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

Biology of Reproduction

Volumn 56, Issue 5, 1997, Pages 1077-1087

  Sanders, Sheryl L ^a   Stouffer, Richard L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3BETA HYDROXY DELTA5 STEROID DEHYDROGENASE; AROMATASE; CYTOCHROME P450; STEROID 17ALPHA MONOOXYGENASE;

ANIMAL TISSUE; ARTICLE; CORPUS LUTEUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; ESTROGEN SYNTHESIS; FEMALE; IMMUNOHISTOCHEMISTRY; MACACA; MENSTRUAL CYCLE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; TISSUE DISTRIBUTION;

ANIMALIA; MACACA; MACACA MULATTA; PRIMATES;

EID: 0030978581     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod56.5.1077     Document Type: Article

References (56)

1. Stouffer RL, Bennett LA, Hodgen GD. Estrogen production by luteal cells isolated from rhesus monkeys during the menstrual cycle: correlation with spontaneous luteolysis. Endocrinology 1980; 106:519-525.
2. Hild-Petito SA, Shiigi SM, Stouffer RL. Isolation and characterization of cell subpopulations from the monkey corpus luteum of the menstrual cycle. Biol Reprod 1989; 40:1075-1085.
3. Sanders SL, Stouffer RL, Brannian JD. Androgen production by monkey luteal cell subpopulations at different stages of the menstrual cycle. J Clin Endocrinol & Metab 1996; 81:591-596.
4. 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.
5. Retamales I, Carrasco I, Troncoso JL, Las Heras J, Devoto L, Vega M. Morpho-functional study of human luteal cell subpopulations. Hum Reprod 1994; 9:591-596.
6. Sasano H, Okamoto M, Mason JI, Simpson ER, Mendelson CR, Sasano N, Silverberg SG. Immunolocalization of aromatase, 17α-hydroxylase and side-chain-cleavage cytochromes P450 in the human ovary. J Reprod Fertil 1989; 85:163-165.
7. Tamura T, Kitawaki J, Yamamoto T, Osawa Y, Kominami S, Takemori S, Okada H. Immunohistochemical localization of 17α-hydroxylase/ C17-20 lyase and aromatase cytochrome P-450 in the human ovary during the menstrual cycle. J Endocrinol 1992; 135:589-595.
8. Strauss III JF, Golos TG, Silavin SL, Soto EA, Takagi K. Involvement of cyclic AMP in the function of granulosa and luteal cells: regulation of steroidogenesis. In: Haseltine FP, First NL (eds.), Meiotic Inhibition: Molecular Control of Meiosis. New York: Alan R. Liss, Inc.; 1988: 177-200.
9. Brannian JD, Stouffer RL. Progesterone production by monkey luteal cell subpopulations at different stages of the menstrual cycle: changes in agonist responsiveness. Biol Reprod 1991; 44:141-149.
10. Sanders SL, Stouffer RL. Gonadotropin- and lipoprotein-supported progesterone production by primate luteal cell types in culture. Endocrine 1995; 3:169-175.
11. Strauss III JF, Miller WL. Molecular basis of ovarian steroid synthesis. In: Hillier SG (ed.), Ovarian Endocrinology. Oxford: Blackwell Scientific; 1991: 25-72.
12. Doody KJ, Lorence MD, Mason JI, Simpson ER. Expression of messenger ribonucleic acid species encoding steroidogenic enzymes in human follicles and corpora lutea throughout the menstrual cycle. J Clin Endocrinol & Metab 1990; 70:1041-1045.
13. Bassett SG, Little-Ihrig LL, Mason JI, Zeleznik AJ. Expression of messenger ribonucleic acids that encode for 3β-hydroxysteroid dehydrogenase and cholesterol side-chain cleavage enzyme throughout the luteal phase of the macaque menstrual cycle. J Clin Endocrinol & Metab 1991; 72:362-366.
14. 5-4 isomerase messenger ribonucleic acids in the primate corpus luteum. Endocrinology 1992; 131:2065-2070.
15. Benyo DF, Little-Ihrig L, Zeleznik AJ. Noncoordinated expression of luteal cell messenger ribonucleic acids during human chorionic gonadotropin stimulation of the primate corpus luteum. Endocrinology 1993; 133:699-704.
16. Sasano H, Mori T, Sasano N, Nagura H, Mason JI. Immunolocalization of 3β-hydroxysteroid dehydrogenase in human ovary. J Reprod Fertil 1990; 89:743-751.
17. 4-isomerase in human ovary. J Clin Endocrinol & Metab 1992; 74:994-998.
18. Suzuki T, Sasano H, Tamura M, Aoki H, Fukaya T, Yajima A, Nagura H, Mason JI. Temporal and spatial localization of steroidogenic enzymes in premenopausal human ovaries: in situ hybridization and immunohistochemical study. Mol Cell Endocrinol 1993; 97:135-143.
19. Mossman HW, Duke KL. Comparative morphology of specific ovarian tissues and structures. In: Mossman HW, Duke KL (eds.), Comparative Morphology of the Mammalian Ovary. Madison: University of Wisconsin Press; 1973: 100-116.
20. Corner GW, Hartman CG, Bartelmez GW. Development, organization, and breakdown of the corpus luteum in the rhesus monkey. Contrib Embryol 1945; 204:119-146.
21. VandeVoort CA, Molskness TA, Stouffer RL. Adenylate cyclase in the primate corpus luteum during chorionic gonadotropin treatment simulating early pregnancy: homologous versus heterologous desensitization. Endocrinology 1988; 122:734-740.
22. Resko JA, Norman RL, Niswender GD, Spies HG. The relationship between progestins and gonadotropins during the late luteal phase of the menstrual cycle in rhesus monkeys. Endocrinology 1974; 94:128-135.
23. Resko JA, Ploem JG, Stadelman HL. Estrogens in fetal and maternal plasma of the rhesus monkey. Endocrinology 1975; 97:425-430.
24. Stouffer RL, Dahl KD, Hess DL, Woodruff TK, Mather JP, Molskness TA. Systemic and intraluteal infusion of inhibin A or activin A in rhesus monkeys during the luteal phase of the menstrual cycle. Biol Reprod 1994; 50:888-895.
25. Duffy DM, Hutchison JS, Stewart DR, Stouffer RL. Stimulation of primate luteal function by recombinant hCG and modulation of steroid, but not relaxin, production by an inhibitor of 3β-hydroxysteroid dehydrogenase during simulated early pregnancy. J Clin Endocrinol & Metab 1996; 81:2307-2313.
26. Slayden OD, Hirst JJ, Brenner RM. Estrogen action in the reproductive tract of rhesus monkeys during antiprogestin treatment. Endocrinology 1993; 132:1845-1856.
27. Christenson LK, Stouffer RL. Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology 1996; 137:367-374.
28. Black SM, Szklarz GD, Harikrishna JA, Lin D, Wolf CR, Miller WL. Regulation of proteins in the cholesterol side-chain cleavage system in JEG-3 and Y-1 cells. Endocrinology 1993; 132:539-545.
29. arom), and their use in its purification. Arch Biochem Biophys 1985; 243:480-491.
30. Shi S, Key ME, Kalra KL. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J Histochem Cytochem 1991; 39:741-748.
31. Duffy DM, Stouffer RL. Macaque luteal progesterone receptors and ovarian activity are regulated by CG and steroids during simulated early pregnancy. Biol Reprod 1995; 52(suppl 1):68 (abstract 48).
32. Deane HW, Lobel BL, Romney SL. Enzymic histochemistry of normal human ovaries of the menstrual cycle, pregnancy, and the early puerperium. Am J Obstet Gynecol 1962; 83:281-294.
33. Feinberg R, Cohen RB. A comparative histochemical study of the ovarian stromal lipid band, stromal theca cell, and normal ovarian follicular apparatus. Am J Obstet Gynecol 1965; 92:958-969.
34. Seegar Jones GE, Goldberg B, Woodruff JD. Histochemistry as a guide for interpretation of cell function. Am J Obstet Gynecol 1968; 100:76-83.
35. Brannian JD, Shiigi SM, Stouffer RL. 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.
36. Conley AJ, Kaminski MA, Dubowsky SA, Jablonka-Shariff A, Redmer DA, Reynolds LP. Immunohistochemical localization of 3β-hydroxysteroid dehydrogenase and P450 17α-hydroxylase during follicular and luteal development in pigs, sheep, and cows. Biol Reprod 1995; 52:1081-1094.
37. Lemon M, Loir M. Steroid release in vitro by two luteal cell types in the corpus luteum of the pregnant sow. J Endocrinol 1977; 72:351-359.
38. Ursely J, Leymarie P. Varying response to luteinizing hormone of two luteal cell types isolated from bovine corpus luteum. J Endocrinol 1979; 83:303-310.
39. Koos RD, Hansel W. The large and small cells of the bovine corpus luteum: ultrastructural and functional differences. In: Schwartz NB, Hunzicker-Dunn M (eds.), Dynamics of Ovarian Function. New York: Raven Press; 1981: 197-203.
40. Fritz MA, Fitz TA. The functional microscopic anatomy of the corpus luteum: the "small cell"-"large cell" controversy. Clin Obstet Gynecol 1991; 34:144-156.
41. McLean MP, Nelson SE, Billheimer JT, Gibori G. Differential capacity for cholesterol transport and processing in large and small rat luteal cells. Endocrinology 1992; 131:2203-2212.
42. 4 isomerase in the ovine corpus luteum. Biol Reprod 1993; 48:1185-1190.
43. 2α-induced luteolysis in cattle. Biol Reprod 1994; 50:349-356.
44. 4 isomerase messenger ribonucleic acid, activity and protein levels during the estrous cycle in the bovine ovary. Endocrinology 1990; 127:2141-2148.
45. 17α, adrenodoxin, and reduced nicotinamide adenine dinucleotide phosphate-cytochrome P-450 reductase in bovine follicles and corpora lutea. Changes in specific contents during the ovarian cycle. Endocrinology 1986; 118:1366-1374.
46. Voss AK, Fortune JE. Levels of messenger ribonucleic acid for cholesterol side-chain cleavage cytochrome P-450 and 3β-hydroxysteroid dehydrogenase in bovine preovulalory follicles decrease after the luteinizing hormone surge. Endocrinology 1993; 132:888-894.
47. Goldring NB, Durica JM, Lifka J, Hedin L, Ratoosh SL, Miller WL, Orly J, Richard JS. Cholesterol side-chain cleavage P450 messenger ribonucleic acid: evidence for hormonal regulation in rat ovarian follicles and constitutive expression in corpora lutea. Endocrinology 1987; 120:1942-1950.
48. Inkster SE, Brodie AMH. Expression of aromatase cytochrome P-450 in premenopausal and postmenopausal human ovaries: an immunocytochemical study. J Clin Endocrinol & Metab 1991; 73:717-726.
49. Suzuki T, Sasano H, Sasaki H, Fukaya T, Nagura H. Quantitation of P450 aromatase immunoreactivity in human ovary during the menstrual cycle: relationship between the enzyme activity and immunointensity. J Histochem Cytochem 1994; 42:1565-1573.
50. Fisch B, Margara RA, Winston RML, Hillier SG. Cellular basis of luteal steroidogenesis in the human ovary. J Endocrinol 1989; 122: 303-311.
51. Hodgen GD, Tullner WW, Vaitukaitis JL, Ward DN, Ross GT. Specific radioimmunoassay of chorionic gonadotropin during implantation in rhesus monkeys. J Clin Endocrinol & Metab 1974; 39:457-464.
52. Atkinson LE, Hotchkiss J, Fritz GR, Surve AH, Neill JD, Knobil E. Circulating levels of steroids and chorionic gonadotropin during pregnancy in the rhesus monkey, with special attention to the rescue of the corpus luteum in early pregnancy. Biol Reprod 1975; 12:335-345.
53. diZerega GS, Hodgen GD. Changing functional status of the monkey corpus luteum. Biol Reprod 1980; 23:253-263.
54. Ottobre JS, Stouffer RL. Persistent versus transient stimulation of the macaque corpus luteum during prolonged exposure to human chorionic gonadotropin: a function of age of the corpus luteum. Endocrinology 1984; 114:2175-2182.
55. Wilks JW, Noble AS. Steroidogenic responsiveness of the monkey corpus luteum to exogenous chorionic gonadotropin. Endocrinology 1983; 112:1256-1266.
56. Ellinwood WE, Stanczyk FZ, Lazur JJ, Novy MJ. Dynamics of steroid biosynthesis during the luteal-placental shift in rhesus monkeys. J Clin Endocrinol & Metab 1989; 69:348-355.