Role of miR-300-3p in Leydig cell function and differentiation: A therapeutic target for obesity-related testosterone deficiency

Wang, 2019, Phthalate-induced fetal leydig cell dysfunction mediates male reproductive tract anomalies, Front. Pharmacol., 10, 1309, 10.3389/fphar.2019.01309 Zhou, 2019, The roles and mechanisms of Leydig cells and myoid cells in regulating spermatogenesis, Cell. Mol. Life Sci., 76, 2681, 10.1007/s00018-019-03101-9 Ge, 2006, In search of rat stem Leydig cells: identification, isolation, and lineage-specific development, Proc. Natl. Acad. Sci. USA, 103, 2719, 10.1073/pnas.0507692103 Jarow, 2005, The androgen microenvironment of the human testis and hormonal control of spermatogenesis, Ann. N. Y. Acad. Sci., 1061, 208, 10.1196/annals.1336.023 Chimento, 2014, Role of estrogen receptors and g protein-coupled estrogen receptor in regulation of hypothalamus-pituitary-testis axis and spermatogenesis, Front. Endocrinol., 5, 1, 10.3389/fendo.2014.00001 Mendis-Handagama, 1997, Luteinizing hormone on Leydig cell structure and function, Histol. Histopathol., 12, 869 Sinha Hikim, 1999, Hormonal and genetic control of germ cell apoptosis in the testis, Rev. Reprod., 4, 38, 10.1530/ror.0.0040038 Williams-Ashman, 1983, Regulatory features of seminal vesicle development and function, Curr. Top. Cell. Regul., 22, 201, 10.1016/B978-0-12-152822-5.50011-7 Lei, 2001, Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene, Mol. Endocrinol., 15, 184, 10.1210/mend.15.1.0586 Yang, 2021, Melatonin promotes male reproductive performance and increases testosterone synthesis in mammalian Leydig cells, Biol. Reprod., 104, 1322, 10.1093/biolre/ioab046 Gregoraszczuk, 2013, Supraphysiological leptin levels shift the profile of steroidogenesis in porcine ovarian follicles toward progesterone and testosterone secretion through increased expressions of CYP11A1 and 17b-HSD: a tissue culture approach, Reproduction, 145, 311, 10.1530/REP-12-0269 Lardone, 2018, Leydig cell dysfunction is associated with post-transcriptional deregulation of CYP17A1 in men with Sertoli cell-only syndrome, Mol. Hum. Reprod., 24, 203, 10.1093/molehr/gay006 Wu, 2017, A brief exposure to cadmium impairs Leydig cell regeneration in the adult rat testis, Sci. Rep., 7, 6337, 10.1038/s41598-017-06870-0 Chen, 2019, Identification and functional characterization of microRNAs in rat Leydig cells during development from the progenitor to the adult stage, Mol. Cell. Endocrinol., 493, 110453, 10.1016/j.mce.2019.110453 Liang, 2021, Sertoli cell-derived exosome-mediated transfer of miR-145-5p inhibits Leydig cell steroidogenesis by targeting steroidogenic factor 1, Faseb. J., 35, e21660, 10.1096/fj.202002589RRRR Duan, 2020, miR-142-5p/DAX1-dependent regulation of P450c17 contributes to triclosan-mediated testosterone suppression, Sci. Total Environ., 717, 137280, 10.1016/j.scitotenv.2020.137280 Gao, 2017, Differential expression of microRNAs in TM3 Leydig cells of mice treated with brain-derived neurotrophic factor, Cell Biochem. Funct., 35, 364, 10.1002/cbf.3283 An, 2019, MiR-1197-3p regulates testosterone secretion in goat Leydig cells via targeting PPARGC1A, Gene, 710, 131, 10.1016/j.gene.2019.05.057 Zhang, 2020, Down-regulation of LINC00472 promotes osteosarcoma tumorigenesis by reducing FOXO1 expressions via miR-300, Cancer Cell Int., 20, 100, 10.1186/s12935-020-01170-6 Wang, 2016, miR-300 promotes proliferation and EMT-mediated colorectal cancer migration and invasion by targeting p53, Oncol. Rep., 36, 3225, 10.3892/or.2016.5193 Cruz, 2015, miR-300 mediates Bmi1 function and regulates differentiation in primitive cardiac progenitors, Cell Death Dis., 6, e1953, 10.1038/cddis.2015.255 Pan, 2020, Maternal exposure to zearalenone in masculinization window affects the fetal Leydig cell development in rat male fetus, Environ. Pollut., 263, 114357, 10.1016/j.envpol.2020.114357 Kang, 2018, MicroRNA-300 suppresses metastasis of oral squamous cell carcinoma by inhibiting epithelial-to-mesenchymal transition, OncoTargets Ther., 11, 5657, 10.2147/OTT.S173236 Honda, 1993, Ad4BP regulating steroidogenic P-450 gene is a member of steroid hormone receptor superfamily, J. Biol. Chem., 268, 7494, 10.1016/S0021-9258(18)53202-6 Lynch, 1993, Steroidogenic factor 1, an orphan nuclear receptor, regulates the expression of the rat aromatase gene in gonadal tissues, Mol. Endocrinol., 7, 776 Lala, 1992, Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I, Mol. Endocrinol., 6, 1249 Val, 2003, SF-1 a key player in the development and differentiation of steroidogenic tissues, Nucl. Recept., 1, 8, 10.1186/1478-1336-1-8 Aoki, 2004, Proteasomal degradation of the FoxO1 transcriptional regulator in cells transformed by the P3k and Akt oncoproteins, Proc. Natl. Acad. Sci. USA, 101, 13613, 10.1073/pnas.0405454101 Zhao, 2017, Post-transcriptional gene regulation by mRNA modifications, Nat. Rev. Mol. Cell Biol., 18, 31, 10.1038/nrm.2016.132 Kierzek, 2003, The thermodynamic stability of RNA duplexes and hairpins containing N6-alkyladenosines and 2-methylthio-N6-alkyladenosines, Nucleic Acids Res., 31, 4472, 10.1093/nar/gkg633 Li, 2020, m(6)A regulates liver metabolic disorders and hepatogenous diabetes, Dev. Reprod. Biol., 18, 371 Li, 2016, Regulation of seminiferous tubule-associated stem Leydig cells in adult rat testes, Proc. Natl. Acad. Sci. USA, 113, 2666, 10.1073/pnas.1519395113 Miller, 2011, The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders, Endocr. Rev., 32, 81, 10.1210/er.2010-0013 Martin, 2016, Cell interactions and genetic regulation that contribute to testicular Leydig cell development and differentiation, Mol. Reprod. Dev., 83, 470, 10.1002/mrd.22648 Zirkin, 1987, Leydig cell differentiation during maturation of the rat testis: a stereological study of cell number and ultrastructure, Anat. Rec., 219, 157, 10.1002/ar.1092190208 Zirkin, 2018, Leydig cells: formation, function, and regulation, Biol. Reprod., 99, 101, 10.1093/biolre/ioy059 Morohashi, 1996, Ad4BP/SF-1, a transcription factor essential for the transcription of steroidogenic cytochrome P450 genes and for the establishment of the reproductive function, Faseb. J., 10, 1569, 10.1096/fasebj.10.14.9002548 Yazawa, 2006, Differentiation of adult stem cells derived from bone marrow stroma into Leydig or adrenocortical cells, Endocrinology, 147, 4104, 10.1210/en.2006-0162 Yazawa, 2009, Liver receptor homolog-1 regulates the transcription of steroidogenic enzymes and induces the differentiation of mesenchymal stem cells into steroidogenic cells, Endocrinology, 150, 3885, 10.1210/en.2008-1310 Gondo, 2008, Adipose tissue-derived and bone marrow-derived mesenchymal cells develop into different lineage of steroidogenic cells by forced expression of steroidogenic factor 1, Endocrinology, 149, 4717, 10.1210/en.2007-1808 Yang, 2015, Directed mouse embryonic stem cells into leydig-like cells rescue testosterone-deficient male rats in vivo, Stem Cells Dev., 24, 459, 10.1089/scd.2014.0370 Glass, 1977, Low serum testosterone and sex-hormone-binding-globulin in massively obese men, J. Clin. Endocrinol. Metab., 45, 1211, 10.1210/jcem-45-6-1211 Allan, 2010, Androgens and obesity, Curr. Opin. Endocrinol. Diabetes Obes., 17, 224, 10.1097/MED.0b013e3283398ee2 Van de Velde, 2020, The effects of age and obesity on postprandial dynamics of serum testosterone levels in men, Clin. Endocrinol., 92, 214, 10.1111/cen.14141 Hausser, 2013, Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation, Genome Res., 23, 604, 10.1101/gr.139758.112 Liu, 2015, Functional conservation of both CDS- and 3'-UTR-located microRNA binding sites between species, Mol. Biol. Evol., 32, 623, 10.1093/molbev/msu323 Rigoutsos, 2009, New tricks for animal microRNAS: targeting of amino acid coding regions at conserved and nonconserved sites, Cancer Res., 69, 3245, 10.1158/0008-5472.CAN-09-0352 Accili, 2004, FoxOs at the crossroads of cellular metabolism, differentiation, and transformation, Cell, 117, 421, 10.1016/S0092-8674(04)00452-0 Vivar, 2016, FoxO1 mediates TGF-beta1-dependent cardiac myofibroblast differentiation, Biochim. Biophys. Acta, 1863, 128, 10.1016/j.bbamcr.2015.10.019 Sinha, 2018, Cep55 overexpression causes male-specific sterility in mice by suppressing Foxo1 nuclear retention through sustained activation of PI3K/Akt signaling, FASEB J, 32, 4984, 10.1096/fj.201701096RR Alarcón, 2015, N6-methyladenosine marks primary microRNAs for processing, Nature, 519, 482, 10.1038/nature14281 Wang, 2020, METTL3 is essential for postnatal development of brown adipose tissue and energy expenditure in mice, Nat. Commun., 11, 1648, 10.1038/s41467-020-15488-2 Xie, 2019, METTL3 inhibits hepatic insulin sensitivity via N6-methyladenosine modification of Fasn mRNA and promoting fatty acid metabolism, Biochem. Biophys. Res. Commun., 518, 120, 10.1016/j.bbrc.2019.08.018 Chen, 2021, m(6)A mRNA methylation regulates testosterone synthesis through modulating autophagy in Leydig cells, Autophagy, 17, 457, 10.1080/15548627.2020.1720431 Liu, 2016, Structural and functional characterization of the proteins responsible for N(6)-methyladenosine modification and recognition, Curr. Protein Pept. Sci., 17, 306, 10.2174/1389203716666150901113553 Lin, 2000, Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling, J. Biol. Chem., 275, 36818, 10.1074/jbc.C000580200 Liang, 2021, Isolation of primary leydig cells from murine testis, Bio. Protoc., 11, e4223, 10.21769/BioProtoc.4223