Dynamic and regulated TAF gene expression during mouse embryonic germ cell development

English version

Autoři: Megan A. Gura ^aff001; Maria M. Mikedis ^aff002; Kimberly A. Seymour ^aff001; Dirk G. de Rooij ^aff002; David C. Page ^aff002; Richard N. Freiman ^aff001
Působiště autorů: Brown University, MCB Graduate Program and Department of Molecular Biology, Cell Biology and Biochemistry, Providence, RI, United States of America ^aff001; Whitehead Institute, Cambridge, MA, United States of America ^aff002; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, United States of America ^aff003; Howard Hughes Medical Institute, Whitehead Institute, Cambridge, MA, United States of America ^aff004
Vyšlo v časopise: Dynamic and regulated TAF gene expression during mouse embryonic germ cell development. PLoS Genet 16(1): e1008515. doi:10.1371/journal.pgen.1008515
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008515

Souhrn

Germ cells undergo many developmental transitions before ultimately becoming either eggs or sperm, and during embryonic development these transitions include epigenetic reprogramming, quiescence, and meiosis. To begin understanding the transcriptional regulation underlying these complex processes, we examined the spatial and temporal expression of TAF4b, a variant TFIID subunit required for fertility, during embryonic germ cell development. By analyzing published datasets and using our own experimental system to validate these expression studies, we determined that both Taf4b mRNA and protein are highly germ cell-enriched and that Taf4b mRNA levels dramatically increase from embryonic day 12.5–18.5. Surprisingly, additional mRNAs encoding other TFIID subunits are coordinately upregulated through this time course, including Taf7l and Taf9b. The expression of several of these germ cell-enriched TFIID genes is dependent upon Dazl and/or Stra8, known regulators of germ cell development and meiosis. Together, these data suggest that germ cells employ a highly specialized and dynamic form of TFIID to drive the transcriptional programs that underlie mammalian germ cell development.

Klíčová slova:

Gene expression – Germ cells – Gonads – Meiosis – Messenger RNA – Mouse models – Ovaries – Spermatocytes

Zdroje

1. Chandra A, Copen CE, Stephen EH. Infertility and impaired fecundity in the United States, 1982–2010: data from the National Survey of Family Growth. Natl Health Stat Report. 2013; doi: 10.1093/humrep/des207

2. Nelson LM. Clinical practice. Primary ovarian insufficiency. N Engl J Med. 2009;360: 606–14. doi: 10.1056/NEJMcp0808697 19196677

3. Rossetti R, Ferrari I, Bonomi M, Persani L. Genetics of primary ovarian insufficiency. Clinical Genetics. 2017. pp. 183–198. doi: 10.1111/cge.12921 27861765

4. Grive KJ, Seymour K a., Mehta R, Freiman RN. TAF4b promotes mouse primordial follicle assembly and oocyte survival. Dev Biol. Elsevier; 2014;392: 42–51. doi: 10.1016/j.ydbio.2014.05.001 24836512

5. Freiman RN, Albright SR, Zheng S, Sha WC, Hammer RE, Tjian R. Requirement of tissue-selective TBP-associated factor TAFII105 in ovarian development. Science. 2001;293: 2084–2087. doi: 10.1126/science.1061935 11557891

6. Lovasco LA, Gustafson EA, Seymour KA, De Rooij DG, Freiman RN. TAF4b is required for mouse spermatogonial stem cell development. Stem Cells. 2015;33: 1267–1276. doi: 10.1002/stem.1914 25727968

7. Knauff EAH, Franke L, van Es MA, van den Berg LH, van der Schouw YT, Laven JSE, et al. Genome-wide association study in premature ovarian failure patients suggests ADAMTS19 as a possible candidate gene. Hum Reprod. 2009;24: 2372–8. doi: 10.1093/humrep/dep197 19508998

8. Di Pietro C, Vento M, Ragusa M, Barbagallo D, Guglielmino MR, Maniscalchi T, et al. Expression analysis of TFIID in single human oocytes: new potential molecular markers of oocyte quality. Reprod Biomed Online. 2008;17: 338–49. doi: 10.1016/s1472-6483(10)60217-9 18765004

9. Ayhan Ö, Balkan M, Guven A, Hazan R, Atar M, Tok A, et al. Truncating mutations in TAF4B and ZMYND15 causing recessive azoospermia. J Med Genet. 2014; doi: 10.1136/jmedgenet-2013-102102 24431330

10. Antonova S V., Boeren J, Timmers HTM, Snel B. Epigenetics and transcription regulation during eukaryotic diversification: the saga of TFIID. Genes Dev. 2019;33: 1–15. doi: 10.1101/gad.322990.118

11. Grive KJ, Gustafson EA, Seymour KA, Baddoo M, Schorl C, Golnoski K, et al. TAF4b Regulates Oocyte-Specific Genes Essential for Meiosis. PLoS Genet. 2016;12: 1–18. doi: 10.1371/journal.pgen.1006128 27341508

12. Li H, Liang Z, Yang J, Wang D, Wang H, Zhu M, et al. DAZL is a master translational regulator of murine spermatogenesis. Natl Sci Rev. 2019; doi: 10.1093/nsr/nwy163 31355046

13. Zagore LL, Sweet TJ, Hannigan MM, Weyn-Vanhentenryck SM, Jobava R, Hatzoglou M, et al. DAZL Regulates Germ Cell Survival through a Network of PolyA-Proximal mRNA Interactions. Cell Rep. 2018; doi: 10.1016/j.celrep.2018.10.012 30380414

14. Kojima ML, de Rooij DG, Page DC. Amplification of a broad transcriptional program by a common factor triggers the meiotic cell cycle in mice. Elife. 2019; doi: 10.7554/elife.43738 30810530

15. Falender AE, Freiman RN, Geles KG, Lo KC, Hwang KS, Lamb DJ, et al. Maintenance of spermatogenesis requires TAF4b, a gonad-specific subunit of TFIID. Genes Dev. 2005; doi: 10.1101/gad.1290105 15774719

16. Gura MA, Freiman RN. Primordial Follicle. Encycl Reprod. Elsevier; 2018; 65–71. doi: 10.1016/B978-0-12-801238-3.64394–5

17. Cheng Y, Buffone MG, Kouadio M, Goodheart M, Page DC, Gerton GL, et al. Abnormal Sperm in Mice Lacking the Taf7l Gene. Mol Cell Biol. 2007; doi: 10.1128/mcb.01722-06 17242199

18. Zhou H, Grubisic I, Zheng K, He Y, Wang PJ, Kaplan T, et al. Taf7l cooperates with Trf2 to regulate spermiogenesis. Proc Natl Acad Sci. 2013; doi: 10.1073/pnas.1317034110 24082143

19. Sangrithi MN, Royo H, Mahadevaiah SK, Ojarikre O, Bhaw L, Sesay A, et al. Non-Canonical and Sexually Dimorphic X Dosage Compensation States in the Mouse and Human Germline. Dev Cell. 2017; doi: 10.1016/j.devcel.2016.12.023 28132849

20. Yoshimizu T, Sugiyama N, Felice M De, Ii Y, Ohbo K, Masuko K, et al. Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev Growth, Differ. 1999;41: 675–684. Available: https://doi.org/10.1046/j.1440-169x.1999.00474.x

21. Gkountela S, Zhang KX, Shafiq TA, Liao WW, Hargan-Calvopiña J, Chen PY, et al. DNA demethylation dynamics in the human prenatal germline. Cell. 2015;161: 1425–1436. doi: 10.1016/j.cell.2015.05.012 26004067

22. Irie N, Weinberger L, Tang WWC, Kobayashi T, Viukov S, Manor YS, et al. SOX17 is a critical specifier of human primordial germ cell fate. Cell. 2015; doi: 10.1016/j.cell.2014.12.013 25543152

23. Tang WWC, Dietmann S, Irie N, Leitch HG, Floros VI, Bradshaw CR, et al. A Unique Gene Regulatory Network Resets the Human Germline Epigenome for Development. Cell. 2015; doi: 10.1016/j.cell.2015.04.053 26046444

24. Fischer DS, Theis FJ, Yosef N. Impulse model-based differential expression analysis of time course sequencing data. Nucleic Acids Res. 2018; doi: 10.1093/nar/gky675 30102402

25. Soh YQS, Junker JP, Gill ME, Mueller JL, van Oudenaarden A, Page DC. A Gene Regulatory Program for Meiotic Prophase in the Fetal Ovary. PLoS Genet. 2015;11. doi: 10.1371/journal.pgen.1005531 26378784

26. De Gasperi R, Rocher AB, Sosa MAG, Wearne SL, Perez GM, Friedrich VL, et al. The IRG mouse: A two-color fluorescent reporter for assessing Cre-mediated recombination and imaging complex cellular relationships in situ. Genesis. 2008; doi: 10.1002/dvg.20400 18543298

27. Huppertz I, Attig J, D’Ambrogio A, Easton LE, Sibley CR, Sugimoto Y, et al. iCLIP: Protein-RNA interactions at nucleotide resolution. Methods. 2014;65: 274–287. doi: 10.1016/j.ymeth.2013.10.011 24184352

28. van Pelt AM, de Rooij DG. Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol Reprod. 1990;43: 363–67. doi: 10.1095/biolreprod43.3.363 2271719

29. Endo T, Romer KA, Anderson EL, Baltus AE, de Rooij DG, Page DC. Periodic retinoic acid-STRA8 signaling intersects with periodic germ-cell competencies to regulate spermatogenesis. Proc Natl Acad Sci U S A. 2015;112: E2347–56. doi: 10.1073/pnas.1505683112 25902548

30. Russell LD, Ettlin RA, Hikim APS, Clegg ED. Histological and Histopathological Evaluation of the Testis. Int J Androl. 1993; doi: 10.1111/j.1365-2605.1993.tb01156.x

31. Rosario R, Smith RWP, Adams IR, Anderson RA. RNA immunoprecipitation identifies novel targets of DAZL in human foetal ovary. Mol Hum Reprod. 2017; doi: 10.1093/molehr/gax004 28364521

32. Reynolds N, Collier B, Maratou K, Bingham V, Speed RM, Taggart M, et al. Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells. Hum Mol Genet. 2005; doi: 10.1093/hmg/ddi414 16278232

33. Reynolds N, Collier B, Bingham V, Gray NK, Cooke HJ. Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA. 2007; doi: 10.1261/rna.465507 17526644

34. Martins JPS, Liu X, Oke A, Arora R, Franciosi F, Viville S, et al. DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation. J Cell Sci. 2016; doi: 10.1242/jcs.179218 26826184

35. Jenkins HT, Malkova B, Edwards TA. Kinked β-strands mediate high-affinity recognition of mRNA targets by the germ-cell regulator DAZL. Proc Natl Acad Sci U S A. 2011; doi: 10.1073/pnas.1105211108 22021443

36. Miyauchi H, Ohta H, Nagaoka S, Nakaki F, Sasaki K, Hayashi K, et al. Bone morphogenetic protein and retinoic acid synergistically specify female germ‐cell fate in mice. EMBO J. 2017; doi: 10.15252/embj.201796875 28928204

37. Koutelou E, Hirsch CL, Dent SYR. Multiple faces of the SAGA complex. Current Opinion in Cell Biology. 2010. doi: 10.1016/j.ceb.2010.03.005 20363118

38. Sisakhtnezhad S, Heshmati P. Comparative analysis of single-cell RNA sequencing data from mouse spermatogonial and mesenchymal stem cells to identify differentially expressed genes and transcriptional regulators of germline cells. J Cell Physiol. 2018; doi: 10.1002/jcp.26303 29194616

39. Percharde M, Wong P, Ramalho-Santos M. Global Hypertranscription in the Mouse Embryonic Germline. Cell Rep. 2017; doi: 10.1016/j.celrep.2017.05.036 28591571

40. Herrera FJ, Yamaguchi T, Roelink H, Tjian R. Core promoter factor TAF9B regulates neuronal gene expression. Elife. 2014; doi: 10.7554/elife.02559 25006164

41. Zhou H, Kaplan T, Li Y, Grubisic I, Zhang Z, Wang PJ, et al. Dual functions of TAF7L in adipocyte differentiation. Elife. 2013; doi: 10.7554/eLife.00170 23326641

42. Zhou H, Wan B, Grubisic I, Kaplan T, Tjian R. TAF7L modulates brown adipose tissue formation. Elife. 2014; doi: 10.7554/eLife.02811 24876128

43. Hill PWS, Leitch HG, Requena CE, Sun Z, Amouroux R, Roman-Trufero M, et al. Epigenetic reprogramming enables the transition from primordial germ cell to gonocyte. Nature. 2018; doi: 10.1038/nature25964 29513657

44. Hermann BP, Cheng K, Singh A, Roa-De La Cruz L, Mutoji KN, Chen IC, et al. The Mammalian Spermatogenesis Single-Cell Transcriptome, from Spermatogonial Stem Cells to Spermatids. Cell Rep. 2018; doi: 10.1016/j.celrep.2018.10.026 30404016

45. Hiller M. Testis-specific TAF homologs collaborate to control a tissue-specific transcription program. Development. 2004; doi: 10.1242/dev.01314 15456720

46. Lago C, Clerici E, Mizzi L, Colombo L, Kater MM. TBP-associated factors in Arabidopsis. Gene. 2004; doi: 10.1016/j.gene.2004.08.023 15527982

47. Lawrence EJ, Gao H, Tock AJ, Lambing C, Blackwell AR, Feng X, et al. Natural Variation in TBP-ASSOCIATED FACTOR 4b Controls Meiotic Crossover and Germline Transcription in Arabidopsis. Curr Biol. 2019; doi: 10.1016/j.cub.2019.06.084 31378616

48. Andrews S. FastQC: A quality control tool for high throughput sequence data. In: Http://Www.Bioinformatics.Babraham.Ac.Uk/Projects/Fastqc/. 2010 p. http://www.bioinformatics.babraham.ac.uk/projects/. citeulike-article-id:11583827

49. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016; doi: 10.1038/nprot.2016.095 27560171

50. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

51. Anders S, Pyl PT, Huber W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics. 2015; doi: 10.1093/bioinformatics/btu638 25260700

52. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281

53. Wickham H. ggplot2: Elegant Graphics for Data Analysis [Internet]. 2nd ed. Wiley Interdisciplinary Reviews: Computational Statistics. Springer-Verlag; 2016. Available: ggplot.org doi: 10.1002/wics.1383 29657666

54. Ge SX, Son EW, Yao R. iDEP: An integrated web application for differential expression and pathway analysis of RNA-Seq data. BMC Bioinformatics. 2018; doi: 10.1186/s12859-018-2486-6 30567491

55. Hogarth CA, Evanoff R, Mitchell D, Kent T, Small C, Amory JK, et al. Turning a Spermatogenic Wave into a Tsunami: Synchronizing Murine Spermatogenesis Using WIN 18,4461. Biol Reprod. 2013; doi: 10.1095/biolreprod.112.105346 23284139

56. Romer KA, de Rooij DG, Kojima ML, Page DC. Isolating mitotic and meiotic germ cells from male mice by developmental synchronization, staging, and sorting. Dev Biol. 2018; doi: 10.1016/j.ydbio.2018.08.009 30149006

57. Oulad-Abdelghani M, Bouillet P, Décimo D, Gansmuller A, Heyberger S, Dollé P, et al. Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J Cell Biol. 1996;135: 469–477. doi: 10.1083/jcb.135.2.469 8896602

58. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, et al. Expression of Stimulated by Retinoic Acid Gene 8 (Stra8) in Spermatogenic Cells Induced by Retinoic Acid: An In Vivo Study in Vitamin A-Sufficient Postnatal Murine Testes1. Biol Reprod. 2008; doi: 10.1095/biolreprod.107.066795 18322276

59. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011; doi: 10.14806/ej.17.1.200

60. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29: 15–21. doi: 10.1093/bioinformatics/bts635 23104886

61. König J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol. 2010;17: 909–915. doi: 10.1038/nsmb.1838 20601959

62. Kucukural A, Ozadam H, Singh G, Moore MJ, Cenik C. ASPeak: an abundance sensitive peak detection algorithm for RIP-Seq. Bioinformatics. 2013;29: 2485–2486. doi: 10.1093/bioinformatics/btt428 23929032

63. McLeay RC, Bailey TL. Motif Enrichment Analysis: a unified framework and an evaluation on ChIP data. BMC Bioinformatics. 2010;11: 165. doi: 10.1186/1471-2105-11-165 20356413

64. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 22388286

65. Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; doi: 10.1093/bioinformatics/btq033 20110278

66. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29: 24–26. doi: 10.1038/nbt.1754 21221095

67. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9: R137. doi: 10.1186/gb-2008-9-9-r137 18798982