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Published in: Reproductive Biology and Endocrinology 1/2003

Open Access 01-12-2003 | Review

Angiogenesis in the corpus luteum

Authors: Hamish M Fraser, Christine Wulff

Published in: Reproductive Biology and Endocrinology | Issue 1/2003

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Abstract

The corpus luteum (CL) is a site of intense angiogenesis. Within a short period, this is followed either by controlled regression of the microvascular tree in the non-fertile cycle, or maintenance and stabilisation of the new vasculature a conceptual cycle. The molecular regulation of these diverse aspects is examined. The CL provides a unique model system in which to study the cellular and molecular regulation of angiogenesis. Vascular endothelial growth factor (VEGF) has been found to have a major role in the CL. By targeting its action at specific stages of the luteal phase in vivo by antagonists, profound inhibitory effects on luteal angiogenesis and function are observed.
Literature
1.
go back to reference Gaytán F, Morales C, García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE: A quantitative study of changes in the human corpus luteum microvasulature during the menstrual cycle. Biol Reprod. 1999, 60: 914-919.CrossRefPubMed Gaytán F, Morales C, García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE: A quantitative study of changes in the human corpus luteum microvasulature during the menstrual cycle. Biol Reprod. 1999, 60: 914-919.CrossRefPubMed
2.
go back to reference Fraser HM, Lunn SF: Regulation and manipulation of angiogenesis in the primate corpus luteum. Reproduction. 2001, 121: 355-362. 10.1530/reprod/121.3.355.CrossRefPubMed Fraser HM, Lunn SF: Regulation and manipulation of angiogenesis in the primate corpus luteum. Reproduction. 2001, 121: 355-362. 10.1530/reprod/121.3.355.CrossRefPubMed
3.
go back to reference Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Nagura H: Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum Reprod. 1998, 13: 953-959. 10.1093/humrep/13.4.953.CrossRefPubMed Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Nagura H: Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum Reprod. 1998, 13: 953-959. 10.1093/humrep/13.4.953.CrossRefPubMed
4.
go back to reference Kamat BR, Brown LF, Manseau EJ, Senger DR, Dvorak HF: Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Am J Pathol. 1995, 146: 157-165.PubMedCentralPubMed Kamat BR, Brown LF, Manseau EJ, Senger DR, Dvorak HF: Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Am J Pathol. 1995, 146: 157-165.PubMedCentralPubMed
5.
go back to reference Meyer GT, McGeachie JK: Angiogenesis in the developing corpus luteum of pregnant rats: a stereologic and autoradiographic study. Anat Rec. 1988, 222: 18-25.CrossRefPubMed Meyer GT, McGeachie JK: Angiogenesis in the developing corpus luteum of pregnant rats: a stereologic and autoradiographic study. Anat Rec. 1988, 222: 18-25.CrossRefPubMed
6.
go back to reference Jablonka-Shariff A, AT Grazul-Bilska, Redmer DA, Reynolds LP: Growth and cellular proliferation of ovine corpora lutea throughout the estrous cycle. Endocrinology. 1993, 133: 1871-1879. 10.1210/en.133.4.1871.PubMed Jablonka-Shariff A, AT Grazul-Bilska, Redmer DA, Reynolds LP: Growth and cellular proliferation of ovine corpora lutea throughout the estrous cycle. Endocrinology. 1993, 133: 1871-1879. 10.1210/en.133.4.1871.PubMed
7.
go back to reference Zheng J, Fricke PM, Reynolds LP, Redmer DA: Evaluation of growth, cell proliferation, and cell death in bovine corpora lutea throughout the estrous cycle. Biol Reprod. 1994, 51: 623-632.CrossRefPubMed Zheng J, Fricke PM, Reynolds LP, Redmer DA: Evaluation of growth, cell proliferation, and cell death in bovine corpora lutea throughout the estrous cycle. Biol Reprod. 1994, 51: 623-632.CrossRefPubMed
8.
go back to reference Al-Zi'abi MO, Watson ED, Fraser HM: Angiogenesis and vascular endothelial growth factor expression in the equine corpus luteum. Reproduction. 2003, 125: 259-70. 10.1530/reprod/125.2.259.CrossRefPubMed Al-Zi'abi MO, Watson ED, Fraser HM: Angiogenesis and vascular endothelial growth factor expression in the equine corpus luteum. Reproduction. 2003, 125: 259-70. 10.1530/reprod/125.2.259.CrossRefPubMed
9.
go back to reference Dickson SE, Fraser HM: Inhibition of early luteal angiogenesis by gonadotropin-releasing hormone antagonist treatment in the primate. J Clin Endocrinol Metab. 2000, 85: 2339-2344. 10.1210/jc.85.6.2339.CrossRefPubMed Dickson SE, Fraser HM: Inhibition of early luteal angiogenesis by gonadotropin-releasing hormone antagonist treatment in the primate. J Clin Endocrinol Metab. 2000, 85: 2339-2344. 10.1210/jc.85.6.2339.CrossRefPubMed
10.
go back to reference Christenson LK, Stouffer RL: Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology. 1996, 137: 367-374. 10.1210/en.137.1.367.PubMed Christenson LK, Stouffer RL: Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology. 1996, 137: 367-374. 10.1210/en.137.1.367.PubMed
11.
go back to reference Rodger FE, Young FM, Fraser HM, Illingworth PJ: Endothelial cell proliferation follows the mid-cycle luteinizing hormone surge, but not human chorionic gonadotrophin rescue, in the human corpus luteum. Hum Reprod. 1997, 12: 1723-1729. 10.1093/humrep/12.8.1723.CrossRefPubMed Rodger FE, Young FM, Fraser HM, Illingworth PJ: Endothelial cell proliferation follows the mid-cycle luteinizing hormone surge, but not human chorionic gonadotrophin rescue, in the human corpus luteum. Hum Reprod. 1997, 12: 1723-1729. 10.1093/humrep/12.8.1723.CrossRefPubMed
12.
go back to reference Gaytán F, Morales C, García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE: Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod. 1998, 59: 417-425.CrossRefPubMed Gaytán F, Morales C, García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE: Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod. 1998, 59: 417-425.CrossRefPubMed
13.
go back to reference Goede V, Schmidt T, Kimmina S, Kozian D, Augustin HG: Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Lab Invest. 1998, 78: 1385-94.PubMed Goede V, Schmidt T, Kimmina S, Kozian D, Augustin HG: Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Lab Invest. 1998, 78: 1385-94.PubMed
14.
go back to reference Wulff C, Dickson SE, Duncan WC, Fraser HM: Angiogenesis in the human corpus luteum: simulated early pregnancy by HCG treatment is associated with both angiogenesis and vessel stabilization. Hum Reprod. 2001, 16: 2515-24. 10.1093/humrep/16.12.2515.CrossRefPubMed Wulff C, Dickson SE, Duncan WC, Fraser HM: Angiogenesis in the human corpus luteum: simulated early pregnancy by HCG treatment is associated with both angiogenesis and vessel stabilization. Hum Reprod. 2001, 16: 2515-24. 10.1093/humrep/16.12.2515.CrossRefPubMed
15.
go back to reference Redmer DA, Doraiswamy V, Bortnem BJ, Fisher K, Jablonka-Shariff A, Grazul-Bilska AT, Reynolds LP: Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol Reprod. 2001, 65: 879-89.CrossRefPubMed Redmer DA, Doraiswamy V, Bortnem BJ, Fisher K, Jablonka-Shariff A, Grazul-Bilska AT, Reynolds LP: Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol Reprod. 2001, 65: 879-89.CrossRefPubMed
16.
go back to reference Ferrara N, Davis-Smyth T: The biology of vascular endothelial growth factor. Endocr Rev. 1997, 18: 4-25. 10.1210/er.18.1.4.CrossRefPubMed Ferrara N, Davis-Smyth T: The biology of vascular endothelial growth factor. Endocr Rev. 1997, 18: 4-25. 10.1210/er.18.1.4.CrossRefPubMed
17.
go back to reference Laitinen M, Ristimäki A, Honkasalo M, Narko K, Paavonen K, Ritvos O: Differential hormonal regulation of vascular endothelial grwoth factors VEGF, VEGF-B, and VEGF-C messenger ribonucleic acid levels in cultured human granulosa-luteal cells. Endocrinology. 1997, 138: 4748-4756. 10.1210/en.138.11.4748.PubMed Laitinen M, Ristimäki A, Honkasalo M, Narko K, Paavonen K, Ritvos O: Differential hormonal regulation of vascular endothelial grwoth factors VEGF, VEGF-B, and VEGF-C messenger ribonucleic acid levels in cultured human granulosa-luteal cells. Endocrinology. 1997, 138: 4748-4756. 10.1210/en.138.11.4748.PubMed
18.
go back to reference Christenson LK, Stouffer RL: Follicle-stimulating hormone and luteinizing hormone/chorionic gonadotropin stimulation of vascular endothelial growth factor production by macaque granulosa cells from pre- and periovulatory follicles. J Clin Endocrinol Metab. 1997, 82: 2135-2142. 10.1210/jc.82.7.2135.PubMed Christenson LK, Stouffer RL: Follicle-stimulating hormone and luteinizing hormone/chorionic gonadotropin stimulation of vascular endothelial growth factor production by macaque granulosa cells from pre- and periovulatory follicles. J Clin Endocrinol Metab. 1997, 82: 2135-2142. 10.1210/jc.82.7.2135.PubMed
19.
go back to reference Neulen J, Raczek S, Pogorzelski M, Grunwald K, Yeo TK, Dvorak HF, Weich HA, Breckwoldt M: Secretion of vascular endothelial growth factor/vascular permeability factor from human luteinized granulosa cells is human chorionic gonadotrophin dependent. Molec Hum Reprod. 1998, 4: 203-206. 10.1093/molehr/4.3.203.CrossRefPubMed Neulen J, Raczek S, Pogorzelski M, Grunwald K, Yeo TK, Dvorak HF, Weich HA, Breckwoldt M: Secretion of vascular endothelial growth factor/vascular permeability factor from human luteinized granulosa cells is human chorionic gonadotrophin dependent. Molec Hum Reprod. 1998, 4: 203-206. 10.1093/molehr/4.3.203.CrossRefPubMed
20.
go back to reference Shweiki D, Itin A, Neufeld G, Gitay-Goren H, Keshet E: Patterns of vascular endotheilial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J Clin Invest. 1993, 91: 2235-2243.PubMedCentralCrossRefPubMed Shweiki D, Itin A, Neufeld G, Gitay-Goren H, Keshet E: Patterns of vascular endotheilial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J Clin Invest. 1993, 91: 2235-2243.PubMedCentralCrossRefPubMed
21.
go back to reference Sugino N, Kashida S, Takiguchi S, Kato H: Expression of vascular endothelail growth factor and its receptors in the human corpus luteum during the mestrual cycle and in early pregnancy. J Clin Endocrinol Metab. 2000, 85: 3919-3924. 10.1210/jc.85.10.3919.PubMed Sugino N, Kashida S, Takiguchi S, Kato H: Expression of vascular endothelail growth factor and its receptors in the human corpus luteum during the mestrual cycle and in early pregnancy. J Clin Endocrinol Metab. 2000, 85: 3919-3924. 10.1210/jc.85.10.3919.PubMed
22.
go back to reference Wulff C, Wilson H, Largue P, Duncan WC, Armstrong D, Fraser HM: Angiogenesis in the human corpus luteum: Localization and changes in angiopoietins, Tie-2 and vascular endothelial growth factor messenger ribonucleic acid. J Clin Endocrinol Metab. 2000, 85: 4302-4309. 10.1210/jc.85.11.4302.PubMed Wulff C, Wilson H, Largue P, Duncan WC, Armstrong D, Fraser HM: Angiogenesis in the human corpus luteum: Localization and changes in angiopoietins, Tie-2 and vascular endothelial growth factor messenger ribonucleic acid. J Clin Endocrinol Metab. 2000, 85: 4302-4309. 10.1210/jc.85.11.4302.PubMed
23.
go back to reference Hazzard TM, Christenson LK, Stouffer RL: Changes in expression of vascular endothelial growth factor and angiopoietin-1 and -2 in the macaque corpus luteum during the menstrual cycle. Molec Hum Reprod. 2000, 6: 993-8. 10.1093/molehr/6.11.993.CrossRefPubMed Hazzard TM, Christenson LK, Stouffer RL: Changes in expression of vascular endothelial growth factor and angiopoietin-1 and -2 in the macaque corpus luteum during the menstrual cycle. Molec Hum Reprod. 2000, 6: 993-8. 10.1093/molehr/6.11.993.CrossRefPubMed
24.
go back to reference Otani N, Sawako M, Yamoto M, Shikone T, Otani H, Nishiyama R, Otani T, Nakano R: The vascular endothelial growth factor/fms-like tyrosine kinase system in human ovary during the menstrual cycle and early pregnancy. J Clin Endocrinol Metab. 1999, 84: 3845-3851. 10.1210/jc.84.10.3845.CrossRefPubMed Otani N, Sawako M, Yamoto M, Shikone T, Otani H, Nishiyama R, Otani T, Nakano R: The vascular endothelial growth factor/fms-like tyrosine kinase system in human ovary during the menstrual cycle and early pregnancy. J Clin Endocrinol Metab. 1999, 84: 3845-3851. 10.1210/jc.84.10.3845.CrossRefPubMed
25.
go back to reference Endo T, Kitajima Y, Nishikawa A, Manase K, Shibuya M, Kudo R: Cyclic changes in expression of mRNA of vascular endothelial growth factor, its receptors Flt-1 and KDR/Flk-1, and Ets-1 in human corpora lutea. Fertil Steril. 2001, 76: 762-8. 10.1016/S0015-0282(01)02012-X.CrossRefPubMed Endo T, Kitajima Y, Nishikawa A, Manase K, Shibuya M, Kudo R: Cyclic changes in expression of mRNA of vascular endothelial growth factor, its receptors Flt-1 and KDR/Flk-1, and Ets-1 in human corpora lutea. Fertil Steril. 2001, 76: 762-8. 10.1016/S0015-0282(01)02012-X.CrossRefPubMed
26.
go back to reference Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McLain J, Aldrich TH, Papadopoulos N, et al: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997, 277: 55-60. 10.1126/science.277.5322.55.CrossRefPubMed Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McLain J, Aldrich TH, Papadopoulos N, et al: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997, 277: 55-60. 10.1126/science.277.5322.55.CrossRefPubMed
27.
go back to reference Augustin HG: Development of the vascular sytem of the corpus luteum. In: Morphogenesis of Endothelium. Edited by: Risau W. 2000, U.K: Harwood Academic Publishers, 237-254. Augustin HG: Development of the vascular sytem of the corpus luteum. In: Morphogenesis of Endothelium. Edited by: Risau W. 2000, U.K: Harwood Academic Publishers, 237-254.
28.
go back to reference Wandji SA, Gadsby JE, Barber JA, Hammond JM: Messenger ribonucleic acids for MAC25 and connevtive tissue growth factor (CTGF) are inversely regulated during folliculogenesis and early luteogenesis. Endocinology. 2000, 141: 2648-2657. 10.1210/en.141.7.2648. Wandji SA, Gadsby JE, Barber JA, Hammond JM: Messenger ribonucleic acids for MAC25 and connevtive tissue growth factor (CTGF) are inversely regulated during folliculogenesis and early luteogenesis. Endocinology. 2000, 141: 2648-2657. 10.1210/en.141.7.2648.
29.
go back to reference Fraser HM, Lunn SF, Kim H, Erickson GF: Insulin-like growth factor binding protein-3 (IGFBP-3) mRNA in the endothelial cells of the primate corpus luteum. Hum Reprod. 1998, 13: 2180-2185. 10.1093/humrep/13.8.2180.CrossRefPubMed Fraser HM, Lunn SF, Kim H, Erickson GF: Insulin-like growth factor binding protein-3 (IGFBP-3) mRNA in the endothelial cells of the primate corpus luteum. Hum Reprod. 1998, 13: 2180-2185. 10.1093/humrep/13.8.2180.CrossRefPubMed
30.
go back to reference LeCouter J, Kowalski J, Foster J, Hass P, Zhang Z, Dillard-Telm L, Frantz G, Rangell L, DeGuzman L, Keller GA, et al: Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature. 2001, 412: 877-884. 10.1038/35091000.CrossRefPubMed LeCouter J, Kowalski J, Foster J, Hass P, Zhang Z, Dillard-Telm L, Frantz G, Rangell L, DeGuzman L, Keller GA, et al: Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature. 2001, 412: 877-884. 10.1038/35091000.CrossRefPubMed
31.
go back to reference Li M, Bullock CM, Knauer DJ, Ehlert FJ, Zhou QY: Identification of two prokineticin cDNAs: recombinant proteins potently contract gastrointestinal smooth muscle. Mol Pharmacol. 2001, 59: 692-698.PubMed Li M, Bullock CM, Knauer DJ, Ehlert FJ, Zhou QY: Identification of two prokineticin cDNAs: recombinant proteins potently contract gastrointestinal smooth muscle. Mol Pharmacol. 2001, 59: 692-698.PubMed
32.
go back to reference LeCouter J, Lin R, Ferrara N: Endocrine gland-derived VEGF and the emerging hypothesis of organ-specific regulation of angiogenesis. Nat Med. 2002, 8: 913-917. 10.1038/nm0902-913.CrossRefPubMed LeCouter J, Lin R, Ferrara N: Endocrine gland-derived VEGF and the emerging hypothesis of organ-specific regulation of angiogenesis. Nat Med. 2002, 8: 913-917. 10.1038/nm0902-913.CrossRefPubMed
33.
go back to reference Lin DC, Bullock CM, Ehlert FJ, Chen J, Tian H, Zhou QY: Identification and molecular charecterisation of two closely related G protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J Biol Chem. 2001, 277: 19276-19280. 10.1074/jbc.M202139200.CrossRef Lin DC, Bullock CM, Ehlert FJ, Chen J, Tian H, Zhou QY: Identification and molecular charecterisation of two closely related G protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J Biol Chem. 2001, 277: 19276-19280. 10.1074/jbc.M202139200.CrossRef
34.
go back to reference Borman SM, Hennebold JD, Stouffer RL: Endocrine gland-vascular endothelial growth factor (EG-VEGF) expression in the nonhuman primate corpus luteum during the natural menstrual cycle. XIVth Serono Symposia International Ovarian Workshop 2002, Baltimore, MD. 2002 Borman SM, Hennebold JD, Stouffer RL: Endocrine gland-vascular endothelial growth factor (EG-VEGF) expression in the nonhuman primate corpus luteum during the natural menstrual cycle. XIVth Serono Symposia International Ovarian Workshop 2002, Baltimore, MD. 2002
35.
go back to reference Ferrara N, Frantz G, LeCouter J, Dillard-Telm L, Pham T, Draksharapu A, Giordano T, Peale F: Differential expression of the angiogenic factor genes vascular endothelial growth factor (VEGF) and endocrine-gland-derived VEGF in normal and polycystic human ovaries. Am J Pathol. 2003, 162: 1881-1893.PubMedCentralCrossRefPubMed Ferrara N, Frantz G, LeCouter J, Dillard-Telm L, Pham T, Draksharapu A, Giordano T, Peale F: Differential expression of the angiogenic factor genes vascular endothelial growth factor (VEGF) and endocrine-gland-derived VEGF in normal and polycystic human ovaries. Am J Pathol. 2003, 162: 1881-1893.PubMedCentralCrossRefPubMed
36.
go back to reference Gaytán F, Morales C, Bellido C, Aguilar E, Sánchez-Criado JE: Role of prolactin in the regulation of macrophages and in the proliferative activity of vascular cells in newly formed and regressing rat corpora lutea. Biol Reprod. 1997, 57: 478-486.CrossRefPubMed Gaytán F, Morales C, Bellido C, Aguilar E, Sánchez-Criado JE: Role of prolactin in the regulation of macrophages and in the proliferative activity of vascular cells in newly formed and regressing rat corpora lutea. Biol Reprod. 1997, 57: 478-486.CrossRefPubMed
37.
go back to reference Grosdemouge I, Bachelot A, Lucas A, Baran N, Kelly PA, Binart N: Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod Biol Endocrinol. 2003, 1: 12-10.1186/1477-7827-1-12.PubMedCentralCrossRefPubMed Grosdemouge I, Bachelot A, Lucas A, Baran N, Kelly PA, Binart N: Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod Biol Endocrinol. 2003, 1: 12-10.1186/1477-7827-1-12.PubMedCentralCrossRefPubMed
38.
go back to reference Rowe AJ, Morris KD, Bicknell R, Fraser HM: Angiogenesis in the corpus luteum of early pregnancy in the marmoset and the effects of vascular endothelial growth factor immunoneutrlaization on establishment of pregnancy. Biol Reprod. 2002, 67: 1180-1188.CrossRefPubMed Rowe AJ, Morris KD, Bicknell R, Fraser HM: Angiogenesis in the corpus luteum of early pregnancy in the marmoset and the effects of vascular endothelial growth factor immunoneutrlaization on establishment of pregnancy. Biol Reprod. 2002, 67: 1180-1188.CrossRefPubMed
39.
go back to reference Sawyer HR, Niswender KD, Braden TD, Niswender GD: Nuclear changes in ovine luteal cells in response to PGF2α. Dom An Endocrinol. 1990, 72: 229-238. 10.1016/0739-7240(90)90029-Y.CrossRef Sawyer HR, Niswender KD, Braden TD, Niswender GD: Nuclear changes in ovine luteal cells in response to PGF. Dom An Endocrinol. 1990, 72: 229-238. 10.1016/0739-7240(90)90029-Y.CrossRef
40.
go back to reference Azmi TI, O'Shea JD: Mechanism of deletion of endothelial cells during regression of the corpus luteum. Lab Invest. 1984, 51: 206-217.PubMed Azmi TI, O'Shea JD: Mechanism of deletion of endothelial cells during regression of the corpus luteum. Lab Invest. 1984, 51: 206-217.PubMed
41.
go back to reference McCormack JT, Friedrichs MG, Limback SD, Greenwald GS: Apoptosis during spontaneous luteolysis in the cyclic golden hamster: biochemical and morphological evidence. Biol Reprod. 1998, 58: 255-260.CrossRefPubMed McCormack JT, Friedrichs MG, Limback SD, Greenwald GS: Apoptosis during spontaneous luteolysis in the cyclic golden hamster: biochemical and morphological evidence. Biol Reprod. 1998, 58: 255-260.CrossRefPubMed
42.
go back to reference Morales C, Garcia-Pardo L, Reymundo C, Bellido C, Sanchez-Criado JE, Gaytan F: Different patterns of structural luteolysis in the human corpus luteum of menstruation. Hum Reprod. 2000, 15: 2119-2128. 10.1093/humrep/15.10.2119.CrossRefPubMed Morales C, Garcia-Pardo L, Reymundo C, Bellido C, Sanchez-Criado JE, Gaytan F: Different patterns of structural luteolysis in the human corpus luteum of menstruation. Hum Reprod. 2000, 15: 2119-2128. 10.1093/humrep/15.10.2119.CrossRefPubMed
43.
go back to reference Young FM, Illingworth PJ, Lunn SF, Harrison DJ, Fraser HM: Cell death during luteal regression in the marmoset monkey (Callithrix jacchus). J Reprod Fertil. 1997, 111: 109-119.CrossRefPubMed Young FM, Illingworth PJ, Lunn SF, Harrison DJ, Fraser HM: Cell death during luteal regression in the marmoset monkey (Callithrix jacchus). J Reprod Fertil. 1997, 111: 109-119.CrossRefPubMed
44.
go back to reference Funayama Y, Sasano H, Suzuki T, Tamura M, Fukaya T, Yajima A: Cell turnover in normal cycling human ovary. J Clin Endocrinol Metab. 1996, 81: 828-834. 10.1210/jc.81.2.828.PubMed Funayama Y, Sasano H, Suzuki T, Tamura M, Fukaya T, Yajima A: Cell turnover in normal cycling human ovary. J Clin Endocrinol Metab. 1996, 81: 828-834. 10.1210/jc.81.2.828.PubMed
45.
go back to reference Acosta TJ, Yoshizawa N, Ohtani M, Miyamoto A: Local changes in blood flow within the early and midcycle corpus luteum after prostraglandin F2a injection in cow. Biol Reprod. 2002, 66: 651-658.CrossRefPubMed Acosta TJ, Yoshizawa N, Ohtani M, Miyamoto A: Local changes in blood flow within the early and midcycle corpus luteum after prostraglandin F2a injection in cow. Biol Reprod. 2002, 66: 651-658.CrossRefPubMed
46.
go back to reference Young FM, Rodger FE, Illingworth PJ, Fraser HM: Cell proliferation and vascular morphology in the marmoset corpus luteum. Hum Reprod. 2000, 15: 557-566. 10.1093/humrep/15.3.557.CrossRefPubMed Young FM, Rodger FE, Illingworth PJ, Fraser HM: Cell proliferation and vascular morphology in the marmoset corpus luteum. Hum Reprod. 2000, 15: 557-566. 10.1093/humrep/15.3.557.CrossRefPubMed
47.
go back to reference Zimmermann RC, Xiao E, Husami N, Sauer MV, Lobo R, Kitajewski J, Ferin M: Short-term administration of antivascular endothelial growth factor antibody in the late follicular phase delays follicular development in the rhesus monkey. J Clin Endocrinol Metab. 2001, 86: 768-772. 10.1210/jc.86.2.768.PubMed Zimmermann RC, Xiao E, Husami N, Sauer MV, Lobo R, Kitajewski J, Ferin M: Short-term administration of antivascular endothelial growth factor antibody in the late follicular phase delays follicular development in the rhesus monkey. J Clin Endocrinol Metab. 2001, 86: 768-772. 10.1210/jc.86.2.768.PubMed
48.
go back to reference Zimmermann RC, Xiao E, Bohlen P, Ferin M: Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey. Endocinology. 2002, 143: 2496-2502. 10.1210/en.143.7.2496.CrossRef Zimmermann RC, Xiao E, Bohlen P, Ferin M: Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey. Endocinology. 2002, 143: 2496-2502. 10.1210/en.143.7.2496.CrossRef
49.
go back to reference Ferrara N, Chen H, Davis-Smyth T, Hans-Peter G, Nguyen T-N, Peers D, Chisholm V, Hillan K, Schwall R: Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med. 1998, 4: 336-340.CrossRefPubMed Ferrara N, Chen H, Davis-Smyth T, Hans-Peter G, Nguyen T-N, Peers D, Chisholm V, Hillan K, Schwall R: Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med. 1998, 4: 336-340.CrossRefPubMed
50.
go back to reference Wulff C, Wilson H, Rudge JS, Wiegand SJ, Lunn SF, Fraser HM: Luteal angiogenesis: prevention and intervention by treatment with vascular endothelial growth factor trap A40. J Clin Endocrinol Metab. 2001, 86: 3377-3386. 10.1210/jc.86.7.3377.PubMed Wulff C, Wilson H, Rudge JS, Wiegand SJ, Lunn SF, Fraser HM: Luteal angiogenesis: prevention and intervention by treatment with vascular endothelial growth factor trap A40. J Clin Endocrinol Metab. 2001, 86: 3377-3386. 10.1210/jc.86.7.3377.PubMed
51.
go back to reference Wulff C, Wilson H, Wiegand SJ, Rudge JS, Fraser HM: Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor trap R1R2. Endocrinology. 2002, 143: 2797-2807. 10.1210/en.143.7.2797.CrossRefPubMed Wulff C, Wilson H, Wiegand SJ, Rudge JS, Fraser HM: Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor trap R1R2. Endocrinology. 2002, 143: 2797-2807. 10.1210/en.143.7.2797.CrossRefPubMed
52.
go back to reference Hazzard TM, Xu F, Stouffer RL: Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal funaction in rhesus monkeys. Biol Reprod. 2002, 67: 1305-1312.CrossRefPubMed Hazzard TM, Xu F, Stouffer RL: Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal funaction in rhesus monkeys. Biol Reprod. 2002, 67: 1305-1312.CrossRefPubMed
53.
go back to reference Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD, Carroll V, Bicknell R: Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology. 2000, 141: 995-1000. 10.1210/en.141.3.995.PubMed Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD, Carroll V, Bicknell R: Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology. 2000, 141: 995-1000. 10.1210/en.141.3.995.PubMed
54.
go back to reference Dickson SE, Bicknell R, Fraser HM: Mid-luteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor. J Endocrionol. 2001, 168: 409-416.CrossRef Dickson SE, Bicknell R, Fraser HM: Mid-luteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor. J Endocrionol. 2001, 168: 409-416.CrossRef
55.
go back to reference Fraser HM, Wiegand SJ, Rudge JS: Treatment with Vascular Endothelial Growth Factor Trap R1R2 suppresses luteal function in the primate when administered at the 'post angiogenic' period. In: Gordon Conference on Angiogenesis & Microcirculation; Newport, RI. 2003 Fraser HM, Wiegand SJ, Rudge JS: Treatment with Vascular Endothelial Growth Factor Trap R1R2 suppresses luteal function in the primate when administered at the 'post angiogenic' period. In: Gordon Conference on Angiogenesis & Microcirculation; Newport, RI. 2003
Metadata
Title
Angiogenesis in the corpus luteum
Authors
Hamish M Fraser
Christine Wulff
Publication date
01-12-2003
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2003
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-1-88

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