Autophagy in male reproduction

References

• Ahmed N, Liu Y, Chen H, Yang P, Waqas Y, Liu T, Gandahi JA, Huang Y, Wang L, Song X, et al. 2016. Novel cellular evidence of lipophagy within the Sertoli cells during spermatogenesis in the turtle. Aging. 9(1):41–51.
   PubMedGoogle Scholar
• Ahmed N, Yang P, Huang Y, Chen H, Liu T, Wang L, Nabi F, Liu Y, Chen Q. 2017. Entosis acts as a novel way within Sertoli cells to eliminate spermatozoa in seminiferous tubule. Front Physiol. 8:361.
   PubMed Web of Science ®Google Scholar
• Al Rawi S, Louvet-Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V. 2012. Allophagy: a macroautophagic process degrading spermatozoid-inherited organelles. Autophagy. 8(3):421–423.
   PubMed Web of Science ®Google Scholar
• Azhar S, Leers-Sucheta S, Reaven E. 2003. Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and ‘selective‘ pathway connection. Front Biosci. 8:s998–1029.
   PubMed Web of Science ®Google Scholar
• Azhar S, Reaven E. 2002. Scavenger receptor class BI and selective cholesteryl ester uptake: partners in the regulation of steroidogenesis. Mol Cell Endocrinol. 195((1–2):1–26).
   PubMed Web of Science ®Google Scholar
• Chen Y, Zhou Y, Wang X, Qian W, Han X. 2013. Microcystin-LR induces autophagy and apoptosis in rat Sertoli cells in vitro. Toxicon. 76:84–93.
   PubMed Web of Science ®Google Scholar
• Choi AM, Ryter SW, Levine B. 2013. Autophagy in human health and disease. N Engl J Med. 368(19):1845–1846.
   PubMed Web of Science ®Google Scholar
• Clewell RA, Pluta L, Thomas RS, Andersen ME. 2009. In utero exposure to chloroquine alters sexual development in the male fetal rat. Toxicol Appl Pharmacol. 237(3):366–374.
   PubMed Web of Science ®Google Scholar
• Danzo BJ, Pavlou SN, Anthony HL. 1990. Hormonal regulation of androgen-binding protein in the rat. Endocrinology. 127(6):2829–2838.
   PubMed Web of Science ®Google Scholar
• Della-Maria J, Gerard A, Franck P, Gerard H. 2002. Effects of androgen-binding protein (ABP) on spermatid Tnp1 gene expression in vitro. Mol Cell Endocrinol. 198(1–2):131–141.
   PubMed Web of Science ®Google Scholar
• Den Hond E, Tournaye H, De Sutter P, Ombelet W, Baeyens W, Covaci A, Cox B, Nawrot TS, Van Larebeke N, D‘Hooghe T. 2015. Human exposure to endocrine disrupting chemicals and fertility: a case-control study in male subfertility patients. Environ Int. 84:154–160.
   PubMed Web of Science ®Google Scholar
• Duan P, Hu C, Quan C, Yu T, Zhou W, Yuan M, Shi Y, Yang K. 2016. 4-nonylphenol induces apoptosis, autophagy and necrosis in Sertoli cells: involvement of ROS-mediated AMPK/AKT-mTOR and JNK pathways. Toxicology. 341–343:28–40.
   PubMed Web of Science ®Google Scholar
• Eid N, Ito Y, Otsuki Y. 2012. Enhanced mitophagy in Sertoli cells of ethanol-treated rats: morphological evidence and clinical relevance. J Mol Histol. 43(1):71–80.
   PubMed Web of Science ®Google Scholar
• Gao F, Li G, Liu C, Gao H, Wang H, Liu W, Chen M, Shang Y, Wang L, Shi J, et al. 2018. Autophagy regulates testosterone synthesis by facilitating cholesterol uptake in Leydig cells. J Cell Biol. 217(6):2103–2119.
   PubMed Web of Science ®Google Scholar
• He M, Ding Y, Chu C, Tang J, Xiao Q, Luo ZG. 2016. Autophagy induction stabilizes microtubules and promotes axon regeneration after spinal cord injury. Proc Natl Acad Sci USA. 113(40):11324–11329.
   PubMed Web of Science ®Google Scholar
• Horibe A, Eid N, Ito Y, Otsuki Y, Kondo Y. 2019. Ethanol-induced autophagy in Sertoli cells is specifically marked at androgen-dependent stages of the spermatogenic cycle: potential mechanisms and implications. Int J Mol Sci. 20:1.
   Web of Science ®Google Scholar
• Jung CH, Ro SH, Cao J, Otto NM, Kim DH. 2010. mTOR regulation of autophagy. FEBS Lett. 584(7):1287–1295.
   PubMed Web of Science ®Google Scholar
• Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, Krausz C; European association of urology working group on male infertility. 2012. European association of urology guidelines on male infertility: the 2012 update. Eur Urol. 62(2): 324–332.
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 19(21):5720–5728.
   PubMed Web of Science ®Google Scholar
• Kast DJ, Dominguez R. 2017. The cytoskeleton-autophagy connection. Curr Biol. 27(8):R318–R326.
   PubMed Web of Science ®Google Scholar
• Khire A, Jo KH, Kong D, Akhshi T, Blachon S, Cekic AR, Hynek S, Ha A, Loncarek J, Mennella V, et al. 2016. Centriole remodeling during spermiogenesis in Drosophila. Curr Biol. 26(23):3183–3189.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ. 2005. The molecular machinery of autophagy: unanswered questions. J Cell Sci. 118(Pt 1):7–18.
   PubMed Web of Science ®Google Scholar
• Knez J. 2013. Endocrine-disrupting chemicals and male reproductive health. Reprod Biomed Online. 26(5):440–448.
   PubMed Web of Science ®Google Scholar
• Levine B, Klionsky DJ. 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 6(4):463–477.
   PubMed Web of Science ®Google Scholar
• Li WR, Chen L, Chang ZJ, Xin H, Liu T, Zhang YQ, Li GY, Zhou F, Gong YQ, Gao ZZ, et al. 2011. Autophagic deficiency is related to steroidogenic decline in aged rat Leydig cells. Asian J Androl. 13(6):881–888.
   PubMed Web of Science ®Google Scholar
• Lin L, Baehrecke EH. 2015. Autophagy, cell death, and cancer. Mol Cell Oncol. 2(3):e985913.
   PubMed Web of Science ®Google Scholar
• Liu C, Wang H, Shang Y, Liu W, Song Z, Zhao H, Wang L, Jia P, Gao F, Xu Z, et al. 2016. Autophagy is required for ectoplasmic specialization assembly in sertoli cells. Autophagy. 12(5):814–832.
   PubMed Web of Science ®Google Scholar
• Liu K, Czaja MJ. 2013. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ. 20(1):3–11.
   PubMed Web of Science ®Google Scholar
• Luke B. 2017. Pregnancy and birth outcomes in couples with infertility with and without assisted reproductive technology: with an emphasis on US population-based studies. Am J Obstet Gynecol. 217(3):270–281.
   PubMed Web of Science ®Google Scholar
• Luo SM, Schatten H, Sun QY. 2013. Sperm mitochondria in reproduction: good or bad and where do they go? J Genet Genomics. 40(11):549–556.
   PubMed Web of Science ®Google Scholar
• Ma Y, Yang HZ, Xu LM, Huang YR, Dai HL, Kang XN. 2015. Testosterone regulates the autophagic clearance of androgen binding protein in rat Sertoli cells. Sci Rep. 5:8894.
   PubMed Web of Science ®Google Scholar
• Ma Y, Zhou Y, Zhu YC, Wang SQ, Ping P, Chen XF. 2018. Lipophagy contributes to testosterone biosynthesis in male rat Leydig cells. Endocrinology. 159(2):1119–1129.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell. 140(3):313–326.
   PubMed Web of Science ®Google Scholar
• Nicola WG, Khayria MI, Osfor MM. 1997. Plasma testosterone level and the male genital system after chloroquine therapy. Boll Chim Farm. 136(1):39–43.
   PubMedGoogle Scholar
• Okanlawon AO, Noronha CC, Ashiru OA. 1993. An investigation into the effects of chloroquine on fertility of male rats. West Afr J Med. 12(2):118–121.
   PubMedGoogle Scholar
• Pegoraro AF, Janmey P, Weitz DA. 2017. Mechanical properties of the cytoskeleton and cells. Cold Spring Harb Perspect Biol. 9:11.
   Web of Science ®Google Scholar
• Politi Y, Gal L, Kalifa Y, Ravid L, Elazar Z, Arama E. 2014. Paternal mitochondrial destruction after fertilization is mediated by a common endocytic and autophagic pathway in Drosophila. Dev Cell. 29(3):305–320.
   PubMed Web of Science ®Google Scholar
• Qian X, Mruk DD, Cheng YH, Tang EI, Han D, Lee WM, Wong EW, Cheng CY. 2014. Actin binding proteins, spermatid transport and spermiation. Semin Cell Dev Biol. 30:75–85.
   PubMed Web of Science ®Google Scholar
• Rainsford KD, Parke AL, Clifford-Rashotte M, Kean WF. 2015. Therapy and pharmacological properties of hydroxychloroquine and chloroquine in treatment of systemic lupus erythematosus, rheumatoid arthritis and related diseases. Inflammopharmacology. 23(5):231–269.
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al. 2010. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev. 90(4):1383–1435.
   PubMed Web of Science ®Google Scholar
• Rojansky R, Cha MY, Chan DC. 2016. Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. eLife. 5:e17896.
   PubMed Web of Science ®Google Scholar
• Sato M, Sato K. 2011. Degradation of paternal mitochondria by fertilization-triggered autophagy in C. Elegans Embryos Sci. 334(6059):1141–1144.
   Google Scholar
• Schlatt S, Ehmcke J. 2014. Regulation of spermatogenesis: an evolutionary biologist‘s perspective. Semin Cell Dev Biol. 29:2–16.
   PubMed Web of Science ®Google Scholar
• Shang Y, Wang H, Jia P, Zhao H, Liu C, Liu W, Song Z, Xu Z, Yang L, Wang Y, et al. 2016. Autophagy regulates spermatid differentiation via degradation of PDLIM1. Autophagy. 12(9):1575–1592.
   PubMed Web of Science ®Google Scholar
• Sharlip ID, Jarow JP, Belker AM, Lipshultz LI, Sigman M, Thomas AJ, Schlegel PN, Howards SS, Nehra A, Damewood MD, et al. 2002. Best practice policies for male infertility. Fertil Steril. 77(5):873–882.
   PubMed Web of Science ®Google Scholar
• Shen WJ, Azhar S, Kraemer FB. 2016. Lipid droplets and steroidogenic cells. Exp Cell Res. 340(2):209–214.
   PubMed Web of Science ®Google Scholar
• Singh R, Cuervo AM. 2012. Lipophagy: connecting autophagy and lipid metabolism. Int J Cell Biol. 2012:282041.
   PubMedGoogle Scholar
• Song WH, Yi YJ, Sutovsky M, Meyers S, Sutovsky P. 2016. Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization. Proc Natl Acad Sci USA. 113(36):E5261–5270.
   PubMed Web of Science ®Google Scholar
• Stocco DM. 1999. Steroidogenic acute regulatory (StAR) protein: what‘s new? Bioessays. 21(9):768–775.
   PubMed Web of Science ®Google Scholar
• Sun Y, Shen J, Zeng L, Yang D, Shao S, Wang J, Wei J, Xiong J, Chen J. 2018. Role of autophagy in di-2-ethylhexyl phthalate (DEHP)-induced apoptosis in mouse Leydig cells. Environ Pollut. 243(Pt A):563–572.
   PubMedGoogle Scholar
• Tarique I, Vistro WA, Bai X, Yang P, Hong C, Huang Y, Haseeb A, Liu E, Gandahi NS, Xu M, et al. 2019. LIPOPHAGY: a novel form of steroidogenic activity within the Leydig cell during the reproductive cycle of turtle. Reprod Biol Endocrinol. 17(1):19.
   PubMedGoogle Scholar
• Tolkovsky AM. 2009. Mitophagy. Biochim Biophys Acta. 1793(9):1508–1515.
   PubMed Web of Science ®Google Scholar
• Wang BJ, Zheng WL, Feng NN, Wang T, Zou H, Gu JH, Yuan Y, Liu XZ, Liu ZP, Bian JC. 2018. The effects of autophagy and PI3K/AKT/m-TOR signaling pathway on the cell-cycle arrest of rats primary Sertoli cells induced by Zearalenone. Toxins(Basel). 10:10.
   Web of Science ®Google Scholar
• Wang H, Wan H, Li X, Liu W, Chen Q, Wang Y, Yang L, Tang H, Zhang X, Duan E, et al. 2014. Atg7 is required for acrosome biogenesis during spermatogenesis in mice. Cell Res. 24(7):852–869.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zheng W, Bian X, Yuan Y, Gu J, Liu X, Liu Z, Bian J. 2014. Zearalenone induces apoptosis and cytoprotective autophagy in primary Leydig cells. Toxicol Lett. 226(2):182–191.
   PubMed Web of Science ®Google Scholar
• Weckman A, Di Ieva A, Rotondo F, Syro LV, Ortiz LD, Kovacs K, Cusimano MD. 2014. Autophagy in the endocrine glands. J Mol Endocrinol. 52(2):R151–163.
   PubMed Web of Science ®Google Scholar
• Weidberg H, Shvets E, Elazar Z. 2011. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem. 80:125–156.
   PubMed Web of Science ®Google Scholar
• Yang W, Li L, Huang X, Kan G, Lin L, Cheng J, Xu C, Sun W, Cong W, Zhao S, et al. 2017. Levels of Leydig cell autophagy regulate the fertility of male naked mole-rats. Oncotarget. 8(58):98677–98690.
   PubMedGoogle Scholar
• Ye L, Zj S, Ge RS. 2011. Inhibitors of testosterone biosynthetic and metabolic activation enzymes. Molecules. 16(12):9983–10001.
   PubMed Web of Science ®Google Scholar
• Zhang G, Liu K, Ling X, Wang Z, Zou P, Wang X, Gao J, Yin L, Zhang X, Liu J, et al. 2016. DBP-induced endoplasmic reticulum stress in male germ cells causes autophagy, which has a cytoprotective role against apoptosis in vitro and in vivo. Toxicol Lett. 245:86–98.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Han L, Yang H, Pang J, Li P, Zhang G, Li F, Wang F. 2017. Bisphenol A affects cell viability involved in autophagy and apoptosis in goat testis sertoli cell. Environ Toxicol Pharmacol. 55:137–147.
   PubMed Web of Science ®Google Scholar
• Zhuo C, Ji Y, Chen Z, Kitazato K, Xiang Y, Zhong M, Wang Q, Pei Y, Ju H, Wang Y. 2013. Proteomics analysis of autophagy-deficient Atg7-/- MEFs reveals a close relationship between F-actin and autophagy. Biochem Biophys Res Commun. 437(3):482–488.
   PubMed Web of Science ®Google Scholar