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Publication Date: 2011-12-23
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Uribe Velásquez, L. F., Osorio, J. H., & Correa Orozco, A. (2011). Corpus luteum: An inmunological view. Biosalud, 10(2), 87–100. Retrieved from https://revistasojs.ucaldas.edu.co/index.php/biosalud/article/view/4743
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Abstract
The aim of the present review is to describe the current concepts of the local mechanism for the cascade of development and regression of the corpus luteum (CL) as regulated by macrophages, immunological cells and cytokines. The cow CL is a dynamic organ which has a life time of approximately 17-18 days. The main function of the CL is to secrete a large amount of progesterone (P4). As the CL matures, the steroidogenic cells establish contact with many capillaries and the matured CL is composed of many vascular endothelial cells that account for up to 50 % of all CL cells. In cattle and other species, the CL plays a central role in the regulation of cyclicity and maintenance of pregnancy. In many species, luteal regression is initiated by uterine release of PGF2α, which inhibits steroidogenesis and may launch a cascade of events leading to the tissue final disappearance. Immune cells, primarily macrophages and T lymphocites are important for ingestion of cellular remnants that result from the death of luteal cells. Macrophages are multifunctional cells that play key roles in the immune response and are abundant throughout female reproductive tissues. Their specific localization and variations in distribution in the ovary during different stages of the cycle, suggest that macrophages play diverse roles in intra-ovarian events including folliculogenese, tissue restructuring at ovulation and CL formation and regression.
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References
Schams D, Berisha, B. Regulation of corpus luteum function in cattle - an overview. Reprod Dom Anim 2004; 39:241-251.
Souza MIL, Ramírez GFB, Uribe-Velásquez LF. Papel del factor de crecimiento semejante a insulina-1 (IGF-1) en la regulación de la función ovárica. Biosalud 2007; 6:149-59.
Milvae RA. Inter-relationships between endothelin and prostaglandin F2α in corpus luteum function. Rev Reprod 2000; 5:1-5.
Gonzalez de Bulnes A, Moreno JS, Gomez A, Lopez Sebastian A. Relationship between ultrasonographic assesment of the corpus luteum and plasma progesterone concentration during the oestrous cycle in monovular ewes. Reprod Dom Anim 2000; 35:65-68.
Uribe-Velásquez LF, Oba E, Souza MIL. Población folicular y concentraciones plasmáticas de progesterona (P4) en ovejas sometidas a diferentes protocolos de sincronización. Arch Med Vet 2008; 40:83-88.
Fierro S, Olivera-Muzante J, Gil J, Viñoles C. Effects of prostaglandin administration on ovarian follicular dynamics, conception, prolificacy, and fecundity in sheep. Theriogenology 2011; 76:630-639.
Peter AT, Levine H, Drost M, Bergfelt DR. Compilation of classical and contemporary terminology used to describe morphological aspects of ovarian dynamics in cattle. Theriogenology 2009; 71:1343-1357.
Perez-Marín C. Formation of corpora lutea and central luteal cavities and their relationship with plasma progesterone levels and other metabolic parameters in dairy cattle. Reprod Dom Anim 2009; 44:384-389.
O’Shea JD, Rodgers RJ, D’Occhio MJ. Celular composition of the cyclic corpus luteum of the cow. J Reprod Fert 1989; 85:483-487.
Selvaraju S, Raghavendra BS, Siva Subramani T, Priyadharsini R, Reddy IJ, Ravindra JP. Changes in luteal cells distribution, apoptotic rate, lipid peroxidation levels and antioxidant enzyme activities in buffalo (Bubalus bubalis) corpus luteum. Anim Reprod Sci 2010; 120:39-46.
Sangha GK, Sharma RK, Guraya SS. Biology of corpus luteum in small ruminants. Small Rumin Res 2002; 43:53-64.
Lüttgenau J, Ulbrich SE, Beindorff N, Honnens A, Herzog K, Bollwein H. Plasma progesterone concentrations in the mid-luteal phase are dependen on luteal size, but independent of luteal blood flow and gene expression in lactating dairy cows. Anim Reprod Sci 2011; 125:20-29.
Reynolds LP, Grazul-Bilska AT, Redmer DA. Angiogenesis in the corpus luteum. Endocrine 2000; 12:1-9.
Rekawiecki R, Kowalik MK, Slonina D, Kotwica J. Regulation of progesterone synthesis and action in bovine corpus luteum. J Physiol Pharmacol Suppl 2008; 59:75-89.
Ginther OJ, Araujo RR, Palhao MO, Rodrigues BL, Beg MA. Necessity of sequencial pulses of prostaglandin F2-alpha for complete physiologic luteolysis in cattle. Biol Reprod 2009; 80:641-648.
Ferrara N, Gerber HP, LeCouter J. The biology of VEFG and its receptors. Nat Med 2003; 9:669-676.
Wiedlocha A, Sorensen V. Signaling, internalization and intracellular activity of fibroblast growth factor. Curr Top Microbiol Immunol 2004; 286:45-79.
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; 37:159-169.
Rosiansky-Sultan M, Klipper E, Spanel-Borowski K, Meidan R. Inverse relationship between nitric oxide synthases and endothelin-1 synthesis in bovine corpus luteum: interactions at the level of luteal endothelial cell. Endocrinology 2006; 147:5228-5235.
Ialenti A, Ianaro A, Moncada S, Di Rosa M. Modulation of acute inflammation by endogenous nitric oxide. Eur J Pharmacol 1992; 211:177-182.
Khan FA & Dan GK. Follicular fluid nitric oxide and ascorbic acid concentrations in relation to follicle size, functional status and stage of estrous cycle in buffalo. Anim Reprod Sci 2011; 125:62-68.
Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997; 18:4-25.
Connolly DT. Vascular permeability factor: a unique regulator of blood vessel function. J Cell Biochem 1991; 47:219-223.
Neuvians TP, Schams D, Berisha B, Pfaffl MW. Involvement of pro-inflammatory cytokines, mediators of inflammation, and basic fibroblast growth factor in prostaglandin F2α - Induced luteolysis in bovine corpus luteum. Biol Reprod 2004; 70:473-480.
Niswender GD & Nett TM. Corpus luteum and its control in infraprimate species. In: The Physiology of Reproduction. Vol. 1. New York: E Knobil & JD Neill Raven Press Eds.; 1994. p. 781-816.
Niswender GD. Molecular control of luteal secretion of progesterone. Reproduction 2002; 123:333-339.
McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event. Physiol Rev 1999; 79:263-323.
Jaroszewski JJ, Hansel W. Intraluteal administration of a nitric oxid synthase blocker stimulates progesterone and oxytocin secretion and prolongs the lifespan in the bovine corpus luteum. Proc Soc Exp Biol Med 2000; 224:50-55.
Pate JL, Keyes PL. Immune cells in the corpus luteum: friends or foes? Reproduction 2001; 122:665-676.
Lea RG, Sandra O. Immunoendocrine aspects of endometrial function and implantation. Reproduction 2007; 134:389-404.
Rae MT, Niven D, Critchley HO, Harlow CR, Hillier SG. Antiinflamatory steroid action in human ovarian surface epithelial cells. J Clin Endocrinol Metab 2004; 89:389-404.
Wang M. The role of glucocorticoid action in the pathophysiology of the metabolic syndrome. Nutr Metab 2005; 2:3.
Rae MT, Hillier SG. Steroid signaling in the ovarian surface epithelium. Trends Endocrinol Metab 2005; 16:327-333.
Komiyama J, Nishimura R, Lee HY, Sakumoto R, Tetsuka M, Acosta TJ, Skarzynski DJ, Okuda K. Cortisol is a suppressor of apoptosis in bovine corpus luteum? Biol Reprod 2008; 78: 888-95.
Townson DH, O’Connor CL, Pru JK. Expression of monocyte chemoattractant protein-1 and distribution of immune cell population in the bovine corpus luteum throughout the estrous cycle. Biol Reprod 2002; 66:361-366.
Penny LA, Armstrong DG, Baxter G, Hogg C, Kindahl H. Expression of monocyte chemoattractant protein-1 in the bovine corpus luteum around the time of natural luteolysis. Biol Reprod 1998; 59:1464-1469.
Bowen JM, Towns R, Warren JS, Keyes PL. Luteal regression in the normally cycling rat: apoptosis, monocyte chemoattractant protein-1 and inflammatory cell involvement. Biol Reprod 1999; 60:740-746.
Penny LA. Monocyte chemoattractant protein-1 in luteolysis. Rev Reprod 2000; 5:63-66.
Lobel BL, Levy E. Enzymatic correlates of development, secretory function and regression of follicles and corpora lutea in the bovine ovary. II Formation, development and involution of corpora lutea. Acta Endoc 1968; 132:35-63.
Bauer M, Reibiger I, Spanel-Borowski K. Leukocyte proliferation in the bovine corpus luteum. Reproduction 2001; 121:297-305.
Buford WI, Ahmad N, Schrick FN, Butcher RL, Lewis PE. Embryotoxiciy of a regressing corpus luteum in beef cows supplemented with progestogen. Biol Reprod 1996; 54:531-537.
Bulmer D. The histochemystry of ovarian macrophages in the rat. J Anat 1964; 98:313-319.
Wu R, Van der Hoek KH, Ryan NK, Norman RJ, Robker RL. Macrophage contributions to ovarian function. Hum Reprod Update 2004; 2:119-133.
Katabuchi H, Fukumatsu Y, Araki M, Suenaga, Y, Ohtake H, Okamura H. Role of macrophages in ovarian follicular development. Horm Res 1996; 46:45-51.
Szóstek AZ, Lukasik K, Majewska M, Bah MM, Znaniecki R, Okuda K, Skarzynski DJ. Tumor necrosis factor-α inhibits the stimulatory effect of luteinizing hormone and prostaglandin E2 on progesterone secretion by the bovine corpus luteum. Dom Anim Endoc 2011; 40:183-191.
Souza MIL, Uribe-Velásquez LF. O fator de necrose tumoral-A (TNF-A) na reprodução de fêmeas - Revisão de literatura. Arq Cien Vet Zool Unipar 2008; 1:47-53.
Sakumoto R, Vermehren M, Kenngott RA, Okuda K, Sinowatz F. Localization of gene and protein expressions of tumor necrosis factor-α and tumor necrosis factor receptor types I and II in the bovine corpus luteum during the estrous cycle. J Anim Sci 2011; 89:3040-3047.
Benyo DF, Pate JL. Tumor necrosis factor-α alters bovine luteal cell synthetic capacity and viability. Endocrinology 1992; 130:751-756.
Petroff MG, Petroff BK, Pate JL. Mechanism of cytokine-induced death of cultured bovine luteal cells. Reproduction 2001; 121:753-760.
Meidan R, Milvae RA, Weiss S, Levy S, Friedman A. Intraovarian regulation of luteolysis. J Reprod Fert Suppl 1999; 54:217-228.
Skarzynski DJ, Woclawek-Potocka I, Korzekwa AJ. Infusion of exogenous tumor necrosis factor-α dose dependently alters the length of the luteal phase in cattle: differential responses to treatment with indomethacin and L-NAME, a nitric oxide synthase inhibitor. Biol Reprod 2007; 76:619-627.
Owen CA, Campbell EJ. The cell biology of leukocyte-mediated proteolysis. J Leukoc Biol 1999; 65:137-150.
Bauvois B. Transmembrane proteases in focus: diversity and redundancy? J Leukoc Biol 2001; 70:11-17.
Souza MIL, Ramírez GFB, Uribe-Velásquez LF. Papel del factor de crecimiento semejante a insulina-1 (IGF-1) en la regulación de la función ovárica. Biosalud 2007; 6:149-59.
Milvae RA. Inter-relationships between endothelin and prostaglandin F2α in corpus luteum function. Rev Reprod 2000; 5:1-5.
Gonzalez de Bulnes A, Moreno JS, Gomez A, Lopez Sebastian A. Relationship between ultrasonographic assesment of the corpus luteum and plasma progesterone concentration during the oestrous cycle in monovular ewes. Reprod Dom Anim 2000; 35:65-68.
Uribe-Velásquez LF, Oba E, Souza MIL. Población folicular y concentraciones plasmáticas de progesterona (P4) en ovejas sometidas a diferentes protocolos de sincronización. Arch Med Vet 2008; 40:83-88.
Fierro S, Olivera-Muzante J, Gil J, Viñoles C. Effects of prostaglandin administration on ovarian follicular dynamics, conception, prolificacy, and fecundity in sheep. Theriogenology 2011; 76:630-639.
Peter AT, Levine H, Drost M, Bergfelt DR. Compilation of classical and contemporary terminology used to describe morphological aspects of ovarian dynamics in cattle. Theriogenology 2009; 71:1343-1357.
Perez-Marín C. Formation of corpora lutea and central luteal cavities and their relationship with plasma progesterone levels and other metabolic parameters in dairy cattle. Reprod Dom Anim 2009; 44:384-389.
O’Shea JD, Rodgers RJ, D’Occhio MJ. Celular composition of the cyclic corpus luteum of the cow. J Reprod Fert 1989; 85:483-487.
Selvaraju S, Raghavendra BS, Siva Subramani T, Priyadharsini R, Reddy IJ, Ravindra JP. Changes in luteal cells distribution, apoptotic rate, lipid peroxidation levels and antioxidant enzyme activities in buffalo (Bubalus bubalis) corpus luteum. Anim Reprod Sci 2010; 120:39-46.
Sangha GK, Sharma RK, Guraya SS. Biology of corpus luteum in small ruminants. Small Rumin Res 2002; 43:53-64.
Lüttgenau J, Ulbrich SE, Beindorff N, Honnens A, Herzog K, Bollwein H. Plasma progesterone concentrations in the mid-luteal phase are dependen on luteal size, but independent of luteal blood flow and gene expression in lactating dairy cows. Anim Reprod Sci 2011; 125:20-29.
Reynolds LP, Grazul-Bilska AT, Redmer DA. Angiogenesis in the corpus luteum. Endocrine 2000; 12:1-9.
Rekawiecki R, Kowalik MK, Slonina D, Kotwica J. Regulation of progesterone synthesis and action in bovine corpus luteum. J Physiol Pharmacol Suppl 2008; 59:75-89.
Ginther OJ, Araujo RR, Palhao MO, Rodrigues BL, Beg MA. Necessity of sequencial pulses of prostaglandin F2-alpha for complete physiologic luteolysis in cattle. Biol Reprod 2009; 80:641-648.
Ferrara N, Gerber HP, LeCouter J. The biology of VEFG and its receptors. Nat Med 2003; 9:669-676.
Wiedlocha A, Sorensen V. Signaling, internalization and intracellular activity of fibroblast growth factor. Curr Top Microbiol Immunol 2004; 286:45-79.
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; 37:159-169.
Rosiansky-Sultan M, Klipper E, Spanel-Borowski K, Meidan R. Inverse relationship between nitric oxide synthases and endothelin-1 synthesis in bovine corpus luteum: interactions at the level of luteal endothelial cell. Endocrinology 2006; 147:5228-5235.
Ialenti A, Ianaro A, Moncada S, Di Rosa M. Modulation of acute inflammation by endogenous nitric oxide. Eur J Pharmacol 1992; 211:177-182.
Khan FA & Dan GK. Follicular fluid nitric oxide and ascorbic acid concentrations in relation to follicle size, functional status and stage of estrous cycle in buffalo. Anim Reprod Sci 2011; 125:62-68.
Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997; 18:4-25.
Connolly DT. Vascular permeability factor: a unique regulator of blood vessel function. J Cell Biochem 1991; 47:219-223.
Neuvians TP, Schams D, Berisha B, Pfaffl MW. Involvement of pro-inflammatory cytokines, mediators of inflammation, and basic fibroblast growth factor in prostaglandin F2α - Induced luteolysis in bovine corpus luteum. Biol Reprod 2004; 70:473-480.
Niswender GD & Nett TM. Corpus luteum and its control in infraprimate species. In: The Physiology of Reproduction. Vol. 1. New York: E Knobil & JD Neill Raven Press Eds.; 1994. p. 781-816.
Niswender GD. Molecular control of luteal secretion of progesterone. Reproduction 2002; 123:333-339.
McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event. Physiol Rev 1999; 79:263-323.
Jaroszewski JJ, Hansel W. Intraluteal administration of a nitric oxid synthase blocker stimulates progesterone and oxytocin secretion and prolongs the lifespan in the bovine corpus luteum. Proc Soc Exp Biol Med 2000; 224:50-55.
Pate JL, Keyes PL. Immune cells in the corpus luteum: friends or foes? Reproduction 2001; 122:665-676.
Lea RG, Sandra O. Immunoendocrine aspects of endometrial function and implantation. Reproduction 2007; 134:389-404.
Rae MT, Niven D, Critchley HO, Harlow CR, Hillier SG. Antiinflamatory steroid action in human ovarian surface epithelial cells. J Clin Endocrinol Metab 2004; 89:389-404.
Wang M. The role of glucocorticoid action in the pathophysiology of the metabolic syndrome. Nutr Metab 2005; 2:3.
Rae MT, Hillier SG. Steroid signaling in the ovarian surface epithelium. Trends Endocrinol Metab 2005; 16:327-333.
Komiyama J, Nishimura R, Lee HY, Sakumoto R, Tetsuka M, Acosta TJ, Skarzynski DJ, Okuda K. Cortisol is a suppressor of apoptosis in bovine corpus luteum? Biol Reprod 2008; 78: 888-95.
Townson DH, O’Connor CL, Pru JK. Expression of monocyte chemoattractant protein-1 and distribution of immune cell population in the bovine corpus luteum throughout the estrous cycle. Biol Reprod 2002; 66:361-366.
Penny LA, Armstrong DG, Baxter G, Hogg C, Kindahl H. Expression of monocyte chemoattractant protein-1 in the bovine corpus luteum around the time of natural luteolysis. Biol Reprod 1998; 59:1464-1469.
Bowen JM, Towns R, Warren JS, Keyes PL. Luteal regression in the normally cycling rat: apoptosis, monocyte chemoattractant protein-1 and inflammatory cell involvement. Biol Reprod 1999; 60:740-746.
Penny LA. Monocyte chemoattractant protein-1 in luteolysis. Rev Reprod 2000; 5:63-66.
Lobel BL, Levy E. Enzymatic correlates of development, secretory function and regression of follicles and corpora lutea in the bovine ovary. II Formation, development and involution of corpora lutea. Acta Endoc 1968; 132:35-63.
Bauer M, Reibiger I, Spanel-Borowski K. Leukocyte proliferation in the bovine corpus luteum. Reproduction 2001; 121:297-305.
Buford WI, Ahmad N, Schrick FN, Butcher RL, Lewis PE. Embryotoxiciy of a regressing corpus luteum in beef cows supplemented with progestogen. Biol Reprod 1996; 54:531-537.
Bulmer D. The histochemystry of ovarian macrophages in the rat. J Anat 1964; 98:313-319.
Wu R, Van der Hoek KH, Ryan NK, Norman RJ, Robker RL. Macrophage contributions to ovarian function. Hum Reprod Update 2004; 2:119-133.
Katabuchi H, Fukumatsu Y, Araki M, Suenaga, Y, Ohtake H, Okamura H. Role of macrophages in ovarian follicular development. Horm Res 1996; 46:45-51.
Szóstek AZ, Lukasik K, Majewska M, Bah MM, Znaniecki R, Okuda K, Skarzynski DJ. Tumor necrosis factor-α inhibits the stimulatory effect of luteinizing hormone and prostaglandin E2 on progesterone secretion by the bovine corpus luteum. Dom Anim Endoc 2011; 40:183-191.
Souza MIL, Uribe-Velásquez LF. O fator de necrose tumoral-A (TNF-A) na reprodução de fêmeas - Revisão de literatura. Arq Cien Vet Zool Unipar 2008; 1:47-53.
Sakumoto R, Vermehren M, Kenngott RA, Okuda K, Sinowatz F. Localization of gene and protein expressions of tumor necrosis factor-α and tumor necrosis factor receptor types I and II in the bovine corpus luteum during the estrous cycle. J Anim Sci 2011; 89:3040-3047.
Benyo DF, Pate JL. Tumor necrosis factor-α alters bovine luteal cell synthetic capacity and viability. Endocrinology 1992; 130:751-756.
Petroff MG, Petroff BK, Pate JL. Mechanism of cytokine-induced death of cultured bovine luteal cells. Reproduction 2001; 121:753-760.
Meidan R, Milvae RA, Weiss S, Levy S, Friedman A. Intraovarian regulation of luteolysis. J Reprod Fert Suppl 1999; 54:217-228.
Skarzynski DJ, Woclawek-Potocka I, Korzekwa AJ. Infusion of exogenous tumor necrosis factor-α dose dependently alters the length of the luteal phase in cattle: differential responses to treatment with indomethacin and L-NAME, a nitric oxide synthase inhibitor. Biol Reprod 2007; 76:619-627.
Owen CA, Campbell EJ. The cell biology of leukocyte-mediated proteolysis. J Leukoc Biol 1999; 65:137-150.
Bauvois B. Transmembrane proteases in focus: diversity and redundancy? J Leukoc Biol 2001; 70:11-17.
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