The immunoexpression patterns of fibroblast growth factors in the pregnant and postpartum rat ovary
Emel Alan A * and Yasin Kulak BA Faculty of Veterinary Medicine, Department of Histology and Embryology, University of Erciyes, Kayseri, Turkey.
B Republic of Turkey Ministry of Education, Kayseri, Turkey.
Reproduction, Fertility and Development 33(16) 817-830 https://doi.org/10.1071/RD21025
Published online: 11 November 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Fibroblast growth factors (FGFs) are polypeptides involved in the regulation of oogenesis and folliculogenesis by inducing ovarian mitogenic, homeostatic and angiogenic activity. This study was aimed at determining the localisation of FGF ligands (FGF1 and FGF2) and FGF receptor 2 (FGFR2) in the rat ovary by immunohistochemical analyses, at pregnancy and the postpartum period. During pregnancy and the postpartum period, positive FGF1 immunoreactions were observed in the nucleus and cytoplasm of germinative epithelial cells, granulosa cells of follicles in different developmental stages, theca interna cells, interstitial cells, luteal cells and atretic follicles. FGF2 immunoreactivity was strong in the cytoplasm of the endothelial cells and smooth muscle cells of the ovarian blood vessels and in the smooth muscle cells of the ovarian cortex and medulla. Strong FGFR2 immunoreactivity was observed in the stromal cells surrounding the blood vessels and rete ovarii. Immunoreaction intensity of the FGF1, FGF2 and FGFR2 had relatively similar abundances between the periods examined. Considering that FGFs act as local regulators in oogenesis, folliculogenesis, follicular atresia, ovulation, corpus luteum formation and regression and angiogenesis, this study supports the idea that FGFs may also be involved in these physiological functions in rat ovaries during pregnancy and postpartum period.
Keywords: corpus luteum, fibroblast growth factors, FGF1, FGF2, immunohistochemistry, ovarian follicle, postpartum, pregnancy, rat.
References
Almeida, AP, Saraiva, MVA, Alves Filho, JG, Silva, GM, Gonçalves, RFB, Brito, IR, Silva, AWB, Lima, AKF, Cunha, RMS, Silva, JRV, and Figueiredo, JR (2012). Gene expression and immunolocalization of fibroblast growth factor 2 in the ovary and its effect on the in vitro culture of caprine preantral ovarian follicles. Reproduction in Domestic Animals 47, 20–25.| Gene expression and immunolocalization of fibroblast growth factor 2 in the ovary and its effect on the in vitro culture of caprine preantral ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 21518029PubMed |
Asakai, R, Song, S-Y, Itoh, N, Yamakuni, T, Tamura, K, and Okamoto, R (1994). Differential gene expression of fibroblast growth factor receptor isoforms in rat ovary. Molecular and Cellular Endocrinology 104, 75–80.
| Differential gene expression of fibroblast growth factor receptor isoforms in rat ovary.Crossref | GoogleScholarGoogle Scholar | 7821708PubMed |
Ben-Haroush, A, Abir, R, Ao, A, Jin, S, Kessler-Icekson, G, Feldberg, D, and Fisch, B (2005). Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses. Fertility and Sterility 84, 1257–1268.
| Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses.Crossref | GoogleScholarGoogle Scholar | 16210019PubMed |
Berisha, B, Schams, D, Kosmann, M, Amselgruber, W, and Einspanier, R (2000). Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles. Journal of Endocrinology 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 |
Berisha, B, Sinowatz, F, and Schams, D (2004). Expression and localization of fibroblast growth factor (FGF) family members during the final growth of bovine ovarian follicles. Molecular Reproduction and Development 67, 162–171.
| Expression and localization of fibroblast growth factor (FGF) family members during the final growth of bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 14694431PubMed |
Berisha, B, Welter, H, Shimizu, T, Miyamoto, A, Meyer, HHD, and Schams, D (2006). Expression of fibroblast growth factor 1 (FGF1) and FGF7 in mature follicles during the periovulatory period after GnRH in the cow. Journal of Reproduction and Development 52, 307–313.
| Expression of fibroblast growth factor 1 (FGF1) and FGF7 in mature follicles during the periovulatory period after GnRH in the cow.Crossref | GoogleScholarGoogle Scholar |
Bulgurcuoğlu, S, Özsait, B, and Attar, E (2003). Büyüme faktörlerinin oosit ve embriyo gelişimi üzerindeki etkisi. Artemis 4, 18–26.
Buratini, J, Pinto, MGL, Castilho, AC, Amorim, RL, Giometti, IC, Portela, VM, Nicola, ES, and Price, CA (2007). Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2b, in bovine follicles. Biology of Reproduction 77, 743–750.
| Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2b, in bovine follicles.Crossref | GoogleScholarGoogle Scholar | 17582010PubMed |
Chaves, RN, Tavares de Matos, MH, Buratini, J, and Ricardo de Figueiredo, J (2012). The fibroblast growth factor family: involvement in the regulation of folliculogenesis. Reproduction, Fertility and Development 24, 905–1050.
| The fibroblast growth factor family: involvement in the regulation of folliculogenesis.Crossref | GoogleScholarGoogle Scholar |
Crossman, G (1937). A modification of mallory’s connective tissue stain with a discussion of the principles involved. The Anatomical Record 69, 33–38.
| A modification of mallory’s connective tissue stain with a discussion of the principles involved.Crossref | GoogleScholarGoogle Scholar |
Detre, S, Saccani Jotti, G, and Dowsett, M (1995). A “quickscore” method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas. Journal of Clinical Pathology 48, 876–878.
| A “quickscore” method for immunohistochemical semiquantitation: validation for oestrogen receptor in breast carcinomas.Crossref | GoogleScholarGoogle Scholar | 7490328PubMed |
Du, S, Liu, X, Deng, K, Zhou, W, Lu, F, and Shi, D (2018). The expression pattern of fibroblast growth factor 10 and its receptors during buffalo follicular development. International Journal of Clinical and Experimental Pathology 11, 4934–4941.
| 31949569PubMed |
Elmetwally, MA (2018). Uterine involution and ovarian activity in postpartum Holstein dairy cows. A review. Journal of Veterinary Health Care 1, 29–40.
| Uterine involution and ovarian activity in postpartum Holstein dairy cows. A review.Crossref | GoogleScholarGoogle Scholar |
Elvin JA, Matzuk MM (2001) Control of ovarian function. In ‘Transgenics in endocrinology’. Contemporary endocrinology. (Eds MM Matzuk, CW Brown, TR Kumar) pp. 61–89. (Humana Press: Totowa, NJ, USA)
Farrell, B, and Breeze, AL (2018). Structure, activation and dysregulation of fibroblast growth factor receptor kinases: perspectives for clinical targeting. Biochemical Society Transactions 46, 1753–1770.
| Structure, activation and dysregulation of fibroblast growth factor receptor kinases: perspectives for clinical targeting.Crossref | GoogleScholarGoogle Scholar | 30545934PubMed |
Fortune, JE (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Animal Reproduction Science 78, 135–163.
| The early stages of follicular development: activation of primordial follicles and growth of preantral follicles.Crossref | GoogleScholarGoogle Scholar | 12818642PubMed |
Gabler, C, Plath-Gabler, A, Killian, GJ, 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. Reproduction in Domestic Animals 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 | 15367264PubMed |
Gilchrist, RB, Ritter, LJ, and Armstrong, DT (2004). Oocyte–somatic cell interactions during follicle development in mammals. Animal Reproduction Science 82–83, 431–446.
| Oocyte–somatic cell interactions during follicle development in mammals.Crossref | GoogleScholarGoogle Scholar | 15271471PubMed |
Gospodarowicz, D, Plouet, J, and Fujii, DK (1989). Ovarian germinal epithelial cells respond to basic fibroblast growth factor and express its gene: implications for early folliculogenesis. Endocrinology 125, 1266–1276.
| Ovarian germinal epithelial cells respond to basic fibroblast growth factor and express its gene: implications for early folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 2474436PubMed |
Grazul-Bilska, AT, Redmer, DA, Killilca, SD, Zheng, J, and Reynolds, LP (1993). Initial characterization of endothelial mitogens produced by bovine corpora lutea from thc estrous cycle. Biochemistry and Cell Biology 71, 270–277.
| Initial characterization of endothelial mitogens produced by bovine corpora lutea from thc estrous cycle.Crossref | GoogleScholarGoogle Scholar | 7506042PubMed |
Grazul-Bilska, AT, Redmer, DA, Jablonka-Shariff, A, Biondini, ME, and Reynolds, LP (1995). Proliferation and progesterone production of ovine luteal cells from several stages of the estrous cycle: effects of fibroblast growth factors and luteinizing hormone. Canadian Journal of Physiology and Pharmacology 73, 491–500.
| Proliferation and progesterone production of ovine luteal cells from several stages of the estrous cycle: effects of fibroblast growth factors and luteinizing hormone.Crossref | GoogleScholarGoogle Scholar | 7545534PubMed |
Gültekin, SE, Tokman, B, and Mollaoğlu, N (2002). Epidermal büyüme faktörü ve fibroblast büyüme faktörünün folliküler kist ve ameloblastomadaki varlığının immünhistokimyasal olarak değerlendirilmesi. Ondokuz Mayıs Üniversitesi Diş Hekimliği Fakültesi Dergisi 4, 12–16.
Jablonka-Shariff, A, Grazul-Bilska, AT, Redmer, DA, and Reynolds, LP (1997). Cellular proliferation and fibroblast growth factors in the corpus luteum during early pregnancy in ewes. Growth Factors 14, 15–23.
| Cellular proliferation and fibroblast growth factors in the corpus luteum during early pregnancy in ewes.Crossref | GoogleScholarGoogle Scholar | 9086325PubMed |
Jewgenow, K (1996). Impact of peptide growth factors on the culture of small preantral follicles of domestic cats. Theriogenology 45, 889–895.
| Impact of peptide growth factors on the culture of small preantral follicles of domestic cats.Crossref | GoogleScholarGoogle Scholar | 16727850PubMed |
Knee, RS, Pitcher, SE, and Murphy, PR (1994). Basic fibroblast growth factor sense (FGF) and antisense (GFG) RNA transcripts are expressed in unfertilize human oocytes and in differentiated adult tissues. Biochemical and Biophysical Research Communications 205, 577–583.
| Basic fibroblast growth factor sense (FGF) and antisense (GFG) RNA transcripts are expressed in unfertilize human oocytes and in differentiated adult tissues.Crossref | GoogleScholarGoogle Scholar | 7999082PubMed |
Knight, PG, and Glister, C (2006). TGF-β superfamily members and ovarian follicle development. Reproduction 132, 191–206.
| TGF-β superfamily members and ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 16885529PubMed |
Koos, RD, and Olson, CE (1989). Expression of basic fibroblast growth factor in the rat ovary: detection of mRNA using reverse transcription-polymerase chain reaction amplification. Molecular Endocrinology 3, 2041–2048.
| Expression of basic fibroblast growth factor in the rat ovary: detection of mRNA using reverse transcription-polymerase chain reaction amplification.Crossref | GoogleScholarGoogle Scholar | 2628738PubMed |
Koos, RD, and Seidel, RH (1989). Detection of acidic fibroblast growth factor mRNA in the rat ovary using reverse transcription-polymerase chain reaction amplification. Biochemical and Biophysical Research Communications 165, 82–88.
| Detection of acidic fibroblast growth factor mRNA in the rat ovary using reverse transcription-polymerase chain reaction amplification.Crossref | GoogleScholarGoogle Scholar | 2480128PubMed |
Lapolt, PS, Yamato, M, Veljkovic, M, Sincich, C, Ny, T, Tsafriri, A, and Hsueh, AJW (1990). Basic fibroblast growth factor ınduction of granulosa cell tissue-type plasminogen activator expression and oocyte maturation: potential role as a paracrine ovarian hormone. Endocrinology 127, 2357–2363.
| Basic fibroblast growth factor ınduction of granulosa cell tissue-type plasminogen activator expression and oocyte maturation: potential role as a paracrine ovarian hormone.Crossref | GoogleScholarGoogle Scholar | 2171912PubMed |
Neufeld, G, Ferrara, N, Schweigerer, L, Mitchell, R, and Gospodarowicz, D (1987). Bovine granulosa cells produce basic fibroblast growth factor. Endocrinology 121, 597–603.
| Bovine granulosa cells produce basic fibroblast growth factor.Crossref | GoogleScholarGoogle Scholar | 3036478PubMed |
Nilsson, E, Parrott, JA, and Skinner, MK (2001). Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Molecular and Cellular Endocrinology 175, 123–130.
| Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 11325522PubMed |
Oktay, K, Schenken, RS, and Nelson, JF (1995). Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biology of Reproduction 53, 295–301.
| Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat.Crossref | GoogleScholarGoogle Scholar | 7492681PubMed |
Ornitz, DM, and Itoh, N (2001). Fibroblast growth factors. Genome Biology 2, .
| Fibroblast growth factors.Crossref | GoogleScholarGoogle Scholar | 11276432PubMed |
Paulini, F, Silva, RC, de Paula Rôlo, JLJ, and Lucci, CM (2014). Ultrastructural changes in oocytes during folliculogenesis in domestic mammals. Journal of Ovarian Research 7, 102.
| Ultrastructural changes in oocytes during folliculogenesis in domestic mammals.Crossref | GoogleScholarGoogle Scholar | 25358389PubMed |
Pepper, MS, and Mandriota, SJ (1998). Regulation of vascular endothelial growth factor receptor-2 (flk-1) expression in vascular endothelial cells. Experimental Cell Research 241, 414–425.
| Regulation of vascular endothelial growth factor receptor-2 (flk-1) expression in vascular endothelial cells.Crossref | GoogleScholarGoogle Scholar | 9637783PubMed |
Portela, VM, Machado, MF, Goncalves, PB, Zamberlam, GO, Buratini, J, and Price, CA (2009). Follicle atresia is regulated by fibroblast growth factor-18 in cattle. Biology of Reproduction 81, 105.
| Follicle atresia is regulated by fibroblast growth factor-18 in cattle.Crossref | GoogleScholarGoogle Scholar |
Reynolds, LP, and Redmer, DA (1998). Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary. Journal of Animal Science 76, 1671–1681.
| Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary.Crossref | GoogleScholarGoogle Scholar | 9655588PubMed |
Rifkin, DB, and Moscatelli, D (1989). Recent developments in the cell biology of basic fibroblast growth factor. Journal of Cell Biology 109, 1–6.
| Recent developments in the cell biology of basic fibroblast growth factor.Crossref | GoogleScholarGoogle Scholar |
Rodgers, RJ, and Irving-Rodgers, HF (2010). Morphological classification of bovine ovarian follicles. Reproduction 139, 309–318.
| Morphological classification of bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 19786400PubMed |
Schams, D, Steinberg, V, Steffl, M, Meyer, HHD, and Berisha, B (2009). Expression and possible role of fibroblast growth factor family members in porcine antral follicles during final maturation. Reproduction 138, 141–149.
| Expression and possible role of fibroblast growth factor family members in porcine antral follicles during final maturation.Crossref | GoogleScholarGoogle Scholar | 19380425PubMed |
Sheldon, IM, Cronin, J, Goetze, L, Donofrio, G, and Schuberth, H-J (2009). Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction 81, 1025–1032.
| Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle.Crossref | GoogleScholarGoogle Scholar | 19439727PubMed |
Stirling, D, Waterman, MR, and Simpson, ER (1991). Expression of mRNA encoding basic fibroblast growth factor (bFGF) in bovine corpora lutea and cultured luteal cells. Journal of Reproduction and Fertility 91, 1–8.
| Expression of mRNA encoding basic fibroblast growth factor (bFGF) in bovine corpora lutea and cultured luteal cells.Crossref | GoogleScholarGoogle Scholar | 1847419PubMed |
Sudo, N, Shimizu, T, Kawashima, C, Kaneko, E, Tetsuka, M, and Miyamoto, A (2007). Insulin-like growth factor-1 (IGF-1) system during follicle development in the bovine ovary: relationship among IGF-1, type 1 IGF receptor (IGFR-1) and pregnancy-associated plasma protein-A (PAPP-A). Molecular and Cellular Endocrinology 264, 197–203.
| Insulin-like growth factor-1 (IGF-1) system during follicle development in the bovine ovary: relationship among IGF-1, type 1 IGF receptor (IGFR-1) and pregnancy-associated plasma protein-A (PAPP-A).Crossref | GoogleScholarGoogle Scholar | 17116363PubMed |
Uzumcu, M, Kuhn, PE, Marano, JE, Armenti, AE, and Passantino, L (2006). Early postnatal methoxychlor exposure inhibits folliculogenesis and stimulates anti-Mullerian hormone production in the rat ovary. Journal of Endocrinology 191, 549–558.
| Early postnatal methoxychlor exposure inhibits folliculogenesis and stimulates anti-Mullerian hormone production in the rat ovary.Crossref | GoogleScholarGoogle Scholar |
van Wezel, IL, Umapathysivam, K, Tilley, WD, and Rodgers, RJ (1995). Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Molecular and Cellular Endocrinology 115, 133–140.
| Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 8824888PubMed |
Wang, W, Liu, H-L, Tian, W, Zhang, F-F, Gong, Y, Chen, J-W, Mao, D-G, and Shi, F-X (2010). Morphologic observation and classification criteria of atretic follicles in guinea pigs. Journal of Zhejiang University Science B 11, 307–314.
| Morphologic observation and classification criteria of atretic follicles in guinea pigs.Crossref | GoogleScholarGoogle Scholar | 20443208PubMed |
Weiner, HL, and Swain, JL (1989). Acidic fibroblast growth factor mRNA is expressed by cardiac myocytes in culture and the protein is localized to the extracellular matrix. Proceedings of the National Academy of Sciences of the United States of America 86, 2683–2687.
| Acidic fibroblast growth factor mRNA is expressed by cardiac myocytes in culture and the protein is localized to the extracellular matrix.Crossref | GoogleScholarGoogle Scholar | 2468157PubMed |
Woad, KJ, Hunter, MG, Mann, GE, Laird, M, Hammond, AJ, and Robinson, RS (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 | 21998077PubMed |
Wordinger, RJ, Brun-Zinkernagel, A-M, and Chang, I-FC (1993). Immunohistochemical localization of basic fibroblast growth factor (bFGF) within growing and atretic mouse ovarian follicles. Growth Factors 9, 279–289.
| Immunohistochemical localization of basic fibroblast growth factor (bFGF) within growing and atretic mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 8148157PubMed |
Yamamoto, S, Konishi, I, Nanbu, K, Komatsu, T, Mandai, M, Kuroda, H, Matsushita, K, and Mori, T (1997). Immunohistochemical localization of basic fibroblast growth factor (bFGF) during folliculogenesis in the human ovary. Gynecological Endocrinology 11, 223–230.
| Immunohistochemical localization of basic fibroblast growth factor (bFGF) during folliculogenesis in the human ovary.Crossref | GoogleScholarGoogle Scholar | 9272417PubMed |
Zhang, X, Ibrahimi, OA, Olsen, SK, Umemori, H, Mohammadi, M, and Ornitz, DM (2006). Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. Journal of Biological Chemistry 281, 15694–15700.
| Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family.Crossref | GoogleScholarGoogle Scholar |