Thyroxine treatment stimulated ovarian follicular angiogenesis in immature hypothyroid rats

Histology and Histopathology

Volumn 23, Issue 11, 2008, Pages 1387-1398

  Jiang, Jin Yi ^a,d   Miyabayashi, Kanako ^a   Nottola, Stefania A ^b   Umezu, Motoaki ^e   Cecconi, Sandra ^c   Sato, Eimei ^a   Macchiarelli, Guido ^c  

^a TOHOKU UNIVERSITY   (Japan)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e UTSUNOMIYA UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Angiogenic factor; Angiogenic receptor; Hypothyroid rat; Ovarian follicle; SEM; TEM; Thyroid hormone

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CHORIONIC GONADOTROPIN; MESSENGER RNA; THYROXINE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ANGIOGENIC PROTEIN; FIBROBLAST GROWTH FACTOR 2; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HYPOTHYROIDISM; IMMATURITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; PROTEIN EXPRESSION; RAT; UPREGULATION; ANGIOGENESIS; ANIMAL; DISEASE MODEL; DRUG EFFECT; FEMALE; GENETICS; HISTOLOGY; METABOLISM; MICROCIRCULATION; OVARY FOLLICLE; PATHOLOGY; PATHOPHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; VASCULARIZATION; WISTAR RAT;

EQUIDAE; RATTUS;

ANGIOGENIC PROTEINS; ANIMALS; CHORIONIC GONADOTROPIN; CORROSION CASTING; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLAST GROWTH FACTOR 2; HYPOTHYROIDISM; MICROCIRCULATION; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; NEOVASCULARIZATION, PHYSIOLOGIC; OVARIAN FOLLICLE; RATS; RATS, WISTAR; RNA, MESSENGER; THYROXINE; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 58149113194     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Braw R.H. and Tsafriri A. (1980). Effect of PMSG on follicular atresia in the immature rat ovary. J. Reprod. Fertil. 59, 267-272.
2. Breisch E.A., White F.C., Hammond H.K., Flynn S. and Bloor C.M. (1989). Myocardial characteristics of thyroxine stimulated hypertrophy. A structural and functional study. Basic Res. Cardiol. 84, 345-358.
3. Cecconi S., Rossi G., Coticchio G., Macchiarelli G., Borini A. and Canipari R. (2004). Influence of thyroid hormone on mouse preantral follicle development in vitro. Fertil. Steril. 81 (Suppl 1), 919-924.
4. Chilian W.M., Wangler R.D., Peters K.G., Tomanek R.J. and Marcus M.L. (1985). Thyroxine-induced left ventricular hypertrophy in the rat. Anatomical and physiological evidence for angiogenesis. Circ. Res. 57, 591-598.
5. Curiel T.J., Cheng P., Mottram P., Alvarez X., Moons L., Evdemon-Hogan M., Wei S., Zou L., Kryczek I., Hoyle G., Lackner A., Carmeliet P. and Zou W. (2004). Dendritic cell subsets differentially regulate angiogenesis in human ovarian cancer. Cancer Res. 64, 5535-5538.
6. Davis F.B., Mousa S.A., O'Connor L., Mohamed S., Lin H.Y., Cao H.J. and Davis P.J. (2004). Proangiogenic action of thyroid hormone is fibroblast growth factor-dependent and is initiated at the cell surface. Circ. Res. 94, 1500-1506.
7. Dissen G.A., Lara H.E., Fahrenbach W.H., Costa M.E. and Ojeda S.R. (1994). Immature rat ovaries become revascularized rapidly after autotransplantation and show a gonadotropin-dependent increase in angiogenic factor gene expression. Endocrinology 134, 1146-1154.
8. Distler J.H., Hirth A., Kurowska-Stolarska M., Gay R.E., Gay S. and Distler O. (2003). Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q. J. Nucl. Med. 47, 149-161.
9. Egginton S., Zhou A.L., Brown M.D. and Hudlicka O. (2000). The role of pericytes in controlling angiogenesis in vivo. Adv. Exp. Med. Biol. 476, 81-99.
10. Ferrara N., Chen H., Davis-Smyth T., Gerber H.P., Nguyen T.N., Peers D., Chisholm V., Hillan K.J. and Schwall R.H. (1998). Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat. Med. 4, 336-340.
11. Ferrara N. and Davis-Smyth T. (1997). The biology of vascular endothelial growth factor. Endocr. Rev. 18, 4-25.
12. Frater-Schroder M., Risau W., Hallmann R., Gautschi P. and Bohlen P. (1987). Tumor necrosis factor type alpha, a potent inhibitor of endothelial cell growth in vitro, is angiogenic in vivo. Proc. Natl. Acad. Sci. USA 84, 5277-5281.
13. Hanemaaijer R., Koolwijk P., le Clercq L., de Vree W.J. and van Hinsbergh V.W. (1993). Regulation of matrix metalloproteinase expression in human vein and microvascular endothelial cells. Effects of tumour necrosis factor alpha, interleukin 1 and phorbol ester. Biochem. J. 296 (Pt 3), 803-809.
14. Hansen-Smith F.M., Hudlicka O. and Egginton S. (1996). In vivo angiogenesis in adult rat skeletal muscle: early changes in capillary network architecture and ultrastructure. Cell Tissue Res. 286, 123-136.
15. Hirshfield A.N. and Midgley A.R. Jr (1978). Morphometric analysis of follicular development in the rat. Biol. Reprod. 19, 597-605.
16. Hudlicka O., Brown M.D., Walter H., Weiss J.B. and Bate A. (1995). Factors involved in capillary growth in the heart. Mol. Cell Biochem. 147, 57-68.
17. Iijima K., Jiang J.Y., Shimizu T., Sasada H. and Sato E. (2005). Acceleration of follicular development by administration of vascular endothelial growth factor in cycling female rats. J. Reprod. Dev. 51, 161-168.
18. Israely T., Dafni H., Granot D., Nevo N., Tsafriri A. and Neeman M. (2003). Vascular remodeling and angiogenesis in ectopic ovarian transplants: a crucial role of pericytes and vascular smooth muscle cells in maintenance of ovarian grafts. Biol. Reprod. 68, 2055-2064.
19. Jiang J.Y., Miyoshi K., Umezu M. and Sato E. (1999a). Superovulation of immature hypothyroid rdw rats by thyroxine therapy and the development of eggs after in vitro fertilization. J. Reprod. Fertil. 116, 19-24.
20. Jiang J.Y., Umezu M. and Sato E. (1999b). Vitrification of two-cell rat embryos derived from immature hypothyroid rdw rats by in vitro fertilization in ethylene glycol-based solutions. Cryobiology 38, 160-164.
21. Jiang J.Y., Umezu M. and Sato E. (2000). Improvement of follicular development rather than gonadotrophin secretion by thyroxine treatment in infertile immature hypothyroid rdw rats. J. Reprod. Fertil 119, 193-199.
22. Jiang J.Y., Umezu M., Macchiarelli G. and Sato E. (2001). Ovarian microvasculature and angiogenic regulation in follicular development and atresia. In: Reproductive Biotechnology. Miyamoto H. and Manabe N. (eds). Hokuto Shobo (publisher). Kyoto. pp 73-80.
23. Jiang J.Y., Macchiarelli G., Miyabayashi K. and Sato E. (2002). Follicular microvasculature in the porcine ovary. Cell Tissue Res. 310, 93-101.
24. Jiang J.Y., Cheung C.K., Wang Y. and Tsang B.K. (2003a) Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front. Biosci. 8, D222-D237.
25. Jiang J.Y., Macchiarelli G., Tsang B.K. and Sato E. (2003b). Capillary angiogenesis and degeneration in bovine ovarian antral follicles. Reproduction 125, 211-223.
26. Jiang J.Y., Shimizu T., Sasada H., Tsang B.K. and Sato E. (2004). Increased ovarian follicular angiogenesis and dynamic changes of follicular vascular plexuses induced by equine chorionic gonadotropin in the gilt. Cell. Tissue Res. 316, 349-357.
27. Kanzaki H., Okamura H., Okuda Y., Takenaka A., Morimoto K. and Nishimura T. (1982). Scanning electron microscopic study of rabbit ovarian follicle microvasculature using resin injection-corrosion casts. J. Anat. 134, 697-704.
28. Kikuta A., Macchiarelli G. and Murakami T. (1991). Microvasculature of the ovary. In: Ultrastructure of the ovary. Familiari G., Makabe S. and Motta P.M. (eds). Kluwer Academic Publishers: Boston. pp 239-254.
29. Kitai H., Yoshimura Y., Wright K.H., Santulli R. and Wallach E.E. (1985). Microvasculature of preovulatory follicles: comparison of in situ and in vitro perfused rabbit ovaries following stimulation of ovulation. Am. J. Obstet. Gynecol. 152, 889-895.
30. Koolwijk P., van Erck M.G., de Vree W.J., Vermeer M.A., Weich H.A., Hanemaaijer R. and van Hinsbergh V.W. (1996). Cooperative effect of TNFalpha, bFGF, and VEGF on the formation of tubular structures of human microvascular endothelial cells in a fibrin matrix. Role of urokinase activity. J. Cell Biol. 132, 1177-1188.
31. Koos R.D. and LeMaire W.J. (1983). Evidence for an angiogenic factor from rat follicles. In: Factors regulating ovarian function. 8th ed. Greenwald G.S. and Terranova P.F. (eds). Raven Press: New York. pp 191-195.
32. Lehmann W., Edgar C.M., Wang K., Cho T.J., Barnes G.L., Kakar S., Graves D.T., Rueger J.M., Gerstenfeld L.C. and Einhorn T.A. (2005). Tumor necrosis factor alpha (TNF-alpha) coordinately regulates the expression of specific matrix metalloproteinases (MMPS) and angiogenic factors during fracture healing. Bone 36, 300-310.
33. Leibovich S.J., Polverini P.J., Shepard H.M., Wiseman D.M., Shively V. and Nuseir N. (1987). Macrophage-induced angiogenesis is mediated by tumour necrosis factor-alpha. Nature 329, 630-632.
34. Macchiarelli G. (2000). The microvasculature of the ovary: A review by SEM of vascular corrosion casts. J. Reprod. Dev. 46, 207-225.
35. Macchiarelli G., Jiang J.Y., Nottola S.A. and Sato E. (2006). Morphological patterns of angiogenesis in ovarian follicle capillary networks. A scanning electron microscopy study of corrosion cast. Microsc. Res. Tech. 69, 459-468.
36. Macchiarelli G., Nottola S.A., Picucci K., Stallone T. and Motta P.M. (1998). The microvasculature of the corpus luteum in pregnant rabbit. A scanning electron microscopy study of corrosion casts. Ital. J. Anat. Embryol. 103, 191-202.
37. Macchiarelli G., Nottola S.A., Vizza E., Correr S. and Motta P.M. (1995). Changes of ovarian microvasculature in hCG stimulated rabbits. A scanning electron microscopic study of corrosion casts. Ital. J. Anat. Embryol. 100 (Suppl 1), 469-477.
38. Macchiarelli G., Nottola S.A., Vizza E., Familiari G., Kikuta A, Murakami T, Motta PM (1993) Microvasculature of growing and atretic follicles in the rabbit ovary: a SEM study of corrosion casts. Arch. Histol. Cytol. 56, 1-12.
39. Macchiarelli G., Nottola S.A., Vizza E., Kikuta A., Murakami T. and Motta P.M. (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.
40. Macchiarelli G., Vizza E., Nottola S.A., Familiari G. and Motta P.M. (1992). Cellular and microvascular changes of the ovarian follicle during folliculogenesis: a scanning electron microscopic study. Arch. Histol. Cytol. 55 (Suppl), 191-204.
41. Maruo T., Katayama K., Barnea E.R. and Mochizuki M. (1992). A role for thyroid hormone in the induction of ovulation and corpus luteum function. Horm. Res. 37 (Suppl 1), 12-18.
42. Mattioli M., Barboni B., Turriani M., Galeati G., Zannoni A., Castellani G., Berardinelli P. and Scapolo P.A. (2001). Follicle activation involves vascular endothelial growth factor production and increased blood vessel extension. Biol. Reprod. 65, 1014-1019.
43. Miyamoto Y., Nakayama T., Haraguchi S., Miyamoto H. and Sato E. (1996). Morphological evaluation of microvascular networks and angiogenic factors in the selective growth of oocytes and follicles in the ovaries of mouse fetuses and newborns. Dev. Growth Differ. 38, 291-298.
44. Motta P.M., Nottola S.A., Familiari G., Makabe S., Stallone T. and Macchiarelli G. (2003). Morphodynamics of the follicular-luteal complex during early ovarian development and reproductive life. Int. Rev. Cytol. 223, 177-288.
45. Murakami T. (1971). Application of the scanning electron microscope to the study of fine distribution of the blood vessels. Arch. Histol. Jpn. 32, 445-454.
46. Murakami T., Ikebuchi Y., Ohtsuka A., Kikuta A., Taguchi T. and Ohtani O. (1988). The blood vascular wreath of 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.
47. Nehls V., Denzer K. and Drenckhahn D. (1992). Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res. 270, 469-474.
48. Nicosia R.F. and Villaschi S. (1995). Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab. Invest. 73, 658-666.
49. Nicosia R.F. and Villaschi S. (1999). Autoregulation of angiogenesis by cells of the vessel wall. Int. Rev. Cytol. 185, 1-43.
50. Prange-Kiel J., Kreutzkamm C., Wehrenberg U. and Rune G.M. (2001). Role of tumor necrosis factor in preovulatory follicles of swine. Biol. Reprod. 65, 928-935.
51. Pyter L.M., Hotchkiss A.K. and Nelson R.J. (2005). Photoperiod-induced differential expression of angiogenesis genes in testes of adult Peromyscus leucopus. Reproduction 129, 201-209.
52. Redmer D.A., Doraiswamy V., Bortnem B.J., Fisher K., Jablonka-Shariff A., Grazul-Bilska A.T. and Reynolds L.P. (2001). Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol. Reprod. 65, 879-889.
53. Redmer D.A. and Reynolds L.P. (1996). Angiogenesis in the ovary. Rev. Reprod. 1, 182-192.
54. Rhodin J.A. and Fujita H. (1989). Capillary growth in the mesentery of normal young rats. Intravital video and electron microscope analyses. J. Submicrosc. Cytol. Pathol. 21, 1-34.
55. Ryuto M., Ono M., Izumi H., Yoshida S., Weich H.A., Kohno K. and Kuwano M. (1996). Induction of vascular endothelial growth factor by tumor necrosis factor alpha in human glioma cells. Possible roles of SP-1. J. Biol. Chem. 271, 28220-28228.
56. Sato E. and Jiang J.Y. (2001). Follicular development and ovulation in hypothyroid rdw rats. Ital. J. Anat. Embryol. 106, 249-256.
57. Sato E., Ishibashi T. and Koide S.S. (1982). Inducement of blood vessel formation by ovarian extracts from mice injected with gonadotropins. Experientia 38, 1248-1249.
58. Sato N., Fukuda K., Nariuchi H. and Sagara N. (1987). Tumor necrosis factor inhibiting angiogenesis in vitro. J. Natl. Cancer Inst. 79, 1383-1391.
59. Scott B.B., Zaratin P.F., Gilmartin A.G., Hansbury M.J., Colombo A., Belpasso C., Winkler J.D. and Jackson J.R. (2005). TNF-alpha modulates angiopoietin-1 expression in rheumatoid synovial fibroblasts via the NF-kappa B signalling pathway. Biochem. Biophys. Res. Commun. 328, 409-414.
60. Shimizu T., Jiang J.Y., Sasada H. and Sato E. (2002). Changes of messenger RNA expression of angiogenic factors and related receptors during follicular development in gilts. Biol. Reprod. 67, 1846-1852.
61. Shimizu T., Jiang J.Y., Sasada H. and Sato E. (2003). Angiogenesis during porcine follicular development. In: Animal Frontier Sciences - Life science update in animal science. Sato E., Miyamoto H. and Manabe N. (eds). Hokuto Shobo (publisher). Kyoto, Japan. pp 109-116.
62. Stouffer R.L., Martinez-Chequer J.C., Molskness T.A., Xu F. and Hazzard T.M. (2001). Regulation and action of angiogenic factors in the primate ovary. Arch. Med. Res. 32, 567-575.
63. Tapia G., Fernandez V., Varela P., Cornejo P., Guerrero J. and Videla L.A. (2003). Thyroid hormone-induced oxidative stress triggers nuclear factor-kappaB activation and cytokine gene expression in rat liver. Free Radic. Biol. Med. 35, 257-265.
64. Terranova P.F. (1997). Potential roles of tumor necrosis factor-alpha in follicular development, ovulation, and the life span of the corpus luteum. Domest. Anim. Endocrinol. 14, 1-15.
65. Tomanek R.J., Connell P.M., Butters C.A. and Torry R.J. (1995). Compensated coronary microvascular growth in senescent rats with thyroxine-induced cardiac hypertrophy. Am. J. Physiol. 268, 419-425.
66. Tomanek R.J., Doty M.K. and Sandra A. (1998). Early coronary angiogenesis in response to thyroxine: growth characteristics and upregulation of basic fibroblast growth factor. Circ. Res. 82, 587-593.
67. van Hinsbergh V.W., van den Berg E.A., Fiers W. and Dooijewaard G. (1990). Tumor necrosis factor induces the production of urokinase-type plasminogen activator by human endothelial cells. Blood 75, 1991-1998.
68. Wakim N.G., Ramani N. and Rao C.V. (1987). Triiodothyronine receptors in porcine granulosa cells. Am. J. Obstet. Gynecol. 156, 237-240.
69. Wakim A.N., Polizotto S.L., Buffo M.J., Marrero M.A. and Burholt D.R. (1993). Thyroid hormones in human follicular fluid and thyroid hormone receptors in human granulosa cells. Fertil. Steril. 59, 1187-1890.
70. Wakim A.N., Paljug W.R., Jasnosz K.M., Alhakim N., Brown A.B. and Burholt D.R. (1994). Thyroid hormone receptor messenger ribonucleic acid in human granulosa and ovarian stromal cells. Fertil. Steril. 62, 531-534.
71. Wakim A.N., Polizotto S.L. and Burholt D.R. (1995). Influence of thyroxine on human granulosa cell steroidogenesis in vitro. J. Assist. Reprod. Genet. 12, 274-277.
72. Watanabe Y., Lee S.W., Detmar M., Ajioka I. and Dvorak H.F. (1997). Vascular permeability factor/vascular endothelial growth factor (VPF/ VEGF) delays and induces escape from senescence in human dermal microvascular endothelial cells. Oncogene 14, 2025-2032.
73. Yamada O., Abe M., Takehana K., Hiraga T., Iwasa K. and Hiratsuka T. (1995). Microvascular changes during the development of follicles in bovine ovaries: a study of corrosion casts by scanning electron microscopy. Arch. Histol. Cytol. 58, 567-574.
74. Zhang S.S., Carrillo A.J. and Darling D.S. (1997). Expression of multiple thyroid hormone receptor mRNAs in human oocytes, cumulus cells, and granulosa cells. Mol. Hum. Reprod. 3, 555-562.
75. Zhou A., Egginton S., Hudlicka O. and Brown M.D. (1998a). Internal division of capillaries in rat skeletal muscle in response to chronic vasodilator treatment with alpha 1-antagonist prazosin. Cell Tissue Res. 293, 293-303.
76. Zhou A.L., Egginton S., Brown M.D. and Hudlicka O. (1998b). Capillary growth in overloaded, hypertrophic adult rat skeletal muscle: an ultrastructural study. Anat. Rec. 252, 49-63.