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Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep

Year 2020, , 50 - 56, 23.03.2020
https://doi.org/10.32707/ercivet.697815

Abstract

Prostaglandins (PGs) in particular PGE2 by regulating luteal angiogenesis and steroidogenesis, play an important role in ovarian as well as luteal function in many mammalian species. While the direct luteotrophic effect of PGE2 has been studied intensively, there is still not much information available regarding the indirect effects of PGE2 in ovine corpus luteum (CL). Therefore, in the present study, possible effects of PGE2 stimulation on expression of some steroidogenic hormone receptors (ERα/ER1, ERβ/ER2 and PGR) and growth factors (IGF1, IGF2 and VEGF) were investigated using the isolated primary luteal and -microvascular endothelial cells. Neither the expression of steroidogenic hormone receptors (ERα/ER1, ERβ/ER2 and PGR) nor growth factors (IGF1, IGF2 and VEGF) were affected by PGE2 stimulation in primary luteal cells. However, there was statistically significant difference between the expression of both ERα/ER1 and ERβ/ER2 following PGE2 treatment in primary microvascular endothelial cells. Moreover, while the expression of IGF2 was upregulated, there was no statistically significant change between the expression of IGF1 and VEGF following PGE2 treatment in ovine primary microvascular endothelial cells. In conclusion, by regulating expression of estrogen receptors (ERα/ER1 and ERβ/ER2) and IGF2 in ovine luteal endothelial cells, PGE2 might involve in luteal angiogenesis and vasculogenesis during early luteal phase in sheep.

References

  • Boiti C, Zampini D, Zerani M, Guelfi G, Gobbetti A. Prostaglandin receptors and role of G protein-activated pathways on corpora lutea of pseudopregnant rabbit in vitro. J Endocrinol 2001; 168: 141-51.
  • Cárdenas H, Burke KA, Bigsby RM, Pope WF, Nephew KP. Estrogen receptor beta in the sheep ovary during the estrous cycle and early pregnancy. Biol Reprod 2001; 65(1): 128-34.
  • Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axinbeta-catenin signaling axis. Science 2005; 310: 1504-10.
  • Cha YI, DuBois RN. NSAIDs and cancer prevention: targets downstream of COX-2. Annu Rev Med 2007; 58: 239-52.
  • Channing CP, Schaerf FW, Anderson LD, Tsafriri A. Ovarian follicular and luteal physiology. Int Rev Physiol 1980; 22: 117-201.
  • Ford SP, Christenson K. Direct effects of oestradiol-17β and prostaglandin E-2 in protecting pig corpora lutea from a luteolytic dose of prostaglandin F2α. J Reprod Fertil 1991; 93(1): 203-9.
  • Fraser HM, Wulff C. Angiogenesis in the corpus luteum. Reprod Biol Endocrinol 2003; 1: 88.
  • Gram A, Grazul-Bilska AT, Boos A, Rahman NA, Kowalewski MP. Lipopolysaccharide disrupts gap junctional intercellular communication in an immortalized ovine luteal endothelial cell line. Toxicol In Vitro 2019; 60: 437-49.
  • Gram A, Latter S, Boos A, Hoffmann B, Kowalewski MP. Expression and functional implications of luteal endothelins in pregnant and non-pregnant dogs. Reproduction 2015; 150(5): 405-15.
  • Gram A, Tavares Pereira M, Boos A, Grazul-Bilska AT, Kowalewski MP. Luteal ANGPT-TIE system during selected stages of pregnancy, and normal and antigestagen-induced luteolysis in the dog. Reproduction 2018; 156(5): 451-61.
  • Grazul-Bilska AT, Navanukraw C, Johnson ML, Vonnahme KA, Ford SP, Reynolds LP, Redmer DA. Vascularity and expression of angiogenic factors in bovine dominant follicles of the first follicular wave. J Anim Sci 2007; 85(8): 1914-22.
  • Hahlin M, Dennefors B, Johanson C, Hamberger L. Luteotropic effects of prostaglandin E2 on the human corpus luteum of the menstrual cycle and early pregnancy. J Clin Endocrinol Metab 1988; 66(5): 909-14.
  • Hastie PM, Haresign W. A role for LH in the regulation of expression of mRNAs encoding components of the insulin-like growth factor (IGF) system in the ovine corpus luteum. Anim Reprod Sci 2006; 96(1-2): 196-209.
  • Janowski T, Fingerhut J, Kowalewski MP, Zdunczyk S, Domoslawska A, Jurczak A, Boos A, Schuler G, Hoffmann B. In vivo investigations on luteotropic activity of prostaglandins during early diestrus in nonpregnant bitches. Theriogenology 2014; 82 (6): 915-20.
  • Juengel JL, Nett TM, Anthony RV, Niswender GD. Effects of luteotrophic and luteolytic hormones on expression of mRNA encoding insulin-like growth factor I and growth hormone receptor in the ovine corpus luteum. J Reprod Fertil 1997; 110(2): 291-8.
  • Kowalewski MP, Fox B, Gram A, Boos A, Reichler I. Prostaglandin E-2 functions as a luteotrophic factor in the dog. Reproduction 2013; 145: 213-26.
  • Kowalewski MP, Schuler G, Taubert A, Engel E, Hoffmann B. Expression of cyclooxygenase 1 and 2 in the canine corpus luteum during diestrus. Theriogenology 2006; 66: 1423-30.
  • Martelli A, Palmerini MG, Russo V, Rinaldi C, Bernabo N, Di Giacinto O, Berardinelli P, Nottola SA, Macchiarelli G, Barboni B. Blood vessel remodeling in pig ovarian follicles during the periovulatory period: an immunohistochemistry and SEM-corrosion casting study. Reprod Biol Endocrinol 2009; 7: 72.
  • Namkoong S, Lee SJ, Kim CK, Kim YM, Chung HT, Lee H, Han JA, Ha KS, Kwon YG, Kim YM. Prostaglandin E2 stimulates angiogenesis by activating the nitric oxide/cGMP pathway in human umbilical vein endothelial cells. Exp Mol Med 2005; 37(6): 588-600.
  • Narumiya S, Sugimoto Y, Ushikubi F. Prostanoid receptors: Structures, properties, and functions. Physiol Rev 1999; 79: 1193-226.
  • Reynolds LP, Stigler J, Hoyer GL, Magness RR, Huie JM, Huecksteadt TP, Whysong GL, Behrman HR, Weems CW. Effect of PGE1 or PGE2 on PGF2α-induced luteolysis in nonbred ewes. Prostaglandins 1981; 21(6): 957-72.
  • Smith MF, McIntush EW, Smith GW. Mechanisms associated with corpus luteum development. J Anim Sci 1994; 72(7): 1857-72.
  • Smith WL, Dewitt DL. Prostaglandin endoperoxide H synthases-1 and -2. Adv Immunol 1996; 62: 167-215.
  • Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Nagura H. Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum reprod 1998; 13(4): 953-59.
  • Tai HH, Ensor CM, Tong M, Zhou H, Yan F. Prostaglandin catabolizing enzymes. Prostaglandins Other Lipid Mediat 2002; 68-69: 483-93.
  • Tomanek M, Pisselet C, Monget P, Madigou T, Thieulant ML, Monniaux D. Estrogen receptor protein and mRNA expression in the ovary of sheep. Mol Reprod Dev 1997; 48(1): 53-62.
  • Trau HA, Brännström M, Curry TE Jr, Duffy DM. Prostaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cells. Hum Reprod 2016; 31(2): 436-44.
  • Weems CW, Huie M, Hoyer GL, Magness RR, Whysong GL. Maternal recognition of pregnancy in ruminants. Davis WC, Shelton JN, Weems CW, ed. In: Characterization of the Bovine Immune System and the Genes Regulating Expression of Immunity With Particular Reference to Their Role in Disease Resistance. Pullman, WA: Washington State University Press 1985; pp. 193-210.
  • Weems CW, Weems YS, Randel RD. Prostaglandins and reproduction in female farm animals. Vet J 2006; 171: 206-28.
  • Weems CW, Weems YS, Vincent DL. Maternal recognition of pregnancy and maintenance of gestation in sheep. Enne G, Greppi GF, Lauria A, ed. In: Reproduction and Animal Breeding: Advances and Strategies. Proceedings XXX International Simposia Societa Italiana Zootechnica, Milan, Italy. Amsterdam, Holland: Elsevier Press; 1995; pp. 277-93.
  • Wiltbank MC, Mezera MA, Toledo MZ, Drum JN, Baez GM, García-Guerra A, Sartori R. Physiological mechanisms involved in maintaining the corpus luteum during the first two months of pregnancy. Anim Reprod 2018; 15 (1): 805-21.

Prostaglandin E2`nin Koyunlarda Erken Luteal Dönemde Korpus Luteum Üzerine Etkisi

Year 2020, , 50 - 56, 23.03.2020
https://doi.org/10.32707/ercivet.697815

Abstract

Prostaglandinler (PG'ler) özellikle de PGE2 luteal anjiyogenezis ve steroidogenezis’i düzenleyerek, birçok memeli türünde ovaryumun yanı sıra luteal fonksiyonun düzenlenmesinde önemli rol oynamaktadır. PGE2'nin direkt luteotropik etkisi yoğun olarak çalışılsa da PGE2'nin koyun korpus luteumundaki (CL) indirekt etkileri hakkında hala çok fazla bilgi bulunmamaktadır. Bu nedenle, bu çalışmada, korpus luteumdan izole edilen primer luteal ve mikrovasküler endotel hücreleri kullanılarak, PGE2 stimülasyonunun bazı steroidogenik hormon reseptörlerinin (ERα / ER1, ERβ / ER2 ve PGR) ve büyüme faktörlerinin (IGF1, IGF2 ve VEGF) ekspresyonu üzerindeki olası etkileri araştırılmıştır. Primer luteal hücrelerin PGE2 ile stimülasyonunu takiben ne steroidogenik hormon reseptörlerinin (ERα / ER1, ERβ / ER2 ve PGR) ne de büyüme faktörlerinin (IGF1, IGF2 ve VEGF) ekspresyonu etkilendi. Ancak, PGE2 ile primer mikrovasküler endotel hücrelerininin stimülasyonunu takiben ERα / ER1 ve ERβ / ER2`in ekspresyonu belirgin olarak arttı. Aynı zamanda, primer mikrovasküler endotel hücrelerinde IGF2’nin ekspresyonu upregüle olurken, IGF1 ve VEGF’in ekspresyonu PGE2 stimülasyonundan etkilenmedi. Sonuç olarak, PGE2 östrojen reseptörlerinin (ERα / ER1 and ERβ / ER2) ve IGF2`in ekspresyonunu düzenleyerek erken luteal dönemde luteal anjiyogenez ve vaskülogeneze katıldığı düşünülmektedir.

References

  • Boiti C, Zampini D, Zerani M, Guelfi G, Gobbetti A. Prostaglandin receptors and role of G protein-activated pathways on corpora lutea of pseudopregnant rabbit in vitro. J Endocrinol 2001; 168: 141-51.
  • Cárdenas H, Burke KA, Bigsby RM, Pope WF, Nephew KP. Estrogen receptor beta in the sheep ovary during the estrous cycle and early pregnancy. Biol Reprod 2001; 65(1): 128-34.
  • Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axinbeta-catenin signaling axis. Science 2005; 310: 1504-10.
  • Cha YI, DuBois RN. NSAIDs and cancer prevention: targets downstream of COX-2. Annu Rev Med 2007; 58: 239-52.
  • Channing CP, Schaerf FW, Anderson LD, Tsafriri A. Ovarian follicular and luteal physiology. Int Rev Physiol 1980; 22: 117-201.
  • Ford SP, Christenson K. Direct effects of oestradiol-17β and prostaglandin E-2 in protecting pig corpora lutea from a luteolytic dose of prostaglandin F2α. J Reprod Fertil 1991; 93(1): 203-9.
  • Fraser HM, Wulff C. Angiogenesis in the corpus luteum. Reprod Biol Endocrinol 2003; 1: 88.
  • Gram A, Grazul-Bilska AT, Boos A, Rahman NA, Kowalewski MP. Lipopolysaccharide disrupts gap junctional intercellular communication in an immortalized ovine luteal endothelial cell line. Toxicol In Vitro 2019; 60: 437-49.
  • Gram A, Latter S, Boos A, Hoffmann B, Kowalewski MP. Expression and functional implications of luteal endothelins in pregnant and non-pregnant dogs. Reproduction 2015; 150(5): 405-15.
  • Gram A, Tavares Pereira M, Boos A, Grazul-Bilska AT, Kowalewski MP. Luteal ANGPT-TIE system during selected stages of pregnancy, and normal and antigestagen-induced luteolysis in the dog. Reproduction 2018; 156(5): 451-61.
  • Grazul-Bilska AT, Navanukraw C, Johnson ML, Vonnahme KA, Ford SP, Reynolds LP, Redmer DA. Vascularity and expression of angiogenic factors in bovine dominant follicles of the first follicular wave. J Anim Sci 2007; 85(8): 1914-22.
  • Hahlin M, Dennefors B, Johanson C, Hamberger L. Luteotropic effects of prostaglandin E2 on the human corpus luteum of the menstrual cycle and early pregnancy. J Clin Endocrinol Metab 1988; 66(5): 909-14.
  • Hastie PM, Haresign W. A role for LH in the regulation of expression of mRNAs encoding components of the insulin-like growth factor (IGF) system in the ovine corpus luteum. Anim Reprod Sci 2006; 96(1-2): 196-209.
  • Janowski T, Fingerhut J, Kowalewski MP, Zdunczyk S, Domoslawska A, Jurczak A, Boos A, Schuler G, Hoffmann B. In vivo investigations on luteotropic activity of prostaglandins during early diestrus in nonpregnant bitches. Theriogenology 2014; 82 (6): 915-20.
  • Juengel JL, Nett TM, Anthony RV, Niswender GD. Effects of luteotrophic and luteolytic hormones on expression of mRNA encoding insulin-like growth factor I and growth hormone receptor in the ovine corpus luteum. J Reprod Fertil 1997; 110(2): 291-8.
  • Kowalewski MP, Fox B, Gram A, Boos A, Reichler I. Prostaglandin E-2 functions as a luteotrophic factor in the dog. Reproduction 2013; 145: 213-26.
  • Kowalewski MP, Schuler G, Taubert A, Engel E, Hoffmann B. Expression of cyclooxygenase 1 and 2 in the canine corpus luteum during diestrus. Theriogenology 2006; 66: 1423-30.
  • Martelli A, Palmerini MG, Russo V, Rinaldi C, Bernabo N, Di Giacinto O, Berardinelli P, Nottola SA, Macchiarelli G, Barboni B. Blood vessel remodeling in pig ovarian follicles during the periovulatory period: an immunohistochemistry and SEM-corrosion casting study. Reprod Biol Endocrinol 2009; 7: 72.
  • Namkoong S, Lee SJ, Kim CK, Kim YM, Chung HT, Lee H, Han JA, Ha KS, Kwon YG, Kim YM. Prostaglandin E2 stimulates angiogenesis by activating the nitric oxide/cGMP pathway in human umbilical vein endothelial cells. Exp Mol Med 2005; 37(6): 588-600.
  • Narumiya S, Sugimoto Y, Ushikubi F. Prostanoid receptors: Structures, properties, and functions. Physiol Rev 1999; 79: 1193-226.
  • Reynolds LP, Stigler J, Hoyer GL, Magness RR, Huie JM, Huecksteadt TP, Whysong GL, Behrman HR, Weems CW. Effect of PGE1 or PGE2 on PGF2α-induced luteolysis in nonbred ewes. Prostaglandins 1981; 21(6): 957-72.
  • Smith MF, McIntush EW, Smith GW. Mechanisms associated with corpus luteum development. J Anim Sci 1994; 72(7): 1857-72.
  • Smith WL, Dewitt DL. Prostaglandin endoperoxide H synthases-1 and -2. Adv Immunol 1996; 62: 167-215.
  • Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Nagura H. Cyclic changes of vasculature and vascular phenotypes in normal human ovaries. Hum reprod 1998; 13(4): 953-59.
  • Tai HH, Ensor CM, Tong M, Zhou H, Yan F. Prostaglandin catabolizing enzymes. Prostaglandins Other Lipid Mediat 2002; 68-69: 483-93.
  • Tomanek M, Pisselet C, Monget P, Madigou T, Thieulant ML, Monniaux D. Estrogen receptor protein and mRNA expression in the ovary of sheep. Mol Reprod Dev 1997; 48(1): 53-62.
  • Trau HA, Brännström M, Curry TE Jr, Duffy DM. Prostaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cells. Hum Reprod 2016; 31(2): 436-44.
  • Weems CW, Huie M, Hoyer GL, Magness RR, Whysong GL. Maternal recognition of pregnancy in ruminants. Davis WC, Shelton JN, Weems CW, ed. In: Characterization of the Bovine Immune System and the Genes Regulating Expression of Immunity With Particular Reference to Their Role in Disease Resistance. Pullman, WA: Washington State University Press 1985; pp. 193-210.
  • Weems CW, Weems YS, Randel RD. Prostaglandins and reproduction in female farm animals. Vet J 2006; 171: 206-28.
  • Weems CW, Weems YS, Vincent DL. Maternal recognition of pregnancy and maintenance of gestation in sheep. Enne G, Greppi GF, Lauria A, ed. In: Reproduction and Animal Breeding: Advances and Strategies. Proceedings XXX International Simposia Societa Italiana Zootechnica, Milan, Italy. Amsterdam, Holland: Elsevier Press; 1995; pp. 277-93.
  • Wiltbank MC, Mezera MA, Toledo MZ, Drum JN, Baez GM, García-Guerra A, Sartori R. Physiological mechanisms involved in maintaining the corpus luteum during the first two months of pregnancy. Anim Reprod 2018; 15 (1): 805-21.
There are 31 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Aykut Gram This is me

Publication Date March 23, 2020
Submission Date November 26, 2019
Published in Issue Year 2020

Cite

APA Gram, A. (2020). Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 17(1), 50-56. https://doi.org/10.32707/ercivet.697815
AMA Gram A. Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep. Erciyes Üniv Vet Fak Derg. March 2020;17(1):50-56. doi:10.32707/ercivet.697815
Chicago Gram, Aykut. “Effect of Prostaglandin E2 on Corpus Luteum Function During Early Luteal Phase in Sheep”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17, no. 1 (March 2020): 50-56. https://doi.org/10.32707/ercivet.697815.
EndNote Gram A (March 1, 2020) Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17 1 50–56.
IEEE A. Gram, “Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep”, Erciyes Üniv Vet Fak Derg, vol. 17, no. 1, pp. 50–56, 2020, doi: 10.32707/ercivet.697815.
ISNAD Gram, Aykut. “Effect of Prostaglandin E2 on Corpus Luteum Function During Early Luteal Phase in Sheep”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17/1 (March 2020), 50-56. https://doi.org/10.32707/ercivet.697815.
JAMA Gram A. Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep. Erciyes Üniv Vet Fak Derg. 2020;17:50–56.
MLA Gram, Aykut. “Effect of Prostaglandin E2 on Corpus Luteum Function During Early Luteal Phase in Sheep”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 17, no. 1, 2020, pp. 50-56, doi:10.32707/ercivet.697815.
Vancouver Gram A. Effect of Prostaglandin E2 on Corpus Luteum Function during Early Luteal Phase in Sheep. Erciyes Üniv Vet Fak Derg. 2020;17(1):50-6.