Fetal programming of adult Leydig cell function by androgenic effects on stem/progenitor cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 18, 2014, Pages

  Kilcoyne, Karen R ^a   Smith, Lee B ^a   Atanassova, Nina ^b   Macpherson, Sheila ^a   McKinnell, Chris ^a   Van Den Driesche, Sander ^a   Jobling, Matthew S ^a   Chambers, Thomas J G ^a   De Gendt, Karel ^c   Verhoeven, Guido ^c   O'Hara, Laura ^a   Platts, Sophie ^a   De Franca, Luiz Renato ^d   Lara, Nathália L M ^d   Anderson, Richard A ^a   Sharpe, Richard M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Adult Leydig stem progenitor cells; Compensated Leydig cell failure; Ethane dimethane sulfonate; GATA4

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; LUTEINIZING HORMONE; OVALBUMIN; PHTHALIC ACID DIBUTYL ESTER; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; TESTOSTERONE; TRANSCRIPTION FACTOR II;

ADULT; ADULT LEYDIG CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL REGENERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HISTONE METHYLATION; HISTONE MODIFICATION; HORMONE SYNTHESIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LEYDIG CELL; MACROPHAGE; MALE; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; STEM CELL;

ADULT LEYDIG STEM/PROGENITOR CELLS; COMPENSATED LEYDIG CELL FAILURE; ETHANE DIMETHANE SULFONATE; GATA4;

ADULT STEM CELLS; ANDROGENS; ANIMALS; CALLITHRIX; CELL LINEAGE; DIBUTYL PHTHALATE; FEMALE; FETAL DEVELOPMENT; FETAL STEM CELLS; HUMANS; LEYDIG CELLS; LUTEINIZING HORMONE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, ANIMAL; PREGNANCY; RATS; RATS, TRANSGENIC; RATS, WISTAR; RECEPTORS, ANDROGEN; REGENERATION; TESTIS; TESTOSTERONE;

EID: 84899798514     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1320735111     Document Type: Article

References (74)

1. Aiken CE, Ozanne SE (2014) Tra nsgenerational developmental programming. Hum Reprod Update 20(1):63-75.
2. Vickers MH (2011) Developmental programming of the metabolic syndrome-critical windows for intervention. World J Diabetes 2(9):137-148.
3. Traish AM, Miner MM, Morgentaler A, Zitzmann M (2011) Testosterone deficiency. Am J Med 124(7):578-587.
4. Travison TG Araujo AB O'Donnell AB Kupelian V McKinlay JB 2007 A populationlevel decline in serum testos terone levels in American men J Clin Endocrinol Metab 92 1 196-202
5. Andersson AM, et al. (2007) Secular decline in male testosterone and sex hormone binding globulin serum levels in Danish popu lation surveys. J Clin Endocrinol Metab 92(12):4696-4705.
6. Perheentupa A, et al. (2013) A cohort effect on serum testosterone levels in Finnish men. Eur J Endocrinol 168(2):227-233.
7. Tajar A, et al.; EMAS Group (2010) Characteristics of secondary, primary, and compensated hypogonadism in aging men: Evidence from the European Male Ageing Study. J Clin Endocrinol Metab 95(4):1810 -1818.
8. Travison TG, Araujo AB, Kupelian V, O'Donnell AB, McKinlay JB (2007) The relative contributions of aging, health, and lifestyle factors to serum testosterone decline in men. J Clin Endocrinol Metab 92(2):549-555.
9. Khaw KT, et al. (2007) Endogenous testosterone and mortality due to all causes, cardiovascular disease, and cancer in men: European prospective investigation into cancer in Norfo lk (EPIC-Norfolk) Prospective Population Study. Circulation 116(23):2694-2701.
10. Malkin CJ, et al. (2004) The effect of testosterone replacement on endogenous inflammatory cytokines and lipid prof iles in hypogonadal men. J Clin Endocrinol Metab 89(7):3313-3318.
11. Bobjer J, Katrinaki M, Tsatsanis C, Lundberg Giwercman Y, Giwercman A (2013) Negative association between testosterone c oncentration and inflammatory markers in young men: A nested cross-sectional study. PLoS ONE 8(4):e61466.
12. Snyder PJ (2008) Might testosterone actually reduce mortality J Clin Endocrinol Metab 93(1):32-33.
13. Vanbillemont G, et al. (2010) Birth weight in relation to sex steroid status and body composition in young healthy male siblings. J Clin Endocrinol Metab 95(4):1587-1594.
14. Eisenberg ML, Jensen TK, Walters RC, Skakkebaek NE, Lipshultz LI (2012) The relationship between anogenital distance and reproductive hormone levels in adult men. J Urol 187(2):594-598.
15. Drake AJ, et al. (2009) Glucocorticoids amplify dibutyl phthalate-induced disruption of testosterone production and male reproductive development. Endocrinology 150(11):5055-5064.
16. Dean A, Sharpe RM (2013) Clinical review: Anogenital distance or digit length ratio as measures of fetal androgen exposure: Relationship to male reproductive development and its disorders. J Clin Endocrinol Metab 98(6):2230-2238.
17. Eisenberg ML, Hsieh MH, Walters RC, Krasnow R, Lipshultz LI (2011) The relationship between anogenital distance, fatherhood, and fertility in adult men. PLoS ONE 6(5):e18973.
18. Andersson AM, Jørgensen N, Frydelund-Larsen L, Rajpert-De Meyts E, Skakkebaek NE (2004) Impaired Leydig cell function in infertile men: A study of 357 idiopathic infertile men and 318 proven fertile controls. J Clin Endocrinol Metab 89(7):3161-3167.
19. Chen H, Ge RS, Zirkin BR (2009) Leydig cells: From stem cells to aging. Mol Cell Endocrinol 306(1-2):9-16.
20. Scott HM, Mason JI, Sharpe RM (2009) Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr Rev 30(7):883-925.
21. O'Shaughnessy PJ, Fowler PA (2011) Endocrinology of the mammalian fetal testis. Reproduction 141(1):37-46.
22. Mendis-Handagama SMLC, Ariyaratne HBS (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65(3):660-671.
23. Zirkin BR (2010) Where do adult Leydig cells come from Biol Reprod 82(6):1019-1020.
24. Hardy MP, Zirkin BR, Ewing LL (1989) Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 124(2):762-770.
25. O'Shaughnessy PJ, Willerton L Baker PJ 2002 Changes in Leydig cell gene expression during development in the mouse Biol Reprod 66 4 966-975
26. Ge R-S, et al. (2005) Gene expression in rat leydig cells during development from the progenitor to adult stage: A cluster analysis. Biol Reprod 72(6):1405-1415.
27. Ge R-S, et al. (2006) In search of rat stem Leydig cells: Identification, isolation, and lineage-specific development. Proc Natl Acad Sci USA 103(8):2719-2724.
28. Guo JJ, et al. (2013) Effects of luteinizing hormone and androgen on the development of rat progenitor Leydig cells in vitro and in vivo. Asian J Androl 15(5):685-691.
29. Landreh L, Stukenborg JB, Söder O, Svechnikov K (2013) Phenotype and steroidogenic potential of PDGFR-positive rat neonatal peritubular cells. Mol Cell Endocrinol 372(1 -2):96-104.
30. Qin J, Tsai MJ, Tsai SY (2008) Essential roles of COUP-TFII in Leydig cell differentiation and male fertility. PLoS ONE 3(9):e3285.
31. Teerds KJ, de Boer-Brouwer M, Dorrington JH, Balvers M, Ivell R (1999) Identification of markers for precursor and leydig cell differentiation in the adult rat test is following ethane dimethyl sulphonate administration. Biol Reprod 60(6):1437-1445.
32. Sharpe RM, Maddocks S, Kerr JB (1990) Cell-cell interactions in the control of spermatogenesis as studied using Leydig cell destruction and testosterone replacement. Am J Anat 188(1):3-20.
33. van den Driesche S, et al. (2012) Proposed role for COUP-TFII in regulating fetal Leydig cell steroidogenesis, per turbation of which leads to masculinization disorders in rodents. PLoS ONE 7(5):e37064.
34. Bielinska M, Seehra A, Toppari J, Heikinheimo M, Wilson DB (2007) GATA-4 is required for sex s teroidogenic cell development in the fetal mouse. Dev Dyn 236(1):203-213.
35. Ketola I, et al. (2002) Developmental expression and spermatogenic stage specificity of transcription factors GATA-1 and GATA-4 and their cofactors FOG-1 and FOG-2 in the mouse testis. Eur J Endocrinol 147(3):397-406.
36. Ketola I, et al. (2000) Expression of transcription factor GATA-4 during human testicular development and disease. J Clin Endocrinol Metab 85(10):3925-3931.
37. He W, et al. (2003) Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and l iver but not in muscle. Proc Natl Acad Sci USA 100(26):15712-15717.
38. Welsh M, Saunders PTK, Atanassova N, Sharpe RM, Smith LB (2009) Androgen action via testicular peritubular myoid cells is ess ential for male fertility. FASEB J 23(12):4218-4230.
39. WelshM, et al. (2012) Androgen receptor signalling in peritubular myoid cells is essential for normal differentiation and function of adult Leydig cells. Int J Androl 35(1):25-40.
40. Welsh M, et al. (2008) Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorc hidism. J Clin Invest 118(4):1479-1490.
41. Hutchison GR, et al. (2008) Sertoli cell development and function in an animal model of testicular dysgenesis syndrome. Biol Reprod 78(2):352-360.
42. Fan J, Papadopoulos V (2013) Evolutionary origin of the mitochondrial cholesterol transport machinery reveals a universal mechanism of steroid hormone biosynthesis in animals. PLoS ONE 8(10) :e76701.
43. Miller WL, Bose HS (2011) Early steps in steroidogenesis: Intracellular cholesterol trafficking. J Lipid Res 52(12):2111-2135.
44. Papadopoulos V, Miller WL (2012) Role of mitochondria in steroidogenesis. Best Pract Res Clin Endocrinol Metab 26(6):771-790.
45. Silverman E, Eimerl S, Orly J (1999) CCAAT enhancer-binding protein beta and GATA-4 binding regions within the promoter of the steroidogenic acute regulatory protein (StAR) gene are required for transcription in rat ovarian cells. J Biol Chem 274(25):17987-17996.
46. LaVoie HA (2005) Epigenetic control of ovarian function: The emerging role of histone modifications. Mol Cell Endocrinol 243(1-2):12-18.
47. Lee L, et al. (2013) Cha nges in histone modification and DNA methylation of the StAR and Cyp19a1 promoter regions in granulosa cells undergoing luteinization during ovulation in rats. Endocrinology 154(1):458-470.
48. Manna P R, Dyson MT, Stocco DM(2009) Regulation of the steroidogenic acute regulatory protein gene expression: Present and future perspectives. Mol Hum Reprod 15(6):321-333.
49. Li B, Carey M, W orkman JL (2007) The role of chromatin during transcription. Cell 128(4):707-719.
50. Reddington JP, et al. (2013) Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of Polycomb target genes. Genome Biol 14(3):R25.
51. Young MD, et al. (2011) ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res 39(17):7415-7427.
52. Thurisch B, et al. (2009) Transgenic mice expressing small interfering RNA against Gata4 point to a crucial role of Gata4 in the heart and gonads. J Mol Endocrinol 43(4): 157-169.
53. Tremblay JJ, Viger RS (2001) GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 142(3):977-986.
54. Ariyaratne HBS, Chamindrani Mendis-Handagama S (2000) Changes in the testis interstitium of Sprague Dawley rats from birth to sexualmaturity. Biol Reprod 62(3):680-690.
55. Davidoff MS, et al. (2004) Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 167(5):935-944.
56. Davidoff MS, Middendorff R, Müller D, Holstein AF (2009) The neuroendocrine Leydig cells and their stem cell progenitors, the pericytes. Adv Anat Embryol Cell Biol 205:1-107.
57. Stanley E, et al. (2012) Identification, proliferation, and differentiation of adult Leydig stem cells. Endocrinology 153(10):5002-5010.
58. De Gendt K, et al. (2004) A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA 101(5):1327-1332.
59. Scott HM, et al. (2007) Role of androgens in fetal testis development and dysgenesis. Endocrinology 148(5):2027-2036.
60. de Kretser DM (2004) Editorial: Is spermatogenic damage associated with Leydig cell dysfunction J Clin Endocrinol Metab 89(7):3158-3160.
61. Hansen KH, et al. (2008) A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10(11):1291-1300.
62. Margueron R, et al. (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461(7265):762-767.
63. Clark BJ, et al. (1995) Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol Endocrinol 9(10):1346-1355.
64. García-Galiano D, Pinilla L, Tena-Sempere M (2012) Sex steroids and the control of the Kiss1 system: Developmental roles and major regulatory actions. J Neuroendocrinol 24(1):22-33.
65. Martinez-Arguelles DB, Culty M, Zirki n BR, Papadopoulos V (2009) In utero exposure to di-(2-ethylhexyl) phthalate decreases mineralocorticoid receptor expression in the adult testis. Endocrinology 150(12):5575-5585.
66. Martinez-Arguelles DB, Guichard T, Culty M, Zirkin BR, Papadopoulos V (2011) In utero exposure to the antiandrogen di-(2-ethylhexyl) phthalate decreases adrenal aldosterone production in the adult rat. Biol Reprod 85(1):51-61.
67. Giagulli VA, Vermeulen A (1988) Leydig cell function in infertile men with idiopathic oligospermic infertility. J Clin Endocrinol Metab 66(1):62-67.
68. Jørgensen N Asklund C Carlsen E Skakkebaek NE 2006 Coordinated European investigations of semen quality: Results from studies of Scandinavian young men is a matter of concern Int J Androl 29 1 54-61
69. Finkelstein JS, et al. (2013) Gonadal steroids and body composition, strength, and sexual function in men. N Engl J Med 369(11):1011-1022.
70. Polkinghorne J (1989) Review of the Guidance on the Research Use of Fetuses and Fetal Material (Her Majesty's Stationary Office, London).
71. Mitchell RT, et al. (2010) Xenografting of human fetal testis tissue: A new approach to study fetal testis development and germ cell differentiation. Hum Reprod 25(10):2405-2414.
72. Mitchell RT, et al. (2008) Germcell differentiation in the marmoset (Callithrix jacchus) during fetal and neonatal life closely parallels that in the human. Hum Reprod 23(12):2755-2765.
73. Srinivas S, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
74. Tyndall V, et al. (2012) Effect of androgen treatment during foetal and/or neonatal life on ovarian function in prepubertal and adult rats. Reproduction 143(1):21-33.