Oocyte-follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans

Microscopy Research and Technique

Volumn 69, Issue 6, 2006, Pages 436-449

  Makabe, Sayoko ^a,d   Naguro, Tomonori ^b   Stallone, Tiziana ^c  

^a TOHO UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d Kanda 2nd Clinic   (Japan)

Author keywords

Follicle cells; Folliculogenesis; Human; ODO maceration; Oocyte; Ovary; Ultrastructure

Indexed keywords

CELLS; CYTOLOGY; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; SCANNING ELECTRON MICROSCOPY;

CELL INTERACTION; FOLLICLE CELLS; FOLLICULOGENESIS; HUMAN; MICROVILLI; OOCYTE; OSMIUM-DIMETHYL SULPHOXIDE-OSMIUM MACERATION; OVARY; ULTRASTRUCTURE; ZONA PELLUCIDA;

DIMETHYL SULFOXIDE;

DIMETHYL SULFOXIDE; OSMIUM DERIVATIVE;

ARTICLE; CELL INTERACTION; CELL JUNCTION; CELL METABOLISM; CELL NUCLEUS; CELL ORGANELLE; CELL ULTRASTRUCTURE; CORONA CELL; CYTOSKELETON; FEMALE; FUNCTIONAL MORPHOLOGY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MACULA ADHERENS; MEMBRANE STRUCTURE; METABOLITE; MICROVILLUS; NUTRIENT; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; OVULATION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SOMATIC CELL; TISSUE PREPARATION; TRANSMISSION ELECTRON MICROSCOPY; ZONA PELLUCIDA; ZONULA ADHERENS;

EID: 33745022290     PISSN: 1059910X     EISSN: 10970029     Source Type: Journal    
DOI: 10.1002/jemt.20303     Document Type: Article

References (95)

1. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppa L, Louhio H, Tuuri T, Sjoberg J, Butzow R, Hovatta O, Dale L, Ritvos O. 1999. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab 84:2744-2750.
2. Ackert CL, Gittens JE, O'Brien MJ, Eppig JJ, Kidder GM. 2001. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 233:258-270.
3. Albertini DF, Anderson E. 1974. The appearance and structure of intercellular connections during the ontogeny of the rabbit ovarian follicle with particular reference to gap junctions. J Cell Biol 63:234-250.
4. Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. 2001. Cellular basis of paracrine regulation of ovarian follicle development. Reproduction 121:647-653.
5. Amsterdam A, Suh BS, Himmelhoch S, Baum G, Ben-Ze'ev A. 1991. Modulation of granulosa cell ultrastructure during differentiation: the role of the cytoskeleton. In: Familiari G, Makabe S, Motta PM, editors. Ultrastructure of the ovary. Boston: Kluwer Academic Publishers, pp. 101-112.
6. Baca M, Zamboni L. 1967. The fine structure of human follicular oocytes. J Ultrastruct Res 19:354-381.
7. Baker TG. 1982. Oogenesis and ovulation. In: Austin CR, Short RV, editors. Reproduction in mammals. I. Germ cells and fertilization. 2nd ed. Cambridge: Cambridge University Press. pp. 17-45.
8. Brower PT, Schultz RM. 1982. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 90:144-153.
9. Bruzzone R, White TW, Paul DL. 1996. Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27.
10. Buccione R, Schroeder AC, Eppig JJ. 1990. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod 43:543-547.
11. Combelles CM, Carabatsos MJ, Kumar TR, Matzuk MM, Albertini DF. 2004. Hormonal control of somatic cell oocyte interactions during ovarian follicle development. Mol Reprod Dev 69:347-355.
12. Dunbar BS, Wolgemuth DJ. 1984. Structure and function of the mammalian zona pellucida, a unique extracellular matrix. In: Satir BH, editor. Modern cell biology, Vol III. New York: Alan Liss Inc. pp. 77-111.
13. Dvorak M, Tesarik J. 1980. Ultrastructure of human ovarian follicles. In: Motta PM, Hafez ESE, editors. Biology of the ovary. The Hague: Martinus Nijhoff Publishers. pp. 121-137.
14. Eddy EM. 1996, The germ line and development. Dev Genet 19:287-289.
15. El-Fouly MA, Cook B, Nekola M, Nalbandov AV. 1970. Role of the ovum in follicular luteinization. Endocrinology 87:286-293.
16. Eppig JJ. 1982. The relationship between cumulus cell-oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev Biol 89:268-272.
17. Eppig JJ. 1991. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13:569-574.
18. Eppig JJ, Chesnel F, Hirao Y, O'Brien MJ, Pendola FL, Watanabe S, Wigglesworth K. 1997. Oocyte control of granulosa cell development: how and why. Hum Reprod 12 (Suppl):127-132.
19. Erickson GF, Shimasaki S. 2000. The role of the oocyte in folliculogenesis. Trends Endocrinol Metab 11:193-198.
20. Familiari G, Nottola SA, Micara G, Aragona C, Motta PM. 1988. Is the sperm-binding capability of the zona pellucida linked to its surface structure? A scanning electron microscopic study of human in vitro fertilization. J In Vitro Fert Embryo Transf 5:134-143.
21. Familiari G, Makabe S, Motta PM. 1989a. The ovary and the ovulation: a three-dimensional ultrastructural study. In: Van Blerkom J, Motta PM, editors. Ultrastructure of human gametogenesis and early embryogenesis. Boston: Kluwer Academic Publishers. pp. 85-124.
22. Familiari G, Nottola SA, Micara G, Aragona C, Motta PM. 1989b. Human in vitro fertilization: the fine three-dimensional architecture of the zona pellucida. In: Motta PM, editor. Developments in ultrastructure of reproduction. New York: Alan R Liss Inc. pp. 335-344.
23. Prog Clin Biol Res 296:335-344.
24. Familiari G, Vizza E, Miani A, Motta PM. 1991. Ultrastructural and functional development of the theca interna. In: Familiari G, Makabe S, Motta PM editors. Ultrastructure of the ovary. Boston: Kluwer Academic Publishers. pp. 113-128.
25. Familiari G, Nottola SA, Macchiarelli G, Micara G, Aragona C, Motta PM. 1992. Human zona pellucida during in vitro fertilization: an ultrastructural study using saponin, ruthenium red, and osmium-thiocarbohydrazide. Mol Reprod Dev 32:51-61.
26. Familiari G, Caggiati A, Nottola SA, Ermini M, Di Benedetto MR, Motta PM. 1993. Ultrastructure of human ovarian primordial follicles after combination chemotherapy for Hodgkin's disease. Hum Reprod 8:2080-2087.
27. Fawcett DW. 1981. The cell. 2nd ed. Philadelphia: WB Saunders Company.
28. Francavilla S, Cordeschi G, Properzi G, Concordia N, Cappa F, Pozzi V. 1990. Ultrastructure of fetal human gonad before sexual differentiation and during early testicular and ovarian development. J Submicrosc Cytol Pathol 22:389-400.
29. Gilchrist RB, Ritter LJ, Armstrong DT. 2004. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 82-83:431-446.
30. Gilula LA. 1977. A simplified stress device for knee arthrography. Radiology 122:828-829.
31. Gondos B, Bhiraleus P, Hobel CJ. 1971. Ultrastructural observations on germ cells in human fetal ovaries. Am J Obstet Gynecol 110:644-652.
32. Greenwald GS, Terranova PF. 1988. Follicular selection and its control. In: Knobil E, Neill G, editors. The physiology of reproduction. New York: Raven Press Ltd. pp. 387-445.
33. Hertig AT. 1968. The primary human oocyte: some observations on the fine structure of Balbiani's vitelline body and the origin of the annulate lamellae. Am J Anat 122:107-137.
34. Hertig AT, Adams EC. 1967. Studies on the human oocyte and its follicle. I. Ultrastructural and histochemical observations on the primordial follicle stage. J Cell Biol 34:647-675.
35. Hope J. 1965. The fine structure of the developing follicle of the Rhesus ovary. J Ultrastruct Res 12:592-610.
36. Hubbard GM, Erickson GF. 1988. Luteinizing hormone-independent luteinization and ovulation in the hypophysectomized rat: a possible role for the oocyte? Biol Reprod 39:183-194.
37. Kellokumpu-Lehtinen PL, Söderström KO. 1978. Occurrence of nuage in fetal germ cells. Cell Tissue Res 194:171-177.
38. Kidder GM, Mhawi AA. 2002. Gap junctions and ovarian folliculogenesis. Reproduction 123:613-620.
39. Knight PG, Glister C. 2003. Local roles of TGF-β superfamily members in the control of ovarian follicle development. Anim Reprod Sci 78:165-183.
40. Larsen WJ, Wert SE, Brunner GD. 1987. Differential modulation of rat follicle cell gap junction populations at ovulation. Dev Biol 122:61-71.
41. Macchiarelli G. 2000. The microvasculature of the ovary. A review by SEM of vascular corrosion casts. J Reprod Dev 46:207-225.
42. Macchiarelli G, Nottola SA, Vizza E, Kikuta A, Murakami T, Motta PM. 1991. Ovarian microvasculature in normal and hCG stimulated rabbits. A study of vascular corrosion casts with particular regard to the interstitium. J Submicrosc Cytol Pathol 23:391-395.
43. Macchiarelli G, Vizza E, Nottola SA, Familiari G, Motta PM. 1992. Cellular and microvascular changes of the ovarian follicle during folliculogenesis: a scanning electron microscopic study. Arch Histol Cytol 55 (Suppl):191-204.
44. Makabe S, Naguro T, Nottola SA, Pereda J, Motta PM. 1991. Migration of germ cells, development of the ovary, and folliculogenesis. In: Familiari G, Makabe S, Motta PM, editors. Ultrastructure of the ovary. Boston: Kluwer Academic Publishers. pp. 1-27.
45. Makabe S, Naguro T, Motta PM. 1992. A new approach to the study of ovarian follicles by scanning electron microscopy and ODO maceration. Arch Histol Cytol 55 (Suppl):183-190.
46. Motta P. 1965a. Electron microscopic demonstration of the presence of cilia and centrioles in ovarian granulosa cells of Lepus cuniculus (Linn). Boll Soc Ital Biol Sper 41:31-33.
47. Motta P. 1965b. Sur l'ultrastructure des "corps de Call et Exner" dans l'ovaire du lapin. Cell Tissue Res 68:308-320.
48. Motta P, Nesci E. 1969. The "Call and Exner bodies" of mammalian ovaries with reference to the problem of rosette formation. Arch Anat Microsc Morphol Exp 58:283-290.
49. Motta PM, DiDio LJA. 1974. Microfilaments in granulosa cells during the development of the follicle and its transformation in corpus luteum in the rabbit ovary. J Submicrosc Cytol 6:15-27.
50. Motta PM, Van Blerkom J. 1974. A scanning electron microscopic study of the luteo-follicular complex. I. Follicle and oocyte. J Submicrosc Cytol 6:297-310.
51. Motta PM, Van Blerkom J. 1975. A scanning electron microscopic study of the luteo- follicular complex. II. Events leading to ovulation. Am J Anat 143:241-264.
52. Motta PM, Van Blerkom J. 1979. Structure and ultrastructure of ovarian follicles. In: Hafez ESE, editor. Human ovulation. Amsterdam: Elsevier/North Holland Biomedical Press. pp. 17-38.
53. Motta PM, Van Blerkom J. 1980. Scanning electron microscopy of the mammalian ovary. In: Motta PM, Hafez ESE, editors. Biology of the ovary. The Hague: Martinus Njihoff Publishers. pp. 162-175.
54. Motta PM, Takeva Z, Nesci E. 1971a. Etude ultrastructurale et histochimique des rapports entre les cellules folliculaires et l'ovocyte pendant le developpement du follicle ovarien chez les mammifères. Acta Anat 80:537-562.
55. Motta PM, Takeva Z, Palermo D. 1971b. On the presence of cilia in different cells of mammalian ovary. Acta Anat 78:591-603.
56. Motta PM, Nottola SA, Micara G, Familiari G. 1988. Ultrastructure of human unfertilized oocytes and polyspermic embryos in an IVF-ET program. Ann N Y Acad Sci 541:367-383.
57. Motta PM, Familiari G, Nottola SA, Micara G, Aragona C. 1991. Microstructural events of human egg investments during in vitro fertilization. Ultrastructure of the zona pellucida and cumulus oophorus. Bull Assoc Anat (Nancy) 75:89-91.
58. Motta PM, Nottola SA, Familiari G, Macchiarelli G, Vizza E. 1992. Follicular structures: an ultrastructural study by scanning and transmission electron microscopy and correlated techniques. In: Sjoberg NO, Hamberger L, Janson PO, Owman Ch, Coeling Bennink HJT, editors. Local regulation of ovarian function. Carnforth, Lanes: Parthenon Publisher. pp. 39-53.
59. Motta PM, Makabe S, Naguro T, Correr S. 1994. Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy. Arch Histol Cytol 57:369-394.
60. Motta PM, Nottola SA, Familiari G, Macchiarelli G, Vizza E, Correr S. 1995a. Ultrastructure of human reproduction from folliculogenesis to early embryo development. A review. Ital J Anat Embryol 100:9-72.
61. Motta PM, Nottola SA, Pereda J, Croxatto HB, Familiari G. 1995b. Ultrastructure of human cumulus oophorus: a transmission electron microscopic study on oviductal oocytes and fertilized eggs. Hum Reprod 10:2361-2367.
62. Motta PM, Makabe S, Nottola SA. 1997. The ultrastructure of human reproduction. I. The natural history of the female germ cell: origin, migration and differentiation inside the developing ovary. Hum Reprod Update 3:281-295.
63. Motta PM, Makabe S, Nottola SA, Macchiarelli G, Familiari G, Correr S. 1998. Morphodynamic events of human oocytes during folliculo-genesis and in the extraovarian microfollicular unit. Assist Reprod Rev 8:205-216.
64. Motta PM, Nottola SA, Familiari G, Macchiarelli G, Correr S, Makabe S. 1999. Structure and function of the human oocyte cumulus-corona cell complex before and after ovulation. Protoplasma 206:270-277.
65. Motta PM, Nottola SA, Makabe S, Heyn R. 2000. Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod 15 (Suppl 2):129-147.
66. Motta PM, Nottola SA, Familiari G, Makabe S, Stallone T, Macchiarelli G. 2003. Morphodynamics of the follicular-luteal complex during early ovarian development and reproductive life. Int Rev Cytol 223:177-288.
67. Murakami T, Ikebuchi Y, Ohtsuka A, Kikuta A, Taguchi T, Ohtani O. 1988. The blood vascular wreath of the rat ovarian follicle, with special reference to its changes in ovulation and luteinization: a scanning electron microscopic study of corrosion casts. Arch Histol Cytol 51:299-313.
68. Nekola MV, Nalbandov AV. 1971. Morphological changes of rat follicular cells as influenced by oocytes. Biol Reprod 4:154-160.
69. Nottola SA, Familiari G, Micara C, Aragona C, Motta PM. 1989. The role of cumulus-corona cells surrounding in vitro human oocytes and polypronuclear ova: An ultrastructural study. In: Motta PM, editor. Developments in ultrastructure of reproduction. New York: Alan R. Liss Inc. pp. 345-354.
70. Prog Clin Biol Res 296:345-354.
71. Nottola SA, Familiari G, Micara G, Aragona C, Motta PM. 1991. The ultrastructure of human cumulus-corona cells at the time of fertilization and early embryogenesis. A scanning and transmission electron microscopic study in an in vitro fertilization program. Arch Histol Cytol 54:145-161.
72. Nottola SA, Macchiarelli G, Familiari G, Stallone T, Sathananthan AH, Motta PM. 1998. Egg-sperm interactions in humans: ultrastructural aspects. Ital J Anat Embryol 103 (Suppl 1):85-101.
73. Phillips DM. 1991. Structure and function of the zona pellucida. In: Familiari G, Makabe S, Motta PM, editors. Ultrastructure of the ovary. Boston: Kluwer Academic Publishers. pp. 63-72.
74. Pozo J, Corral E, Pereda J. 1990. Subcellular structure of prenatal human ovary: mitochondrial distribution during meiotic prophase. J Submicrosc Cytol Pathol 22:601-607.
75. Salustri A, Yanagishita M, Hascall VC. 1990. Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol 138:26-32.
76. Sathananthan AH, Ng SC, Chia CM, Law HY, Edirisinghe WR, Ratnam SS. 1985. The origin and distribution of cortical granules in human oocytes with reference to Golgi, nucleolar, and microfilament activity. Ann N Y Acad Sci 442:251-264.
77. Sathananthan H, Trounson A, Wood C. 1986. Atlas of fine structure of human sperm penetration, eggs and embryos cultured in vitro. New York: Praeger Publishers.
78. Sathananthan AH, Ng SC, Bongso A, Trounson A, Ratnam SS. 1993. Visual atlas of early human development for assisted reproductive technology. Singapore: National University of Singapore.
79. Schultz RM. 1985. Roles of cell-to-cell communication in development. Biol Reprod 32:27-42.
80. Sotelo JR, Porter KR. 1959. An electron microscope study of the rat ovum. J Biophys Biochem Cytol 5:327-341.
81. Stankova J, Cech S, Sedlackova M, Kristek F. 1985. A morphometiic comparative study of healthy and atretic human primordial and primary follicles. Z Mikrosk Anat Forsch 99:510-518.
82. Sundstrom P, Nilsson BO, Liedholm P, Larsson E. 1985. Ultrastructure of maturing human oocytes. Ann N Y Acad Sci 442:324-331.
83. Tanaka K, Naguro T. 1981. High resolution scanning electron microscopy of cell organelles by a new specimen preparation method. Biomed Res 2:63-70.
84. Tesarik J, Dvorak M. 1982. Human cumulus oophorus preovulatory development. J Ultrastruct Res 78:60-72.
85. Valve E, Penttila TL, Paranko J, Harkonen P. 1997. FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem Biophys Res Commun 232:173-177.
86. Van Blerkom J, Motta PM. 1979. Fertilization and preimplantation embryogenesis. In: Van Blerkom J, Motta PM, editors. The cellular basis of mammalian reproduction. Munich: Urban and Schwarzenberg. pp. 165-189.
87. Vanderhyden BC, Macdonald EA. 1998. Mouse oocytes regulate granulosa cell steroidogenesis throughout follicular development. Biol Reprod 59:1296-1301.
88. Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ. 1990. Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol 140:307-317.
89. Wartenberg H, Stegner HE. 1960. Uber die elektronenmikroskopische Feinstruktur des menschlichen ovarialeis. Z Zellforsch Mikrosk Anat 52:450-474.
90. Wassarman PM. 1991. Construction of the zona pellucida during production of fertilizable mouse eggs. Bull Assoc Anat (Nancy) 75:115-117.
91. Weakley BS. 1971. Basic protein and ribonucleic acid in the cytoplasm of the ovarian oocyte in the golden hamster. Z Zellforsch Mikrosk Anat 112:69-84.
92. Zamboni L. 1971. Fine morphology of mammalian fertilization. New York: Harper and Row.
93. Zamboni L. 1974. Fine morphology of the follicle wall and follicle cell-oocyte association. Biol Reprod 10:125-149.
94. Zamboni L, Thompson RS, Smith DM. 1972. Fine morphology of human oocyte maturation in vitro. Biol Reprod 7:425-457.
95. Zoller LC. 1991. Quantitative analysis of the membrana granulosa in developing and ovulatory follicles. In: Familiari G, Makabe S, Motta PM, editors. Ultrastructure of the ovary. Boston: Kluwer Academic Publishers. pp. 73-89.