The role of ovarian surface epithelium in folliculogenesis during fetal development of the bovine ovary: A histological and immunohistochemical study

Sexual Development

Volumn 7, Issue 4, 2013, Pages 180-195

  Kenngott, R A M ^a   Vermehren, M ^a   Ebach, K ^a   Sinowatz, F ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Bovine; Development; Ovary; Surface epithelium

Indexed keywords

BOVINAE;

KI 67 ANTIGEN; PROTEIN S 100;

ANIMAL; APOPTOSIS; BOVINAE; CYTOLOGY; EMBRYOLOGY; EPITHELIUM; EPITHELIUM CELL; FEMALE; FETUS DEVELOPMENT; IMMUNOHISTOCHEMISTRY; METABOLISM; ORGANOGENESIS; OVARY FOLLICLE;

ANIMALS; APOPTOSIS; CATTLE; EPITHELIAL CELLS; EPITHELIUM; FEMALE; FETAL DEVELOPMENT; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; ORGANOGENESIS; OVARIAN FOLLICLE; S100 PROTEINS;

EID: 84875819225     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000348881     Document Type: Article

References (71)

1. Aerts JM, Bols PE: Ovarian follicular dynamics. A review with emphasis on the bovine species. Part II: Antral development, exogenous influence and future prospects. Reprod Domest Anim 45: 180-187 (2010).
2. Anderson R, Fässler R, Georges-Labouesse E, Hynes RO, Bader B.L., et al: Mouse primordial germ cells lacking beta1 integrins enter the germline but fail to migrate normally to the gonads. Development 126: 1655-1664 (1999). (Pubitemid 29204330)
3. Baumgartner EA: Zur Entwicklung des Genitaltraktes beim Rind. Thesis, Bern (1910).
4. Brambell FWR: The development and morphology of the gonads of the mouse. I: the morphogenesis of the indifferent gonad and of the ovary. Proc Roy Soc Lond B: 391 (1927).
5. Burkhart MN, Juengel JL, Smith P.R., Heath DA, Perry GA, et al: Morphological development and characterization of aromatase and estrogen receptors alpha and beta in fetal ovaries of cattle from days 110 to 250. Anim Reprod Sci 117: 43-54 (2010).
6. Byskov AG: The role of the rete ovarii in meiosis and follicle formation in the cat, mink and ferret. J Reprod Fertil 45: 201-209 (1975).
7. Byskov AG: Sexual differentiation of the mammalian ovary, in Motta PM, Hafez ESE (eds): Biology of the Ovary (Martinus Nijhoff Publishers, The Hague 1980).
8. Byskov AG: Differentiation of mammalian embryonic gonad. Physiol Rev 66: 71-117 (1986).
9. Byskov AG, Lintern-Moore S: Follicle formation in the immature mouse ovary: the role of the rete ovarii. J Anat 116: 207-217 (1973).
10. Byskov AG, Skakkebaek NE, Stafanger G, Peters H: Influence of ovarian surface epithelium and rete ovarii on follicle formation. J Anat 123: 77-86 (1977). (Pubitemid 8034885)
11. Clara M: Entwicklungsgeschichte des Menschen, ed 5 (Thieme, Leipzig 1965).
12. Daikoku E, Ito Y, Otsuki Y: The induction of apoptosis in ovaries and uteri of bcl-2-deficient mice. Med Electron Microsc 31: 68-76 (1998). (Pubitemid 28376887)
13. De Pol A., Marzona L, Vaccino F., Negro R, Sena P, Forabosco A: Apoptosis in different stages of humen oogenesis. Anticancer Res 18: 3457-3461 (1998). (Pubitemid 28546475)
14. Didier E: Recherches sur la morphogenese du canal de müller chez les oiseaux. Wilhelm Roux Arch 172: 287-302 (1973).
15. Dominguez MM, Liptrap RM, Basrur PK: Steroidogenesis in fetal bovine gonads. Can J Vet Res 52: 401-406 (1988).
16. Eckery DC, Tisdall DJ, Heath D.A., McNatty KP: Morphology and function of the ovary during fetal and early neonatal life: a comparison between the sheep and brushtail possum (Trichosurus Vulpecula). Anim Rep Sci 42: 551-561 (1996). (Pubitemid 26352253)
17. Edson MA, Nagaraja AK, Matzuk MM: The mammalian ovary from genesis to revelation. Endocr Rev 30: 624-712 (2009).
18. Erickson BH: Development and radio response of the prenatal bovine ovary. J Reprod Fertil 11: 91-105 (1966a).
19. Erickson BH: Development and senescence of the postnatal bovine ovary. J Anim Sci 25: 800-805 (1966b).
20. Fischel A: Lehrbuch der Entwicklung des Menschen. (Springer Verlag, Wien, Berlin 1929).
21. Fortune JE: The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci 78: 135-163 (2003). (Pubitemid 37096411)
22. Fulton N, Martins da Silva SJ, Bayne RA, Anderson RA: Germ cell proliferation and apoptosis in the developing human ovary. J Clin Endocrinol Metab 90: 4664-4670 (2005). (Pubitemid 41166527)
23. Gondos B: Surface epithelium of the developing ovary. Possible correlation with ovarian neoplasia. Am J Pathol 81: 303-321 (1975).
24. Grünwald P: The relation of the growing müllerian duct to the wollfian duct and its importance of the genesis of malformations. Anat Record 81: 1-19 (1941).
25. Haimoto H, Hosoda S, Kato K: Differential distribution of immunoreactive s100-alpha and s100-beta proteins in normal nonnervous human tissues. Lab Invest 57: 489-498 (1987). (Pubitemid 18016483)
26. Hirshfield AN: Heterogeneity of cell populations that contribute to the formation of primordial follicles in rats. Biol Reprod 47: 466-472 (1992).
27. Ireland JJ, Ward F, Jimenez-Krassel F, Ireland J.L., Smith GW, et al: Follicle numbers are highly repeatable within individual animals but are inversely correlated with FSH concentrations and the proportion of good-quality embryos after ovarian stimulation in cattle. Hum Reprod 22: 1687-1695 (2007). (Pubitemid 47055161)
28. Jost AJ, Vigier B, Prépin J, Perchellet JP: Studies in the sex differentiation in mammals. Recent Prog Horm Res 29: 1-41 (1973).
29. Juengel JL, Sawyer HR, Smith P.R., Quirke LD, Heath DA, et al: Origins of follicular cells and ontogeny of steroidogenesis in ovine fetal ovaries. Mol Cell Endocrinol 191: 1-10 (2002). (Pubitemid 34580555)
30. Kamiya S, Tsukushi M, Yamano S., Daigo M: S-100 protein-immunoreactive cells in the bovine ovary. Anat Rec 223: 384-386 (1989). (Pubitemid 19105044)
31. Kenngott R, Sinowatz F: Prenatal development of the bovine ovidcut. Anat Histol Embryol 36: 272-283 (2007).
32. Kenngott R, Sinowatz F: Expression and distribution of intermediate-filament proteins and laminin during the development of the bovine Müllerian duct. Anat Histol Embryol 37: 223-230 (2008). (Pubitemid 351691555)
33. Kenngott R, Vermehren M, Sauer U., Ebach K, Sinowatz F: Cellular expression and localization of estrogen receptor α and progesterone receptor mRNA in the bovine oviduct combining laser-assisted microdissection, quantitative PCR, and in situ hybridization. J Histochem Cytochem 2011:59:312-327.
34. Leung PCK, Adashi EY: The Ovary, ed 2 (Academic Press, San Diego 2003).
35. Mauleon P: Oogenesis and folliculogenesis, in Cole H, Cupps PT (eds): Reproduction in Domestic Animals, pp 187-215 (Academic Press, New York 1969).
36. McGee EA, Hsu SY, Kaipia A, Hsueh AJ: Cell death and survival during ovarian follicle development. Mol Cell Endocrinol 140: 15-18 (1998). (Pubitemid 28375205)
37. McLaren A: Primordial germ cells in the mouse. Dev Biol 262: 1-15 (2003). (Pubitemid 37153101)
38. Michetti F, Lauriola L, Rende M., Stolfi VM, Battaglia F, Cocchia D: S-100 protein in the testis. An immunochemical and immunohistochemical study. Cell Tissue Res 240: 137-142 (1985). (Pubitemid 15112085)
39. Mirecka J, Brinck U, Korabiowska M., Schauer A: Localization of S-100 protein in pig ovarian structures. Folia Histochem and Cytobiol 32: 177-180 (1994). (Pubitemid 24306294)
40. Mosimann W, Kohler T: Zytologie, Histologie und mikroskopische Anatomie der Haussäugetiere. (Paul Parey, Berlin 1990).
41. Motta PM, Makabe S: Development of the ovarian surface and associated germ cells in the human fetus. A correlated study by scanning and transmission electron microscopy. Cell Tissue Res 226: 493-510 (1982). (Pubitemid 13199019)
42. Motta PM, Nottola SA, Makabe S: Natural history of the female germ cell from its origin to full maturation through prenatal ovarian development. Eur J Obstet Gynecol Reprod Biol 75: 5-10 (1997). (Pubitemid 28009858)
43. Mulisch M, Welsch U: Romeis Mikroskopische Technik, ed 18 (Spektrum Akademischer Verlag, Heidelberg 2010).
44. Noden DM, de Lahunta A: The Embryology of Domestic Animals. Development Mechanisms and Malformations. (Williams and Wilkins, London 1985).
45. Noll S, Schaub-Kuhnen S: Praxis der Immunhistochemie. (Urban & Fischer, 2000).
46. Pelliniemi LJ, Salonius AL: Cytological identification of sex in pig embryos at different gonadal stages. Acta Anat (Basel) 95: 558-564 (1976).
47. Pepling ME, Spradling AC: Female mouse germ cells form synchronously dividing cysts. Development 125: 3323-3328 (1998). (Pubitemid 28458332)
48. Pereda J, Zorn T, Soto-Suazo M: Migration of human and mouse primordial germ cells and colonization of the developing ovary: an ultrastructural and cytochemical study. Microsc Res Tech 69: 386-395 (2006). (Pubitemid 43878049)
49. Picton H, Briggs D, Gosden R: The molecular basis of oocyte growth and development. Mol Cell Endocrinol 145: 27-37 (1998). (Pubitemid 29003174)
50. Qi A, Zhang Z, Cao G., Zhang Y: Histological study of germ cells development and apoptosis in Mongolian sheep fetal ovaries. Anim Reprod Sci 103: 179-186 (2008). (Pubitemid 350103854)
51. Romeis B, Böck P: 1989: Mikroskopische Technik. Vol. 17. (Urban und Schwarzenegger, München 1989).
52. Rüsse I: Oogenesis in cattle and sheep. Bibl Anat 24: 77-92 (1983).
53. Rüsse I., Sinowatz F: Lehrbuch der Embryologie der Haustiere (Paul Parey, Berlin/Hamburg 1998).
54. Sarraj MA, Drummond AE: Mammalian foetal ovarian development: consequences for health and disease. Reproduction 143: 151-163 (2012).
55. Sawyer HR, Smith P, Heath D.A., Juengel JL, Wakefield SJ, McNatty KP: Formation of ovarian follicles during fetal development in sheep. Biol Reprod 66: 1134-1150 (2002). (Pubitemid 34266089)
56. Smith P, O W.S., Hudson NL, Shaw L, Heath DA, et al: Effects of the Booroola gene (Fecb) on body weight, ovarian development and hormone concentrations during fetal life. J Reprod Fertil 98: 41-54 (1993). (Pubitemid 23204744)
57. Smith P, O W.S., Corrigan KA, Smith T, Lundy T, et al: Ovarian morphology and endocrine characteristics of female sheep fetuses that are heterozygous or homozygous for the inverdale prolificacy gene (FecX1). Biol Reprod 57: 1183-1192 (1997). (Pubitemid 27461698)
58. Smitz JE, Cortvrindt RG: The earliest stages of folliculogenesis in vitro. Reproduction 123: 185-202 (2002). (Pubitemid 34144669)
59. Stoop H, Honecker F, Cools M., de Krijger R, Bokemeyer C, Looijenga L H: Differentiation and development of human female germ cells during prenatal gonadogenesis: an immunohistochemical study. Hum Reprod 20: 1466-1476 (2005). (Pubitemid 40852235)
60. Tanaka Y, Nakada K, Moriyoshi M., Sawamukai Y: Appearance and number of follicles and change in the concentration of serum FSH in female bovine fetuses. Reproduction 121: 777-782 (2001). (Pubitemid 32475728)
61. Torrey TW: The development of the urinogenital system of the albino rat; the urinogenital union. Am J Anat 81: 139-157 (1947).
62. Vanstapel MJ, Gatter KC, de Wolf-Peeters C, Mason DY, Desmet VD: New sites of human S-100 immunoreactivity detected with monoclonal antibodies. Am J Clin Pathol 85: 160-168 (1986). (Pubitemid 16167114)
63. Vaskivuo TE, Tapanainen JS: Apoptosis in the human ovary. Reprod Biomed Online 6: 24-35 (2003). (Pubitemid 36857115)
64. Viebahn C, Lane EB, Ramaekers FC: The mesonephric (Wolffian) and paramesonephric (Müllerian) ducts of golden hamsters express different intermediate-filament proteins during development. Differentiation 34: 175-188 (1987).
65. Wartenberg H, Hilscher B, Hilscher W: Germ cell kinetics during early ovarian differentiation: an analysis of the oogonial cell cycle and the subsequent changes in oocyte development during the onset of meiosis in the rat. Microsc Res Tech 40: 377-397 (1998). (Pubitemid 28152587)
66. Witschi E: Migration of the germ cells of human embryos from the yolk sac to the primitive gonadal fold. Contr Embryol Carnegie Inst 37: 67 (1948).
67. Wrobel KH, Suss F: Identification and temporospatial distribution of bovine primordial germ cells prior to gonadal sexual differentiation. Anat Embryol (Berl) 197: 451-467 (1998). (Pubitemid 28287057)
68. Wylie C: Germ cells. Cell 96: 165-174 (1999). (Pubitemid 29059347)
69. Yang MY, Fortune JE: The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol Reprod 78: 1153-1161 (2008). (Pubitemid 351749297)
70. Zamboni L, Bezard J, Mauleon P: The role of the mesonephros in the development of the sheep fetal ovary. Ann Biol Anim Biochem Biophys 19: 1153-1178 (1979). (Pubitemid 10237530)
71. Zayed AE, Abd-Elnaeim MM, Abd-Elghaffar S, Hild A., Brehm R, Steger K: Prenatal development of murine gonads with special reference to germ cell differentiation: a morphological and immunohistochemical study. Andrologia 39: 93-100 (2007). (Pubitemid 47245110)