The Functions and Regulation of Cell Populations Comprising the Corpus Luteum during the Ovarian Cycle

The Ovary: Second Edition

Volumn , Issue , 2004, Pages 169-184

  Stouffer, Richard L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

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[No Author keywords available]

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EID: 84942795652     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012444562-8/50011-2     Document Type: Chapter

References (122)

1. Stouffer R.L., Brannian J.D. The function and regulation of cell populations composing the corpus luteum of the ovarian cycle. The Ovary 1993, 245-259. Raven Press, New York. 1st ed. E.Y. Adashi, P.C.K. Leung (Eds.).
2. Hazzard T.M., Stouffer R.L. Angiogenesis in ovarian follicular and luteal development. Clinical Obstetrics and Gynaecology: Angiogenesis in the Female Reproductive Tract 2000, 883-900. Bailliere Tindall, London. S. Arulkumaran (Ed.).
3. Lei Z.M., Chegini N., Rao C.V. Quantitative cell composition of human and bovine corpora lutea from various reproductive states. Biol. Reprod. 1991, 44:1148-1156.
4. Christenson L.K., Stouffer R.L. Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology 1996, 137:367-374.
5. Knickerbocker J.J., Wiltbank M.C., Niswender G.D. Mechanisms of luteolysis in domestic livestock. Domest. Anim. Endocrinol. 1988, 5:91-107.
6. Paavola L.G. 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. 1979, 154:337-364.
7. Gaytan F., Morales C., Garcia-Pardo L., Reymundo C., Bellido C., Sanchez-Criado J.E. A quantitative study of changes in the human corpus luteum microvasculature during the menstrual cycle. Biol. Reprod. 1999, 60:914-919.
8. Reynolds L.P., Redmer D.A. Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary. J. Anim. Sci. 1998, 76:1671-1681.
9. Koos R.D. Ovarian angiogenesis. The Ovary 1993, 433-453. Raven Press, New York. 1st ed. E.Y. Adashi, P.C.K. Leung (Eds.).
10. Stacker S.A., Achen M.G. The vascular endothelial growth factor family: Signalling for vascular development. Growth Factors 1999, 17:1-11.
11. Ancelin M., Buteau-Lozano H., Meduri G., Osborne-Pellegrin M., Sordello S., Plouet J., Perrot-Applanat M. A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus. Proc. Natl. Acad. Sci. USA 2002, 99:6023-6028.
12. Stalmans I., Ng Y.-S., Rohan R., Fruttiger M., Bouche A., Yuce A., Fujisawa H., Hermans B., Shani M., Jansen S., Hicklin D., Anderson D.J., Gardiner T., Hammes H.-P., Moons L., Dewerchin M., Collen D., Carmeliet P., D'Amore P.A. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 2001, 109:327-336.
13. Robinson C.J., Stringer S.E. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J. Cell Sci. 2001, 114:853-865.
14. Ravindranath N., Little-Ihrig L., Phillips H.S., Ferrara N., Zeleznik A.J. Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology 1992, 131:254-260.
15. Hazzard T.M., Christenson L.K., Stouffer R.L. Changes in expression of vascular endothelial growth factor and angiopoietin-1 and -2 in the macaque corpus luteum during the menstrual cycle. Mol. Hum. Reprod. 2000, 6:993-998.
16. Redmer D.A., Doraiswamy V., Bortnem B.J., Fisher K., Jablonka-Shariff A., Grazul-Bilska A.T., Reynolds L.P. Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol. Reprod. 2001, 65:879-889.
17. Laitinen M., Ristimaki A., Honkasalo M., Narko K., Paavonen K., Ritvos O. Differential hormonal regulation of vascular endothelial growth factors VEGF, VEGF-B, and VEGF-C messenger ribonucleic acid levels in cultured human granulosa-luteal cells. Endocrinology 1997, 138:4748-4756.
18. Martinez-Chequer J.C., Stouffer R.L., Hazzard T.M., Patton P.E., Molskness T.A. Insulin-like growth factor (IGF)-1 and -2, but not hypoxia, synergize with gonadotropin hormone to promote vascular endothelial growth factor (VEGF)-A secretion by monkey granulosa cells from preovulatory follicles. Biol. Reprod. 2003, 68:1112-1118.
19. Koos R.D. Increased expression of vascular endothelial growth/permeability factor in the rat ovary following an ovulatory gonadotropin stimulus: Potential roles in follicle rupture. Biol. Reprod. 1995, 52:1426-1435.
20. Christenson L.K., Stouffer R.L. Follicle-stimulating hormone and luteinizing hormone/chorionic gonadotropin stimulation of vascular endothelial growth factor production by macaque granulosa cells from pre- and periovulatory follicles. J. Clin. Endocrinol. Metab. 1997, 82:2135-2142.
21. Molskness T.A., Stouffer R.L. Hypoxia, but not gonadotropin, stimulates vascular endothelial growth factor production by primate luteal cells in vitro. Biol. Reprod. 2002, 66(Suppl 1):283-284. (abstract 457).
22. Doraiswamy V., Grazul-Bilska A.T., Ricke W.A., Redmer D.A., Reynolds L.P. Immunoneutralization of angiogenic activity from ovine corpora lutea (CL) with antibodies against fibroblast growth factor (FGF)-2 and vascular endothelial growth factor (VEGF). Biol. Reprod. 1995, 52(Suppl 1):112. (abstract 223).
23. Zimmermann R.C., Hartman T., Bohlen P., Sauer M.V., Kitajewski J. Preovulatory treatment of mice with anti-VEGF receptor 2 antibody inhibits angiogenesis in corpora lutea. Microvasc. Res. 2001, 62:15-25.
24. Fraser H.M., Dickson S.E., Lunn S.F., Wulff C., Morris K.D., Carroll V.A., Bicknell R. Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 2000, 141:995-1000.
25. Dickson S.E., Bicknell R., Fraser H.M. Midluteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor. J. Endocrinol. 2001, 168:409-416.
26. Hazzard T.M., Xu F., Stouffer R.L. Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biol. Reprod. 2002, 67:1305-1312.
27. Zimmermann R.C., Xiao E., Bohlen P., Ferin M. Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey. Endocrinology 2002, 143:2496-2502.
28. Christenson L.K., Stouffer R.L. Isolation and culture of microvascular endothelial cells from the primate corpus luteum. Biol. Reprod. 1996, 55:1397-1404.
29. Ward N.L., Dumont D.J. The angiopoietins and Tie2/Tek: Adding to the complexity of cardiovascular development. Cell Dev. Biol. 2002, 13:19-27.
30. Hanahan D. Signaling vascular morphogenesis and maintenance. Science 1997, 277:48-50.
31. Wulff C., Wilson H., Largue P., Duncan W.C., Armstrong D.G., Fraser H.M. Angiogenesis in the human corpus luteum: Localization and changes in angiopoietins, Tie-2, and vascular endothelial growth factor messenger ribonucleic acid. J. Clin. Endocrinol. Metab. 2000, 85:4302-4309.
32. Goede V., Schmidt T., Kimmina S., Kozian D., Augustin H.G. Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Lab. Invest. 1998, 78:1385-1394.
33. Hazzard T.M., Molskness T.A., Chaffin C.L., Stouffer R.L. Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the periovulatory interval. Mol. Hum. Reprod. 1999, 5:1115-1121.
34. LeCouter J., Kowalski J., Foster J., Hass P., Zhang Z., Dillard-Telm L., Frantz G., Rangell L., DeGuzman L., Keller G.A., Peale F., Gurney A., Hillan K.J., Ferrara N. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 2001, 412:877-884.
35. Masuda Y., Takatsu Y., Terao Y., Kumano S., Ishibashi Y., Suenaga M., Abe M., Fukusumi S., Watanabe T., Shintani Y., Yamada T., Hinuma S., Inatomi N., Ohtaki T., Onda H., Fujino M. Isolation and identification of EG-VEGF/prokineticins as cognate ligands for two orphan G-protein-coupled receptors. Biochem. Biophys. Res. Commun. 2002, 293:396-402.
36. Borman S.M., Hennebold J.D., Stouffer R.L. Endocrine gland-vascular endothelial growth factor (EG-VEGF) expression in the nonhuman primate corpus luteum during the natural menstrual cycle. Proceedings of the XIVth Ovarian Workshop 2002, Abstract from.
37. 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, 13:953-959.
38. Ratcliffe K.E., Anthony F.W., Richardson M.C., Stones R.W. Morphology and functional characteristics of human ovarian microvascular endothelium. Hum. Reprod. 2000, 14:1549-1554.
39. Fenyves A.M., Saxer M., Spanel-Borowski K. Bovine microvascular endothelial cells of separate morphology differ in growth and response to the action of interferon-gamma. Experientia 1994, 50:99-104.
40. Hixenbaugh E.A., Strauss J.F., Paavola L.G. Establishment of heterogeneity among blood vessels: Hormone-influenced appearance of hepatic lipase in specific subsets of the ovarian microvasculature. Anat. Rec. 1993, 235:487-500.
41. Corner G.W. On the origin of the corpus luteum of the sow from both granulosa and theca interna. Am. J. Anat. 1919, 26:117-183.
42. Fields P.A. Relaxin and other luteal secretory peptides: Cell localization and function in the ovary. Ultrastructure of the Ovary 1991, 177-198. Kluwer Academic Publishers, Norwell, Mass. G. Familiari, S. Makabe, P.M. Motta (Eds.).
43. Meidan R., Girsh E., Blum O., Aberdam E. In vitro differentiation of bovine theca and granulosa cells into small and large luteal-like cells: Morphological and functional characteristics. Biol. Reprod. 1990, 43:913-921.
44. Alila H.W., Hansel W. Origin of different cell types in the bovine corpus luteum as characterized by specific monoclonal antibodies. Biol. Reprod. 1984, 31:1015-1025.
45. Sanders S.L., Stouffer R.L. Localization of steroidogenic enzymes in macaque luteal tissue during the menstrual cycle and simulated early pregnancy: Immunohistochemical evidence supporting the two-cell model for estrogen production in the primate corpus luteum. Biol. Reprod. 1996, 56:1077-1087.
46. Sasano H., Okamoto M., Mason J.I., Simpson E.R., Mendelson C.R., Sasano N., Silverberg S.G. Immunolocalization of aromatase, 17α-hydroxylase and side-chain-cleavage cytochromes P450 in the human ovary. J. Reprod. Fertil. 1989, 85:163-165.
47. Watson E.D. Compartmentalization of steroidogenesis by the equine corpus luteum. Theriogenology 2000, 53:1459-1466.
48. Marut E.L., Huang S.-C., Hodgen G.D. Distinguishing the steroidogenic roles of granulosa and theca cells of the dominant ovarian follicle and corpus luteum. J. Clin. Endocrinol. Metab. 1983, 57:925-930.
49. Milvae R.A., Alila H.W., Bushmich S.L., Hansel W. Bovine corpus luteum function after removal of granulosa cells from the preovulatory follicle. Domest. Anim. Endocrinol. 1991, 8:439-443.
50. Juengel J.L., Niswender G.D. Molecular regulatiion of luteal progesterone synthesis in domestic ruminants. J. Reprod. Fertil. 1999, 54:193-205. (Suppl.).
51. Sasano H., Suzuki T. Localization of steroidogenesis and steroid receptors in human corpus luteum. Semin. Reprod. Endocrinol. 1997, 15:345-351.
52. Hoyer P.B. Regulation of luteal regression: The ewe as a model. J. Soc. Gynecol. Invest. 1998, 5:49-57.
53. Diaz F.J., Anderson L.E., Wu Y.L., Rabot A., Tsai S.J., Wiltbank M.C. Regulation of progesterone and prostaglandin F2α production in the CL. Mol. Cell. Endocrinol. 2002, 191:65-80.
54. Meidan R., Levy N. Endothelin-1 receptors and biosynthesis in the corpus luteum: Molecular and physiological implications. Domest. Anim. Endocrinol. 2002, 5340:1-12.
55. Denning-Kendall P.A., Guldenaar S.E.F., Wathes D.C. Evidence for a switch in the site of relaxin production from small theca-derived cells to large luteal cells during early pregnancy in the pig. J. Reprod. Fert. 1989, 85:261-271.
56. Brannian J.D., Stouffer R.L. Cellular approaches to understanding the function and regulation of the primate corpus luteum. Semin. Reprod. Endocrinol. 1991, 9:341-351.
57. Stoelk E., Chegini N., Lei Z.M., Rao C.V., Bryant-Greenwood G., Sanfilippo J. Immunocytochemical localization of relaxin in human corpora lutea: Cellular and subcellular distribution and dependence on reproductive state. Biol. Reprod. 1991, 44:1140-1147.
58. Taylor M.J., Clark C.L., Frawley L.S. Evidence for the existence of a luteal cell type that is steroidogenic and releases relaxin. Proc. Soc. Exp. Biol. Med. 1987, 185:469-473.
59. Brannian J.D., Shiigi S.M., Stouffer R.L. Differential uptake of fluorescent-tagged low-density lipoprotein by cells from the primate corpus luteum: Isolation and characterization of subtypes of small and large luteal cells. Endocrinology 1991, 129:3247-3253.
60. Fehr S., Ivell R., Koll R., Schams D., Fields M., Richter D. Expression of the oxytocin gene in the large cells of the bovine corpus luteum. FEBS Lett. 1987, 210:45-50.
61. Jarry H., Hornschuh R., Pitzel L., Wuttke W. Demonstration of oxytocin release by bovine luteal cells utilizing the reverse hemolytic plaque assay. Biol. Reprod. 1992, 46:408-413.
62. Hild-Petito S.A., Shiigi S.M., Stouffer R.L. Isolation and characterization of cell subpopulations from the monkey corpus luteum of the menstrual cycle. Biol. Reprod. 1989, 40:1075-1085.
63. Brannian J.D., Stouffer R.L. Progesterone production by monkey luteal cell subpopulations at different stages of the menstrual cycle: Changes in agonist responsiveness. Biol. Reprod. 1991, 44:141-149.
64. Ohara A., Mori T., Taii S., Ban C., Narimoto K. Functional differentiation in steroidogenesis of two types of luteal cells isolated from mature human corpora lutea of menstrual cycle. J. Clin. Endocrinol. Metab. 1987, 65:1192-1200.
65. Di Simone N., Castellani R., Lanzone A., Caruso A., Mancuso S. Human growth hormone enhances progesterone production by human luteal cells in vitro. II. Evidence of a distinct effect on two luteal cell types. Fertil. Steril. 1993, 60:47-52.
66. Mori T., Nihnobu K., Takeuchi S., Ohno Y., Tojo S. Interrelation between luteal cell types in steroidogenesis in vitro of human corpus luteum. J. Steroid. Biochem. 1983, 19:811-815.
67. Sanders S.L., Stouffer R.L., Brannian J.D. Androgen production by monkey luteal cell subpopulations at different stages of the menstrual cycle. J. Clin. Endocrinol. Metab. 1996, 81:591-596.
68. Retamales I., Carrasco I., Troncoso J.L., Las Heras J., Devoto L., Vega M. Morpho-functional study of human luteal cell subpopulations. Hum. Reprod. 1994, 9:591-596.
69. 2α. Endocrinology 1992, 131:743-748.
70. Metcalf M.G., Braiden V., Livesey J.H. Retention of normal ovarian function after hysterectomy. J. Endocrinol. 1992, 135:597-602.
71. Carrasco I., Troncoso J.L., Devoto L., Vega M. Differential steroidogenic response of human luteal cell subpopulations. Hum. Reprod. 1996, 11:1609-1614.
72. Friden B.E., Hagstrom H.-G., Lindblom B., Sjoblom P., Wallin A., Brännström M., Hahlin M. Cell characteristics and functions of two enriched fractions of human luteal cells during prolonged culture. Mol. Hum. Reprod. 1999, 5:714-719.
73. Sanders S.L., Stouffer R.L. Gonadotropin- and lipoprotein-supported progesterone production by primate luteal cell types in culture. Endocrine 1995, 3:169-175.
74. Broadley C., Menzies G.S., Bramley T.A., Watson E.D. Isolation of cell populations from the mare corpus luteum: Comparison of mechanical and collagenase dissociation. J. Reprod. Fertil. 1994, 102:7-15.
75. Brannian J.D., Stouffer R.L., Shiigi S.M., Hoyer P.B. Isolation of ovine luteal cell subpopulations by flow cytometry. Biol. Reprod. 1993, 48:495-502.
76. Duffy D.M., Stewart D.R., Stouffer R.L. Titrating luteinizing hormone replacement to sustain the structure and function of the corpus luteum after gonadotropin-releasing hormone antagonist treatment in rhesus monkeys. J. Clin. Endocrinol. Metab. 1999, 84:342-349.
77. Mais V., Kazer R.R., Cetel N.S., Rivier J., Vale W., Yen S.S.C. The dependency of folliculogenesis and corpus luteum function on pulsatile gonadotropin secretion in cycling women using a gonadotropin-releasing hormone antagonist as a probe. J. Clin. Endocrinol. Metab. 1986, 62:1250-1255.
78. Ellinwood W.E., Norman R.L., Spies H.G. Changing frequency of pulsatile luteinizing hormone and progesterone secretion during the luteal phase of the menstrual cycle of rhesus monkeys. Biol. Reprod. 1984, 31:714-722.
79. Arioua R.K., Benhaim A., Feral C., Leymarie P. Luteotrophic factors in hyperstimulated pseudopregnant rabbit: II-High sensitivity to hCG of luteal tissue and small luteal cells. J. Endocrinol. 1997, 154:259-265.
80. Gregorasczuk E.L. Different response of porcine large and small luteal cells to PRL in terms of progesterone and estradiol secretion in vitro. Exp. Clin. Endocrinol. 1990, 96:234-237.
81. Meduri G., Vuhai-Luuthi M.T., Jolivet A., Milgrom E. New functional zonation in the ovary as shown by immunohistochemistry of luteinizing hormone receptor. Endocrinology 1992, 131:366-373.
82. Ottander U., Nakata M., Backstrom T., Liu K., Ny T., Olofsson J.I. Compartmentalization of human chorionic gonadotrophin sensitivity and luteinizing hormone receptor mRNA in different subtypes of the human corpus luteum. Hum. Reprod. 1997, 12:1037-1042.
83. Giudice L.C. Insulin-like growth factor family in Graafian follicle development and function. J. Soc. Gynecol. Invest. 2001, 8:S26-S29.
84. Hartshorne G.M., Bell S.C., Waites G.T. Binding proteins for insulin-like growth factors in the human ovary: Identification, follicular fluid levels, and immunohistological localization of the 29-32 Kd type 1 binding protein, IGF-BP1. Hum. Reprod. 1990, 5:649-660.
85. Fraser H.M., Lunn S.F., Kim H., Erickson G.F. Insulin-like growth factor binding protein-3 mRNA expression in endothelial cells of the primate corpus luteum. Hum. Reprod. 1998, 13:2180-2185.
86. Young K.A., Hennebold J.D., Stouffer R.L. Dynamic expression of mRNAs and proteins for matrix metalloproteinases and their tissue inhibitors in the primate corpus luteum during the menstrual cycle. Mol. Hum. Reprod. 2002, 8:833-840.
87. Itskovitz-Eldor J., Bruneval P., Soubrier F., Thaler I., Corvol P., Sealey J.E. Localization of renin gene expression to monkey ovarian theca cells by in situ hybridization. J. Clin. Endocrinol. Metab. 1992, 75:1374-1380.
88. Grazul-Bilska A.T., Redmer D.A., Reynolds L.P. Cellular interactions in the corpus luteum. Semin. Reprod. Endocrinol. 1997, 15:383-393.
89. 2α in corpus luteum function. Rev. Reprod. 2000, 5:1-5.
90. Nussdorfer G.G., Rossi G.P., Malendowicz L.K., Mazzocchi G. Autocrine-paracrine endothelin system in the physiology and pathology of steroid-secreting tissues. Pharmacol. Rev. 1999, 51:406-437.
91. Kennedy R.L., Haynes W.G., Webb D.J. Endothelins as regulators of growth and function in endocrine tissues. Clin. Endocrinol. 1993, 39:259-265.
92. Girsh E., Milvae R.A., Wang W., Meidan R. Effect of endothelin-1 on bovine luteal cell function: Role in PGF2α-induced anti-steroidogenic action. Endocrinology 1996, 137:1306-1312.
93. 2α-induced luteal regression in the ewe. Biol. Reprod. 2001, 64:1619-1623.
94. Mancina R., Barni T., Calogero A.E., Filippi S., Amerini S., Peri A., Susini T., Vannelli G.B., Burrello N., Forti G., Maggi M. Identification, characterization, and biological activity of endothelin receptors in human ovary. J. Clin. Endocrinol. Metab. 1997, 82:4122-4129.
95. Apa R., Miceli F., de Feo D., Mastrandrea M.L., Mancuso S., Napolitano M., Lanzone A. Endothelin-1 inhibits basal and human chorionic gonadotrophin-stimulated progesterone production. Hum. Reprod. 1998, 13:2425-2429.
96. Yoshioka S., Fujiwara H., Yamada S., Tatsumi K., Nakayama T., Higuchi T., Inoue T., Maeda M., Fujii S. Endothelin-converting enzyme-1 is expressed on human ovarian follicles and corpora lutea of menstrual cycle and early pregnancy. J. Clin. Endocrinol. Metab. 1998, 83:3943-3950.
97. Brännström M., Friden B. Immune regulation of corpus luteum function. Semin. Reprod. Endocrinol. 1997, 15:363-370.
98. Bukulmez O., Arici A. Leukocytes in ovarian function. Hum. Reprod. Update 2000, 6:1-15.
99. Brännström M., Giesecke L., van den Heuvel C.J., Moore I.C., Robertson S.A. Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol. Reprod. 1994, 50:1161-1167.
100. Standaert F.S., Zamor C.S., Chew B.P. Quantitative and qualitative changes in blood leukocytes in the porcine ovary. Am. J. Reprod. Immunol. 1991, 215:163-168.
101. Brännström M., Pascoe V., Norman R.J., McClure N. Localization of leukocyte subsets in the follicle wall and in the corpus luteum throughout the human menstrual cycle. Fertil. Steril. 1994, 61:488-495.
102. Wang L.J., Pascoe V., Petrucco O.M., Norman R.J. Distribution of leukocyte subpopulations in the human corpus luteum. Hum. Reprod. 1992, 7:197-202.
103. Bagavandoss P., Wiggins R.C., Kunkel S.L., Remick D.G., Keyes P.L. Tumor necrosis factor production and accumulation of inflammatory cells in the corpus luteum of pseudopregnancy and pregnancy in rabbits. Biol. Reprod. 1990, 42:367-376.
104. Murdoch W.J., Steadman L.E., Belden E.L. Immunoregulation of luteolysis. Med. Hypotheses 1988, 27:197-199.
105. Mori T. Immuno-endocrinology of cyclic ovarian function. Am. J. Reprod. Immunol. 1990, 23:80-89.
106. Bukovsky A., Caudle M.R., Keenan J.A., Wimalasena J., Upadhyaya N.B., Van Meter S.E. Is corpus luteum regression an immune-mediated event? Localization of immune system components and luteinizing hormone receptor in human corpora lutea. Biol. Reprod. 1995, 53:1373-1384.
107. Pate J.L., Keyes P.L. Immune cells in the corpus luteum: Friends or foes. Reproduction 2001, 122:665-676.
108. Castro A., Castro O., Troncoso J.L., Kohen P., Simon C., Vega M., Devoto L. Luteal leukocytes are modulators of the steroidogenic process of human mid-luteal cells. Hum. Reprod. 1998, 13:1584-1589.
109. Hashii K., Fujiwara H., Yoshioka S., Kataoka N., Yamada S., Hirano T., Mori T., Fujii S., Maeda M. Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and nonpregnant women: Possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation. Hum. Reprod. 1998, 13:2738-2744.
110. Seiner S.J., Schramm W., Keyes P.L. Effect of treatment with methylprednisolone on duration of pseudopregnancy and on macrophages and T lymphocytes in rabbit corpora lutea. J. Reprod. Fertil. 1992, 96:347-353.
111. Wang F., Riley J.C.M., Behrman H.R. Immunosuppressive levels of glucocorticoid block extrauterine luteolysins in the rat. Biol. Reprod. 1993, 49:66-73.
112. Gaytan F., Morales C., Bellido C., Sanchez-Criado J.E. Selective apoptosis of luteal endothelial cells in dexamethasone-treated rats leads to ischemic necrosis of luteal tissue. Biol. Reprod. 2002, 66:232-240.
113. Bagavant H., Adams S., Terranova P., Chang A., Kraemer F.W., Lou Y., Kasai K., Luo A.M., Tung K.S.K. Autoimmune ovarian inflammation triggered by proinflammatory (Th1) T cells is compatible with normal ovarian function in mice. Biol. Reprod. 1999, 61:635-642.
114. Arici A., Oral E., Bukulmez O., Buradagunta S., Engin O., Olive D.L. Interleukin-8 expression and modulation in human prevulatory follicles and ovarian cells. Endocrinology 1996, 137:3762-3769.
115. Ujioka T., Matsukawa A., Tanaka N., Matsuura K., Yoshinaga M., Okamura H. Interleukin-8 as an essential factor in the human chorionic gonadotropin-induced rabbit ovulatory process: Interleukin-8 induces neutrophil accumulation and activation in ovulation. Biol. Reprod. 1998, 58:526-530.
116. Townson D.H., Warren J.S., Flory C.M., Keyes P.L. Expression of monocyte chemoattractant protein-1 in the corpus luteum in the rat. Biol. Reprod. 1996, 54:513-520.
117. Penny L.A., Armstrong D.G., Baxter G., Hogg C., Kindahl H., Bramley T., Watson E.D., Webb R. Expression of monocyte chemoattractant protein-1 in the bovine corpus luteum around the time of natural luteolysis. Biol. Reprod. 1998, 59:1464-1469.
118. Senturk L.M., Seli E., Gutierrez L.S. Monocyte chemotactic protein-1 expression in human corpus luteum. Mol. Hum. Reprod. 1999, 5:697-702.
119. Penny L.A. Monocyte chemoattractant protein 1 in luteolysis. Rev. Reprod. 2000, 5:63-66.
120. 2α. Biol. Reprod. 1998, 58:169-174.
121. Hosang K., Knoke I., Klaudiny J., Wempe F., Wuttke W., Scheit K.H. Porcine luteal cells express monocyte chemoattractant protein 1 (MCP-1): Analysis by polymerase chain reaction and cDNA cloning. Biochem. Biophys. Res. Commun. 1994, 199:962-968.
122. Ichikawa S., Uchino S., Hirata Y. Lymphatic and blood vasculature of the forming corpus luteum. Lymphology 1987, 20:73-83.