Licensing of Primordial Germ Cells for Gametogenesis Depends on Genital Ridge Signaling
During embryonic development, stem cell-like primordial germ cells travel across the developing embryo to the genital ridge, which gives rise to the gonad. Around the time of their arrival, the primordial germ cells gain the capacity to undertake sexual specialization and meiosis—a process called germ cell licensing. Based on the observation that meiosis and sexual differentiation can occur when primordial germ cells stray into the area of the adrenal gland, the primordial germ cell has been thought to be responsible for its own licensing. We tested this notion by examining the licensing process in mutant mouse embryos that did not form a genital ridge. We discovered that in the absence of the genital ridge, primordial germ cells migrate across the developing embryo properly, but instead of undergoing licensing, these cells retain their primordial germ cell characteristics. We conclude that licensing of embryonic primordial germ cells for gametogenesis is dependent on signaling from the genital ridge.
Vyšlo v časopise:
Licensing of Primordial Germ Cells for Gametogenesis Depends on Genital Ridge Signaling. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005019
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005019
Souhrn
During embryonic development, stem cell-like primordial germ cells travel across the developing embryo to the genital ridge, which gives rise to the gonad. Around the time of their arrival, the primordial germ cells gain the capacity to undertake sexual specialization and meiosis—a process called germ cell licensing. Based on the observation that meiosis and sexual differentiation can occur when primordial germ cells stray into the area of the adrenal gland, the primordial germ cell has been thought to be responsible for its own licensing. We tested this notion by examining the licensing process in mutant mouse embryos that did not form a genital ridge. We discovered that in the absence of the genital ridge, primordial germ cells migrate across the developing embryo properly, but instead of undergoing licensing, these cells retain their primordial germ cell characteristics. We conclude that licensing of embryonic primordial germ cells for gametogenesis is dependent on signaling from the genital ridge.
Zdroje
1. Brambell FWR (1927) The development and morphology of the gonads of the mouse—Part I The morphogenesis of the indifferent gonad and of the ovary. Proc R Soc Lond B Biol Sci 101: 391–409.
2. Hu YC, Okumura LM, Page DC (2013) Gata4 is required for formation of the genital ridge in mice. PLoS Genet 9: e1003629. doi: 10.1371/journal.pgen.1003629 23874227
3. Hacker A, Capel B, Goodfellow P, Lovell-Badge R (1995) Expression of Sry, the mouse sex determining gene. Development 121: 1603–1614. 7600978
4. Schmahl J, Eicher EM, Washburn LL, Capel B (2000) Sry induces cell proliferation in the mouse gonad. Development 127: 65–73. 10654601
5. Hayashi K, de Sousa Lopes SM, Surani MA (2007) Germ cell specification in mice. Science 316: 394–396. 17446386
6. Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4: a008375. doi: 10.1101/cshperspect.a008375 23125014
7. Chuma S, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, et al. (2005) Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 132: 117–122. 15576408
8. Molyneaux KA, Wang Y, Schaible K, Wylie C (2004) Transcriptional profiling identifies genes differentially expressed during and after migration in murine primordial germ cells. Gene Expr Patterns 4: 167–181. 15161097
9. Rolland AD, Lehmann KP, Johnson KJ, Gaido KW, Koopman P (2011) Uncovering gene regulatory networks during mouse fetal germ cell development. Biol Reprod 84: 790–800. doi: 10.1095/biolreprod.110.088443 21148109
10. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, et al. (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48: 849–862. doi: 10.1016/j.molcel.2012.11.001 23219530
11. Gill ME, Hu YC, Lin Y, Page DC (2011) Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells. Proc Natl Acad Sci U S A 108: 7443–7448. doi: 10.1073/pnas.1104501108 21504946
12. Adams IR, McLaren A (2002) Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development 129: 1155–1164. 11874911
13. McLaren A, Southee D (1997) Entry of mouse embryonic germ cells into meiosis. Dev Biol 187: 107–113. 9224678
14. Seligman J, Page DC (1998) The Dazh gene is expressed in male and female embryonic gonads before germ cell sex differentiation. Biochem Biophys Res Commun 245: 878–882. 9588208
15. Lin Y, Gill ME, Koubova J, Page DC (2008) Germ cell-intrinsic and-extrinsic factors govern meiotic initiation in mouse embryos. Science 322: 1685–1687. doi: 10.1126/science.1166340 19074348
16. Stallock J, Molyneaux K, Schaible K, Knudson CM, Wylie C (2003) The pro-apoptotic gene Bax is required for the death of ectopic primordial germ cells during their migration in the mouse embryo. Development 130: 6589–6597. 14660547
17. Runyan C, Gu Y, Shoemaker A, Looijenga L, Wylie C (2008) The distribution and behavior of extragonadal primordial germ cells in Bax mutant mice suggest a novel origin for sacrococcygeal germ cell tumors. Int J Dev Biol 52: 333–344. doi: 10.1387/ijdb.072486cr 18415933
18. Molyneaux KA, Stallock J, Schaible K, Wylie C (2001) Time-lapse analysis of living mouse germ cell migration. Dev Biol 240: 488–498. 11784078
19. Upadhyay S, Zamboni L (1982) Ectopic germ cells: natural model for the study of germ cell sexual differentiation. Proc Natl Acad Sci U S A 79: 6584–6588. 6959138
20. Zamboni L, Upadhyay S (1983) Germ cell differentiation in mouse adrenal glands. J Exp Zool 228: 173–193. 6663256
21. Richards AJ, Enders GC, Resnick JL (1999) Differentiation of murine premigratory primordial germ cells in culture. Biol Reprod 61: 1146–1151. 10491656
22. Chuma S, Nakatsuji N (2001) Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev Biol 229: 468–479. 11203703
23. Tedesco M, Desimio MG, Klinger FG, De Felici M, Farini D (2013) Minimal concentrations of retinoic acid induce stimulation by retinoic acid 8 and promote entry into meiosis in isolated pregonadal and gonadal mouse primordial germ cells. Biol Reprod 88: 145. doi: 10.1095/biolreprod.112.106526 23636811
24. Hatano O, Takakusu A, Nomura M, Morohashi K (1996) Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells 1: 663–671. 9078392
25. Laufer E, Kesper D, Vortkamp A, King P (2012) Sonic hedgehog signaling during adrenal development. Mol Cell Endocrinol 351: 19–27. doi: 10.1016/j.mce.2011.10.002 22020162
26. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877–879. doi: 10.1038/nmeth.1253 18806792
27. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, et al. (2000) Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93: 139–149. 10781947
28. Chen SR, Zheng QS, Zhang Y, Gao F, Liu YX (2013) Disruption of genital ridge development causes aberrant primordial germ cell proliferation but does not affect their directional migration. BMC Biol 11: 22. doi: 10.1186/1741-7007-11-22 23497137
29. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, et al. (1993) WT-1 is required for early kidney development. Cell 74: 679–691. 8395349
30. Wang Q, Lan Y, Cho ES, Maltby KM, Jiang R (2005) Odd-skipped related 1 (Odd 1) is an essential regulator of heart and urogenital development. Dev Biol 288: 582–594. 16223478
31. Donovan PJ, Stott D, Cairns LA, Heasman J, Wylie CC (1986) Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44: 831–838. 3955652
32. Dudley B, Palumbo C, Nalepka J, Molyneaux K (2010) BMP signaling controls formation of a primordial germ cell niche within the early genital ridges. Dev Biol 343: 84–93. doi: 10.1016/j.ydbio.2010.04.011 20417197
33. Godin I, Wylie C, Heasman J (1990) Genital ridges exert long-range effects on mouse primordial germ cell numbers and direction of migration in culture. Development 108: 357–363. 2351075
34. Medeiros LA, Dennis LM, Gill ME, Houbaviy H, Markoulaki S, et al. (2011) Mir-290–295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects. Proc Natl Acad Sci U S A 108: 14163–14168. doi: 10.1073/pnas.1111241108 21844366
35. Luoh SW, Bain PA, Polakiewicz RD, Goodheart ML, Gardner H, et al. (1997) Zfx mutation results in small animal size and reduced germ cell number in male and female mice. Development 124: 2275–2284. 9187153
36. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, et al. (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 103: 2474–2479. 16461896
37. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, et al. (2006) Retinoid signaling determines germ cell fate in mice. Science 312: 596–600. 16574820
38. Baltus AE, Menke DB, Hu YC, Goodheart ML, Carpenter AE, et al. (2006) In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet 38: 1430–1434. 17115059
39. Koubova J, Hu YC, Bhattacharyya T, Soh YQ, Gill ME, et al. (2014) Retinoic acid activates two pathways required for meiosis in mice. PLoS Genet 10: e1004541. doi: 10.1371/journal.pgen.1004541 25102060
40. Menke DB, Koubova J, Page DC (2003) Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev Biol 262: 303–312. 14550793
41. Yao HH, DiNapoli L, Capel B (2003) Meiotic germ cells antagonize mesonephric cell migration and testis cord formation in mouse gonads. Development 130: 5895–5902. 14561636
42. Watt AJ, Battle MA, Li J, Duncan SA (2004) GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc Natl Acad Sci U S A 101: 12573–12578. 15310850
43. Hayashi S, McMahon AP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305–318. 11944939
44. Mugford JW, Sipila P, McMahon JA, McMahon AP (2008) Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev Biol 324: 88–98. doi: 10.1016/j.ydbio.2008.09.010 18835385
45. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, et al. (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109–113. doi: 10.1038/nature07060 18568026
46. Grun D, Kester L, van Oudenaarden A (2014) Validation of noise models for single-cell transcriptomics. Nat Methods 11: 637–640. doi: 10.1038/nmeth.2930 24747814
47. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B (1997) Male-specific cell migration into the developing gonad. Curr Biol 7: 958–968. 9382843
48. Ozdzenski W (1972) Differentiation of the genital ridges of mouse embryos in the kidney of adult mice. Arch Anat Microsc Morphol Exp 61: 267–278. 4667754
49. Byskov AG, Fenger M, Westergaard L, Andersen CY (1993) Forskolin and the meiosis inducing substance synergistically initiate meiosis in fetal male germ cells. Mol Reprod Dev 34: 47–52. 8418816
50. Hu YC, de Rooij DG, Page DC (2013) Tumor suppressor gene Rb is required for self-renewal of spermatogonial stem cells in mice. Proc Natl Acad Sci U S A 110: 12685–12690. doi: 10.1073/pnas.1311548110 23858447
51. Enders GC, May JJ 2nd (1994) Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice. Dev Biol 163: 331–340. 8200475
52. 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. 17446352
53. Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, et al. (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13: 424–436. 10049358
54. Tam PP, Zhou SX (1996) The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol 178: 124–132. 8812114
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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