Morphometric and gene expression analyses of stromal expansion during development of the bovine fetal ovary
M. D. Hartanti A , K. Hummitzsch A , H. F. Irving-Rodgers A B , W. M. Bonner A , K. J. Copping A , R. A. Anderson C , I. C. McMillen D , V. E. A. Perry E and R. J. Rodgers
A F
+ Author Affiliations
- Author Affiliations
A Discipline of Obstetrics and Gynaecology, School of Medicine, Robinson Research Institute, The University of Adelaide, Adelaide, SA 5005, Australia.
B School of Medical Science, Griffith University, Gold Coast Campus, Qld 4222, Australia.
C Medical Research Council Centre for Reproductive Health, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
D The Chancellery, University of Newcastle, Callaghan, NSW 2308, Australia.
E School of Veterinary and Medical Science, University of Nottingham, Sutton Bonington, LE12 5RD, UK.
F Corresponding author. Email: ray.rodgers@adelaide.edu.au
Reproduction, Fertility and Development 31(3) 482-495 https://doi.org/10.1071/RD18218
Submitted: 9 June 2018 Accepted: 18 August 2018 Published: 3 December 2018
Journal Compilation © CSIRO 2018 Open Access CC BY-NC-ND
Abstract
During ovarian development stroma from the mesonephros penetrates and expands into the ovarian primordium and thus appears to be involved, at least physically, in the formation of ovigerous cords, follicles and surface epithelium. Cortical stromal development during gestation in bovine fetal ovaries (n = 27) was characterised by immunohistochemistry and by mRNA analyses. Stroma was identified by immunostaining of stromal matrix collagen type I and proliferating cells were identified by Ki67 expression. The cortical and medullar volume expanded across gestation, with the rate of cortical expansion slowing over time. During gestation, the proportion of stroma in the cortex and total volume in the cortex significantly increased (P < 0.05). The proliferation index and numerical density of proliferating cells in the stroma significantly decreased (P < 0.05), whereas the numerical density of cells in the stroma did not change (P > 0.05). The expression levels of 12 genes out of 18 examined, including osteoglycin (OGN) and lumican (LUM), were significantly increased later in development (P < 0.05) and the expression of many genes was positively correlated with other genes and with gestational age. Thus, the rate of cortical stromal expansion peaked in early gestation due to cell proliferation, whilst late in development expression of extracellular matrix genes increased.
Additional keywords: extracellular matrix, proliferation, stroma.
References
Abbott, D. H., Padmanabhan, V., and Dumesic, D. A. (2006). Contributions of androgen and estrogen to fetal programming of ovarian dysfunction. Reprod. Biol. Endocrinol. 4, 17.| Contributions of androgen and estrogen to fetal programming of ovarian dysfunction.Crossref | GoogleScholarGoogle Scholar |
Adams, G. P., and Pierson, R. A. (1995). Bovine model for study of ovarian follicular dynamics in humans. Theriogenology 43, 113–120.
| Bovine model for study of ovarian follicular dynamics in humans.Crossref | GoogleScholarGoogle Scholar |
Ameye, L., and Young, M. F. (2002). Mouse deficient in small leucine-rich proteoglycans novel in vivo models for osteoporosis, osteoarthritis, Ehlers–Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12, 107R–116R.
| Mouse deficient in small leucine-rich proteoglycans novel in vivo models for osteoporosis, osteoarthritis, Ehlers–Danlos syndrome, muscular dystrophy, and corneal diseases.Crossref | GoogleScholarGoogle Scholar |
Bandeira, F. T., Carvalho, A. A., Castro, S. V., Lima, L. F., Viana, D. A., Evangelista, J., Pereira, M., Campello, C. C., Figueiredo, J. R., and Rodrigues, A. (2015). Two methods of vitrification followed by in vitro culture of the ovine ovary: evaluation of the follicular development and ovarian extracellular matrix. Reprod. Domest. Anim. 50, 177–185.
| Two methods of vitrification followed by in vitro culture of the ovine ovary: evaluation of the follicular development and ovarian extracellular matrix.Crossref | GoogleScholarGoogle Scholar |
Bastian, N. A., Bayne, R. A., Hummitzsch, K., Hatzirodos, N., Bonner, W. M., Hartanti, M. D., Irving-Rodgers, H. F., Anderson, R. A., and Rodgers, R. J. (2016). Regulation of fibrillins and modulators of TGFβ in fetal bovine and human ovaries. Reproduction 152, 127–137.
| Regulation of fibrillins and modulators of TGFβ in fetal bovine and human ovaries.Crossref | GoogleScholarGoogle Scholar |
Berger, M., Bergers, G., Arnold, B., Hammerling, G. J., and Ganss, R. (2005). Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood 105, 1094–1101.
| Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization.Crossref | GoogleScholarGoogle Scholar |
Berisha, B., Pfaffl, M. W., and Schams, D. (2002). Expression of estrogen and progesterone receptors in the bovine ovary during estrous cycle and pregnancy. Endocrine 17, 207–214.
| Expression of estrogen and progesterone receptors in the bovine ovary during estrous cycle and pregnancy.Crossref | GoogleScholarGoogle Scholar |
Berkholtz, C. B., Lai, B. E., Woodruff, T. K., and Shea, L. D. (2006). Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis. Histochem. Cell Biol. 126, 583–592.
| Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis.Crossref | GoogleScholarGoogle Scholar |
Bonaldo, P., Russo, V., Bucciotti, F., Doliana, R., and Colombatti, A. (1990). Structural and functional features of the alpha3 chain indicate a bridging role for chicken collagen VI in connective tissues. Biochemistry 29, 1245–1254.
| Structural and functional features of the alpha3 chain indicate a bridging role for chicken collagen VI in connective tissues.Crossref | GoogleScholarGoogle Scholar |
Bondjers, C., Kalén, M., Hellström, M., Scheidl, S. J., Abramsson, A., Renner, O., Lindahl, P., Cho, H., Kehrl, J., and Betsholtz, C. (2003). Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am. J. Pathol. 162, 721–729.
| Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells.Crossref | GoogleScholarGoogle Scholar |
Castellani, P., Viale, G., Dorcaratto, A., Nicolo, G., Kaczmarek, J., Querze, G., and Zardi, L. (1994). The fibronectin isoform containing the ED-B oncofetal domain: a marker of angiogenesis. Int. J. Cancer 59, 612–618.
| The fibronectin isoform containing the ED-B oncofetal domain: a marker of angiogenesis.Crossref | GoogleScholarGoogle Scholar |
Cescon, M., Gattazzo, F., Chen, P., and Bonaldo, P. (2015). Collagen VI at a glance. J. Cell Sci. 128, 3525–3531.
| Collagen VI at a glance.Crossref | GoogleScholarGoogle Scholar |
Colman-Lerner, A., Fischman, M. L., Lanuza, G. M., Bissel, D. M., Kornblihtt, A. R., and Baranao, J. L. (1999). Evidence for a role of the alternatively spliced ED-I sequence of fibronectin during ovarian follicular development. Endocrinology 140, 2541–2548.
| Evidence for a role of the alternatively spliced ED-I sequence of fibronectin during ovarian follicular development.Crossref | GoogleScholarGoogle Scholar |
Copping, K. J., Hoare, A., Callaghan, M., McMillen, I. C., Rodgers, R. J., and Perry, V. E. A. (2014). Fetal programming in 2-year-old calving heifers: peri-conception and first trimester protein restriction alters fetal growth in a gender-specific manner. Anim. Prod. Sci. 54, 1333–1337.
De Candia, L. M., and Rodgers, R. J. (1999). Characterization of the expression of the alternative splicing of the ED-A, ED-B and V regions of fibronectin mRNA in bovine ovarian follicles and corpora lutea. Reprod. Fertil. Dev. 11, 367–377.
| Characterization of the expression of the alternative splicing of the ED-A, ED-B and V regions of fibronectin mRNA in bovine ovarian follicles and corpora lutea.Crossref | GoogleScholarGoogle Scholar |
Epskamp, S., Cramer, A. O. J., Waldorp, L. J., Schmittmann, V. D., and Borsboom, D. (2012). qgraph: network visualizations of relationships in psychometric data. J. Stat. Softw. 48, 1–18.
| qgraph: network visualizations of relationships in psychometric data.Crossref | GoogleScholarGoogle Scholar |
Figueiredo, J. R., Hulshof, S. C. J., Thiry, M., Van den Hurk, R., Bevers, M. M., Nusgens, B., and Beckers, J. F. (1995). Extracellular matrix proteins and basement membrane: their identification in bovine ovaries and significance for the attachment of cultured preantral follicles. Theriogenology 43, 845–858.
| Extracellular matrix proteins and basement membrane: their identification in bovine ovaries and significance for the attachment of cultured preantral follicles.Crossref | GoogleScholarGoogle Scholar |
Fulghesu, A. M., Clampelli, M., Belosi, C., Apa, R., Pavone, V., and Lanzone, A. (2001). A new ultrasound criterion for the diagnosis of polycystic ovary syndrome: the ovarian stroma/total area ratio. Fertil. Steril. 76, 326–331.
| A new ultrasound criterion for the diagnosis of polycystic ovary syndrome: the ovarian stroma/total area ratio.Crossref | GoogleScholarGoogle Scholar |
Ge, G., Seo, N. S., Liang, X., Hopkins, D. R., Hook, M., and Greenspan, D. S. (2004). Bone morphogenetic protein-1/tolloid-related metalloproteinases process osteoglycin and enhance its ability to regulate collagen fibrillogenesis. J. Biol. Chem. 279, 41626–41633.
| Bone morphogenetic protein-1/tolloid-related metalloproteinases process osteoglycin and enhance its ability to regulate collagen fibrillogenesis.Crossref | GoogleScholarGoogle Scholar |
Goldberg, M., Septier, D., Oldberg, A., Young, M. F., and Ameye, L. G. (2006). Fibromodulin-deficient mice display impaired collagen fibrillogenesis in predentin as well as altered dentin mineralization and enamel formation. J. Histochem. Cytochem. 54, 525–537.
| Fibromodulin-deficient mice display impaired collagen fibrillogenesis in predentin as well as altered dentin mineralization and enamel formation.Crossref | GoogleScholarGoogle Scholar |
Hatzirodos, N., Bayne, R. A., Irving-Rodgers, H. F., Hummitzsch, K., Sabatier, L., Lee, S., Bonner, W., Gibson, M. A., Rainey, W. E., Carr, B. R., Mason, H. D., Reinhardt, D. P., Anderson, R. A., and Rodgers, R. J. (2011). Linkage of regulators of TGF-beta activity in the fetal ovary to polycystic ovary syndrome. FASEB J. 25, 2256–2265.
| Linkage of regulators of TGF-beta activity in the fetal ovary to polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar |
Heeren, A. M., van Iperen, L., Klootwijk, D. B., de Melo Bernardo, A., Roost, M. S., Gomes Fernandes, M. M., Louwe, L. A., Hilders, C. G., Helmerhorst, F. M., van der Westerlaken, L. A., and Chuva de Sousa Lopes, S. M. (2015). Development of the follicular basement membrane during human gametogenesis and early folliculogenesis. BMC Dev. Biol. 15, 4.
| Development of the follicular basement membrane during human gametogenesis and early folliculogenesis.Crossref | GoogleScholarGoogle Scholar |
Huet, C., Pisselet, C., Mandon-Pépin, B., Monget, P., and Monniaux, D. (2001). Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function. J. Endocrinol. 169, 347–360.
| Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function.Crossref | GoogleScholarGoogle Scholar |
Hughesdon, P. E. (1982). Morphology and morphogenesis of the Stein–Leventhal ovary and of so-called “hyperthecosis”. Obstet. Gynecol. Surv. 37, 59–77.
| Morphology and morphogenesis of the Stein–Leventhal ovary and of so-called “hyperthecosis”.Crossref | GoogleScholarGoogle Scholar |
Hummitzsch, K., Irving-Rodgers, H. F., Hatzirodos, N., Bonner, W., Sabatier, L., Reinhardt, D. P., Sado, Y., Ninomiya, Y., Wilhelm, D., and Rodgers, R. J. (2013). A new model of development of the mammalian ovary and follicles. PLoS One 8, e55578.
| A new model of development of the mammalian ovary and follicles.Crossref | GoogleScholarGoogle Scholar |
Hummitzsch, K., Anderson, R. A., Wilhelm, D., Wu, J., Telfer, E. E., Russell, D. L., Robertson, S. A., and Rodgers, R. J. (2015). Stem cells, progenitor cells, and lineage decisions in the ovary. Endocr. Rev. 36, 65–91.
| Stem cells, progenitor cells, and lineage decisions in the ovary.Crossref | GoogleScholarGoogle Scholar |
Irving-Rodgers, H. F., and Rodgers, R. J. (2007). Extracellular matrix in ovarian follicular and luteal development. In ‘Novel Concepts in Ovarian Endocrinology’. (Ed. A. Gonzalez-Bulnes.) pp. 83–112. (Transworld Research Network: Kerala, India.)
Irving-Rodgers, H. F., Bathgate, R. A. D., Ivell, R., Domagalski, R., and Rodgers, R. J. (2002). Dynamic changes in the expression of relaxin-like factor (Insl3), cholesterol side-chain cleavage cytochrome p450, and 3beta-hydroxysteroid dehydrogenase in bovine ovarian follicles during growth and atresia. Biol. Reprod. 66, 934–943.
| Dynamic changes in the expression of relaxin-like factor (Insl3), cholesterol side-chain cleavage cytochrome p450, and 3beta-hydroxysteroid dehydrogenase in bovine ovarian follicles during growth and atresia.Crossref | GoogleScholarGoogle Scholar |
Iwahashi, M., Muragaki, Y., Ooshima, A., and Nakano, R. (2000). Type VI collagen expression during growth of human ovarian follicles. Fertil. Steril. 74, 343–347.
| Type VI collagen expression during growth of human ovarian follicles.Crossref | GoogleScholarGoogle Scholar |
Kagawa, N., Silber, S., and Kuwayama, M. (2009). Successful vitrification of bovine and human ovarian tussue. Reprod. Biomed. Online 18, 568–577.
| Successful vitrification of bovine and human ovarian tussue.Crossref | GoogleScholarGoogle Scholar |
Kalamajski, S., and Oldberg, A. (2009). Homologous sequence in lumican and fibromodulin leucine-rich repeat 5–7 competes for collagen binding. J. Biol. Chem. 284, 534–539.
| Homologous sequence in lumican and fibromodulin leucine-rich repeat 5–7 competes for collagen binding.Crossref | GoogleScholarGoogle Scholar |
Kalamajski, S., Aspberg, A., Lindblom, K., Heinegard, D., and Oldberg, A. (2009). Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization. Biochem. J. 423, 53–59.
| Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization.Crossref | GoogleScholarGoogle Scholar |
Kirsch, T., Wellner, M., Luft, F. C., Haller, H., and Lippoldt, A. (2001). Altered gene expression in cerebral capillaries of stroke-prone spontaneously hypertensive rats. Brain Res. 910, 106–115.
| Altered gene expression in cerebral capillaries of stroke-prone spontaneously hypertensive rats.Crossref | GoogleScholarGoogle Scholar |
Kobayashi, H., Sun, W. G., and Terao, T. (1999). Immunolocalization of hyaluronic acid and inter-alpha-trypsin inhibitor in mice. Cell Tissue Res. 296, 587–597.
| Immunolocalization of hyaluronic acid and inter-alpha-trypsin inhibitor in mice.Crossref | GoogleScholarGoogle Scholar |
Kuo, H.-J., Maslen, C. L., Keene, D. R., and Glanville, R. W. (1997). Type VI collagen anchors endothelial basement membranes by interacting with type IV collagen. J. Biol. Chem. 272, 26522–26529.
| Type VI collagen anchors endothelial basement membranes by interacting with type IV collagen.Crossref | GoogleScholarGoogle Scholar |
Li, Z., and Huang, H. (2008). Epigenetic abnormality: a possible mechanism underlying the fetal origin of polycystic ovary syndrome. Med. Hypotheses 70, 638–642.
| Epigenetic abnormality: a possible mechanism underlying the fetal origin of polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar |
Lind, A. K., Weijdegard, B., Dahm-Kahler, P., Molne, J., Sundfeldt, K., and Brannstrom, M. (2006). Collagens in the human ovary and their changes in the perifollicular stroma during ovulation. Acta Obstet. Gynecol. Scand. 85, 1476–1484.
| Collagens in the human ovary and their changes in the perifollicular stroma during ovulation.Crossref | GoogleScholarGoogle Scholar |
Loverro, G., De Pergola, G., Di Naro, E., Tartagni, M., Lavopa, C., and Caringella, A. M. (2010). Predictive value of ovarian stroma measurement for cardiovascular risk in polycyctic ovary syndrome: a case control study. J. Ovarian Res. 3, 25.
| Predictive value of ovarian stroma measurement for cardiovascular risk in polycyctic ovary syndrome: a case control study.Crossref | GoogleScholarGoogle Scholar |
Matti, N., Irving-Rodgers, H. F., Hatzirodos, N., Sullivan, T. R., and Rodgers, R. J. (2010). Differential expression of focimatrix and steroidogenic enzymes before size deviation during waves of follicular development in bovine ovarian follicles. Mol. Cell. Endocrinol. 321, 207–214.
| Differential expression of focimatrix and steroidogenic enzymes before size deviation during waves of follicular development in bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar |
McArthur, M. E., Irving-Rodgers, H. F., Byers, S., and Rodgers, R. J. (2000). Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles. Biol. Reprod. 63, 913–924.
| Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles.Crossref | GoogleScholarGoogle Scholar |
Niculescu, M., Novac, L., Mateescu, G. O., Mihail, S. R., Neamtu, S., and Papachristu, A. (2011). Original study the vasculogenesis of the fetal ovary – morphological and immunohistochemical study. Analele Universitatii “Dunarea De Jos” Galati Medicina 17, 5–9.
Oksjoki, S., Sallinen, S., Vuorio, E., and Anttila, L. (1999). Cyclic expression of mRNA transcripts for connective tissue components in the mouse ovary. Mol. Hum. Reprod. 5, 803–808.
| Cyclic expression of mRNA transcripts for connective tissue components in the mouse ovary.Crossref | GoogleScholarGoogle Scholar |
Paranko, J. (1987). Expression of type I and III collagen during morphogenesis of fetal rat testis and ovary. Anat. Rec. 219, 91–101.
| Expression of type I and III collagen during morphogenesis of fetal rat testis and ovary.Crossref | GoogleScholarGoogle Scholar |
Prodoehl, M. J., Irving-Rodgers, H. F., Bonner, W. M., Sullivan, T. M., Micke, G. C., Gibson, M. A., Perry, V. E., and Rodgers, R. J. (2009). Fibrillins and latent TGFbeta binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol. Cell. Endocrinol. 307, 133–141.
| Fibrillins and latent TGFbeta binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams.Crossref | GoogleScholarGoogle Scholar |
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 |
Roy, S. K., and Kole, A. R. (1998). Ovarian transforming growth factor-b (TGF-b) receptors: in vitro effects of follicle stimulating hormone, epidermal growth factor and TGF-b on receptor expression in human preantral follicles. Mol. Hum. Reprod. 4, 207–214.
| Ovarian transforming growth factor-b (TGF-b) receptors: in vitro effects of follicle stimulating hormone, epidermal growth factor and TGF-b on receptor expression in human preantral follicles.Crossref | GoogleScholarGoogle Scholar |
Rozen, S., and Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S. Krawetz and S. Misener.) pp. 365–386. (Humana Press: Totowa, NJ, USA.)
Russe, I. (1983). Oogenesis in cattle and sheep. Bibl. Anat 24, 77–92.
Sabatelli, P., Bonaldob, P., Lattanzia, G., Braghettab, P., Bergaminb, N., Capannic, C., Mattiolid, E., Columbarod, M., Ognibenec, A., Pepee, G., Bertinif, E., Merlinid, L., Maraldia, N. M., and Squarzonia, S. (2001). Collagen VI deficiency affects the organization of fibronectin in the extracellular matrix of cultured fibroblasts. Matrix Biol. 20, 475–486.
| Collagen VI deficiency affects the organization of fibronectin in the extracellular matrix of cultured fibroblasts.Crossref | GoogleScholarGoogle Scholar |
Santos, S. S., Ferreira, M. A., Pinto, J. A., Sampaio, R. V., Carvalho, A. C., Silva, T. V., Costa, N. N., Cordeiro, M. S., Miranda, M. S., Ribeiro, H. F., and Ohashi, O. M. (2013). Characterization of folliculogenesis and the occurrence of apoptosis in the development of the bovine fetal ovary. Theriogenology 79, 344–350.
| Characterization of folliculogenesis and the occurrence of apoptosis in the development of the bovine fetal ovary.Crossref | GoogleScholarGoogle Scholar |
Sarraj, M. A., and Drummond, A. E. (2012). Mammalian foetal ovarian development: consequences for health and disease. Reproduction 143, 151–163.
| Mammalian foetal ovarian development: consequences for health and disease.Crossref | GoogleScholarGoogle Scholar |
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682.
| Fiji: an open-source platform for biological-image analysis.Crossref | GoogleScholarGoogle Scholar |
Sforza, C., Ferrario, V. F., De Pol, A., Marzona, L., Forni, M., and Forabosco, A. (1993). Morphometric study of the human ovary during compartmentalization. Anat. Rec. 236, 626–634.
| Morphometric study of the human ovary during compartmentalization.Crossref | GoogleScholarGoogle Scholar |
Smith, P., Wilhelm, D., and Rodgers, R. J. (2014). Development of mammalian ovary. J. Endocrinol. 221, R145–R161.
| Development of mammalian ovary.Crossref | GoogleScholarGoogle Scholar |
Spencer, J. A., Hacker, S. L., Davis, E. C., Mecham, R. P., Knutsen, R. H., Li, D. Y., Gerard, R. D., Richardson, J. A., Olson, E. N., and Yanagisawa, H. (2005). Altered vascular remodeling in fibulin-5-deficient mice reveals a role of fibulin-5 in smooth muscle cell proliferation and migration. Proc. Natl. Acad. Sci. USA 102, 2946–2951.
| Altered vascular remodeling in fibulin-5-deficient mice reveals a role of fibulin-5 in smooth muscle cell proliferation and migration.Crossref | GoogleScholarGoogle Scholar |
Wandji, S. A., Sršeň, V., Voss, A. K., Eppig, J. J., and Fortune, J. E. (1996). Initiation in vitro of growth of bovine primordial follicles 1. Biol. Reprod. 55, 942–948.
| Initiation in vitro of growth of bovine primordial follicles 1.Crossref | GoogleScholarGoogle Scholar |
Weng, Q., Wang, H., Medan, M. S., Jin, W., Xia, G., Watanabe, G., and Taya, K. (2006). Expression of inhibin-activin subunits in the ovaries of fetal and neonatal mice. J. Reprod. Dev. 52, 607–616.
| Expression of inhibin-activin subunits in the ovaries of fetal and neonatal mice.Crossref | GoogleScholarGoogle Scholar |
