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Functions and mechanism of noncoding RNA in the somatic cells of the testis

Published online by Cambridge University Press:  02 December 2019

Chunjie Li ,
Baiqi Chen  and
Jing Wang Open the ORCID record for Jing Wang [Opens in a new window]
Chunjie Li
Affiliation:
Basic Medical College, Nanchang University, Nanchang, Jiangxi, People’s Republic of China
Baiqi Chen
Affiliation:
School of Public Health, Nanchang University, Nanchang, Jiangxi, People’s Republic of China
Jing Wang*
Affiliation:
Basic Medical College, Nanchang University, Nanchang, Jiangxi, People’s Republic of China
*
Author for correspondence: Jing Wang, Basic Medical College, Nanchang University, Nanchang, Jiangxi, People’s Republic of China. Tel: +86 15727635809. E-mail: [email protected]
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Summary

ncRNAs are involved in numerous biological processes by regulating gene expression and cell stability. Studies have shown that ncRNAs also contribute to spermatogenesis. Leydig cells (LCs) and Sertoli cells (SCs) are somatic cells of the testis that support spermatogenesis and are vital to male fertility. In this review, we summarized the findings from studies on ncRNAs in SCs and LCs. In SCs, ncRNAs play key roles in phagocytosis, immunoprotection and development of SCs. In LCs, ncRNAs are involved in steroidogenesis, in particular production of testosterone as well as development of LCs. Here, we discuss the possible target genes and functions of ncRNAs in both types of cells. These ncRNAs regulate the expression of target genes or mRNA coding sequence regions, resulting in a chain reaction that influences cell function. In addition, microRNAs, lncRNAs, piRNA-like RNAs (pilRNAs) and natural antisense transcripts (NATs) are discussed in this review. In summary, we suggest that these ncRNAs might act in coordination to control spermatogenesis and maintain the environmental homeostasis of the testis.

Keywords

Leydig cellsmiRNAsncRNAsSertoli cells
Type
Review Article
Information
Zygote , Volume 28 , Issue 2 , April 2020 , pp. 87 - 92
Copyright
© Cambridge University Press 2019

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References

Akinjo, OO, Gant, TW and Marczylo, EL (2018) Perturbation of microRNA signalling by doxoRubiconin in spermatogonial, Leydig and Sertoli cell lines in vitro. Toxicol Res 7, 760–70.CrossRefGoogle ScholarPubMed
Aravin, AA, Sachidanandam, R, Girard, A, Fejes-Toth, K and Hannon, GJ (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316(5825), 744–7.CrossRefGoogle Scholar
Ayupe, AC, Tahira, AC, Camargo, L, Beckedorff, FC, Verjovski-Almeida, S and Reis, EM (2015) Global analysis of biogenesis, stability and sub-cellular localization of lncRNAs mapping to intragenic regions of the human genome. RNA Biol 12, 877–92.CrossRefGoogle ScholarPubMed
Balbin, OA, Malik, R, Dhanasekaran, SM, Prensner, JR, Cao, X, Wu, YM, Robinson, D, Wang, R, Chen, G, Beer, DGet al. (2015) The landscape of antisense gene expression in human cancers. Genome Res 25, 1068–79.CrossRefGoogle ScholarPubMed
Bernstein, E, Caudy, AA, Hammond, SM and Hannon, GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409(6818), 363–6.CrossRefGoogle ScholarPubMed
Birney, E, Stamatoyannopoulos, JA, Dutta, A, Guigo, R, Gingeras, TR, Margulies, EH, Weng, Z, Snyder, M, Dermitzakis, ET, Thurman, REet al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447(7146), 799–816.Google ScholarPubMed
Bjork, JK, Sandqvist, A, Elsing, AN, Kotaja, N and Sistonen, L (2010) miR-18, a member of Oncomir-1, targets heat shock transcription factor 2 in spermatogenesis. Development 137, 3177–84.CrossRefGoogle ScholarPubMed
Brosnan, CA and Voinnet, O (2009) The long and the short of noncoding RNAs. Curr Opin Cell Biol 21, 416–25.CrossRefGoogle Scholar
Carmell, MA, Girard, A, van de Kant, HJ, Bourc’his, D, Bestor, TH, de Rooij, DG and Hannon, GJ (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12, 503–14.CrossRefGoogle ScholarPubMed
Castillo, AF, Fan, J, Papadopoulos, V and Podesta, EJ (2011) Hormone-dependent expression of a steroidogenic acute regulatory protein natural antisense transcript in MA-10 mouse tumor Leydig cells. PLoS One 6, e22822.CrossRefGoogle ScholarPubMed
Chen, Y, Zhou, Y, Wang, J, Wang, L, Xiang, Z, Li, D and Han, X (2016) Microcystin-leucine arginine causes cytotoxic effects in Sertoli cells resulting in reproductive dysfunction in male mice. Sci Rep 6, 39238.CrossRefGoogle ScholarPubMed
Cheng, CY and Mruk, DD (2012) The blood–testis barrier and its implications for male contraception. Pharmacol Rev 64, 16–64.CrossRefGoogle ScholarPubMed
Choi, JS, Oh, JH, Park, HJ, Choi, MS, Park, SM, Kang, SJ, Oh, MJ, Kim, SJ, Hwang, SY and Yoon, S (2011) miRNA regulation of cytotoxic effects in mouse Sertoli cells exposed to nonylphenol. Reprod Biol Endocrinol 9, 126.CrossRefGoogle ScholarPubMed
Chung, JY, Chen, H, Midzak, A, Burnett, AL, Papadopoulos, V and Zirkin, BR (2013) Drug ligand-induced activation of translocator protein (TSPO) stimulates steroid production by aged brown Norway rat Leydig cells. Endocrinology 154, 2156–65.CrossRefGoogle ScholarPubMed
Dabaja, AA, Mielnik, A, Robinson, BD, Wosnitzer, MS, Schlegel, PN and Paduch, DA (2015) Possible germ cell–Sertoli cell interactions are critical for establishing appropriate expression levels for the Sertoli cell-specific microRNA, miR-202-5p, in human testis. Basic Clin Androl 25, 2.CrossRefGoogle ScholarPubMed
de Mateo, S and Sassone-Corsi, P (2014) Regulation of spermatogenesis by small noncoding RNAs: role of the germ granule. Semin Cell Dev Biol 29, 84–92.CrossRefGoogle Scholar
Derrien, T, Johnson, R, Bussotti, G, Tanzer, A, Djebali, S, Tilgner, H, Guernec, G, Martin, D, Merkel, A, Knowles, DGet al. (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution and expression. Genome Res 22, 1775–89.CrossRefGoogle ScholarPubMed
Ebbesen, KK, Kjems, J and Hansen, TB (2016) Circular RNAs: identification, biogenesis and function. Biochim Biophys Acta 1859, 163–8.CrossRefGoogle ScholarPubMed
The ENCODE Project Consortium (2004) The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306(5696), 636–40.CrossRefGoogle Scholar
The ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome (2012) Nature 489(7414), 57–74.CrossRefGoogle Scholar
Fan, J and Papadopoulos, V (2012) Transcriptional regulation of translocator protein (Tspo) via a SINE B2-mediated natural antisense transcript in MA-10 Leydig cells. Biol Reprod 86, 147.CrossRefGoogle Scholar
Geisler, S and Coller, J (2013) RNA in unexpected places: long noncoding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol 14, 699–712.CrossRefGoogle ScholarPubMed
Gu, H, Wu, W, Yuan, B, Tang, Q, Guo, D, Chen, Y, Xia, Y, Hu, L, Chen, D, Sha, Jet al. (2017) Genistein up-regulates miR-20a to disrupt spermatogenesis via targeting Limk1. Oncotarget 8, 58728–37.Google ScholarPubMed
Guan, D, Zhang, W, Zhang, W, Liu, GH and Belmonte, JC (2013) Switching cell fate, ncRNAs coming to play. Cell Death Dis 4, e464.CrossRefGoogle Scholar
Guo, J, Liu, X, Yang, Y, Liang, M, Bai, C, Zhao, Z and Sun, B (2018) miR-375 down-regulation of the rearranged L-myc fusion and hypoxia-induced gene domain protein 1A genes and effects on Sertoli cell proliferation. Asian Australas J Anim Sci 31, 1103–9.CrossRefGoogle ScholarPubMed
Hai, Y, Hou, J, Liu, Y, Liu, Y, Yang, H, Li, Z and He, Z (2014) The roles and regulation of Sertoli cells in fate determinations of spermatogonial stem cells and spermatogenesis. Semin Cell Dev Biol 29, 66–75.CrossRefGoogle ScholarPubMed
Hu, Z, Shen, WJ, Kraemer, FB and Azhar, S (2012) MicroRNAs 125a and 455 repress lipoprotein-supported steroidogenesis by targeting scavenger receptor class B type I in steroidogenic cells. Mol Cell Biol 32, 5035–45.CrossRefGoogle Scholar
Hu, Z, Shen, WJ, Cortez, Y, Tang, X, Liu, LF, Kraemer, FB and Azhar, S (2013) Hormonal regulation of microRNA expression in steroid producing cells of the ovary, testis and adrenal gland. PLoS One 8, e78040.CrossRefGoogle ScholarPubMed
Huang, B, Zhao, J, Lei, Z, Shen, S, Li, D, Shen, GX, Zhang, GM and Feng, ZH (2009) miR-142-3p restricts cAMP production in CD4+CD25– T cells and CD4+CD25+ Treg cells by targeting AC9 mRNA. EMBO Rep 10, 180–5.CrossRefGoogle ScholarPubMed
Huhtaniemi, IT (2014) Andropause—lessons from the European male ageing study. Ann Endocrinol 75, 128–31.CrossRefGoogle ScholarPubMed
Huhtaniemi, I (2015) A short evolutionary history of FSH-stimulated spermatogenesis. Hormones 14, 468–78.Google Scholar
Jan, SZ, Hamer, G, Repping, S, de Rooij, DG, van Pelt, AM and Vormer, TL (2012) Molecular control of rodent spermatogenesis. Biochim Biophys Acta 1822, 1838–50.CrossRefGoogle ScholarPubMed
Jimenez-Badillo, SE, Oviedo, N, Hernandez-Guzman, C, Gonzalez-Mariscal, L and Hernandez-Sanchez, J (2017) Catsper1 promoter is bidirectional and regulates the expression of a novel lncRNA. Sci Rep 7, 13351.CrossRefGoogle ScholarPubMed
Jovanovic, M and Hengartner, MO (2006) miRNAs and apoptosis: RNAs to die for. Oncogene 25, 6176–87.CrossRefGoogle Scholar
Kapranov, P, Cheng, J, Dike, S, Nix, DA, Duttagupta, R, Willingham, AT, Stadler, PF, Hertel, J, Hackermuller, J, Hofacker, ILet al. (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316(5830), 1484–8.CrossRefGoogle Scholar
Kim, VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6, 376–85.CrossRefGoogle ScholarPubMed
Kloner, RA, Carson, C, 3rd, Dobs, A, Kopecky, S and Mohler, ER, 3rd (2016) Testosterone and cardiovascular disease J Am Coll Cardiol 67, 545–57.CrossRefGoogle ScholarPubMed
Krol, J, Loedige, I and Filipowicz, W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11, 597–610.CrossRefGoogle ScholarPubMed
Kupelian, V, Page, ST, Araújo, AB, Travison, TG, Bremner, WJ and McKinlay, JB (2006) Low sex hormone-binding globulin, total testosterone and symptomatic androgen deficiency are associated with development of the metabolic syndrome in nonobese men. J Clin Endocrinol Metab 91, 843–50.CrossRefGoogle ScholarPubMed
Laslett, AL, McFarlane, JR and Risbridger, GP (1997) Developmental response by Leydig cells to acidic and basic fibroblast growth factor. J Steroid Biochem Mol Biol 60(3–4), 171–9.CrossRefGoogle ScholarPubMed
Latge, G, Poulet, C, Bours, V, Josse, C and Jerusalem, G (2018) Natural antisense transcripts: molecular mechanisms and implications in breast cancers. Int J Mol Sci 19, pii: E123.CrossRefGoogle ScholarPubMed
Lian, C, Sun, B, Niu, S, Yang, R, Liu, B, Lu, C, Meng, J, Qiu, Z, Zhang, L and Zhao, Z (2012) A comparative profile of the microRNA transcriptome in immature and mature porcine testes using Solexa deep sequencing. FEBS J 279, 964–75.CrossRefGoogle ScholarPubMed
Lin, S, Zhang, L, Luo, W and Zhang, X (2015) Characteristics of antisense transcript promoters and the regulation of their activity. Int J Mol Sci 17, 9.CrossRefGoogle ScholarPubMed
Liu, H, Yang, Y, Zhang, L, Liang, R, Ge, RS, Zhang, Y, Zhang, Q, Xiang, Q, Huang, Y and Su, Z (2014) Basic fibroblast growth factor promotes stem Leydig cell development and inhibits LH-stimulated androgen production by regulating microRNA expression. J Steroid Biochem Mol Biol 144(Pt B), 483–91.CrossRefGoogle ScholarPubMed
Liu, H, Wang, R, Mao, B, Zhao, B and Wang, J (2019) Identification of lncRNAs involved in rice ovule development and female gametophyte abortion by genome-wide screening and functional analysis. BMC Genome 20, 90.CrossRefGoogle ScholarPubMed
Lucas, K and Raikhel, AS (2013) Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochem Mol Biol 43, 24–38.CrossRefGoogle ScholarPubMed
Lui, WY, Lee, WM and Cheng, CY (2003) Sertoli-germ cell adherens junction dynamics in the testis are regulated by RhoB GTPase via the ROCK/LIMK signalling pathway. Biol Reprod 68, 2189–206.CrossRefGoogle Scholar
Ma, C, Song, H, Yu, L, Guan, K, Hu, P, Li, Y, Xia, X, Li, J, Jiang, S and Li, F (2016) miR-762 promotes porcine immature Sertoli cell growth via the ring finger protein 4 (RNF4) gene. Sci Rep 6, 32783.CrossRefGoogle ScholarPubMed
Ma, L, Li, A, Zou, D, Xu, X, Xia, L, Yu, J, Bajic, VB and Zhang, Z (2015) LncRNAWiki: harnessing community knowledge in collaborative curation of human long noncoding RNAs. Nucl Acids Res 43, D187–92.CrossRefGoogle Scholar
Manna, PR, Cohen-Tannoudji, J, Counis, R, Garner, CW, Huhtaniemi, I, Kraemer, FB and Stocco, DM (2013) Mechanisms of action of hormone-sensitive lipase in mouse Leydig cells: its role in the regulation of the steroidogenic acute regulatory protein. J Biol Chem 288, 8505–18.CrossRefGoogle ScholarPubMed
Manna, PR, Slominski, AT, King, SR, Stetson, CL and Stocco, DM (2014) Synergistic activation of steroidogenic acute regulatory protein expression and steroid biosynthesis by retinoids: involvement of cAMP/PKA signalling. Endocrinology 155, 576–91.CrossRefGoogle Scholar
Matzkin, ME, Yamashita, S and Ascoli, M (2013) The ERK1/2 pathway regulates testosterone synthesis by coordinately regulating the expression of steroidogenic genes in Leydig cells. Mol Cell Endocrinol 370(1–2), 130–7.CrossRefGoogle ScholarPubMed
McCabe, MJ, Tarulli, GA, Laven-Law, G, Matthiesson, KL, Meachem, SJ, McLachlan, RI, Dinger, ME and Stanton, PG (2016) Gonadotropin suppression in men leads to a reduction in claudin-11 at the Sertoli cell tight junction. Hum Reprod 31, 875–86.CrossRefGoogle ScholarPubMed
Neph, S, Vierstra, J, Stergachis, AB, Reynolds, AP, Haugen, E, Vernot, B, Thurman, RE, John, S, Sandstrom, R, Johnson, AKet al. (2012) An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489(7414), 83–90.CrossRefGoogle ScholarPubMed
Ng, WL, Marinov, GK, Liau, ES, Lam, YL, Lim, YY and Ea, CK. (2016) Inducible RasGEF1B circular RNA is a positive regulator of ICAM-1 in the TLR4/LPS pathway. RNA Biol 13, 861–71.CrossRefGoogle ScholarPubMed
Nishizawa, M, Ikeya, Y, Okumura, T and Kimura, T (2015) Post-transcriptional inducible gene regulation by natural antisense RNA. Front Biosci 20, 1–36.CrossRefGoogle ScholarPubMed
Niu, Z, Goodyear, SM, Rao, S, Wu, X, Tobias, JW, Avarbock, MR and Brinster, RL (2011) MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 108, 12740–5.CrossRefGoogle ScholarPubMed
Oatley, JM and Brinster, RL (2012) The germline stem cell niche unit in mammalian testes. Phys Rev 92, 577–95.Google ScholarPubMed
Ohno, S (1972) So much ‘junk’ DNA in our genome. Brookhaven Symp Biol 23, 366–70.Google ScholarPubMed
Ortogero, N, Hennig, GW, Langille, C, Ro, S, McCarrey, JR and Yan, W (2013) Computer-assisted annotation of murine Sertoli cell small RNA transcriptome. Biol Reprod 88, 3.CrossRefGoogle ScholarPubMed
Ortogero, N, Schuster, AS, Oliver, DK, Riordan, CR, Hong, AS, Hennig, GW, Luong, D, Báo, J, Bhetwal, BP, Ro, Set al. (2014) A novel class of somatic small RNAs similar to germ cell pachytene PIWI-interacting small RNAs. J Biol Chem 289, 32824–34.CrossRefGoogle ScholarPubMed
Panneerdoss, S, Viswanadhapalli, S, Abdelfattah, N, Onyeagucha, BC, Timilsina, S, Mohammad, TA, Chen, Y, Drake, M, Vuori, K, Kumar, TRet al. (2017) Cross-talk between miR-471-5p and autophagy component proteins regulates LC3-associated phagocytosis (LAP) of apoptotic germ cells. Nat Commun 8, 598.CrossRefGoogle ScholarPubMed
Papaioannou, MD, Pitetti, JL, Ro, S, Park, C, Aubry, F, Schaad, O, Vejnar, CE, Kuhne, F, Descombes, P, Zdobnov, EMet al. (2009) Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326, 250–9.CrossRefGoogle ScholarPubMed
Papaioannou, MD, Lagarrigue, M, Vejnar, CE, Rolland, AD, Kuhne, F, Aubry, F, Schaad, O, Fort, A, Descombes, P, Neerman-Arbez, Met al. (2011) Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice. Mol Cell Proteom 10, M900587mcp900200.CrossRefGoogle Scholar
Patil, VS, Zhou, R and Rana, TM (2014) Gene regulation by noncoding RNAs. Crit Rev Biochem Mol Biol 49, 16–32.CrossRefGoogle Scholar
Pelechano, V and Steinmetz, LM (2013) Gene regulation by antisense transcription. Nat Rev Genet 14, 880–93.CrossRefGoogle ScholarPubMed
Qin, L, Lin, J and Xie, X (2019) CircRNA-9119 suppresses poly I:C induced inflammation in Leydig and Sertoli cells via TLR3 and RIG-I signal pathways. Mol Med 25, 28.CrossRefGoogle ScholarPubMed
Rakoczy, J, Fernandez-Valverde, SL, Glazov, EA, Wainwright, EN, Sato, T, Takada, S, Combes, AN, Korbie, DJ, Miller, D, Grimmond, SMet al. (2013) MicroRNAs-140-5p/140-3p modulate Leydig cell numbers in the developing mouse testis. Biol Reprod 88, 143.CrossRefGoogle ScholarPubMed
Reon, BJ, Anaya, J, Zhang, Y, Mandell, J, Purow, B, Abounader, R and Dutta, A (2016) Expression of lncRNAs in low-grade gliomas and glioblastoma multiforme: an in silico analysis. PLoS Med 13, e1002192.CrossRefGoogle ScholarPubMed
Rybak-Wolf, A, Stottmeister, C, Glazar, P, Jens, M, Pino, N, Giusti, S, Hanan, M, Behm, M, Bartok, O, Ashwal-Fluss, Ret al. (2015) Circular RNAs in the mammalian brain are highly abundant, conserved and dynamically expressed. Mol Cell 58, 870–85.CrossRefGoogle Scholar
Saad, F and Gooren, L (2009) The role of testosterone in the metabolic syndrome: a review. J Steroid Biochem Mol Biol 114(1–2), 40–3.CrossRefGoogle ScholarPubMed
Salviano-Silva, A, Lobo-Alves, SC, Almeida, RC, Malheiros, D and Petzl-Erler, ML (2018) Besides pathology: long noncoding RNA in cell and tissue homeostasis. Noncoding RNA 4(1), E3.Google ScholarPubMed
Satoh, Y, Takei, N, Kawamura, S, Takahashi, N, Kotani, T and Kimura, AP (2019) A novel testis-specific long noncoding RNA, Tesra, activates the Prss42/Tessp-2 gene during mouse spermatogenesis dagger. Biol Reprod 100, 833–48.CrossRefGoogle Scholar
Setchell, BP (2008) Blood-testis barrier, junctional and transport proteins and spermatogenesis. Adv Exp Med Biol 636, 212–33.CrossRefGoogle ScholarPubMed
Shen, WJ, Azhar, S and Kraemer, FB (2018) SR-B1: a unique multifunctional receptor for cholesterol influx and efflux. Ann Rev Physiol 80, 95–116.CrossRefGoogle ScholarPubMed
Shima, Y, Miyabayashi, K, Haraguchi, S, Arakawa, T, Otake, H, Baba, T, Matsuzaki, S, Shishido, Y, Akiyama, H, Tachibana, Tet al. (2013) Contribution of Leydig and Sertoli cells to testosterone production in mouse fetal testes. Mol Endocrinol 27, 63–73.CrossRefGoogle ScholarPubMed
Tay, Y, Zhang, J, Thomson, AM, Lim, B and Rigoutsos, I (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455(7216), 1124–8.CrossRefGoogle ScholarPubMed
Tong, MH, Mitchell, DA, McGowan, SD, Evanoff, R and Griswold, MD (2012) Two miRNA clusters, miR-17-92 (miRc1) and miR-106b-25 (miRc3), are involved in the regulation of spermatogonial differentiation in mice. Biol Reprod 86, 72.CrossRefGoogle Scholar
Unhavaithaya, Y, Hao, Y, Beyret, E, Yin, H, Kuramochi-Miyagawa, S, Nakano, T and Lin, H (2009) MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem 284, 6507–19.CrossRefGoogle ScholarPubMed
Wainwright, EN, Jorgensen, JS, Kim, Y, Truong, V, Bagheri-Fam, S, Davidson, T, Svingen, T, Fernandez-Valverde, SL, McClelland, KS, Taft, RJet al. (2013) SOX9 regulates microRNA miR-202-5p/3p expression during mouse testis differentiation. Biol Reprod 89, 34.CrossRefGoogle ScholarPubMed
Wang, H, Wang, H, Xiong, W, Chen, Y, Ma, Q, Ma, J, Ge, Y and Han, D (2006) Evaluation on the phagocytosis of apoptotic spermatogenic cells by Sertoli cells in vitro through detecting lipid droplet formation by Oil Red O staining. Reproduction 132, 485–92.CrossRefGoogle ScholarPubMed
Wang, M, Wu, W, Li, L, He, J, Huang, S, Chen, S, Chen, J, Long, M, Yang, S and Li, P (2019) Analysis of the miRNA expression profiles in the zearalenone-exposed TM3 Leydig cell line. Int J Mol Sci 20, 635.CrossRefGoogle ScholarPubMed
Wang, S, Tang, Y, Cui, H, Zhao, X, Luo, X, Pan, W, Huang, X and Shen, N (2011) Let-7/miR-98 regulate Fas and Fas-mediated apoptosis. Genes Immun 12, 149–54.CrossRefGoogle ScholarPubMed
Wang, Y, Chen, F, Ye, L, Zirkin, B and Chen, H (2017) Steroidogenesis in Leydig cells: effects of aging and environmental factors. Reproduction 154, R111–22.CrossRefGoogle ScholarPubMed
Wong, CH, Cheng, CY (2005) The blood–testis barrier: its biology, regulation and physiological role in spermatogenesis. Curr Topics Dev Biol 71, 263–96.CrossRefGoogle ScholarPubMed
Yang, C, Yao, C, Tian, R, Zhu, Z, Zhao, L, Li, P, Chen, H, Huang, Y, Zhi, E, Gong, Yet al. (2019) miR-202–3p regulates Sertoli cell proliferation, synthesis function and apoptosis by targeting LRP6 and cyclin D1 of Wnt/beta-catenin signaling. Mol Ther Nucl Acids 14, 1–19.CrossRefGoogle ScholarPubMed
Yang, H, Wang, F, Li, F, Ren, C, Pang, J, Wan, Y, Wang, Z, Feng, X and Zhang, Y (2018) Comprehensive analysis of long noncoding RNA and mRNA expression patterns in sheep testicular maturation. Biol Reprod 99, 650–61.CrossRefGoogle ScholarPubMed
Yao, C, Sun, M, Yuan, Q, Niu, M, Chen, Z, Hou, J, Wang, H, Wen, L, Liu, Y, Li, Zet al. (2016) miRNA-133b promotes the proliferation of human Sertoli cells through targeting GLI3. Oncotarget 7, 2201–19.CrossRefGoogle ScholarPubMed
Zhang, X, Zhao, W, Li, C, Yu, H, Qiao, Y, Li, A, Lu, C, Zhao, Z and Sun, B (2015) Differential expression of miR-34c and its predicted target genes in testicular tissue at different development stages of swine. Asian Australas J Anim Sci 28, 1532–6.CrossRefGoogle ScholarPubMed
Zhang, Z, Shao, S and Meistrich, ML (2007) The radiation-induced block in spermatogonial differentiation is due to damage to the somatic environment, not the germ cells. J Cell Physiol 211, 149–58.CrossRefGoogle Scholar