Regulation of angiogenesis in the primate endometrium: vascular endothelial growth factor

Seminars in Reproductive Medicine

Volumn 27, Issue 1, 2009, Pages 80-89

  Chennazhi, Krishna P ^a   Nayak, Nihar R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Endometrium; Estrogen; Progesterone; Vascular endothelial growth factor (vegf)

Indexed keywords

ACIDIC FIBROBLAST GROWTH FACTOR; ADRENOMEDULLIN; ANGIOPOIETIN 1; ANGIOPOIETIN 2; BASIC FIBROBLAST GROWTH FACTOR; ENDOTHELIN; EPIDERMAL GROWTH FACTOR; ERYTHROPOIETIN; ESTRADIOL; ESTROGEN RECEPTOR; MIDKINE; PLATELET DERIVED GROWTH FACTOR; STROMAL CELL DERIVED FACTOR 1; THROMBOCYTE ACTIVATING FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; ENDOMETRIUM; ENDOTHELIUM CELL; GENETIC TRANSCRIPTION; HORMONAL REGULATION; HUMAN; MENSTRUAL CYCLE; NONHUMAN; PRIMATE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; VASCULARIZATION;

ANGIOGENIC PROTEINS; ANIMALS; ENDOMETRIUM; FEMALE; GONADAL STEROID HORMONES; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PRIMATES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 61449085710     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0028-1108012     Document Type: Review

References (92)

1. Hess AP, Nayak NR, Giudice LC. Oviduct and endometrium: cyclic changes in the primate oviduct and endometrium. In: Neill JD, ed. Knobil and Neill's Physiology of Reproduction. Vol. 1. New York, NY: Elsevier Science & Technology Books; 2005:337-381
2. Brenner RM, Rudolph L, Matrisian L, Slayden OD. Non-human primate models; artificial menstrual cycles, endometrial matrix metalloproteinases and s.c. endometrial grafts. Hum Reprod 1996;11(suppl 2):150-164
3. Markee JE. Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib Embryol 1940;28:219-308
4. Ramsey EM. Vascular anatomy. In: Wynn RM, ed. Biology of the Uterus. Volume 2. New York, NY: Plenum Press; 1982:59-76
5. Bartelmez GW. The phases of the menstrual cycle and their interpretation in terms of the pregnancy cycle. Am J Obstet Gynecol 1957;74(5):931-955
6. Rogers PA. Structure and function of endometrial blood vessels. Hum Reprod Update 1996;2(1):57-62
7. Bartelmez GW. The form and functions of the uterine blood vessels in the rhesus monkey. Contrib Embryol 1957;249: 155-181
8. Nayak NR, Brenner RM. Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium. J Clin Endocrinol Metab 2002;87(4):1845-1855
9. Ferenczy A, Bertrand G, Gelfand MM. Proliferation kinetics of human endometrium during the normal menstrual cycle. Am J Obstet Gynecol 1979;133(8):859-867
10. Rogers PA, Gargett CE. Endometrial angiogenesis. Angiogenesis 998;2(4):287-294
11. Goodger AM, Rogers PA. Endometrial endothelial cell proliferation during the menstrual cycle. Hum Reprod 1994; 9(3):399-405
12. Rogers PA, Abberton KM. Endometrial arteriogenesis: vascular smooth muscle cell proliferation and differentiation during the menstrual cycle and changes associated with endometrial bleeding disorders. Microsc Res Tech 2003; 60(4):412-419
13. Nayak NR, Kuo CJ, Desai TA, et al. Expression, localization and hormonal control of angiopoietin-1 in the rhesus macaque endometrium: potential role in spiral artery growth. Mol Hum Reprod 2005;11(11):791-799
14. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 1993;90(23):11162-11166
15. Brenner RM, Slayden OD. Steroid receptors in blood vessels of the rhesus macaque endometrium: a review. Arch Histol Cytol 2004;67(5):411-416
16. Iruela-Arispe ML, Rodriguez-Manzaneque JC, Abu-Jawdeh G. Endometrial endothelial cells express estrogen and progesterone receptors and exhibit a tissue specific response to angiogenic growth factors. Microcirculation 1999;6(2):127-140
17. Press MF, Udove JA, Greene GL. Progesterone receptor distribution in the human endometrium. Analysis using monoclonal antibodies to the human progesterone receptor. Am J Pathol 1988;131(1):112-124
18. Critchley HO, Brenner RM, Henderson TA, et al. Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium of the human and nonhuman primate endometrium. J Clin Endocrinol Metab 2001;86(3):1370-1378
19. Lecce G, Meduri G, Ancelin M, Bergeron C, Perrot-Applanat M. Presence of estrogen receptor beta in the human endometrium through the cycle: expression in glandular, stromal, and vascular cells. J Clin Endocrinol Metab 2001;86(3):1379-1386
20. Krikun G, Schatz F, Taylor R, et al. Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression. J Clin Endocrinol Metab 2005;90(3):1812-1818
21. Silvestri A, Fraser HM. Oestrogen and progesterone receptors in the marmoset endometrium: changes during the ovulatory cycle, early pregnancy and after inhibition of vascular endothelial growth factor, GnRH or ovariectomy. Reproduction 2007;134(2):341-353
22. Wehling M. Nongenomic aldosterone effects: the cell membrane as a specific target of mineralocorticoid action. Steroids 1995;60(1):153-156
23. Simoncini T, Genazzani AR, Liao JK. Nongenomic mechanisms of endothelial nitric oxide synthase activation by the selective estrogen receptor modulator raloxifene. Circulation 2002;105(11):1368-1373
24. Dvorak HF. Angiogenesis: update 2005. J Thromb Haemost 2005;3(8):1835-1842
25. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005;438(7070):932-936
26. Ferrara N. Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog Horm Res 2000; 55:15-35; discussion 35-36
27. Girling JE, Rogers PA. Recent advances in endometrial angiogenesis research. Angiogenesis 2005;8(2):89-99
28. Risau W. Mechanisms of angiogenesis. Nature 1997;386(6626):671-674
29. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85(3):221-228
30. Burri PH, Djonov V. Intussusceptive angiogenesis - the alternative to capillary sprouting. Mol Aspects Med 2002;23(6S):S1-S27
31. Hewett P, Nijjar S, Shams M, Morgan S, Gupta J, Ahmed A. Down-regulation of angiopoietin-1 expression in menor-rhagia. Am J Pathol 2002;160(3):773-780
32. Hirchenhain J, Huse I, Hess A, Bielfeld P, De Bruyne F, Krussel JS. Differential expression of angiopoietins 1 and 2 and their receptor Tie-2 in human endometrium. Mol Hum Reprod 2003;9(11):663-669
33. Krikun G, Critchley H, Schatz F, et al. Abnormal uterine bleeding during progestin-only contraception may result from free radical-induced alterations in angiopoietin expression. Am J Pathol 2002;161(3):979-986
34. Nelson KG, Takahashi T, Bossert NL, Walmer DK, McLachlan JA. Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation. Proc Natl Acad Sci U S A 1991;88(1):21-25
35. Ferriani RA, Charnock-Jones DS, Prentice A, Thomas EJ, Smith SK. Immunohistochemical localization of acidic and basic fibroblast growth factors in normal human endometrium and endometriosis and the detection of their mRNA by polymerase chain reaction. Hum Reprod 1993;8(1):11-16
36. Samathanam CA, Adesanya OO, Zhou J, Wang J, Bondy CA. Fibroblast growth factors 1 and 2 in the primate uterus. Biol Reprod 1998;59(3):491-496
37. Gold LI, Saxena B, Mittal KR, et al. Increased expression of transforming growth factor beta isoforms and basic fibroblast growth factor in complex hyperplasia and adenocarcinoma of the endometrium: evidence for paracrine and autocrine action. Cancer Res 1994;54(9):2347-2358
38. Horowitz GM, Scott RT Jr, Drews MR, Navot D, Hofmann GE. Immunohistochemical localization of transforming growth factor-alpha in human endometrium, decidua, and trophoblast. J Clin Endocrinol Metab 1993;76(3):786-792
39. Chegini N, Rossi MJ, Masterson BJ. Platelet-derived growth factor (PDGF), epidermal growth factor (EGF), and EGF and PDGF beta-receptors in human endometrial tissue: localization and in vitro action. Endocrinology 1992;130(4):2373-2385
40. Yasuda Y, Masuda S, Chikuma M, Inoue K, Nagao M, Sasaki R. Estrogen-dependent production of erythropoietin in uterus and its implication in uterine angiogenesis. J Biol Chem 1998;273(39):25381-25387
41. Zhao D, Li XP, Gao M, Zhao C, Wang JL, Wei LH. Stromal cell-derived factor 1alpha stimulates human endometrial carcinoma cell growth through the activation of both extracellular signal-regulated kinase 1/2 and Akt. Gynecol Oncol 2006;103(3):932-937
42. Ahmed A, Dearn S. The role of platelet-activating factor and its receptor in endometrial receptivity. Adv Exp Med Biol 1996;416:277-290
43. Tsutsui J, Uehara K, Kadomatsu K, Matsubara S, Muramatsu T. A new family of heparin-binding factors: strong conservation of midkine (MK) sequences between the human and the mouse. Biochem Biophys Res Commun 1991;176(2): 792-797
44. Zhao Y, Hague S, Manek S, Zhang L, Bicknell R, Rees MC. PCR display identifies tamoxifen induction of the novel angiogenic factor adrenomedullin by a non estrogenic mechanism in the human endometrium. Oncogene 1998; 16(3):409-415
45. Frater-Schroder M, Risau W, Hallmann R, Gautschi P, Bohlen P. Tumor necrosis factor type alpha, a potent inhibitor of endothelial cell growth in vitro, is angiogenic in vivo. Proc Natl Acad Sci U S A 1987;84(15):5277-5281
46. Marsh MM, Hampton AL, Riley SC, Findlay JK, Salamonsen LA. Production and characterization of endothelin released by human endometrial epithelial cells in culture. J Clin Endocrinol Metab 1994;79(6):1625-1631
47. Philippeaux MM, Piguet PF. Expression of tumor necrosis factor-alpha and its mRNA in the endometrial mucosa during the menstrual cycle. Am J Pathol 1993;143(2):480-486
48. Tabibzadeh S, Kong QF, Kapur S, Satyaswaroop PG, Aktories K. Tumour necrosis factor-alpha-mediated dysco-hesion of epithelial cells is associated with disordered expression of cadherin/beta-catenin and disassembly of actin filaments. Hum Reprod 1995;10(4):994-1004
49. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, et al. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 1993;48(5):1120-1128
50. Shifren JL, Tseng JF, Zaloudek CJ, et al. 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. J Clin Endocrinol Metab 1996;81(8):3112-3118
51. TorryDS,HoltVJ,KeenanJA,HarrisG,CaudleMR, Torry RJ. Vascular endothelial growth factor expression in cycling human endometrium. Fertil Steril 1996;66(1):72-80
52. Ancelin M, Buteau-Lozano H, Meduri G, et al. A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus. Proc Natl Acad Sci U S A 2002;99(9):6023-6028
53. Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G. Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J Biol Chem 2000;275(24):18040-18045
54. Soker S, Miao HQ, Nomi M, Takashima S, Klagsbrun M. VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J Cell Biochem 2002;85(2):357-368
55. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998;92(6):735-745
56. Germeyer A, Hamilton AE, Laughlin LS, et al. Cellular expression and hormonal regulation of neuropilin-1 and -2 messenger ribonucleic acid in the human and rhesus macaque endometrium. J Clin Endocrinol Metab 2005;90(3):1783-1790
57. Nayak NR, Critchley HO, Slayden OD, et al. Progesterone withdrawal up-regulates vascular endothelial growth factor receptor type 2 in the superficial zone stroma of the human and macaque endometrium: potential relevance to menstruation. J Clin Endocrinol Metab 2000;85(9):3442-3452
58. Greb RR, Heikinheimo O, Williams RF, Hodgen GD, Goodman AL. Vascular endothelial growth factor in primate endometrium is regulated by oestrogen-receptor and progesterone-receptor ligands in vivo. Hum Reprod 1997;12(6):1280-1292
59. Bausero P, Cavaille F, Meduri G, Freitas S, Perrot-Applanat M. Paracrine action of vascular endothelial growth factor in the human endometrium: production and target sites, and hormonal regulation. Angiogenesis 1998;2(2):167-182
60. Li XF, Gregory J, Ahmed A. Immunolocalisation of vascular endothelial growth factor in human endometrium. Growth Factors 1994;11(4):277-282
61. Punyadeera C, Thijssen VL, Tchaikovski S, et al. Expression and regulation of vascular endothelial growth factor ligands and receptors during menstruation and post-menstrual repair of human endometrium. Mol Hum Reprod 2006;12(6):367-375
62. Taylor RN, Lebovic DI, Hornung D, Mueller MD. Endocrine and paracrine regulation of endometrial angio-genesis. Ann N Y Acad Sci 2001;943:109-121
63. Huang JC, Liu DY, Dawood MY. The expression of vascular endothelial growth factor isoforms in cultured human endometrial stromal cells and its regulation by 17 beta-oestradiol. Mol Hum Reprod 1998;4(6):603-607
64. Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC, Taylor RN. Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci U S A 2000;97(20):10972- 10977
65. Niklaus AL, Babischkin JS, Aberdeen GW, Pepe GJ, Albrecht ED. Expression of vascular endothelial growth/permeability factor by endometrial glandular epithelial and stromal cells in baboons during the menstrual cycle and after ovariectomy. Endocrinology 2002;143(10):4007-4017
66. Albrecht ED, Aberdeen GW, Niklaus AL, Babischkin JS, Suresch DL, Pepe GJ. Acute temporal regulation of vascular endothelial growth/permeability factor expression and endothelial morphology in the baboon endometrium by ovarian steroids. J Clin Endocrinol Metab 2003;88(6):2844-2852
67. Charnock-Jones DS, Macpherson AM, Archer DF, et al. The effect of progestins on vascular endothelial growth factor, oestrogen receptor and progesterone receptor immu-noreactivity and endothelial cell density in human endometrium. Hum Reprod 2000;15(suppl 3):85-95
68. Meduri G, Bausero P, Perrot-Applanat M. Expression of vascular endothelial growth factor receptors in the human endometrium: modulation during the menstrual cycle. Biol Reprod 2000;62(2):439-447
69. Herve MA, Meduri G, Petit FG, et al. Regulation of the vascular endothelial growth factor (VEGF) receptor Flk-1/KDR by estradiol through VEGF in uterus. J Endocrinol 2006;188(1):91-99
70. Sharkey AM, Day K, McPherson A, et al. Vascular endothelial growth factor expression in human endometrium is regulated by hypoxia. J Clin Endocrinol Metab 2000;85(1):402-409
71. Semenza GL. HIF-1: using two hands to flip the angiogenic switch. Cancer Metastasis Rev 2000;19(1-2):59-65
72. Critchley HO, Osei J, Henderson TA, et al. Hypoxia-inducible factor-1alpha expression in human endometrium and its regulation by prostaglandin E-series prostanoid receptor 2 (EP2). Endocrinology 2006;147(2):744-753
73. Popovici RM, Irwin JC, Giaccia AJ, Giudice LC. Hypoxia and cAMP stimulate vascular endothelial growth factor (VEGF) in human endometrial stromal cells: potential relevance to menstruation and endometrial regeneration. J Clin Endocrinol Metab 1999;84(6):2245-2248
74. Tuder RM, Flook BE, Voelkel NF. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide. J Clin Invest 1995;95(4):1798-1807
75. Li J, Brown LF, Hibberd MG, Grossman JD, Morgan JP, Simons M. VEGF, flk-1, and flt-1 expression in a rat myocardial infarction model of angiogenesis. Am J Physiol 1996;270(5 Pt 2):H1803-H1811
76. Brogi E, Schatteman G, Wu T, et al. Hypoxia-induced paracrine regulation of vascular endothelial growth factor receptor expression. J Clin Invest 1996;97(2):469-476
77. Gerber HP, Condorelli F, Park J, Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem 1997;272(38):23659- 23667
78. Flamme I, Breier G, Risau W. Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 1995;169(2):699-712
79. Wang H, Keiser JA. Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ Res 1998;83(8):832-840
80. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999;341(10):738-746
81. Brown LF, Yeo KT, Berse B, et al. Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J Exp Med 1992;176(5):1375-1379
82. Peters KG, De Vries C, Williams LT. Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci U S A 1993;90(19): 8915-8919
83. Frank S, Hubner G, Breier G, Longaker MT, Greenhalgh DG, Werner S. Regulation of vascular endothelial growth factor expression in cultured keratinocytes. Implications for normal and impaired wound healing. J Biol Chem 1995;270(21):12607-12613
84. Lauer G, Sollberg S, Cole M, et al. Expression and proteolysis of vascular endothelial growth factor is increased in chronic wounds. J Invest Dermatol 2000;115(1):12-18
85. Howdieshell TR, Callaway D, Webb WL, et al. Antibody neutralization of vascular endothelial growth factor inhibits wound granulation tissue formation. J Surg Res 2001;96(2):173-182
86. Jacobi J, Tam BY, Sundram U, et al. Discordant effects of a soluble VEGF receptor on wound healing and angiogenesis. Gene Ther 2004;11(3):302-309
87. Brown LF, Detmar M, Claffey K, et al. Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. EXS 1997;79:233-269
88. Gargett CE, Rogers PA. Human endometrial angiogenesis. Reproduction 2001;121(2):181-186
89. Gargett CE, Lederman FL, Lau TM, Taylor NH, Rogers PA. Lack of correlation between vascular endothelial growth factor production and endothelial cell proliferation in the human endometrium. Hum Reprod 1999;14(8):2080-2088
90. Goodger AM, Rogers PA, Affandi B. Endometrial endo- thelial cell proliferation in long-term users of subdermal levonorgestrel. Hum Reprod 1994;9(9):1647-1651
91. Nayak NR, Brenner RM, Wiegand SJ, Giudice LC. Blockade of vascular development in the rhesus macaque endometrium by treatment with VEGF-trap: role of VEGF in postmenstrual endometrial angiogenesis. J Soc Gynecol Investig 2004;11(suppl):186A
92. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature 2005;438(7070):967-974