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Fecha Publicación: 2011-12-23
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Uribe Velásquez, L. F., Osorio, J. H., & Correa Orozco, A. (2011). El cuerpo lúteo: Una visión inmunológica. Biosalud, 10(2), 87–100. Recuperado a partir de https://revistasojs.ucaldas.edu.co/index.php/biosalud/article/view/4743
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El objetivo de la presenta revisión es describir los conceptos actuales sobre el mecanismo local de la cascada de desarrollo y regresión del cuerpo lúteo (CL) regulado por macrófagos, células inmunológicas y citoquinas. El CL de la vaca es un órgano dinámico, el cual tiene una vida media de aproximadamente 17 a 18 días. La principal función del CL es secretar grandes cantidades de progesterona (P4). Cuando el CL madura, las células esteroidogénicas establecen contacto con muchos capilares. Además, el CL maduro está compuesto de muchas células endoteliales vasculares, las cuales pueden alcanzar hasta el 50 % de todas las células del CL. En el ganado bovino y otras especies, el CL juega un papel central en la regulación de la ciclicidad y en el mantenimiento de la preñez. En muchas especies, la regresión luteal es iniciada por la liberación uterina de prostaglandina F2α (PGF2α), la cual inhibe la esteroidogénesis, desencadenando una cascada de eventos que llevan a la desaparición final del tejido. Las células inmunes, principalmente los macrófagos y los linfocitos T, son importantes para la ingestión de los restos celulares que resultan de la muerte de las células luteales. Los macrófagos son células multifuncionales que juegan un papel clave en la respuesta inmune y son abundantes en todo el tejido reproductivo de la hembra. Su localización específica y las variaciones de la distribución en el ovario durante los diferentes estados del ciclo, sugieren que los macrófagos juegan diversas funciones en los eventos intraováricos, lo que incluye: la foliculogénesis, la reestructuración del tejido en la ovulación y la formación y regresión del CL.
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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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