Growth of primordial oocytes in neonatal and adult mammals

Journal of Reproduction and Development

Volumn 56, Issue 6, 2010, Pages 559-566

  Moniruzzaman, Mohammad ^a   Miyano, Takashi ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

Adult; Neonatal; Oocyte growth; Ovary; Primordial follicle

Indexed keywords

ADULT; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; NEWBORN; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE; REVIEW; SEXUAL DEVELOPMENT;

ADULT; ANIMALS; ANIMALS, NEWBORN; FEMALE; HUMANS; INFANT, NEWBORN; MODELS, BIOLOGICAL; OOCYTES; OOGENESIS; OOGONIA; OVARIAN FOLLICLE; SEXUAL DEVELOPMENT;

ANIMALIA; MAMMALIA; SUIDAE;

EID: 79251529849     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.10-071H     Document Type: Review

References (102)

1. Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 1996; 54: 197-207.
2. Lintern-Moore S, Moore GP. The initiation of follicle and oocyte growth in the mouse ovary. Biol Reprod 1979; 20: 773-778.
3. Peters H. The development of the mouse ovary from birth to maturity. Acta Endocrinol 1969; 62: 98-116.
4. Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991; 124: 43-101.
5. Russe I. Oogenesis in cattle and sheep. Biblio Anato 1983; 24: 77-92.
6. Gougeon A. Dynamics of human follicular growth: morphologic, dynamic, and functional aspects. In: Leung PCK and Adashi EY (eds.), The Ovary, 2nd ed, California: Elsevier Academic Press; 2004: 25-43.
7. Oxender WD, Colenbrander B, van deWiel DFM, Wensing CJG. Ovarian development in fetal and prepubertal pigs. Biol Reprod 1979; 21: 715-721.
8. Black JL, Erickson BH. Oogenesis and ovarian development in the prenatal pig. Anat Rec 1968; 161: 45-56.
9. Rajah R, Glaser EM, Hirshfield AN. The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn 1992; 194: 177-192.
10. Martinovitch PN. Development in vitro of the mammalian gonad. Nature 1937; 139: 413.
11. Martinovitch PN. The development in vitro of the mammalian gonad. Ovary and ovogenesis. Proc Royal Soc (Biol) 1938; 125: 232-249.
12. Wandji SA, Sršeò V, Voss AK, Eppig JJ, Fortune JE. Initiation in vitro of growth of bovine primordial follicles. Biol Reprod 1996; 55: 942-948.
13. Wandji SA, Sršeò V, Nathanielsz PW, Eppig JJ, Fortune JE. Initiation of growth of baboon primordial follicles in vitro. Hum Reprod 1997; 12: 1993-2001.
14. Muruvi W, Picton HM, Rodway RG, Joyce IM. In vitro growth of oocytes from primordial follicles isolated from frozen-thawed lamb ovaries. Theriogenology 2005; 64: 1357-1370.
15. Nugent D, Meirow D, Brook PF, Aubard Y, Gosden RG. Transplantation in reproductive medicine: previous experience, present knowledge and future prospects. Hum Reprod Update 1997; 3: 267-280.
16. SP. 'Nude', a new hairless gene with pleiotropic effects in the mouse. Genet Res 1966; 8: 295-309.
17. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983; 301: 527-530.
18. Bosma MJ, Carroll AM. The SCID mouse mutant: Definition, characterization, and potential uses. Annu Rev Immun 1991; 9: 323-350.
19. Gosden RG, Boulton MI, Grant K, Webb R. Follicular development from ovarian xenografts in SCID mice. J Reprod Fertil 1994; 101: 619-623.
20. Moniruzzaman M, Sakamaki K, Akazawa Y, Miyano T. Oocyte growth and follicular development in KIT-deficient Fas-knockout mice. Reproduction 2007; 133: 117-125.
21. Liu J, Van der Elst J, Van den Broecke R, Dhont M. Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biol Reprod 2001; 64: 171-178.
22. Hosoe M, Noguchi J, Kikuchi K, Kaneko H, Tokunaga T. Follicular development and the oocyte maturation in bovine fetal ovaries by xenotransplantation. Cloning Stem Cell 2002; 4: 298-299.
23. Kaneko H, Kikuchi K, Noguchi J, Hosoe M, Akita T. Maturation and fertilization of porcine oocytes from primordial follicles by a combination of xenografting and in vitro culture. Biol Reprod 2003; 69: 1488-1493.
24. Moniruzzaman M, Miyano T. KIT-KIT ligand in the growth of porcine oocytes in primordial follicles. J Reprod Dev 2007; 53: 1273-1281.
25. Miyano T. Bringing up small oocytes to eggs in pigs and cows. Theriogenology 2003; 59: 61-72.
26. Oktay K, Newton H, Mullan J, Gosden RG. Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum Reprod 1998; 13: 1133-1138.
27. Senbon S, Ota A, Tachibana M, Miyano T. Bovine oocytes in secondary follicles grow and acquire meiotic competence in severe combined immunodeficient mice. Zygote 2003; 11: 139-149.
28. Moniruzzaman M, Lee J, Zengyo M, Miyano T. Knockdown of FOXO3 induces primordial oocyte activation in pigs. Reproduction 2010; 139: 337-348.
29. Hage AJ, Groen-Klevant AC, Welschen R. Follicle growth in the immature rat ovary. Acta Endocrinol 1978; 88: 375-382.
30. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122: 829-838.
31. Driancourt M, Reynaud K, Cortvrindt R, Smitz J. Roles of KIT and KIT ligand in ovarian function. Rev Reprod 2000; 5: 143-152.
32. Manova K, Huang EJ, Angeles M, De Leon V, Sanchez S, Pronovost SM, Besmer P, Bachvarova RF. The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev Biol 1993; 157: 85-99.
33. Joyce IM, Pendola FL, Wigglesworth K, Eppig JJ. Oocyte regulation of kit ligand expression in mouse ovarian follicles. Dev Biol 1999; 214: 342-353.
34. Brankin V, Hunter MG, Horan TL, Armstrong DG, Webb R. The expression patterns of mRNA-encoding stem cell factor, internal stem cell factor and c-kit in the prepubertal and adult porcine ovary. J Anat 2004; 205: 393-403.
35. Okamura Y, Myoumoto A, Manabe N, Tanaka N, Okamura H, Fukumoto M. Protein tyrosine kinase expression in the porcine ovary. Mol Hum Reprod 2001; 7: 723-729.
36. Tisdall DJ, Fidler AE, Smith P, Quirke LD, Stent VC, Heath DA, McNatty KP. Stem cell factor and KIT gene expression and protein localization in the sheep ovary during fetal development. J Reprod Fertil 1999; 116: 277-291.
37. Abir R, Fisch B, Jin S, Barnnet M, Kessler-Icekson G, Ao A. Expression of stem cell factor and its receptor in human fetal and adult ovaries. Fertil Steril 2004; 82: 1235-1243.
38. Carlsson IB, Laitinen MPE, Scott JE, Louhio H, Velentzis L, Tuuri T, Aoltonen J, Ritvos O, Winston RML, Hovatta O. Kit ligand and c-kit are expressed during early human ovarian follicular development and their interaction is required for the survival of follicles in long-term culture. Reproduction 2006; 131: 641-649.
39. Geissler EN, Ryan MA, Housman DE. The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 1988; 55: 185-192.
40. Chabot B, Stephenson DA, Chapman VM, Besmer P, Bernstein A. The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 1988; 335: 88-89.
41. Copeland NG, Gilbert DJ, Cho BC, Donovan PJ, Jenkins NA, Cosman D, Anderson D, Lyman SD, Williams DE. Mast cell growth factor maps near the steel locus on mouse chromosome 10 and is deleted in a number of steel alleles. Cell 1990; 63: 175-183.
42. Huang E, Nocka K, Beier DR, Chu TY, Buck J, Lahm HW, Wellner D, Leder P, Besmer P. The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell 1990; 63: 225-233.
43. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, Atkins HL, Hsu RY, Birkett NC, Okino KH, Murdock DC, Jacobsen FW, Langley KE, Smith KA, Takeish T, Cattanach BM, Gall SJ, Suggs SV. Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 1990; 63: 213-224.
44. Russell ES. Hereditary anemias of the mouse: a review for geneticists. Adv Genet 1979; 20: 357-459.
45. Besmer P, Manova K, Duttlinger R, Huang EJ, Packer A, Gyssler C, Bachvarova RF. The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melanogenesis. Development Suppl 1993: 125-137.
46. Sakata S, Sakamaki K, Watanabe K, Nakamura N, Toyokuni S, Nishimune Y, Mori C, Yonehara S. Involvement of death receptor Fas in germ cell degeneration in gonads of Kit-deficient Wv/Wv mutant mice. Cell Death Differ 2003; 10: 676-686.
47. Sakamaki K, Yoshida H, Nishimura Y, Nishikawa S, Manabe N, Yonehara S. Involvement of Fas antigen in ovarian follicular atresia and luteolysis. Mol Reprod Dev 1997; 47: 11-18.
48. Bodensteiner KJ, Clay CM, Moeller CL, Sawyer HR. Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/ differentiation factor-9 in ovine and bovine ovaries. Biol Reprod 1999; 60: 381-386.
49. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996; 383: 531-533.
50. McGrath SA, Esquela AF, Lee SJ. Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 1995; 9: 131-136.
51. Jaatinen R, Laitinen MP, Vuojolainen K, Aaltonen J, Louhio H, Heikinheimo K, Lehtonen E, Ritvos O. Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homolog GDF-9B. Mol Cell Endocrinol 1999; 156: 189-193.
52. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppä L, Louhio H, Tuuri T, Sjöberg J, Bützow R, Hovata O, Dale L, Ritvos O. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab 1999; 84: 2744-2750.
53. Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJW, Hovatta O. Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab 2002; 87: 316-321.
54. Martins FS, Celestino JJ, Saraiva MV, Matos MH, Bruno JB, Rocha-Junior CM, Lima-Verde IB, Lucci CM, Báo SN, Figueiredo JR. Growth and differentiation factor-9 stimulates activation of goat primordial follicles in vitro and their progression to secondary follicles. Reprod Fertil Dev 2008; 20: 916-924.
55. Wang J, Roy SK. Growth differentiation factor-9 and stem cell factor promote primor dial follicle formation in the hamster: modulation by follicle-stimulating hormone. Biol Reprod 2004; 70: 577-585.
56. Elvin JA, Yan C, Matzuk MM. Oocyte-expressed TGF-ß superfamily members in female fertility. Mol Cell Endocrinol 2000; 159: 1-5.
57. Otsuka F, Yao Z, Lee T, Yamamoto S, Erickson GF, Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 2000; 275: 39523-39528.
58. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 1998; 12: 1809-1817.
59. Galloway SM, Gregan SM, Wilson T, McNatty KP, Juengel JL, Ritvos O, Davis GH. BMP15 mutations and ovarian function. Mol Cell Endocrinol 2002; 191: 15-18.
60. Colenbrander B, Kruip TAM, Dieleman SJ, Wensing CJG. Changes in serum LH concentrations during normal and abnormal sexual development in the pig. Biol Reprod 1977; 17: 506-513.
61. Peters H, Byskov AG, Lintern-Moore S, Faber M, Andersen M. The effect of gonadotrophin on follicle growth initiation in the neonatal mouse ovary. J Reprod Fertil 1973; 35: 139-141.
62. Eshkol A, Lunenfeld B. Gonadotropic regulation of ovarian development in mice during infancy. In: Saxena BB, Beling CG, Gandy HM (eds.), Gonadotropins. New York & London: Wiley Interscience; 1972: 335-346.
63. Fortune JE, Kito S, Wandji SA, Sršeò V. Activation of bovine and baboon primordial follicles in vitro. Theriogenology 1998; 49: 441-449.
64. Oktay K, Briggs D, Gosden RG. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab 1997; 82: 3748-3751.
65. Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997; 15: 201-204.
66. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M, Sassone-Corsi P. Impairing follicle stimulating hormone (FSH) signaling in vivo: Targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci USA 1998; 95: 13612-13617.
67. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, Charlton HM. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 2000; 141: 1795-1803.
68. Britt KL, Saunders PK, McPherson SJ, Misso ML, Simpson ER, Findlay JK. Estrogen actions on follicle formation and early follicle development. Biol Reprod 2004; 71: 1712-1723.
69. Huynh K, Jones G, Thouas G, Britt KL, Simpson ER, Jones MEE. Estrogen is not directly required for oocyte developmental competence. Biol Reprod 2004; 70: 1263-1269.
70. Fortune JE, Eppig JJ. Effects of gonadotropins on steroid secretion by infantile and juvenile mouse ovaries in vitro. Endocrinology 1979; 105: 760-768.
71. Montano MM, Müller V, Trobaugh A, Katzenellenbogen BS. The carboxy-terminal F domain of the human estrogen receptor: Role in the transcriptional activity of the receptor and the effectiveness of antiestrogens as estrogen antagonists. Mol Endocrinol 1995; 9: 814-825.
72. Kezele P, Skinner MK. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: Endocrine model of follicle assembly. Endocrinology 2003; 144: 3329-3337.
73. Thau R, Lanman JT, Brinson A. Declining plasma progesterone concentration with advancing gestation in blood from umbilical and uterine veins and fetal heart in monkeys. Biol Reprod 1976; 14: 507-509.
74. McGee EA, Hsueh AJW. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000; 21: 200-214.
75. Brenkman AB, Burgering BMT. FoxO3a eggs on fertility and aging. Trends Mol Med 2003; 9: 464-467.
76. Durlinger ALL, Visser JA, Themmen APN. Regulation of ovarian function: The role of anti-Müllerian hormone. Reproduction 2002; 124: 601-609.
77. Durlinger ALL, Gruijters MJG, Kramer P, Karels B, Ingraham HA, Nachtigal MW, Uilenbroek JTJ, Grootegoed JA, Themmen APN. Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002; 143: 1076-1084.
78. Carlsson IB, Scott JE, Visser JA, Ritvos O, Themmen APN, Hovatta O. Anti-Müllerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod 2006; 21: 2223-2227.
79. Weenen C, Laven JSE, Von Bergh ARM, Cranfield M, Groome NP, Visser JA, Kramer P, Fauser BCJM, Themmen APN. Anti-Müllerian hormone expression pattern in the human ovary: Potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod 2004; 10: 77-83.
80. Hirobe S, He WW, Lee MM, Donahoe PK. Müllerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity. Endocrinology 1992; 131: 854-862.
81. Baarends WM, Uilenbroek JTJ, Kramer P, Hoogerbrugge JW, van Leeuwen ECM, Themmen APN, Grootegoed JA. Anti-Müllerian hormone and anti-Müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology 1995; 136: 4951-4962.
82. Weigel D, Jäckle H. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell 1990; 63: 455-456.
83. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 1999; 96 857-868.
84. Nakamura N, Ramaswamy S, Vazquez F, Signoretti S, Loda M, Sellers WR. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol Cell Biol 2000; 20: 8969-8982.
85. Alvarez B, Martinez-A C, Burgering BMT, Carrera AC. Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 2001; 413: 744-747.
86. Reddy P, Shen L, Ren C, Boman K, Lundin E, Ottander U, Lindgren P, Liu YX, Sun QY, Liu K. Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development. Dev Biol 2005; 281: 160-170.
87. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003; 301: 215-218.
88. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007; 120: 2479-2487.
89. Tran H, Brunet A, Griffith EC, Greenberg ME. The many forks in FOXO's road. Sci STKE 2003; 172: RE5.
90. Kops GJPL, de Ruiter ND, De Vries-Smits AMM, Powell DR, Bos JL, Burgering BMT. Direct control of the forkhead transcription factor AFX by protein kinase B. Nature 1999; 398: 630-634.
91. Biggs WH 3rd, Meisenhelder J, Hunter T, Cavenee WK, Arden KC. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA 1999; 96: 7421-7426.
92. Rena G, Guo S, Cichy SC, Unterman TG, Cohen P. Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J Biol Chem 1999; 274: 17179-17183.
93. John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 2008; 321:197-204.
94. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL, Lan ZJ, Cooney AJ, Huhtaniemi I, Liu K. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008; 319: 611-613.
95. Li J, Kawamura K, Cheng Y, Liu S, Klein C, Liu S, Duan EK, Hsueh AJ. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci USA 2010; 107: 10280-10284.
96. John GB, Shidler MJ, Besmer P, Castrillon DH. Kit signaling via PI3K promotes ovarian follicle maturation but is dispensable for primordial follicle activation. Dev Biol 2009; 331: 292-299.
97. Dijkers PF, Medema RH, Pals C, Banerji L, Thomas NSB, Lam EWF, Burgering BMT, Raaijmakers JAM, Lammers JW, Koenderman L, Coffer PJ. Forkhead transcription factor FKHR-L1 modulates cytokine-dependent transcriptional regulation of p27KIP1. Mol Cell Biol 2000; 20: 9138-9148.
98. Kaldis P. Another piece of the p27Kip1 puzzle. Cell 2007; 128: 241-244.
99. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999; 13: 1501-1512.
100. Nakayama K, Ishida N, Shirane M, Inomata A, Inoue T, Shishido N, Horii I, Loh DY, Nakayama K. Mice lacking p27Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 1996; 85: 707-720.
101. Rajareddy S, Reddy P, Du C, Liu L, Jagarlamudi K, Tang W, Shen Y, Berthet C, Peng SL, Kaldis P, Liu K. p27kip1 (cyclin-dependent kinase inhibitor 1B) controls ovarian development by suppressing follicle endowment and activation and promoting follicle atresia in mice. Mol Endocrinol 2007; 21: 2189-2202.
102. Zetterberg A, Larsson O. Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of swiss 3T3 cells. Proc Natl Acad Sci USA 1985; 82: 5365-5369.