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Journal of Clinical Endocrinology & Metabolism, Vol 81, 3112-3118, Copyright © 1996 by Endocrine Society

ARTICLES

Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis

JL Shifren, JF Tseng, CJ Zaloudek, IP Ryan, YG Meng, N Ferrara, RB Jaffe and RN Taylor
Department of Obstetrics, Gynecology and Reproductive Sciences, University of California, San Francisco 94143, USA.

The human endometrium undergoes a complex process of vascular and glandular proliferation, differentiation, and regeneration with each menstrual cycle in preparation for implantation. Vascular endothelial growth factor (VEGF) is an endothelial cell-specific angiogenic protein that appears to play an important role in both physiological and pathological neovascularization. To investigate whether VEGF may regulate human endometrial angiogenesis, we examined VEGF messenger ribonucleic acid (mRNA) and protein throughout the menstrual cycle and studied the regulation of VEGF by reproductive steroids in isolated human endometrial cells. By ribonuclease protection analysis, VEGF mRNA increased relative to early proliferative phase expression by 1.6-,2.0- , and 3.6-fold in midproliferative, late proliferative, and secretory endometrium, respectively. In histological sections, VEGF mRNA and protein were localized focally in glandular epithelial cells and more diffusely in surrounding stroma, with greatest VEGF expression in secretory endometrium. Consistent with these in vivo results, the treatment of isolated human endometrial cells with estradiol (E2), medroxyprogesterone acetate (MPA), or E2 plus MPA significantly increased VEGF mRNA expression over the control value by 3.1-, 2.8-, and 4.7-fold, respectively. The VEGF response to E2 was rapid, with steady state levels of VEGF mRNA reaching 85% maximum 1 h after the addition of steroid. E2 also caused a 46% increase in secreted VEGF protein, and the combination of E2 and MPA caused an 18% increase. VEGF expression in endometriosis, an angiogenesis-dependent, estrogen- sensitive disease was similar to that seen in eutopic endometrium. Peritoneal fluid concentrations of VEGF were significantly higher in women with moderate to severe endometriosis than in women with minimal to mild endometriosis or no disease. VEGF, therefore, may be important in both physiological and pathological angiogenesis of human endometrium, as it is an estrogen-responsive angiogenic factor that varies throughout the menstrual cycle and is elevated in women with endometriosis.


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Effects of levonorgestrel-releasing intra-uterine system on the expression of vascular endothelial growth factor and adrenomedullin in the endometrium in adenomyosis
Hum. Reprod., April 1, 2003; 18(4): 694 - 699.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
T. A. Henderson, P. T. K. Saunders, A. Moffett-King, N. P. Groome, and H. O. D. Critchley
Steroid Receptor Expression in Uterine Natural Killer Cells
J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 440 - 449.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. M. Hastings, D. R. Licence, G. J. Burton, D. S. Charnock-Jones, and S. K. Smith
Soluble Vascular Endothelial Growth Factor Receptor 1 Inhibits Edema and Epithelial Proliferation Induced by 17{beta}-Estradiol in the Mouse Uterus
Endocrinology, January 1, 2003; 144(1): 326 - 334.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. Akoum, A. Lemay, and R. Maheux
Estradiol and Interleukin-1{beta} Exert a Synergistic Stimulatory Effect on the Expression of the Chemokine Regulated upon Activation, Normal T Cell Expressed, and Secreted in Endometriotic Cells
J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5785 - 5792.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
E. Kucera-Sliutz, I. Schiebel, F. Konig, S. Leodolter, G. Sliutz, and H. Koelbl
Vascular endothelial growth factor (VEGF) and discrimination between abnormal intrauterine and ectopic pregnancy
Hum. Reprod., December 1, 2002; 17(12): 3231 - 3234.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
H. O. D. Critchley, T. A. Henderson, R. W. Kelly, G. S. Scobie, L. R. Evans, N. P. Groome, and P. T. K. Saunders
Wild-Type Estrogen Receptor (ER{beta}1) and the Splice Variant (ER{beta}cx/{beta}2) Are Both Expressed within the Human Endometrium throughout the Normal Menstrual Cycle
J. Clin. Endocrinol. Metab., November 1, 2002; 87(11): 5265 - 5273.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. F. Bolontrade, R.-R. Zhou, and E. S. Kleinerman
Vasculogenesis Plays a Role in the Growth of Ewing's Sarcoma in Vivo
Clin. Cancer Res., November 1, 2002; 8(11): 3622 - 3627.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. L. Niklaus, J. S. Babischkin, G. W. Aberdeen, G. J. Pepe, and E. D. Albrecht
Expression of Vascular Endothelial Growth/Permeability Factor by Endometrial Glandular Epithelial and Stromal Cells in Baboons during the Menstrual Cycle and after Ovariectomy
Endocrinology, October 1, 2002; 143(10): 4007 - 4017.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
S. Sebastian, K. Takayama, M. Shozu, and S. E. Bulun
Cloning and Characterization of a Novel Endothelial Promoter of the Human CYP19 (Aromatase P450) Gene that Is Up-Regulated in Breast Cancer Tissue
Mol. Endocrinol., October 1, 2002; 16(10): 2243 - 2254.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
C. J. Lockwood, G. Krikun, A. B. C. Koo, S. Kadner, and F. Schatz
Differential Effects of Thrombin and Hypoxia on Endometrial Stromal and Glandular Epithelial Cell Vascular Endothelial Growth Factor Expression
J. Clin. Endocrinol. Metab., September 1, 2002; 87(9): 4280 - 4286.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Buteau-Lozano, M. Ancelin, B. Lardeux, J. Milanini, and M. Perrot-Applanat
Transcriptional Regulation of Vascular Endothelial Growth Factor by Estradiol and Tamoxifen in Breast Cancer Cells: A Complex Interplay between Estrogen Receptors {alpha} and {beta}
Cancer Res., September 1, 2002; 62(17): 4977 - 4984.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
C. Dabrosin, S. Gyorffy, P. Margetts, C. Ross, and J. Gauldie
Therapeutic Effect of Angiostatin Gene Transfer in a Murine Model of Endometriosis
Am. J. Pathol., September 1, 2002; 161(3): 909 - 918.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
R.M. Sibug, F.M. Helmerhorst, A.M.I. Tijssen, E.R. de Kloet, and J. de Koning
Gonadotrophin stimulation reduces VEGF120 expression in the mouse uterus during the peri-implantation period
Hum. Reprod., June 1, 2002; 17(6): 1643 - 1648.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Ancelin, H. Buteau-Lozano, G. Meduri, M. Osborne-Pellegrin, S. Sordello, J. Plouet, and M. Perrot-Applanat
A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus
PNAS, April 30, 2002; 99(9): 6023 - 6028.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
N. R. Nayak and R. M. Brenner
Vascular Proliferation and Vascular Endothelial Growth Factor Expression in the Rhesus Macaque Endometrium
J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1845 - 1855.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
J.-Y. Kwak, S.-W. Park, K.-H. Kim, Y.-J. Na, and K.-S. Lee
Modulation of neutrophil apoptosis by plasma and peritoneal fluid from patients with advanced endometriosis
Hum. Reprod., March 1, 2002; 17(3): 595 - 600.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. W. Jackson, J. S. Roberts, S. E. Heckford, C. Ricciardelli, J. Stahl, D. J. Horsfall, and W. D. Tilley
A Potential Autocrine Role for Vascular Endothelial Growth Factor in Prostate Cancer
Cancer Res., February 1, 2002; 62(3): 854 - 859.
[Abstract] [Full Text] [PDF]

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 Cold Spring Harb Symp Quant BiolHome page
J. LECOUTER, R. LIN, and N. FERRARA
The Role of EG-VEGF in the Regulation of Angiogenesis in Endocrine Glands
Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 217 - 222.
[Abstract] [PDF]

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 Mol Hum ReprodHome page
A. Akoum, C. Lawson, S. McColl, and M. Villeneuve
Ectopic endometrial cells express high concentrations of interleukin (IL)-8 in vivo regardless of the menstrual cycle phase and respond to oestradiol by up-regulating IL-1-induced IL-8 expression in vitro
Mol. Hum. Reprod., September 1, 2001; 7(9): 859 - 866.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
G. Bocci, A. Fasciani, R. Danesi, P. Viacava, A. R. Genazzani, and M. D. Tacca
In-vitro evidence of autocrine secretion of vascular endothelial growth factor by endothelial cells from human placental blood vessels
Mol. Hum. Reprod., August 1, 2001; 7(8): 771 - 777.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
J. W. M. Maas, P. G. Groothuis, G. A. J. Dunselman, A. F.P.M. de Goeij, H. A.J.S. Boudier, and J. L. H. Evers
Endometrial angiogenesis throughout the human menstrual cycle
Hum. Reprod., August 1, 2001; 16(8): 1557 - 1561.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
R. Grummer, F. Schwarzer, K. Bainczyk, H. Hess-Stumpp, P.-A. Regidor, A. E. Schindler, and E. Winterhager
Peritoneal endometriosis: validation of an in-vivo model
Hum. Reprod., August 1, 2001; 16(8): 1736 - 1743.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
D. Hornung, L. L. Waite, E. A. Ricke, F. Bentzien, D. Wallwiener, and R. N. Taylor
Nuclear Peroxisome Proliferator-Activated Receptors {{alpha}} and {{gamma}} Have Opposing Effects on Monocyte Chemotaxis in Endometriosis
J. Clin. Endocrinol. Metab., July 1, 2001; 86(7): 3108 - 3114.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
C. E. Gargett, F. Lederman, B. Heryanto, L. S. Gambino, and P. A.W. Rogers
Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neutrophils
Hum. Reprod., June 1, 2001; 16(6): 1065 - 1075.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
G. De Placido, C. Alviggi, C. Carravetta, M.L. Pisaturo, V. Sanna, M. Wilding, G.M. Lord, and G. Matarese
The peritoneal fluid concentration of leptin is increased in women with peritoneal but not ovarian endometriosis
Hum. Reprod., June 1, 2001; 16(6): 1251 - 1254.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
D. Hornung, K. Klingel, K. Dohrn, R. Kandolf, D. Wallwiener, and R. N. Taylor
Regulated on Activation, Normal T-Cell-Expressed and -Secreted mRNA Expression in Normal Endometrium and Endometriotic Implants : Assessment of Autocrine/Paracrine Regulation by in Situ Hybridization
Am. J. Pathol., June 1, 2001; 158(6): 1949 - 1954.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
Y.-L. Hu, M.-K. Tee, E. J. Goetzl, N. Auersperg, G. B. Mills, N. Ferrara, and R. B. Jaffe
Lysophosphatidic Acid Induction of Vascular Endothelial Growth Factor Expression in Human Ovarian Cancer Cells
J Natl Cancer Inst, May 16, 2001; 93(10): 762 - 767.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
R. C. Hovey, A. S. Goldhar, J. Baffi, and B. K. Vonderhaar
Transcriptional Regulation of Vascular Endothelial Growth Factor Expression in Epithelial and Stromal Cells during Mouse Mammary Gland Development
Mol. Endocrinol., May 1, 2001; 15(5): 819 - 831.
[Abstract] [Full Text]

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 Toxicol SciHome page
M. S. Cotroneo and C. A. Lamartiniere
Pharmacologic, but Not Dietary, Genistein Supports Endometriosis in a Rat Model
Toxicol. Sci., May 1, 2001; 61(1): 68 - 75.
[Abstract] [Full Text] [PDF]


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