Angiogenesis in the female reproductive organs: Pathological implications

International Journal of Experimental Pathology

Volumn 83, Issue 4, 2002, Pages 151-164

  Reynolds, Lawrence P ^a   Grazul Bilska, Anna T ^a   Redmer, Dale A ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; FIBROBLAST GROWTH FACTOR; VASCULOTROPIN;

ADENOMYOSIS; ANGIOGENESIS; BIOLOGICAL MONITORING; BLOOD FLOW; CANCER INCIDENCE; DISEASE ASSOCIATION; ENDOMETRIOSIS; ENDOMETRIUM CARCINOMA; ENDOMETRIUM HYPERPLASIA; FEMALE GENITAL SYSTEM; FETUS GROWTH; HUMAN; METRORRHAGIA; NIDATION; NONHUMAN; OVARY; OVARY CARCINOMA; OVARY DISEASE; OVARY POLYCYSTIC DISEASE; PATHOLOGY; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; TISSUE GROWTH; UTERUS; UTERUS MYOMA; VASCULARIZATION;

EID: 0036902397     PISSN: 09599673     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2613.2002.00277.x     Document Type: Review

References (99)

1. Abulafia O. & Sherer D.M. (2000) Angiogenesis of the ovary. Am. J. Obstet. Gynecol. 182, 240-246.
2. Adair T.H., Gay W.J. & Montani J.-P. (1990) Growth regulation of the vascular system: Evidence for a metabolic hypothesis. Am. J. Physiol. 259, R393-R404.
3. Amselgruber W.M., Schafer M. & Sinowatz F. (1999) Angiogenesis in the bovine corpus luteum: An immunocytochemical and ultrastructural study. Anat. Histol. Embryol. 28, 157-166.
4. Anthony F.W., Gornall R.J., Lincoln J., Richardson M.C., Hitchcock A. & Stones R.W. (1997) Expression of endothelial nitric oxide synthase in the human corpus luteum. J. Reprod. Fertil. Abstract. Series 19, 63.
5. Arman E., Haffner-Krausz R., Chen Y., Heath J.K. & Lonai P. (1998) Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA 95, 5082-5087.
6. Augustin H.G. (2000) Vascular morphogenesis in the ovary. Bailliere's Clin. Obstet. Gynecol. 14, 867-882.
7. Ballara S.C., Miotla J.M. & Paleolog E.M. (1999) New vessels, new approaches: Angiogenesis as a therapeutic target in musculoskeletal disorders. Int. J. Exp. Pathol. 80, 235-250.
8. Barinaga M. (1997) Cancer research: Designing therapies that target tumor blood vessels. Science 275, 482-484.
9. Bernard C. (1865) An Introduction to the Study of Experimental Medicine. Translated by H.C. Greene (Copyright 1927). New York: Schuman.
10. Brown M.R., Blanchette J.O. & Kohn E.C. (2000) Angiogenesis in ovarian cancer. Bailliere's Clin. Obstet. Gynecol. 14, 901-918.
11. Carmeliet P., Ferreira V., Breier G. et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439.
12. Charnock-Jones S.D. & Smith S.K. (2001) Placental vascular morphogenesis: Introduction and overview. In: Vascular Morphogenesis in the Female Reproductive System. Eds. H.G. Augustin, M.L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 273-284.
13. Christenson L.K. & Stouffer R.L. (1996) Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology 137, 367-374.
14. D'Amore P.A. & Klagsbrun M. (1989) Angiogenesis: Factors and mechanisms. In: The Pathobiology of Neoplasia. Ed: A.E. Sirica: New York: Plenum; pp. 513-531.
15. Denekamp J. (1984) Vasculature as a target for tumour therapy. In: Progress in Applied Microcirculation, Vol 4. Eds: F. Hammersen & O. Hudlicka. Basel: Karger; pp. 28-38.
16. Dharmarajan A.M., Bruce N.W. & Meyer G.T. (1985) Quantitative ultrastructural characteristics relating to transport between luteal cell cytoplasm and blood in the corpus luteum of the pregnant rat. Am. J. Anat. 172, 87-99.
17. Doldi N., Bassau M., Gulisano M., Broccoli V., Boucinelli E. & Ferraria A. (1996) Vascular endothelial growth factor messenger ribonucleic acid expression in human ovarian and endometrial cancer. Gynecol. Endocrinol. 10, 375-382.
18. Dorajswamy V., Knutson D.L., Grazul-Bilska A.T., Redmer D.A. & Reynolds L.P. (1998) Fibroblast growth factor receptor (FGFR) -1 and -2 in the ovine corpus luteum throughout the estrous cycle. Growth Factors 16, 125-135.
19. Edey T.N. (1969) Prenatal mortality in sheep: A review. Anim Breeders Abstract 37, 173-190.
20. Ferenczy A. & Bergeron C. (1989) Endometrial hyperplasia and neoplasia. In: Biology of the Uterus, 4th Edn. Eds: R.M. Wynn & W.P. Jollie. New York: Plenum; pp. 333-353.
21. Ferrara N., Carver-Moore K., Chen H. et al. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442.
22. Ferrara N., Chen H., Davis-Smyth T., Gerber H.P., Nguyen T.N., Peers D., Chisolm V., Hillan K.J. & Schwall R.H. (1998) Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nature Med. 4, 336-340.
23. Ferrara N. & Davis-Smyth T. (1997) The biology of vascular endothelial growth factor. Endocrine Rev. 18, 4-25.
24. Folkman J. & Klagsbrun M. (1987) Angiogenic factors. Science 233, 442-447.
25. Fong G.H., Rossant J., Gertsenstein M. & Breitman M.L. (1995) Role of the flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66-70.
26. Fox S.B. (2001) Angiogenesis in mammary tumors: Quantitation and relation to prognosis. In: Vascular Morphogenesis in the Female Reproductive System. Eds: H.G. Augustin, M. L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 63-85.
27. Fraser H., Dickson S.E., Lunn S.F. et al. (2000) Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 141, 995-1000.
28. Fraser H. & Lunn S.F. (2000) Angiogenesis and its control in the female reproductive system. Br. Med. Bull. 56, 787-797.
29. Fraser H. & Lunn S.F. (2001) Regulation and manipulation of angiogenesis in the primate corpus luteum. Reproduction 121,355-362.
30. Gargett C.E. & Rogers P.A.W. (2001) Human endometrial angiogenesis. Reproduction 121, 181-186.
31. Garrido C., Saule S. & Gospodarowicz D. (1993) Transcriptional regulation of vascular endothelial growth factor gene expression in ovarian bovine granulosa cells. Growth Factors 8, 109-117.
32. Geva E. & Jaffe R.B. (2000) Role of vascular endothelial growth factor in ovarian physiology and pathology. Fert. Steril. 74, 429-438.
33. Goede V., Schmidt T., Kimmina S., Kozian D. & Augustin H.G. (1998) Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Laboratory Invest. 78, 1385-1394.
34. Gospodarowicz D. (1991) Biological activities of fibroblast growth factors. Ann. NY Acad. Sci. 638, 1-8.
35. Grazul-Bilska A.T., Redmer D.A., Jablonka-Shariff A., Biondini M.E. & Reynolds L.P. (1995) Proliferation and progesterone production of ovine luteal cells from several stages of the estrous cycle: Effects of fibroblast growth factors (FGF) and luteinizing hormone (LH). Can. J. Physiol. Pharmacol. 73, 491-500.
36. Grazul-Bilska A.T., Redmer D.A. & Reynolds L.P. (2001) Growth factors during ovarian angiogenesis. In: Vascular Morphogenesis in the Female Reproductive System. Eds: H.G. Augustin, M.L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 131-147.
37. Greenwald G.S. (1989) Temporal and topographic changes in dna synthesis after induced follicular atresia. Biol. Reprod. 41, 175-181.
38. Guidi A.J., Abu-Jawdeh G., Tognazzi K., Dvorak H.F. & Brown L.F. (1996) Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in endometrial carcinoma. Cancer 78, 454-460.
39. Hata K., Nagami H., Ilda K., Miyazaki K. & Collins W.P. (1998) Expression of thymidine phosphorylase in malignant ovarian tumors: Correlation with microvessel density and an ultrasound-derived index of angiogenesis. Ultrasound Obstet. Gynecol. 12, 201-206.
40. Hickey M. & Fraser I.S. (2001) The clinical relevance of disturbances of uterine vascular growth, remodeling, and repair. In: Vascular Morphogenesis in the Female Reproductive System. Eds: H.G. Augustin, M.L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 223-244.
41. Hildebrandt V.A., Babischkin J.S., Koos R.D., Pepe G.J. & Albrecht E.D. (2001) Developmental regulation of vascular endothelial growth/permeability factor messenger ribonucleic acid leveis in and vascularization of the villous placenta during baboon pregnancy. Endocrinology 142, 2050-2057.
42. Hood J.D., Meininger C.J., Ziche M. & Granger H.J. (1998) VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am. J. Physiol. 274, H1054-H1058.
43. Hudlicka O. (1984) Development of microcirculation: Capillary growth and adaptation. In: Handbook of Physiology, Vol. IV. Eds: E.M. Renkin & C.C. Michel. Baltimore: Waverly Press; pp. 165-216.
44. Hyder S.M. & Stancel G.M. (2000) Regulation of VEGF in the reproductive tract by sex-steroid hormones. Histol. Histopathol. 15, 325-334.
45. Jaffe R.B. (2000) Importance of angiogenesis in reproductive physiology. Seminars Perinatol. 24, 79-81.
46. King R.J.B. & D'Arcangues C. (1992) Steroid hormone effects on uterine blood vessels. In: Steroid Hormones and Uterine Bleeding. Eds. N.J. Alexender & C. D'Arcangues. Washington DC: AAAS Press; pp. 25-36.
47. Klein P.S. & Melton D.A. (1994) Hormonal regulation of embryogenesis: The formation of mesoderm on xenopul laevis. Endocrine Rev. 15, 326-341.
48. Kohn E.C. (1997) Angiogenesis in ovarian carcinoma. Cancer 80, 2219-2221.
49. Kohn E.C. & Libutti S.K. (2001) Angiogenesis, vascular imaging, and therapeutic approaches in ovarian tumors. In: Vascular Morphogenesis in the Female Reproductive System. Eds: H.G. Augustin, M. L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 187-205.
50. Koos R.D. (1995) Increased expression of vascular endothelial growth/permeability factor in the rat ovary following an ovulatory gonadotropin stimulus: Potential roles in follicle rupture. Biol. Reprod. 52, 1426-1435.
51. Lamming G.E., Darwash A.O. & Back H.L. (1989) Corpus luteum function in dairy cows and embryo mortality. J. Reprod. Fertil. Supplement 37, 245-252.
52. Magness R.R. (1998) Maternal cardiovascular and other physiological responses to the endocrinology of pregnancy. In: The Endocrinology of Pregnancy., Ed: F.W. Bazer. Totowa, NJ: Humana Press; pp. 507-539.
53. Miller D.L., Ortega S., Bashayan O., Basch R. & Basilico C. (2000) Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotype defects observed in FGF2 null mice. Mol. Cell. Biol. 20, 2260-2268.
54. Moor R.M. & Seamark R.F. (1986) Cell signaling, permeability, and microvasculatory changes during antral follicle development in mammals. J. Dairy Sci. 69, 927-943.
55. Mueller M.D. & Taylor R.N. (2001) Angiogenesis in endometriosis. In: Vascular Morphogenesis in the Female Reproductive System. Eds: H.G. Augustin, M.L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 245-270.
56. Neufeld G., Cohen T., Gengrinovitch S. & Poltorak Z. (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9-22.
57. Niswender G.D. & Nett T.M. (1988) The corpus luteum and its control. In: The Physiology of Reproduction. Eds: E. Knobil et al. New York: Raven Press; pp. 489-525.
58. North R.A., Ferrier C., Long D., Townend K. & Kincaid-Smith P. (1994) Uterine artery Doppler flow velocity waveforms in the second trimester for the prediction of preeclampsia and fetal growth retardation. Obstet. Gynecol. 83, 378-386.
59. Ortega S., Ittmann M., Tsang S.H., Ehrlich M. & Basilico C. (1998) Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. USA 95, 5672-5677.
60. Plendl J. (2000) Angiogenesis and vascular regression in the ovary. Anat. Histol. Embryol. 29, 257-266.
61. Ravindranath N., Little-Ihrig L., Phillips H.S., Ferrara N. & Zeleznik A.J. (1992) Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology 131,254-260.
62. Redmer D.A., Dai Y., Li J. et al. (1996) Characterization and expression of vascular endothelial growth factor (VEGF) in the ovine corpus luteum. J. Reprod. Fertil. 108, 157-165.
63. Redmer D.A., Doraiswamy V., Bortnem B.J et al. (2001) Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol. Reprod. 65, 879-889.
64. Redmer D.A., Grazul A.T., Kirsch J.D. & Reynolds L.P. (1988) Angiogenic activity of bovine corpus luteum at several stages of luteal development. J. Reprod. Fertil. 82, 627-634.
65. Redmer D.A., Kirsch J.D. & Grazul A.T. (1987) In vitro production of angiotropic factor by bovine corpus luteum partial characterization of activities that are chemotactic and mitogenic for endothelial cells. In: Regulation of Ovarian and Testicular Function. Adv. Exp. Medical Biol. Vol 219. Eds: V.B. Mahesh, D.S. Dhindsa, E. Anderson & S.P. Kalra. New York: Plenum Press: pp. 683-688.
66. Redmer D.A., Kirsch J.D. & Reynolds L.P. (1991) Production of mitogenic factors by cell types of estrogen-active and estrogen-inactive preovulatory bovine follicles. J. Anim. Sci. 69, 237-245.
67. Redmer D.A. & Reynolds L.P. (1996) Angiogenesis in the ovary. Rev. Reprod. 1, 182-192.
68. Redmer D.A., Rone J.D. & Goodman A.L. (1985) Evidence for a non-steroidal angiotropic factor from the primate corpus luteum: Stimulation of endothelial cell migration in vitro. Proc. Soc. Exp. Biol. Medical 179, 136-140.
69. Reynolds L.P. (1986) Utero-ovarian interactions during early pregnancy: Role of conceptus-induced vasodilation. J. Anim. Sci. 62 (Suppl. 2), 47-61.
70. Reynolds L.P., Grazul-Bilska A.T. & Redmer D.A. (2000) Angiogenesis in the corpus luteum. Endocrine 12, 1-9.
71. Reynolds L.P., Killilea S.D., Grazul-Bilska A.T. & Redmer D.A. (1994) Mitogenic factors of corpora lutea. Progr. Growth Factor Res. 5, 159-175.
72. Reynolds L.P., Killilea S.D. & Redmer D.A. (1992) Angiogenesis in the female reproductive system. FASEB J. 6, 886-892.
73. Reynolds L.P., Kirsch J.D., Kraft K.C. & Redmer D.A. (1998a) Time-course of the uterine response to estradiol-17â in ovariectomized ewes: Expression of angiogenic factors. Biol. Reprod. 59, 613-620.
74. Reynolds L.P., Kirsch J.D., Kraft K.C., Knutson D.L., McClaflin W.J. & Redmer D.A. (1998b) Time-course of the uterine response to estradiol-17â in ovariectomized ewes: Uterine growth and microvascular development. Biol. Reprod. 59, 606-612.
75. Reynolds L.P., Millaway D.S., Kirsch J.D., Infeld J.E. & Redmer D.A. (1990) Growth and in vitro metabolism of placental tissues of cows from Day 100 to Day 250 of gestation. J. Reprod. Fertil. 89, 213-222.
76. Reynolds L.P. & Redmer D.A. (1992) Growth and microvascular development of the uterus during early pregnancy in ewes. Biol. Reprod. 47, 698-708.
77. Reynolds L.P. & Redmer D.A. (1995) Utero-placental vascular development and placental function. J. Anim. Sci. 73, 1839-1851.
78. Reynolds L.P. & Redmer D.A. (1998) Expression of the angiogenic factors, basic fibroblast growth factor (bFGF) and vascular endothelial growth factor (VEGF), in the ovary. J. Anim. Sci. 76, 1671-1681.
79. Reynolds L.P. & Redmer D.A. (1999) Growth and development of the corpus luteum. J. Reprod. Fertil. Supplement 54, 179-189.
80. Reynolds L.P. & Redmer D.A. (2001) Angiogenesis in the placenta. Biol. Reprod. 64, 1033-1040.
81. Rider V. & Piva M. (1998) Role of growth factors of uterine and fetal-placental origin during pregnancy. In: The Endocrinology of Pregnancy. Ed: F.W. Bazer. Totowa, NJ: Humana Press; pp. 83-124.
82. Rogers P.A.W. & Gargett C.E. (2001) The vascular system in the endometrium: Introduction and overview. In: Vascular Morphogenesis in the Female Reproductive System. Eds: H.G. Augustin, M.L. Iruela-Arispe, P.A.W. Rogers & S.K. Smith. Boston: Birkhauser; pp. 209-222.
83. Rogers P.A.W., Lederman R., Kooy J., Taylor N.H. & Healy D.L. (1996) Endometrial vascular smooth muscle oestrogen and progesterone receptor distribution in women with and without menorrhagia. Hum. Reprod. 11, 2003-2008.
84. Schiffenbauer Y.S., Abramovitch R., Mele G. et al. 1997) Loss of ovarian function promotes angiogenesis in human ovarian carcinoma. Proc. Natl. Acad. Sci. USA 94, 13203-13208.
85. Shalaby F., Rossant J., Yamaguchi T.P. et al. (1995) Failure of blood island formation and vasculogenesis in flk-1 deficient mice. Nature 376, 62-66.
86. Short R.V. (1984) Species differences in reproductive mechanisms. In: Reproduction in Mammals, 2nd Edn. Book 4. Eds: C.R. Austin & R.V. Short. Cambridge, UK: Cambridge University Press; pp. 24-61.
87. Short R.E., Bellows R.A., Staigmiller R.B., Berardinelli J.G. & Custer E.E. (1990) Physiological mechanisms controlling anestrus and infertility in postpartum beef cattle. J. Anim. Sci. 68, 799-816.
88. Silvester L.M. & Luck M.R. (1999) Distribution of extracellular matrix components in the developing ruminant corpus luteum: A wound repair hypothesis for luteinization. J. Reprod. Fertil. 116, 187-198.
89. Slack J.M.W., Darlington B.G., Heath J.K. & Godsave S.F. (1987) Mesoderm induction in early xenopus embryos by heparin-binding growth factors. Nature 326, 197-200.
90. Stirling D.T., Waterman M.F. & Simpson E.R. (1991) Expression of mRNA encoding basic fibroblast growth factor (bFGF) in bovine corpora lutea and cultured cells. J. Reprod. Fertil. 91, 1-8.
91. Taraska T., Reynolds L.P. & Redmer D.A. (1989) In vitro secretion of angiogenic activity by ovine follicles. In: Growth Factors and the Ovary, Ed A.N. Hirshfield. New York: Plenum Press; pp. 267-272.
92. Toutges M.J., Grazul-Bilska A.T., Kirsch J.D., Reynolds L.P. & Redmer D.A. (1999) Effects of luteinizing hormone (LH) and oxygen (02) leveis on vascular endothelial growth factor (VEGF) mRNA expression by ovine luteal cells in culture. Biol. Reprod. 60 (Suppl. 1), 280.
93. Trudinger B.J., Giles W.B. & Cook C.M. (1985) Uteroplacental blood flow velocity-time waveforms in normal and complicated pregnancy. Br. J. Obstet. Gynecol. 92, 39-45.
94. Wang H., Eriksson H. & Sahlin L. (2000) Estrogen receptors alpha and beta in the female reproductive tract of the rat during the estrous cycle. Biol. Reprod. 63, 1331-1340.
95. WinSPIRS (2001) SilverPlatter International N.V. (http://www.silverplatter.com/).
96. Wulff C., Wilson H., Rudge J.S., Wiegand S.J., Lunn S.F. & Fraser H.M. (2001) Luteal angiogenesis: Prevention and intervention by treatment with vascular endothelial growth factor trapA40. J. Clin. Endocrinol. Metab. 86, 3377-3386.
97. Yamagishi S.-I., Yonekura H., Yamamoto Y. et al. (1999) Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Laboratory Invest. 79, 501-509.
98. Zheng J., Bird I.M., Melsaether A.N. & Magness R.R. (1999) Activation of the mitogen-activated protein kinase cascade is necessary but not sufficient for basic fibroblast growth factor- and epidermal growth factor-stimulated expression of endothelial nitric oxide synthase in ovine fetoplacental artery endothelial cells. Endocrinology 140, 1399-1407.
99. Zimmermann R.C., Hartman T., Bohlen P., Sauer M.V. & Kitajewski J. (2001) Preovulatory treatment of mice with antiVEGF receptor 2 antibody inhibits angiogenesis in corpora lutea. Microvasc. Res. 62, 15-25.