Cell cycle analysis of fetal germ cells during sex differentiation in mice

Biology of the Cell

Volumn 101, Issue 10, 2009, Pages 587-598

  Spiller, Cassy ^a   Wilhelm, Dagmar ^a   Koopman, Peter ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cell cycle array; Fetal ovary; Fetal testis; G1 G0 arrest; Germ cell; Meiosis

Indexed keywords

ATM PROTEIN; PROTEIN P21; PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CONTROLLED STUDY; DOWN REGULATION; FERTILITY; GENE EXPRESSION; GENE IDENTIFICATION; GERM CELL; MEIOSIS; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; APOPTOSIS; CALCIUM SIGNALING; CELL CYCLE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; GONADS; MALE; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARY; SEX CHARACTERISTICS; SEX DIFFERENTIATION; TESTIS;

ATAXIA TELANGIECTASIA; MUS;

EID: 70350109516     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20090021     Document Type: Article

References (68)

1. Atchison, F.W., Capel, B. and Means, A.R. (2003) PIN1 regulates the timing of mammalian primordial germ cell proliferation. Development 130, 3579-3586
2. Bahar, R., J, O.W., Kawamura, K., Seimiya, M., Wang, Y., Hatano, M., Okada, S., Tokuhisa, T., Watanabe, T. and Tagawa, M. (2002) Growth retardation, polyploidy, and multinucleation induced by Clast3, a novel cell cycle-regulated protein. J. Biol. Chem. 277, 40012-40019
3. Barbacid, M., Ortega, S., Sotillo, R., Odajima, J., Martin, A., Santamaria, D., Dubus, P. and Malumbres, M. (2005) Cell cycle and cancer: genetic analysis of the role of cyclin-dependent kinases. Cold Spring Harb. Symp. Quant. Biol. 70, 233-240
4. Bartkova, J., Thullberg, M., Rajpert-De Meyts, E., Skakkebaek, N.E. and Bartek, J. (2000) Cell cycle regulators in testicular cancer: loss of p18INK4C marks progression from CIS to invasive germ cell tumours. Int. J. Cancer 85, 370-375
5. Bartkova, J., Lukas, C., Sorensen, C.S., Meyts, E.R., Skakkebaek, N.E., Lukas, J. and Bartek, J. (2003) Deregulation of the RB pathway in human testicular germ cell tumours. J. Pathol. 200, 149-156
6. Bilyy, R., Kit, Y., Hellman, U., Tryndyak, V., Kaminskyy, V. and Stoika, R. (2005) In vivo expression and characteristics of novel alpha-d-mannose-rich glycoprotein markers of apoptotic cells. Cell Biol. Int. 29, 920-928
7. Bok, J., Wang, Q., Huang, J. and Green, S.H. (2007) CaMKII and CaMKIV mediate distinct prosurvival signaling pathways in response to depolarization in neurons. Mol. Cell Neurosci. 36, 13-26
8. Borum, K. (1961) Oogenesis in the mouse. A study of the meiotic prophase. Exp. Cell Res. 24, 495-507
9. Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M.J., Rossant, J. et al. (2006) Retinoid signaling determines germ cell fate in mice. Science 312, 596-600
10. Cai, H., Liu, D. and Garcia, J.G. (2008) CaM kinase II-dependent pathophysiological signalling in endothelial cells. Cardiovasc. Res. 77, 30-34
11. Chiquoine, A.D. (1954) The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat. Rec. 118, 135-146
12. Coucouvanis, E.C., Sherwood, S.W., Carswell-Crumpton, C., Spack, E.G. and Jones, P.P. (1993) Evidence that the mechanism of prenatal germ cell death in the mouse is apoptosis. Exp. Cell Res. 209, 238-247
13. Dallas, P.B., Gottardo, N.G., Firth, M.J., Beesley, A.H., Hoffmann, K., Terry, P.A., Freitas, J.R., Boag, J.M., Cummings, A.J. and Kees, U.R. (2005) Gene expression levels assessed by oligonucleotide microarray analysis and quantitative real-time RT-PCR - how well do they correlate? BMC Genomics 6, 59
14. 1 checkpoint control. Cell 82, 675-684
15. Donovan, P.J. and Reed, S.I. (2003) Germline exclusion of Cks1 in the mouse reveals a metaphase I role for Cks proteins in male and female meiosis. Cell Cycle 2, 275-276
16. Donovan, P.J., Stott, D., Cairns, L.A., Heasman, J. and Wylie, C.C. (1986) Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44, 831-838
17. 1 arrest and apoptosis. Cancer Res. 54, 1169-1174
18. Elson, A., Wang, Y., Daugherty, C.J., Morton, C.C., Zhou, F., Campos-Torres, J. and Leder, P. (1996) Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93, 13084-13089
19. Fukunaga, K. and Miyamoto, E. (1999) Current studies on a working model of CaM kinase II in hippocampal long-term potentiation and memory. Japan. J. Pharmacol. 79, 7-15
20. Ginsburg, M., Snow, M.H. and McLaren, A. (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110, 521-528
21. Gougeon, A. (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 17, 121-155
22. Hilscher, W. (1974) [Kinetics of prespermatogenesis and spermatogenesis]. Verh. Anat. Ges. 68, 39-62
23. Hoei-Hansen, C.E., Rajpert-De Meyts, E., Daugaard, G. and Skakkebaek, N.E. (2005) Carcinoma in situ testis, the progenitor of testicular germ cell tumours: a clinical review. Ann. Oncol. 16, 863-868
24. Kimura, T., Tomooka, M., Yamano, N., Murayama, K., Matoba, S., Umehara, H., Kanai, Y. and Nakano, T. (2008) AKT signaling promotes derivation of embryonic germ cells from primordial germ cells. Development 135, 869-879
25. Kopnin, P.B., Agapova, L.S., Kopnin, B.P. and Chumakov, P.M. (2007) Repression of sestrin family genes contributes to oncogenic Ras-induced reactive oxygen species up-regulation and genetic instability. Cancer Res. 67, 4671-4678
26. Koubova, J., Menke, D.B., Zhou, Q., Capel, B., Griswold, M.D. and Page, D.C. (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl. Acad. Sci. U.S.A. 103, 2474-2479
27. Lawson, K.A. and Hage, W.J. (1994) Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182, 68-84; discussion 84-91
28. Lincoln, A.J., Wickramasinghe, D., Stein, P., Schultz, R.M., Palko, M.E., De Miguel, M.P., Tessarollo, L. and Donovan, P.J. (2002) Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat. Genet. 30, 446-449
29. Lu, K.P., Hanes, S.D. and Hunter, T. (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380, 544-547
30. Matsui, Y. (1998) Developmental fates of the mouse germ cell line. Int. J. Dev. Biol. 42, 1037-1042
31. Matthews, R.P., Guthrie, C.R., Wailes, L.M., Zhao, X., Means, A.R. and McKnight, G.S. (1994) Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell. Biol. 14, 6107-6116
32. McHale, C.M., Zhang, L., Lan, Q., Li, G., Hubbard, A.E., Forrest, M.S., Vermeulen, R., Chen, J., Shen, M., Rappaport, S.M. et al. (2009) Changes in the peripheral blood transcriptome associated with occupational benzene exposure identified by crosscomparison on two microarray platforms. Genomics 93, 343-349
33. McLaren, A. (1984) Meiosis and differentiation of mouse germ cells. Symp. Soc. Exp. Biol. 38, 7-23
34. McLaren, A. (1988) Somatic and germ-cell sex in mammals. Philos. Trans. R. Soc. London Ser. B 322, 3-9
35. McLaren, A. (2000) Germ and somatic cell lineages in the developing gonad. Mol. Cell. Endocrinol. 163, 3-9
36. McLaren, A. and Buehr, M. (1990) Development of mouse germ cells in cultures of fetal gonads. Cell Differ. Dev. 31, 185-195
37. Memon, M.A., Anway, M.D., Covert, T.R., Uzumcu, M. and Skinner, M.K. (2008) Transforming growth factor beta (TGFbeta1, TGFbeta2 and TGFbeta3) null-mutant phenotypes in embryonic gonadal development. Mol. Cell. Endocrinol. 294, 70-80
38. Meulmeester, E. and Jochemsen, A.G. (2008) p53: a guide to apoptosis. Curr. Cancer Drug Targets 8, 87-97
39. Moreno, S.G., Dutrillaux, B. and Coffigny, H. (2001) Status of p53, p21, mdm2, pRb proteins, and DNA methylation in gonocytes of control and gamma-irradiated rats during testicular development. Biol. Reprod. 64, 1422-1431
40. Mostert, M., Rosenberg, C., Stoop, H., Schuyer, M., Timmer, A., Oosterhuis, W. and Looijenga, L. (2000) Comparative genomic and in situ hybridization of germ cell tumors of the infantile testis. Lab. Invest. 80, 1055-1064
41. Nakatsuji, N. and Chuma, S. (2001) Differentiation of mouse primordial germ cells into female or male germ cells. Int. J. Dev. Biol. 45, 541-548
42. Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S.C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A. et al. (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436, 207-213
43. Pedersen, T. and Peters, H. (1968) Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555-557
44. Petre-Lazar, B., Livera, G., Moreno, S.G., Trautmann, E., Duquenne, C., Hanoux, V., Habert, R. and Coffigny, H. (2007) The role of p63 in germ cell apoptosis in the developing testis. J. Cell. Physiol. 210, 87-98
45. Pohlers, M., Truss, M., Frede, U., Scholz, A., Strehle, M., Kuban, R.J., Hoffmann, B., Morkel, M., Birchmeier, C. and Hagemeier, C. (2005) A role for E2F6 in the restriction of male-germ-cell-specific gene expression. Curr. Biol. 15, 1051-1057
46. Saitou, M., Barton, S.C. and Surani, M.A. (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418, 293-300
47. Sasai, N., Yakura, R., Kamiya, D., Nakazawa, Y. and Sasai, Y. (2008) Ectodermal factor restricts mesoderm differentiation by inhibiting p53. Cell 133, 878-890
48. Setchell, B.P. and Main, S.J. (1978) Drugs and the blood-testis barrier. Environ. Health Perspect. 24, 61-64
49. 2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252, 1427-1430
50. Solc, P., Saskova, A., Baran, V., Kubelka, M., Schultz, R.M. and Motlik, J. (2008) CDC25A phosphatase controls meiosis I progression in mouse oocytes. Dev. Biol. 317, 260-269
51. Sorrentino, E., Nazzicone, V., Farini, D., Campagnolo, L. and De Felici, M. (2007) Comparative transcript profiles of cell cycle-related genes in mouse primordial germ cells, embryonic stem cells and embryonic germ cells. Gene Expression Patterns 7, 714-721
52. Speed, R.M. (1982) Meiosis in the foetal mouse ovary. I. An analysis at the light microscope level using surface-spreading. Chromosoma 85, 427-437
53. Stone, J.E., Ozbirn, R.G., Petes, T.D. and Jinks-Robertson, S. (2008) Role of proliferating cell nuclear antigen interactions in the mismatch repair-dependent processing of mitotic and meiotic recombination intermediates in yeast. Genetics 178, 1221-1236
54. Sweeney, C., Murphy, M., Kubelka, M., Ravnik, S.E., Hawkins, C.F., Wolgemuth, D.J. and Carrington, M. (1996) A distinct cyclin A is expressed in germ cells in the mouse. Development 122, 53-64
55. Swiech, L., Kisiel, K., Czolowska, R., Zientarski, M. and Borsuk, E. (2007) Accumulation and dynamics of proteins of the MCM family during mouse oogenesis and the first embryonic cell cycle. Int. J. Dev. Biol. 51, 283-295
56. Takubo, K., Ohmura, M., Azuma, M., Nagamatsu, G., Yamada, W., Arai, F., Hirao, A. and Suda, T. (2008) Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA damage-induced cell-cycle arrest. Cell Stem Cell 2, 170-182
57. Tam, P.P. and Snow, M.H. (1981) Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morphol. 64, 133-147
58. Tanaka, K. and Nigg, E.A. (1999) Cloning and characterization of the murine Nek3 protein kinase, a novel member of the NIMA family of putative cell cycle regulators. J. Biol. Chem. 274, 13491-13497
59. Toppari, J., Suominenf, J.S. and Yan, W. (2003) The role of retinoblastoma protein family in the control of germ cell proliferation, differentiation and survival. APMIS 111, 245-251; discussion 251
60. Vainio, S., Heikkila, M., Kispert, A., Chin, N. and McMahon, A.P. (1999) Female development in mammals is regulated by Wnt-4 signalling. Nature 397, 405-409
61. van Adelsberg, J.S. (1999) The role of the polycystins in kidney development. Pediatr. Nephrol. 13, 454-459
62. Velasco, A., Riquelme, E., Schultz, M., Wistuba, I.I., Villarroel, L., Pizarro, J., Berlin, A., Ittmann, M., Koh, M.S. and Leach, F.S. (2004) Mismatch repair gene expression and genetic instability in testicular germ cell tumor. Cancer Biol. Ther. 3, 977-982
63. Western, P.S., Miles, D.C., van den Bergen, J.A., Burton, M. and Sinclair, A.H. (2008) Dynamic regulation of mitotic arrest in fetal male germ cells. Stem Cells 26, 339-347
64. Wilhelm, D., Martinson, F., Bradford, S., Wilson, M.J., Combes, A.N., Beverdam, A., Bowles, J., Mizusaki, H. and Koopman, P. (2005) Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev. Biol. 287, 111-124
65. Winkler, K.E., Swenson, K.I., Kornbluth, S. and Means, A.R. (2000) Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 287, 1644-1647
66. Wolgemuth, D.J., Lele, K.M., Jobanputra, V. and Salazar, G. (2004) The A-type cyclins and the meiotic cell cycle in mammalian male germ cells. Int. J. Androl. 27, 192-199
67. Yan, W., Kero, J., Suominen, J. and Toppari, J. (2001) Differential expression and regulation of the retinoblastoma family of proteins during testicular development and spermatogenesis: roles in the control of germ cell proliferation, differentiation and apoptosis. Oncogene 20, 1343-1356
68. Yano, S., Tokumitsu, H. and Soderling, T.R. (1998) Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature 396, 584-587