#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Germ cell-intrinsic effects of sex chromosomes on early oocyte differentiation in mice


Autoři: Norio Hamada aff001;  Nobuhiko Hamazaki aff001;  So Shimamoto aff001;  Orie Hikabe aff001;  Go Nagamatsu aff001;  Yuki Takada aff001;  Kiyoko Kato aff002;  Katsuhiko Hayashi aff001
Působiště autorů: Department of Stem Cell Biology and Medicine, Graduate School of Medical Sciences, Kyushu University, Maidashi, Higashi-ku, Fukuoka, Japan aff001;  Department of Obstetrics and Gynecology, Graduate School of Medical Sciences, Kyushu University, Maidashi, Higashi-ku, Fukuoka, Japan aff002
Vyšlo v časopise: Germ cell-intrinsic effects of sex chromosomes on early oocyte differentiation in mice. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008676
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008676

Souhrn

A set of sex chromosomes is required for gametogenesis in both males and females, as represented by sex chromosome disorders causing agametic phenotypes. Although studies using model animals have investigated the functional requirement of sex chromosomes, involvement of these chromosomes in gametogenesis remains elusive. Here, we elicit a germ cell-intrinsic effect of sex chromosomes on oogenesis, using a novel culture system in which oocytes were induced from embryonic stem cells (ESCs) harboring XX, XO or XY. In the culture system, oogenesis using XO and XY ESCs was severely disturbed, with XY ESCs being more strongly affected. The culture system revealed multiple defects in the oogenesis of XO and XY ESCs, such as delayed meiotic entry and progression, and mispairing of the homologous chromosomes. Interestingly, Eif2s3y, a Y-linked gene that promotes proliferation of spermatogonia, had an inhibitory effect on oogenesis. This led us to the concept that male and female gametogenesis appear to be in mutual conflict at an early stage. This study provides a deeper understanding of oogenesis under a sex-reversal condition.

Klíčová slova:

Cell differentiation – Gene expression – Germ cells – Homologous chromosomes – Oocytes – Oogenesis – Sex chromosomes – X chromosomes


Zdroje

1. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol. 2000;163(1–2):3–9. doi: 10.1016/s0303-7207(99)00234-8 10963867

2. Saitou M, Yamaji M. Primordial germ cells in mice. Cold Spring Harbor perspectives in biology. 2012;4(11). Epub 2012/11/06. doi: 10.1101/cshperspect.a008375 23125014.

3. Adams IR, McLaren A. Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development. 2002;129(5):1155–64. 11874911.

4. Jameson SA, Natarajan A, Cool J, DeFalco T, Maatouk DM, Mork L, et al. Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet. 2012;8(3):e1002575. Epub 2012/03/23. doi: 10.1371/journal.pgen.1002575 22438826; PubMed Central PMCID: PMC3305395.

5. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A. 2006;103(8):2474–9. Epub 2006/02/08. doi: 10.1073/pnas.0510813103 16461896; PubMed Central PMCID: PMC1413806.

6. 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. The EMBO journal. 2017;36(21):3100–19. Epub 2017/09/21. doi: 10.15252/embj.201796875 28928204; PubMed Central PMCID: PMC5666620.

7. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, et al. Retinoid signaling determines germ cell fate in mice. Science. 2006;312(5773):596–600. Epub 2006/04/01. doi: 10.1126/science.1125691 16574820.

8. Ohta H, Kurimoto K, Okamoto I, Nakamura T, Yabuta Y, Miyauchi H, et al. In vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate. The EMBO journal. 2017;36(13):1888–907. Epub 2017/06/01. doi: 10.15252/embj.201695862 28559416; PubMed Central PMCID: PMC5494472.

9. Burgoyne PS. The role of the mammalian Y chromosome in spermatogenesis. Development. 1987;101 Suppl:133–41. Epub 1987/01/01. 3503711.

10. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature. 1991;351(6322):117–21. Epub 1991/05/09. doi: 10.1038/351117a0 2030730.

11. Mahadevaiah SK, Lovell-Badge R, Burgoyne PS. Tdy-negative XY, XXY and XYY female mice: breeding data and synaptonemal complex analysis. J Reprod Fertil. 1993;97(1):151–60. Epub 1993/01/01. doi: 10.1530/jrf.0.0970151 8464005.

12. Wang H, Hu YC, Markoulaki S, Welstead GG, Cheng AW, Shivalila CS, et al. TALEN-mediated editing of the mouse Y chromosome. Nat Biotechnol. 2013;31(6):530–2. Epub 2013/05/15. doi: 10.1038/nbt.2595 PubMed Central PMCID: PMC3681814. 23666012

13. Taketo T. The role of sex chromosomes in mammalian germ cell differentiation: can the germ cells carrying X and Y chromosomes differentiate into fertile oocytes? Asian journal of andrology. 2015;17(3):360–6. Epub 2015/01/13. doi: 10.4103/1008-682X.143306 25578929; PubMed Central PMCID: PMC4430933.

14. Turner JM. Meiotic Silencing in Mammals. Annual review of genetics. 2015;49:395–412. Epub 2015/12/04. doi: 10.1146/annurev-genet-112414-055145 26631513.

15. Vernet N, Szot M, Mahadevaiah SK, Ellis PJ, Decarpentrie F, Ojarikre OA, et al. The expression of Y-linked Zfy2 in XY mouse oocytes leads to frequent meiosis 2 defects, a high incidence of subsequent early cleavage stage arrest and infertility. Development. 2014;141(4):855–66. Epub 2014/02/06. doi: 10.1242/dev.091165 24496622; PubMed Central PMCID: PMC3912830.

16. Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, et al. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539(7628):299–303. Epub 2016/11/04. doi: 10.1038/nature20104 27750280.

17. Matsumura H, Tada M, Otsuji T, Yasuchika K, Nakatsuji N, Surani A, et al. Targeted chromosome elimination from ES-somatic hybrid cells. Nature methods. 2007;4(1):23–5. Epub 2006/11/07. doi: 10.1038/nmeth973 17086180.

18. Sakashita A, Wakai T, Kawabata Y, Nishimura C, Sotomaru Y, Alavattam KG, et al. XY oocytes of sex-reversed females with a Sry mutation deviate from the normal developmental process beyond the mitotic stagedagger. Biol Reprod. 2019;100(3):697–710. Epub 2018/10/06. doi: 10.1093/biolre/ioy214 30289439; PubMed Central PMCID: PMC6437265.

19. Crichton JH, Read D, Adams IR. Defects in meiotic recombination delay progression through pachytene in Tex19.1(-/-) mouse spermatocytes. Chromosoma. 2018;127(4):437–59. Epub 2018/06/17. doi: 10.1007/s00412-018-0674-9 29907896; PubMed Central PMCID: PMC6208735.

20. Alton M, Lau MP, Villemure M, Taketo T. The behavior of the X- and Y-chromosomes in the oocyte during meiotic prophase in the B6.Y(TIR)sex-reversed mouse ovary. Reproduction. 2008;135(2):241–52. Epub 2008/02/02. doi: 10.1530/REP-07-0383 18239052.

21. Taketo T, Naumova AK. Oocyte heterogeneity with respect to the meiotic silencing of unsynapsed X chromosomes in the XY female mouse. Chromosoma. 2013;122(5):337–49. Epub 2013/06/14. doi: 10.1007/s00412-013-0415-z 23760560.

22. Rinaldi VD, Bolcun-Filas E, Kogo H, Kurahashi H, Schimenti JC. The DNA Damage Checkpoint Eliminates Mouse Oocytes with Chromosome Synapsis Failure. Mol Cell. 2017;67(6):1026–36 e2. Epub 2017/08/29. doi: 10.1016/j.molcel.2017.07.027 28844861; PubMed Central PMCID: PMC5621520.

23. Baarends WM, Wassenaar E, van der Laan R, Hoogerbrugge J, Sleddens-Linkels E, Hoeijmakers JH, et al. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol. 2005;25(3):1041–53. Epub 2005/01/20. doi: 10.1128/MCB.25.3.1041-1053.2005 15657431; PubMed Central PMCID: PMC543997.

24. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, et al. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet. 2005;37(1):41–7. Epub 2004/12/08. doi: 10.1038/ng1484 15580272.

25. 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;40(3):289–301 e3. Epub 2017/01/31. doi: 10.1016/j.devcel.2016.12.023 28132849; PubMed Central PMCID: PMC5300051.

26. Cloutier JM, Mahadevaiah SK, ElInati E, Nussenzweig A, Toth A, Turner JM. Histone H2AFX Links Meiotic Chromosome Asynapsis to Prophase I Oocyte Loss in Mammals. PLoS Genet. 2015;11(10):e1005462. Epub 2015/10/29. doi: 10.1371/journal.pgen.1005462 26509888; PubMed Central PMCID: PMC4624946.

27. Cloutier JM, Mahadevaiah SK, ElInati E, Toth A, Turner J. Mammalian meiotic silencing exhibits sexually dimorphic features. Chromosoma. 2016;125(2):215–26. Epub 2015/12/30. doi: 10.1007/s00412-015-0568-z 26712235; PubMed Central PMCID: PMC4830877.

28. Park EH, Taketo T. Onset and progress of meiotic prophase in the oocytes in the B6.YTIR sex-reversed mouse ovary. Biology of reproduction. 2003;69(6):1879–89. Epub 2003/08/09. doi: 10.1095/biolreprod.103.017541 12904311.

29. Maatouk DM, Kellam LD, Mann MR, Lei H, Li E, Bartolomei MS, et al. DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development. 2006;133(17):3411–8. doi: 10.1242/dev.02500 16887828.

30. Yamaguchi S, Hong K, Liu R, Shen L, Inoue A, Diep D, et al. Tet1 controls meiosis by regulating meiotic gene expression. Nature. 2012;492(7429):443–7. Epub 2012/11/16. doi: 10.1038/nature11709 23151479; PubMed Central PMCID: PMC3528851.

31. Shirane K, Kurimoto K, Yabuta Y, Yamaji M, Satoh J, Ito S, et al. Global Landscape and Regulatory Principles of DNA Methylation Reprogramming for Germ Cell Specification by Mouse Pluripotent Stem Cells. Dev Cell. 2016;39(1):87–103. Epub 2016/09/20. doi: 10.1016/j.devcel.2016.08.008 27642137.

32. Kobayashi H, Sakurai T, Miura F, Imai M, Mochiduki K, Yanagisawa E, et al. High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome research. 2013;23(4):616–27. Epub 2013/02/16. doi: 10.1101/gr.148023.112 23410886; PubMed Central PMCID: PMC3613579.

33. Zvetkova I, Apedaile A, Ramsahoye B, Mermoud JE, Crompton LA, John R, et al. Global hypomethylation of the genome in XX embryonic stem cells. Nat Genet. 2005;37(11):1274–9. Epub 2005/10/26. doi: 10.1038/ng1663 16244654.

34. Nguyen N, Zhang X, Olashaw N, Seto E. Molecular cloning and functional characterization of the transcription factor YY2. J Biol Chem. 2004;279(24):25927–34. Epub 2004/04/17. doi: 10.1074/jbc.M402525200 15087442.

35. Kim JD, Faulk C, Kim J. Retroposition and evolution of the DNA-binding motifs of YY1, YY2 and REX1. Nucleic Acids Res. 2007;35(10):3442–52. Epub 2007/05/05. doi: 10.1093/nar/gkm235 17478514; PubMed Central PMCID: PMC1904287.

36. Klar M, Fenske P, Vega FR, Dame C, Brauer AU. Transcription factor Yin-Yang 2 alters neuronal outgrowth in vitro. Cell and tissue research. 2015;362(2):453–60. Epub 2015/09/10. doi: 10.1007/s00441-015-2268-7 26350623; PubMed Central PMCID: PMC4657790.

37. Donohoe ME, Zhang LF, Xu N, Shi Y, Lee JT. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol Cell. 2007;25(1):43–56. Epub 2007/01/16. doi: 10.1016/j.molcel.2006.11.017 17218270.

38. Morelli MA, Cohen PE. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction. 2005;130(6):761–81. Epub 2005/12/03. doi: 10.1530/rep.1.00865 16322537.

39. Bolcun-Filas E, Rinaldi VD, White ME, Schimenti JC. Reversal of female infertility by Chk2 ablation reveals the oocyte DNA damage checkpoint pathway. Science. 2014;343(6170):533–6. Epub 2014/02/01. doi: 10.1126/science.1247671 24482479; PubMed Central PMCID: PMC4048839.

40. Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T, Yamamoto M, et al. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science. 2012;336(6082):732–6. Epub 2012/05/15. doi: 10.1126/science.1219518 22582262.

41. Sugimoto M, Abe K. X chromosome reactivation initiates in nascent primordial germ cells in mice. PLoS Genet. 2007;3(7):e116. doi: 10.1371/journal.pgen.0030116 17676999.

42. Chuva de Sousa Lopes SM, Hayashi K, Shovlin TC, Mifsud W, Surani MA, McLaren A. X chromosome activity in mouse XX primordial germ cells. PLoS Genet. 2008;4(2):e30. doi: 10.1371/journal.pgen.0040030 18266475.

43. Mazeyrat S, Saut N, Grigoriev V, Mahadevaiah SK, Ojarikre OA, Rattigan A, et al. A Y-encoded subunit of the translation initiation factor Eif2 is essential for mouse spermatogenesis. Nat Genet. 2001;29(1):49–53. Epub 2001/08/31. doi: 10.1038/ng717 11528390.

44. Yamauchi Y, Riel JM, Stoytcheva Z, Ward MA. Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse. Science. 2014;343(6166):69–72. Epub 2013/11/23. doi: 10.1126/science.1242544 24263135; PubMed Central PMCID: PMC3880637.

45. Yamauchi Y, Riel JM, Ruthig VA, Ortega EA, Mitchell MJ, Ward MA. Two genes substitute for the mouse Y chromosome for spermatogenesis and reproduction. Science. 2016;351(6272):514–6. Epub 2016/01/30. doi: 10.1126/science.aad1795 26823431; PubMed Central PMCID: PMC5500212.

46. Ehrmann IE, Ellis PS, Mazeyrat S, Duthie S, Brockdorff N, Mattei MG, et al. Characterization of genes encoding translation initiation factor eIF-2gamma in mouse and human: sex chromosome localization, escape from X-inactivation and evolution. Hum Mol Genet. 1998;7(11):1725–37. Epub 1998/09/16. doi: 10.1093/hmg/7.11.1725 9736774.

47. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863–4. Epub 2011/02/01. doi: 10.1093/bioinformatics/btr026 21278185; PubMed Central PMCID: PMC3051327.

48. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. Epub 2012/10/30. doi: 10.1093/bioinformatics/bts635 23104886; PubMed Central PMCID: PMC3530905.

49. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30. Epub 2013/11/15. doi: 10.1093/bioinformatics/btt656 24227677.

50. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. Epub 2009/11/17. doi: 10.1093/bioinformatics/btp616 19910308; PubMed Central PMCID: PMC2796818.


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 3
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#