The transcription factor TCFL5 responds to A-MYB to elaborate the male meiotic program in mice

in Reproduction
Authors:
Katharine Cecchini RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA

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Adriano Biasini RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA

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Tianxiong Yu Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, Massachusetts, USA

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Martin Säflund Department of Molecular Biosciences, The Wenner–Gren Institute, Stockholm University, Stockholm, Sweden

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Haiwei Mou Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA

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Amena Arif RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA
Beam Therapeutics, Cambridge, Massachusetts, USA

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Atiyeh Eghbali Department of Molecular Biosciences, The Wenner–Gren Institute, Stockholm University, Stockholm, Sweden

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Cansu Colpan RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA
Voyager Therapeutics, Cambridge, Massachusetts, USA

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Ildar Gainetdinov RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA

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Dirk G de Rooij Reproductive Biology Group, Division of Developmental Biology, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands

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Zhiping Weng Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, Massachusetts, USA

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Phillip D Zamore RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA

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https://orcid.org/0000-0002-4505-9618
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Deniz M Özata Department of Molecular Biosciences, The Wenner–Gren Institute, Stockholm University, Stockholm, Sweden

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https://orcid.org/0000-0001-5215-8684

Correspondence should be addressed to D M Ozata; Email: deniz.ozata@su.se

*(K Cecchini, A Biasini and T Yu contributed equally to this work)

DOI:
https://doi.org/10.1530/REP-22-0355
Volume/Issue:
Volume 165: Issue 2
Page Range:
183–196
Article Type:
Research Article
Online Publication Date:
04 Jan 2023
Copyright:
© Society for Reproduction and Fertility 2023
Restricted access
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In brief

The testis-specific transcription factor, TCFL5, expressed in pachytene spermatocytes regulates the meiotic gene expression program in collaboration with the transcription factor A-MYB.

Abstract

In male mice, the transcription factors STRA8 and MEISON initiate meiosis I. We report that STRA8/MEISON activates the transcription factors A-MYB and TCFL5, which together reprogram gene expression after spermatogonia enter into meiosis. TCFL5 promotes the transcription of genes required for meiosis, mRNA turnover, miR-34/449 production, meiotic exit, and spermiogenesis. This transcriptional architecture is conserved in rhesus macaque, suggesting TCFL5 plays a central role in meiosis and spermiogenesis in placental mammals. Tcfl5em1/em1 mutants are sterile, and spermatogenesis arrests at the mid- or late-pachytene stage of meiosis. Moreover, Tcfl5+/em1 mutants produce fewer motile sperm.

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Sept 2018 onwards Past Year Past 30 Days
Full Text Views 683 160 7
PDF Downloads 635 97 12

 

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Alon U 2007 Network motifs: theory and experimental approaches. Nature Reviews. Genetics 8 450–461. (https://doi.org/10.1038/nrg2102)

  • Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S & Nakano T et al.2006 A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442 203–207. (https://doi.org/10.1038/nature04916)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, Bestor T & Hannon GJ 2008 A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Molecular Cell 31 785–799. (https://doi.org/10.1016/j.molcel.2008.09.003)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K & Hannon GJ 2007 Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316 744–747. (https://doi.org/10.1126/science.1142612)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bao J, Li D, Wang L, Wu J, Hu Y, Wang Z, Chen Y, Cao X, Jiang C & Yan W et al.2012 MicroRNA-449 and microRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. Journal of Biological Chemistry 287 21686–21698. (https://doi.org/10.1074/jbc.M111.328054)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bastos H, Lassalle B, Chicheportiche A, Riou L, Testart J, Allemand I & Fouchet P 2005 Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry. Part A 65 40–49. (https://doi.org/10.1002/cyto.a.20129)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Beckers A, Ott T, Schuster-Gossler K, Boldt K, Alten L, Ueffing M, Blum M & Gossler A 2018 The evolutionary conserved FOXJ1 target gene Fam183b is essential for motile cilia in Xenopus but dispensable for ciliary function in mice. Scientific Reports 8 14678. (https://doi.org/10.1038/s41598-018-33045-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bhattacharya A & Baker NE 2011 A network of broadly expressed HLH genes regulates tissue-specific cell fates. Cell 147 881–892. (https://doi.org/10.1016/j.cell.2011.08.055)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bolcun-Filas E, Bannister LA, Barash A, Schimenti KJ, Hartford SA, Eppig JJ, Handel MA, Shen L & Schimenti JC 2011 A-MYB (MYBL1) transcription factor is a master regulator of male meiosis. Development 138 3319–3330. (https://doi.org/10.1242/dev.067645)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Comazzetto S, Di Giacomo M, Rasmussen KD, Much C, Azzi C, Perlas E, Morgan M & O’Carroll D 2014 Oligoasthenoteratozoospermia and infertility in mice deficient for miR-34b/c and miR-449 loci. PLOS Genetics 10 e1004597. (https://doi.org/10.1371/journal.pgen.1004597)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Endo T, Freinkman E, de Rooij DG & Page DC 2017 Periodic production of retinoic acid by meiotic and somatic cells coordinates four transitions in mouse spermatogenesis. Proceedings of the National Academy of Sciences of the United States of America 114 E10132–E10141. (https://doi.org/10.1073/pnas.1710837114)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Endo T, Romer KA, Anderson EL, Baltus AE, de Rooij DG & Page DC 2015 Periodic retinoic acid-STRA8 signaling intersects with periodic germ-cell competencies to regulate spermatogenesis. Proceedings of the National Academy of Sciences of the United States of America 112 E2347–E2356. (https://doi.org/10.1073/pnas.1505683112)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Feng CA, Spiller C, Merriner DJ, O’Bryan MK, Bowles J & Koopman P 2017 SOX30 is required for male fertility in mice. Scientific Reports 7 17619. (https://doi.org/10.1038/s41598-017-17854-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K & Zhang Y 2002 Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Current Biology 12 1052–1058. (https://doi.org/10.1016/s0960-9822(0200901-6)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gainetdinov I, Colpan C, Arif A, Cecchini K & Zamore PD 2018 A single mechanism of biogenesis, initiated and directed by PIWI proteins, explains piRNA production in most animals. Molecular Cell 71 775–790.e5. (https://doi.org/10.1016/j.molcel.2018.08.007)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Galán-Martínez J, Berenguer I, Del Carmen Maza M, Stamatakis K, Gironès N & Fresno M 2022 TCFL5 deficiency impairs the pachytene to diplotene transition during spermatogenesis in the mouse. Scientific Reports 12 10956. (https://doi.org/10.1038/s41598-022-15167-w)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Godfrey L, Crump NT, Thorne R, Lau IJ, Repapi E, Dimou D, Smith AL, Harman JR, Telenius JM & Oudelaar AM et al.2019 DOT1L inhibition reveals a distinct subset of enhancers dependent on H3K79 methylation. Nature Communications 10 2803. (https://doi.org/10.1038/s41467-019-10844-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Goodson SG, Zhang Z, Tsuruta JK, Wang W & O’Brien DA 2011 Classification of mouse sperm motility patterns using an automated multiclass support vector machines model. Biology of Reproduction 84 1207–1215. (https://doi.org/10.1095/biolreprod.110.088989)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Grunewald S, Paasch U, Glander HJ & Anderegg U 2005 Mature human spermatozoa do not transcribe novel RNA. Andrologia 37 69–71. (https://doi.org/10.1111/j.1439-0272.2005.00656.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Handel MA & Schimenti JC 2010 Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nature Reviews. Genetics 11 124–136. (https://doi.org/10.1038/nrg2723)

  • Horisawa-Takada Y, Kodera C, Takemoto K, Sakashita A, Horisawa K, Maeda R, Shimada R, Usuki S, Fujimura S & Tani N et al.2021 Meiosis-specific ZFP541 repressor complex promotes developmental progression of meiotic prophase towards completion during mouse spermatogenesis. Nature Communications 12 3184. (https://doi.org/10.1038/s41467-021-23378-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ishiguro KI, Matsuura K, Tani N, Takeda N, Usuki S, Yamane M, Sugimoto M, Fujimura S, Hosokawa M & Chuma S et al.2020 MEIOSIN directs the switch from mitosis to meiosis in mammalian germ cells. Developmental Cell 52 429–445.e10. (https://doi.org/10.1016/j.devcel.2020.01.010)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kierszenbaum AL & Tres LL 1975 Structural and transcriptional features of the mouse spermatid genome. Journal of Cell Biology 65 258–270. (https://doi.org/10.1083/jcb.65.2.258)

  • Kojima ML, de Rooij DG & Page DC 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)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y & Ijiri TW et al.2008 DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes and Development 22 908–917. (https://doi.org/10.1101/gad.1640708)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Langmead B & Salzberg SL 2012 Fast gapped-read alignment with Bowtie 2. Nature Methods 9 357–359. (https://doi.org/10.1038/nmeth.1923)

  • Lascarez-Lagunas LI, Herruzo E, Grishok A, San-Segundo PA & Colaiácovo MP 2020 DOT-1.1-dependent H3K79 methylation promotes normal meiotic progression and meiotic checkpoint function in C. elegans. PLOS Genetics 16 e1009171. (https://doi.org/10.1371/journal.pgen.1009171)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J, Moore MJ, Schimenti JC & Weng Z et al.2013 An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Molecular Cell 50 67–81. (https://doi.org/10.1016/j.molcel.2013.02.016)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Maezawa S, Sakashita A, Yukawa M, Chen X, Takahashi K, Alavattam KG, Nakata I, Weirauch MT, Barski A & Namekawa SH 2020 Super-enhancer switching drives a burst in gene expression at the mitosis-to-meiosis transition. Nature Structural and Molecular Biology 27 978–988. (https://doi.org/10.1038/s41594-020-0488-3)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B & Moreilhon C et al.2011 Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nature Cell Biology 13 693–699. (https://doi.org/10.1038/ncb2241)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Maruyama O, Nishimori H, Katagiri T, Miki Y, Ueno A & Nakamura Y 1998 Cloning of TCFL5 encoding a novel human basic helix-loop-helix motif protein that is specifically expressed in primary spermatocytes at the pachytene stage. Cytogenetics and Cell Genetics 82 41–45. (https://doi.org/10.1159/000015061)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Meers MP, Tenenbaum D & Henikoff S 2019 Peak calling by Sparse Enrichment Analysis for CUT&RUN chromatin profiling. Epigenetics and Chromatin 12 42. (https://doi.org/10.1186/s13072-019-0287-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Merkin J, Russell C, Chen P & Burge CB 2012 Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science 338 1593–1599. (https://doi.org/10.1126/science.1228186)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Morgan M, Kabayama Y, Much C, Ivanova I, Di Giacomo M, Auchynnikava T, Monahan JM, Vitsios DM, Vasiliauskaitė L & Comazzetto S et al.2019 A programmed wave of uridylation-primed mRNA degradation is essential for meiotic progression and mammalian spermatogenesis. Cell Research 29 221–232. (https://doi.org/10.1038/s41422-018-0128-1)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ostermeier GC, Dix DJ, Miller D, Khatri P & Krawetz SA 2002 Spermatozoal RNA profiles of normal fertile men. Lancet 360 772–777. (https://doi.org/10.1016/S0140-6736(0209899-9)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Oura S, Koyano T, Kodera C, Horisawa-Takada Y, Matsuyama M, Ishiguro KI & Ikawa M 2021 KCTD19 and its associated protein ZFP541 are independently essential for meiosis in male mice. PLOS Genetics 17 e1009412. (https://doi.org/10.1371/journal.pgen.1009412)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ozata DM, Gainetdinov I, Zoch A, O’Carroll D & Zamore PD 2019 PIWI-interacting RNAs: small RNAs with big functions. Nature Reviews. Genetics 20 89–108. (https://doi.org/10.1038/s41576-018-0073-3)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Özata DM, Yu T, Mou H, Gainetdinov I, Colpan C, Cecchini K, Kaymaz Y, Wu PH, Fan K & Kucukural A et al.2020 Evolutionarily conserved pachytene piRNA loci are highly divergent among modern humans. Nature Ecology and Evolution 4 156–168. (https://doi.org/10.1038/s41559-019-1065-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Payen E, Verkerk T, Michalovich D, Dreyer SD, Winterpacht A, Lee B, De Zeeuw CI, Grosveld F & Galjart N 1998 The centromeric/nucleolar chromatin protein ZFP-37 may function to specify neuronal nuclear domains. Journal of Biological Chemistry 273 9099–9109. (https://doi.org/10.1074/jbc.273.15.9099)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sakashita A, Maezawa S, Takahashi K, Alavattam KG, Yukawa M, Hu YC, Kojima S, Parrish NF, Barski A & Pavlicev M et al.2020 Endogenous retroviruses drive species-specific germline transcriptomes in mammals. Nature Structural and Molecular Biology 27 967–977. (https://doi.org/10.1038/s41594-020-0487-4)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shively CA, Liu J, Chen X, Loell K & Mitra RD 2019 Homotypic cooperativity and collective binding are determinants of bHLH specificity and function. Proceedings of the National Academy of Sciences of the United States of America 116 16143–16152. (https://doi.org/10.1073/pnas.1818015116)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Siep M, Sleddens-Linkels E, Mulders S, van Eenennaam H, Wassenaar E, Van Cappellen WA, Hoogerbrugge J, Grootegoed JA & Baarends WM 2004 Basic helix-loop-helix transcription factor Tcfl5 interacts with the calmegin gene promoter in mouse spermatogenesis. Nucleic Acids Research 32 6425–6436. (https://doi.org/10.1093/nar/gkh979)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Song R, Walentek P, Sponer N, Klimke A, Lee JS, Dixon G, Harland R, Wan Y, Lishko P & Lize M et al.2014 miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110. Nature 510 115–120. (https://doi.org/10.1038/nature13413)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Stubbs JL, Oishi I, Izpisúa Belmonte JC & Kintner C 2008 The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nature Genetics 40 1454–1460. (https://doi.org/10.1038/ng.267)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tachibana M, Nozaki M, Takeda N & Shinkai Y 2007 Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO Journal 26 3346–3359. (https://doi.org/10.1038/sj.emboj.7601767)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wu J, Bao J, Kim M, Yuan S, Tang C, Zheng H, Mastick GS, Xu C & Yan W 2014 Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proceedings of the National Academy of Sciences of the United States of America 111 E2851–E2857. (https://doi.org/10.1073/pnas.1407777111)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wu Y, Hu X, Li Z, Wang M, Li S, Wang X, Lin X, Liao S, Zhang Z & Feng X et al.2016 Transcription factor RFX2 is a key regulator of mouse spermiogenesis. Scientific Reports 6 20435. (https://doi.org/10.1038/srep20435)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Xu W, Zhang Y, Qin D, Gui Y, Wang S, Du G, Yang F, Li L, Yuan S & Wang M et al.2022 Transcription factor-like 5 is a potential DNA- and RNA-binding protein essential for maintaining male fertility in mice. Journal of Cell Science 135 jcs259036. (https://doi.org/10.1242/jcs.259036)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu T, Biasini A, Cecchini K, Saflund M, Mou H, Arif A, Eghbali A, de Rooij D, Weng Z & Zamore PD et al.2022 A-MYB/TCFL5 regulatory architecture ensures the production of pachytene piRNAs in placental mammals. RNA 079472.122. (https://doi.org/10.1261/rna.079472.122)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu T, Fan K, Özata DM, Zhang G, Fu Y, Theurkauf WE, Zamore PD & Weng Z 2021 Long first exons and epigenetic marks distinguish conserved pachytene piRNA clusters from other mammalian genes. Nature Communications 12 73. (https://doi.org/10.1038/s41467-020-20345-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu X, Ng CP, Habacher H & Roy S 2008 Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nature Genetics 40 1445–1453. (https://doi.org/10.1038/ng.263)

  • Zhang D, Xie D, Lin X, Ma L, Chen J, Zhang D, Wang Y, Duo S, Feng Y & Zheng C et al.2018 The transcription factor SOX30 is a key regulator of mouse spermiogenesis. Development 145 dev164723. (https://doi.org/10.1242/dev.164723)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M & Li W et al.2008 Model-based analysis of ChIP-Seq (MACS). Genome Biology 9 R137. (https://doi.org/10.1186/gb-2008-9-9-r137)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhou Q, Li Y, Nie R, Friel P, Mitchell D, Evanoff RM, Pouchnik D, Banasik B, McCarrey JR & Small C et al.2008 Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biology of Reproduction 78 537–545. (https://doi.org/10.1095/biolreprod.107.064337)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation