BMP signaling in the human fetal ovary is developmentally regulated and promotes primordial germ cell apoptosis

Stem Cells

Volumn 28, Issue 8, 2010, Pages 1368-1378

  Childs, Andrew J ^a   Kinnell, Hazel L ^a   Collins, Craig S ^a   Hogg, Kirsten ^a   Bayne, Rosemary A L ^a   Green, Samira J ^a   McNeilly, Alan S ^a   Anderson, Richard A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Apoptosis; Bone morphogenetic protein; Oocyte; Ovary; Primordial germ cell; SMAD

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; GROWTH FACTOR; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR MSX2;

ADULT; APOPTOSIS; APPARATUS; ARTICLE; BONE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; FEMALE; FETUS; GAMETE; HOMEOBOX; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MUSCLE; ORGANISM; OVARY; OVARY FOLLICLE; PLURIPOTENT STEM CELL; PRECURSOR; PRIMORDIAL GERM CELL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SURVIVAL; UPREGULATION;

APOPTOSIS; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 7; BONE MORPHOGENETIC PROTEINS; CELL PROLIFERATION; FEMALE; FETUS; FLUORESCENT ANTIBODY TECHNIQUE; GERM CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MSX1 TRANSCRIPTION FACTOR; OVARY; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE CULTURE TECHNIQUES;

EID: 77955814304     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.440     Document Type: Article

References (70)

1. McLaren A. Primordial germ cells in the mouse. Dev Biol 2003;262:1-15.
2. Lawson KA, Hage WJ. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp 1994;182:68-84; Discussion 84-91.
3. Saitou M, Barton SC, Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature 2002;418:293-300. (Pubitemid 34790674)
4. Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development 1998;125:3323-3328.
5. Pepling ME, Spradling AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001;234:339-351.
6. Sawyer HR, Smith P, Heath DA et al. Formation of ovarian follicles during fetal development in sheep. Biol Reprod 2002;66:1134-1150.
7. Tingen C, Kim A, Woodruff TK. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 2009;15:795-803.
8. Anderson RA, Fulton N, Cowan G et al. Conserved and divergent patterns of expression of DAZL, VASA and OCT4 in the germ cells of the human fetal ovary and testis. BMC Dev Biol 2007;7:136.
9. Fulton N, Martins da Silva SJ, Bayne RA et al. Germ cell proliferation and apoptosis in the developing human ovary. J Clin Endocrinol Metab 2005;90:4664-4670. (Pubitemid 41166527)
10. Stoop H, Honecker F, Cools M et al. Differentiation and development of human female germ cells during prenatal gonadogenesis: An immunohistochemical study. Hum Reprod 2005;20:1466-1476.
11. Johnson J, Canning J, Kaneko T et al. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004;428:145-150. (Pubitemid 38374304)
12. Zou K, Yuan Z, Yang Z et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol 2009;11:631-636.
13. Ross A, Munger S, Capel B. Bmp7 regulates germ cell proliferation in mouse fetal gonads. Sex Dev 2007;1:127-137.
14. Molyneaux KA, Zinszner H, Kunwar PS et al. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 2003;130:4279-4286.
15. Gu Y, Runyan C, Shoemaker A et al. Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Development 2009;136:1295-1303.
16. Donovan PJ. Growth factor regulation of mouse primordial germ cell development. Curr Top Dev Biol 1994;29:189-225. (Pubitemid 2155692)
17. Nakatsuji N, Chuma S. Differentiation of mouse primordial germ cells into female or male germ cells. Int J Dev Biol 2001;45:541-548.
18. Chuma S, Nakatsuji N. Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev Biol 2001;229:468-479. (Pubitemid 32108706)
19. Koshimizu U, Taga T, Watanabe M et al. Functional requirement of gp130-mediated signaling for growth and survival of mouse primordial germ cells in vitro and derivation of embryonic germ (EG) cells. Development 1996;122:1235-1242.
20. Molyneaux KA, Schaible K, Wylie C. GP130, the shared receptor for the LIF/IL6 cytokine family in the mouse, is not required for early germ cell differentiation, but is required cell-autonomously in oocytes for ovulation. Development 2003;130:4287-4294.
21. Lawson KA, Dunn NR, Roelen BA et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 1999;13:424-436. (Pubitemid 29108758)
22. de Sousa Lopes SM, Roelen BA, Monteiro RM et al. BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev 2004;18:1838-1849.
23. Ying Y, Liu XM, Marble A et al. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol 2000;14:1053-1063.
24. Ying Y, Zhao GQ. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol 2001;232:484-492. (Pubitemid 32337109)
25. Dudley BM, Runyan C, Takeuchi Y et al. BMP signaling regulates PGC numbers and motility in organ culture. Mech Dev 2007;124:68-77.
26. Ross AJ, Tilman C, Yao H et al. AMH induces mesonephric cell migration in XX gonads. Mol Cell Endocrinol 2003;211:1-7.
27. Pesce M, Gioia Klinger F, De Felici M. Derivation in culture of primordial germ cells from cells of the mouse epiblast: Phenotypic induction and growth control by Bmp4 signalling. Mech Dev 2002;112:15-24. (Pubitemid 34163217)
28. Hogan BL. Bone morphogenetic proteins in development. Curr Opin Genet Dev 1996;6:432-438.
29. Coucouvanis E, Martin GR. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 1999;126:535-546.
30. Furuta Y, Piston DW, Hogan BL. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 1997;124:2203-2212.
31. Graham A, Francis-West P, Brickell P et al. The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 1994;372:684-686.
32. Trousse F, Esteve P, Bovolenta P. Bmp4 mediates apoptotic cell death in the developing chick eye. J Neurosci 2001;21:1292-1301.
33. Zou H, Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 1996;272:738-741. (Pubitemid 26152785)
34. Guha U, Gomes WA, Kobayashi T et al. In vivo evidence that BMP signaling is necessary for apoptosis in the mouse limb. Dev Biol 2002;249:108-120.
35. Marazzi G, Wang Y, Sassoon D. Msx2 is a transcriptional regulator in the BMP4-mediated programmed cell death pathway. Dev Biol 1997;186:127-138.
36. Takahashi K, Nuckolls GH, Tanaka O et al. Adenovirus-mediated ectopic expression of Msx2 in even-numbered rhombomeres induces apoptotic elimination of cranial neural crest cells in ovo. Development 1998;125:1627-1635.
37. Ferrari D, Lichtler AC, Pan ZZ et al. Ectopic expression of Msx-2 in posterior limb bud mesoderm impairs limb morphogenesis while inducing BMP-4 expression, inhibiting cell proliferation, and promoting apoptosis. Dev Biol 1998;197:12-24.
38. Gomes WA, Kessler JA. Msx-2 and p21 mediate the pro-apoptotic but not the anti-proliferative effects of BMP4 on cultured sympathetic neuroblasts. Dev Biol 2001;237:212-221.
39. Israsena N, Kessler JA. Msx2 and p21(CIP1/WAF1) mediate the proapoptotic effects of bone morphogenetic protein-4 on ventricular zone progenitor cells. J Neurosci Res 2002;69:803-809. (Pubitemid 34984698)
40. Liu CF, Parker K, Yao H. The role of Wnt4/β-catenin signaling in maintaining germ cell survival in the fetal ovary. Biol Reprod 2009;81:175 (Abstract).
41. Friel A, Houghton JA, Glennon M et al. A preliminary report on the implication of RT-PCR detection of DAZ, RBMY1, USP9Y and Protamine-2 mRNA in testicular biopsy samples from azoospermic men. Int J Androl 2002;25:59-64.
42. Bayne RA, Eddie SL, Collins CS et al. Prostaglandin E2 as a regulator of germ cells during ovarian development. J Clin Endocrinol Metab 2009;94:4053-4060.
43. Duffin K, Bayne RA, Childs AJ et al. The forkhead transcription factor FOXL2 is expressed in somatic cells of the human ovary prior to follicle formation. Mol Hum Reprod 2009;15:771-777.
44. Martins da Silva SJ, Bayne RA, Cambray N et al. Expression of activin subunits and receptors in the developing human ovary: Activin A promotes germ cell survival and proliferation before primordial follicle formation. Dev Biol 2004;266:334-345.
45. McClellan KA, Gosden R, Taketo T. Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Dev Biol 2003;258:334-348.
46. Pellegrini M, Grimaldi P, Rossi P et al. Developmental expression of BMP4/ALK3/SMAD5 signaling pathway in the mouse testis: A potential role of BMP4 in spermatogonia differentiation. J Cell Sci 2003;116:3363-3372. (Pubitemid 37038984)
47. Hata A, Lagna G, Massague J et al. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 1998;12:186-197.
48. Hoei-Hansen CE, Nielsen JE, Almstrup K et al. Transcription factor AP-2γ is a developmentally regulated marker of testicular carcinoma in situ and germ cell tumors. Clin Cancer Res 2004;10:8521-8530.
49. Bendsen E, Byskov AG, Andersen CY et al. Number of germ cells and somatic cells in human fetal ovaries during the first weeks after sex differentiation. Hum Reprod 2006;21:30-35. (Pubitemid 41794289)
50. Shamblott MJ, Axelman J, Wang S et al. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 1998;95:13726-13731.
51. Turnpenny L, Brickwood S, Spalluto CM et al. Derivation of human embryonic germ cells: An alternative source of pluripotent stem cells. Stem Cells 2003;21:598-609.
52. Yao HH, Matzuk MM, Jorgez CJ et al. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn 2004;230:210-215.
53. Massague J. How cells read TGF-β signals. Nat Rev Mol Cell Biol 2000;1:169-178.
54. Abir R, Ben-Haroush A, Melamed N et al. Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. Fertil Steril 2008;89:1430-1440.
55. Aoki H, Fujii M, Imamura T et al. Synergistic effects of different bone morphogenetic protein type I receptors on alkaline phosphatase induction. J Cell Sci 2001;114:1483-1489.
56. Ebisawa T, Tada K, Kitajima I et al. Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation. J Cell Sci 1999;112:3519-3527.
57. Kretzschmar M, Doody J, Massague J. Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature 1997;389:618-622. (Pubitemid 27446181)
58. Xiao Z, Liu X, Lodish HF. Importing β mediates nuclear translocation of Smad 3. J Biol Chem 2000;275:23425-23428.
59. Hogarth CA, Jans DA, Loveland KL. Subcellular distribution of importins correlates with germ cell maturation. Dev Dyn 2007;236:2311-2320.
60. Itman C, Small C, Griswold M et al. Developmentally regulated SMAD2 and SMAD3 utilization directs activin signaling outcomes. Dev Dyn 2009;238:1688-1700.
61. Koshimizu U, Watanabe M, Nakatsuji N. Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev Biol 1995;168:683-685.
62. Bowles J, Knight D, Smith C et al. Retinoid signaling determines germ cell fate in mice. Science 2006;312:596-600.
63. Koubova J, Menke DB, Zhou Q et al. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA 2006;103:2474-2479.
64. Pesce M, Farrace MG, Piacentini M et al. Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development 1993;118:1089-1094. (Pubitemid 23252399)
65. Ware CB, Horowitz MC, Renshaw BR et al. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 1995;121:1283-1299.
66. Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 2008;9:285-296.
67. Kee K, Gonsalves JM, Clark AT et al. Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev 2006;15:831-837.
68. Young JC, Dias VL, Loveland KL. Defining the window of germline genesis in vitro from murine embryonic stem cells. Biol Reprod 2010;82:390-401.
69. West FD, Roche-Rios MI, Abraham S et al. KIT ligand and bone morphogenetic protein signaling enhances human embryonic stem cell to germ-like cell differentiation. Hum Reprod 2010;25:168-178.
70. Tilgner K, Atkinson SP, Golebiewska A et al. Isolation of primordial germ cells from differentiating human embryonic stem cells. Stem Cells 2008;26:3075-3085.