Heterogeneity of ovarian theca and interstitial gland cells in Mice

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Miyabayashi, Kanako ^a   Tokunaga, Kaori ^a   Otake, Hiroyuki ^a   Baba, Takashi ^a   Shima, Yuichi ^a   Morohashi, Kenichirou ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; PHOTOPROTEIN; RED FLUORESCENT PROTEIN; STEROIDOGENIC FACTOR 1; STEROIDOGENIC FACTOR 1, MOUSE;

AD4BP GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CELL SUBPOPULATION; CONTROLLED STUDY; EGFP GENE; ENHANCER REGION; FEMALE; FEMALE GENITAL TRACT PARAMETERS; FETUS; GENE EXPRESSION; GENOME ANALYSIS; IMMUNOCOMPETENT CELL; LEYDIG CELL; MALE; MARKER GENE; MOUSE; NONHUMAN; OVARIAN THECA; PERINATAL PERIOD; REPORTER GENE; SF 1 GENE; TRANSGENIC MOUSE; ADRENAL GLAND; AGING; ANIMAL; CELL LINEAGE; CLASSIFICATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPOPHYSIS; METABOLISM; NEWBORN; SIGNAL TRANSDUCTION; THECA CELL;

MAMMALIA; MUS; MUS MUSCULUS;

ADRENAL GLANDS; AGING; ANIMALS; ANIMALS, NEWBORN; CELL LINEAGE; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; LEYDIG CELLS; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; PITUITARY GLAND; SIGNAL TRANSDUCTION; STEROIDOGENIC FACTOR 1; THECA CELLS;

EID: 84935037788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128352     Document Type: Article

References (40)

1. Morohashi K, Baba T, Tanaka M. Steroid hormones and the development of reproductive organs. Sex Dev. 2013;7(1-3):61-79. doi: 10.1159/000356948 PMID: 24334966
2. Chaffin CL, Vandevoort CA. Follicle growth, ovulation, and luteal formation in primates and rodents: a comparative perspective. Exp Biol Med (Maywood). 2013;238(5):539-48. doi: 10.1177/1535370213489437 PMID:23856905
3. Juneau C, Dupont E, Luu-The V, Labrie F, Pelletier G. Ontogenesis of 3 beta-hydroxysteroid dehydrogenase delta 5-delta 4 isomerase in the rat ovary as studied by immunocytochemistry and in situ hybridization. Biol Reprod. 1993;48(2):226-34. PMID: 8439611
4. Morohashi K, Honda S, Inomata Y, Handa H, Omura T. A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J BiolChem. 1992;267(25):17913-9. PMID: 1517227
5. Honda S, Morohashi K, Nomura M, Takeya H, Kitajima M, Omura T. Ad4BP regulating steroidogenic P-450 gene is a member of steroid hormone receptor superfamily. J Biol Chem. 1993;268(10):7494-502. PMID: 8463279
6. Ikeda Y, Lala DS, Luo X, Kim E, Moisan MP, Parker KL. Characterization of the mouse FTZ-F1 gene, which encodes a key regulator of steroid hydroxylase gene expression. Mol Endocrinol. 1993;7(7):852-60. PMID: 8413309
7. Hoivik EA, Lewis AE, Aumo L, Bakke M. Molecular aspects of steroidogenic factor 1 (SF-1). Mol Cell Endocrinol. 2010;315(1-2):27-39. doi: 10.1016/j.mce.2009.11.006 PMID: 19932151
8. Schimmer BP, White PC. Minireview: steroidogenic factor 1: its roles in differentiation, development, and disease. Mol Endocrinol. 2010;24(7):1322-37. doi: 10.1210/me.2009-0519 PMID: 20203099
9. Luo X, Ikeda Y, Parker KL. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell. 1994;77(4):481-90. PMID: 8187173
10. Shinoda K, Lei H, Yoshii H, Nomura M, Nagano M, Shiba H, et al. Developmental defects of the ventromedial hypothalamic nucleus and pituitary gonadotroph in the Ftz-F1 disrupted mice. Developmental dynamics: an official publication of the American Association of Anatomists. 1995;204(1):22-9. PMID: 8563022
11. Sadovsky Y, Crawford PA, Woodson KG, Polish JA, Clements MA, Tourtellotte LM, et al. Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 sidechain-cleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proceedings of the National Academy of Sciences of the United States of America. 1995;92(24):10939-43. PMID: 7479914
12. Lalli E, Doghman M, Latre De Late P, El Wakil A, Mus-Veteau I. Beyond steroidogenesis: novel target genes for SF-1 discovered by genomics. Mol Cell Endocrinol. 2013;371(1-2):154-9. doi: 10.1016/j. mce.2013.02.006 PMID: 23419499
13. Baba T, Otake H, Sato T, Miyabayashi K, Shishido Y, Wang CY, et al. Glycolytic genes are targets of the nuclear receptor Ad4BP/SF-1. NatCommun. 2014;5:3634. doi: 10.1038/ncomms4634 PMID: 24727981
14. Griswold SL, Behringer RR. Fetal Leydigcell origin and development. Sex Dev. 2009;3(1):1-15. doi: 10.1159/000200077 PMID: 19339813
15. O'Shaughnessy PJ, Baker PJ, Heikkila M, Vainio S, McMahon AP. Localization of 17beta-hydroxysteroid dehydrogenase/17-ketosteroid reductase isoform expression in the developing mouse testis-androstenedione is the major androgen secreted by fetal/neonatal leydig cells. Endocrinology. 2000;141(7):2631-7. PMID: 10875268
16. O'Shaughnessy PJ, Willerton L, Baker PJ. Changes in Leydigcell gene expression during development in the mouse. Biol Reprod. 2002;66(4):966-75. PMID: 11906915
17. Douglas GC, O'Bryan MK, Hedger MP, Lee DK, Yarski MA, Smith AI, et al. The novel angiotensin-converting enzyme (ACE) homolog, ACE2, is selectively expressed by adult Leydig cells of the testis. Endocrinology. 2004;145(10):4703-11. PMID: 15231706
18. McDowell EN, Kisielewski AE, Pike JW, Franco HL, Yao HH, Johnson KJ. A transcriptome-wide screen for mRNAs enriched in fetal Leydig cells: CRHR1 agonism stimulates rat and mouse fetal testis steroidogenesis. PLoSOne. 2012;7(10):e47359. doi: 10.1371/journal.pone.0047359 PMID: 23133512
19. Shima Y, Miyabayashi K, Baba T, Otake H, Katsura Y, Oka S, et al. Identification of an enhancer in the Ad4BP/SF-1 gene specific for fetal Leydig cells. Endocrinology. 2012;153(1):417-25. doi: 10.1210/en. 2011-1407 PMID: 22128023
20. Shima Y, Miyabayashi K, Haraguchi S, Arakawa T, Otake H, Baba T, et al. Contribution of Leydig and Sertoli cells to testosterone production in mouse fetal testes. Mol Endocrinol. 2013;27(1):63-73. doi: 10.1210/me.2012-1256 PMID: 23125070
21. Shima Y, Zubair M, Ishihara S, Shinohara Y, Oka S, Kimura S, et al. Ventromedial hypothalamic nucleus-specific enhancer of Ad4BP/SF-1 gene. Mol Endocrinol. 2005;19(11):2812-23. PMID: 15994202
22. Zubair M, Ishihara S, Oka S, Okumura K, Morohashi K. Two-step regulation of Ad4BP/SF-1 gene transcription during fetal adrenal development: initiation by aHox-Pbx1-Prep1 complex and maintenance viaautoregulation by Ad4BP/SF-1. Mol Cell Biol. 2006;26(11):4111-21. PMID: 16705164
23. Copeland NG, Jenkins NA, Court DL. Recombineering: a powerful new tool for mouse functional genomics. Nature reviews Genetics. 2001;2(10):769-79. PMID: 11584293
24. Lee EC, Yu D, Martinez De Velasco J, Tessarollo L, Swing DA, Court DL, et al. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloningof BAC DNA. Genomics. 2001;73(1):56-65. PMID: 11352566
25. Liu P, Jenkins NA, Copeland NG. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 2003;13(3):476-84. PMID: 12618378
26. Fatchiyah, Zubair M, Shima Y, Oka S, Ishihara S, Fukui-Katoh Y, et al. Differential gene dosage effects of Ad4BP/SF-1 on target tissue development. Biochem Biophys ResCommun. 2006;341(4):1036-45. PMID: 16458255
27. Miyabayashi K, Katoh-Fukui Y, Ogawa H, Baba T, Shima Y, Sugiyama N, et al. Aristaless related homeoboxgene, Arx, is implicated in mouse fetal Leydigcell differentiation possibly through expressing in the progenitor cells. PLoSOne. 2013;8(6):e68050. doi: 10.1371/journal.pone.0068050 PMID: 23840809
28. Morohashi K, Iida H, Nomura M, Hatano O, Honda S, Tsukiyama T, et al. Functional difference between Ad4BPand ELP, and their distributions in steroidogenic tissues. Mol Endocrinol. 1994;8(5):643-53. PMID: 8058072
29. Shima Y, Zubair M, Komatsu T, Oka S, Yokoyama C, Tachibana T, et al. Pituitary homeobox2 regulates adrenal4 binding protein/steroidogenic factor-1 gene transcription in the pituitary gonadotrope through interaction with the intronic enhancer. Mol Endocrinol. 2008;22(7):1633-46. doi: 10.1210/me. 2007-0444 PMID: 18417734
30. Hinshelwood MM, Repa JJ, Shelton JM, Richardson JA, Mangelsdorf DJ, Mendelson CR. Expression of LRH-1 and SF-1 in the mouse ovary: localization in different cell types correlates with differing function. Molecular and cellular endocrinology. 2003;207(1-2):39-45. PMID: 12972182
31. Stocco C. Aromatase expression in the ovary: hormonal and molecular regulation. Steroids. 2008;73(5):473-87. doi: 10.1016/j.steroids.2008.01.017 PMID: 18321551
32. Karpova T, Presley J, Manimaran RR, Scherrer SP, Tejada L, Peterson KR, et al. A FTZ-F1-containing yeast artificial chromosome recapitulates expression of steroidogenic factor 1 in vivo. Mol Endocrinol. 2005;19(10):2549-63. PMID: 15961510
33. Morohashi K, Tsuboi-Asai H, Matsushita S, Suda M, Nakashima M, Sasano H, et al. Structural and functional abnormalities in the spleen of an mFtz-F1 gene-disrupted mouse. Blood. 1999;93(5):1586-94. PMID: 10029587
34. Keegan CE, Hammer GD. Recent insights into organogenesis of the adrenal cortex. Trends Endocrinol Metab. 2002;13(5):200-8. PMID: 12185666
35. Zubair M, Parker KL, Morohashi K. Developmental links between the fetal and adult zones of the adrenal cortex revealed by lineage tracing. Mol Cell Biol. 2008;28(23):7030-40. doi: 10.1128/MCB.00900-08 PMID: 18809574
36. Russo J, De Rosas JC. Differentiation of the Leydigcell of the mouse testis during the fetal period-an ultrastructural study. Am J Anat. 1971;130(4):461-80. PMID: 5581229
37. Tanaka S, Matsuzawa A. Comparison of adrenocortical zonation in C57BL/6J and DDD mice. Exp Anim. 1995;44(4):285-91. PMID: 8575542
38. Kerr JB, Knell CM. The fate of fetal Leydig cells during the development of the fetal and postnatal rat testis. Development. 1988;103(3):535-44. PMID: 3246223
39. Kuopio T, Tapanainen J, Pelliniemi LJ, Huhtaniemi I. Developmental stages of fetal-type Leydig cells in prepubertal rats. Development. 1989;107(2):213-20. PMID: 2632220
40. Nakamura S, Kurokawa H, Asakawa S, Shimizu N, Tanaka M. Two distinct types of theca cells in the medaka gonad: germ cell-dependent maintenance of cyp19a1-expressing theca cells. Dev Dyn. 2009;238(10):2652-7. doi: 10.1002/dvdy.22068 PMID: 19705448