Targeting angiogenesis in the pathological ovary

Reproduction, Fertility and Development

Volumn 25, Issue 2, 2013, Pages 362-371

  Duncan, W Colin ^a   Nio Kobayashi, Junko ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

corpus luteum; notch signalling; thrombospondin; VEGF.

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; CD36 ANTIGEN; CD47 ANTIGEN; CELL SURFACE RECEPTOR; CYCLOOXYGENASE 1 INHIBITOR; ENDOCRINE GLAND DERIVED VASCULAR ENDOTHELIAL GROWTH FACTOR; LUTEINIZING HORMONE RECEPTOR; MELOXICAM; N ACETYLSARCOSYLGLYCYLVALYL DEXTRO ALLOISOLEUCYLTHREONYLNORVALYLISOLEUCYLARGINYLPROLINE ETHYLAMIDE; PROSTAGLANDIN E2; SOMATOMEDIN C; THROMBOSPONDIN 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; BLOOD VESSEL PERMEABILITY; CELL FUNCTION; CELL SURVIVAL; CORPUS LUTEUM; ENDOTHELIUM CELL; FEMALE FERTILITY; HUMAN; NONHUMAN; ORAL CONTRACEPTION; OVARY; OVARY BLOOD FLOW; OVARY CANCER; OVARY CARCINOMA; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE CELL; OVARY HYPERSTIMULATION; OVARY POLYCYSTIC DISEASE; PREGNANCY RATE; REVIEW; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR MICROENVIRONMENT;

AMINOQUINOLINES; CHORIONIC GONADOTROPIN; CORPUS LUTEUM; DINOPROSTONE; DRUG DELIVERY SYSTEMS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUTEINIZING HORMONE; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; OVARIAN DISEASES; OVARIAN NEOPLASMS; POLYCYSTIC OVARY SYNDROME; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84873865936     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD12112     Document Type: Review

References (112)

1. Abd El Aal, D. E., Mohamed, S. A., Amine, A. F., and Meki, A. R. (2005). Vascular endothelial growth factor and insulin-like growth factor-1 in polycystic ovary syndrome and their relation to ovarian blood flow. Eur. J. Obstet. Gynecol. Reprod. Biol. 118, 219-224. doi:10.1016/J.EJOGRB.2004.07.024
2. Abramovich, D., Irusta, G., Parborell, F., and Tesone, M. (2010). Intrabursal injection of vascular endothelial growth factor trap in eCG-treated prepubertal rats inhibits proliferation and increases apoptosis of follicu-lar cells involving the PI3K/AKT signalling pathway. Fertil. Steril. 93, 1369-1377. doi:10.1016/J.FERTNSTERT.2009.01.127
3. Agrawal, R., Sladkevicius, P., Engmann, L., Conway, G. S., Payne, N. N., Bekis, J., Tan, S. L., Campbell, S., and Jacobs, H. S. (1998). Serum vascular endothelial growth factor concentrations and ovarian stromal blood flow are increased in women with polycystic ovaries. Hum. Reprod. 13, 651-655. doi:10.1093/HUMREP/13.3.651
4. Alvarez, A. A., Axelrod, J. R., Whitaker, R. S., Isner, P. D., Bentley, R. C., Dodge, R. K., and Rodriguez, G. C. (2001). Thrombospondin-1 expression in epithelial ovarian carcinoma: association with p53 status, tumour angiogenesis and survival in platinum-treated patients. Gynecol. Oncol. 82, 273-278. doi:10.1006/GYNO.2001.6287
5. Amin, A. F., Abd el-Aal, D. E., Darwish, A. M., and Meki, A. R. (2003). Evaluation of the impact of laparoscopic ovarian drilling on Doppler indices of ovarian stromal blood flow, serum vascular endothelial growth factor and insulin-like growth factor-1 in women with polycystic ovary syndrome. Fertil. Steril. 79, 938-941. doi:10.1016/S0015-0282 (02)04849-5
6. Araújo, V. R., Silva, G. M., Duarte, A. B., Magalhães, D. M., Almeida, A. P., Gonçalves, R. F., Bruno, J. B., Silva, T. F., Campello, C. C., Rodrigues, A. P., and Figueiredo, J. R.(2011). Vascular endothelial growth factor-A (165) (VEGF-A(165)) stimulates the in vitro development and oocyte competence of goat preantral follicles. Cell Tissue Res. 346, 273-281. doi:10.1007/S00441-011-1251-1
7. Armstrong, L. C., and Bornstein, P. (2003). Thrombospondins 1 and 2 function as inhibitors of angiogenesis. Matrix Biol. 22, 63-71. doi:10.1016/S0945-053X(03)00005-2
8. Badawy, A., and Elnashar, A.(2011). Treatment options for polycystic ovary syndrome. Int. J. Womens Health. 3, 25-35. doi:10.2147/IJWH.S11304
9. Balasubramanian, R., Plummer, L., Sidis, Y., Pitteloud, N., Martin, C., Zhou, Q. Y., and Crowley, W. F.Jr (2011). The puzzles of the prokine-ticin 2 pathway in human reproduction. Mol. Cell. Endocrinol. 346, 44-50. doi:10.1016/J.MCE.2011.05.040
10. Busso, C., Fernández-Sánchez, M., Garćia-Velasco, J. A., Landeras, J., Ballesteros, A., Muñoz, E., González, S., Simón, C., Arce, J. C., and Pellicer, A. (2010). The non-ergot-derived dopamine agonist quinago-lide in prevention of early ovarian hyperstimulation syndrome in IVF patients: a randomised, double-blind, placebo-controlled trial. Hum. Reprod. 25, 995-1004. doi:10.1093/HUMREP/DEQ005
11. Campbell, N. E., Greenaway, J., Henkin, J., Moorehead, R. A., and Petrik, J. (2010). The thrombospondin-1 mimetic ABT-510 increases the uptake and effectiveness of cisplatin and paclitaxel in a mouse model of epithelial ovarian cancer. Neoplasia 12, 275-283.
12. Chen, L., Zhang, J. J., Rafii, S., and Huang, X. Y. (2009). Suppression of tumour angiogenesis by Galpha(13) haploinsufficiency. J. Biol. Chem. 284, 27 409-27 415. doi:10.1074/JBC.M109.025460
13. Cristina, C., D́iaz-Torga, G., Baldi, A., Góngora, A., Rubinstein, M., Low, M. J., and Becú-Villalobos, D. (2005). Increased pituitary vascular endothelial growth factor-a in dopaminergic D2 receptor knockout female mice. Endocrinology 146, 2952-2962. doi:10.1210/EN. 2004-1445
14. Damous, L. L., Silva, S. M., Simões, R. S., Morello, R. J., Carbonel, A. P., Simões, M. J., and Montero, E. F. (2008). Remote ischemic preconditioning on neovascularization and follicle viability on ovary autotransplantation in rats. Transplant. Proc. 40, 861-864. doi:10.1016/J. TRANSPROCEED.2008.02.065
15. Delvigne, A., and Rozenberg, S. (2002). Epidemiology and prevention of ovarian hyperstimulation syndrome (OHSS): a review. Hum. Reprod. Update 8, 559-577. doi:10.1093/HUMUPD/8.6.559
16. Donnez, J., and Dolmans, M. M. (2010). Cryopreservation and transplantation of ovarian tissue. Clin. Obstet. Gynecol. 53, 787-796. doi:10.1097/GRF.0B013E3181F97A55
17. Duffy, D. M., and Stouffer, R. L. (2002). Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys. Hum. Reprod. 17, 2825-2831. doi:10.1093/HUMREP/17.11.2825
18. Duncan, W. C. (2000). The human corpus luteum: remodelling during luteolysis and maternal recognition of pregnancy. Rev. Reprod. 5, 12-17. doi:10.1530/ROR.0.0050012
19. Duncan, W. C., van den Driesche, S., and Fraser, H. M. (2008). Inhibition of vascular endothelial growth factor in the primate ovary up-regulates hypoxia-inducible factor-1alpha in the follicle and corpus luteum. Endocrinology 149, 3313-3320. doi:10.1210/EN.2007-1649
20. Duncan, W. C., Myers, M., Dickinson, R. E., van den Driesche, S., and Fraser, H. M. (2009). Luteal development and luteolysis in the primate corpus luteum. Anim. Reprod. 6, 34-46.
21. El Behery, M. M., Diab, A. E., Mowafy, H., Ebrahiem, M. A., and Shehata, A. E. (2011). Effect of laparoscopic ovarian drilling on vascular endothelial growth factor and ovarian stromal blood flow using 3-dimensional power Doppler. Int. J. Gynaecol. Obstet. 112, 119-121. doi:10.1016/J.IJGO.2010.08.018
22. Fauser, B. C., Tarlatzis, B. C., Rebar, R. W., Legro, R. S., Balen, A. H., Lobo, R., Carmina, E., Chang, J., Yildiz, B. O., Laven, J. S., Boivin, J., Petraglia, F., Wijeyeratne, C. N., Norman, R. J., Dunaif, A., Franks, S., Wild, R. A., Dumesic, D., and Barnhart, K. (2012). Consensus on women's health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group.Fertil. Steril. 97, 28-38. doi:10.1016/J. FERTNSTERT.2011.09.024
23. Fernandez, H., Morin-Surruca, M., Torre, A., Faivre, E., Deffieux, X., and Gervaise, A. (2011). Ovarian drilling for surgical treatmentof polycystic ovarian syndrome:acomprehensive review.Reprod. Biomed. Online22, 556-568. doi:10.1016/J.RBMO.2011.03.013
24. Ferrara, N., Frantz, G., LeCouter, J., Dillard-Telm, L., Pham, T., Draksharapu, A., Giordano, T., and Peale, F. (2003). 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. 162, 1881-1893. doi:10.1016/S0002-9440(10)64322-2
25. Franks, S. (2009). Do animal models of polycystic ovary syndrome help to understand its pathogenesis and management? Yes, but their limitations should be recognized. Endocrinology 150, 3983-3985. doi:10.1210/EN. 2009-0652
26. Fraser, H. M., and Duncan, W. C. (2005). Vascular morphogenesis in the primate ovary. Angiogenesis 8, 101-116. doi:10.1007/S10456-005-9004-Y
27. Fraser, H. M., and Duncan, W. C. (2009). SRB Reproduction, Fertility and Development Award Lecture 2008. Regulation and manipulation of angiogenesis in the ovary and endometrium. Reprod. Fertil. Dev. 21, 377-392. doi:10.1071/RD08272
28. Fraser, H. M., Bell, J., Wilson, H., Taylor, P. D., Morgan, K., Anderson, R. A., and Duncan, W. C. (2005). Localization and quantification of cyclic changes in the expression of endocrine gland vascular endothelial growth factor in the human corpus luteum. J. Clin. Endocrinol. Metab. 90, 427-434. doi:10.1210/JC.2004-0843
29. Fraser, H.M., Wilson, H., Wulff, C., Rudge, J. S., and Wiegand, S. J. (2006). Administration of vascular endothelial growth factor Trap during the 'post-angiogenic' period of the luteal phase causes rapid functional luteolysis and selective endothelial cell death in the marmoset. Reproduction 132, 589-600. doi:10.1530/REP.1.01064
30. Fraser, H. M., Morris, K. D., Wiegand, S. J., and Wilson, H. (2010). Inhibition of vascular endothelial growth factor during the postovulatory period prevents pregnancy in the marmoset.Contraception 82, 572-578. doi:10.1016/J.CONTRACEPTION.2010.04.020
31. Fraser, H. M., Hastings, J. M., Allan, D., Morris, K. D., Rudge, J. S., and Wiegand, S. J. (2012). Inhibition of delta-like ligand 4 induces luteal hypervascularisation followed by functional and structural luteolysis in the primate ovary. Endocrinology 153, 1972-1983. doi:10.1210/EN. 2011-1688
32. Friedman, O., Orvieto, R., Fisch, B., Felz, C., Freud, E., Ben-Haroush, A., and Abir, R. (2012). Possible improvements in human ovarian grafting by various host and graft treatments. Hum. Reprod. 27, 474-482. doi:10.1093/HUMREP/DER385
33. Fujii, E. Y., and Nakayama, M. (2010). The measurements of RAGE, VEGF and AGEs in the plasma and follicular fluid of reproductive women: the influenceof aging. Fertil. Steril. 94, 694-700. doi:10.1016/J.FERTN STERT.2009.03.029
34. Gaitskell, K., Martinek, I., Bryant, A., Kehoe, S., Nicum, S., and Morrison, J. (2011). Angiogenesis inhibitors for the treatment of ovarian cancer. Cochrane Database Syst. Rev. 7, CD007930.
35. Gao, M.Z., Zhao, X. M., Sun, Z. G., Hong, Y., Zhao, L. W., and Zhang, H.Q. (2011). Endocrine gland-derived vascular endothelial growth factor concentrations in follicular fluid and serum may predict ovarian hyperstimulation syndrome in women undergoing controlled ovarian hyperstimulation. Fertil. Steril. 95, 673-678. doi:10.1016/J.FERTN STERT.2010.09.044
36. Garside, S. A., Harlow, C. R., Hillier, S. G., Fraser, H. M., and Thomas, F.H. (2010a). Thrombospondin-1 inhibits angiogenesis and promotes follicular atresia in a novel in vitro angiogenesis assay. Endocrinology 151, 1280-1289. doi:10.1210/EN.2009-0686
37. Garside, S. A., Henkin, J., Morris, K. D., Norvell, S. M., Thomas, F. H., and Fraser, H. M. (2010b). A thrombospondin-mimetic peptide, ABT-898, suppresses angiogenesis and promotes follicular atresiain pre-and early-antral follicles in vivo. Endocrinology 151, 5905-5915. doi:10.1210/EN.2010-0283
38. Gaytan, F., Morales, C., Bellido, C., Aguilar, E., and Sanchez-Criado, J. E. (1997). 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. 57, 478-486. doi:10.1095/BIOLRE PROD57.2.478
39. Ginther, O. J., Gastal, E. L., Gastal, M. O., and Beg, M. A. (2005). In vivo effects of pregnancy-associated plasma protein-A, activin-A and vascular endothelial growth factor on other follicular-fluid factors during follicle deviation in mares. Reproduction 129, 489-496. doi:10.1530/REP.1.00555
40. Goldhar, A. S., Vonderhaar, B. K., Trott, J. F., and Hovey, R. C. (2005). Prolactin-induced expression of vascular endothelial growth factor via Egr-1. Mol. Cell. Endocrinol. 232, 9-19. doi:10.1016/J.MCE.2005. 01.005
41. Gómez, R., Simón, C., Remoh'i, J., and Pellicer, A. (2002). Vascular endothelial growth factor receptor-2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade. Endocrinology 143, 4339-4348. doi:10.1210/EN.2002-220204
42. Gómez, R., Gonzalez-Izquierdo, M., Zimmermann, R. C., Novella-Maestre, E., Alonso-Muriel, I., Sanchez-Criado, J., Remohi, J., Simon, C., and Pellicer, A. (2006). Low-dose dopamine agonist administration blocks vascular endothelial growth factor (VEGF)-mediated vascular hyper-permeability without altering VEGF receptor 2-dependent luteal angio-genesis in a rat ovarian hyperstimulation model. Endocrinology 147, 5400-5411. doi:10.1210/EN.2006-0657
43. Gómez, R., Ferrero, H., Delgado-Rosas, F., Gaytan, M., Morales, C., Zimmermann, R. C., Simón, C., Gaytan, F., and Pellicer, A. (2011). Evidences for the existence of a low dopaminergic tone in polycystic ovarian syndrome: implications for OHSS development and treatment. J. Clin. Endocrinol. Metab. 96, 2484-2492. doi:10.1210/JC.2011-0075
44. Goodheart, M.J., Ritchie, J.M., Rose, S. L., Fruehauf, J. P., DeYoung, B. R., and Buller, R. E. (2005). The relationship of molecular markers of p53 function and angiogenesis to prognosis of stage I epithelial ovarian cancer. Clin. Cancer Res. 11, 3733-3742. doi:10.1158/1078-0432.CCR-04-0056
45. Grosdemouge, I., Bachelot, A., Lucas, A., Baran, N., Kelly, P. A., and Binart, N. (2003). Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod. Biol. Endocrinol. 1, 12. doi:10.1186/1477-7827-1-12
46. Gutman, G., Barak, V., Maslovitz, S., Amit, A., Lessing, J. B., and Geva, E. (2008). Regulation of vascular endothelial growth factor-A and its soluble receptor sFlt-1 by luteinizing hormone in vivo: implication for ovarian follicle angiogenesis. Fertil. Steril. 89, 922-926. doi:10.1016/J.FERTNSTERT.2007.03.097
47. Hanahan, D. (1997). Signalling vascular morphogenesis and maintenance. Science 277, 48-50. doi:10.1126/SCIENCE.277.5322.48
48. Hazzard, T. M., Molskness, T. A., Chaffin, C. L., and Stouffer, R. L. (1999). Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the peri-ovulatory interval. Mol. Hum. Reprod. 5, 1115-1121. doi:10.1093/MOLEHR/5.12.1115
49. Hazzard, T. M., Christenson, L. K., and Stouffer, R. L. (2000). Changes in expression of vascular endothelial growth factor and angiopoietin-1 and-2 in the macaque corpus luteum during the menstrual cycle. Mol. Hum. Reprod. 6, 993-998. doi:10.1093/MOLEHR/6.11.993
50. Hazzard, T.M., Xu, F., and Stouffer, R.L.(2002). Injectionofsoluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function inrhesus monkeys. Biol. Reprod. 67, 1305-1312. doi:10.1095/BIOLREPROD67.4.1305
51. Hellström, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N., Yoon, K., Rossant, J., Iruela-Arispe, M. L., Kalen, M., Gerhardt, H., and Betsholtz, C. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780. doi:10.1038/NATURE05571
52. Henkin, J., and Volpert, O. V. (2011). Therapies using anti-angiogenic peptide mimetics of thrombospondin-1. Expert Opin. Ther. Targets 15, 1369-1386. doi:10.1517/14728222.2011.640319
53. Hu, W., Lu, C., Dong, H. H., Huang, J., Shen, D. Y., Stone, R. L., Nick, A. M., Shahzad, M. M., Mora, E., Jennings, N. B., Lee, S. J., Roh, J. W., Matsuo, K., Nishimura, M., Goodman, B. W., Jaffe, R. B., Langley, R. R., Deavers, M. T., Lopez-Berestein, G., Coleman, R. L., and Sood, A. K. (2011). Biological roles of the Delta family Notch ligand Dll4 in tumour and endothelial cells in ovarian cancer. Cancer Res. 71, 6030-6039. doi:10.1158/0008-5472.CAN- 10-2719
54. Huang, Y., Hua, K., Zhou, X., Jin, H., Chen, X., Lu, X., Yu, Y., Zha, X., and Feng, Y. (2008). Activation of the PI3K/AKT pathway mediates FSH-stimulated VEGF expression in ovarian serous cystadenocarcinoma. Cell Res. 18, 780-791. doi:10.1038/CR.2008.70
55. Lawler, J. (2002). Thrombospondin-1 as an endogenous inhibitor of angio-genesis and tumour growth. J. Cell. Mol. Med. 6, 1-12. doi:10.1111/J.1582-4934.2002.TB00307.X
56. Levit, A., Yarnitzky, T., Wiener, A., Meidan, R., and Niv, M. Y. (2011). Modelling of human prokineticin receptors: interactions with novel small-molecule binders and potential off-target drugs. PLoS ONE 6, e27990. doi:10.1371/JOURNAL.PONE.0027990
57. Li, W., Ji, Z. L., Zhuo, G. C., Xu, R. J., Wang, J., and Jiang, H. R. (2010). Effects of a selective cyclooxygenase-1 inhibitor in SKOV-3 ovarian carcinoma xenograft-bearing mice. Med. Oncol. 27, 98-104. doi:10.1007/S12032- 009-9179-Y
58. Li, W., Wang, J., Jiang, H. R., Xu, X.L., Zhang, J., Liu, M. L., and Zhai, L.Y. (2011). Combined effects of cyclooxygenase-1 and cyclooxygenase-2 selective inhibitors on ovarian carcinoma in vivo. Int. J. Mol. Sci. 12, 668-681. doi:10.3390/IJMS12010668
59. Lobov, I. B., Renard, R. A., Papadopoulos, N., Gale, N. W., Thurston, G., Yancopoulos, G. D., and Wiegand, S. J. (2007). Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc. Natl. Acad. Sci. USA 104, 3219-3224. doi:10.1073/PNAS.0611206104
60. Malaguarnera, L., Imbesi, R. M., Scuto, A., D'Amico, F., Licata, F., Messina, A., and Sanfilippo, S. (2004). Prolactin increases HO-1 expression and induces VEGF production in human macrophages. J. Cell. Biochem. 93, 197-206. doi:10.1002/JCB.20167
61. Maldonado-Pérez, D., Evans, J., Denison, F., Millar, R. P., and Jabbour, H. N. (2007). Potential roles of the prokineticins in reproduction. Trends Endocrinol. Metab. 18, 66-72. doi:10.1016/J.TEM.2006.12.002
62. Martelli, A., Bernabò, N., Berardinelli, P., Russo, V., Rinaldi, C., Di Giacinto, O., Mauro, A., and Barboni, B. (2009). Vascular supply as a discriminating factor for pig preantral follicle selection. Reproduction 137, 45-58. doi:10.1530/REP-08-0117
63. Mathur, R., Kailasam, C., and Jenkins, J. (2007). Review of the evidence base of strategies to prevent ovarian hyperstimulation syndrome. Hum. Fertil. 10, 75-85. doi:10.1080/14647270601111239
64. McFee, R. M., Rozell, T. G., and Cupp, A. S. (2012). The balance of pro-angiogenic and anti-angiogenic VEGFA isoforms regulate follicle development. Cell Tissue Res. [Epub ahead of print]. doi:10.1007/S00441-012-1330-Y
65. Monnier, J., and Samson, M. (2010). Prokineticins in angiogenesis and cancer. Cancer Lett. 296, 144-149. doi:10.1016/J.CANLET.2010. 06.011
66. Monteleone, P., Giovanni Artini, P., Simi, G., Casarosa, E., Cela, V., and Genazzani, A. R. (2008). Follicular fluid VEGF levels directly correlate with perifollicular blood flow in normoresponder patients undergoing IVF. J. Assist. Reprod. Genet. 25, 183-186. doi:10.1007/S10815-008-9218-1
67. Oberaigner, W., Minicozzi, P., Bielska-Lasota, M., Allemani, C., de Angelis, R., Mangone, L., and Sant, M. (2012). Survival for ovarian cancer in europe: the across-country variation did not shrink in the past decade. Acta Oncol. [Epub ahead of print]. doi:10.3109/0284186X. 2011.653437
68. Obermajer, N., Muthuswamy, R., Odunsi, K., Edwards, R. P., and Kalinski, P. (2011). PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res. 71, 7463-7470. doi:10.1158/0008-5472.CAN-11-2449
69. Palomba, S., Falbo, A., Zullo, F., and Orio, F., Jr (2009). Evidence-based and potential benefits of metformin in the polycystic ovary syndrome: a comprehensive review. Endocr. Rev. 30, 1-50. doi:10.1210/ER.2008- 0030
70. Palomba, S., Falbo, A., Carrillo, L., Villani, M. T., Orio, F., Russo, T., Di Cello, A., Cappiello, F., Capasso, S., Tolino, A., Colao, A., Mastrantonio, P., La Sala, G. B., Zullo, F., and Cittadini, E.; METformin in High Responder Italian Group (2011). Metformin reduces risk of ovarian hyperstimulation syndrome in patients with polycystic ovary syndrome during gonadotrophin-stimulated in vitro fertilisation cycles: a randomised, controlled trial. Fertil. Steril. 96, 1384-1390. doi:10.1016/J.FERTNSTERT.2011.09.020
71. Peitsidis, P., and Agrawal, R. (2010). Role of vascular endothelial growth factor in women with PCO and PCOS: a systematic review. Reprod. Biomed. Online 20, 444-452. doi:10.1016/J.RBMO.2010.01.007
72. Pezzuto, A., Ferrari, B., Coppola, F., and Nardelli, G. B. (2010). LH supplementation in down-regulated women undergoing assisted reproduction with baseline low serum LH levels. Gynecol. Endocrinol. 26, 118-124. doi:10.3109/09513590903215516
73. Pietrowski, D., Szabo, L., Sator, M., Just, A., and Egarter, C. (2012). Ovarian hyperstimulation syndrome is correlated with a reduction of soluble VEGF receptor protein level and a higher amount of VEGF-A. Hum. Reprod. 27, 196-199. doi:10.1093/HUMREP/DER349
74. Qiu, Y., Seager, M., Osman, A., Castle-Miller, J.S., Bevan, H.S., Tortonese, D. J., Murphy, D., Harper, S. J., Fraser, H. M., Donaldson, L. F., and Bates, D. O. (2012). Ovarian VEGF165b expression regulates follicular development, corpus luteum function and fertility. Reproduction [Epub ahead of print]. doi:10.1530/REP-11-0091
75. Quintana, R., Kopcow, L., Marconi, G., Young, E., Yovanovich, C., and Paz, D. A. (2008). Inhibition of cyclooxygenase-2 (COX-2) by meloxicam decreases the incidence of ovarian hyperstimulation syndrome in a rat model. Fertil. Steril. 90, 1511-1516. doi:10.1016/J.FERTNSTERT. 2007.09.028
76. Rizk, B. (2009). Symposium: update on prediction and management of OHSS. Genetics of ovarian hyperstimulation syndrome. Reprod. Biomed. Online 19, 14-27. doi:10.1016/S1472-6483(10)60041-7
77. Rodewald, M., Herr, D., Fraser, H.M., Hack, G., Kreienberg, R., and Wulff, C. (2007). Regulation of tight-junction proteins occludin and claudin 5 in the primate ovary during the ovulatory cycle and after inhibition of vascular endothelial growth factor. Mol. Hum. Reprod. 13, 781-789. doi:10.1093/MOLEHR/ GAM066
78. Rodewald, M., Herr, D., Duncan, W. C., Fraser, H. M., Hack, G., Konrad, R., Gagsteiger, F., Kreienberg, R., and Wulff, C. (2009). Molecular mechanisms of ovarian hyperstimulation syndrome: paracrine reduction of endothelial claudin 5 by hCG in vitro is associated with increased endothelial permeability. Hum. Reprod. 24, 1191-1199. doi:10.1093/HUMREP/DEN479
79. Rogosin, S., and Sandler, A. B. (2012). Beyond Bevacizumab: anti-angiogenic agents. Clin. Lung Cancer [Epub ahead of print]. doi:10.1016/J.CLLC.2011.12.001
80. Rubatt, J. M., Darcy, K. M., Hutson, A., Bean, S. M., Havrilesky, L. J., Grace, L. A., Berchuck, A., and Secord, A. A. (2009). Independent prognostic relevance of microvessel density in advanced epithelial ovarian cancer and associations between CD31, CD105, p53 status and angiogenic marker expression: a Gynecologic Oncology Group study. Gynecol. Oncol. 112, 469-474. doi:10.1016/J.YGYNO.2008. 11.030
81. Sakurai, T., Suzuki, K., Yoshie, M., Hashimoto, K., Tachikawa, E., and Tamura, K. (2011). Stimulation of tube formation mediated through the prostaglandin EP2 receptor in rat luteal endothelial cells. J. Endocrinol. 209, 33-43. doi:10.1530/JOE-10-0357
82. Sboros, V., Averkiou, M., Lampaskis, M., Thomas, D. H., Silva, N., Strouthos, C., Docherty, J., and McNeilly, A. S. (2011). Imaging of the ovine corpus luteum microcirculation with contrast ultrasound. Ultrasound Med. Biol. 37, 59-68. doi:10.1016/J.ULTRASMEDBIO. 2010.10.013
83. Seekallu, S. V., Toosi, B. M., and Rawlings, N. C. (2009). LH pulse frequency and the emergence and growth of ovarian antral follicular waves in the ewe during the luteal phase of the oestrous cycle. Reprod. Biol. Endocrinol. 7, 78. doi:10.1186/1477-7827-7-78
84. Shah, D. K., Menon, K. M., Cabrera, L. M., Vahratian, A., Kavoussi, S. K., and Lebovic, D. I. (2010). Thiazolidinediones decrease vascular endo-thelial growth factor (VEGF) production by human luteinised granulosa cells in vitro. Fertil. Steril. 93, 2042-2047. doi:10.1016/J.FERTN STERT.2009.02.059
85. Shikanov, A., Zhang, Z., Xu, M., Smith, R. M., Rajan, A., Woodruff, T. K., and Shea, L. D. (2011). Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng. Part A 17, 3095-3104. doi:10.1089/TEN.TEA.2011.0204
86. Skaznik-Wikiel, M. E., Sharma, R. K., Selesniemi, K., Lee, H. J., Tilly, J. L., and Falcone, T. (2011). Granulocyte colony-stimulating factor in conjunction with vascular endothelial growth factor maintains primordial follicle numbers in transplanted mouse ovaries. Fertil. Steril. 95, 1405-1409. doi:10.1016/J.FERTNSTERT.2010.12.036
87. Stanek, M. B., Borman, S. M., Molskness, T. A., Larson, J. M., Stouffer, R. L., and Patton, P. E. (2007). Insulin and insulin-like growth factor stimulation of vascular endothelial growth factor production by lutei-nised granulosa cells: comparison between polycystic ovarian syndrome (PCOS) and non-PCOS women. J. Clin. Endocrinol. Metab. 92, 2726-2733. doi:10.1210/JC.2006- 2846
88. Stocco, C., Telleria, C., and Gibori, G. (2007). The molecular control of corpus luteum formation, function and regression. Endocr. Rev. 28, 117-149. doi:10.1210/ER.2006-0022
89. Suchting, S., Freitas, C., le Noble, F., Benedito, R., Breant, C., Duarte, A., and Eichmann, A. (2007). The Notch ligand-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. USA 104, 3225-3230. doi:10.1073/PNAS.0611177104
90. Sugino, N., Suzuki, T., Sakata, A., Miwa, I., Asada, H., Taketani, T., Yamagata, Y., and Tamura, H. (2005). Angiogenesis in the human corpus luteum: changes in expression of angiopoietins in the corpus luteum throughout the menstrual cycle and in early pregnancy. J. Clin. Endocrinol. Metab. 90, 6141-6148. doi:10.1210/JC.2005-0643
91. Swanton, A., Lighten, A., Granne, I., McVeigh, E., Lavery, S., Trew, G., Talmor, A., Raine-Fenning, N., Jayaprakasan, K., and Child, T. (2011). Do women with ovaries of polycystic morphology without any other features of PCOS benefit from short-term metformin co-treatment during IVF? A double-blind, placebo-controlled, randomised trial. Hum. Reprod. 26, 2178-2184. doi:10.1093/HUMREP/DER120
92. Tamasi, G., Casolaro, M., Magnani, A., Sega, A., Chiasserini, L., Messori, L., Gabbiani, C., Valiahdi, S. M., Jakupec, M. A., Keppler, B. K., Hursthouse, M. B., and Cini, R. (2010). New platinum-oxicam complexes as anti-cancer drugs. Synthesis, characterization, release studies from smart hydrogels, evaluation of reactivity with selected proteins and cytotoxic activity in vitro. J. Inorg. Biochem. 104, 799-814. doi:10.1016/J.JINORGBIO. 2010.03.010
93. Tatone, C., Amicarelli, F., Carbone, M. C., Monteleone, P., Caserta, D., Marci, R., Artini, P. G., Piomboni, P., and Focarelli, R. (2008). Cellular and molecular aspects of ovarian follicle ageing. Hum. Reprod. Update 14, 131-142. doi:10.1093/HUMUPD/DMM048
94. Teoh, D., and Secord, A. A. (2012). Anti-angiogenic agents in combination with chemotherapy for the treatment of epithelial ovarian cancer. Int. J. Gynecol. Cancer 22, 348-359. doi:10.1097/IGC.0B013E31823C6EFD
95. Thierry van Dessel, H. J., Lee, P. D., Faessen, G., Fauser, B. C., and Giudice, L. C. (1999). Elevated serum levels of free insulin-like growth factor I in polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 84, 3030-3035. doi:10.1210/JC.84.9.3030
96. Thomas, C. M., Boss, E. A., Boonstra, H., van Tienoven, D., Sweep, C. G., and Massuger, L. F. (2008). Gonadotrophins and female sex steroid hormones in cyst fluid and serum from patients with ovarian tumours. Eur. J. Gynaecol. Oncol. 29, 468-472.
97. Tso, L.O., Costello, M. F., Albuquerque, L.E., Andriolo, R.B., and Freitas, V. (2009). Metformin treatment before and during IVF or ICSI in women with polycystic ovary syndrome. Cochrane Database Syst. Rev. 15, CD006105.
98. Uddin, S., Ahmed, M., Hussain, A., Assad, L., Al-Dayel, F., Bavi, P., Al-Kuraya, K. S., and Munkarah, A. (2010). Cyclooxygenase-2 inhibition inhibits PI3K/AKT kinase activity in epithelial ovarian cancer. Int. J. Cancer 126, 382-394. doi:10.1002/IJC.24757
99. van de Lagemaat, R., Raafs, B. C., van Koppen, C., Timmers, C. M., Mulders, S. M., and Hanssen, R. G. (2011). Prevention of the onset of ovarian hyperstimulation syndrome (OHSS) in the rat after ovulation induction with a low molecular weight agonist of the LH receptor compared with hCG and rec-LH. Endocrinology 152, 4350-4357. doi:10.1210/EN.2011-1077
100. van den Driesche, S., Myers, M., Gay, E., Thong, K. J., and Duncan, W. C. (2008). Human chorionic gonadotrophin up-regulates hypoxia inducible factor-1 alphainluteinised granulosa cells: implications for the hormonal regulation of vascular endothelial growth factor A in the human corpus luteum. Mol. Hum. Reprod. 14, 455-464. doi:10.1093/MOLEHR/GAN040
101. Vardhana, P. A., Julius, M. A., Pollak, S. V., Lustbader, E. G., Trousdale, R. K., and Lustbader, J. W. (2009). A unique human chorionic gonado-trophin antagonist suppresses ovarian hyperstimulation syndrome in rats. Endocrinology 150, 3807-3814. doi:10.1210/EN.2009-0107
102. Várnagy, A., Bódis, J., Mánfai, Z., Wilhelm, F., Busznyák, C., and Koppán, M. (2010). Low-dose aspirin therapy to prevent ovarian hyperstimulation syndrome. Fertil. Steril. 93, 2281-2284. doi:10.1016/J.FERTNSTERT. 2009.01.085
103. Vikhanskaya, F., Bani, M. R., Borsotti, P., Ghilardi, C., Ceruti, R., Ghisleni, G., Marabese, M., Giavazzi, R., Broggini, M., and Taraboletti, G. (2001). p73 overexpression increases VEGF and reduces thrombospondin-1 production: implications for tumour angiogenesis. Oncogene 20, 7293-7300. doi:10.1038/SJ.ONC.1204896
104. Vlahos, N. P., Bugg, E. M., Shamblott, M. J., Phelps, J. Y., Gearhart, J. D., and Zacur, H. A. (2001). Prolactin receptor gene expression and immunolocalisation of the prolactin receptor in human luteinised granulosa cells. Mol. Hum. Reprod. 7, 1033-1038. doi:10.1093/MOLEHR/7.11.1033
105. Wulff, C., Wilson, H., Largue, P., Duncan, W. C., Armstrong, D. G., and Fraser, H. M. (2000). Angiogenesis in the human corpus luteum: localisation and changes in angiopoietins, tie-2 and vascular endothelial growth factor messenger ribonucleic acid. J. Clin. Endocrinol. Metab. 85, 4302-4309. doi:10.1210/JC.85.11.4302
106. Wulff, C., Wilson, H., Wiegand, S. J., Rudge, J. S., and Fraser, H. M. (2002). Prevention of thecal angiogenesis, antral follicular growth and ovulation in the primate by treatment with vascular endothelial growth factor Trap R1R2. Endocrinology 143, 2797-2807. doi:10.1210/EN. 143.7.2797
107. Xin, B., Yokoyama, Y., Shigeto, T., Futagami, M., and Mizunuma, H. (2007b). Inhibitory effect of meloxicam, a selective cyclooxygenase-2 inhibitor, and ciglitazone, a peroxisome proliferator-activated receptor gamma ligand, on the growth of human ovarian cancers. Cancer 110, 791-800. doi:10.1002/CNCR.22854
108. Xin, B., Yokoyama, Y., Shigeto, T., and Mizunuma, H. (2007a). Anti-tumour effect of non-steroidal anti-inflammatory drugs on human ovarian cancers. Pathol. Oncol. Res. 13, 365-369. doi:10.1007/BF02940318
109. Xu, F., and Stouffer, R. L. (2005). Local delivery of angiopoietin-2 into the preovulatory follicle terminates the menstrual cycle in rhesus monkeys. Biol. Reprod. 72, 1352-1358. doi:10.1095/BIOLREPROD.104.037143
110. Yan, M., and Plowman, G. D. (2007). Delta-like 4/Notch signalling and its therapeutic implications.Clin. Cancer Res.13, 7243-7246. doi:10.1158/1078-0432. CCR-07-1393
111. Youssef, M. A., van Wely, M., Hassan, M. A., Al-Inany, H. G., Mochtar, M., Khattab, S., and van der Veen, F. (2010). Can dopamine agonists reduce the incidence and severity of OHSS in IVF/ICSI treatment cycles? A systematic review and meta-analysis. Hum. Reprod. Update 16, 459-466. doi:10.1093/HUMUPD/DMQ006
112. Zhang, L., Yang, N., Conejo-Garcia, J.R., Katsaros, D., Mohamed-Hadley, A., Fracchioli, S., Schlienger, K., Toll, A., Levine, B., Rubin, S. C., and Coukos, G. (2003). Expression of endocrine gland-derived vascular endothelial growth factor in ovarian carcinoma. Clin. Cancer Res. 9, 264-272.