1. bookVolume 50 (2016): Issue 3 (July 2016)
Journal Details
License
Format
Journal
eISSN
1336-0329
First Published
30 Mar 2016
Publication timeframe
4 times per year
Languages
English
access type Open Access

The role of retinoic acid receptors and their cognate ligands in reproduction in a context of triorganotin based endocrine disrupting chemicals

Published Online: 20 Aug 2016
Volume & Issue: Volume 50 (2016) - Issue 3 (July 2016)
Page range: 154 - 164
Journal Details
License
Format
Journal
eISSN
1336-0329
First Published
30 Mar 2016
Publication timeframe
4 times per year
Languages
English
Abstract

Retinoic acid (RA), an active form of vitamin A, regulates the embryonic development, male and female reproduction and induces important effects on the cell development, proliferation, and differentiation. These effects are mediated by the retinoid (RAR) and rexinoid nuclear receptors (RXR), which are considered to be a ligand-activated, DNA-binding, trans-acting, and transcription-modulating proteins, involved in a general molecular mechanism responsible for the transcriptional responses in target genes. Organotin compounds are typical environmental contaminants and suspected endocrine disrupting substances. They may affect processes of reproductive system in mammals, predominantly via nuclear receptor signaling pathways. Triorganotins, such as tributyltin chloride (TBTCl) and triphenyltin chloride (TPTCl), are capable to bind to RXR molecules, and thus represent potent agonists of RXR subtypes of nuclear receptors not sharing any structural characteristics with endogenous ligands of nuclear receptors. Th is article summarizes selected effects of biologically active retinoids and rexinoids on both male and female reproduction and also deals with the effects of organotin compounds evoking endocrine disrupting actions in reproduction.

Keywords

Adeeko A, Li D, Forsyth DS, Casey V, Cooke GM, Barthelemy J, Cyr DG, Trasler JM, Robaire B, Hales BF. Eff ects of in utero tributyltin chloride exposure in the rat on pregnancy outcome. Toxicol Sci 74, 407−415, 2003.10.1093/toxsci/kfg131Search in Google Scholar

Akmal KM, Dufour JM, Vo M, Higginson S, Kim KH. Ligand-dependent regulation of retinoic acid receptor alpha in rat testis: in vivo response to depletion and repletion of vitamin A. Endocrinology 139, 1239−1248, 1998.10.1210/endo.139.3.5775Search in Google Scholar

Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM, Page DC. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci USA. 105, 14976-14980, 2008.10.1073/pnas.0807297105Search in Google Scholar

Bailey JS, Siu CH. Unique tissue distribution of two distinct cellular retinoic acid binding proteins in neonatal and adult rat. Biochim Biophys Acta 1033, 267-272, 1990.10.1016/0304-4165(90)90131-FSearch in Google Scholar

Baltus AE, Menke DB, Hu YC, Goodheart ML, Carpenter AE, de Rooij DG, Page DC. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic dna replication. Nat Genet 38, 1430-1434, 2006.10.1038/ng191917115059Search in Google Scholar

Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC. Positional cloning and characterization of mouse mei8, a disrupted allelle of the meiotic cohesin rec8. Genesis 40, 184-194, 2004.10.1002/gene.2008515515002Search in Google Scholar

Bass NM. Cellular binding proteins for fatty acids and retinoids: similar or specialized functions? Mol Cell Biochem 123, 191-202, 1993.10.1007/978-1-4615-3096-1_25Search in Google Scholar

Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P. Retinoid signaling determines germ cell fate in mice. Science 312, 596−600, 2006.10.1126/science.112569116574820Search in Google Scholar

Braun KW, Tribley WA, Griswold MD, Kim KH. Folliclestimulating hormone inhibits all-trans-retinoic acid-induced retinoic acid receptor nuclear localization and transcriptional activation in mouse Sertoli cell lines. J Biol Chem 275, 4145-4151, 2000.10.1074/jbc.275.6.414510660575Search in Google Scholar

Braun KW, Vo MN, Kim KH. Positive regulation of retinoic acid receptor _ by protein kinase C and mitogen-activated protein kinase in Sertoli cells. Biol Reprod 67, 29-37, 2002.10.1095/biolreprod67.1.2912079996Search in Google Scholar

Brtko J. Retinoids, rexinoids and their cognate nuclear receptors: character and their role in chemoprevention of selected malignant diseases. Biomed Pap Med Fac Univ Palacky (Olomouc, Czech Repub) 151, 187−194, 2007.10.5507/bp.2007.03318345250Search in Google Scholar

Brtko J, Dvorak Z. Triorganotin compounds-ligands for “rexinoid” inducible transcription factors: biological effects. Toxicol Lett 234, 50−58, 2015.10.1016/j.toxlet.2015.02.00925683035Search in Google Scholar

Carmichael SL, Shaw GM, Laurent C, Croughan MS, Olney RS, Lammer EJ. Maternal progestin intake and risk of hypospadias, Arch Pediatr Adolesc Med 159, 957-962, 2005.10.1001/archpedi.159.10.95716203941Search in Google Scholar

Childs AJ, Cowan G, Kinnell HL, Anderson RA, Saunders PTK. Retinoic acid signalling and the control of meiotic entry in the human fetal gonads. PLoS One 6, e20249, 2011.10.1371/journal.pone.0020249310859421674038Search in Google Scholar

Chung SS, Wang X, Wolgemuth DJ. Male sterility in mice lacking retinoic acid receptor alpha involves specific abnormalities in spermiogenesis. Differentiation 73, 188−198, 2005.10.1111/j.1432-0436.2005.00018.x378531315901285Search in Google Scholar

Cooke HJ, Saunders PT. Mouse models of male infertility. Nature reviews. Genetics 3, 790−801, 2002.10.1038/nrg91112360237Search in Google Scholar

Cooke GM, Forsyth DS, Bondy GS, Tachon R, Tague B, Coady L. Organotin speciation and tissue distribution in rat dams, fetuses, and neonates following oral administration of tributyltin chloride. J Toxicol Environ Health A 71, 384−395, 2008.10.1080/1528739070180165318246498Search in Google Scholar

Dalton S. Cell cycle control of chromosomal DNA replication. Immunol Cell Biol 76, 467-472, 1998.10.1046/j.1440-1711.1998.00777.x9797469Search in Google Scholar

Delgado Filho VS, Lopes PF, Podratz PL, Graceli JB. Triorganotin as a compound with potential reproductive toxicity in mammals. Braz J Med Biol Res 44, 958−965, 2011.10.1590/S0100-879X201100750011021876874Search in Google Scholar

Deltour L, Haselbeck RJ, Ang HL, Duester G. Localization of class I and class IV alcohol dehydrogenases in mouse testis and epididymis: potential retinol dehydrogenases for endogenous retinoic acid synthesis. Biol Reprod 56, 102-109, 1997. 10.1095/biolreprod56.1.1029002638Search in Google Scholar

de Kretser DM, Loveland KL, Meehan T, O’Bryan MK, Phillips DJ, Wreford NG. Inhibins, activins and follistatin: actions on the testis. Mol Cell Endocrinol 180, 87−92, 2001.10.1016/S0303-7207(01)00502-0Search in Google Scholar

Doering DD, Steckelbroeck S, Doering T, Klingmuller D. Effects of butyltins on human 5alpha-reductase type 1 and type 2 activity. Steroids 67, 859-867, 2002.10.1016/S0039-128X(02)00051-XSearch in Google Scholar

Doyle TJ, Braun KW, McLean DJ, Wright RW, Griswold MD, Kim KH. Potential Functions of Retinoic Acid Receptor A in Sertoli Cells and Germ Cells During Spermatogenesis. Ann N Y Acad Sci 1120, 114−130, 2007.10.1196/annals.1411.008Search in Google Scholar

Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell 134, 921-931, 2008.10.1016/j.cell.2008.09.002Search in Google Scholar

Dufour JM, Kim KH. Cellular and subcellular localization of six retinoid receptors in rat testis during postnatal development: identification of potential heterodimeric receptors. Biol Reprod 61, 1300−1308, 1999.10.1095/biolreprod61.5.1300Search in Google Scholar

Eguizabal C, Shovlin TC, Durcova-Hills G, Surani A, McLaren A. Generation of primordial germ cells from pluripotent stem cells. Differentiation 78, 116-123, 2009.10.1016/j.diff.2009.07.001Search in Google Scholar

Eskola V, Nikula H, Huhtaniemi I. Age-related variation of follicle-stimulating hormone-stimulated cAMP production, protein kinase C activity and their interactions in the rat testis. Mol Cell Endocrinol 93, 143-148, 1993.10.1016/0303-7207(93)90117-3Search in Google Scholar

Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427, 148-154, 2004.10.1038/nature0224714668819Search in Google Scholar

Griswold MD, Bishop PD, Kim KH, Ping R, Siiteri JE, Morales C. Function of vitamin A in normal and synchronized seminiferous tubules. Ann N Y Acad Sci 564, 154-172, 1989.10.1111/j.1749-6632.1989.tb25895.x2672955Search in Google Scholar

Griswold MD, Cathryn A, Hogarth CA, Bowles J, Koopman P. Initiating Meiosis: The Case for Retinoic Acid. Biol Reprod 86, 35, 1-7, 2012. 10.1095/biolreprod.111.096610329066522075477Search in Google Scholar

Grote K, Stahlschmidt B, Talsness CE, Gericke C, Appel KE, Chahoud I. Eff ects of organotin compounds on pubertal male rats. Toxicology 202, 145−158, 2004.10.1016/j.tox.2004.05.003Search in Google Scholar

Grote K, Hobler C, Andrade AJ, Grande SW, Gericke C, Talsness CE, Appel KE, Chahoud I. Sex differences in effects on sexual development in rat off spring after pre- and postnatal exposure to triphenyltin chloride. Toxicology 260, 53−59, 2009.10.1016/j.tox.2009.03.006Search in Google Scholar

Grun F. The obesogen tributyltin. Vitam Horm 94, 277-325, 2014.10.1016/B978-0-12-800095-3.00011-0Search in Google Scholar

Haneji T, Maekawa M, Nishimune Y. Vitamin A and follicle-stimulating hormone synergistically induce differentiation of type A spermatogonia in adult mouse cryptorchid testes in vitro. Endocrinology 114, 801-805, 1984.10.1210/endo-114-3-801Search in Google Scholar

Hiromori Y, Nishikawa J, Yoshida I, Nagase H, Nakanishi T. Structure-dependent activation of peroxisome proliferator- activated receptor (PPAR)γ by organotin compounds. Chem Biol Interact 180, 238-244, 2009.10.1016/j.cbi.2009.03.006Search in Google Scholar

Hiromori Y, Yui H, Nishikawa J, Nagase H, Nakanishi T. Organotin compounds cause structure-dependent induction of progesterone in human choriocarcinoma Jar cells. J Steroid Biochem Mol Biol 155, 190−198, 2016.10.1016/j.jsbmb.2014.10.010Search in Google Scholar

Huang HS, Dyrenfurth I, Gunsalus GL, Hembree WC. Eff ect of vitamin A deficiency upon gonadotropin response to gonadotropin-releasing hormone. Biol Reprod 33, 1176-1187, 1985.10.1095/biolreprod33.5.1176Search in Google Scholar

Hunakova L, Macejova D, Toporova L, Brtko J. Anticancer effects of tributyltin chloride and triphenyltin chloride in human breast cancer cell lines MCF-7 and MDA-MB-231. Tumor Biol, 2015. [Epub ahead of print].10.1016/S0959-8049(16)61382-5Search in Google Scholar

Illes P, Brtko J, Dvorak Z. Development and Characterization of a Human Reporter Cell Line for the Assessment of Th yroid Receptor Transcriptional Activity: A Case of Organotin Endocrine Disruptors. J Agric Food Chem 63, 7074−7083, 2015.10.1021/acs.jafc.5b0151926208032Search in Google Scholar

Itami T, Ema M, Amano H, Murai T, Kawasaki H. Teratogenic evaluation of tributyltin chloride in rats following oral exposure. Drug Chem Toxicol 13, 283−295, 1990.10.3109/014805490090322872279458Search in Google Scholar

Jirawatnotai S, Hu Y, Livingston DM, Sicinski P. Proteomic identification of a direct role for cyclin d1 in DNA damage repair. Cancer Res 72, 4289-4293, 2012.10.1158/0008-5472.CAN-11-3549Search in Google Scholar

Johnson AT, Wang L, Gillett SJ, Chandraratna RA. High afinity retinoic acid receptor antagonists: analogs of AGN 193109. Bioorg Med Chem Lett 9, 573-576, 1999.10.1016/S0960-894X(99)00047-5Search in Google Scholar

Kashimada K, Svingen T, Feng CW, Pelosi E, Bagheri-Fam S, Harley VR, Schlessinger D, Bowles J, Koopman P. Antagonistic regulation of Cyp26b1 by transcription factors SOX9/SF1 and FOXL2 during gonadal development in mice. FASEB J 25, 3561-3569, 2011.10.1096/fj.11-184333317756621757499Search in Google Scholar

Kipp JL, Golebiowski A, Rodriguez G, Demczuk M, Kilen SM, Mayo KE. Gene expression profiling reveals Cyp26b1 to be an activin regulated gene involved in ovarian granulosa cell proliferation. Endocrinology 152, 303−312, 2011.10.1210/en.2010-0749303306021084447Search in Google Scholar

Kishta O, Adeeko A, Li D, Luu T, Brawer JR, Morales C, et al. In utero exposure to tributyltin chloride differentially alters male and female fetal gonad morphology and gene expression profiles in the Sprague-Dawley rat. Reprod Toxicol 23, 1−11, 2007.10.1016/j.reprotox.2006.08.01417095186Search in Google Scholar

Kliewer SA, Umesono K, Noonan DJ, Heyman RA, Evans RM. Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors, Nature 358, 771-774, 1992.10.1038/358771a061598831324435Search in Google Scholar

Koshimizu U, Watanabe M, Nakatsuji N. Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev Biol 168, 683-685, 1995.10.1006/dbio.1995.11137729599Search in Google Scholar

Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA 103, 2474−2479, 2006.10.1073/pnas.0510813103141380616461896Search in Google Scholar

Koubova J, Hu YC, Bhattacharyya T, Soh YQ, Gill ME, Goodheart ML, Hogarth CA, Griswold MD, Page DC. Retinoic acid activates two pathways required for meiosis in mice. PLoS Genet 10, 1−9, 2014.10.1371/journal.pgen.1004541412510225102060Search in Google Scholar

Kumar S, Chatzi C, Brade T, Cunningham TJ, Zhao X, Duester G. Sex-specific timing of meiotic initiation is regulated by Cyp26b1 independent of retinoic acid signalling. Nat Commun 2, 151, 2011.10.1038/ncomms1136303473621224842Search in Google Scholar

Lamano Carvalho TL, Lopes RA, Azoubel R, Ferreira AL. Morphometric study of the reversibility of testicle alterations in rats submitted to hypervitaminosis A. Int J Vitam Nutr Res 48, 316-324, 1978.Search in Google Scholar

Laurence PA, Sobel AE. Changes in serum vitamin A level during the human menstrual cycle. J Clin Endocrinol Metab 13, 1192-1199, 1953.10.1210/jcem-13-10-1192Search in Google Scholar

Law SM. Retinoic acid receptor alpha in germ cells is important for mitosis of spermatogonia, spermatogonial differentiation and meiosis. Dissertation. Washington State University. 2013.Search in Google Scholar

Lin Y, Gill ME, Koubova J, Page DC. Germ cell-intrinsic and -extrinsic factors govern meiotic initiation in mouse embryos. Science 322, 1685-1687, 2008.10.1126/science.1166340Search in Google Scholar

Lo S, Allera A, Albers P, Heimbrecht J, Jantzen E, Klingmuller D, Steckelbroeck S. Dithioerythritol (DTE) prevents inhibitory effects of triphenyltin (TPT) on the key enzymes of the human sex steroid hormone metabolism. J Steroid Biochem Mol Biol 84, 569−576, 2003. 10.1016/S0960-0760(03)00074-8Search in Google Scholar

Luo J, Pasceri P, Conlon RA, Rossant J, Giguere V. Mice lacking all isoforms of retinoic acid receptor beta develop normally and are susceptible to the teratogenic effects of retinoic acid. Mech Dev 53, 61-71, 1995.10.1016/0925-4773(95)00424-6Search in Google Scholar

Ma JJ, Han BC, Yang Y, Peng JP. Retinoic acid synthesis and metabolism are concurrent in the mouse uterus during peri-implantation. Cell Tissue Res 350, 525-537, 2012.10.1007/s00441-012-1507-4Search in Google Scholar

Macejova D, Bialesova L, Toporova L, Brtko J. Biological effects of selected triorganotin compounds - retinoid X receptor ligands in estrogen receptor negative MDA-MB-231 human breast cancer cells. Toxicol Lett 238S, S374, 2015.10.1016/j.toxlet.2015.08.1067Search in Google Scholar

MacLean G, Li H, Metzger D, Chambon P, Petkovich M. Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology 148, 4560-4567, 2007.10.1210/en.2007-0492Search in Google Scholar

Malassine A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update 9, 531-539, 2003.10.1093/humupd/dmg043Search in Google Scholar

McVey MJ, Cooke GM. Inhibition of rat testis microsomal 3betahydroxysteroid dehydrogenase activity by tributyltin. J Steroid Biochem Mol Biol 86, 99-105, 2003.10.1016/S0960-0760(03)00256-5Search in Google Scholar

Mahony S, Mazzoni EO, Mccuine S, Young RA, Wichterle H, Gifford DK. Ligand-dependent dynamics of retinoic acid receptor binding during early neurogenesis. Gen Biol 12, r2, 2011.10.1186/gb-2011-12-1-r2309130021232103Search in Google Scholar

McCarthy PT, Cerecedo LR. Vitamin A deficiency in the mouse. J Nutr 46,361-376, 1952.10.1093/jn/46.3.36114939072Search in Google Scholar

McLaren A. Meiosis and differentiation of mouse germ cells. Symposia of the Society for Experimental Biology 38, 7−23, 1984.Search in Google Scholar

Minegishi T, Hirakawa T, Kishi H, Abe K, Ibuki Y, Miyamoto K. Retinoic acid (RA) represses follicle stimulating hormone (FSH)-induced luteinizing hormone (LH) receptor in rat granulosa cells. Arch Biochem Biophys 373, 203−210, 2000.10.1006/abbi.1999.152810620339Search in Google Scholar

Morita Y, Tilly JL. Segregation of retinoic acid effects on fetal ovarian germ cell mitosis versus apoptosis by requirement for new macromolecular synthesis. Endocrinology 140, 2696-2703, 1999.10.1210/endo.140.6.682610342860Search in Google Scholar

Nakanishi T, Kohroki J, Suzuki S, Ishizaki J, Hiromori Y, Takasuga S, Itoh N, Watanabe Y, Utoguchi N, Tanaka K. Trialkyltin compounds enhance human CG secretion and aromatase activity in human placental choriocarcinoma cells. J Clin Endocrinol Metab 87, 2830−2837, 2002.10.1210/jcem.87.6.854012050258Search in Google Scholar

Nakanishi T, Nishikawa J, Hiromori Y, Yokoyama H, Koyanagi M, Takasuga S, Ishizaki J, Watanabe M, Isa S, Utoguchi N, Itoh N, Kohno Y, Nishihara T, Tanaka K. Trialkyltin compounds bind retinoid X receptor to alter human placental endocrine functions. Mol Endocrinol 19, 2502−2516, 2005.10.1210/me.2004-039715941851Search in Google Scholar

Nakanishi T, Hiromori Y, Yokoyama H, Koyanagi M, Itoh N, Nishikawa J, Tanaka K. Organotin compounds enhance 17β-hydroxysteroid dehydrogenase type I activity in human choriocarcinoma JAr cells: potential promotion of 17β-estradiol biosynthesis in human placenta. Biochem Pharmacol 71, 1349-1357, 2006.10.1016/j.bcp.2006.01.01416513093Search in Google Scholar

Nakanishi T. Endocrine disruption induced by organotin compounds; organotins function as a powerful agonist for nuclear receptors rather than an aromatase inhibitor. J Toxicol Sci 33, 269−276, 2008.10.2131/jts.33.26918670157Search in Google Scholar

Nourashrafeddin S. Potential roles of gonadotropins to control pulsatile retinoic acid signaling during spermatogenesis. Med Hypotheses 85, 303−304, 2015.10.1016/j.mehy.2015.05.02126141633Search in Google Scholar

Ogata R, Omura M, Shimasaki Y, Kubo K, Oshima Y, Aou S, Inoue N. Two-generation reproductive toxicity study of tributyltin chloride in female rats. J Toxicol Environ Health A 63, 127−144, 2001.10.1080/1528739015112646911393799Search in Google Scholar

Ohno S, Nakajima Y, Nakajin S. Triphenyltin and tributyltin inhibit pig testicular 17beta-hydroxysteroid dehydrogenase activity and suppress testicular testosterone biosynthesis. Steroids 70, 645-651, 2005.10.1016/j.steroids.2005.03.00515899506Search in Google Scholar

Omura M, Ogata R, Kubo K, Shimasaki Y, Aou S, Oshima Y, Tanaka A, Hirata M, Makita Y, Inoue N. Two-generation reproductive toxicity study of tributyltin chloride in male rats. Toxicol Sci 64, 224−232, 2001.10.1093/toxsci/64.2.22411719705Search in Google Scholar

Oulad-Abdelghani M, Bouillet P, Decimo D, Gansmuller A, Heyberger S, Dolle P, Bronner S, Lutz Y, Chambon P. Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by stra8, a novel retinoic acid-responsive gene. J Cell Biol 135, 469-477, 1996.10.1083/jcb.135.2.46921210348896602Search in Google Scholar

Piprek RP, Pecio A, Laskowska-Kaszub K, Kloc M, Kubiak JZ, Szymura JM. Retinoic acid homeostasis regulates meiotic entry in developing anuran gonads and in Bidder’s organ through Raldh2 and Cyp26b1 proteins. Mech Dev 130, 613−27, 2013.10.1016/j.mod.2013.09.00124056063Search in Google Scholar

Richards JS. Maturation of ovarian follicles: actions and interactions of pituitary and ovarian hormones on follicular cell differentiation. Physiol Rev 60, 51-89, 1980.10.1152/physrev.1980.60.1.516243782Search in Google Scholar

Saitoh M, Yanase T, Morinaga H, Tanabe M, Mu YM, Nishi Y, Nomura M, Okabe T, Goto K, Takayanagi R, Nawata H. Tributyltin or triphenyltin inhibits aromatase activity in the human granulosa-like tumor cell line KGN. Biochem Biophys Res Commun 289, 198−204, 2001.10.1006/bbrc.2001.595211708799Search in Google Scholar

Saitou M, Yamaji M. Primordial germ cells in mice. Cold Spring Harbor Perspectives in Biology 4, 2012.10.1101/cshperspect.a008375353633923125014Search in Google Scholar

Santos NC, Kim KH. Activity of retinoic acid receptor-alpha is directly regulated at its protein kinase A sites in response to follicle-stimulating hormone signaling. Endocrinology 151, 2361−2372, 2010. 10.1210/en.2009-1338286925720215566Search in Google Scholar

Schupp M, Curtin JC, Kim RJ, Billin AN, Lazar MA. A widely used retinoic acid receptor antagonist induces peroxisome proliferator-activated receptor-gamma activity. Mol Pharmacol 71, 1251-1257, 2007.10.1124/mol.106.03366217290005Search in Google Scholar

Simard J, Ricketts ML, Gingras S, Soucy P, Feltus FA, Melner MH. Molecular biology of the 3β-hydroxysteroid dehydrogenase/ delta5-delta4 isomerase gene family. Endocr Rev 26, 525-582, 2005.10.1210/er.2002-005015632317Search in Google Scholar

Smith CA, Roeszler KN, Bowles J, Koopman P, Sinclair AH. Onset of meiosis in the chicken embryo; evidence of a role for retinoic acid. BMC Dev Biol 8, 85, 2008.10.1186/1471-213X-8-85256492818799012Search in Google Scholar

Stel J, Legler J. The Role of Epigenetics in the Latent Effects of Early Life Exposure to Obesogenic Endocrine Disrupting Chemicals. Endocrinology 156, 3466-3472, 2015.10.1210/en.2015-1434458882426241072Search in Google Scholar

Sylvester SR, Griswold MD. Th e testicular iron shuttle: a “nurse” function of the Sertoli cells. J Androl 15, 381−385, 1994.Search in Google Scholar

Tabassum S, Pettinary C. Chemical and biotechnological developments in organotin cancer chemotherapy. J Organomet Chem 691, 1761-1766, 2006.10.1016/j.jorganchem.2005.12.033Search in Google Scholar

Tan H, Wang JJ, Cheng SF, Ge W, Sun YC, Sun XF, Sun R, Li L, Li B, Shen W. Retinoic acid promotes the proliferation of primordial germ cell-like cells differentiated from mouse skin-derived stem cells in vitro. Theriogenology 85, 408−418, 2016.10.1016/j.theriogenology.2015.09.00226456183Search in Google Scholar

Tarrade A, Schoonjans K, Guibourdenche J, Bidart JM, Vidaud M, Auwerx J, Rochette-Egly C, Evain-Brion D. PPAR gamma/RXR alpha heterodimers are involved in human CG beta synthesis and human trophoblast differentiation. Endocrinology 142, 4504-4514, 2001.10.1210/endo.142.10.844811564716Search in Google Scholar

Tatone C, Benedetti E, Vitti M, Di Emidio G, Ciriminna R, Vento ME, Cela V, Borzi P, Carta G, Lispi M, Cimini AM, Artini PG. Modulating Intrafollicular Hormonal Milieu in Controlled Ovarian Stimulation: Insights From PPAR Expression in Human Granulosa Cells. J Cell Physiol 231, 908−914, 2016.10.1002/jcp.2518226332656Search in Google Scholar

Toporova L, Macejova D, Brtko J. Radioligand binding assay for accurate determination of nuclear retinoid X receptors: A case of triorganotin endocrine disrupting ligands. Toxicol Lett 254, 32−36, 2016.10.1016/j.toxlet.2016.05.00527153798Search in Google Scholar

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 93, 233−243, 1991.10.1530/jrf.0.09302331920294Search in Google Scholar

Walker WH. Molecular mechanisms controlling Sertoli cell proliferation and differentiation. Endocrinology 144, 3719-3721, 2003.10.1210/en.2003-076512933639Search in Google Scholar

Zhang J, Zuo Z, He C, Wu D, Chen Y, Wang C. Inhibition of thyroidal status related to depression of testicular development in Sebastiscus marmoratus exposed to tributyltin. Aquat Toxicol 94, 62−67, 2009.10.1016/j.aquatox.2009.06.00319577312Search in Google Scholar

Zheng WL, Bucco RA, Sierra Rievera E, Osteen KG, Melner MH, Ong DE. Synthesis of retinoic acid by rat ovarian cells that express cellular retinoic acid-binding protein-II. Biol Reprod 60, 110-114, 1999.10.1095/biolreprod60.1.1109858493Search in Google Scholar

Zhuang Y H, Ylikomi T, Lindfors M, Piippo S, Tuohimaa P. Immunolocalization of retinoic acid receptors in rat, mouse and human ovary and uterus. J Steroid Biochem Mol Biol 48, 61-68, 1994.10.1016/0960-0760(94)90251-8Search in Google Scholar

Yu WJ, Lee BJ, Nam SY, Kim YC, Lee YS, Yun YW. Spermatogenetic disorders in adult rats exposed to tributyltin chloride during puberty. J Vet Med Sci 65, 1331−1335, 2003.10.1292/jvms.65.133114709822Search in Google Scholar

Yu M, Guan K, Zhang C. Th e promoting effect of retinoic acid on proliferation of chicken primordial germ cells by increased expression of cadherin and catenins. Amino Acids 40, 933-941, 2011.10.1007/s00726-010-0717-x20717697Search in Google Scholar

Yu M, Ge C, Zeng W, Mi Y, Zhang C. Retinoic acid promotes proliferation of chicken primordial germ cells via activation of PI3K/Aktmediated NF-kB signalling cascade. Cell Biol Int 36, 705-712, 2012. 10.1042/CBI2011054222548360Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo