Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Xu, Bo ^a   Hua, Juan ^a   Zhang, Yuanwei ^a   Jiang, Xiaohua ^a   Zhang, Huan ^a   Ma, Tieliang ^a   Zheng, Wei ^a   Sun, Rui ^a   Shen, Wei ^b   Sha, Jiahao ^c   Cooke, Howard J ^d   Shi, Qinghua ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF GUELPH   (Canada)

^c NANJING MEDICAL UNIVERSITY   (China)

^d WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CASPASE 3; CYCLINE; PROTEIN BAX; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 2; APOPTOSIS REGULATORY PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FETUS; GRANULOSA CELL; INHIBITION KINETICS; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEIOTIC PROPHASE I; MOUSE; NEWBORN; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; PACHYTENE; PHASE TRANSITION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; RNA INTERFERENCE; SOMATIC CELL; UPREGULATION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; OVARY; OVARY FOLLICLE; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT;

MAMMALIA;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELLS, CULTURED; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED ICR; OOCYTES; OVARIAN FOLLICLE; OVARY; PREGNANCY; PROLIFERATING CELL NUCLEAR ANTIGEN; RNA, SMALL INTERFERING;

EID: 79251577733     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016046     Document Type: Article

References (76)

1. De Felici M, Scaldaferri ML, Lobascio M, Iona S, Nazzicone V, et al. (2004) Experimental approaches to the study of primordial germ cell lineage and proliferation. Hum Reprod Update 10: 197-206.
2. McLaren A (2000) Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 163: 3-9.
3. Monk M, McLaren A (1981) X-chromosome activity in foetal germ cells of the mouse. J Embryol Exp Morphol 63: 75-84.
4. Borum K (1967) Oogenesis in the mouse. A study of the origin of the mature ova. Exp Cell Res 45: 39-47.
5. Pepling ME (2006) From primordial germ cell to primordial follicle: mammalian female germ cell development. Genesis 44: 622-632.
6. Kezele P, Nilsson E, Skinner MK (2002) Cell-cell interactions in primordial follicle assembly and development. Front Biosci 7: d1990-1996.
7. Pepling ME, Spradling AC (2001) Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 234: 339-351.
8. De Pol A, Vaccina F, Forabosco A, Cavazzuti E, Marzona L (1997) Apoptosis of germ cells during human prenatal oogenesis. Hum Reprod 12: 2235-2241.
9. Coucouvanis EC, Sherwood SW, Carswell-Crumpton C, Spack EG, Jones PP (1993) Evidence that the mechanism of prenatal germ cell death in the mouse is apoptosis. Exp Cell Res 209: 238-247.
10. Lobascio AM, Klinger FG, Scaldaferri ML, Farini D, De Felici M (2007) Analysis of programmed cell death in mouse fetal oocytes. Reproduction 134: 241-252.
11. De Felici M, Lobascio AM, Klinger FG (2008) Cell death in fetal oocytes: many players for multiple pathways. Autophagy 4: 240-242.
12. Rodrigues P, Limback D, McGinnis LK, Plancha CE, Albertini DF (2009) Multiple mechanisms of germ cell loss in the perinatal mouse ovary. Reproduction 137: 709-720.
13. Flaws JA, Marion SL, Miller KP, Christian PJ, Babus JK, et al. (2006) Effect of bcl-2 overexpression in mice on ovotoxicity caused by 4-vinylcyclohexene. Toxicol Appl Pharmacol 215: 51-56.
14. Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL (1995) Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136: 3665-3668.
15. Zhang Z, Shen B, Wang Y, Chen Y, Wang G, et al. (2010) Molecular cloning of proliferating cell nuclear antigen and its differential expression analysis in the developing ovary and testis of penaeid shrimp Marsupenaeus japonicus. DNA Cell Biol 29: 163-170.
16. Picut CA, Swanson CL, Scully KL, Roseman VC, Parker RF, et al. (2008) Ovarian follicle counts using proliferating cell nuclear antigen (PCNA) and semiautomated image analysis in rats. Toxicol Pathol 36: 674-679.
17. Oktay K, Schenken RS, Nelson JF (1995) Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol Reprod 53: 295-301.
18. Muskhelishvili L, Wingard SK, Latendresse JR (2005) Proliferating cell nuclear antigen-a marker for ovarian follicle counts. Toxicol Pathol 33: 365-368.
19. Korfsmeier KH (2002) PCNA in the ovary of zebrafish (Brachydanio rerio, Ham.-Buch.). Acta Histochem 104: 73-76.
20. Kerr JB, Duckett R, Myers M, Britt KL, Mladenovska T, et al. (2006) Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132: 95-109.
21. Hutt KJ, McLaughlin EA, Holland MK (2006) Primordial follicle activation and follicular development in the juvenile rabbit ovary. Cell Tissue Res 326: 809-822.
22. Balla M, Angelopoulou R, Lavranos G, Kittas C (2008) Follicular cells versus oocytes: cell population dynamics in the developing ovary. Tissue Cell 40: 373-381.
23. Wandji SA, Srsen V, Nathanielsz PW, Eppig JJ, Fortune JE (1997) Initiation of growth of baboon primordial follicles in vitro. Human Reproduction 12: 1993-2001.
24. Wandji SA, Srsen V, Voss AK, Eppig JJ, Fortune JE (1996) Initiation in vitro of growth of bovine primordial follicles. Biology of Reproduction 55: 942-948.
25. Tomanek M, Chronowska E (2006) Immunohistochemical localization of proliferating cell nuclear antigen (PCNA) in the pig ovary. Folia Histochemica Et Cytobiologica 44: 269-274.
26. Stoimenov I, Helleday T (2009) PCNA on the crossroad of cancer. Biochem Soc Trans 37: 605-613.
27. Prakash S, Johnson RE, Prakash L (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 74: 317-353.
28. Mirkin EV, Mirkin SM (2007) Replication fork stalling at natural impediments. Microbiol Mol Biol Rev 71: 13-35.
29. Helleday T, Lo J, van Gent DC, Engelward BP (2007) DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst) 6: 923-935.
30. Langerak P, Nygren AO, Krijger PH, van den Berk PC, Jacobs H (2007) A/T mutagenesis in hypermutated immunoglobulin genes strongly depends on PCNAK164 modification. J Exp Med 204: 1989-1998.
31. Morita Y, Perez GI, Paris F, Miranda SR, Ehleiter D, et al. (2000) Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nat Med 6: 1109-1114.
32. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, et al. (1998) Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 12: 1304-1314.
33. Nilsson EE, Skinner MK (2003) Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biology of Reproduction 69: 1265-1272.
34. Wang C, Roy SK (2010) Expression of E-Cadherin and N-Cadherin in Perinatal Hamster Ovary: Possible Involvement in Primordial Follicle Formation and Regulation by Follicle-Stimulating Hormone. Endocrinology.
35. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, et al. (2002) Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 143: 1076-1084.
36. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME (2007) Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 148: 3580-3590.
37. Roa S, Avdievich E, Peled JU, Maccarthy T, Werling U, et al. (2008) Ubiquitylated PCNA plays a role in somatic hypermutation and class-switch recombination and is required for meiotic progression. Proc Natl Acad Sci U S A 105: 16248-16253.
38. Wang C, Roy SK (2006) Expression of growth differentiation factor 9 in the oocytes is essential for the development of primordial follicles in the hamster ovary. Endocrinology 147: 1725-1734.
39. Ogonuki N, Mochida K, Miki H, Inoue K, Fray M, et al. (2006) Spermatozoa and spermatids retrieved from frozen reproductive organs or frozen whole bodies of male mice can produce normal offspring. Proc Natl Acad Sci U S A 103: 13098-13103.
40. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, et al. (2006) Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev Biol 298: 132-148.
41. Wang N, Zhang P, Guo X, Xie J, Huo R, et al. (2009) Comparative proteome profile of immature rat ovary during primordial follicle assembly and development. Proteomics 9: 3425-3434.
42. Shen W, Li L, Bai Z, Pan Q, Ding M, et al. (2007) In vitro development of mouse fetal germ cells into mature oocytes. Reproduction 134: 223-231.
43. Samuel CE (2001) Antiviral actions of interferons. Clin Microbiol Rev 14: 778-809, table of contents.
44. Pebernard S, Iggo RD (2004) Determinants of interferon-stimulated gene induction by RNAi vectors. Differentiation 72: 103-111.
45. Paddison PJ, Silva JM, Conklin DS, Schlabach M, Li M, et al. (2004) A resource for large-scale RNA-interference-based screens in mammals. Nature 428: 427-431.
46. Cleary MA, Kilian K, Wang Y, Bradshaw J, Cavet G, et al. (2004) Production of complex nucleic acid libraries using highly parallel in situ oligonucleotide synthesis. Nat Methods 1: 241-248.
47. Garcia-Rudaz C, Luna F, Tapia V, Kerr B, Colgin L, et al. (2007) Fxna, a novel gene differentially expressed in the rat ovary at the time of folliculogenesis, is required for normal ovarian histogenesis. Development 134: 945-957.
48. De Felici M, McLaren A (1982) Isolation of mouse primordial germ cells. Exp Cell Res 142: 476-482.
49. Soyal SM, Amleh A, Dean J (2000) FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development 127: 4645-4654.
50. Kamat A, Graves KH, Smith ME, Richardson JA, Mendelson CR (1999) A 500-bp region, approximately 40 kb upstream of the human CYP19 (aromatase) gene, mediates placenta-specific expression in transgenic mice. Proc Natl Acad Sci U S A 96: 4575-4580.
51. Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, et al. (1994) Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci U S A 91: 12258-12262.
52. Meredith S, Dudenhoeffer G, Jackson K (2000) Classification of small type B/C follicles as primordial follicles in mature rats. J Reprod Fertil 119: 43-48.
53. Barlow AL, Hulten MA (1998) Crossing over analysis at pachytene in man. Eur J Hum Genet 6: 350-358.
54. Pinon-Lataillade G, Masson C, Bernardino-Sgherri J, Henriot V, Mauffrey P, et al. (2004) KIN17 encodes an RNA-binding protein and is expressed during mouse spermatogenesis. J Cell Sci 117: 3691-3702.
55. Siomi H, Siomi MC (2009) on the road to reading the RNA-interference code. Nature 457: 396-404.
56. Sledz CA, Holko M, de Veer MJ, Silverman RH, Williams BR (2003) Activation of the interferon system by short-interfering RNAs. Nat Cell Biol 5: 834-839.
57. Scott M, Bonnefin P, Vieyra D, Boisvert FM, Young D, et al. (2001) UVinduced binding of ING1 to PCNA regulates the induction of apoptosis. J Cell Sci 114: 3455-3462.
58. Felici MD, Carlo AD, Pesce M, Iona S, Farrace MG, et al. (1999) Bcl-2 and Bax regulation of apoptosis in germ cells during prenatal oogenesis in the mouse embryo. Cell Death Differ 6: 908-915.
59. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721.
60. Vairapandi M, Azam N, Balliet AG, Hoffman B, Liebermann DA (2000) Characterization of MyD118, Gadd45, and proliferating cell nuclear antigen (PCNA) interacting domains. PCNA impedes MyD118 AND Gadd45-mediated negative growth control. J Biol Chem 275: 16810-16819.
61. Greenfeld CR, Pepling ME, Babus JK, Furth PA, Flaws JA (2007) BAX regulates follicular endowment in mice. Reproduction 133: 865-876.
62. Flaws JA, Hirshfield AN, Hewitt JA, Babus JK, Furth PA (2001) Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol Reprod 64: 1153-1159.
63. Rucker EB, 3rd, Dierisseau P, Wagner KU, Garrett L, Wynshaw-Boris A, et al. (2000) Bcl-x and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Mol Endocrinol 14: 1038-1052.
64. Marcinkiewicz JL, Balchak SK, Morrison LJ (2002) The involvement of tumor necrosis factor-alpha (TNF) as an intraovarian regulator of oocyte apoptosis in the neonatal rat. Front Biosci 7: d1997-2005.
65. Wen J, Zhang H, Li G, Mao G, Chen X, et al. (2009) PAR6, a potential marker for the germ cells selected to form primordial follicles in mouse ovary. PLoS One 4: e7372.
66. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM (2004) NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305: 1157-1159.
67. Dissen GA, Romero C, Hirshfield AN, Ojeda SR (2001) Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142: 2078-2086.
68. Choi Y, Ballow DJ, Xin Y, Rajkovic A (2008) Lim homeobox gene, lhx8, is essential for mouse oocyte differentiation and survival. Biol Reprod 79: 442-449.
69. Skinner MK (2005) Regulation of primordial follicle assembly and development. Hum Reprod Update 11: 461-471.
70. Gapienko EF, Markelova IV (1976) [Autoradiographic study of the early stages of human female meiosis in organ culture]. Arkh Anat Gistol Embriol 70: 30-41.
71. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, et al. (2005) Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 25: 9350-9359.
72. Suh EK, Yang A, Kettenbach A, Bamberger C, Michaelis AH, et al. (2006) p63 protects the female germ line during meiotic arrest. Nature 444: 624-628.
73. Livera G, Petre-Lazar B, Guerquin MJ, Trautmann E, Coffigny H, et al. (2008) p63 null mutation protects mouse oocytes from radio-induced apoptosis. Reproduction 135: 3-12.
74. Greenfeld CR, Roby KF, Pepling ME, Babus JK, Terranova PF, et al. (2007) Tumor necrosis factor (TNF) receptor type 2 is an important mediator of TNF alpha function in the mouse ovary. Biol Reprod 76: 224-231.
75. Robker RL, Richards JS (1998) Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol 12: 924-940.
76. Knight PG, Glister C (2006) TGF-beta superfamily members and ovarian follicle development. Reproduction 132: 191-206.