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Effects of angiogenin on granulosa and theca cell function in cattle

Published online by Cambridge University Press:  20 October 2016

J. L. Dentis ,
N. B. Schreiber ,
A. M. Burress  and
L. J. Spicer
J. L. Dentis
Affiliation:
Department of Animal Science, Oklahoma State University, Stillwater, OK 74078, USA
N. B. Schreiber
Affiliation:
Department of Animal Science, Oklahoma State University, Stillwater, OK 74078, USA
A. M. Burress
Affiliation:
Department of Animal Science, Oklahoma State University, Stillwater, OK 74078, USA
L. J. Spicer*
Affiliation:
Department of Animal Science, Oklahoma State University, Stillwater, OK 74078, USA
*
†E-mail: [email protected]
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Abstract

Angiogenin is a member of the ribonuclease A superfamily of proteins that has been implicated in stimulating angiogenesis but whether angiogenin can directly affect ovarian granulosa or theca cell function is unknown. Therefore, the objective of these studies was to determine the effect of angiogenin on proliferation and steroidogenesis of bovine granulosa and theca cells. In experiments 1 and 2, granulosa cells from small (1 to 5 mm diameter) follicles and theca cells from large (8 to 22 mm diameter) follicles were cultured to evaluate the dose-response effect of recombinant human angiogenin on steroidogenesis. At 30 and 100 ng/ml, angiogenin inhibited (P<0.05) granulosa cell progesterone production and theca cell androstenedione production but did not affect (P>0.10) granulosa cell estradiol production or theca cell progesterone production, and did not affect numbers of granulosa or theca cells. In experiments 3 and 4, granulosa and theca cells from both small and large follicles were cultured with 300 ng/ml of angiogenin to determine if size of follicle influenced responses to angiogenin. At 300 ng/ml, angiogenin increased large follicle granulosa cell proliferation but decreased small follicle granulosa cell progesterone and estradiol production and large follicle theca cell progesterone production. In experiments 5 and 6, angiogenin stimulated (P<0.05) proliferation and DNA synthesis in large follicle granulosa cells. In experiment 7, 300 ng/ml of angiogenin increased (P<0.05) CYP19A1 messenger RNA (mRNA) abundance in granulosa cells but did not affect CYP11A1 mRNA abundance in granulosa or theca cells and did not affect CYP17A1 mRNA abundance in theca cells. We conclude that angiogenin appears to target both granulosa and theca cells in cattle, but additional research is needed to further understand the mechanism of action of angiogenin in granulosa and theca cells, as well as its precise role in folliculogenesis.

Keywords

angiogenin (ANG)granulosa cellstheca cellsIGF1tumor necrosis factor α (TNFα)
Type
Research Article
Information
animal , Volume 11 , Issue 5 , May 2017 , pp. 811 - 819
Copyright
© The Animal Consortium 2016 

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References

Aad, PY, Voge, JL, Santiago, CA, Malayer, JR and Spicer, LJ 2006. Real-time RT-PCR quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: effects of hormones in vitro. Domestic Animal Endocrinology 31, 357–372.Google Scholar
Appelmann, I, Liersch, R, Kessler, T, Mesters, RM and Berdel, WE 2010. Angiogenesis inhibition in cancer therapy: platelet-derived growth factor (PDGF) and vascular endothelial growth factor (VEGF) and their receptors: biological function and role in malignancy. Recent Results in Cancer Research 180, 51–81.CrossRefGoogle Scholar
Bond, MD, Strydom, DJ and Vallee, BL 1993. Characterization and sequencing of rabbit pig and mouse angiogenins. Biochimica et Biophysica Acta 1162, 177–186.Google Scholar
Bond, MD and Vallee, BL 1988. Isolation of bovine angiogenin using a placental ribonuclease inhibitor binding assay. Biochemistry 27, 6282–6287.CrossRefGoogle ScholarPubMed
Chang, S-I, Jeong, G-B, Park, S-H, Ahn, B-C, Choi, J-D, Chae, Q, Namgoong, SK and Chung, S-I 1997. Detection, quantitation, and localization of bovine angiogenin by immunological assays. Biochemical and Biophysical Research Communications 232, 323–327.Google Scholar
Davoren, JB, Hsueh, JW and Li, CH 1985. Somatomedin C augments FSH-induced differentiation of cultured rat granulosa cells. Am. J. Physiol 249, E26–E33.Google Scholar
Fett, JW, Strydom, DJ, Lobb, RR, Alderman, EM, Bethune, JL, Riordan, JF and Vallee, BL 1985. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24, 5480–5486.Google Scholar
Gao, X and Xu, Z 2008. Mechanisms of action of angiogenin. Acta Biochimica et Biophysica Sinica 40, 619–624.Google Scholar
Gho, YS, Yoon, WH and Chae, CB 2002. Antiplasmin activity of a peptide that binds to the receptor-binding site of angiogenin. Journal of Biological Chemistry 277, 9690–9694.Google Scholar
Grado-Ahuir, JA, Aad, PY and Spicer, LJ 2011. New insights into the pathogenesis of cystic follicles in cattle: microarray analysis of gene expression in granulosa cells. Journal of Animal Science 89, 1769–1786.Google Scholar
Gupta, SK, Haigh, BJ, Griffin, FJ and Wheeler, TT 2013. The mammalian secreted RNases: mechanisms of action in host defence. Innate Immunology 19, 86–97.Google Scholar
Hatzi, E and Badet, J 1999. Expression of receptors for human angiogenin in vascular smooth muscle cells. European Journal of Biochemistry 260, 825–832.Google Scholar
Hu, GF, Riordan, JF and Vallee, BL 1997. A putative angiogenin receptor in angiogenin-responsive human endothelial cells. Proceedings of the National Academy of Sciences of the United States of America 94, 2204–2209.Google Scholar
Jiang, JY, Macchiarelli, G, Miyabayashi, K and Sato, E 2002. Follicular microvasculature in the porcine ovary. Cell and Tissue Research 310, 93–101.Google Scholar
Jiang, JY, Macchiarelli, G, Tsang, BK and Sato, E 2003. Capillary angiogenesis and degeneration in bovine ovarian antral follicles. Reproduction 125, 211–223.Google Scholar
Kawano, Y, Zeineh Hasan, K, Fukuda, J, Mine, S and Miyakawa, I 2003. Production of vascular endothelial growth factor and angiogenic factor in human follicular fluid. Molecular and Cellular Endocrinology 202, 19–23.Google Scholar
Kim, HM, Kang, DK, Kim, HY, Kang, SS and Chang, SI 2007. Angiogenin-induced protein kinase B/Akt activation is necessary for angiogenesis but is independent of nuclear translocation of angiogenin in HUVE cells. Biochemical and Biophysical Research Communications 352, 509–513.Google Scholar
Koga, K, Osuga, Y, Tsutsumi, O, Momoeda, M, Suenaga, A, Kuga, K, Fujiwara, T, Takai, Y, Yano, T and Taketani, Y 2000. Evidence for the presence of angiogenin in human follicular fluid and the up-regulation of its production by human chorionic gonadotropin and hypoxia. Journal of Clinical Endocrinology and Metabolism 85, 3352–3355.Google ScholarPubMed
Lagaly, DV, Aad, PY, Grado-Ahuir, JA, Hulsey, LB and Spicer, LJ 2008. Role of adiponectin in regulating ovarian granulosa and theca cell function. Molecular and Cellular Endocrinology 284, 38–45.Google Scholar
Langhout, DJ, Spicer, LJ and Geisert, RD 1991. Development of a culture system for bovine granulosa cells: effects of growth hormone, estradiol, and gonadotrophins on cell proliferation, steroidogenesis, and protein synthesis. Journal of Animal Science 69, 3321–3334.Google Scholar
Lee, HS, Lee, I-S, Kang, T-C, Jeong, GB and Chang, S-I 1999. Angiogenin is involved in morphological changes and angiogenesis in the ovary. Biochemical and Biophysical Research Communications 257, 182–186.Google Scholar
Li, S and Hu, GF 2012. Emerging role of angiogenin in stress response and cell survival under adverse conditions. Journal of Cellular Physiology 227, 2822–2826.Google Scholar
Liu, S, Yu, D, Xu, ZP, Riordan, JF and Hu, GF 2001. Angiogenin activates Erk1/2 in human umbilical vein endothelial cells. Biochemical and Biophysical Research Communications 287, 305–310.Google Scholar
Maes, P, Damart, D, Rommens, C, Montreuil, J, Spik, G and Tartar, A 1988. The complete amino acid sequence of bovine milk angiogenin. FEBS Letters 241, 41–45.Google Scholar
Malamitsi-Puchner, A, Sarandakou, A, Baka, SG, Tziotis, J, Rizos, D, Hassiakos, D and Creatsas, G 2001. Concentrations of angiogenic factors in follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: association with oocyte maturity and fertilization. Fertility and Sterility 76, 98–101.Google Scholar
Moonmanee, T, Navanukraw, C, Uriyapongson, S, Kraisoon, A, Aiumlamai, S, Guntaprom, S, Rittirod, T, Borowicz, PP and Redmer, DA 2013. Relationships among vasculature, mitotic activity, and endothelial nitric oxide synthase (eNOS) in bovine antral follicles of the first follicular wave. Domestic Animal Endocrinology 45, 11–21.CrossRefGoogle ScholarPubMed
Ott, L 1977. An Introduction to Statistical Methods and Data Analysis. Duxbury Press, North Scituate, MA.Google Scholar
Premzl, M 2014. Comparative genomic analysis of eutherian ribonuclease A genes. Molecular Genetics and Genomics 289, 161–167.CrossRefGoogle ScholarPubMed
Przybylski, M 2009. A review of the current research on the role of bFGF and VEGF in angiogenesis. Journal of Wound Care 12, 516–519.CrossRefGoogle Scholar
Redmer, DA and Reynolds, LP 1996. Angiogenesis in the ovary. Reviews of Reproduction 1, 182–192.Google Scholar
Saikia, M, Jobava, R, Parisien, M, Putnam, A, Krokowski, D, Gao, XH, Guan, BJ, Yuan, Y, Jankowsky, E, Feng, Z, Hu, GF, Pusztai-Carey, M, Gorla, M, Sepuri, NB, Pan, T and Hatzoglou, M 2014. Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Molecular and Cellular Biology 34, 2450–2463.Google Scholar
Schreiber, NB and Spicer, LJ 2012. Effects of fibroblast growth factor 9 (FGF9) on steroidogenesis and gene expression and control of FGF9 mRNA in bovine granulosa cells. Endocrinology 153, 4491–4501.CrossRefGoogle ScholarPubMed
Shapiro, R, Strydom, DJ, Olson, KA and Vallee, BL 1987. Isolation of angiogenin from normal human plasma. Biochemistry 26, 5141–5146.Google Scholar
Soncin, F, Shapiro, R and Fett, JW 1994. A cell-surface proteoglycan mediates human adenocarcinoma HT-29 cell adhesion to human angiogenin. Journal of Biological Chemistry 269, 8999–9005.Google Scholar
Spicer, LJ and Aad, P 2007. Insulin-like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle-stimulating hormone and IGF2 receptor. Biology of Reproduction 77, 18–27.Google Scholar
Spicer, LJ, Aad, PY, Allen, DT, Mazerbourg, S, Payne, AH and Hsueh, AJ 2008. Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biology of Reproduction 78, 243–253.Google Scholar
Spicer, LJ and Chamberlain, CS 1998. Influence of cortisol on insulin- and insulin-like growth factor 1 (IGF-1)-induced steroid production and on IGF-1 receptors in cultured bovine granulosa cells and thecal cells. Endocrine 9, 153–161.CrossRefGoogle ScholarPubMed
Spicer, LJ, Chamberlain, CS and Maciel, SM 2002. Influence of gonadotropins on insulin- and insulin-like growth factor-I (IGF-I)-induced steroid production by bovine granulosa cells. Domestic Animal Endocrinology 22, 237–254.Google Scholar
Spicer, LJ and Stewart, RE 1996. Interaction among bovine somatotropin, insulin, and gonadotropins on steroid production by bovine granulosa and thecal cells. Journal of Dairy Science 79, 813–821.Google Scholar
Stewart, RE, Spicer, LJ, Hamilton, TD and Keefer, BE 1995. Effects of insulin-like growth factor I and insulin on proliferation and on basal and luteinizing hormone-induced steroidogenesis of bovine thecal cells: involvement of glucose and receptors for insulin-like growth factor I and luteinizing hormone. Journal of Animal Science 73, 3719–3731.Google Scholar
Tello-Montoliu, A, Patel, JV and Lip, GYH 2006. Angiogenin: a review of the pathophysiology and potential clinical applications. Journal of Thrombosis and Haemostasis 4, 1864–1874.Google Scholar
Tsuji, T, Sun, Y, Kishimoto, K, Olson, KA, Liu, S, Hirukawa, S and Hu, GF 2005. Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Research 65, 1352–1360.CrossRefGoogle Scholar
Ucuzian, AA, Gassman, AA, East, AT and Greisler, HP 2010. Molecular mediators of angiogenesis. Journal of Burn Care and Research 31, 158–175.Google Scholar
Voge, JL, Santiago, CA, Aad, PY, Goad, DW, Malayer, JR and Spicer, LJ 2004. Effect of insulin-like growth factors (IGF), FSH, and leptin on IGF-binding-protein mRNA expression in bovine granulosa and theca cells: quantitative detection by real-time PCR. Peptides 25, 2195–2203.Google Scholar
Xia, W, Fu, W, Cai, X, Wang, M, Chen, H, Xing, W, Wang, Y, Zou, M, Xu, T and Xu, D 2015. Angiogenin promotes U87MG cell proliferation by activating NF-κB signaling pathway and downregulating its binding partner FHL3. PLoS One 10, e0116983.Google Scholar
Xu, Z, Monti, DM and Hu, G 2001. Angiogenin activates human umbilical artery smooth muscle cells. Biochemical and Biophysical Research Communications 285, 909–914.Google Scholar
Yamada, O, Abe, M, Takehana, K, Hiraga, T, Iwasa, K and Hiratsuka, T 1995. Microvascular changes during the development of follicles in bovine ovaries: a study of corrosion casts by scanning electron microscopy. Archives of Histology Cytology 58, 567–574.Google Scholar
Zhang, G, Garmey, JC and Veldhuis, JD 2000. Interactive stimulation by luteinizing hormone and insulin of the steroidogenic acute regulatory (StAR) protein and 17α-hydroxylase/17,20-lyase (CYP17) genes in porcine theca cells. Endocrinology 141, 2735–2742.Google Scholar
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