{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T09:43:22Z","timestamp":1788947002566,"version":"build-2803163510"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,6,15]],"date-time":"2021-06-15T00:00:00Z","timestamp":1623715200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,6,15]],"date-time":"2021-06-15T00:00:00Z","timestamp":1623715200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["106-2320-B-002-040-MY3"],"award-info":[{"award-number":["106-2320-B-002-040-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["106-2320-B-002-040-MY3"],"award-info":[{"award-number":["106-2320-B-002-040-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["106-2320-B-002-040-MY3"],"award-info":[{"award-number":["106-2320-B-002-040-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["106-2320-B-002-040-MY3"],"award-info":[{"award-number":["106-2320-B-002-040-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["106-2320-B-002-059"],"award-info":[{"award-number":["106-2320-B-002-059"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["106-2320-B-002-040-MY3"],"award-info":[{"award-number":["106-2320-B-002-040-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Obese men have lower circulating testosterone than men with an optimal body mass index. Elevated fatty acids (FAs) caused by obesity have been reported to suppress the steroidogenesis of Leydig cells. Recent studies have demonstrated that autophagy regulates steroidogenesis in endocrine cells; however, few studies have investigated the molecular mechanisms of FA-impaired steroidogenesis. To study FA regulation in the steroidogenesis of Leydig cells, MA-10 cells were treated with an FA mixture and co-treated with 8-Br-cAMP to stimulate the steroidogenesis capacity. We showed that FAs led to cellular lipid accumulation and decreased steroidogenesis of MA-10 cells, and FA-suppressed steroidogenesis was largely recovered by P5 treatment but not by 22R-OHC treatment, suggesting the primary defect was the deficiency of CYP11A1. To examine the involvement of autophagy in the steroidogenesis of Leydig cells, we treated MA-10 cells with autophagy regulators, including rapamycin, bafilomycin, and chloroquine. Inhibition of late-stage autophagy including FA-upregulated Rubicon suppressed the steroidogenesis of MA-10 cells. More interestingly, Rubicon played a novel regulatory role in the steroidogenesis of MA-10 cells, independent of inhibitors of late-stage autophagy. Collectively, this study provides novel targets to investigate the interaction between FAs and steroidogenesis in steroidogenic cells.<\/jats:p>","DOI":"10.1038\/s41598-021-92008-2","type":"journal-article","created":{"date-parts":[[2021,6,15]],"date-time":"2021-06-15T06:04:25Z","timestamp":1623737065000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Fatty acids suppress the steroidogenesis of the MA-10 mouse Leydig cell line by downregulating CYP11A1 and inhibiting late-stage autophagy"],"prefix":"10.1038","volume":"11","author":[{"given":"Chien","family":"Huang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hsiu-Ju","family":"Hsu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mu-En","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng-Chieh","family":"Hsu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leang-Shin","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"De-Shien","family":"Jong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi-Fan","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chih-Hsien","family":"Chiu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,6,15]]},"reference":[{"key":"92008_CR1","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1093\/humrep\/det428","volume":"29","author":"ML Eisenberg","year":"2013","unstructured":"Eisenberg, M. L. et al. The relationship between male BMI and waist circumference on semen quality: Data from the LIFE study. Hum. Reprod. 29, 193\u2013200. https:\/\/doi.org\/10.1093\/humrep\/det428 (2013).","journal-title":"Hum. Reprod."},{"key":"92008_CR2","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1097\/01.ede.0000229953.76862.e5","volume":"17","author":"M Sallm\u00e9n","year":"2006","unstructured":"Sallm\u00e9n, M., Sandler, D. P., Hoppin, J. A., Blair, A. & Baird, D. D. Reduced fertility among overweight and obese men. Epidemiology 17, 520\u2013523. https:\/\/doi.org\/10.1097\/01.ede.0000229953.76862.e5 (2006).","journal-title":"Epidemiology"},{"key":"92008_CR3","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1093\/humupd\/dms050","volume":"19","author":"N Sermondade","year":"2012","unstructured":"Sermondade, N. et al. BMI in relation to sperm count: An updated systematic review and collaborative meta-analysis. Hum. Reprod. Update 19, 221\u2013231. https:\/\/doi.org\/10.1093\/humupd\/dms050 (2012).","journal-title":"Hum. Reprod. Update"},{"key":"92008_CR4","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1007\/s12020-015-0563-4","volume":"50","author":"M Bekaert","year":"2015","unstructured":"Bekaert, M. et al. Determinants of testosterone levels in human male obesity. Endocrine 50, 202\u2013211. https:\/\/doi.org\/10.1007\/s12020-015-0563-4 (2015).","journal-title":"Endocrine"},{"key":"92008_CR5","first-page":"E937","volume":"257","author":"AW Meikle","year":"1989","unstructured":"Meikle, A. W., Benson, S. J., Liu, X. H., Boam, W. D. & Stringham, J. D. Nonesterified fatty acids modulate steroidogenesis in mouse Leydig cells. Am. J. Physiol. 257, E937\u2013E942 (1989).","journal-title":"Am. J. Physiol."},{"key":"92008_CR6","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1186\/s12958-019-0517-4","volume":"17","author":"Z Chen","year":"2019","unstructured":"Chen, Z., Wen, D., Wang, F., Wang, C. & Yang, L. Curcumin protects against palmitic acid-induced apoptosis via the inhibition of endoplasmic reticulum stress in testicular Leydig cells. Reprod. Biol. Endocrinol. 17, 71. https:\/\/doi.org\/10.1186\/s12958-019-0517-4 (2019).","journal-title":"Reprod. Biol. Endocrinol."},{"key":"92008_CR7","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1095\/biolreprod.114.121434","volume":"91","author":"MB Rone","year":"2014","unstructured":"Rone, M. B. et al. Steroidogenesis in MA-10 mouse Leydig cells is altered via fatty acid import into the mitochondria1. Biol. Reprod. 91, 96. https:\/\/doi.org\/10.1095\/biolreprod.114.121434 (2014).","journal-title":"Biol. Reprod."},{"key":"92008_CR8","doi-asserted-by":"publisher","first-page":"659","DOI":"10.1016\/j.devcel.2019.01.007","volume":"48","author":"MJ Texada","year":"2019","unstructured":"Texada, M. J. et al. Autophagy-mediated cholesterol trafficking controls steroid production. Dev. Cell 48, 659-671.e654. https:\/\/doi.org\/10.1016\/j.devcel.2019.01.007 (2019).","journal-title":"Dev. Cell"},{"key":"92008_CR9","doi-asserted-by":"publisher","first-page":"17451","DOI":"10.1038\/s41598-019-53826-7","volume":"9","author":"C Huang","year":"2019","unstructured":"Huang, C. et al. Kisspeptin-Activated Autophagy Independently Suppresses Non-Glucose-Stimulated Insulin Secretion from Pancreatic \u03b2-Cells. Sci. Rep. 9, 17451. https:\/\/doi.org\/10.1038\/s41598-019-53826-7 (2019).","journal-title":"Sci. Rep."},{"key":"92008_CR10","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1210\/er.2016-1103","volume":"38","author":"RA Sinha","year":"2016","unstructured":"Sinha, R. A., Singh, B. K. & Yen, P. M. Reciprocal Crosstalk Between Autophagic and Endocrine Signaling in Metabolic Homeostasis. Endocr. Rev. 38, 69\u2013102. https:\/\/doi.org\/10.1210\/er.2016-1103 (2016).","journal-title":"Endocr. Rev."},{"key":"92008_CR11","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/path.2697","volume":"221","author":"D Glick","year":"2010","unstructured":"Glick, D., Barth, S. & Macleod, K. F. Autophagy: Cellular and molecular mechanisms. J. Pathol. 221, 3\u201312. https:\/\/doi.org\/10.1002\/path.2697 (2010).","journal-title":"J. Pathol."},{"key":"92008_CR12","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1128\/MCB.06159-11","volume":"32","author":"S Alers","year":"2012","unstructured":"Alers, S., L\u00f6ffler, A. S., Wesselborg, S. & Stork, B. Role of AMPK-mTOR-Ulk1\/2 in the regulation of autophagy: Cross talk, shortcuts, and feedbacks. J. Mol. Cell Biol. 32, 2\u201311. https:\/\/doi.org\/10.1128\/MCB.06159-11 (2012).","journal-title":"J. Mol. Cell Biol."},{"key":"92008_CR13","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1038\/ncb0310-207","volume":"12","author":"TE Rusten","year":"2010","unstructured":"Rusten, T. E. & Stenmark, H. p62, an autophagy hero or culprit?. Nat. Cell Biol. 12, 207\u2013209. https:\/\/doi.org\/10.1038\/ncb0310-207 (2010).","journal-title":"Nat. Cell Biol."},{"key":"92008_CR14","doi-asserted-by":"publisher","first-page":"1338","DOI":"10.1038\/s41556-018-0235-8","volume":"20","author":"AM Leidal","year":"2018","unstructured":"Leidal, A. M., Levine, B. & Debnath, J. Autophagy and the cell biology of age-related disease. Nat. Cell Biol. 20, 1338\u20131348. https:\/\/doi.org\/10.1038\/s41556-018-0235-8 (2018).","journal-title":"Nat. Cell Biol."},{"key":"92008_CR15","doi-asserted-by":"publisher","first-page":"2861","DOI":"10.1101\/gad.1599207","volume":"21","author":"N Mizushima","year":"2007","unstructured":"Mizushima, N. Autophagy: Process and function. Genes Dev. 21, 2861\u20132873. https:\/\/doi.org\/10.1101\/gad.1599207 (2007).","journal-title":"Genes Dev."},{"key":"92008_CR16","doi-asserted-by":"publisher","first-page":"1534","DOI":"10.1681\/ASN.2016070731","volume":"28","author":"T Yamamoto","year":"2017","unstructured":"Yamamoto, T. et al. High-fat diet-induced lysosomal dysfunction and impaired autophagic flux contribute to lipotoxicity in the kidney. J. Am. Soc. Nephrol. 28, 1534\u20131551. https:\/\/doi.org\/10.1681\/ASN.2016070731 (2017).","journal-title":"J. Am. Soc. Nephrol."},{"key":"92008_CR17","doi-asserted-by":"publisher","first-page":"13523","DOI":"10.1038\/s41598-020-70347-w","volume":"10","author":"H-S Kim","year":"2020","unstructured":"Kim, H.-S. et al. Metformin reduces saturated fatty acid-induced lipid accumulation and inflammatory response by restoration of autophagic flux in endothelial cells. Sci. Rep. 10, 13523. https:\/\/doi.org\/10.1038\/s41598-020-70347-w (2020).","journal-title":"Sci. Rep."},{"key":"92008_CR18","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1124\/jpet.111.184341","volume":"339","author":"S Mei","year":"2011","unstructured":"Mei, S. et al. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J. Pharmacol. Exp. Ther. 339, 487\u2013498. https:\/\/doi.org\/10.1124\/jpet.111.184341 (2011).","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"92008_CR19","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1053\/j.gastro.2007.10.010","volume":"134","author":"M Vinciguerra","year":"2008","unstructured":"Vinciguerra, M. et al. PTEN down-regulation by unsaturated fatty acids triggers hepatic steatosis via an NF-\u03baBp65\/mTOR-dependent mechanism. Gastroenterology 134, 268\u2013280. https:\/\/doi.org\/10.1053\/j.gastro.2007.10.010 (2008).","journal-title":"Gastroenterology"},{"key":"92008_CR20","doi-asserted-by":"publisher","first-page":"3262","DOI":"10.2337\/db16-0356%JDiabetes","volume":"65","author":"T-Y Liu","year":"2016","unstructured":"Liu, T.-Y. et al. FNDC5 alleviates hepatosteatosis by restoring AMPK\/mTOR-mediated autophagy, fatty acid oxidation, and lipogenesis in mice. Diabetes 65, 3262\u20133275. https:\/\/doi.org\/10.2337\/db16-0356%JDiabetes (2016).","journal-title":"Diabetes"},{"key":"92008_CR21","doi-asserted-by":"publisher","first-page":"3052","DOI":"10.1096\/fj.09-144519","volume":"24","author":"H Koga","year":"2010","unstructured":"Koga, H., Kaushik, S. & Cuervo, A. M. Altered lipid content inhibits autophagic vesicular fusion. FASEB J. 24, 3052\u20133065. https:\/\/doi.org\/10.1096\/fj.09-144519 (2010).","journal-title":"FASEB J."},{"key":"92008_CR22","doi-asserted-by":"publisher","first-page":"13999","DOI":"10.1038\/s41598-017-14376-y","volume":"7","author":"M-E Wang","year":"2017","unstructured":"Wang, M.-E. et al. Increasing dietary medium-chain fatty acid ratio mitigates high-fat diet-induced non-alcoholic steatohepatitis by regulating autophagy. Sci. Rep. 7, 13999. https:\/\/doi.org\/10.1038\/s41598-017-14376-y (2017).","journal-title":"Sci. Rep."},{"key":"92008_CR23","doi-asserted-by":"publisher","first-page":"1994","DOI":"10.1002\/hep.28820","volume":"64","author":"S Tanaka","year":"2016","unstructured":"Tanaka, S. et al. Rubicon inhibits autophagy and accelerates hepatocyte apoptosis and lipid accumulation in nonalcoholic fatty liver disease in mice. Hepatology 64, 1994\u20132014. https:\/\/doi.org\/10.1002\/hep.28820 (2016).","journal-title":"Hepatology"},{"key":"92008_CR24","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1016\/j.bbrc.2011.08.012","volume":"412","author":"Y Inami","year":"2011","unstructured":"Inami, Y. et al. Hepatic steatosis inhibits autophagic proteolysis via impairment of autophagosomal acidification and cathepsin expression. Biochem. Biophys. Res. Commun. 412, 618\u2013625. https:\/\/doi.org\/10.1016\/j.bbrc.2011.08.012 (2011).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"92008_CR25","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1016\/j.cmet.2010.04.005","volume":"11","author":"L Yang","year":"2010","unstructured":"Yang, L., Li, P., Fu, S., Calay, E. S. & Hotamisligil, G. S. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 11, 467\u2013478. https:\/\/doi.org\/10.1016\/j.cmet.2010.04.005 (2010).","journal-title":"Cell Metab."},{"key":"92008_CR26","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1038\/nature07976","volume":"458","author":"R Singh","year":"2009","unstructured":"Singh, R. et al. Autophagy regulates lipid metabolism. Nature 458, 1131\u20131135. https:\/\/doi.org\/10.1038\/nature07976 (2009).","journal-title":"Nature"},{"key":"92008_CR27","doi-asserted-by":"publisher","first-page":"223","DOI":"10.4103\/1008-682x.122365","volume":"16","author":"MN Fui","year":"2014","unstructured":"Fui, M. N., Dupuis, P. & Grossmann, M. Lowered testosterone in male obesity: Mechanisms, morbidity and management. Asian J. Androl. 16, 223\u2013231. https:\/\/doi.org\/10.4103\/1008-682x.122365 (2014).","journal-title":"Asian J. Androl."},{"key":"92008_CR28","doi-asserted-by":"publisher","first-page":"1186","DOI":"10.2337\/dc09-1649","volume":"33","author":"S Dhindsa","year":"2010","unstructured":"Dhindsa, S. et al. Testosterone concentrations in diabetic and nondiabetic obese men. Diabetes Care 33, 1186\u20131192. https:\/\/doi.org\/10.2337\/dc09-1649 (2010).","journal-title":"Diabetes Care"},{"key":"92008_CR29","doi-asserted-by":"publisher","first-page":"3077","DOI":"10.1073\/pnas.0630588100","volume":"100","author":"LL Listenberger","year":"2003","unstructured":"Listenberger, L. L. et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. PNAS 100, 3077\u20133082. https:\/\/doi.org\/10.1073\/pnas.0630588100 (2003).","journal-title":"PNAS"},{"key":"92008_CR30","doi-asserted-by":"publisher","first-page":"257","DOI":"10.3389\/fphar.2018.00257","volume":"9","author":"D Gr\u00fcnig","year":"2018","unstructured":"Gr\u00fcnig, D., Duthaler, U. & Kr\u00e4henb\u00fchl, S. Effect of toxicants on fatty acid metabolism in HepG2 cells. Front. Pharmacol. 9, 257. https:\/\/doi.org\/10.3389\/fphar.2018.00257 (2018).","journal-title":"Front. Pharmacol."},{"key":"92008_CR31","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1038\/s41387-017-0005-x","volume":"7","author":"T Pl\u00f6tz","year":"2017","unstructured":"Pl\u00f6tz, T. et al. The monounsaturated fatty acid oleate is the major physiological toxic free fatty acid for human beta cells. Nutr. Diabetes 7, 305. https:\/\/doi.org\/10.1038\/s41387-017-0005-x (2017).","journal-title":"Nutr. Diabetes"},{"key":"92008_CR32","doi-asserted-by":"publisher","first-page":"e0163214","DOI":"10.1371\/journal.pone.0163214","volume":"11","author":"AK Elshorbagy","year":"2016","unstructured":"Elshorbagy, A. K. et al. Exploring the lean phenotype of glutathione-depleted mice: Thiol, amino acid and fatty acid profiles. PLoS ONE 11, e0163214. https:\/\/doi.org\/10.1371\/journal.pone.0163214 (2016).","journal-title":"PLoS ONE"},{"key":"92008_CR33","doi-asserted-by":"publisher","first-page":"3308","DOI":"10.1210\/en.2008-1668","volume":"150","author":"PR Manna","year":"2009","unstructured":"Manna, P. R., Huhtaniemi, I. T. & Stocco, D. M. Mechanisms of protein kinase C signaling in the modulation of 3\u2032,5\u2032-cyclic adenosine monophosphate-mediated steroidogenesis in mouse gonadal cells. Endocrinology 150, 3308\u20133317. https:\/\/doi.org\/10.1210\/en.2008-1668 (2009).","journal-title":"Endocrinology"},{"key":"92008_CR34","doi-asserted-by":"publisher","first-page":"915","DOI":"10.1016\/j.jhep.2010.08.032","volume":"54","author":"S Dasarathy","year":"2011","unstructured":"Dasarathy, S. et al. Sarcopenia associated with portosystemic shunting is reversed by follistatin. J. Hepatol. 54, 915\u2013921. https:\/\/doi.org\/10.1016\/j.jhep.2010.08.032 (2011).","journal-title":"J. Hepatol."},{"key":"92008_CR35","doi-asserted-by":"publisher","first-page":"3137","DOI":"10.3892\/or.2017.5988","volume":"38","author":"B Kou","year":"2017","unstructured":"Kou, B. et al. Autophagy induction enhances tetrandrine-induced apoptosis via the AMPK\/mTOR pathway in human bladder cancer cells. Oncol. Rep. 38, 3137\u20133143. https:\/\/doi.org\/10.3892\/or.2017.5988 (2017).","journal-title":"Oncol. Rep."},{"key":"92008_CR36","doi-asserted-by":"publisher","first-page":"PR15","DOI":"10.1158\/1538-7445.TIM2013-PR15","volume":"73","author":"EAI Fonseca","year":"2013","unstructured":"Fonseca, E. A. I. et al. Abstract PR15: Antitumor effect of metformin in breast cancer is associated with AMPK and FOXO3a activation. Cancer Res. 73, PR15. https:\/\/doi.org\/10.1158\/1538-7445.TIM2013-PR15 (2013).","journal-title":"Cancer Res."},{"key":"92008_CR37","doi-asserted-by":"publisher","first-page":"3475","DOI":"10.1091\/mbc.E10-03-0182","volume":"21","author":"A Soulard","year":"2010","unstructured":"Soulard, A. et al. The rapamycin-sensitive phosphoproteome reveals that TOR controls protein kinase A toward some but not all substrates. Mol. Biol. Cell 21, 3475\u20133486. https:\/\/doi.org\/10.1091\/mbc.E10-03-0182 (2010).","journal-title":"Mol. Biol. Cell"},{"key":"92008_CR38","doi-asserted-by":"publisher","first-page":"19338","DOI":"10.1073\/pnas.1010554107","volume":"107","author":"Q Sun","year":"2010","unstructured":"Sun, Q., Westphal, W., Wong, K. N., Tan, I. & Zhong, Q. Rubicon controls endosome maturation as a Rab7 effector. PNAS 107, 19338\u201319343. https:\/\/doi.org\/10.1073\/pnas.1010554107 (2010).","journal-title":"PNAS"},{"key":"92008_CR39","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1016\/j.chom.2012.01.019","volume":"11","author":"CS Yang","year":"2012","unstructured":"Yang, C. S. et al. The autophagy regulator Rubicon is a feedback inhibitor of CARD9-mediated host innate immunity. Cell Host Microbe 11, 277\u2013289. https:\/\/doi.org\/10.1016\/j.chom.2012.01.019 (2012).","journal-title":"Cell Host Microbe"},{"key":"92008_CR40","doi-asserted-by":"publisher","first-page":"1379","DOI":"10.1111\/febs.14354","volume":"285","author":"S-W Wong","year":"2018","unstructured":"Wong, S.-W., Sil, P. & Martinez, J. Rubicon: LC3-associated phagocytosis and beyond. FEBS J. 285, 1379\u20131388. https:\/\/doi.org\/10.1111\/febs.14354 (2018).","journal-title":"FEBS J."},{"key":"92008_CR41","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1142\/S0192415X0000043X","volume":"28","author":"LS Wu","year":"2000","unstructured":"Wu, L. S. et al. Ginseng flowers stimulate progesterone production from bovine luteal cells. Am. J. Chin. Med. 28, 371\u2013377. https:\/\/doi.org\/10.1142\/S0192415X0000043X (2000).","journal-title":"Am. J. Chin. Med."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-92008-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-92008-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-92008-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T04:53:07Z","timestamp":1670043187000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-92008-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,15]]},"references-count":41,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["92008"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-92008-2","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,15]]},"assertion":[{"value":"13 January 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 June 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"12561"}}