CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Reproduction, Fertility and Development   
Reproduction, Fertility and Development
Journal Banner
  Vertebrate Reproductive Science & Technology
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Structure
Contacts
Content
Online Early
Current Issue
Just Accepted
All Issues
Special Issues
Research Fronts
Virtual Issues
Sample Issue
For Authors
General Information
Scope
Submit Article
Author Instructions
Open Access
Awards and Prizes
For Referees
Referee Guidelines
Review an Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates
Library Recommendation

blue arrow e-Alerts
blank image
Subscribe to our email Early Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter logo LinkedIn

red arrow Connect with SRB
blank image
facebook TwitterIcon

Affiliated Societies

RFD is the official journal of the International Embryo Transfer Society and the Society for Reproductive Biology.


 

Article << Previous     |     Next >>   Contents Vol 25(2)

Fibroblast growth factor 2 induces the precocious development of endothelial cell networks in bovine luteinising follicular cells

Mhairi Laird A B C, Kathryn J. Woad A B, Morag G. Hunter B, George E. Mann B and Robert S. Robinson A D

A School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK.
B School of Biosciences, University of Nottingham, Sutton Bonington campus, Loughborough, Leicestershire LE12 5RD, UK.
C Present address: Institute of Reproductive and Developmental Biology, Imperial College London, Hammersmith Hospital, London W12 0NN, UK.
D Corresponding author. Email: bob.robinson@nottingham.ac.uk

Reproduction, Fertility and Development 25(2) 372-386 http://dx.doi.org/10.1071/RD12182
Submitted: 9 June 2012  Accepted: 11 October 2012   Published: 16 November 2012


 
PDF (3.4 MB) $25
 Supplementary Material
 Export Citation
 Print
  
Abstract

The transition from follicle to corpus luteum represents a period of intense angiogenesis; however, the exact roles of angiogenic factors during this time remain to be elucidated. Thus, the roles of vascular endothelial growth factor (VEGF) A, fibroblast growth factor (FGF) 2 and LH in controlling angiogenesis were examined in the present study. A novel serum-free luteinising follicular angiogenesis culture system was developed in which progesterone production increased during the first 5 days and was increased by LH (P < 0.01). Blockade of signalling from FGF receptors (SU5402; P < 0.001) and, to a lesser extent, VEGF receptors (SU1498; P < 0.001) decreased the development of endothelial cell (EC) networks. Conversely, FGF2 dose-dependently (P < 0.001) induced the precocious transition of undeveloped EC islands into branched networks associated with a twofold increase in the number of branch points (P < 0.001). In contrast, VEGFA had no effect on the area of EC networks or the number of branch points. LH had no effect on the area of EC networks, but it marginally increased the number of branch points (P < 0.05) and FGF2 production (P < 0.001). Surprisingly, progesterone production was decreased by FGF2 (P < 0.01) but only on Day 5 of culture. Progesterone production was increased by SU5402 (P < 0.001) and decreased by SU1498 (P < 0.001). These results demonstrate that FGF and VEGF receptors play a fundamental role in the formation of luteal EC networks in vitro, which includes a novel role for FGF2 in induction of EC sprouting.

Additional keywords: angiogenesis, cow, sprouting.


References

Amselgruber, W. M., Schafer, M., and Sinowatz, F. (1999). Angiogenesis in the bovine corpus luteum: an immunocytochemical and ultrastructural study. Anat. Histol. Embryol. 28, 157–166.
CrossRef | PubMed |

Ball, S. G., Shuttleworth, C. A., and Kielty, C. M. (2007). Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J. Cell Biol. 177, 489–500.
CrossRef | PubMed |

Beckman, J. D., Grazul-Bilska, A. T., Johnson, M. L., Reynolds, L. P., and Redmer, D. A. (2006). Isolation and characterization of ovine luteal pericytes and effects of nitric oxide on pericyte expression of angiogenic factors. Endocrine 29, 467–476.
CrossRef | PubMed |

Berisha, B., Schams, D., Kosmann, M., Amselgruber, W., and Einspanier, R. (2000). Expression and tissue concentration of vascular endothelial growth factor, its receptors, and localization in the bovine corpus luteum during estrous cycle and pregnancy. Biol. Reprod. 63, 1106–1114.
CrossRef | PubMed |

Berisha, B., Steffl, M., Amselgruber, W., and Schams, D. (2006). Changes in fibroblast growth factor 2 and its receptors in bovine follicles before and after GnRH application and after ovulation. Reproduction 131, 319–329.
CrossRef | PubMed |

Berisha, B., Steffl, M., Welter, H., Kliem, H., Meyer, H. H. D., Schams, D., and Amselgruber, W. (2008). Effect of the luteinising hormone surge on regulation of vascular endothelial growth factor and extracellular matrix-degrading proteinases and their inhibitors in bovine follicles. Reprod. Fertil. Dev. 20, 258–268.
CrossRef | PubMed |

De Smet, F., Segura, I., De Bock, K., Hohensinner, P. J., and Carmeliet, P. (2009). Mechanisms of vessel branching filopodia on endothelial tip cells lead the way. Arterioscler. Thromb. Vasc. Biol. 29, 639–649.
CrossRef | PubMed |

Eilken, H. M., and Adams, R. H. (2010). Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22, 617–625.
CrossRef | PubMed |

Finney, D. J. (1988). Was this in your statistics textbook? 3. Design and analysis. Exp. Agric. 24, 421–432.

Fraser, H. M., Dickson, S. E., Lunn, S. F., Wulff, C., Morris, K. D., Carroll, V. A., and Bicknell, R. (2000). Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 141, 995–1000.
CrossRef | PubMed |

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 hypervascularization followed by functional and structural luteolysis in the primate ovary. Endocrinology 153, 1972–1983.
CrossRef | PubMed |

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.
CrossRef | PubMed |

Gilbert, I., Robert, C., Dieleman, S., Blondin, P., and Sirard, M. A. (2011). Transcriptional effect of the LH surge in bovine granulosa cells during the peri-ovulation period. Reproduction 141, 193–205.
CrossRef | PubMed |

Gridley, T. (2007). Notch signaling in vascular development and physiology. Development 134, 2709–2718.
CrossRef | PubMed |

Hatziapostolou, M., Polytarchou, C., Katsoris, P., Courty, J., and Papadimitriou, E. (2006). Heparin affinity regulatory peptide/pleiotrophin mediates fibroblast growth factor 2 stimulatory effects on human prostate cancer cells. J. Biol. Chem. 281, 32 217–32 226.
CrossRef |

Hazzard, T. M., Rohan, R. M., Molskness, T. A., Fanton, J. W., D’Amato, R. J., and Stouffer, R. L. (2002). Injection of antiangiogenic agents into the macaque preovulatory follicle: disruption of corpus luteum development and function. Endocrine 17, 199–206.
CrossRef | PubMed |

Hirschberg, R. M., Plendl, J., and Kaessmeyer, S. (2012). Alpha smooth muscle actin in the cycling ovary: an immunohistochemical study. Clin. Hemorheol. Microcirc. 50, 113–129.
| PubMed |

Hünigen, H., Bisplinghoff, P., Plendl, J., and Bahramsoltani, M. (2008). Vascular dynamics in relation to immunolocalisation of VEGF-A, VEGFR-2 and Ang-2 in the bovine corpus luteum. Acta Histochem. 110, 462–472.
CrossRef | PubMed |

Irving-Rodgers, H. F., Catanzariti, K. D., Aspden, W. J., D’Occhio, M. J., and Rodgers, R. J. (2006). Remodeling of extracellular matrix at ovulation of the bovine ovarian follicle. Mol. Reprod. Dev. 73, 1292–1302.
CrossRef | PubMed |

Joseph, C., Hunter, M. G., Sinclair, K. D., and Robinson, R. S. (2012). The expression, regulation and function of secreted protein, acidic, cysteine-rich in the follicle–luteal transition. Reproduction 144, 361–372.
CrossRef | PubMed |

Kanda, S., Miyata, Y., and Kanetake, H. (2004). Fibroblast growth factor-2-mediated capillary morphogenesis of endothelial cells requires signals via Flt-1/vascular endothelial growth factor receptor-1: possible involvement of c-Akt. J. Biol. Chem. 279, 4007–4016.
CrossRef | PubMed |

Katanasaka, Y., Ida, T., Asai, T., Maeda, N., and Oku, N. (2008). Effective delivery of an angiogenesis inhibitor by neovessel-targeted liposomes. Int. J. Pharm. 360, 219–224.
| PubMed |

Kobayashi, S., Berisha, B., Amselgruber, W. M., Schams, D., and Miyamoto, A. (2001). Production and localisation of angiotensin II in the bovine early corpus luteum: a possible interaction with luteal angiogenic factors and prostaglandin F2 alpha. J. Endocrinol. 170, 369–380.
CrossRef | PubMed |

Kuhnert, F., Tam, B. Y. Y., Sennino, B., Gray, J. T., Yuan, J., Jocson, A., Nayak, N. R., Mulligan, R. C., McDonald, D. M., and Kuo, C. J. (2008). Soluble receptor-mediated selective inhibition of VEGFR and PDGFR beta signaling during physiologic and tumor angiogenesis. Proc. Natl Acad. Sci. USA 105, 10 185–10 190.
CrossRef |

Kurz, H., Fehr, J., Nitschke, R., and Burkhardt, H. (2008). Pericytes in the mature chorioallantoic membrane capillary plexus contain desmin and alpha-smooth muscle actin: relevance for non-sprouting angiogenesis. Histochem. Cell Biol. 130, 1027–1040.
CrossRef | PubMed |

Lee, A., Christenson, L. K., Patton, P. E., Burry, K. A., and Stouffer, R. L. (1997). Vascular endothelial growth factor production by human luteinized granulosa cells in vitro. Hum. Reprod. 12, 2756–2761.
CrossRef | PubMed |

Lowry, S. R. (1992). Use and misuse of multiple comparisons in animal-experiments. J. Anim. Sci. 70, 1971–1977.
| PubMed |

Masri, F. A., Xu, W., Comhair, S. A. A., Asosingh, K., Koo, M., Vasanji, A., Drazba, J., Anand-Apte, B., and Erzurum, S. C. (2007). Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L548–L554.
CrossRef | PubMed |

Miyamoto, A., Shirasuna, K., Shimizu, T., Bollwein, H., and Schams, D. (2010). Regulation of corpus luteum development and maintenance: specific roles of angiogenesis and action of prostaglandin F2alpha. Soc. Reprod. Fertil. Suppl. 67, 289–304.
| PubMed |

Mohammadi, M., McMahon, G., Sun, L., Tang, C., Hirth, P., Yeh, B. K., Hubbard, S. R., and Schlessinger, J. (1997). Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276, 955–960.
CrossRef | PubMed |

Nissen, L. J., Cao, R., Hedlund, E. M., Wang, Z., Zhao, X., Wetterskog, D., Funa, K., Brakenhielm, E., and Cao, Y. (2007). Angiogenic factors FGF2 and PDGF-BB synergistically promote murine tumor neovascularization and metastasis. J. Clin. Invest. 117, 2766–2777.
CrossRef | PubMed |

Niswender, G. D. (2002). Molecular control of luteal secretion of progesterone. Reproduction 123, 333–339.
CrossRef | PubMed |

Ozerdem, U., and Stallcup, W. B. (2003). Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6, 241–249.
CrossRef | PubMed |

Papetti, M., Shujath, J., Riley, K. N., and Herman, I. M. (2003). FGF-2 antagonizes the TGF-beta1-mediated induction of pericyte alpha-smooth muscle actin expression: a role for myf-5 and Smad-mediated signaling pathways. Invest. Ophthalmol. Vis. Sci. 44, 4994–5005.
CrossRef | PubMed |

Presta, M., Dell’Era, P., Mitola, S., Moroni, E., Ronca, R., and Rusnati, M. (2005). Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 16, 159–178.
CrossRef | PubMed |

Ravindranath, N., Littleihrig, L., Phillips, H. S., Ferrara, N., and Zeleznik, A. J. (1992). Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology 131, 254–260.
CrossRef | PubMed |

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.
CrossRef | PubMed |

Reynolds, L., and Redmer, D. (1999). Growth and development of the corpus luteum. J. Reprod. Fertil. Suppl. 54, 181–191.
| PubMed |

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.
CrossRef | PubMed |

Robinson, R. S., Hammond, A. J., Mann, G. E., and Hunter, M. G. (2008). A novel physiological culture system that mimics luteal angiogenesis. Reproduction 135, 405–413.
CrossRef | PubMed |

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.
CrossRef | PubMed |

Schams, D., and Berisha, B. (2004). Regulation of corpus luteum function in cattle: an overview. Reprod. Domest. Anim. 39, 241–251.
CrossRef | PubMed |

Schams, D., Kosmann, M., Berisha, B., Amselgruber, W. M., and Miyamoto, A. (2001). Stimulatory and synergistic effects of luteinising hormone and insulin like growth factor 1 on the secretion of vascular endothelial growth factor and progesterone of cultured bovine granulosa cells. Exp. Clin. Endocrinol. Diabetes 109, 155–162.
CrossRef | PubMed |

Seghezzi, G., Patel, S., Ren, C. J., Gualandris, A., Pintucci, G., Robbins, E. S., Shapiro, R. L., Galloway, A. C., Rifkin, D. B., and Mignatti, P. (1998). Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J. Cell Biol. 141, 1659–1673.
CrossRef | PubMed |

Shirakihara, T., Horiguchi, K., Miyazawa, K., Ehata, S., Shibata, T., Morita, I., Miyazono, K., and Saitoh, M. (2011). TGF-beta regulates isoform switching of FGF receptors and epithelial–mesenchymal transition. EMBO J. 30, 783–795.
CrossRef | PubMed |

Spicer, L. J., and Stewart, R. E. (1996). Interactions among basic fibroblast growth factor, epidermal growth factor, insulin, and insulin-like growth factor-I (IGF-I) on cell numbers and steroidogenesis of bovine thecal cells: role of IGF-I receptors. Biol. Reprod. 54, 255–263.
CrossRef | PubMed |

Strawn, L. M., McMahon, G., App, H., Schreck, R., Kuchler, W. R., Longhi, M. P., Hui, T. H., Tang, C., Levitzki, A., Gazit, A., Chen, I., Keri, G., Orfi, L., Risau, W., Flamme, I., Ullrich, A., Hirth, K. P., and Shawver, L. K. (1996). Flk-1 as a target for tumor growth inhibition. Cancer Res. 56, 3540–3545.
| PubMed |

Sugino, N., Kashida, S., Takiguchi, S., Karube, A., and Kato, H. (2000). Expression of vascular endothelial growth factor and its receptors in the human corpus luteum during the menstrual cycle and in early pregnancy. J. Clin. Endocrinol. Metab. 85, 3919–3924.
CrossRef | PubMed |

Sugiura, K., Su, Y. Q., Diaz, F. J., Pangas, S. A., Sharma, S., Wigglesworth, K., O’Brien, M. J., Matzuk, M. M., Shimasaki, S., and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593–2603.
CrossRef | PubMed |

Vitorino, P., and Meyer, T. (2008). Modular control of endothelial sheet migration. Genes Dev. 22, 3268–3281.
CrossRef | PubMed |

Wang, Y., Chang, J., Chen, K. D., Li, S., Li, J. Y., Wu, C., and Chien, S. (2007). Selective adapter recruitment and differential signaling networks by VEGF vs. shear stress. Proc. Natl Acad. Sci. USA 104, 8875–8879.
CrossRef | PubMed |

Woad, K. J., Hammond, A. J., Hunter, M., Mann, G. E., Hunter, M. G., and Robinson, R. S. (2009). FGF2 is crucial for the development of bovine luteal endothelial networks in vitro. Reproduction 138, 581–588.
CrossRef | PubMed |

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.
CrossRef | PubMed |

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.
CrossRef | PubMed |

Zimmermann, R. C., Hartman, T., Bohlen, P., Sauer, M. V., and Kitajewski, J. (2001). Preovulatory treatment of mice with anti-VEGF receptor 2 antibody inhibits angiogenesis in corpora lutea. Microvasc. Res. 62, 15–25.
CrossRef | PubMed |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2016