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The role of hypoxia-induced genes in ovarian angiogenesis

Rina Meidan A B , Eyal Klipper A , Yulia Zalman A and Ronit Yalu A
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, The Hebrew University of Jerusalem, The Robert H. Smith Faculty of Agriculture, Food and Environment, Rehovot 76100, Israel.

B Corresponding author. Email: rina.meidan@huji.ac.il

Reproduction, Fertility and Development 25(2) 343-350 https://doi.org/10.1071/RD12139
Submitted: 30 April 2012  Accepted: 26 July 2012   Published: 4 September 2012

Abstract

The hypoxic microenvironment that occurs in fast-growing tissue such as the corpus luteum (CL) is a major contributor to its ability to survive via the induction of an intricate vascular network. Cellular responses to hypoxia are mediated by hypoxia-inducible factor-1 (HIF-1), an oxygen-regulated transcriptional activator. HIF-1, a heterodimer consisting of a constitutively-expressed β subunit and an oxygen-regulated α subunit, binds to the hypoxia responsive element (HRE) present in the promoter regions of responsive genes. This review summarises evidence for the involvement of hypoxia and HIF-1α in CL development and function. Special emphasis is given to hypoxia-induced, luteal cell-specific expression of multiple genes (vascular endothelial growth factor A (VEGFA), fibroblast growth factor 2 (FGF-2), prokineticin receptor 2 (PK-R2), stanniocalcin 1 (STC-1) and endothelin 2 (EDN-2) that participate in the angiogenic process during CL formation.

Additional keywords: basic fibroblast growth factor, corpus luteum, follicle, luteal endothelial cells, lutel steroidogenic cells, vascular endothelial growth factor.


References

Adams, J. M., Difazio, L. T., Rolandelli, R. H., Lujan, J. J., Hasko, G., Csoka, B., Selmeczy, Z., and Nemeth, Z. H. (2009). HIF-1: a key mediator in hypoxia. Acta Physiol. Hung. 96, 19–28.
HIF-1: a key mediator in hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvFOmu74%3D&md5=59314770b9b9973ccd63e8845038c7a2CAS | 19264039PubMed |

Ahluwalia, A., and Tarnawski, A. S. (2004). Critical role of hypoxia sensor HIF-1alpha in VEGF gene activation. Implications for angiogenesis and tissue injury healing. Curr. Med. Chem. 19, 90–97.

Alam, H., Maizels, E. T., Park, Y., Ghaey, S., Feiger, Z. J., Chandel, N. S., and Hunzicker-Dunn, M. (2004). Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT/Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation. J. Biol. Chem. 279, 19 431–19 440.
Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT/Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1WjtLs%3D&md5=ad9e24833d15f92c4ed24b77e9fd8954CAS |

Alam, H., Weck, J., Maizels, E., Park, Y., Lee, E. J., Ashcroft, M., and Hunzicker-Dunn, M. (2009). Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 150, 915–928.
Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sgtr8%3D&md5=bcf19bea2c958474862aba3265e9ef66CAS | 18845636PubMed |

Basini, G., Baioni, L., Bussolati, S., Grolli, S., Kramer, L. H., Wagner, G. F., and Grasselli, F. (2010). Expression and localization of stanniocalcin 1 in swine ovary. Gen. Comp. Endocrinol. 166, 404–408.
Expression and localization of stanniocalcin 1 in swine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtVCgur8%3D&md5=23d581b5d76cd8541754321b6340706fCAS | 20035757PubMed |

Ben-Yosef, Y., Lahat, N., Shapiro, S., Bitterman, H., and Miller, A. (2002). Regulation of endothelial matrix metalloproteinase-2 by hypoxia/reoxygenation. Circ. Res. 90, 784–791.
Regulation of endothelial matrix metalloproteinase-2 by hypoxia/reoxygenation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Krurc%3D&md5=4147e0fa470a86c908774dc1d8f51bd7CAS | 11964371PubMed |

Berisha, B., and Schams, D. (2005). Ovarian function in ruminants. Domest. Anim. Endocrinol. 29, 305–317.
Ovarian function in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFKns74%3D&md5=6a80980a7a27b07411a736a1ed962316CAS | 15998502PubMed |

Berisha, B., Schams, D., Kosmann, M., Amselgruber, W., and Einspanier, R. (2000a). Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles. J. Endocrinol. 167, 371–382.
Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVCqtg%3D%3D&md5=0f8806384fabf30cace81e1b086963edCAS | 11115764PubMed |

Berisha, B., Schams, D., Kosmann, M., Amselgruber, W., and Einspanier, R. (2000b). Expression and tissue concentration of vascular endothelial growth factor, its receptors and localization in the bovine corpus luteum during oestrous cycle and pregnancy. Biol. Reprod. 63, 1106–1114.
Expression and tissue concentration of vascular endothelial growth factor, its receptors and localization in the bovine corpus luteum during oestrous cycle and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslyltbk%3D&md5=8c7402aeb730b087d47c87154ab0a51aCAS | 10993833PubMed |

Boonyaprakob, U., Gadsby, J. E., Hedgpeth, V., Routh, P. A., and Almond, G. W. (2005). Expression and localization of hypoxia inducible factor-1 alpha mRNA in the porcine ovary. Can. J. Vet. Res. 69, 215–222.
| 1:CAS:528:DC%2BD2MXpvVWhtro%3D&md5=c753fa0b1b9a94027649717060b66cbfCAS | 16187552PubMed |

Brahimi-Horn, M. C., and Pouyssegur, J. (2009). HIF at a glance. J. Cell Sci. 122, 1055–1057.
HIF at a glance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFSrt7w%3D&md5=3f2964adf40a01710e671b236854194bCAS | 19339544PubMed |

Brouillet, S., Hoffmann, P., Chauvet, S., Salomon, A., Chamboredon, S., Sergent, F., Benharouga, M., Feige, J. J., and Alfaidy, N. (2012). Revisiting the role of hCG: new regulation of the angiogenic factor EG-VEGF and its receptors. Cell. Mol. Life Sci. 69, 1537–1550.
Revisiting the role of hCG: new regulation of the angiogenic factor EG-VEGF and its receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFSntbg%3D&md5=f5a65e840247cf42a6691910c0bf6fceCAS | 22138749PubMed |

Calvani, M., Rapisarda, A., Uranchimeg, B., Shoemaker, R. H., and Melillo, G. (2006). Hypoxic induction of an HIF-1alpha-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells. Blood 107, 2705–2712.
Hypoxic induction of an HIF-1alpha-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtlKlurg%3D&md5=b86ebbebdc527fe9a3a7a53c22e48b4aCAS | 16304044PubMed |

Chen, T. H., Wang, J. F., Chan, P., and Lee, H. M. (2005). Angiotensin II stimulates hypoxia-inducible factor 1 alpha accumulation in glomerular mesangial cells. Ann. N. Y. Acad. Sci. 1042, 286–293.
Angiotensin II stimulates hypoxia-inducible factor 1 alpha accumulation in glomerular mesangial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXot1Cqt78%3D&md5=277b16465dd9dbcf242674c0974e384cCAS | 15965074PubMed |

Clerici, C., and Planes, C. (2009). Gene regulation in the adaptive process to hypoxia in lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L267–L274.
Gene regulation in the adaptive process to hypoxia in lung epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtFGru7w%3D&md5=a19d31f2310c67147f99187784ebb45bCAS | 19118091PubMed |

Crews, S. T. (1998). Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 12, 607–620.
Control of cell lineage-specific development and transcription by bHLH-PAS proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVegu78%3D&md5=8e64deaecbf1a9fd54d33ceabcf865fbCAS | 9499397PubMed |

Duncan, W. C., van den Driesche, S., and Fraser, H. M. (2008). Inhibition of vascular endothelial growth factor in the primate ovary upregulates hypoxia-inducible factor-1 alpha in the follicle and corpus luteum. Endocrinology 149, 3313–3320.
Inhibition of vascular endothelial growth factor in the primate ovary upregulates hypoxia-inducible factor-1 alpha in the follicle and corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1amurY%3D&md5=318d49684e873121f73fabcdc2a38eb7CAS | 18388198PubMed |

Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O’Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. I., Dhanda, A., Tian, Y. M., Masson, N., Hamilton, D. L., Jaakkola, P., Barstead, R., Hodgkin, J., Maxwell, P. H., Pugh, C. W., Schofield, C. J., and Ratcliffe, P. J. (2001). C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43–54.
C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsFOntL0%3D&md5=e6733cf479e1b5cd80cd1b93ef60d57eCAS | 11595184PubMed |

Ferrara, N., and Davis-Smyth, T. (1997). The biology of vascular endothelial growth factor. Endocr. Rev. 18, 4–25.
The biology of vascular endothelial growth factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFCiu7s%3D&md5=02480064e29b82c9deaa51be12bfe149CAS | 9034784PubMed |

Ferrara, N., LeCouter, J., Lin, R., and Peale, F. (2004). EG-VEGF and Bv8: a novel family of tissue-restricted angiogenic factors. Biochim. Biophys. Acta 1654, 69–78.
| 1:CAS:528:DC%2BD2cXhsVKhsbo%3D&md5=40c9d187f56bdf532e2439f507df1b8cCAS | 14984768PubMed |

Fraser, H. M. (2006). Regulation of the ovarian follicular vasculature. Reprod. Biol. Endocrinol. 4, 18.
Regulation of the ovarian follicular vasculature.Crossref | GoogleScholarGoogle Scholar | 16611363PubMed |

Fraser, H. M., and Lunn, S. F. (2001). Regulation and manipulation of angiogenesis in the primate corpus luteum. Reproduction 121, 355–362.
Regulation and manipulation of angiogenesis in the primate corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFSqurk%3D&md5=6304635b4a7fe16b780a953f1e94d7ebCAS | 11226061PubMed |

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.
Inhibition of vascular endothelial growth factor during the postovulatory period prevents pregnancy in the marmoset.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVWqt7bK&md5=1e93b9f66f88c74a6e9ebbaeb9eeff96CAS | 21074022PubMed |

Gabler, C., Plath-Gabler, A., Killian, G. J., Berisha, B., and Schams, D. (2004). Expression pattern of fibroblast growth factor (FGF) and vascular endothelial growth factor (VEGF) system members in bovine corpus luteum endothelial cells during treatment with FGF-2, VEGF or oestradiol. Reprod. Domest. Anim. 39, 321–327.
Expression pattern of fibroblast growth factor (FGF) and vascular endothelial growth factor (VEGF) system members in bovine corpus luteum endothelial cells during treatment with FGF-2, VEGF or oestradiol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvF2qu78%3D&md5=fa7627b0e8fd093206372144785f2fd9CAS | 15367264PubMed |

Gerber, H. P., Condorelli, F., Park, J., and Ferrara, N. (1997). Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is upregulated by hypoxia. J. Biol. Chem. 272, 23 659–23 667.
Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is upregulated by hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtlOiu7Y%3D&md5=e4600e03a0168fe406b3488eb431a71dCAS |

Giordano, F. J., and Johnson, R. S. (2001). Angiogenesis: the role of the microenvironment in flipping the switch. Curr. Opin. Genet. Dev. 11, 35–40.
Angiogenesis: the role of the microenvironment in flipping the switch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFSnt7k%3D&md5=210eeaf9dbbbe87076bfafcc141b6ea8CAS | 11163148PubMed |

Gospodarowicz, D., Cheng, J., Lui, G. M., Baird, A., Esch, F., and Bohlen, P. (1985). Corpus luteum angiogenic factor is related to fibroblast growth factor. Endocrinology 117, 2383–2391.
Corpus luteum angiogenic factor is related to fibroblast growth factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhsFalsg%3D%3D&md5=1b22b4ac8c6e396ae35f0f0c67efd05aCAS | 4065037PubMed |

Groulx, I., and Lee, S. (2002). Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel–Lindau tumour suppressor protein. Mol. Cell. Biol. 22, 5319–5336.
Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel–Lindau tumour suppressor protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlGnsbs%3D&md5=87de9fb248ec60c9fcad6bab279c6e4fCAS | 12101228PubMed |

Guilini, C., Urayama, K., Turkeri, G., Dedeoglu, D. B., Kurose, H., Messaddeq, N., and Nebigil, C. G. (2010). Divergent roles of prokineticin receptors in the endothelial cells: angiogenesis and fenestration. Am. J. Physiol. Heart Circ. Physiol. 298, H844–H852.
Divergent roles of prokineticin receptors in the endothelial cells: angiogenesis and fenestration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFGgu7g%3D&md5=ed1e2f1dc1798a27a0fee61aa6394047CAS | 20023120PubMed |

Han, Z. B., Ren, H., Zhao, H., Chi, Y., Chen, K., Zhou, B., Liu, Y. J., Zhang, L., Xu, B., Liu, B., Yang, R., and Han, Z. C. (2008). Hypoxia-inducible factor (HIF)-1 alpha directly enhances the transcriptional activity of stem cell factor (SCF) in response to hypoxia and epidermal growth factor (EGF). Carcinogenesis 29, 1853–1861.
Hypoxia-inducible factor (HIF)-1 alpha directly enhances the transcriptional activity of stem cell factor (SCF) in response to hypoxia and epidermal growth factor (EGF).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1SitL3E&md5=51d5b94d4f9980ec6f776eba6e59e9ceCAS | 18339685PubMed |

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.
Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the peri-ovulatory interval.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVelsQ%3D%3D&md5=8cf4de376a7bacbd507568129b39e747CAS | 10587365PubMed |

He, L. F., Wang, T. T., Gao, Q. Y., Zhao, G. F., Huang, Y. H., Yu, L. K., and Hou, Y. Y. (2011). Stanniocalcin-1 promotes tumour angiogenesis through upregulation of VEGF in gastric cancer cells. J. Biomed. Sci. 18, 39.
Stanniocalcin-1 promotes tumour angiogenesis through upregulation of VEGF in gastric cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFehsbo%3D&md5=748207d8cfa90fc08baa1dbf9e27a648CAS | 21672207PubMed |

Hewitson, K. S., Schofield, C. J., and Ratcliffe, P. J. (2007). Hypoxia-inducible factor prolyl-hydroxylase: purification and assays of PHD2. Methods Enzymol. 435, 25–42.
Hypoxia-inducible factor prolyl-hydroxylase: purification and assays of PHD2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOjtrY%3D&md5=07494d39b23ad2f1c8299dbfa652542fCAS | 17998047PubMed |

Huang, L. E., Arany, Z., Livingston, D. M., and Bunn, H. F. (1996). Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J. Biol. Chem. 271, 32 253–32 259.
Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXit1ehsA%3D%3D&md5=1410f65a7aa3e0d62fb373bd3457268bCAS |

Jiang, B. H., Rue, E., Wang, G. L., Roe, R., and Semenza, G. L. (1996). Dimerization, DNA binding and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271, 17 771–17 778.
Dimerization, DNA binding and transactivation properties of hypoxia-inducible factor 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFyit70%3D&md5=eb0f8743711a58bc7badc45d8b53e8c0CAS |

Jiang, Y. F., Tsui, K. H., Wang, P. H., Lin, C. W., Wang, J. Y., Hsu, M. C., Chen, Y. C., and Chiu, C. H. (2011). Hypoxia regulates cell proliferation and steroidogenesis through protein kinase A signalling in bovine corpus luteum. Anim. Reprod. Sci. 129, 152–161.
Hypoxia regulates cell proliferation and steroidogenesis through protein kinase A signalling in bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1OmsLs%3D&md5=a6fa37871090a086adb0c7ff2bfb5816CAS | 22226573PubMed |

Kaczmarek, M. M., Schams, D., and Ziecik, A. J. (2005). Role of vascular endothelial growth factor in ovarian physiology – an overview. Reprod. Biol. 5, 111–136.
| 16100562PubMed |

Kallio, P. J., Pongratz, I., Gradin, K., McGuire, J., and Poellinger, L. (1997). Activation of hypoxia-inducible factor 1 alpha: post-transcriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc. Natl. Acad. Sci. USA 94, 5667–5672.
Activation of hypoxia-inducible factor 1 alpha: post-transcriptional regulation and conformational change by recruitment of the Arnt transcription factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFKku7g%3D&md5=31ac134e220ebd512d08158e5cb975c5CAS | 9159130PubMed |

Kallio, P. J., Wilson, W. J., O’Brien, S., Makino, Y., and Poellinger, L. (1999). Regulation of the hypoxia-inducible transcription factor 1 alpha by the ubiquitin-proteasome pathway. J. Biol. Chem. 274, 6519–6525.
Regulation of the hypoxia-inducible transcription factor 1 alpha by the ubiquitin-proteasome pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1Cjsr8%3D&md5=80beb06efbc7441e967ecc522116e73bCAS | 10037745PubMed |

Kietzmann, T., Roth, U., and Jungermann, K. (1999). Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia-inducible factor-1 in rat hepatocytes. Blood 94, 4177–4185.
| 1:CAS:528:DyaK1MXnvFOjsbc%3D&md5=9c159952c4277621cfe1cf68024f44b8CAS | 10590062PubMed |

Kim, M. R., Choi, H. S., Heo, T. H., Hwang, S. W., and Kang, K. W. (2008). Induction of vascular endothelial growth factor by peptidyl-prolyl isomerase Pin1 in breast cancer cells. Biochem. Biophys. Res. Commun. 369, 547–553.
Induction of vascular endothelial growth factor by peptidyl-prolyl isomerase Pin1 in breast cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs12gurw%3D&md5=f785f7950a94d60d4a5b05af8d5fc33dCAS | 18294451PubMed |

Kim, J., Bagchi, I. C., and Bagchi, M. K. (2009). Signalling by hypoxia-inducible factors is critical for ovulation in mice. Endocrinology 150, 3392–3400.
Signalling by hypoxia-inducible factors is critical for ovulation in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlCrtr4%3D&md5=2e4731e72b75047dbd5e1a4d66d7d287CAS | 19325003PubMed |

Kisliouk, T., Levy, N., Hurwitz, A., and Meidan, R. (2003). Presence and regulation of endocrine gland vascular endothelial growth factor/prokineticin-1 and its receptors in ovarian cells. J. Clin. Endocrinol. Metab. 88, 3700–3707.
Presence and regulation of endocrine gland vascular endothelial growth factor/prokineticin-1 and its receptors in ovarian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsFOkt7g%3D&md5=89691f217e3e4936ba8f417e6555a116CAS | 12915658PubMed |

Kisliouk, T., Podlovni, H., and Meidan, R. (2005). Unique expression and regulatory mechanisms of EG-VEGF/prokineticin-1 and its receptors in the corpus luteum. Ann. Anat. 187, 529–537.
Unique expression and regulatory mechanisms of EG-VEGF/prokineticin-1 and its receptors in the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xks1Gkuw%3D%3D&md5=29f3a979f37454d9f1ecb64aca19b7b2CAS | 16320832PubMed |

Klipper, E., Levit, A., Mastich, Y., Berisha, B., Schams, D., and Meidan, R. (2010). Induction of endothelin-2 expression by luteinizing hormone and hypoxia: possible role in bovine corpus luteum formation. Endocrinology 151, 1914–1922.
Induction of endothelin-2 expression by luteinizing hormone and hypoxia: possible role in bovine corpus luteum formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Cmurc%3D&md5=465d5a9cf34dceb4f122c244b5e62b7cCAS | 20176726PubMed |

Ko, C., Gieske, M. C., Al-Alem, L., Hahn, Y., Su, W., Gong, M. C., Iglarz, M., and Koo, Y. (2006). Endothelin-2 in ovarian follicle rupture. Endocrinology 147, 1770–1779.
Endothelin-2 in ovarian follicle rupture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1Oht7w%3D&md5=33f1db8a6bf27f454c905eff6c334912CAS | 16410304PubMed |

Lecouter, J., Lin, R., and Ferrara, N. (2004). EG-VEGF: a novel mediator of endocrine-specific angiogenesis, endothelial phenotype and function. Ann. N. Y. Acad. Sci. 1014, 50–57.
EG-VEGF: a novel mediator of endocrine-specific angiogenesis, endothelial phenotype and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvVehs7Y%3D&md5=ac846cf68260504bccc2518f4a176a96CAS | 15153419PubMed |

Lee, A., Christenson, L. K., Patton, P. E., Burry, K. A., and Stouffer, R. L. (1997a). Vascular endothelial growth factor production by human luteinized granulosa cells in vitro. Hum. Reprod. 12, 2756–2761.
Vascular endothelial growth factor production by human luteinized granulosa cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVOhug%3D%3D&md5=875be274f5fb08136b73ebcf0341e443CAS | 9455848PubMed |

Lee, P. J., Jiang, B. H., Chin, B. Y., Iyer, N. V., Alam, J., Semenza, G. L., and Choi, A. M. (1997b). Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272, 5375–5381.
Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhslamurk%3D&md5=216bad35dcabd1a441985c527f10612cCAS | 9038135PubMed |

Levy, N. S., Chung, S., Furneaux, H., and Levy, A. P. (1998). Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273, 6417–6423.
Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFalt78%3D&md5=ab9185fc87217a5cbddd264cac069701CAS | 9497373PubMed |

Maeda, M., Hasebe, Y., Egawa, K., Shibanuma, M., and Nose, K. (2006). Inhibition of angiogenesis and HIF-1alpha activity by antimycin A1. Biol. Pharm. Bull. 29, 1344–1348.
Inhibition of angiogenesis and HIF-1alpha activity by antimycin A1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovFKqsb4%3D&md5=cd3cdc925d07c7a222422b1321098a82CAS | 16819166PubMed |

Manalo, D. J., Rowan, A., Lavoie, T., Natarajan, L., Kelly, B. D., Ye, S. Q., Garcia, J. G., and Semenza, G. L. (2005). Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105, 659–669.
Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlGgtg%3D%3D&md5=fef1294f12bdb52e906edc3a6b47c7c3CAS | 15374877PubMed |

Melillo, G., Musso, T., Sica, A., Taylor, L. S., Cox, G. W., and Varesio, L. (1995). A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182, 1683–1693.
A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpslymtLo%3D&md5=b726cb75888c9a5ad57d6c369d6b6e41CAS | 7500013PubMed |

Na, G., Bridges, P. J., Koo, Y., and Ko, C. (2008). Role of hypoxia in the regulation of periovulatory EDN2 expression in the mouse. Can. J. Physiol. Pharmacol. 86, 310–319.
Role of hypoxia in the regulation of periovulatory EDN2 expression in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1CgsLk%3D&md5=34f5e498e89385508c9a3aa14b9a466bCAS | 18516093PubMed |

Nakayama, K. (2009). Cellular signal transduction of the hypoxia response. J. Biochem. 146, 757–765.
Cellular signal transduction of the hypoxia response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFaktLfO&md5=ccc4fcafc56710a793c72b96cc793556CAS | 19864435PubMed |

Neeman, M., Abramovitch, R., Schiffenbauer, Y. S., and Tempel, C. (1997). Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle. Int. J. Exp. Pathol. 78, 57–70.
Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szksl2isQ%3D%3D&md5=40753c5fdcf0f2475e6559c2c2f74774CAS | 9203980PubMed |

Neulen, J., Yan, Z., Raczek, S., Weindel, K., Keck, C., Weich, H. A., Marme, D., and Breckwoldt, M. (1995). Human chorionic gonadotrophin-dependent expression of vascular endothelial growth factor/vascular permeability factor in human granulosa cells: importance in ovarian hyperstimulation syndrome. J. Clin. Endocrinol. Metab. 80, 1967–1971.
Human chorionic gonadotrophin-dependent expression of vascular endothelial growth factor/vascular permeability factor in human granulosa cells: importance in ovarian hyperstimulation syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFOmsb0%3D&md5=7abb5bf0040d8d6e1c5e7ec03eae6db4CAS | 7775647PubMed |

Nishimura, R., and Okuda, K. (2010). Hypoxia is important for establishing vascularization during corpus luteum formation in cattle. J. Reprod. Dev. 56, 110–116.
Hypoxia is important for establishing vascularization during corpus luteum formation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVymtr0%3D&md5=e4459ceee97b3bc205c9595ac33fc4f3CAS | 19881217PubMed |

Podlovni, H., Ovadia, O., Kisliouk, T., Klipper, E., Zhou, Q. Y., Friedman, A., Alfaidy, N., and Meidan, R. (2006). Differential expression of prokineticin receptors by endothelial cells derived from different vascular beds: a physiological basis for distinct endothelial function. Cell. Physiol. Biochem. 18, 315–326.
Differential expression of prokineticin receptors by endothelial cells derived from different vascular beds: a physiological basis for distinct endothelial function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlSrs73F&md5=b6e8b90d004567d3e1230fe9cdb5f836CAS | 17170518PubMed |

Poulaki, V., Joussen, A. M., Mitsiades, N., Mitsiades, C. S., Iliaki, E. F., and Adamis, A. P. (2004). Insulin-like growth factor-I plays a pathogenetic role in diabetic retinopathy. Am. J. Pathol. 165, 457–469.
Insulin-like growth factor-I plays a pathogenetic role in diabetic retinopathy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFSqu7k%3D&md5=daa12b45cc17249f1853da97d1577d27CAS | 15277220PubMed |

Pugh, C. W., and Ratcliffe, P. J. (2003). Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 9, 677–684.
Regulation of angiogenesis by hypoxia: role of the HIF system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFOnur8%3D&md5=50f5d0cf34bb5881933ddcfdcaaa1cfbCAS | 12778166PubMed |

Redmer, D. A., Doraiswamy, V., Bortnem, B. J., Fisher, K., Jablonka-Shariff, A., Grazul-Bilska, A. T., and Reynolds, L. P. (2001). Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol. Reprod. 65, 879–889.
Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFemsLo%3D&md5=7bb482130a0f3917a3de8bd110517967CAS | 11514354PubMed |

Reynolds, L. P., and Redmer, D. A. (1999). Growth and development of the corpus luteum. J. Reprod. Fertil. Suppl. 54, 181–191.
| 1:STN:280:DC%2BD3c7lslansQ%3D%3D&md5=38b3900f6a6bd81b2206afea63c97dbfCAS | 10692854PubMed |

Reynolds, L. P., Grazul-Bilska, A. T., and Redmer, D. A. (2000). Angiogenesis in the corpus luteum. Endocrine 12, 1–9.
Angiogenesis in the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtlKrurY%3D&md5=b21f84c704f844e799d1d0d2891ac840CAS | 10855683PubMed |

Richard, D. E., Berra, E., and Pouyssegur, J. (1999). Angiogenesis: how a tumour adapts to hypoxia. Biochem. Biophys. Res. Commun. 266, 718–722.
Angiogenesis: how a tumour adapts to hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotVSjs78%3D&md5=227229312619d5f0b9618b0208ce38d9CAS | 10603309PubMed |

Robinson, R. S., Nicklin, L. T., Hammond, A. J., Schams, D., Hunter, M. G., and Mann, G. E. (2007). Fibroblast growth factor 2 is more dynamic than vascular endothelial growth factor A during the follicle–luteal transition in the cow. Biol. Reprod. 77, 28–36.
Fibroblast growth factor 2 is more dynamic than vascular endothelial growth factor A during the follicle–luteal transition in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntV2gsbs%3D&md5=5c61b1a4dde303950f68d6f0ae668deeCAS | 17360962PubMed |

Robinson, R. S., Woad, K. J., Hammond, A. J., Laird, M., Hunter, M. G., and Mann, G. E. (2009). Angiogenesis and vascular function in the ovary. Reproduction 138, 869–881.
Angiogenesis and vascular function in the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFKlur7F&md5=2807c01ccae7bd95634b8b0d89ed94c3CAS | 19786399PubMed |

Robker, R. L., Russell, D. L., Yoshioka, S., Sharma, S. C., Lydon, J. P., O’Malley, B. W., Espey, L. L., and Richards, J. S. (2000). Ovulation: a multi-gene, multi-step process. Steroids 65, 559–570.
Ovulation: a multi-gene, multi-step process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFCju70%3D&md5=181e94fdd548a465ca7d6a961ed569b2CAS | 11108860PubMed |

Sandau, K. B., Faus, H. G., and Brune, B. (2000). Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI-3K pathway. Biochem. Biophys. Res. Commun. 278, 263–267.
Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI-3K pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvVekuro%3D&md5=ee983ebc82a9459f45665d52d7047798CAS | 11071882PubMed |

Semenza, G. L. (2000). HIF-1: using two hands to flip the angiogenic switch. Cancer Metastasis Rev. 19, 59–65.
HIF-1: using two hands to flip the angiogenic switch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlSntg%3D%3D&md5=def5789ced2e2868b0423094c71ab728CAS | 11191064PubMed |

Semenza, G. L. (2007). Hypoxia-inducible factor 1 (HIF-1) pathway. Sci. STKE 2007, cm8.
Hypoxia-inducible factor 1 (HIF-1) pathway.Crossref | GoogleScholarGoogle Scholar | 17925579PubMed |

Semenza, G. L., Rue, E. A., Iyer, N. V., Pang, M. G., and Kearns, W. G. (1996). Assignment of the hypoxia-inducible factor 1 alpha gene to a region of conserved synteny on mouse chromosome 12 and human chromosome 14q. Genomics 34, 437–439.
Assignment of the hypoxia-inducible factor 1 alpha gene to a region of conserved synteny on mouse chromosome 12 and human chromosome 14q.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XktV2ht7Y%3D&md5=50e03cdc51e622c0359f5d7eb432ee7aCAS | 8786149PubMed |

Shi, D. Y., Xie, F. Z., Zhai, C., Stern, J. S., Liu, Y., and Liu, S. L. (2009). The role of cellular oxidative stress in regulating glycolysis energy metabolism in hepatoma cells. Mol. Cancer 8, 32.
The role of cellular oxidative stress in regulating glycolysis energy metabolism in hepatoma cells.Crossref | GoogleScholarGoogle Scholar | 19497135PubMed |

Singh, N., Sharma, G., and Mishra, V. (2012). Hypoxia inducible factor-1: its potential role in cerebral ischemia. Cell. Mol. Neurobiol. 32, 491–507.
Hypoxia inducible factor-1: its potential role in cerebral ischemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFarurk%3D&md5=6a29d365c5a313d73fd401b66ec94108CAS | 22297543PubMed |

Smith, M. F., McIntush, E. W., Ricke, W. A., Kojima, F. N., and Smith, G. W. (1999). Regulation of ovarian extracellular matrix remodelling by metalloproteinases and their tissue inhibitors: effects on follicular development, ovulation and luteal function. J. Reprod. Fertil. Suppl. 54, 367–381.
| 1:CAS:528:DyaK1MXnslSit7o%3D&md5=be226d22e93261c6d62abe035755ee95CAS | 10692869PubMed |

Stein, I., Itin, A., Einat, P., Skaliter, R., Grossman, Z., and Keshet, E. (1998). Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol. Cell. Biol. 18, 3112–3119.
| 1:CAS:528:DyaK1cXjsFSkur4%3D&md5=a2aaba9692637ec996f4dac8166630d3CAS | 9584152PubMed |

Takahashi, Y., Takahashi, S., Shiga, Y., Yoshimi, T., and Miura, T. (2000). Hypoxic induction of prolyl 4-hydroxylase alpha (I) in cultured cells. J. Biol. Chem. 275, 14 139–14 146.
Hypoxic induction of prolyl 4-hydroxylase alpha (I) in cultured cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjt1Cgu74%3D&md5=0e2964018f763a559834de1f5f0cd25dCAS |

Tam, K. K., Russell, D. L., Peet, D. J., Bracken, C. P., Rodgers, R. J., Thompson, J. G., and Kind, K. L. (2010). Hormonally regulated follicle differentiation and luteinization in the mouse is associated with hypoxia-inducible factor activity. Mol. Cell. Endocrinol. 327, 47–55.
Hormonally regulated follicle differentiation and luteinization in the mouse is associated with hypoxia-inducible factor activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFSrtrg%3D&md5=f70a6fb1323a43084dab1baa84943ea3CAS | 20600586PubMed |

Tesone, M., Stouffer, R. L., Borman, S. M., Hennebold, J. D., and Molskness, T. A. (2005). Vascular endothelial growth factor (VEGF) production by the monkey corpus luteum during the menstrual cycle: isoform-selective messenger RNA expression in vivo and hypoxia-regulated protein secretion in vitro. Biol. Reprod. 73, 927–934.
Vascular endothelial growth factor (VEGF) production by the monkey corpus luteum during the menstrual cycle: isoform-selective messenger RNA expression in vivo and hypoxia-regulated protein secretion in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGktb7E&md5=3488a37c73557e6506a52d462417d5aaCAS | 15987827PubMed |

Treins, C., Giorgetti-Peraldi, S., Murdaca, J., Monthouel-Kartmann, M. N., and Van Obberghen, E. (2005). Regulation of hypoxia-inducible factor (HIF)-1 activity and expression of HIF hydroxylases in response to insulin-like growth factor I. Mol. Endocrinol. 19, 1304–1317.
Regulation of hypoxia-inducible factor (HIF)-1 activity and expression of HIF hydroxylases in response to insulin-like growth factor I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFent74%3D&md5=76ba8076bac39507711e3c892d85d1a8CAS | 15695372PubMed |

van den Driesche, S., Myers, M., Gay, E., Thong, K. J., and Duncan, W. C. (2008). HCG up-regulates hypoxia inducible factor-1 alpha in luteinized granulosa cells: implications for the hormonal regulation of vascular endothelial growth factor A in the human corpus luteum. Mol. Hum. Reprod. 14, 455–464.
HCG up-regulates hypoxia inducible factor-1 alpha in luteinized granulosa cells: implications for the hormonal regulation of vascular endothelial growth factor A in the human corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSjsr7M&md5=3848b4cf81b423252eeadb5474f18600CAS | 18591213PubMed |

Varghese, R., Wong, C. K., Deol, H., Wagner, G. F., and DiMattia, G. E. (1998). Comparative analysis of mammalian stanniocalcin genes. Endocrinology 139, 4714–4725.
Comparative analysis of mammalian stanniocalcin genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFWltbY%3D&md5=f7e544a009655cd2adddb95d8278d61cCAS | 9794484PubMed |

Waltenberger, J., Mayr, U., Pentz, S., and Hombach, V. (1996). Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia. Circulation 94, 1647–1654.
Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsFSntLo%3D&md5=eed12a4f2b53651b4347bafd96a56004CAS | 8840857PubMed |

Wang, G. L., and Semenza, G. L. (1993). Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 82, 3610–3615.
| 1:CAS:528:DyaK2cXhtlSlsLw%3D&md5=58e6eb05b807216befec6727ee1a5029CAS | 8260699PubMed |

Wang, G. L., and Semenza, G. L. (1995). Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270, 1230–1237.
Purification and characterization of hypoxia-inducible factor 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtFOktr4%3D&md5=777f564fcba0ea22d5b14db62bb6414cCAS | 7836384PubMed |

Wang, M. T., Honn, K. V., and Nie, D. (2007). Cyclooxygenases, prostanoids and tumour progression. Cancer Metastasis Rev. 26, 525–534.
Cyclooxygenases, prostanoids and tumour progression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yktLbP&md5=439759cdeb48c6ed0c06f6de23c5dd9bCAS | 17763971PubMed |

Wang, K., Jiang, Y. Z., Chen, D. B., and Zheng, J. (2009). Hypoxia enhances FGF-2- and VEGF-stimulated human placental artery endothelial cell proliferation: roles of MEK1/2/ERK1/2 and PI3K/AKT1 pathways. Placenta 30, 1045–1051.
Hypoxia enhances FGF-2- and VEGF-stimulated human placental artery endothelial cell proliferation: roles of MEK1/2/ERK1/2 and PI3K/AKT1 pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGlsL7L&md5=28cff312b47bc33e93ef96014859b6fcCAS | 19892399PubMed |

Woad, K. J., Hammond, A. J., Hunter, M., Mann, G. E., Hunter, M. G., and Robinson, R. S. (2009). FGF-2 is crucial for the development of bovine luteal endothelial networks in vitro. Reproduction 138, 581–588.
FGF-2 is crucial for the development of bovine luteal endothelial networks in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrjJ&md5=e9d045b4a5b3e60a34881fafa4bfd2a7CAS | 19542253PubMed |

Woad, K. J., Hunter, M. G., Mann, G. E., Laird, M., Hammond, A. J., and Robinson, R. S. (2012). Fibroblast growth factor 2 is a key determinant of vascular sprouting during bovine luteal angiogenesis. Reproduction 143, 35–43.
Fibroblast growth factor 2 is a key determinant of vascular sprouting during bovine luteal angiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1yht7c%3D&md5=60df3dc9fb2b35d7f83b7e6b9f8cf647CAS | 21998077PubMed |

Wulff, C., Wilson, H., Largue, P., Duncan, W. C., Armstrong, D. G., and Fraser, H. M. (2000). 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. 85, 4302–4309.
Angiogenesis in the human corpus luteum: localization and changes in angiopoietins, tie-2, and vascular endothelial growth factor messenger ribonucleic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlWms70%3D&md5=df1bc28438c6eb86028bed57ef222328CAS | 11095472PubMed |

Wulff, C., Wiegand, S. J., Saunders, P. T., Scobie, G. A., and Fraser, H. M. (2001). Angiogenesis during follicular development in the primate and its inhibition by treatment with truncated Flt-1-Fc (vascular endothelial growth factor Trap(A40)). Endocrinology 142, 3244–3254.
Angiogenesis during follicular development in the primate and its inhibition by treatment with truncated Flt-1-Fc (vascular endothelial growth factor Trap(A40)).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksleltLY%3D&md5=a14d76a9e9ffb953e8994c8d7ba3eb91CAS | 11416048PubMed |

Yamashita, H., Kamada, D., Shirasuna, K., Matsui, M., Shimizu, T., Kida, K., Berisha, B., Schams, D., and Miyamoto, A. (2008). Effect of local neutralization of basic fibroblast growth factor or vascular endothelial growth factor by a specific antibody on the development of the corpus luteum in the cow. Mol. Reprod. Dev. 75, 1449–1456.
Effect of local neutralization of basic fibroblast growth factor or vascular endothelial growth factor by a specific antibody on the development of the corpus luteum in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVGjsb4%3D&md5=3858004646614f6a625e410eab3eaea1CAS | 18213648PubMed |

Young, R. M., Wang, S. J., Gordan, J. D., Ji, X., Liebhaber, S. A., and Simon, M. C. (2008). Hypoxia-mediated selective mRNA translation by an internal ribosome entry site-independent mechanism. J. Biol. Chem. 283, 16 309–16 319.
Hypoxia-mediated selective mRNA translation by an internal ribosome entry site-independent mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmslOjsLs%3D&md5=16743e251c4f217c6b92eb8cd29eb609CAS |

Zalman, Y., Klipper, E., Farberov, S., Mondal, M., Wee, G., Folger, J. K., Smith, G. W., and Meidan, R. (2012a). Regulation of angiogenesis-related prostaglandin f2alpha-induced genes in the bovine corpus luteum. Biol. Reprod. 86, 92.
Regulation of angiogenesis-related prostaglandin f2alpha-induced genes in the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 22174022PubMed |

Zalman, Y., Yalu, R., Klipper, E., and Meidan, R. (2012b) Pleiotropic effects of FGF-2 in cells of the developing corpus luteum. In ‘Proceedings of the 41st Annual Meeting of the Israel Endocrine Society’. (Israel Endocrine Society: Tel Aviv.)

Zhang, Z., Yin, D., and Wang, Z. (2011). Contribution of hypoxia-inducible factor-1 alpha to transcriptional regulation of vascular endothelial growth factor in bovine developing luteal cells. Anim. Sci. J. 82, 244–250.
Contribution of hypoxia-inducible factor-1 alpha to transcriptional regulation of vascular endothelial growth factor in bovine developing luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1Wns74%3D&md5=fd09b9ee90e431f78e6403527125413eCAS | 21729202PubMed |

Zhou, Q. Y., and Meidan, R. (2008). Biological function of prokineticins. Results Probl. Cell Differ. 46, 181–199.
Biological function of prokineticins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOnt7fL&md5=cb8951793e7d2418b2b293762789ede3CAS | 18202926PubMed |

Zlot, C., Ingle, G., Hongo, J., Yang, S., Sheng, Z., Schwall, R., Paoni, N., Wang, F., Peale, F. V., and Gerritsen, M. E. (2003). Stanniocalcin 1 is an autocrine modulator of endothelial angiogenic responses to hepatocyte growth factor. J. Biol. Chem. 278, 47 654–47 659.
Stanniocalcin 1 is an autocrine modulator of endothelial angiogenic responses to hepatocyte growth factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Cqtbw%3D&md5=84210f704cf9e98c84719354a9f234eaCAS |