DNA Demethylation and USF Regulate the Meiosis-Specific Expression of the Mouse

English version České info

Miwi, a member of the Argonaute family, is required for initiating spermiogenesis; however, the mechanisms that regulate the expression of the Miwi gene remain unknown. By mutation analysis and transgenic models, we identified a 303 bp proximal promoter region of the mouse Miwi gene, which controls specific expression from midpachytene spermatocytes to round spermatids during meiosis. We characterized the binding sites of transcription factors NF-Y (Nuclear Factor Y) and USF (Upstream Stimulatory Factor) within the core promoter and found that both factors specifically bind to and activate the Miwi promoter. Methylation profiling of three CpG islands within the proximal promoter reveals a markedly inverse correlation between the methylation status of the CpG islands and germ cell type–specific expression of Miwi. CpG methylation at the USF–binding site within the E2 box in the promoter inhibits the binding of USF. Transgenic Miwi-EGFP and endogenous Miwi reveal a subcellular co-localization pattern in the germ cells of the Miwi-EGFP transgenic mouse. Furthermore, the DNA methylation profile of the Miwi promoter–driven transgene is consistent with that of the endogenous Miwi promoter, indicating that Miwi transgene is epigenetically modified through methylation in vivo to ensure its spatio-temporal expression. Our findings suggest that USF controls Miwi expression from midpachytene spermatocytes to round spermatids through methylation-mediated regulation. This work identifies an epigenetic regulation mechanism for the spatio-temporal expression of mouse Miwi during spermatogenesis.

Vyšlo v časopise: DNA Demethylation and USF Regulate the Meiosis-Specific Expression of the Mouse. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002716
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002716

Souhrn

Zdroje

1. TanakaHBabaT 2005 Gene expression in spermiogenesis. Cell Mol Life Sci 62 344 354

2. OakesCCLa SalleSSmiragliaDJRobaireBTraslerJM 2007 A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci U S A 104 228 233

3. OakesCCLa SalleSSmiragliaDJRobaireBTraslerJM 2007 Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol 307 368 379

4. MaatoukDMKellamLDMannMRLeiHLiE 2006 DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 133 3411 3418

5. FajardoMAHaugenHSCleggCHBraunRE 1997 Separate elements in the 3′ untranslated region of the mouse protamine 1 mRNA regulate translational repression and activation during murine spermatogenesis. Dev Biol 191 42 52

6. GiorginiFDaviesHGBraunRE 2002 Translational repression by MSY4 inhibits spermatid differentiation in mice. Development 129 3669 3679

7. YangJMedvedevSReddiPPSchultzRMHechtNB 2005 The DNA/RNA-binding protein MSY2 marks specific transcripts for cytoplasmic storage in mouse male germ cells. Proc Natl Acad Sci U S A 102 1513 1518

8. ZhaoWZhouFZhouXHouYHeY 2010 Mago, a vertebrate homolog of Drosophila Mago nashi protein, is a component of the chromatoid body in the cytoplasm of the postmeiotic spermatid. J Exp Zool B Mol Dev Evol 314 232 241

9. Valencia-SanchezMALiuJHannonGJParkerR 2006 Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20 515 524

10. DengWLinH 2002 miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2 819 830

11. GirardASachidanandamRHannonGJCarmellMA 2006 A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442 199 202

12. GrivnaSTBeyretEWangZLinH 2006 A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20 1709 1714

13. WatanabeTTakedaATsukiyamaTMiseKOkunoT 2006 Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 20 1732 1743

14. GrivnaSTPyhtilaBLinH 2006 MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A 103 13415 13420

15. Kuramochi-MiyagawaSKimuraTYomogidaKKuroiwaATadokoroY 2001 Two mouse piwi-related genes: miwi and mili. Mech Dev 108 121 133

16. KotajaNBhattacharyyaSNJaskiewiczLKimminsSParvinenM 2006 The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci U S A 103 2647 2652

17. KojimaKKuramochi-MiyagawaSChumaSTanakaTNakatsujiN 2009 Associations between PIWI proteins and TDRD1/MTR-1 are critical for integrated subcellular localization in murine male germ cells. Genes Cells 14 1155 1165

18. ChenCJinJJamesDAAdams-CioabaMAParkJG 2009 Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi. Proc Natl Acad Sci U S A 106 20336 20341

19. VaginVVWohlschlegelJQuJJonssonZHuangX 2009 Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 23 1749 1762

20. SiomiMCMannenTSiomiH 2010 How does the royal family of Tudor rule the PIWI-interacting RNA pathway? Genes Dev 24 636 646

21. MantovaniRLiXYPessaraUHooft van HuisjduijnenRBenoistC 1994 Dominant negative analogs of NF-YA. J Biol Chem 269 20340 20346

22. QyangYLuoXLuTIsmailPMKrylovD 1999 Cell-type-dependent activity of the ubiquitous transcription factor USF in cellular proliferation and transcriptional activation. Mol Cell Biol 19 1508 1517

23. LuoXSawadogoM 1996 Functional domains of the transcription factor USF2: atypical nuclear localization signals and context-dependent transcriptional activation domains. Mol Cell Biol 16 1367 1375

24. NicholasCRXuEYBananiSFHammerREHamraFK 2009 Characterization of a Dazl-GFP germ cell-specific reporter. Genesis 47 74 84

25. BartellJGDavisTKremerEJDeweyMJKistlerWS 1996 Expression of the rat testis-specific histone H1t gene in transgenic mice. One kilobase of 5′-flanking sequence mediates correct expression of a lacZ fusion gene. J Biol Chem 271 4046 4054

26. GregorPDSawadogoMRoederRG 1990 The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer. Genes Dev 4 1730 1740

27. JiangBMendelsonCR 2003 USF1 and USF2 mediate inhibition of human trophoblast differentiation and CYP19 gene expression by Mash-2 and hypoxia. Mol Cell Biol 23 6117 6128

28. JiangBMendelsonCR 2005 O2 enhancement of human trophoblast differentiation and hCYP19 (aromatase) gene expression are mediated by proteasomal degradation of USF1 and USF2. Mol Cell Biol 25 8824 8833

29. ZhaoHLiMPurwantiYILiuRChenT 2012 Mitf is a transcriptional activator of medaka germ genes in culture. Biochimie 94 759 767

30. GaoEWangYAlcornJLMendelsonCR 1997 The basic helix-loop-helix-zipper transcription factor USF1 regulates expression of the surfactant protein-A gene. J Biol Chem 272 23398 23406

31. FujiiGNakamuraYTsukamotoDItoMShibaT 2006 CpG methylation at the USF-binding site is important for the liver-specific transcription of the chipmunk HP-27 gene. Biochem J 395 203 209

32. ChenLShenYHWangXWangJGanY 2006 Human prolyl-4-hydroxylase alpha(I) transcription is mediated by upstream stimulatory factors. J Biol Chem 281 10849 10855

33. HarrisANMellonPL 1998 The basic helix-loop-helix, leucine zipper transcription factor, USF (upstream stimulatory factor), is a key regulator of SF-1 (steroidogenic factor-1) gene expression in pituitary gonadotrope and steroidogenic cells. Mol Endocrinol 12 714 726

34. BengtssonSHMadeyski-BengtsonKNilssonJBjursellG 2002 Transcriptional regulation of the human carboxyl ester lipase gene in THP-1 monocytes: an E-box required for activation binds upstream stimulatory factors 1 and 2. Biochem J 365 481 488

35. ZhuJGiannolaDMZhangYRiveraAJEmersonSG 2003 NF-Y cooperates with USF1/2 to induce the hematopoietic expression of HOXB4. Blood 102 2420 2427

36. GruenbaumYSteinRCedarHRazinA 1981 Methylation of CpG sequences in eukaryotic DNA. FEBS Lett 124 67 71

37. OrdwayJMCurranT 2002 Methylation matters: modeling a manageable genome. Cell Growth Differ 13 149 162

38. NishinoKHattoriNTanakaSShiotaK 2004 DNA methylation-mediated control of Sry gene expression in mouse gonadal development. J Biol Chem 279 22306 22313

39. ChoiYCChaeCB 1991 DNA hypomethylation and germ cell-specific expression of testis-specific H2B histone gene. J Biol Chem 266 20504 20511

40. IannelloRCGouldJAYoungJCGiudiceAMedcalfR 2000 Methylation-dependent silencing of the testis-specific Pdha-2 basal promoter occurs through selective targeting of an activating transcription factor/cAMP-responsive element-binding site. J Biol Chem 275 19603 19608

41. XieWHanSKhanMDeJongJ 2002 Regulation of ALF gene expression in somatic and male germ line tissues involves partial and site-specific patterns of methylation. J Biol Chem 277 17765 17774

42. McCarreyJRGeyerCBYoshiokaH 2005 Epigenetic regulation of testis-specific gene expression. Ann N Y Acad Sci 1061 226 242

43. ArielMCedarHMcCarreyJ 1994 Developmental changes in methylation of spermatogenesis-specific genes include reprogramming in the epididymis. Nat Genet 7 59 63

44. GollMGBestorTH 2005 Eukaryotic cytosine methyltransferases. Annual review of biochemistry 74 481 514

45. La SalleSTraslerJM 2006 Dynamic expression of DNMT3a and DNMT3b isoforms during male germ cell development in the mouse. Dev Biol 296 71 82

46. KatoYKanedaMHataKKumakiKHisanoM 2007 Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet 16 2272 2280

47. OoiSKBestorTH 2008 The colorful history of active DNA demethylation. Cell 133 1145 1148

48. KangaspeskaSStrideBMetivierRPolycarpou-SchwarzMIbbersonD 2008 Transient cyclical methylation of promoter DNA. Nature 452 112 115

49. MetivierRGallaisRTiffocheCLe PeronCJurkowskaRZ 2008 Cyclical DNA methylation of a transcriptionally active promoter. Nature 452 45 50

50. Mays-HoopesLLBolenJRiggsADSinger-SamJ 1995 Preparation of spermatogonia, spermatocytes, and round spermatids for analysis of gene expression using fluorescence-activated cell sorting. Biol Reprod 53 1003 1011