Cellular microenvironment dictates androgen production by murine fetal Leydig cells in primary culture

Biology of Reproduction

Volumn 91, Issue 4, 2014, Pages

  Carney, Colleen M ^a   Muszynski, Jessica L ^a   Strotman, Lindsay N ^b,c   Lewis, Samantha R ^a   O'Connell, Rachel L ^b,c   Beebe, David J ^b,c,d   Theberge, Ashleigh B ^b,c,d   Jorgensen, Joan S ^a,c,d  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Health   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Androstenedione; Fetal Leydig cell; Fetal testis; Microfluidic device; Steroidogenesis; Testicular culture; Testosterone

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANDROSTENEDIONE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); TESTOSTERONE; ABIRATERONE; ANDROGEN; ANDROSTANE DERIVATIVE; CULTURE MEDIUM;

ANDROGEN SYNTHESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL CONTACT; CELL POPULATION; COCULTURE; CONTROLLED STUDY; FETUS; IMMUNOHISTOCHEMISTRY; LEYDIG CELL; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIMARY CULTURE; PRIORITY JOURNAL; STEROID METABOLISM; STEROIDOGENESIS; TESTIS CELL; TESTOSTERONE SYNTHESIS; TUMOR MICROENVIRONMENT; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CULTURE MEDIUM; CULTURE TECHNIQUE; CYTOLOGY; DEVICES; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROFLUIDIC ANALYSIS; PARACRINE SIGNALING; PROCEDURES;

LYCOPERSICON ESCULENTUM; MURINAE; MUS;

ANDROGENS; ANDROSTENES; ANIMALS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; CULTURE MEDIA; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; LEYDIG CELLS; MALE; MICE; MICROFLUIDIC ANALYTICAL TECHNIQUES; PARACRINE COMMUNICATION;

EID: 84925010086     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.118570     Document Type: Article

References (64)

1. Jost A. Research on sexual differentiation of the rabbit embryo. Arch Anat Microsc Morph Exp 1947; 36:271-315.
2. Scott HM, Mason JI, Sharpe RM. Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr Rev 2009; 30:883-925.
3. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009; 30:293-342.
4. Chen H, Ge RS, Zirkin BR. Leydig cells: from stem cells to aging. Mol Cell Endocrinol 2009; 306:9-16.
5. Dong L, Jelinsky SA, Finger JN, Johnston DS, Kopf GS, Sottas CM, Hardy MP, Ge RS. Gene expression during development of fetal and adult Leydig cells. Ann N Y Acad Sci 2007; 1120:16-35.
6. Chen H, Stanley E, Jin S, Zirkin BR. Stem Leydig cells: from fetal to aged animals. Birth Defects Res C Embryo Today 2010; 90:272-283.
7. Barsoum IB, Kaur J, Ge RS, Cooke PS, Yao HH. Dynamic changes in fetal Leydig cell populations influence adult Leydig cell populations in mice. FASEB J 2013; 27:2657-2666.
8. O'Shaughnessy PJ, Baker P, Sohnius U, Haavisto AM, Charlton HM, Huhtaniemi I. F et al. development of Leydig cell activity in the mouse is independent of pituitary gonadotroph function. Endocrinology 1998; 139: 1141-1146.
9. Yao HH, Whoriskey W, Capel B. Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 2002; 16:1433-1440.
10. Brennan J, Tilmann C, Capel B. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003; 17:800-810.
11. Habert R, Lejeune H, Saez JM. Origin, differentiation and regulation of fetal and adult Leydig cells. Mol Cell Endocrinol 2001; 179:47-74.
12. Barsoum I, Yao HH. The road to maleness: from testis to Wolffian duct. Trends Endocrinol Metab 2006; 17:223-228.
13. Yao HH, Capel B. Disruption of testis cords by cyclopamine or forskolin reveals independent cellular pathways in testis organogenesis. Dev Biol 2002; 246:356-365.
14. Orth JM. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 1982; 203:485-492.
15. Byskov AG. Differentiation of mammalian embryonic gonad. Physiol Rev 1986; 66:71-117.
16. Migrenne S, Pairault C, Racine C, Livera G, Geloso A, Habert R. Luteinizing hormone-dependent activity and luteinizing hormone-independent differentiation of rat fetal Leydig cells. Mol Cell Endocrinol 2001; 172:193-202.
17. Barsoum IB, Yao HH. F et al. Leydig cells: progenitor cell maintenance and differentiation. J Androl 2010; 31:11-15.
18. Merchant-Larios H, Moreno-Mendoza N. Mesonephric stromal cells differentiate into Leydig cells in the mouse fetal testis. Exp Cell Res 1998; 244:230-238.
19. Defalco T, Takahashi S, Capel B. Two distinct origins for Leydig cell progenitors in the fetal testis. Dev Biol 2011; 352:14-26.
20. Karl J, Capel B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev Biol 1998; 203:323-333.
21. Tang H, Brennan J, Karl J, Hamada Y, Raetzman L, Capel B. Notch signaling maintains Leydig progenitor cells in the mouse testis. Development 2008; 135:3745-3753.
22. Defalco T, Saraswathula A, Briot A, Iruela-Arispe ML, Capel B. Testosterone levels influence mouse fetal Leydig cell progenitors through notch signaling. Biol Reprod 2013; 88:91.
23. Shima Y, Miyabayashi K, Haraguchi S, Arakawa T, Otake H, Baba T, Matsuzaki S, Shishido Y, Akiyama H, Tachibana T, Tsutsui K, Morohashi K. Contribution of Leydig and Sertoli cells to testosterone production in mouse fetal testes. Mol Endocrinol 2013; 27:63-73.
24. 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; 141:2631-2637.
25. Klinefelter GR, Hall PF, Ewing LL. Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol Reprod 1987; 36:769-783.
26. Salva A, Klinefelter GR, Hardy MP. Purification of rat Leydig cells: increased yields after unit-gravity sedimentation of collagenase-dispersed interstitial cells. J Androl 2001; 22:665-671.
27. Ascoli M, Puett D. Gonadotropin binding and stimulation of steroidogenesis in Leydig tumor cells. Proc Natl Acad Sci U S A 1978; 75:99-102.
28. Mather JP. Establishment and characterization of two distinct mouse testicular epithelial cell lines. Biol Reprod 1980; 23:243-252.
29. Domenech M, Bjerregaard R, Bushman W, Beebe DJ. Hedgehog signaling in myofibroblasts directly promotes prostate tumor cell growth. Integr Biol (Camb) 2012; 4:142-152.
30. Domenech M, Yu H, Warrick J, Badders NM, Meyvantsson I, Alexander CM, Beebe DJ. Cellular observations enabled by microculture: paracrine signaling and population demographics. Integr Biol (Camb) 2009; 1: 267-274.
31. Casavant BP, Berthier E, Theberge AB, Berthier J, Montanez-Sauri SI, Bischel LL, Brakke K, Hedman CJ, Bushman W, Keller NP, Beebe DJ. Suspended microfluidics. Proc Natl Acad Sci U S A 2013; 110: 10111-10116.
32. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global doublefluorescent Cre reporter mouse. Genesis 2007; 45:593-605.
33. O'Hara L, York JP, Zhang P, Smith LB. Targeting of GFP-Cre to the mouse Cyp11a1 locus both drives Cre recombinase expression in steroidogenic cells and permits generation of Cyp11a1 knock out mice. PLoS One 2014; 9:e84541.
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(_delta delta C[T]) Method. Methods 2001; 25:402-408.
35. Young EW, Berthier E, Guckenberger DJ, Sackmann E, Lamers C, Meyvantsson I, Huttenlocher A, Beebe DJ. Rapid prototyping of arrayed microfluidic systems in polystyrene for cell-based assays. Anal Chem 2011; 83:1408-1417.
36. Capel B, Hawkins JR, Hirst E, Kioussis D, Lovell-Badge R. Establishment and characterization of conditionally immortalized cells from the mouse urogenital ridge. J Cell Sci 1996; 109(Pt 5):899-909.
37. Rasmussen FE, Wiltbank MC, Christensen JO, Grummer RR. Effects of fenprostalene and estradiol-17 beta benzoate on parturition and retained placenta in dairy cows and heifers. J Dairy Sci 1996; 79:227-234.
38. Su X, Theberge AB, January CT, Beebe DJ. Effect of microculture on cell metabolism and biochemistry: do cells get stressed in microchannels? Anal Chem 2013; 85:1562-1570.
39. Tam PP, Snow MH. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J Embryol Exp Morphol 1981; 64:133-147.
40. Baker PJ, O'Shaughnessy PJ. Role of gonadotrophins in regulating numbers of Leydig and Sertoli cells during fetal and postnatal development in mice. Reproduction 2001; 122:227-234.
41. Ikeda Y, Shen WH, Ingraham HA, Parker KL. Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 1994; 8:654-662.
42. Greco TL, Payne AH. Ontogeny of expression of the genes for steroidogenic enzymes P450 side-chain cleavage, 3 beta-hydroxysteroid dehydrogenase, P450 17 alpha-hydroxylase/C17-20 lyase, and P450 aromatase in fetal mouse gonads. Endocrinology 1994; 135:262-268.
43. Payne AH, Hales DB. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 2004; 25: 947-970.
44. Lang JD, Berry SM, Powers GL, Beebe DJ, Alarid ET. Hormonally responsive breast cancer cells in a microfluidic co-culture model as a sensor of microenvironmental activity. Integr Biol (Camb) 2013; 5: 807-816.
45. Spencer KH, Kim MY, Hughes CC, Hui EE. A screen for short-range paracrine interactions. Integr Biol (Camb) 2014; 6:382-387.
46. Murphy PR, Moger WH. Short-term primary culture of mouse interstitial cells: effects of culture conditions of androgen production. Biol Reprod 1982; 27:38-47.
47. Klinefelter GR, Ewing LL. Maintenance of testosterone production by purified adult rat Leydig cells for 3 days in vitro. In Vitro Cell Dev Biol 1989; 25:283-288.
48. Verhoeven G, Cailleau J. Influence of coculture with Sertoli cells on steroidogenesis in immature rat Leydig cells. Mol Cell Endocrinol 1990; 71:239-251.
49. Hunter MG, Cooke BA. The functional activity of adult mouse Leydig cells in monolayer culture: effect of lipoproteins, pregnenolone and cholera-toxin. Mol Cell Endocrinol 1985; 39:217-228.
50. Lin T, Haskell J, Vinson N, Terracio L. Characterization of insulin and insulin-like growth factor I receptors of purified Leydig cells and their role in steroidogenesis in primary culture: a comparative study. Endocrinology 1986; 119:1641-1647.
51. Klinefelter GR, Ewing LL. Optimizing testosterone production by purified adult rat Leydig cells in vitro. In Vitro Cell Dev Biol 1988; 24:545-549.
52. Risbridger GP, Hedger MP. Adult rat Leydig cell cultures: minimum requirements for maintenance of luteinizing hormone responsiveness and testosterone production. Mol Cell Endocrinol 1992; 83:125-132.
53. Rommerts FFG. Testosterone: an overview of biosynthesis, transport, metabolism and non-genomic actions In: Nieschlag E, Behre HM (eds.), Testosterone: Action, Deficiency, Substitution, 3rd ed. Cambridge, UK: Cambridge University Press; 2004:1-38.
54. Bird IM, Clyne CD, Lightly ER, Williams BC, Walker SW. Further characterization of the steroidogenic responsiveness of purified zona fasciculata/reticularis cells from bovine adrenal cortex before and after primary culture: changing responsiveness to phosphoinositidase C agonists. J Endocrinol 1992; 133:21-28.
55. Williams BC, Lightly ER, Ross AR, Bird IM, Walker SW. Characterization of the steroidogenic responsiveness and ultrastructure of purified zona fasciculata/reticularis cells from bovine adrenal cortex before and after primary culture. J Endocrinol 1989; 121:317-324.
56. Mahendroo M, Wilson JD, Richardson JA, Auchus RJ. Steroid 5alphareductase 1 promotes 5alpha-androstane-3alpha,17beta-diol synthesis in immature mouse testes by two pathways. Mol Cell Endocrinol 2004; 222: 113-120.
57. Cool J, DeFalco TJ, Capel B. Vascular-mesenchymal cross-talk through Vegf and Pdgf drives organ patterning. Proc Natl Acad Sci U S A 2011; 108:167-172.
58. DeFalco T, Bhattacharya I, Williams AV, Sams DM, Capel B. Yolk-sacderived macrophages regulate fetal testis vascularization and morphogenesis. Proc Natl Acad Sci U S A 2014; 111:E2384-2393.
59. Meyvantsson I, Warrick JW, Hayes S, Skoien A, Beebe DJ. Automated cell culture in high density tubeless microfluidic device arrays. Lab Chip 2008; 8:717-724.
60. Puccinelli JP, Su X, Beebe DJ. Automated high-throughput microchannel assays for cell biology: operational optimization and characterization. JALA Charlottesv Va 2010; 15:25-32.
61. O'Shaughnessy PJ, Willerton L, Baker PJ. Changes in Leydig cell gene expression during development in the mouse. Biol Reprod 2002; 66: 966-975.
62. Hazra R, Jimenez M, Desai R, Handelsman DJ, Allan CM. Sertoli cell androgen receptor expression regulates temporal fetal and adult Leydig cell differentiation, function, and population size. Endocrinology 2013; 154:3410-3422.
63. Salmon NA, Handyside AH, Joyce IM. Expression of Sox8, Sf1, Gata4, Wt1, Dax1, and Fog2 in the mouse ovarian follicle: implications for the regulation of Amh expression. Mol Reprod Dev 2005; 70:271-277.
64. Polanco JC, Wilhelm D, Davidson TL, Knight D, Koopman P. Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development. Hum Mol Genet 2010; 19: 506-516.