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The urokinase plasminogen activator system components are regulated by vascular endothelial growth factor D in bovine oviduct

Published online by Cambridge University Press:  08 June 2018

Daniela C. García ,
Agostina Russo-Maenza ,
Dora C. Miceli ,
Pablo A. Valdecantos  and
Mariela Roldán-Olarte Open the ORCID record for Mariela Roldán-Olarte [Opens in a new window]
Daniela C. García
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, Argentina. Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI – San Miguel de Tucumán, Argentina.
Agostina Russo-Maenza
Affiliation:
Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI – San Miguel de Tucumán, Argentina.
Dora C. Miceli
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, Argentina. Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI – San Miguel de Tucumán, Argentina.
Pablo A. Valdecantos
Affiliation:
Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, UNT. Chacabuco 461, T4000ILI – San Miguel de Tucumán, Argentina.
Mariela Roldán-Olarte*
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán. Chacabuco 461, T4000ILI – San Miguel de Tucumán, Argentina.
*
All correspondence to: Mariela Roldán-Olarte. Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Biología ‘Dr. Francisco D. Barbieri,’ Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán. Chacabuco 461, T4000ILI – San Miguel de Tucumán, Argentina. Tel: +54 381 4247752 (ext. 7099); Fax: +54 381 4247752 (ext. 7004). E-mail: emroldanolarte@fbqf.unt.edu.ar
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Summary

The mammalian oviduct plays a pivotal role in the success of early reproductive events. The urokinase plasminogen activator system (uPAS) is present in the bovine oviduct and is involved in extracellular matrix remodelling through plasmin generation. This system can be regulated by several members of the vascular endothelial growth factors (VEGF) and their receptors. In this study, the VEGF-D effect on the regulation of uPAS was evaluated. First, RT-polymerase chain reaction (PCR) analyses were used to evidence the expression of VEGF-D and its receptors in oviductal epithelial cells (BOEC). VEGF-D, VEGFR2 and VEGFR3 transcripts were found in ex vivo and in vitro BOEC, while only VEGFR2 mRNA was present after in vitro conditions. VEGF-D showed a regulatory effect on uPAS gene expression in a dose-dependent manner, inducing an increase in the expression of both uPA and its receptor (uPAR) at 24 h post-induction and decreases in the expression of its inhibitor (PAI-1). In addition, the regulation of cell migration induced by VEGF-D and uPA in BOEC monolayer cultures was analyzed. The wound areas of monolayer cultures incubated with VEGF-D 10 ng/ml or uPA 10 nM were modified and significant differences were found at 24 h for both stimulations. These results indicated that uPAS and VEGF-D systems can modify the arrangement of the bovine oviductal epithelium and contribute to the correct maintenance of the oviductal microenvironment.

Keywords

Cell culturesCell migrationOviductuPASVEGF-D
Type
Research Article
Information
Zygote , Volume 26 , Issue 3 , June 2018 , pp. 242 - 249
Copyright
Copyright © Cambridge University Press 2018 

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References

Achen, M.G., Jeltsch, M., Kukk, E., Makinen, T., Vitali, A., Wilks, A.F., Alitalo, K. & Stacker, S.A. (1998). Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc. Natl. Acad. Sci. USA 95, 548–53.CrossRefGoogle ScholarPubMed
Baldwin, J.F., Sood, V., Elfline, M.A., Luke, C.E., Dewyer, N.A., Díaz, J.A., Myers, D.D., Wakefield, T. & Henke, P.K. (2012). The role of urokinase plasminogen activator and plasmin activator inhibitor-1 on vein wall remodelling in experimental deep vein thrombosis. J. Vasc. Surg. 56, 1089–97.Google Scholar
Behzadian, M.A., Windsor, L.J., Ghaly, N., Liou, G., Tsai, N.T. & Caldwell, R.B. (2003). VEGF-induced paracellular permeability in cultured endothelial cells involves urokinase and its receptor. FASEB J. 17, 752–4.CrossRefGoogle ScholarPubMed
Cardona, A. (2015). Automatic image segmentation method for in vitro wound healing assay quantitative analysis. IFMBE Proc. 49, 381–4.CrossRefGoogle Scholar
Costache, M.I., Ioana, M., Iordache, S., Ene, D., Costache, C.A. & Saftoiu, A. (2015). VEGF expression in pancreatic cancer and other malignancies: a review of the literature. Rom. J. Intern. Med. 53, 199–208.Google ScholarPubMed
Ferrara, N. (2010). Pathways mediating VEGF-independent tumor angiogenesis. Cytokine Growth Factor Rev. 21, 21–6.Google Scholar
Gabler, C., Einspanier, A., Schams, D. & Einspanier, R. (1999). Expression of vascular endothelial growth factor (VEGF) and its corresponding receptors (flt-1 and flk-1) in the bovine oviduct. Mol. Reprod. Dev. 53, 376–83.Google Scholar
Gabler, C., Killian, G.J. & Einspanier, R. (2001). Differential expression of extracellular matrix components in the bovine oviduct during the oestrous cycle. Reproduction 122, 121–30.Google Scholar
García, D.C., Miceli, D.C., Rizo, G., García, E.V., Valdecantos, P.A. & Roldán-Olarte, M. (2016). Expression and localization of urokinase-type plasminogen activator receptor in bovine cumulus–oocyte complexes. Zygote 24, 230–5.CrossRefGoogle ScholarPubMed
García, D.C., Miceli, D.C., Valdecantos, P.A., García, E.V. & Roldán-Olarte, M. (2014). Expression of urokinase type plasminogen activator receptor (uPAR) in the bovine oviduct: relationship with uPA effect on oviductal epithelial cells. Res. Vet. Sci. 97, 118–23.Google Scholar
García, D.C., Valdecantos, P.A., Miceli, D.C. & Roldán-Olarte, M. (2017). Genistein affects proliferation and migration of bovine oviductal epithelial cells. Res. Vet. Sci. 114, 59–63.Google Scholar
Harris, N.C., Davydova, N., Roufail, S., Paquet-Fifield, S., Paavonen, K., Karnezis, T., Zhang, Y.F., Sato, T., Rothacker, J., Nice, E.C., Stacker, S.A. & Achen, M.G. (2013). The propeptides of VEGF-D determine heparin binding, receptor heterodimerization, and effects on tumor biology. J. Biol. Chem. 288, 8176–86.Google Scholar
Hildenbrand, R., Allgayer, H., Marx, A. & Stroebel, P. (2010). Modulators of the urokinase-type plasminogen activation system for cancer. Expert Opin. Investig. Drugs 19, 641–52.Google Scholar
Hunter, R.H. (2012). Components of oviduct physiology in eutherian mammals. Biol. Rev. Camb. Philos. Soc. 87, 244–55.CrossRefGoogle ScholarPubMed
Jia, H., Bagherzadeh, A., Bicknell, R., Duchen, M.R., Liu, D. & Zachary, I. (2004). Vascular endothelial growth factor (VEGF)-D and VEGF-A differentially regulate KDR-mediated signaling and biological function in vascular endothelial cells. J. Biol. Chem. 279, 36148–57.Google Scholar
Jiménez-Díaz, M., Giunta, S., Valz-Gianinet, J., Pereyra-Alfonso, S., Flores, V. & Miceli, D. (2000). Proteases with plasminogen activator activity in hamster oviduct. Mol. Reprod. Dev. 55, 47–54.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Jordaens, L., Arias-Alvarez, M., Pintelon, I., Thys, S., Valckx, S., Dezhkam, Y., Bols, P.E. & Leroy, J.L. (2015). Elevated non-esterified fatty acid concentrations hamper bovine oviductal epithelial cell physiology in three different in vitro culture systems. Theriogenology 84, 899–910.Google Scholar
Killian, G.J. (2004). Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim. Reprod. Sci. 82–83, 141–53.Google Scholar
Lee, S.H., Jeong, D., Han, Y.S. & Baek, M.J. (2015). Pivotal role of vascular endothelial growth factor pathway in tumor angiogenesis. Ann. Surg. Treat. Res. 89, 1–8.Google Scholar
Li, Z.D., Bork, J.P., Krueger, B., Patsenker, E., Schulze-Krebs, A., Hahn, E.G. & Schuppan, D. (2005). VEGF induces proliferation, migration, and TGF-beta1 expression in mouse glomerular endothelial cells via mitogen-activated protein kinase and phosphatidylinositol 3-kinase. Biochem. Biophys. Res. Commun. 334, 1049–60.Google Scholar
López-Albors, O., Olsson, F., Llinares, A.B., Gutiérrez, H., Latorre, R., Candanosa, E., Guillen-Martinez, A. & Izquierdo-Rico, M.J. (2017). Expression of the vascular endothelial growth factor system (VEGF) in the porcine oviduct during the estrous cycle. Theriogenology 93, 46–54.Google Scholar
Maillo, V., Lopera-Vásquez, R., Hamdi, M., Gutiérrez-Adán, A., Lonergan, P. & Rizos, D. (2016a). Maternal-embryo interaction in the bovine oviduct: evidence from in vivo and in vitro studies. Theriogenology 86, 443–50.Google Scholar
Maillo, V., Sánchez-Calabuig, M.J., Lopera-Vásquez, R., Hamdi, M., Gutiérrez-Adán, A., Lonergan, P. & Rizos, D. (2016b). Oviductal response to gametes and early embryos in mammals. Reproduction 152, R127–41.Google Scholar
Mandriota, S.J., Seghezzi, G., Vassalli, J.D., Ferrara, N., Wasi, S., Mazzieri, R., Mignatti, P. & Pepper, M.S. (1995). Vascular endothelial growth factor increases urokinase receptor expression in vascular endothelial cells. J. Biol. Chem. 270, 9709–16.Google Scholar
Olofsson, B., Korpelainen, E., Pepper, M.S., Mandriota, S.J., Aase, K., Kumar, V., Gunji, Y., Jeltsch, M.M., Shibuya, M., Alitalo, K. & Eriksson, U. (1998). Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc. Natl. Acad. Sci. USA 95, 11709–14.Google Scholar
Plouët, J., Moro, F., Bertagnolli, S., Coldeboeuf, N., Mazarguil, H., Clamens, S. & Bayard, F. (1997). Extracellular cleavage of the vascular endothelial growth factor 189-amino acid form by urokinase is required for its mitogenic effect. J. Biol. Chem. 272, 13390–6.Google Scholar
Prager, G.W., Mihaly, J., Brunner, P.M., Koshelnick, Y., Hoyer-Hansen, G. & Binder, B.R. (2009). Urokinase mediates endothelial cell survival via induction of the X-linked inhibitor of apoptosis protein. Blood 113, 1383–90.CrossRefGoogle ScholarPubMed
Roldán-Olarte, M., García, D.C., Jiménez-Díaz, M., Valdecantos, P.A. & Miceli, D.C. (2012). In vivo and in vitro expression of the plasminogen activators and urokinase type plasminogen activator receptor (uPAR) in the pig oviduct. Anim. Reprod. Sci. 136, 90–9.Google Scholar
Roldán-Olarte, M., Maillo, V., Sánchez-Calabuig, M.J., Beltrán-Brena, P., Rizos, D. & Gutiérrez-Adán, A. (2017). Effect of urokinase type plasminogen activator on in vitro bovine oocyte maturation. Reproduction 154, 231–40.Google Scholar
Rottmayer, R., Ulbrich, S.E., Kolle, S., Prelle, K., Neumueller, C., Sinowatz, F., Meyer, H.H., Wolf, E. & Hiendleder, S. (2006). A bovine oviduct epithelial cell suspension culture system suitable for studying embryo-maternal interactions: morphological and functional characterization. Reproduction 132, 637–48.Google Scholar
Salajegheh, A. (2016). Introduction to Angiogenesis in Normal Physiology Disease and Malignancy Angiogenesis in Health Disease and Malignancy. Springer International Publishing.Google Scholar
Shibuya, M. (2014). VEGF–VEGFR signals in health and disease. Biomol. Ther. (Seoul) 22, 1–9.Google Scholar
Soutar, R.L., Dillon, J. & Ralston, S.H. (1997). Control genes for reverse-transcription-polymerase chain reaction: a comparison of beta actin and glyceraldehyde phosphate dehydrogenase. Br. J. Haematol. 97, 247–8.Google Scholar
Valdecantos, P.A., Bravo-Miana, R., García, E.V., García, D.C., Roldán-Olarte, M. & Miceli, D.C. (2017). Expression of bone morphogenetic protein receptors in bovine oviductal epithelial cells: evidences of autocrine BMP signaling. Anim. Reprod. Sci. 185, 89–96.Google Scholar
Varricchi, G., Granata, F., Loffredo, S., Genovese, A. & Marone, G. (2015). Angiogenesis and lymphangiogenesis in inflammatory skin disorders. J. Am. Acad. Dermatol. 73, 144–53.Google Scholar
Vempati, P., Popel, A.S. & MacGabhann, F. (2014). Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning. Cytokine Growth Factor Rev. 25, 1–19.Google Scholar
Vlahakis, N.E., Young, B.A., Atakilit, A. & Sheppard, D. (2005). The lymphangiogenic vascular endothelial growth factors VEGF-C and -D are ligands for the integrin α9β1. J. Biol. Chem. 280, 4544–52.Google Scholar
Wijayagunawardane, M.P., Kodithuwakku, S.P., Yamamoto, D. & Miyamoto, A. (2005). Vascular endothelial growth factor system in the cow oviduct: a possible involvement in the regulation of oviductal motility and embryo transport. Mol. Reprod. Dev. 72, 511–20.Google Scholar
Yan, L. & Shi, Z. (2016). Research progress of the influence of VEGF on female mammalian reproduction. J. Agric. Biotechnol. 24, 443–53.Google Scholar
Zhao, T., Zhao, W., Meng, W., Liu, C., Chen, Y. & Sun, Y. (2014). Vascular endothelial growth factor-C: its unrevealed role in fibrogenesis. Am. J. Physiol. Heart Circ. Physiol. 306, H789–96.Google Scholar