Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2012

Open Access 01-12-2012 | Research

Roles of prostaglandin F2alpha and hydrogen peroxide in the regulation of Copper/Zinc superoxide dismutase in bovine corpus luteum and luteal endothelial cells

Authors: Hai V Vu, Tomas J Acosta, Shin Yoshioka, Hironori Abe, Kiyoshi Okuda

Published in: Reproductive Biology and Endocrinology | Issue 1/2012

Login to get access

Abstract

Background

Prostaglandin F2alpha (PGF) induces luteolysis in cow by inducing a rapid reduction in progesterone production (functional luteolysis) followed by tissue degeneration (structural luteolysis). However the mechanisms of action of PGF remain unclear. Reactive oxygen species (ROS) play important roles in regulating the luteolytic action of PGF. The local concentration of ROS is controlled by superoxide dismutase (SOD), the main enzyme involved in the control of intraluteal ROS. Thus SOD seems to be involved in luteolysis process induced by PGF in cow.

Methods

To determine the dynamic relationship between PGF and ROS in bovine corpus luteum (CL) during luteolysis, we determined the time-dependent change of Copper/Zinc SOD (SOD1) in CL tissues after PGF treatment in vivo. We also investigated whether PGF and hydrogen peroxide (H2O2) modulates SOD1 expression and SOD activity in cultured bovine luteal endothelial cells (LECs) in vitro.

Results

Following administration of a luteolytic dose of PGF analogue (0 h) to cows at the mid-luteal stage, the expression of SOD1 mRNA and protein, and total SOD activity in CL tissues increased between 0.5 and 2 h, but fell below the initial (0 h) level at 24 h post-treatment. In cultured LECs, the expression of SOD1 mRNA was stimulated by PGF (1–10 microM) and H2O2 (10–100 microM) at 2 h (P<0.05). PGF and H2O2 increased SOD1 protein expression and total SOD activity at 2 h (P<0.05), whereas PGF and H2O2 inhibited SOD1 protein expressions and total SOD activity at 24 h (P<0.05). In addition, H2O2 stimulated PGF biosynthesis at 2 and 24 h in bovine LECs. Overall results indicate that, SOD is regulated by PGF and ROS in bovine LECs. SOD may play a role in controlling intraluteal PGF and ROS action during functional and structural luteolysis in cows.
Appendix
Available only for authorised users
Literature
1.
go back to reference Auletta FJ, Flint AP: Mechanisms controlling corpus luteum function in sheep, cows, nonhuman primates, and women especially in relation to the time of luteolysis. Endocr Rev. 1988, 9: 88-105. 10.1210/edrv-9-1-88.CrossRefPubMed Auletta FJ, Flint AP: Mechanisms controlling corpus luteum function in sheep, cows, nonhuman primates, and women especially in relation to the time of luteolysis. Endocr Rev. 1988, 9: 88-105. 10.1210/edrv-9-1-88.CrossRefPubMed
2.
go back to reference McCracken JA, Custer EE, Lamsa JC: Luteolysis: a neuroendocrine-mediated event. Physiol Rev. 1999, 79: 263-323.PubMed McCracken JA, Custer EE, Lamsa JC: Luteolysis: a neuroendocrine-mediated event. Physiol Rev. 1999, 79: 263-323.PubMed
3.
go back to reference Okuda K, Uenoyama Y, Lee KW, Sakumoto R, Skarzynski DJ: Progesterone stimulation by prostaglandin F2alpha involves the protein kinase C pathway in cultured bovine luteal cells. J Reprod Dev. 1998, 44: 79-84. 10.1262/jrd.44.79.CrossRef Okuda K, Uenoyama Y, Lee KW, Sakumoto R, Skarzynski DJ: Progesterone stimulation by prostaglandin F2alpha involves the protein kinase C pathway in cultured bovine luteal cells. J Reprod Dev. 1998, 44: 79-84. 10.1262/jrd.44.79.CrossRef
4.
go back to reference Pate JL, Condon WA: Regulation of steroidogenesis and cholesterol synthesis by prostaglandin F-2alpha and lipoproteins in bovine luteal cells. J Reprod Fertil. 1989, 87: 439-446. 10.1530/jrf.0.0870439.CrossRefPubMed Pate JL, Condon WA: Regulation of steroidogenesis and cholesterol synthesis by prostaglandin F-2alpha and lipoproteins in bovine luteal cells. J Reprod Fertil. 1989, 87: 439-446. 10.1530/jrf.0.0870439.CrossRefPubMed
5.
go back to reference Meidan R, Levy N, Kisliouk T, Podlovny L, Rusiansky M, Klipper E: The yin and yang of corpus luteum-derived endothelial cells: balancing life and death. Domest Anim Endocrinol. 2005, 29: 318-328. 10.1016/j.domaniend.2005.04.003.CrossRefPubMed Meidan R, Levy N, Kisliouk T, Podlovny L, Rusiansky M, Klipper E: The yin and yang of corpus luteum-derived endothelial cells: balancing life and death. Domest Anim Endocrinol. 2005, 29: 318-328. 10.1016/j.domaniend.2005.04.003.CrossRefPubMed
6.
go back to reference Lee SH, Acosta TJ, Yoshioka S, Okuda K: Prostaglandin F2alpha regulates the nitric oxide generating system in bovine luteal endothelial cells. J Reprod Dev. 2009, 55: 418-424. 10.1262/jrd.20205.CrossRefPubMed Lee SH, Acosta TJ, Yoshioka S, Okuda K: Prostaglandin F2alpha regulates the nitric oxide generating system in bovine luteal endothelial cells. J Reprod Dev. 2009, 55: 418-424. 10.1262/jrd.20205.CrossRefPubMed
7.
go back to reference Kato H, Sugino N, Takiguchi S, Kashida S, Nakamura Y: Roles of reactive oxygen species in the regulation of luteal function. Rev Reprod. 1997, 2: 81-83. 10.1530/ror.0.0020081.CrossRefPubMed Kato H, Sugino N, Takiguchi S, Kashida S, Nakamura Y: Roles of reactive oxygen species in the regulation of luteal function. Rev Reprod. 1997, 2: 81-83. 10.1530/ror.0.0020081.CrossRefPubMed
8.
go back to reference Sawada M, Carlson JC: Rapid plasma membrane changes in superoxide radical formation, fluidity, and phospholipase A2 activity in the corpus luteum of the rat during induction of luteolysis. Endocrinology. 1991, 128: 2992-2998. 10.1210/endo-128-6-2992.CrossRefPubMed Sawada M, Carlson JC: Rapid plasma membrane changes in superoxide radical formation, fluidity, and phospholipase A2 activity in the corpus luteum of the rat during induction of luteolysis. Endocrinology. 1991, 128: 2992-2998. 10.1210/endo-128-6-2992.CrossRefPubMed
9.
go back to reference Tanaka M, Miyazaki T, Tanigaki S, Kasai K, Minegishi K, Miyakoshi K, Ishimoto H, Yoshimura Y: Participation of reactive oxygen species in PGF2alpha-induced apoptosis in rat luteal cells. J Reprod Fertil. 2000, 120: 239-245.CrossRefPubMed Tanaka M, Miyazaki T, Tanigaki S, Kasai K, Minegishi K, Miyakoshi K, Ishimoto H, Yoshimura Y: Participation of reactive oxygen species in PGF2alpha-induced apoptosis in rat luteal cells. J Reprod Fertil. 2000, 120: 239-245.CrossRefPubMed
10.
go back to reference Sugino N, Karube-Harada A, Kashida S, Takiguchi S, Kato H: Reactive oxygen species stimulate prostaglandin F2alpha production in human endometrial stromal cells in vitro. Hum Reprod. 2001, 16: 1797-1801. 10.1093/humrep/16.9.1797.CrossRefPubMed Sugino N, Karube-Harada A, Kashida S, Takiguchi S, Kato H: Reactive oxygen species stimulate prostaglandin F2alpha production in human endometrial stromal cells in vitro. Hum Reprod. 2001, 16: 1797-1801. 10.1093/humrep/16.9.1797.CrossRefPubMed
11.
go back to reference Acosta TJ, Bah MB, Korzekwa A, Woclawek-Potocka I, Markiewicz W, Jaroszewski JJ, Okuda K, Skarzynski DJ: Acute changes in circulating concentrations of progesterone and nitric oxide and partial pressure of oxygen during prostaglandin F2alpha-induced luteolysis in cattle. J Reprod Dev. 2009, 55: 149-155. 10.1262/jrd.20133.CrossRefPubMed Acosta TJ, Bah MB, Korzekwa A, Woclawek-Potocka I, Markiewicz W, Jaroszewski JJ, Okuda K, Skarzynski DJ: Acute changes in circulating concentrations of progesterone and nitric oxide and partial pressure of oxygen during prostaglandin F2alpha-induced luteolysis in cattle. J Reprod Dev. 2009, 55: 149-155. 10.1262/jrd.20133.CrossRefPubMed
12.
go back to reference Fridovich I: Superoxide radical and superoxide dismutases. Annu Rev Biochem. 1995, 64: 97-112. 10.1146/annurev.bi.64.070195.000525.CrossRefPubMed Fridovich I: Superoxide radical and superoxide dismutases. Annu Rev Biochem. 1995, 64: 97-112. 10.1146/annurev.bi.64.070195.000525.CrossRefPubMed
13.
14.
go back to reference Sugino N, Nakamura Y, Takeda O, Ishimatsu M, Kato H: Changes in activities of superoxide dismutase and lipid peroxide in corpus luteum during pregnancy in rats. J Reprod Fertil. 1993, 97: 347-351. 10.1530/jrf.0.0970347.CrossRefPubMed Sugino N, Nakamura Y, Takeda O, Ishimatsu M, Kato H: Changes in activities of superoxide dismutase and lipid peroxide in corpus luteum during pregnancy in rats. J Reprod Fertil. 1993, 97: 347-351. 10.1530/jrf.0.0970347.CrossRefPubMed
15.
go back to reference Sugino N, Takiguchi S, Kashida S, Takayama H, Yamagata Y, Nakamura Y, Kato H: Suppression of intracellular superoxide dismutase activity by antisense oligonucleotides causes inhibition of progesterone production by rat luteal cells. Biol Reprod. 1999, 61: 1133-1138. 10.1095/biolreprod61.4.1133.CrossRefPubMed Sugino N, Takiguchi S, Kashida S, Takayama H, Yamagata Y, Nakamura Y, Kato H: Suppression of intracellular superoxide dismutase activity by antisense oligonucleotides causes inhibition of progesterone production by rat luteal cells. Biol Reprod. 1999, 61: 1133-1138. 10.1095/biolreprod61.4.1133.CrossRefPubMed
16.
go back to reference Miyamoto Y, Skarzynski DJ, Okuda K: Is tumor necrosis factor alpha a trigger for the initiation of endometrial prostaglandin F2alpha release at luteolysis in cattle?. Biol Reprod. 2000, 62: 1109-1115. 10.1095/biolreprod62.5.1109.CrossRefPubMed Miyamoto Y, Skarzynski DJ, Okuda K: Is tumor necrosis factor alpha a trigger for the initiation of endometrial prostaglandin F2alpha release at luteolysis in cattle?. Biol Reprod. 2000, 62: 1109-1115. 10.1095/biolreprod62.5.1109.CrossRefPubMed
17.
go back to reference Klipper E, Gilboa T, Levy N, Kisliouk T, Spanel-Borowski K, Meidan R: Characterization of endothelin-1 and nitric oxide generating systems in corpus luteum-derived endothelial cells. Reproduction. 2004, 128: 463-473. 10.1530/rep.1.00271.CrossRefPubMed Klipper E, Gilboa T, Levy N, Kisliouk T, Spanel-Borowski K, Meidan R: Characterization of endothelin-1 and nitric oxide generating systems in corpus luteum-derived endothelial cells. Reproduction. 2004, 128: 463-473. 10.1530/rep.1.00271.CrossRefPubMed
18.
go back to reference Acosta TJ, Yoshioka S, Komiyama J, Lee SH, Grazul-Bilska AT, Skarzynski DJ, Okuda K: Effects of storage and passage of bovine luteal endothelial cells on endothelin-1 and prostaglandin F2alpha production. J Reprod Dev. 2007, 53: 473-480. 10.1262/jrd.18142.CrossRefPubMed Acosta TJ, Yoshioka S, Komiyama J, Lee SH, Grazul-Bilska AT, Skarzynski DJ, Okuda K: Effects of storage and passage of bovine luteal endothelial cells on endothelin-1 and prostaglandin F2alpha production. J Reprod Dev. 2007, 53: 473-480. 10.1262/jrd.18142.CrossRefPubMed
19.
go back to reference Lee S, Acosta TJ, Nakagawa Y, Okuda K: Role of nitric oxide in the regulation of superoxide dismutase and prostaglandin F2alpha production in bovine luteal endothelial cells. J Reprod Dev. 2010, 56: 454-459. 10.1262/jrd.10-013K.CrossRefPubMed Lee S, Acosta TJ, Nakagawa Y, Okuda K: Role of nitric oxide in the regulation of superoxide dismutase and prostaglandin F2alpha production in bovine luteal endothelial cells. J Reprod Dev. 2010, 56: 454-459. 10.1262/jrd.10-013K.CrossRefPubMed
20.
go back to reference Wong H, Anderson WD, Cheng T, Riabowol KT: Monitoring mRNA expression by polymerase chain reaction: the "primer-dropping" method. Anal Biochem. 1994, 223: 251-258. 10.1006/abio.1994.1581.CrossRefPubMed Wong H, Anderson WD, Cheng T, Riabowol KT: Monitoring mRNA expression by polymerase chain reaction: the "primer-dropping" method. Anal Biochem. 1994, 223: 251-258. 10.1006/abio.1994.1581.CrossRefPubMed
21.
go back to reference Okuda K, Kasahara Y, Murakami S, Takahashi H, Woclawek-Potocka I, Skarzynski DJ: Interferon-tau blocks the stimulatory effect of tumor necrosis factor-alpha on prostaglandin F2alpha synthesis by bovine endometrial stromal cells. Biol Reprod. 2004, 70: 191-197.CrossRefPubMed Okuda K, Kasahara Y, Murakami S, Takahashi H, Woclawek-Potocka I, Skarzynski DJ: Interferon-tau blocks the stimulatory effect of tumor necrosis factor-alpha on prostaglandin F2alpha synthesis by bovine endometrial stromal cells. Biol Reprod. 2004, 70: 191-197.CrossRefPubMed
22.
go back to reference Osnes T, Sandstad O, Skar V, Osnes M, Kierulf P: Total protein in common duct bile measured by acetonitrile precipitation and a micro bicinchoninic acid (BCA) method. Scand J Clin Lab Invest. 1993, 53: 757-763. 10.3109/00365519309092582.CrossRefPubMed Osnes T, Sandstad O, Skar V, Osnes M, Kierulf P: Total protein in common duct bile measured by acetonitrile precipitation and a micro bicinchoninic acid (BCA) method. Scand J Clin Lab Invest. 1993, 53: 757-763. 10.3109/00365519309092582.CrossRefPubMed
23.
go back to reference Labarca C, Paigen K: A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980, 102: 344-352. 10.1016/0003-2697(80)90165-7.CrossRefPubMed Labarca C, Paigen K: A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980, 102: 344-352. 10.1016/0003-2697(80)90165-7.CrossRefPubMed
24.
go back to reference Riley JC, Behrman HR: In vivo generation of hydrogen peroxide in the rat corpus luteum during luteolysis. Endocrinology. 1991, 128: 1749-1753. 10.1210/endo-128-4-1749.CrossRefPubMed Riley JC, Behrman HR: In vivo generation of hydrogen peroxide in the rat corpus luteum during luteolysis. Endocrinology. 1991, 128: 1749-1753. 10.1210/endo-128-4-1749.CrossRefPubMed
25.
go back to reference Muzykantov VR: Targeting of superoxide dismutase and catalase to vascular endothelium. J Control Release. 2001, 71: 1-21. 10.1016/S0168-3659(01)00215-2.CrossRefPubMed Muzykantov VR: Targeting of superoxide dismutase and catalase to vascular endothelium. J Control Release. 2001, 71: 1-21. 10.1016/S0168-3659(01)00215-2.CrossRefPubMed
26.
go back to reference Korzekwa AJ, Okuda K, Woclawek-Potocka I, Murakami S, Skarzynski DJ: Nitric oxide induces apoptosis in bovine luteal cells. J Reprod Dev. 2006, 52: 353-361. 10.1262/jrd.17092.CrossRefPubMed Korzekwa AJ, Okuda K, Woclawek-Potocka I, Murakami S, Skarzynski DJ: Nitric oxide induces apoptosis in bovine luteal cells. J Reprod Dev. 2006, 52: 353-361. 10.1262/jrd.17092.CrossRefPubMed
27.
go back to reference Juarez JC, Manuia M, Burnett ME, Betancourt O, Boivin B, Shaw DE, Tonks NK, Mazar AP, Donate F: Superoxide dismutase 1 (SOD1) is essential for H2O2-mediated oxidation and inactivation of phosphatases in growth factor signaling. Proc Natl Acad Sci U S A. 2008, 105: 7147-7152. 10.1073/pnas.0709451105.PubMedCentralCrossRefPubMed Juarez JC, Manuia M, Burnett ME, Betancourt O, Boivin B, Shaw DE, Tonks NK, Mazar AP, Donate F: Superoxide dismutase 1 (SOD1) is essential for H2O2-mediated oxidation and inactivation of phosphatases in growth factor signaling. Proc Natl Acad Sci U S A. 2008, 105: 7147-7152. 10.1073/pnas.0709451105.PubMedCentralCrossRefPubMed
28.
go back to reference Sander VA, Piehl L, Facorro GB, Rubin de Celis E, Motta AB: Regulation of functional and regressing stages of corpus luteum development in mice. Role of reactive oxygen species. Reprod Fertil Dev. 2008, 20: 706-769.CrossRef Sander VA, Piehl L, Facorro GB, Rubin de Celis E, Motta AB: Regulation of functional and regressing stages of corpus luteum development in mice. Role of reactive oxygen species. Reprod Fertil Dev. 2008, 20: 706-769.CrossRef
29.
go back to reference Nakamura T, Sakamoto K: Reactive oxygen species up-regulates cyclooxygenase-2, p53, and Bax mRNA expression in bovine luteal cells. Biochem Biophys Res Commun. 2001, 284: 203-210. 10.1006/bbrc.2001.4927.CrossRefPubMed Nakamura T, Sakamoto K: Reactive oxygen species up-regulates cyclooxygenase-2, p53, and Bax mRNA expression in bovine luteal cells. Biochem Biophys Res Commun. 2001, 284: 203-210. 10.1006/bbrc.2001.4927.CrossRefPubMed
30.
go back to reference Suhara T, Fukuo K, Sugimoto T, Morimoto S, Nakahashi T, Hata S, Shimizu M, Ogihara T: Hydrogen peroxide induces up-regulation of Fas in human endothelial cells. J Immunol. 1998, 160: 4042-4047.PubMed Suhara T, Fukuo K, Sugimoto T, Morimoto S, Nakahashi T, Hata S, Shimizu M, Ogihara T: Hydrogen peroxide induces up-regulation of Fas in human endothelial cells. J Immunol. 1998, 160: 4042-4047.PubMed
31.
go back to reference Raw RE, Silvia WJ: Activity of phospholipase C and release of prostaglandin F2 alpha by endometrial tissue from ovariectomized ewes receiving progesterone and estradiol. Biol Reprod. 1991, 44: 404-412. 10.1095/biolreprod44.3.404.CrossRefPubMed Raw RE, Silvia WJ: Activity of phospholipase C and release of prostaglandin F2 alpha by endometrial tissue from ovariectomized ewes receiving progesterone and estradiol. Biol Reprod. 1991, 44: 404-412. 10.1095/biolreprod44.3.404.CrossRefPubMed
32.
go back to reference Lee J, McCracken JA, Stanley JA, Nithy TK, Banu SK, Arosh JA: Intraluteal Prostaglandin Biosynthesis and Signaling Are Selectively Directed Towards PGF2alpha During Luteolysis but Towards PGE2 During the Establishment of Pregnancy in Sheep. Biol Reprod. 2012, 87: 97-10.1095/biolreprod.112.100438.CrossRefPubMed Lee J, McCracken JA, Stanley JA, Nithy TK, Banu SK, Arosh JA: Intraluteal Prostaglandin Biosynthesis and Signaling Are Selectively Directed Towards PGF2alpha During Luteolysis but Towards PGE2 During the Establishment of Pregnancy in Sheep. Biol Reprod. 2012, 87: 97-10.1095/biolreprod.112.100438.CrossRefPubMed
33.
go back to reference Wu XM, Sawada M, Carlson JC: Stimulation of phospholipase A2 by xanthine oxidase in the rat corpus luteum. Biol Reprod. 1992, 47: 1053-1058. 10.1095/biolreprod47.6.1053.CrossRefPubMed Wu XM, Sawada M, Carlson JC: Stimulation of phospholipase A2 by xanthine oxidase in the rat corpus luteum. Biol Reprod. 1992, 47: 1053-1058. 10.1095/biolreprod47.6.1053.CrossRefPubMed
34.
go back to reference Buttke TM, Sandstrom PA: Oxidative stress as a mediator of apoptosis. Immunol Today. 1994, 15: 7-10. 10.1016/0167-5699(94)90018-3.CrossRefPubMed Buttke TM, Sandstrom PA: Oxidative stress as a mediator of apoptosis. Immunol Today. 1994, 15: 7-10. 10.1016/0167-5699(94)90018-3.CrossRefPubMed
Metadata
Title
Roles of prostaglandin F2alpha and hydrogen peroxide in the regulation of Copper/Zinc superoxide dismutase in bovine corpus luteum and luteal endothelial cells
Authors
Hai V Vu
Tomas J Acosta
Shin Yoshioka
Hironori Abe
Kiyoshi Okuda
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2012
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-10-87

Other articles of this Issue 1/2012

Reproductive Biology and Endocrinology 1/2012 Go to the issue