Interdependence of platelet-derived growth factor and estrogen-signaling pathways in inducing neonatal rat testicular gonocytes proliferation

Biology of Reproduction

Volumn 82, Issue 5, 2010, Pages 825-836

  Thuillier, Raphael ^a,c   Mazer, Monty ^b   Manku, Gurpreet ^b   Boisvert, Annie ^b   Wang, Yan ^a,d   Culty, Martine ^a,b  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c POITIERS UNIVERSITY HOSPITAL   (France)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Crosstalk; Estradiol; Estrogens; Gametogenesis; Growth factors; PDGF; Proliferation; Signal transduction; Testicular gonocytes; Testis

Indexed keywords

ESTRADIOL; FULVESTRANT; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATELET DERIVED GROWTH FACTOR; RAF PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GROWTH STIMULATION; HORMONAL REGULATION; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPERMATOGONIUM; TESTIS DEVELOPMENT;

ANIMALS; CELL PROLIFERATION; ESTRADIOL; GERM CELLS; IMMUNOHISTOCHEMISTRY; MALE; MAP KINASE KINASE 1; MAP KINASE KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR CROSS-TALK; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIA; TESTIS;

RATTUS;

EID: 77953829373     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.081729     Document Type: Article

References (67)

1. McGuinness MP, Orth JM. Reinitiation of gonocyte mitosis and movement of gonocytes to the basement membrane in testes of newborn rats in vivo and in vitro. Anat Rec 1992; 233:527-537.
2. Vergouwen RP, Jacobs SG, Huiskamp R, Davids JA, de Rooij DG. Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice. J Reprod Fertil 1991; 93:233-243.
3. de Rooij DG, Russel LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21:776-798.
4. Li H, Papadopoulos V, Vidic B, Dym M, Culty M. Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol: identification of signaling mechanisms involved. Endocrinology 1997; 138:1289-1298.
5. Hoch RV, Soriano P. Roles of PDGF in animal development. Development 2003; 130:4769-4784.
6. Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008; 22:1276-1312.
7. Mariani S, Basciani S, Arizzi M, Spera G, Gnessi L. PDGF and the testis. Trends Endocrinol Metab 2002; 13:11-17.
8. Basciani S, Mariani S, Arizzi M, Ulisse S, Rucci N, Jannini EA, la Rocca C, Manicone A, Carani C, Spera G, Gnessi L. Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor-alpha and -beta during human testicular development and disease. J Clin Endocrinol Metab 2002; 87:2310-2319.
9. Thuillier R, Wang Y, Culty M. Prenatal exposure to estrogenic compounds alters the expression pattern of platelet-derived growth factor receptors alpha and beta in neonatal rat testis: identification of gonocytes as targets of estrogen exposure. Biol Reprod 2003; 68:867-880.
10. Delbes G, Levacher C, Habert R. Estrogen effects on fetal and neonatal testicular development. Reproduction 2006; 132:527-538. (Pubitemid 44660527)
11. Hess RA, Carnes K. The role of estrogen in testis and the male reproductive tract: a review and species comparison. Anim Reprod 2004; 1:5-30.
12. O'Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev 2001; 22:289-318.
13. Saunders PTK, Sharpe RM, Williams K, Macpherson S, Urquart H, Irvine DS, Millar MR. Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Mol Hum Reprod 2001; 7:227-236.
14. van Pelt AMM, de Rooij DG, van der Burg B, van der Saag PT, Gustafsson JA, Kuiper GGJM. Ontogeny of estrogen receptor-beta expression in rat testis. Endocrinology 1999; 140:478-483.
15. Wang Y, Thuillier R, Culty M. Prenatal estrogen exposure differentially affects estrogen receptor-associated proteins in rat testis gonocytes. Biol Reprod 2004; 71:1652-1664.
16. Petersen DN, Tkalcevic GT, Koza-Taylor PH, Turi TG, Brown TA. Identification of estrogen receptor β2, a functional variant of estrogen receptor β expressed in normal rat tissues. Endocrinology 1998; 139:1082-1092.
17. Saunders PTK, Millar MR, Macpherson S, Irvine DS, Groome NP, Evans LR, Sharpe RM, Scobie GA. ER beta 1 and the ER beta 2 splice variant (ER beta cx/beta 2) are expressed in distinct cell populations in the adult human testis. J Clin Endocrinol Metab 2002; 87:2706-2715.
18. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A 1998; 95:15677-15682.
19. Delbes G, Duquenne C, Szenker J, Taccoen J, Habert R, Levacher C. Developmental changes in testicular sensitivity to estrogens throughout fetal and neonatal life. Toxicol Sci 2007; 99:234-243.
20. Delbes R, Levacher C, Pairault C, Racine C, Duquenne C, Krust A, Habert R. Estrogen receptor beta-mediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endocrinology 2004; 145:3395-3403.
21. Wahlgren A, Svechnikov K, Strand ML, Jahnukainen K, Parvinen M, Gustafsson JA, Soder O. Estrogen receptor b selective ligand 5α-androstane-3β, 17β-diol stimulates spermatogonial deoxyribonucleic acid synthesis in rat seminiferous epithelium in vitro. Endocrinology 2008; 149:2917-2922.
22. Moriarty K, Kim KH, Bender JR. Estrogen receptor-mediated rapid signaling. Endocrinology 2006; 147:5557-5563.
23. Pedram A, Razandi M, Wallace DC, Levin ER. Functional estrogen receptors in the mitochondria of breast cancer cells. Mol Biol Cell 2006; 17:2125-2137.
24. Laemmli UK. Cleavage of structural proteins during the assembly of bacteriophage T4. Nature 1970; 227:680-685.
25. Bryckaert MC, Eldor A, Fontenay M, Gazit A, Osherov N, Gilon C, Levitizki A, Tobelem B. Inhibition of platelet-derived growth factor-induced mitogenesis and tyrosine kinase activity in cultured bone marrow fibroblasts by tyrphostins. Exp Cell Res 1992; 199:255-261.
26. Powis G. Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res 1994; 54:2419-2423. (Pubitemid 24980025)
27. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007; 87:905-931.
28. Wilkinson JM, Hayes S, Thompson D, Whitney P, Bi K. Compound profiling using a panel of steroid hormone receptor cell-based assays. J Biomol Screen 2008; 13:755-765.
29. Williams K, McKinnell C, Saunders PTK, Walker M, Fisher JS, Turner KJ, Atanassova N, Sharpe RM. Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. Hum Reprod Update 2001; 7:236-247. (Pubitemid 32440286)
30. Rajpert-De Meyts EWA, Bartkova J, Samson M, Hoei-Hansen CE, Frydelund-Larsen L, Bartek J, Skakkebaek NE. The emerging phenotype of the testicular carcinoma in situ germ cell. Acta Pathol Microbiol Immunol Scandinavica 2003; 111:267-279.
31. McDonald CA, Millena AC, Reddy S, Finlay S, Vizcarra J, Khan SA, Davis JS. Follicle-stimulating hormone-induced aromatase in immature rat Sertoli cells requires an active phosphatidylinositol 3-kinase pathway and is inhibited via the mitogen-activated protein kinase signaling pathway. Mol Endocrinol 2006; 20:608-618.
32. Basciani S, De Luca G, Dolci S, Brama M, Arizzi M, Mariani S, Rosano G, Spera G, Gnessi L. Platelet-derived growth factor receptor beta-subtype regulates proliferation and migration of gonocytes. Endocrinology 2008; 149:6226-6235.
33. Betsholtz C, Karlsson L, Lindahl P. Developmental roles of plateletderived growth factors. BioEssays 2001; 23:494-507.
34. Puglianiello A, Campagnolo L, Farini D, Cipollone D, Russo MA, Siracusa G. Expression and role of PDGF-BB and PDGFR-beta during testis morphogenesis in the mouse embryo. J Cell Sci 2004; 117:1151-1160.
35. Ricci G, Catizone A, Galdieri M. Embryonic mouse testis development: role of platelet derived growth factor (PDGF-BB). J Cell Physiol 2004; 200:458-467.
36. Smith CA, McClive PJ, Hudson Q, Sinclair AH. Male-specific cell migration into the developing gonad is a conserved process involving PDGF signalling. Dev Biol 2005; 284:337-350.
37. Schmahl J, Raymond CS, Soriano P. PDGF signaling specificity is mediated through multiple immediate early genes. Nat Genet 2007; 39:52-60.
38. Tallquist M, Kazlauskas A. PDGF signaling in cells and mice. Cytokine Growth Factor Rev 2004; 15:205-213.
39. Kim SK, Abdelmegeed MA, Novak RF. The mitogen-activated protein kinase kinase (MEK) inhibitor PD98059 elevates primary cultured rat hepatocyte glutathione levels independent of inhibiting MEK. Drug Metab Dispos 2006; 34:683-689.
40. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 1998; 273:18623-18632.
41. Schmahl J, Rizzolo K, Soriano P. The PDGF signaling pathway controls multiple steroid-producing lineages. Genes Dev 2008; 22:3255-3267.
42. Nagano R, Tabata S, Nakanishi Y, Ohsako S, Kurohmaru M, Hayashi Y. Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat Rec 2000; 258:210-220.
43. Culty M. Gonocytes, the forgotten cells of the germ cell lineage. Birth Defects Res C 2009; 87:1-26.
44. Lassurguere J, Livera G, Habert R, Jegou B. Time- and dose-related effects of estradiol and diethylstilbestrol on the morphology and function of the fetal rat testis in culture. Toxicol Sci 2003; 73:160-169.
45. Dudley MW, Sheeler CQ, Wang H, Khan S. Activation of the human estrogen receptor by the antiestrogens ICI 182,780 and tamoxifen in yeast genetic systems: implications for their mechanism of action. Proc Natl Acad Sci U S A 2000; 97:3696-3701.
46. Zhao L, O'Neill K, Brinton RD. Estrogenic agonist activity of ICI 182,780 (faslodex) in hippocampal neurons: implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. J Pharmacol Exp Ther 2006; 319:1124-1132.
47. Mercier I, Mader S, Calderone A. Tamoxifen and ICI 182,780 negatively influenced cardiac cell growth via an estrogen receptor-independent mechanism. Cardiovasc Res 2003; 59:883-892. (Pubitemid 38366244)
48. Bjornstrom L, Sjoberg M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 2005; 19:833-842.
49. Geffroy N, Guqdin A, Dacquet C, Lefebvre P. Cell cycle regulation of breast cancer cells through estrogen-induced activities of ERK and Akt protein kinases. Mol Cell Endocrinol 2005; 237:11-23.
50. Luconi M, Forti G, Baldi E. Genomic and nongenomic effects of estrogens: molecular mechanisms of action and clinical implications for male reproduction. J Steroid Biochem Mol Biol 2002; 80:369-381.
51. Revelli A, Massobrio M, Tesarik J. Nongenomic actions of steroid hormones in reproductive tissues. Endocr Rev 1998; 19:3-17. (Pubitemid 29122072)
52. Vicini E, Loiarro M, Di Agostino S, Corallini S, Capolunghi F, Carsetti R, Chieffi P, Geremia R, Stefanini M, Sette C. 17β-Estradiol elicits genomic and non-genomic responses in mouse male germ cells. J Cell Physiol 2006; 206:238-245.
53. Bouskine A, Nebout M, Mograbi B, Brucker-Davis F, Roger C, Fenichel P. Estrogens promote human testicular germ cell cancer through a membrane-mediated activation of extracellular regulated kinase and protein kinase A. Endocrinology 2008; 149:565-573.
54. Eckert D, Nettersheim D, Heukamp LC, Kitazawa S, Biermann K, Schorle H. TCam-2 but not JKT-1 cells resemble seminoma in cell culture. Cell Tissue Res 2008; 331:529-538.
55. Young JC, Moarefi I, Hartl FU. Hsp90 a specialized but essential protein-folding tool. J Cell Biol 2001; 154:267-273.
56. Gutendorf B, Westendorf J. Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology 2001; 166:79-89.
57. Kuiper GGJM, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg P, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998; 139:4252-4263.
58. Margeat E, Bourdoncle A, Margueron R, Poujol N, Cavaillès V, Royer C. Ligands differentially modulate the protein interactions of the human estrogen receptors α and β. J Mol Biol 2003; 326:77-92.
59. Ozers MS, Ervin KM, Steffen CL, Fronczak JA, Lebakken CS, Carnahan KA, Lowery RG, Burke TJ. Analysis of ligand-dependent recruitment of coactivator peptides to estrogen receptor using fluorescence polarization. Mol Endocrinol 2005; 19:25-34.
60. Routledge EJ, White R, Parker MG, Sumpter JP. Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) a and ERβ. J Biol Chem 2000; 275:35986-35993.
61. Ratna WN. Inhibition of estrogenic stimulation of gene expression by genistein. Life Sci 2002; 71:865-877.
62. Safe SH, Pallaroni L, Yoon K, Gaido K, Ross S, McDonnell D. Problems for risk assessment of endocrine-active estrogenic compounds. Environ Health Perspect Suppl 2002; 110:925-930. (Pubitemid 36210851)
63. Vigueras-Villasenor RM, Moreno-Mendoza NA, Reyes-Torres G, Molina-Ortiz D, Leon MC, Rojas-Castaneda JC. The effect of estrogen on testicular gonocyte maturation. Reprod Toxicol 2006; 22:513-520. (Pubitemid 44344453)
64. Pentikainen V, Erkkila K, Suomalainen L, Parvinen M, Dunkel L. Estradiol acts as a germ cell survival factor in the human testis in vitro 1. J Clin Endocrinol Metab 2000; 85:2057-2067.
65. Robertson KM, O'Donnell L, Simpson ER, Jones MEE. The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function. Endocrinology 2002; 143:2913-2921.
66. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors a (ERa) and b (ERb) on mouse reproductive phenotypes. Development 2000; 127:4277-4291.
67. Pais V, Leav I, Lau KM, Jiang Z, Ho SM. Estrogen receptor-β expression in human testicular germ cell tumors. Clin Cancer Res 2003; 9:4475-4482. (Pubitemid 37248406)