102250. https://doi.org/10.1016/j.scr.2021.102250.
   PubMed Web of Science ®Google Scholar
• Gonen N, Futtner C, Wood S, Garcia-Moreno S, Salamone I, Samson S, Sekido R, Poulat F, Maatouk D, Lovell-Badge R. 2018. Sex reversal following deletion of a single distal enhancer of Sox9. Science 360:1469–1473. https://doi.org/10.1126/science.aas9408.
   PubMed Web of Science ®Google Scholar
• Guth S, Bösl M, Sock E, Wegner M. 2010. Evolutionary conserved sequence elements with embryonic enhancer activity in the vicinity of the mammalian Sox8 gene. Int J Biochem Cell Biol 42:465–471. https://doi.org/10.1016/j.biocel.2009.07.008.
   PubMed Web of Science ®Google Scholar
• Garcia-Moreno S, Futtner C, Salamone I, Gonen N, Lovell-Badge R, Maatouk D. 2019. Gonadal supporting cells acquire sex-specific chromatin landscapes during mammalian sex determination. Dev Biol 446:168–179. https://doi.org/10.1016/j.ydbio.2018.12.023.
   PubMed Web of Science ®Google Scholar
• Ogbourne S, Antalis T. 1998. Transcriptional control and the role of silencers in transcriptional regulation in eukaryotes. Biochem J 331:1–14. https://doi.org/10.1042/bj3310001.
   PubMed Web of Science ®Google Scholar
• Singh AP, Harada S, Mishina Y. 2009. Downstream genes of Sox8 that would affect adult male fertility. Sex Dev 3:16–25. https://doi.org/10.1159/000200078.
   PubMed Web of Science ®Google Scholar
• Kojima M, de Rooij D, Page D. 2019. Amplification of a broad transcriptional program by a common factor triggers the meiotic cell cycle in mice. Elife 8:e43738. https://doi.org/10.7554/eLife.43738.
   Google Scholar
• Kalwa M, Hänzelmann S, Otto S, Kuo C, Franzen J, Joussen S, Fernandez-Rebollo E, Rath B, Koch C, Hofmann A, Lee S, Teschendorff A, Denecke B, Lin Q, Widschwendter M, Weinhold E, Costa I, Wagner W. 2016. The lncRNA HOTAIR impacts on mesenchymal stem cells via triple helix formation. Nucleic Acids Res 44:10631–10643. https://doi.org/10.1093/nar/gkw802.
   PubMed Web of Science ®Google Scholar
• Blank-Giwojna A, Postepska-Igielska A, Grummt I. 2019. lncRNA KHPS1 activates a poised enhancer by triplex-dependent recruitment of epigenomic regulators. Cell Rep 26:2904–2915. https://doi.org/10.1016/j.celrep.2019.02.059.
   PubMed Web of Science ®Google Scholar
• Yang Y, Li G. 2020. Post-translational modifications of PRC2: signals directing its activity. Epigenetics Chromatin 13:47. https://doi.org/10.1186/s13072-020-00369-1.
   PubMed Web of Science ®Google Scholar
• Kentepozidou E, Aitken S, Feig C, Stefflova K, Ibarra-Soria X, Odom D, Roller M, Flicek P. 2020. Clustered CTCF binding is an evolutionary mechanism to maintain topologically associating domains. Genome Biol 21:5. https://doi.org/10.1186/s13059-019-1894-x.
   PubMed Web of Science ®Google Scholar
• Essien K, Vigneau S, Apreleva S, Singh L, Bartolomei M, Hannenhalli S. 2009. CTCF binding site classes exhibit distinct evolutionary, genomic, epigenomic and transcriptomic features. Genome Biol 10:R131. https://doi.org/10.1186/gb-2009-10-11-r131.
   PubMed Web of Science ®Google Scholar
• Nishana M, Ha C, Rodriguez-Hernaez J, Ranjbaran A, Chio E, Nora E, Badri S, Kloetgen A, Bruneau B, Tsirigos A, Skok J. 2020. Defining the relative and combined contribution of CTCF and CTCFL to genomic regulation. Genome Biol 21:108. https://doi.org/10.1186/s13059-020-02024-0.
   PubMed Web of Science ®Google Scholar
• Pugacheva E, Kubo N, Loukinov D, Tajmul M, Kang S, Kovalchuk A, Strunnikov A, Zentner G, Ren B, Lobanenkov V. 2020. CTCF mediates chromatin looping via N-terminal domain-dependent cohesin retention. Proc Natl Acad Sci USA 117:2020–2031. https://doi.org/10.1073/pnas.1911708117.
   PubMed Web of Science ®Google Scholar
• Marino M, Rega C, Russo R, Valletta M, Gentile M, Esposito S, Baglivo I, De Feis I, Angelini C, Xiao T, Felsenfeld G, Chambery A, Pedone P. 2019. Interactome mapping defines BRG1, a component of the SWI/SNF chromatin remodeling complex, as a new partner of the transcriptional regulator CTCF. J Biol Chem 294:861–873. https://doi.org/10.1074/jbc.RA118.004882.
   PubMed Web of Science ®Google Scholar
• Fisher J, Peterson J, Reimer M, Stelloh C, Pulakanti K, Gerbec Z, Abel A, Strouse J, Strouse C, McNulty M, Malarkannan S, Crispino J, Milanovich S, Rao S. 2016. The cohesin subunit Rad21 is a negative regulator of hematopoietic self-renewal through epigenetic repression of HoxA7 and HoxA9. Blood 128:1708. https://doi.org/10.1182/blood.V128.22.1708.1708.
   Web of Science ®Google Scholar
• Wang J, Wang J, Yang L, Zhao C, Wu L, Xu L, Zhang F, Weng Q, Wegner M, Lu Q. 2020. CTCF-mediated chromatin looping in EGR2 regulation and SUZ12 recruitment critical for peripheral myelination and repair. Nat Commun 11:4133. https://doi.org/10.1038/s41467-020-17955-2.
   PubMed Web of Science ®Google Scholar
• Huang D, Petrykowska H, Miller B, Elnitski L, Ovcharenko I. 2019. Identification of human silencers by correlating cross-tissue epigenetic profiles and gene expression. Genome Res 29:657–667. https://doi.org/10.1101/gr.247007.118.
   PubMed Web of Science ®Google Scholar
• Croft B, Ohnesorg T, Hewitt J, Bowles J, Quinn A, Tan J, Corbin V, Pelosi E, van den Bergen J, Sreenivasan R, Knarston I, Robevska G, Vu D, Hutson J, Harley V, Ayers K, Koopman P, Sinclair A. 2019. Human sex reversal is caused by duplication or deletion of core enhancers upstream of Sox9. Nat Commun 10:3351. https://doi.org/10.1038/s41467-019-11310-w.
   PubMed Web of Science ®Google Scholar
• Pentland I, Campos-León K, Cotic M, Davies K, Wood C, Groves I, Burley M, Coleman N, Stockton J, Noyvert B, Beggs A, West M, Roberts S, Parish J. 2018. Disruption of CTCF-YY1–dependent looping of the human papillomavirus genome activates differentiation-induced viral oncogene transcription. PLoS Biol 16:e2005752. https://doi.org/10.1371/journal.pbio.2005752.
   Google Scholar
• Weintraub A, Li C, Zamudio A, Sigova A, Hannett N, Day D, Abraham B, Cohen M, Nabet B, Buckley D, Guo Y, Hnisz D, Jaenisch R, Bradner J, Gray N, Young R. 2017. YY1 is a structural regulator of enhancer-promoter loops. Cell 171:1573–1588. https://doi.org/10.1016/j.cell.2017.11.008.
   PubMed Web of Science ®Google Scholar
• Schaukowitch K, Joo J-Y, Kim T-K. 2017. UV-RNA immunoprecipitation (UV-RIP) protocol in neurons. Methods Mol Biol 1468:33–38. https://doi.org/10.1007/978-1-4939-4035-6_4.
   PubMedGoogle Scholar
• Spruce C, Dlamini S, Ananda G, Bronkema N, Tian H, Paigen K, Carter G, Baker C. 2020. HELLS and PRDM9 form a pioneer complex to open chromatin at meiotic recombination hot spots. Genes Dev 34:398–412. https://doi.org/10.1101/gad.333542.119.
   PubMed Web of Science ®Google Scholar
• Mumbach M, Rubin A, Flynn R, Dai C, Khavari P, Greenleaf W, Chang H. 2016. HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat Methods 13:919–922. https://doi.org/10.1038/nmeth.3999.
   PubMed Web of Science ®Google Scholar
• Naumova N, Smith E, Zhan Y, Dekker J. 2012. Analysis of long-range chromatin interactions using chromosome conformation capture. Methods 58:192–203. https://doi.org/10.1016/j.ymeth.2012.07.022.
   PubMed Web of Science ®Google Scholar
• Buske F, Bauer D, Mattick J, Bailey T. 2012. Triplexator: detecting nucleic acid triple helices in genomic and transcriptomic data. Genome Res 22:1372–1381. https://doi.org/10.1101/gr.130237.111.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg S. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923.
   PubMed Web of Science ®Google Scholar
• Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352.
   PubMed Web of Science ®Google Scholar
• Feng J, Liu T, Qin B, Zhang Y, Liu X. 2012. Identifying ChIP-seq enrichment using MACS. Nat Protoc 7:1728–1740. https://doi.org/10.1038/nprot.2012.101.
   PubMed Web of Science ®Google Scholar
• Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36.
   PubMed Web of Science ®Google Scholar
• Trapnell C, Williams B, Pertea G, Mortazavi A, Kwan G, van Baren M, Salzberg S, Wold B, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621.
   PubMed Web of Science ®Google Scholar
• Robinson J, Thorvaldsdóttir H, Winckler W, Guttman M, Lander E, Getz G, Mesirov J. 2011. Integrative genomics viewer. Nat Biotechnol 29:24–26. https://doi.org/10.1038/nbt.1754.
   PubMed Web of Science ®Google Scholar