Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2019-0087
Animal Reproduction (AR)
Congress Paper

Contribution of the immune system to follicle differentiation, ovulation and early corpus luteum formation

Noof Abdulrahman, Trudee Fair

Downloads: 1
Views: 1538

Abstract

Much of what we know about the involvement of the immune system in periovulatory follicle differentiation, ovulation and subsequent formation of the corpus luteum in cattle is drawn from the findings of studies in several mammalian livestock species. By integrating published histological data from cattle, sheep and pigs and referring back to the more comprehensive knowledge bank that exists for mouse and humans we can sketch out the key cells of the immune system and the cytokines and growth factors that they produce that are involved in follicle differentiation and luteinization, ovulation and early follicle development. These contributions are reviewed and the key findings, discussed.

Keywords

bovine, ovulation, corpus luteum.

References

Angelucci, S, Ciavardelli D, Di Giuseppe F, Eleuterio E, Sulpizio M, Tiboni GM, Giampietro F, Palumbo P, Di Ilio C. 2006. Proteome analysis of human follicular fluid. Biochim Biophys Acta, 1764(11):1775-1785.

Arosh, JA, Sakhila KB, McCracken JA. 2016. Novel concepts on the role of prostaglandins on luteal maintenance and maternal recognition and establishment of pregnancy in ruminants. J Dairy Sci, 99(7):5926-5940.

Atli MO, Bender RO, Mehta V, Bastos MR, Luo W, Vezina CM Wiltbank MC. 2012. Patterns of gene expression in the bovine corpus luteum following repeated intrauterine infusions of low doses of prostaglandin F2alpha1. Biol Reprod, 86(4):1-13.

Aust G, Heider SU, Hmeidan FA, Blumenauer V, Spanel-Borowski K. 2000. Eosinophils in the human corpus luteum: the role of RANTES and eotaxin in eosinophil attraction into periovulatory structures. Mol Hum Reprod, 6(12):1085-1091.

Bauer M, Reibiger I, Spanel-Borowski K. 2001. Leucocyte proliferation in the bovine corpus luteum. Reproduction, 121(2):297-305.

Benyo DF, Pate JL. 1992. Tumor necrosis factor-α alters bovine luteal cell synthetic capacity and viability. Endocrinology, 130:854-860.

Berisha B, Steffl M, Amselgruber W, Schams D. 2006. Changes in Fibroblast growth factor 2 and its receptors in bovine follicles before and after GnRH application and after ovulation. Reproduction 131(2):319-329.

Berisha B, Schams D, Rodler D, Pfaffl MW. 2016. Angiogenesis in The Ovary - The most important regulatory event for follicle and corpus luteum development and function in cow - An Overview. Anat Histol Embryol, 45(2):124-130.

Berisha B, Schams D, Rodler D, Sinowatz F, Pfaffl MW. 2017. Expression pattern of HIF1alpha and vasohibins during follicle maturation and corpus luteum function in the bovine ovary. Reprod Domest Anim, 52(1):130-139.

Best CL, Pudney J, Welch WR, BurgerN Hill JA. 1996. Localization and characterization of white blood cell populations within the human ovary throughout the menstrual cycle and menopause. Hum Reprod, 11(4):790-797.

Brännström M, Enskog A. 2002. Leukocyte networks and ovulation. J Reprod Immunol, 57(1-2):47-60.

Cannon, MJ, Petroff MG, Pate JL. 2003. Effects of prostaglandin F2alpha and progesterone on the ability of bovine luteal cells to stimulate T lymphocyte proliferation. Biol Reprod, 69(2):695-700.

Castilho ACS, Dalanezi FM, Franchi FF, Price CA, Ferreira JCP, Trevisol E, Buratini J. 2019. expression of fibroblast growth factor 22 (FGF22) and Its receptor, FGFR1B, during development and regression of bovine corpus luteum. Theriogenology, 125:1-5.

Cavender JL, Murdoch WJ. 1988. Morphological studies of the microcirculatory system of periovulatory ovine follicles. Biol Reprod, 39(4):989-997.

Cherry JA, Hou X, Rueda BR, Davis JS, Townson DH. 2008. Microvascular endothelial cells of the bovine corpus luteum: a comparative examination of the estrous cycle and pregnancy. J Reprod Dev, 54(3):183-191.

Choudhary E, Sen A, Inskeep KE, Flores JA. 2005. Developmental sensitivity of the bovine corpus luteum to prostaglandin F2alpha (PGF2alpha) and endothelin-1 (ET-1): Is ET-1 a mediator of the luteolytic actions of PGF2alpha or a tonic inhibitor of progesterone secretion?. Biol Reprod, 72(3):633-642.

Christenson LK., Gunewardena S, Hong X, Spitschak M, Baufeld A, Vanselow J. 2013. research resource: preovulatory LH surge effects on follicular theca and granulosa transcriptomes. Mol Endocrinol, 27(7):1153-1171.

Conti M, Hsieh M, Park JY, Su YQ. 2006. Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol, 20(4):715-723.

Davis TL, Pate JL. 2007. bovine luteal cells stimulate proliferation of major histocompatibility nonrestricted gamma delta T cells. Biol Reprod, 77(6):914-922.

Dieleman SJ, Kruip TA, Fontijne P, de Jong WH, van der Weyden GC. 1983. Changes in oestradiol, progesterone and testosterone concentrations in follicular fluid and in the micromorphology of preovulatory bovine follicles relative to the peak of luteinizing hormone. J Endocrinol, 97(1):31-42.

Duras M, Brzósko E, Kotwica J. 2005. Influence of progesterone, pregnenolone and 17beta-hydroxyprogesterone on the function of bovine luteal cells treated with luteinizing hormone, noradrenaline and prostaglandin E2. Pol J Vet Sci, 8(2):113-119.

Fair T. 2003. follicular oocyte growth and acquisition of developmental competence. Anim Reprod Sci, 78(3-4):203-216.

Fair T. 2010. Mammalian oocyte development: checkpoints for competence. Reprod Fertil Dev, 22(1):13-20.

Farin, CE, Moeller CL, Sawyer HR, Gamboni F, Niswender GD. 1986. Morphometric analysis of cell types in the ovine corpus luteum throughout the estrous cycle. Biol Reprod, 35(5):1299-1308.

Fraser HM. 2006. Regulation of the ovarian follicular vasculature. Reprod Biol Endocrinol, 18(4):1477-7827.

Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM. 2009. polarization of tumor-associated neutrophil phenotype by TGF-Beta: “N1” versus “N2” TAN. Cancer Cell, 16(3):183-194.

Fukumatsu Y, Katabuchi H, Naito M, Takeya M, Takahashi K, Okamura K. 1992. Effect of macrophages on proliferation of granulosa cells in the ovary in rats. J Reprod Fertil, 96(1):241-249.

Gaytán F, Morales C. García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE. 1998. Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod, 59(2):417-425.

Gilbert I, Claude R, Dieleman S, Blondin P, Sirard MA. 2011. Transcriptional effect of the LH surge in bovine granulosa cells during the peri-ovulation period. Reproduction, 141(2):193-205.

Girsh E, Milvae RA, Wang W, Meidan R. 1996. effect of endothelin-1 on bovine luteal cell function: role in prostaglandin F2alpha-induced antisteroidogenic action. Endocrinology, 137(4):1306-1312.

Giuliodori MJ, R. Magnasco P, Becu-Villalobos D, Lacau-Mengido IM, Risco CA, de la Sota RL. 2013. Clinical Endometritis in an argentinean herd of dairy cows: risk factors and reproductive efficiency. J Dairy Sci, 96(1):210-218.

Hansen TR, Henkes LK, Ashley RL, Bott RC, Antoniazzi AQ, Han H. 2010. Endocrine actions of interferon-tau in ruminants. Soc Reprod Fertil Suppl, 67:325-340.

Hatzirodos N, Irving-Rodgers HF, Hummitzsch K, Harland ML, Morris SE, Rodgers RJ. 2014. Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes. BMC Genomics, 15(24):1471-2164.

Hojo T, Akihiro O, Lee SH, Acosta TJ, Okuda K. 2010. effects of tumor necrosis factor α and interferon γ on the viability and MRNA expression of TNF receptor type I in endothelial cells from the bovine corpus luteum. J Reprod Dev, 56(5):515-519.

Ireland JJ, Mihm M, Austin E, Diskin MG, Roche JF. 2000. Historical perspective of turnover of dominant follicles during the bovine estrous cycle: key concepts, studies, advancements, and terms. J Dairy Sci, 83(7):1648-1658.

 

Jiemtaweeboon S, Shirasuna K, Nitta A, Kobayashi A, Schuberth HJ, Shimizu T, Miyamoto A. 2011. Evidence That polymorphonuclear neutrophils infiltrate into the developing corpus luteum and promote angiogenesis with interleukin-8 in the cow. Reprod Biol Endocrinol, 79(9):1477-7827.

Kliem H, Rodler D, Ulbrich SE, Sinowatz F, Berisha B, Meyer HHD, Schams D. 2013. Dexamethasone-induced eosinopenia is associated with lower progesterone production in cattle. Reprod Domest Anim, 48(1):137-148.

Klipper E, Gilboa T, Levy N, Kisliouk T, Spanel-Borowski K, Meidan R. 2004. Characterization of endothelin-1 and nitric oxide generating systems in corpus luteum-derived endothelial cells. Reproduction, 128(4):463-73.

Klipper E, Levit A, Mastich Y, Berisha B, Schams D, Meidan R. 2010. Induction of endothelin-2 expression by luteinizing hormone and hypoxia: possible role in bovine corpus luteum formation. Endocrinology, 151(4):1914-1922.

Koch AE, Polverini PJ, Kunkel SL, Harlow LA, DiPietro LA, Elner VM, Elner SG, Strieter RM. 1992. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science, 258(5089):1798-1801.

Komatsu K, Manabe N, Kiso M, Shimabe M, Miyamoto H. 2003. Changes in localization of immune cells and cytokines in corpora lutea during luteolysis in murine ovaries. J Exp Zool A Comp Exp Biol, Part A, 296(2):152-159.

Korzekwa A, Murakami S, Wocławek-Potocka I, Bah MM, Okuda K, Skarzynski DJ. 2008. The influence of tumor necrosis factor α (TNF) on the secretory function of bovine corpus luteum: TNF and its receptors expression during the estrous cycle. Reprod Biol, 8(3):245-262.

Kuhnert F, Tam BYY, Sennino B, Gray JT, Yuan J, Jocson A, Nayak NR, Mulligan RC, McDonald D, Kuo CJ. 2008. Soluble receptor-mediated selective inhibition of vegfr and pdgfrbeta signaling during physiologic and tumor angiogenesis. Proc Natl Acad Sci U S A, 105(29):10185-10190.

Lawler DF, Hopkins J, Watson ED. 1999. Immune cell populations in the equine corpus luteum throughout the oestrous cycle and early pregnancy: an immunohistochemical and flow cytometric study. J Reprod Fertil, 117(2):281-290.

Lawrence TS., Dekel N, Beers WH. 1980. Binding of human chorionic gonadotropin by rat cumuli oophori and granulosa cells: a comparative study. Endocrinology, 106(4):1114-1118.

Lei ZM, Chegini N, Rao CV. 1991. Quantitative cell composition of human and bovine corpora lutea from various reproductive states. Biol Reprod, 44(6):1148-1156.

Leroy JLMR, Valckx SDM, Jordaens L, De Bie J, Desmet KLJ, Van Hoeck V, Britt JH, Marei WF, Bols PEJ. 2015. Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model. Reprod Fertil Dev, 27(4):693-703.

Li Q, Jimenez-Krassel F, Ireland JJ, and Smith GW. 2009. Gene expression profiling of bovine preovulatory follicles: gonadotropin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process. Reproduction, 137(2):297-307.

Lobel BL, Levy E. 1968. Enzymic correlates of development, secretory function and regression of follicles and corpora lutea in the bovine ovary. Acta Endocrinol (Copenh), Suppl, 132:5-63.

Mamluk R, Levy N, Rueda B, Davis JS, Meidan R. 1999. Characterization and regulation of type a endothelin receptor gene expression in bovine luteal cell types. Endocrinology, 140(5):2110-2116.

Mishra S, Palai T. 2014. Steroidogenesis in luteal cell: a critical pathway for progesterone production. J Invest Biochem, 3(4):170-172.

Miyamoto A, Shirasuna K, Shimizu T, Bollwein H, Schams D. 2010. Regulation of corpus luteum development and maintenance: specific roles of angiogenesis and action of prostaglandin F2alpha. Soc Reprod Fertil Suppl, 67:289-304.

Murdoch WJ, Steadman LE. 1991. Investigations concerning the relationship of ovarian eosinophilia to ovulation and luteal function in the sheep. Am J Reprod Immunol, 25(2):81-87.

Murdoch WJ, McCormick RJ. 1993. Mechanisms and Physiological implications of leucocyte chemoattraction into periovulatory ovine follicles. Reproduction, 97(2):375-380.

Murdoch WJ, Gottsch ML. 2003. Proteolytic mechanisms in the ovulatory folliculo-luteal transformation. Connect Tissue Res, 44(1):50-57.

Niswender GD., Juengel JL, McGuire WJ, Belfiore CF, Wiltbank MC. 1994. Luteal function: the estrous cycle and early pregnancy. Biol Reprod, 50(2):239-247.

Oakley OR, Kim HY, El-Amouri I, Lin PCP, Cho J, Bani-Ahmad M, Ko C. 2010. periovulatory leukocyte infiltration in the rat ovary. Endocrinology, 151(9):4551-4559.

Okuda K, Sakumoto R, Uenoyama Y, Berisha B, Miyamoto A, Schams D. 1999. Tumor necrosis factor alpha receptors in microvascular endothelial cells from bovine corpus luteum. Biolf Reprod, 61(4):1017-1022.

Okuda K, Sakumoto R. 2003. Multiple roles of TNF super family members in corpus luteum function. Reprod Biol Endocrinol, 1:95.

Okuda K, Korzekwa A, Shibaya M, Murakami S, Nishimura R, Tsubouchi M, Woclawek-Potocka I, Skarzynski DJ. 2004. Progesterone is a suppressor of apoptosis in bovine luteal cells. Biol of Reprod, 71(6):2065-2071.

Park, JY, Su YQ, Ariga M, Law E, Jin CSL, Conti M. 2004. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science, 303(5658):682-684.

Pate JL. 2003. Lives in the Balance: responsiveness of the corpus luteum to uterine and embryonic signals. Reprod Suppl, 61:207-217.

Pate JL, Toyokawa K, Walusimbi S, Brzezicka E. 2010. The interface of the immune and reproductive systems in the ovary: lessons learned from the corpus luteum of domestic animal models. Am J Reprod Immunol, 64(4):275-286.

Penny LA, Armstrong D, Bramley TA, Webb R, Collins RA, Watson ED. 1999. Immune cells and cytokine production in the bovine corpus luteum throughout the oestrous cycle and after induced luteolysis. J Reprod Fertil, 115(1):87-96.

Petroff MG, Petroff BK, Pate JL. 2001. Mechanisms of cytokine-induced death of cultured bovine luteal cells. Reproduction, 121(5):753-760.

Petrovská M, Dimitrov DG, Michael SD. 1996. Quantitative changes in macrophage distribution in normal mouse ovary over the course of the estrous cycle examined with an image analysis system. Am J Reprod Immunol, 36(3):175-783.

Poole DH, Pate JL. 2012. Luteal microenvironment directs resident T lymphocyte function in cows. Biol Reprod, 86(2):1-10.

Poulsen LC, Englund ALM, Wissing MLM, Yding Andersen C, Borup R, Grøndahl ML. 2019. Human granulosa cells function as innate immune cells executing an inflammatory reaction during ovulation: a microarray analysis. Mol Cell Endocrinol, 486:34-46.

Ramadan AA, Selim SA, Hassan HM, Wahba MA. 2001. Immune regulation of ovarian function in buffaloes (Bubalus Bubalus). Theriogenology, 55(2):661-669.

Reibiger I, Spanel-Borowski K. 2000. ‘Difference in Localization of Eosinophils and Mast Cells in the Bovine Ovary’. J Reprod Fertil, 118(2):243-249.

Reynolds LP, Redmer DA. 1999. Growth and development of the corpus luteum. J Reprod Fertil Suppl, 54:181-191.

Reynolds LP, Grazul-Bilska AT, Redmer DA. 2000. Angiogenesis in the corpus luteum. Endocrine, 12(1):1-9.

Reynolds LP, Redmer DA. 1999. Growth and Development of the Corpus Luteum. J Reprod Fertil Suppl, 54:181-191.

Richani D, Gilchrist RB. 2018. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update, 24(1):1-14.

Richards, JAS, Liu Z, Shimada M. 2008. Immune-like mechanisms in ovulation. Trends Endocrinol Metab, 19(6):191-196.

Richards JS, Russell DL, Ochsner S, Espey LL. 2002. Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol, 64:69-92.

Ritter LJ, Sugimura S, Gilchrist RB. 2015. Oocyte induction of EGF responsiveness in somatic cells is associated with the acquisition of porcine oocyte developmental competence. Endocrinology, 156(6):2299-2312.

Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG, Mann GE. 2009. Angiogenesis and vascular function in the ovary. Reproduction, 138(6):869-881.

Rohm F, Spanel-Borowski K, Eichler W, Aust G. 2002. Correlation between expression of selectins and migration of eosinophils into the bovine ovary during the periovulatory period. Cell and Tissue Res, 309(2):313-322.

Rosiansky-Sultan M, Klipper E, Spanel-Borowski K, Meidan R. 2006. Inverse relationship between nitric oxide synthases and endothelin-1 synthesis in bovine corpus luteum: interactions at the level of luteal endothelial cell. Endocrinology, 147(11):5228-5235.

Rueda BR, Hendry IR, Hendry III WJ, Stormshak F, Slayden OD, Davis JS. 2000. Decreased Progesterone Levels and progesterone receptor antagonists promote apoptotic cell death in bovine luteal cells. Biol Reprod, 62(2):269-276.

Sakumoto R, Berisha B, Kawate N, Schams D, Okuda K. 2000. Tumor necrosis factor-alpha and its receptor in bovine corpus luteum throughout the estrous cycle. Biol Reprod, 62(1):192-199.

Schams D, Kosmann M, Berisha B, Amselgruber WM, Miyamoto A. 2001. Stimulatory and synergistic effects of luteinising hormone and insulin like growth factor 1 on the secretion of vascular endothelial growth factor and progesterone of cultured bovine granulosa cells. Exp Clin Endocrinol Diabetes, 109(3):155-162.

Schruefer R, Lutze N, Schymeinsky J, Walzog B. 2005. Human Neutrophils Promote angiogenesis by a paracrine feedforward mechanism involving endothelial interleukin-8. Am J Physiol Heart Circ Physiol, 288(3):H1186-1192.

Sheldon IM, Price SB, Cronin J, Gilbert RO, Gadsby JE. 2009. Mechanisms of Infertility associated with clinical and subclinical endometritis in high producing dairy cattle. Reprod Domest Anim, 3(Suppl 44):1-9.

Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS. 2006. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol, 20(6):1352-1365.

Shirasuna K, Nitta A, Sineenard J, Shimizu T, Bollwein H, Miyamoto A. 2012a. Vascular and immune regulation of corpus luteum development, maintenance, and regression in the cow. Domest Anim Endocrinol, 43(2):198-211.

Shirasuna K, Jiemtaweeboon S, Raddatz S, Nitta A, Schuberth HJ, Bollwein H, Shimizu T, Miyamoto A. 2012b. Rapid Accumulation of polymorphonuclear neutrophils in the corpus luteum during prostaglandin F(2α)-induced luteolysis in the cow. PloS One, 7(1):e29054.

Shirasuna K, Asaoka A, Acosta TJ, Wijayagunawardane MPB, Ohtani M, Hayashi M, Matsui M, Miyamoto A. 2004. Real-time relationships in intraluteal release among prostaglandin F2alpha, endothelin-1, and angiotensin II during spontaneous luteolysis in the Cow. Biol Reprod, 71(5):1706-1711.

Skarzynski DJ, Okuda K. 1999. Sensitivity of bovine corpora lutea to prostaglandin F2alpha Is dependent on progesterone, oxytocin, and prostaglandins. Biol Reprod, 60:1292-1298.

Smith, GW, Meidan R. 2014. Ever-Changing Cell interactions during the life span of the corpus luteum: relevance to luteal regression. Reprod Biol, 14(2):75-82. Spanel-Borowski K, Rahner P, Ricken AM. 1997. Immunolocalization of CD18-positive cells in the bovine Ovary. J Reprod Fertil, 111(2):197-205.

Spanel-Borowski K. 2011. Ovulation as danger signaling event of innate immunity. Mol Cell Endocrinol, 333(1):1-7.

Standaert FE, Zamora CS, Chew BP. 1991. Quantitative and qualitative changes in blood leukocytes in the porcine ovary. Am J Reprod Immunol, 25(4):163-168.

Takeda K. 2004. Toll-like receptors in innate immunity. Int Immunol, 17(1):1-14.

Thatcher WW, Santos JEP, Silvestre FT, Kim IH, Staples CR. 2010. Perspective on physiological/ endocrine and nutritional factors influencing fertility in post-partum dairy cows. Reprod Domest Anim, 45(3):2-14.

Townson DH, O’Connor CL, Pru JK. 2002. Expression of monocyte chemoattractant protein-1 and distribution of immune cell populations in the bovine corpus luteum throughout the estrous cycle. Biol Reprod, 66(2):361-366.

Townson DH, Liptak AR. 2003. Chemokines in the corpus luteum: implications of leukocyte chemotaxis. Reprod Biol Endocrinol, 94(1):1477-7827.

Tropea A, Miceli F, Minici F, Tiberi F, Orlando M, Gangale MF, Romani F, Catino S, Mancuso S, Navarra P, Lanzone A, Apa R. 2006. Regulation of vascular endothelial growth factor synthesis and release by human luteal cells in vitro. Clin Endocrinol Metab, 91(6):2303-2309.

Tsai SJ, Wiltbank MC. 1998. Prostaglandin F2α regulates distinct physiological changes in early and mid-cycle bovine corpora lutea1. Biol Reprod, 58(2):346-352.

Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan CW, Fraser HM. 2011. Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction, 141(6):821-831.

Walsh SW, Mehta JP, McGettigan PA, Browne JA, Forde N, Alibrahim RM, Mulligan FJ, Loftus B, Crowe MA, Matthews D, Diskin M, Mihm M, Evans AC. 2012a. Effect of the metabolic environment at key stages of follicle development in cattle: focus on steroid biosynthesis. Physiol Genomics, 44(9):504-517.

Walsh SW, Fair T, Browne JA, Evans ACO, McGettigan PA. 2012b. Physiological status alters immunological regulation of bovine follicle differentiation in dairy cattle. J Reprod Immunol, 96(1-2):34-44.

Watanabe H, Tatsumi K, Yokoi H, Higuchi T, Iwai M, Fukuoka M, Fujiwara H, Fujita K, Nakayama H, Mori T, Fujita J. 1997. Ovulation defect and its restoration by bone marrow transplantation in osteopetrotic mutant mice of MitfMi/MitfMi genotype1. Biol Reprod, 57(6):1394-1400.

Woad KJ, Hammond AJ, Hunter M, Mann GE, Hunter MG, Robinson RS. 2009. FGF2 Is crucial for the development of bovine luteal endothelial networks in vitro. Reproduction 138(3):581-588.

Yamashita H, Kamada D, Shirasuna K, Matsui M, Shimizu T, Kida K, Berisha B, Schams D, Miyamoto A. 2008. Effect of Local Neutralization of basic fibroblast growth factor or vascular endothelial growth factor by a specific antibody on the development of the corpus luteum in the cow. Mol Reprod Dev, 75(9):1449-1456.

Zalman Y, Klipper E, Farberov S, Mondal M, Wee G, Folger JK, Smith GW, Meidan R. 2012. Regulation of Angiogenesis-related prostaglandin f2alpha-induced genes in the bovine corpus luteum. Biol Reprod, 86(3):1-10.

5d52b7dc0e88252c46daee82 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections