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http://dx.doi.org/10.5187/JAST.2006.48.2.191

A Morphological Study on the Macrophages During Luteolysis in the Pig  

김원식 (Department of Anatomy, Chungnam National University)
한승로 (Department of Anatomy, Chungnam National University)
손성경 (Obstetrics & Gynecology, Chungnam National University)
박창식 (Division of Animal Science & Resources, Research Center for Transgenic Cloned Pigs, Chungnam National University)
양윤석 (Department of Obstetrics & Gynecology, Eulji Medical University)
Publication Information
Journal of Animal Science and Technology / v.48, no.2, 2006 , pp. 191-202 More about this Journal
Abstract
In addition to the removal of dying or dead lutein cells by phagocytosis in many species, macrophages exert both luteotropic effect during maturation period and luteolytic effect during degenerative period via mediating autocrine/paracrine actions of self-producing cytokines in the corpus luteum. In this experiment, immunohistochemical and transmission electron microscopic (TEM) studies were performed to observe the morphologic changes of luteal macrophages during luteolysis. A small number of macrophages and low immunoreactivity were present at the mature stage. The number of macrophages and immunoreactivity gradually increased along the advance of luteolysis. Two subtypes of macrophages could be observed through TEM observation. One type of macrophage located between the large lutein cells contained no lipid droplets in their cytoplasm at mature stage. The other type of macrophage located near the blood vessels contained many lipid droplets in their cytoplasm during luteolysis. Particularly, no phagocytic macrophages were observed, which suggested the macrophages in the porcine corpus luteum did not involve in the phagocytotic elimination of dying lutein cells.
Keywords
Corpus luteum; Luteolysis; Macrophage; Immunohistochemistry; TEM;
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1 Bacci, M. L., Barazzoni, A. M., Forni, M. and Lalatta Costerbosa, G. 1996. In Situ detection of apoptosis in regressing corpus luteum of pregnant sow: Evidence of an early presence of DNA fragmentation. Dom. Anim. Endocrinol. 13(4):361372   DOI   ScienceOn
2 Dijkstra, C. D., Dopp, E. A, Joling, P. and Kraal, G. 1985. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies EDl. ED2 and ED3. Immunol. 54:589599
3 Adams, E. C. and Hertig, A. T. 1969. Studies on the corpus lutenm. I. Observation on the ultrastructure of development and regression of the luteal cells during the menstrual cycle. J. Cell Biol. 41:696715   DOI
4 Asselin, E., Xiao, C. W ., Wang, Y. F. and Tsang, B. K. 2000. Mammalian follicular development and atresia: role of apoptosis. Biol. Signals Receipt. 9:87-95   DOI   ScienceOn
5 Azmi, T. I. and O'Shea, . D. 1984. Mechanism of deletion of endothelial cells during regression of the corpus luteum. Lab. Invest. 51:206-217
6 Bagavandoss, P., Wiggins, R. C. Kunkel, S. L., Remick, D. G. and Keyes, P. L. 1990. Tumor necrosis factor production and accumulation of inflammatory cells III the corpus luteum of pseudopregnancy and pregnancy in rabbits. Biol. Reprod. 42:367-376   DOI   ScienceOn
7 Kerr, J. F. R., Wyllie, A. H. and Currie, A. R. 1972. Apoptosis, a basic biological phenomenon with wider implication in tissue kinetics. Br. J. Cancer. 226:239-247
8 Kraal, G., Shiamatey-Koolma, R., Hoffer, M., Baker, D. and Scheper, R. 1988. Histochemical identification of guinea-pig macrophages by monoclonal antibody MR-l. Immunology. 65:523-528
9 Bagavandoss, P., Kunkel. S. L., Wiggins, R. C. and Keyes, P. L. 1988. Tumor necrosis factor-$\alpha$ production and localization of macrophages and T lymphocytes in the rabbit corpus luteum. Endocrinology, 122:1185-1187   DOI   ScienceOn
10 Braden. T. D., Gamboni, F. and Niswender, G. D. 1988. Effects of prostaglandin F2$\alpha$-induced luteolysis on the populations of cells in the ovine corpus luteum. Biol. Reprod. 39:245-253   DOI   ScienceOn
11 Brannstrom. M. B. and Norman. R. J. 1993. Involvement of leukocytes and cytokines in the ovulatory process and corpus luteum function. Hum. Reprod. 8: 1762-1775   DOI
12 Brannstrom, M., Giesecke, L., Moore, I. C., Van Den Heuvel, C. J. and Robertson, S. A. 1994. Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol. Reprod. 50: 1161-1167   DOI   ScienceOn
13 Bulmer, D. 1964, The histochemistry of ovarian macrophages in the rat. J. Anat. 98:313-319
14 Chen, H., Marcinkiewicz, J. L., Sancho-Tello, M., Hunt, J. S. and Terranova, P. F. 1993. Tumor necrosis factor-$\kappa$ gene expression In mouse oocytes and follicular cells. Biol Reprod. 48:707-714   DOI   ScienceOn
15 Grossman, C. J. 1984. Regulation of the immune system by sex steroids. Endocrine Reviews. 5:435-455   DOI   ScienceOn
16 Clarke, P. G. H. 1990. Developmental cell death: Morphological diversity and multiple mechanisms. Anat. Embryol. 181:195-213
17 Fairchild-Benyo, D. L. and Pate, J. L. 1992. Tumor necrosis factor $\kappa$ alters bovine lutealcell synthetic capacity and viability. Endocrinology. 130:854-860   DOI   ScienceOn
18 Fukumatsu, Y., Katabuchi. H., Naito, M., Takeya, M., Takahashi, K. and Okamura, H. 1992. Effect of macrophages on proliferation of granulosa cells in the ovary in rats. J. Reprod. Fertil. 96:241-249   DOI   ScienceOn
19 Hulboy, D. L., Rudolph, L. A. and Matrisian, L. M. 1997. Matrix metalloproteinases as mediators of reproductive function. Mol. Hum. Reprod. 3:27-45   DOI   ScienceOn
20 Hume, D. A., Halpin, D., Charlton, H. and Gordon, S. 1984. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of endocrine organs. Proc. Natl. Acad. Sci. USA. 81:4174
21 Hurwitz, A., Dushnik, M. and Solomon, H. 1993. Cytokine-mediated regulation of rat ovarian function: interleukin-l stimulates the accumulation of a 92-kilodalton gelatinase. Endocrinology. 132:27092714   DOI   ScienceOn
22 Kaipia, A. and Hsueh, A. J. 1997. Regulation of ovarian follicle atresia. Annu. Rev. Physiol. 59: 349-363   DOI   ScienceOn
23 Kelly, R. W. 1994. Pregnancy maintenance and parturition: the role of prostaglandin in manipulating the immune and inflammatory response. Endocrine Reviews. 15:684-706   DOI
24 O'Shea, J. D., Nightingale, M. G. and Charnley, W. A. 1977. Changes in small blood vessels during cyclical regression in sheep. Biol. Reprod. 17:162177   DOI   ScienceOn
25 Mci.rackcn, J. A., Custer, E. E. and Lamsa, J. C. 1999. Luteolysis : A neuroendocrine-mediated event. Physiological Reviews. 79(2):263-324   DOI
26 Endo, T., Atcn, R. F., Wang, F. and Behrman, H. R. 1993. Coordinate induction and activation of metalloproteinase and ascorbate depletion in structural luteolysis. Endocrinology. 133:690-698   DOI   ScienceOn
27 Maylor, M. S., Stamp. G. W. H., Foulkes. W. D., Eccles. D. and Balkwill. F. R. 1993. Tumor necrosis factor and its receptors in human ovarian cancer. J. Clin. Invest. 91 :2194-2206   DOI   ScienceOn
28 McCracken, J. A., Glew, M. E. and Scaramuzzi, R. J. 1970. Corpus luteum regression induced by prostaglandin F2$\alpha$. J. Clin. Endocrinol. Metab. 30:544-547   DOI
29 McGuire. W. J., Juengel, J. L. and Niswender. G. D. 1994. Protein kinase C second messenger system mediates the antisteroidogenic effects of Prostaglandin F2$\kappa$ in the ovine corpus luteum in vivo. Biol. Reprod. 51:800-806   DOI   ScienceOn
30 Miyamoto, A., Luetzow, V. H. and Schams, D. 1993. Acute action of prostaglandin F2$\kappa$, E2, and 12 in microdialyzed bovine corpus luteum in vitro. Biol. Reprod. 49:423-430   DOI   ScienceOn
31 Nett, T. M., McClellen, M. C. and Niswender, G. D. 1976. Effects of prostaglandins on the ovine corpus luteum : blood flow, secretion of progesterone and morphology. Biol. Reprod. 15:66-78   DOI   ScienceOn
32 Niswender, G. D. and Nett, T. M. 1994. Corpus luteum and its control in infraprimate species. In:The Physiology of Reproduction, editied by E. Knobil and JD Neill. New York: Raven, vol. 1, pp., 781-816
33 Niswender, G. D., Juengel, J. L., Silva, P. J., Rollyson, M. K. and Mcintosh, E. R. 2000. Mechanisms controlling the function and life span of the corpus luteum. Physiological Reviews. 80(1):1-29   DOI
34 Parker, C. W. 1991. Neutrophil mechanisms. Am. Rev. Respir. Dis. 143:559-560
35 Nothnick, W. B. and Pate, J. L. 1990. Interleukin-I is a potent stimulator of prostaglandin synthesis In bovine luteal cells. Biol, Reprod. 43: 169-173   DOI   ScienceOn
36 Paavola, L. G. 1977. The corpus luteum of the guinea pig. Fine structure at the time of maximum progesterone secretion and during regression. Am. J. Anat. 150:565-604   DOI   ScienceOn
37 Paavola, L. G. 1979. The corpus luteum of the guinea pig. IV. Fine structure of macrophages during pregnancy and postpartum luteolysis and the phagocytosis of luteal cells. Am. J. Anat. 154:337-364   DOI   ScienceOn
38 Pate, J. L. and Keyes, P. L. 2001. Immune cells in the corpus luteum : friends or foes? Reproduction. 122:665-676   DOI
39 Pepperell, J. R, Wolcott, C. and Behrman, H. R 1991. Effects of neutrophils in rat luteal cells. Endocrinology. 130:1001-1008
40 Quatacker, J. R. 1971. Formation of autophagic vacuoles during human corpus luteum involution. Z. Zellforsch. 122:479-487   DOI
41 Roby, K. F. and Terranova, P. F. 1989. Localization of tumor necrosis factor (TNF) in the rat and bovine ovary using immunohistochemistry and cell blot: evidence for granulosa production. In: Hirshfield AN (ed.), Growth Factors and the Ovary. New York. Plenum Publishing Corporation, pp. 273-278
42 Sakumoto, R. and Okuda, K 2004. Possible actions of TNF-$\kappa$ in ovarian function. J. Reprod. Dev. 50:39-46   DOI   ScienceOn
43 Sawyer, H. R. 1995. Structural and functional properties of the corpus luteum of pregnancy. In Scaranuzzi, R. J., Nancarrow, C. D. and Doberska, C.(eds), Reproduction in Domestic Ruminants III. J. Reprod. Fertil. Dorset. 97: 110
44 Stouffer, R. L. and Brannian, J. D. 1993. The function and regulation of cell populations composing the corpus luyeum of the ovarian cycle. In Adashi, E. Y. and Leung, P. C. K(eds.), The Ovary. Raven Press, New York, pp. 245249
45 Shakil, T. and Whitehead, S. A. 1994. Inhibitory action of peritoneal macrophages on progesterone secretion from co-cultured rat granulosa cells. Biol. Reprod. 50:1183-1189   DOI   ScienceOn
46 Siiteri, P. K and Stites, D. P. 1982. Immunologic and endocrine interrelationships in pregnancy. Biol. Reprod. 26:1-14   DOI   ScienceOn
47 Standaert, F. E., Zamora, C. S. and Chew, B. P. 1991. Quantitative and qualitative changes in blood leukocytes in the porcine ovary. Am. J. Reprod. Immunol. 25:163-168   DOI
48 Tscheshe, H., Fedrowitz, J., Michaelis, J. and Macartney, H. W. 1986. Matrix degrading proteinases from human granulocytes : Type I, II , III collagenase, gelatinase and type IV collagenase. Folia Histochem. Cytobiol. 61:269-273
49 Wang, L. J., Brannstrom, M., Robertson, S. A. and Norman, R. J. 1992. Tumor necrosis factor alpha in the human ovary: presence in follicular fluid and effects on ell proliferation and prostaglandin production. Fertil. Steril. 58:934-940   DOI
50 Yan, Z., Hunter, V., Weed, J., Hutchison, S., Lyles, R. T. and Terranova, P. F. 1993. Tumor necrosis factor-$\alpha$ alters steroidogenesis and stimulates proliferation of human ovarian granulosa cells in vitro. Fertil. Steril. 53:332-338
51 Yuan, W. and Giudice, L. C. 1997. Programmed cell death in human ovary is a function of a follicle and corpus luteum status. J. Clin. Endocrinol. Metab. 82:3148-3155   DOI
52 Zhao, Y., Burbach, J. A., Roby, K. F., Terranova, P. F. and Brannian, J. D. 1998. Macrophages are the major source of tumor necrosis factor $\alpha$ in the porcine corpus luteum. Biol. Reprod. 59: 13851391   DOI   ScienceOn
53 Morales, C, Garcia-Pardo, L., Reymundo, C, Bellido, C, Sanchez-Criado, J. E. and Gaytan, F. 2000. Different patterns of structural luteolysis in the human corpus luteum of menstruation. Hum. Reprod. 15(10):2119-2128   DOI   ScienceOn
54 Zolti. M., Meirom. R., Shemesh, M., Wollach. D., Mashiach. S., Shore, L. and Ben Rafael. Z. 1990. Granulosa cells as a source and target organ for tumor necrosis factor-$\kappa$. FEBS Lett. 261:253-255   DOI   ScienceOn
55 김원식, 한승로, 조근자, 김수일, 박창식. 2005. 흰쥐난소에서 황체내 대식세포에 관한 형태학적 연구 : 면역조직화학적 및 투과전자현미경적 연구. 대한해부학회지. 38(3):251-258
56 Duncan, W. C., Rodger, F. E. and Illingworth, P. J. 1998. The human corpus luteum reduction in macrophages during simulated maternal recognition of pregnancy. Hum, Reprod. 13(9):2435-2442   DOI   ScienceOn
57 Pate, J. L. 1994. Cellular components involved In luteolysis. J. Anim. Sci. 72: 1884-1890
58 Funayama, Y., Sasano, H. and Suzuki, T, 1996. Cell turnover in normal cycling human ovary. J. Clin. Endocrinol. Metab. 81:828-834   DOI
59 Okuda, K., Uenoyama, Y., Lee, K. W., Sakumoto, R. and Skarzynski, D. J. 1998. Progesterone stimulation by prostaglandin F2$\alpha$ involves protein kinase C pathway in cultured bovine luteal cells. J. Reprod. Dev. 44:79-84   DOI   ScienceOn
60 Luck, M. R and Zhao, Y. 1995. Structural remodelling of reproductive tissues. J. Endocrinol. 146:191-195   DOI   ScienceOn
61 Phariss, B. B., Cornette, J. C. and Gutnecht, G. D. 1970. Vascular control of luteal steroidogenesis. J. Reprod. Fertil. Suppl. 10:97-103
62 박창식, 한승로. 김수일, 조근자, 김원식. 2004. 돼지난소에서 난포폐쇄시 과립층세포의 아포토시스와 대식세포에 관한 형태학적 연구. 동물자원과학지 46(4):1-14
63 Bukovsky, A., Caudle, M. R., Keenan, A, Wimalasena, J., Foster, J. S. and van Meter, S. E. 1995. Quantitative evaluation of the cell cycle-related retinoblastoma protein and localization of Thy-l differentiation protein and macrophages during follicular development and atresia, and in human corpora lutea. Biol. Reprod. 52:776-792   DOI   ScienceOn
64 Roby, K. F., Weed, J., Lyles, R. and Terranova, P. F. 1993. Immunological evidence for a human ovarian tumor necrosis factor-alpha. J. Clin. Endocrinol. Metab. 71:1096-1102   DOI
65 Shikone, T., Yamoto, M. and Kokawa, K. 1996. Apoptosis of human corpora lutea during cyclic Luteal regression and early pregnancy. J. Clin. Endocrinol. Metab. 81:2376-2380   DOI
66 Sawyer, H. R., Niswender, K D., Braden, T. D. and Niswender, G. D. 1990. Nuclear changes in ovine luteal cells in response to PGF2$\kappa$. Domest. Anim. Endocrinol. 7:229-238   DOI   ScienceOn
67 Hansel, W., Concannon, P. W. and Lukaszewska, J. H. 1973. Corpora lutea of the large domestic ruminants. Biol. Reprod. 8:222-245   DOI
68 Rodger, F. E., Fraser, H. M. and Duncan, W. C. 1995. Immunolocalization of bcl-2 in the human corpus luteum. Mol. Hum. Reprod. 1:1566-1570
69 Hehnkc. K. E., Christenson, L. K., Ford, S. P. and Taylor, M. 1994. Macrophage infiltration into the porcine corpus luteum during prostaglandin F2$\kappa$ induced luteolysis. Biol. Reprod. 50:10-15   DOI   ScienceOn