Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0146
Animal Reproduction (AR)
Original Article

Transforming growth factor-beta family members are regulated during induced luteolysis in cattle

Cristina Sangoi Haas; Monique Tomazele Rovani; Gustavo Freitas Ilha; Kalyne Bertolin; Juliana Germano Ferst; Alessandra Bridi; Vilceu Bordignon; Raj Duggavathi; Alfredo Quites Antoniazzi; Paulo Bayard Dias Gonçalves; Bernardo Garziera Gasperin

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Abstract

Abstract: The transforming growth factors beta (TGFβ) are local factors produced by ovarian cells which, after binding to their receptors, regulate follicular deviation and ovulation. However, their regulation and function during corpus luteum (CL) regression has been poorly investigated. The present study evaluated the mRNA regulation of some TGFβ family ligands and their receptors in the bovine CL during induced luteolysis in vivo. On day 10 of the estrous cycle, cows received an injection of prostaglandin F2α (PGF) and luteal samples were obtained from separate groups of cows (n= 4-5 cows per time-point) at 0, 2, 12, 24 or 48 h after treatment. Since TGF beta family comprises more than 30 ligands, we focused in some candidates genes such as activin receptors (ACVR-1A, -1B, -2A, -2B) AMH, AMHR2, BMPs (BMP-1, -2, -3, -4, -6 and -7), BMP receptors (BMPR-1A, -1B and -2), inhibin subunits (INH-A, -BA, -BB) and betaglycan (TGFBR3). The mRNA levels of BMP4, BMP6 and INHBA were higher at 2 h after PGF administration (P<0.05) in comparison to 0 h. The relative mRNA abundance of BMP1, BMP2, BMP3, BMP4, BMP6, ACVR1B, INHBA and INHBB was upregulated up to 12 h post PGF (P<0.05). On the other hand, TGFBR3 mRNA that codes for a reservoir of ligands that bind to TGF-beta receptors, was lower at 48 h. In conclusion, findings from this study demonstrated that genes encoding several TGFβ family members are expressed in a time-specific manner after PGF administration.

Keywords

cattle, luteolysis, corpus luteum

References

Almeida FR, Costermans NGJ, Soede NM, Bunschoten A, Keijer J, Kemp B, Teerds KJ. Presence of anti-Müllerian hormone (AMH) during follicular development in the porcine ovary. PLoS One. 2018;13(7):e0197894. http://dx.doi.org/10.1371/journal.pone.0197894. PMid:30063719.

Berisha B, Schilffarth S, Kenngott R, Sinowatz F, Meyer HH, Schams D. Expression of lymphangiogenic vascular endothelial growth factor family members in bovine corpus luteum. Anat Histol Embryol. 2013;42(4):292-303. http://dx.doi.org/10.1111/ahe.12016. PMid:23126445.

Canty-Laird E, Carré G-A, Mandon-Pépin B, Kadler KE, Fabre S. First evidence of bone morphogenetic protein 1 expression and activity in sheep ovarian follicles. Biol Reprod. 2010;83(1):138-46. http://dx.doi.org/10.1095/biolreprod.109.082115. PMid:20357269.

Cikos S, Bukovska A, Koppel J. Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Mol Biol. 2007;8(1):113. http://dx.doi.org/10.1186/1471-2199-8-113. PMid:18093344.

Drost M, Savio JD, Barros CM, Badinga L, Thatcher WW. Ovariectomy by colpotomy in cows. J Am Vet Med Assoc. 1992;200(3):337-9. PMid:1548167.

Erickson GF, Shimasaki S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol. 2003;1(1):9. http://dx.doi.org/10.1186/1477-7827-1-9. PMid:12741959.

Farberov S, Meidan R. Thrombospondin-1 affects bovine luteal function via transforming growth factor-beta1-dependent and independent actions. Biol Reprod. 2016;94(1):25. http://dx.doi.org/10.1095/biolreprod.115.135822. PMid:26658711.

Gangrade BK, Gotcher ED, Davis JS, May JV. The secretion of transforming growth factor-beta by bovine luteal cells in vitro. Mol Cell Endocrinol. 1993;93(2):117-23. http://dx.doi.org/10.1016/0303-7207(93)90114-Y. PMid:8349022.

Gasperin BG, Ferreira R, Rovani MT, Bordignon V, Duggavathi R, Buratini J, Oliveira JF, Goncalves PB. Expression of receptors for BMP15 is differentially regulated in dominant and subordinate follicles during follicle deviation in cattle. Anim Reprod Sci. 2014;144(3-4):72-8. http://dx.doi.org/10.1016/j.anireprosci.2013.12.002. PMid:24388700.

Ge G, Greenspan DS. BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J Cell Biol. 2006;175(1):111-20. http://dx.doi.org/10.1083/jcb.200606058. PMid:17015622.

Glister C, Kemp CF, Knight PG. Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction. 2004;127(2):239-54. http://dx.doi.org/10.1530/rep.1.00090. PMid:15056790.

Gregson E, Webb R, Sheldrick EL, Campbell BK, Mann GE, Liddell S, Sinclair KD. Molecular determinants of a competent bovine corpus luteum: first-vs final-wave dominant follicles. Reproduction. 2016;151(6):563-75. http://dx.doi.org/10.1530/REP-15-0415. PMid:26940100.

Groome NP, Illingworth PJ, O’Brien M, Pai R, Rodger FE, Mather JP, McNeilly AS. Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab. 1996;81(4):1401-5. PMid:8636341.

Hayashi K-G, Ushizawa K, Hosoe M, Takahashi T. Differential genome-wide gene expression profiling of bovine largest and second-largest follicles: identification of genes associated with growth of dominant follicles. Reprod Biol Endocrinol. 2010;8(1):11. http://dx.doi.org/10.1186/1477-7827-8-11. PMid:20132558.

Hou X, Arvisais EW, Jiang C, Chen D, Roy SK, Pate JL, Hansen TR, Rueda BR, Davis JS. Prostaglandin F2alpha stimulates the expression and secretion of transforming growth factor B1 via induction of the early growth response 1 gene (EGR1) in the bovine corpus luteum. Mol Endocrinol. 2008;22(2):403-14. http://dx.doi.org/10.1210/me.2007-0272. PMid:17916653.

Ilha GF, Rovani MT, Gasperin BG, Ferreira R, Macedo MP, Andrade O No, Duggavathi R, Bordignon V, Gonçalves PB. Regulation of anti-Müllerian hormone and its receptor expression around follicle deviation in cattle. Reprod Domest Anim. 2016;51(2):188-94. http://dx.doi.org/10.1111/rda.12662. PMid:26815645.

Jaatinen R, Bondestam J, Raivio T, Hildén K, Dunkel L, Groome N, Ritvos O. Activation of the bone morphogenetic protein signaling pathway induces inhibin βB-subunit mRNA and secreted inhibin B levels in cultured human granulosa-luteal cells. J Clin Endocrinol Metab. 2002;87(3):1254-61. http://dx.doi.org/10.1210/jcem.87.3.8314. PMid:11889196.

Jaatinen R, Rosen V, Tuuri T, Ritvos O. Identification of ovarian granulosa cells as a novel site of expression for bone morphogenetic protein-3 (BMP-3/osteogenin) and regulation of BMP-3 messenger ribonucleic acids by chorionic gonadotropin in cultured human granulosa-luteal cells. J Clin Endocrinol Metab. 1996;81(11):3877-82. PMid:8923832.

Jasuja R, Ge G, Voss NG, Lyman-Gingerich J, Branam AM, Pelegri FJ, Greenspan DS. Bone morphogenetic protein 1 prodomain specifically binds and regulates signaling by bone morphogenetic proteins 2 and 4. J Biol Chem. 2007;282(12):9053-62. http://dx.doi.org/10.1074/jbc.M610929200. PMid:17255107.

Kayani AR, Glister C, Knight PG. Evidence for an inhibitory role of bone morphogenetic protein(s) in the follicular-luteal transition in cattle. Reproduction. 2009;137(1):67-78. http://dx.doi.org/10.1530/REP-08-0198. PMid:18936084.

Knight PG, Glister C. TGF-β superfamily members and ovarian follicle development. Reproduction. 2006;132(2):191-206. http://dx.doi.org/10.1530/rep.1.01074. PMid:16885529.

Lee W-S, Otsuka F, Moore RK, Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod. 2001;65(4):994-9. http://dx.doi.org/10.1095/biolreprod65.4.994. PMid:11566718.

Liu J, Kuulasmaa T, Kosma VM, Butzow R, Vanttinen T, Hyden-Granskog C, Voutilainen R. Expression of betaglycan, an inhibin coreceptor, in normal human ovaries and ovarian sex cord-stromal tumors and its regulation in cultured human granulosa-luteal cells. J Clin Endocrinol Metab. 2003;88(10):5002-8. http://dx.doi.org/10.1210/jc.2003-030704. PMid:14557487.

Maroni D, Davis JS. TGFB1 disrupts the angiogenic potential of microvascular endothelial cells of the corpus luteum. J Cell Sci. 2011;124(Pt 14):2501-10. http://dx.doi.org/10.1242/jcs.084558. PMid:21693577.

Miyamoto A, Shirasuna K, Sasahara K. Local regulation of corpus luteum development and regression in the cow: impact of angiogenic and vasoactive factors. Domest Anim Endocrinol. 2009;37(3):159-69. http://dx.doi.org/10.1016/j.domaniend.2009.04.005. PMid:19592192.

Myers M, Gay E, McNeilly AS, Fraser HM, Duncan WC. In vitro evidence suggests activin-A may promote tissue remodeling associated with human luteolysis. Endocrinology. 2007;148(8):3730-9. http://dx.doi.org/10.1210/en.2007-0244. PMid:17478557.

Neuvians TP, Schams D, Berisha B, Pfaffl MW. Involvement of pro-inflammatory cytokines, mediators of inflammation, and basic fibroblast growth factor in prostaglandin F2alpha-induced luteolysis in bovine corpus luteum. Biol Reprod. 2004;70(2):473-80. http://dx.doi.org/10.1095/biolreprod.103.016154. PMid:14561657.

Nio-Kobayashi J, Narayanan R, Giakoumelou S, Boswell L, Hogg K, Duncan WC. Expression and localization of inhibitor of differentiation (ID) proteins during tissue and vascular remodelling in the human corpus luteum. Mol Hum Reprod. 2013;19(2):82-92. http://dx.doi.org/10.1093/molehr/gas052. PMid:23160862.

Nio-Kobayashi J, Trendell J, Giakoumelou S, Boswell L, Nicol L, Kudo M, Sakuragi N, Iwanaga T, Duncan WC. Bone morphogenetic proteins are mediators of luteolysis in the human corpus luteum. Endocrinology. 2015;156(4):1494-503. http://dx.doi.org/10.1210/en.2014-1704. PMid:25635621.

O’Connell AR, McNatty KP, Hurst PR, Spencer TE, Bazer FW, Reader KL, Johnstone PD, Davis GH, Juengel JL. Activin A and follistatin during the oestrous cycle and early pregnancy in ewes. J Endocrinol. 2016;228(3):193-203. http://dx.doi.org/10.1530/JOE-15-0367. PMid:26733604.

Orisaka M, Tajima K, Mizutani T, Miyamoto K, Tsang BK, Fukuda S, Yoshida Y, Kotsuji F. Granulosa cells promote differentiation of cortical stromal cells into theca cells in the bovine ovary. Biol Reprod. 2006;75(5):734-40. http://dx.doi.org/10.1095/biolreprod.105.050344. PMid:16914692.

Rajesh G, Paul A, Mishra S, Bharati J, Thakur N, Mondal T, Soren S, Harikumar S, Narayanan K, Chouhan V, Bag S, Das BC, Singh G, Maurya VP, Sharma GT, Sarkar M. Expression and functional role of Bone Morphogenetic Proteins (BMPs) in cyclical corpus luteum in buffalo (Bubalus bubalis). Gen Comp Endocrinol. 2017;240:198-213. http://dx.doi.org/10.1016/j.ygcen.2016.10.016. PMid:27815159.

Rico C, Médigue C, Fabre S, Jarrier P, Bontoux M, Clément F, Monniaux D. Regulation of anti-Müllerian hormone production in the cow: a multiscale study at endocrine, ovarian, follicular, and granulosa cell levels. Biol Reprod. 2011;84(3):560-71. http://dx.doi.org/10.1095/biolreprod.110.088187. PMid:21076084.

Rovani MT, Ilha GF, Gasperin BG, Nobrega JE Jr, Siddappa D, Glanzner WG, Antoniazzi AQ, Bordignon V, Duggavathi R, Goncalves PBD. Prostaglandin F2alpha-induced luteolysis involves activation of Signal transducer and activator of transcription 3 and inhibition of AKT signaling in cattle. Mol Reprod Dev. 2017;84(6):486-94. http://dx.doi.org/10.1002/mrd.22798. PMid:28337827.

Shi F-T, Cheung AP, Klausen C, Huang H-F, Leung PC. Growth differentiation factor 9 reverses activin A suppression of steroidogenic acute regulatory protein expression and progesterone production in human granulosa-lutein cells. J Clin Endocrinol Metab. 2010;95(10):E172-80. http://dx.doi.org/10.1210/jc.2010-0477. PMid:20660033.

Shi J, Yoshino O, Osuga Y, Koga K, Hirota Y, Nose E, Nishii O, Yano T, Taketani Y. Bone morphogenetic protein-2 (BMP-2) increases gene expression of FSH receptor and aromatase and decreases gene expression of LH receptor and StAR in human granulosa cells. Am J Reprod Immunol. 2011;65(4):421-7. http://dx.doi.org/10.1111/j.1600-0897.2010.00917.x. PMid:20825377.

Shirasuna K, Nitta A, Sineenard J, Shimizu T, Bollwein H, Miyamoto A. Vascular and immune regulation of corpus luteum development, maintenance, and regression in the cow. Domest Anim Endocrinol. 2012;43(2):198-211. http://dx.doi.org/10.1016/j.domaniend.2012.03.007. PMid:22560178.

Shirasuna K, Sasahara K, Matsui M, Shimizu T, Miyamoto A. Prostaglandin F2alpha differentially affects mRNA expression relating to angiogenesis, vasoactivation and prostaglandins in the early and mid corpus luteum in the cow. J Reprod Dev. 2010;56(4):428-36. http://dx.doi.org/10.1262/jrd.10-004O. PMid:20484870.

Silva JRV, van den Hurk R, van Tol HTA, Roelen BAJ, Figueiredo JR. Gene expression and protein localisation for activin-A, follistatin and activin receptors in goat ovaries. J Endocrinol. 2004;183(2):405-15. http://dx.doi.org/10.1677/joe.1.05756. PMid:15531728.

Skarzynski DJ, Okuda K. Inter- and intra-cellular mechanisms of prostaglandin F2alpha action during corpus luteum regression in cattle. Soc Reprod Fertil Suppl. 2010;67:305-24. PMid:21755681.

Yamashita H, Murayama C, Takasugi R, Miyamoto A, Shimizu T. BMP-4 suppresses progesterone production by inhibiting histone H3 acetylation of StAR in bovine granulosa cells in vitro. Mol Cell Biochem. 2011;348(1-2):183. PMid:21072679.

Zhang H, Klausen C, Zhu H, Chang H-M, Leung PCK. BMP4 and BMP7 suppress StAR and progesterone production via ALK3 and SMAD1/5/8-SMAD4 in human granulosa-lutein cells. Endocrinology. 2015;156(11):4269-80. http://dx.doi.org/10.1210/en.2015-1494. PMid:26302112.
 

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