Uncovering the mechanism of quercetin for treating spermatogenesis impairment by a network pharmacology approach

References

• Agarwal A, Mulgund A, Hamada A, Chyatte MR. 2015. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 13:37. Apr. 26. Epub 2015/05/01.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Rana M, Qiu E, AlBunni H, Bui AD, Henkel R. 2018. Role of oxidative stress, infection and inflammation in male infertility. Andrologia. e13126. Dec. 50. Epub 2018/12/21.
   Web of Science ®Google Scholar
• Akbari Kordkheyli V, Khonakdar Tarsi A, Mishan MA, Tafazoli A, Bardania H, Zarpou S, Bagheri A. 2019. Effects of quercetin on microRNAs: A mechanistic review. J Cell Biochem. Apr 7. Epub 2019/04/09.
   Web of Science ®Google Scholar
• Andres S, Pevny S, Ziegenhagen R, Bakhiya N, Schafer B, Hirsch-Ernst KI, Lampen A. 2018. Safety aspects of the Use of quercetin as a dietary supplement. Mol Nutr Food Res. 62. Jan. Epub 2017/11/12.
   PubMed Web of Science ®Google Scholar
• Boezio B, Audouze K, Ducrot P, Taboureau O. 2017. Network-based approaches in pharmacology. Mol Inform. 36. Oct. Epub 2017/07/12.
   Web of Science ®Google Scholar
• Calogero AE, Duca Y, Condorelli RA, La Vignera S. 2017. Male accessory gland inflammation, infertility, and sexual dysfunctions: a practical approach to diagnosis and therapy. Andrology. 5:1064–1072. Nov. Epub 2017/10/11.
   PubMed Web of Science ®Google Scholar
• Chandran U, Patwardhan B. 2017. Network ethnopharmacological evaluation of the immunomodulatory activity of Withania somnifera. J Ethnopharmacol. 197:250–256. Feb 2. Epub 2016/08/04.
   PubMed Web of Science ®Google Scholar
• Chehrei S, Moradi M, Ghiabi HR, Falahi M, Kaviani S, Ghanbari A. 2017. Pentoxifylline besides naltrexone recovers morphine-induced inflammation in male reproductive system of rats by regulating toll-like receptor pathway. Andrologia. 49. Nov. Epub 2016/12/08.
   Web of Science ®Google Scholar
• Chin CH, Chen SH, Wu HH, Ho CW, Ko MT, Lin CY. 2014. Cytohubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol. 8(Suppl 4):S11. Epub 2014/12/19.
   PubMed Web of Science ®Google Scholar
• Chu KY, Patel P, Ramasamy R. 2019. Consideration of gender differences in infertility evaluation. Curr Opin Urol. Jan 31. Epub 2019/02/06.
   Web of Science ®Google Scholar
• Dhawan P, Richmond A. 2002. A novel NF-κB-inducing kinase-MAPK signaling pathway up-regulates NF-κB activity in melanoma cells. J Biol Chem. 277:7920–7928. Mar. 8. Epub 2002/01/05.
   PubMed Web of Science ®Google Scholar
• Fraczek M, Szumala-Kakol A, Dworacki G, Sanocka D, Kurpisz M. 2013. In vitro reconstruction of inflammatory reaction in human semen: effect on sperm DNA fragmentation. J Reprod Immunol. 100:76–85. Nov. Epub 2013/12/18.
   PubMed Web of Science ®Google Scholar
• Haervig KK, Kierkegaard L, Lund R, Bruunsgaard H, Osler M, Schmidt L. 2018. Is male factor infertility associated with midlife low-grade inflammation? A population based study. Human fertility (Cambridge, England). Jun;21:146-154. Epub 2017/05/20.
   Google Scholar
• Hamza RZ, El-Shenawy NS, Ismail HA. 2015. Protective effects of blackberry and quercetin on sodium fluoride-induced oxidative stress and histological changes in the hepatic, renal, testis and brain tissue of male rat. J Basic Clin Physiol Pharmacol. 26:237–251. May. Epub 2015/04/29.
   PubMedGoogle Scholar
• He M, Wang L, Chen Y, Zhang T, Guo J. 2016. Effect of Wuziyanzong pill on levels of sex hormones, and expressions of nuclear- associated antigen Ki-67 and androgen receptor in testes of young rats. J Traditional Chin Med. 36:743–748. Dec. Epub 2016/12/01.
   Web of Science ®Google Scholar
• Herrera SC, Bach EA. 2019. JAK/STAT signaling in stem cells and regeneration: from Drosophila to vertebrates. Development (Cambridge, England). Jan 29;146. Epub 2019/01/31.
   Google Scholar
• Hong M, Li S, Wang N, Tan HY, Cheung F, Feng Y. 2017. A biomedical investigation of the hepatoprotective effect of Radix salviae miltiorrhizae and network pharmacology-based prediction of the active compounds and molecular targets. Int J Mol Sci. 18. Mar 13. Epub 2017/03/25.
   Web of Science ®Google Scholar
• Huang J, Cheung F, Tan HY, Hong M, Wang N, Yang J, Feng Y, Zheng Q. 2017. Identification of the active compounds and significant pathways of yinchenhao decoction based on network pharmacology. Mol Med Rep. 16:4583–4592. Oct. Epub 2017/08/10.
   PubMed Web of Science ®Google Scholar
• Isomaki P, Junttila I, Vidqvist KL, Korpela M, Silvennoinen O. 2015. The activity of JAK-STAT pathways in rheumatoid arthritis: constitutive activation of STAT3 correlates with interleukin 6 levels. Rheumatology. 54:1103–1113. Jun. Epub 2014/11/20.
   PubMed Web of Science ®Google Scholar
• Jiang D, Coscione A, Li L, Zeng BY. 2017. Effect of Chinese herbal medicine on male infertility. Int Rev Neurobiol. 135:297–311. Epub 2017/08/16.
   PubMed Web of Science ®Google Scholar
• Karna KK, Choi BR, Kim MJ, Kim HK, Park JK. 2019. The effect of Schisandra chinensis baillon on cross-talk between oxidative stress, endoplasmic reticulum stress, and mitochondrial signaling pathway in testes of varicocele-induced SD Rat. Int J Mol Sci. 20. Nov 17. Epub 2019/11/21.
   Web of Science ®Google Scholar
• Katz DJ, Teloken P, Shoshany O. 2017. Male infertility - The other side of the equation. Aust Fam Physician. 46:641–646. Sep. Epub 2017/09/12.
   PubMedGoogle Scholar
• Kliesch S. 2017. [Rational diagnosis and treatment of male infertility]. Urologe. 56:1116–1128. Sep. Epub 2017/07/21.
   Web of Science ®Google Scholar
• Kuprash DV, Nedospasov SA. 2016. Molecular and cellular mechanisms of inflammation. Biochem Biokhim. 81:1237–1239. Nov. Epub 2016/12/05.
   PubMed Web of Science ®Google Scholar
• La Vignera S, Condorelli RA, Vicari E, Tumino D, Morgia G, Favilla V, Cimino S, Calogero AE. 2013. Markers of semen inflammation: supplementary semen analysis? J Reprod Immunol. 100:2–10. Nov. Epub 2013/07/16.
   PubMed Web of Science ®Google Scholar
• Li SJ, Liao YF, Du Q. 2018. [Research and application of quercetin-loaded nano drug delivery system]. Zhongguo Zhong yao za zhi = Zhongguo Zhongyao Zazhi = China Journal of Chinese Materia Medica. 43:1978–1984. May. Epub 2018/06/24.
   Google Scholar
• Li G, Ma A, Shi W, Zhong XH. 2010. Quercetin protects hamster spermatogenic cells from oxidative damage induced by diethylstilboestrol. Andrologia. 42:285–290. Oct. Epub 2010/09/24.
   PubMed Web of Science ®Google Scholar
• Li T, Wernersson R, Hansen RB, Horn H, Mercer J, Slodkowicz G, Workman CT, Rigina O, Rapacki K, Staerfeldt HH, et al. 2017. A scored human protein-protein interaction network to catalyze genomic interpretation. Nat Methods. 14:61–64. Jan. Epub 2016/11/29.
   PubMed Web of Science ®Google Scholar
• Li Y, Yao J, Han C, Yang J, Chaudhry M, Wang S, Liu H, Yin Y. 2016. Quercetin, inflammation and immunity. Nutrients. 3:167. Mar. Epub 2016/05/15.
   Google Scholar
• Lim CP, Cao X. 2001. Regulation of Stat3 activation by MEK kinase 1. J Biol Chem. 276:21004–21011. Jun 15. Epub 2001/03/30.
   PubMed Web of Science ®Google Scholar
• Liu S, Chen Y, Hu S, Li C, Jian G. 2020. Protective effect and mechanism of Wuzi Yanzong Pill in rat sertoli cells under heat stress. J Beijing Univ Traditional Chinese Med. 43:386–392. May.
   Google Scholar
• Liu J, Mu J, Zheng C, Chen X, Guo Z, Huang C, Fu Y, Tian G, Shang H, Wang Y. 2016. Systems-pharmacology dissection of traditional Chinese medicine compound saffron formula reveals multi-scale treatment strategy for cardiovascular diseases. Sci Rep. 6:19809. Jan 27. Epub 2016/01/28.
   PubMed Web of Science ®Google Scholar
• Liu ZH, Sun XB. 2012. [Network pharmacology: new opportunity for the modernization of traditional Chinese medicine]. Acta Pharmaceut Sin. 47:696–703. Jun. Epub 2012/08/25.
   Google Scholar
• Lotti F, Maggi M. 2013. Interleukin 8 and the male genital tract. J Reprod Immunol. 100:54–65. Nov. Epub 2013/04/25.
   PubMed Web of Science ®Google Scholar
• Lou G, Liu Y, Wu S, Xue J, Yang F, Fu H, Zheng M, Chen Z. 2015. The p53/miR-34a/SIRT1 positive feedback loop in quercetin-induced apoptosis. Cell Physiol Biochem. 35:2192–2202. Epub 2015/04/22.
   PubMed Web of Science ®Google Scholar
• Loza-Coll MA, Petrossian CC, Boyle ML, Jones DL. 2019. Heterochromatin protein 1 (HP1) inhibits stem cell proliferation induced by ectopic activation of the Jak/STAT pathway in the Drosophila testis. Exp Cell Res. 377:1–9. Apr 15. Epub 2019/03/01.
   Web of Science ®Google Scholar
• Ma Q, Wawersik M, Matunis EL. 2014. The Jak-STAT target chinmo prevents sex transformation of adult stem cells in the Drosophila testis niche. Dev Cell. 31:474–486. Nov 24. Epub 2014/12/03.
   Web of Science ®Google Scholar
• Mao T, Han C, Wei B, Zhao L, Zhang Q, Deng R, Liu J, Luo Y, Zhang Y. 2018. Protective effects of quercetin against cadmium chloride-induced oxidative injury in goat sperm and zygotes. Biol Trace Elem Res. 185:344–355. Oct. Epub 2018/02/06.
   PubMed Web of Science ®Google Scholar
• Ning K, Zhao X, Poetsch A, Chen WH, Yang J. 2017. Computational molecular networks and network pharmacology. BioMed Res Int. 2017:7573904. Epub 2017/12/19.
   PubMed Web of Science ®Google Scholar
• Pang HQ, Yue SJ, Tang YP, Chen YY, Tan YJ, Cao YJ, Shi XQ, Zhou GS, Kang A, Huang SL, et al. 2018. Integrated metabolomics and network pharmacology approach to explain possible action mechanisms of Xin-Sheng-Hua granule for treating anemia. Front Pharmacol. 9:165. Epub 2018/03/20.
   Web of Science ®Google Scholar
• Pei T, Zheng C, Huang C, Chen X, Guo Z, Fu Y, Liu J, Wang Y. 2016. Systematic understanding the mechanisms of vitiligo pathogenesis and its treatment by Qubaibabuqi formula. J Ethnopharmacol. 190:272–287. Aug 22. Epub 2016/06/07.
   Web of Science ®Google Scholar
• Qin DN, She BR, She YC, Wang JH. 2000. Effects of flavonoids from Semen Cuscutae on the reproductive system in male rats. Asian J Androl. 2:99–102. Jun. Epub 2001/03/10.
   PubMed Web of Science ®Google Scholar
• Rusz A, Pilatz A, Wagenlehner F, Linn T, Diemer T, Schuppe HC, Lohmeyer J, Hossain H, Weidner W. 2012. Influence of urogenital infections and inflammation on semen quality and male fertility. World J Urol. 30:23–30. Feb. Epub 2011/07/13.
   PubMed Web of Science ®Google Scholar
• Seshadri S, Bates M, Vince G, Jones DI. 2011. Cytokine expression in the seminal plasma and its effects on fertilisation rates in an IVF cycle. Andrologia. 43:378–386. Dec. Epub 2011/10/01.
   Web of Science ®Google Scholar
• Shen CH, Stavnezer J. 1998. Interaction of stat6 and NF-kappaB: direct association and synergistic activation of interleukin-4-induced transcription. Mol Cell Biol. 18:3395–3404. Jun. Epub 1998/06/20.
   PubMed Web of Science ®Google Scholar
• Shen X, Zhao Z, Wang H, Guo Z, Hu B, Zhang G. 2017. Elucidation of the anti-inflammatory mechanisms of Bupleuri and Scutellariae Radix using system pharmacological analyses. Mediat Inflamm. 2017:3709874. Epub 2017/02/14.
   Web of Science ®Google Scholar
• Silva EJR, Ribeiro CM, Mirim AFM, Silva AAS, Romano RM, Hallak J, Avellar MCW. 2018. Lipopolysaccharide and lipotheicoic acid differentially modulate epididymal cytokine and chemokine profiles and sperm parameters in experimental acute epididymitis. Sci Rep. 8:103. Jan 8. Epub 2018/01/10.
   Web of Science ®Google Scholar
• Smendziuk CM, Messenberg A, Vogl AW, Tanentzapf G. 2015. Bi-directional gap junction-mediated soma-germline communication is essential for spermatogenesis. Development (Cambridge, England). Aug 1;142:2598-2609. Epub 2015/06/28.
   Google Scholar
• Stelzer G, Plaschkes I, Oz-Levi D, Alkelai A, Olender T, Zimmerman S, Twik M, Belinky F, Fishilevich S, Nudel R, et al. 2016. Varelect: the phenotype-based variation prioritizer of the GeneCards suite. BMC Genomics. 17(Suppl 2):444. Jun 23. Epub 2016/07/01.
   Google Scholar
• Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, et al. 2011. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39:D561–D568. Jan. Epub 2010/11/04.
   PubMed Web of Science ®Google Scholar
• Uygur R, Yagmurca M, Alkoc OA, Genc A, Songur A, Ucok K, Ozen OA. 2014. Effects of quercetin and fish n-3 fatty acids on testicular injury induced by ethanol in rats. Andrologia. 46:356–369. May. Epub 2013/03/16.
   PubMed Web of Science ®Google Scholar
• Wang Z, Yang Y, Yang H, Capó-Aponte JE, Tachado SD, Wolosin JM, Reinach PS. 2011. NF-κB feedback control of JNK1 activation modulates TRPV1-induced increases in IL-6 and IL-8 release by human corneal epithelial cells. Mol Vision. 17:3137–3146. Epub 2011/12/16.
   PubMed Web of Science ®Google Scholar
• Wazea SA, Wadie W, Bahgat AK, El-Abhar HS. 2018. Galantamine anti-colitic effect: role of alpha-7 nicotinic acetylcholine receptor in modulating Jak/STAT3, NF-κB/HMGB1/RAGE and p-AKT/Bcl-2 pathways. Sci Rep. 8:5110. Mar 23. Epub 2018/03/25.
   PubMed Web of Science ®Google Scholar
• Xie T, Chen H, Shen S, Huang T, Huang B, Hu G, Li L, Xu Y. 2019. Proteasome activator REGγ promotes inflammation in Leydig cells via IkBϵ signaling. Int J Mol Med. 43:1961–1968. May. Epub 2019/03/01.
   Web of Science ®Google Scholar
• Xu D, Hu MJ, Wang YQ, Cui YL. 2019. Antioxidant activities of Quercetin and its complexes for medicinal application. Molecules. 24:1123. Mar 21. Epub 2019/03/25.
   Web of Science ®Google Scholar
• Xu L, Qiao YQ, Zheng Q. 2021. Identification of an autophagy-related gene expression signature for colorectal cancer. All Life. 14(1):91–101. Epub 2021/01/22.
   Web of Science ®Google Scholar
• Yelumalai S, Giribabu N, Karim K, Omar SZ, Salleh NB. 2019. In vivo administration of quercetin ameliorates sperm oxidative stress, inflammation, preserves sperm morphology and functions in streptozotocin-nicotinamide induced adult male diabetic rats. Arch Med Sci. 15:240–249. Jan. Epub 2019/01/31.
   Web of Science ®Google Scholar
• Yi X, Gao H, Chen D, Tang D, Huang W, Li T, Ma T, Chang B. 2017. Effects of obesity and exercise on testicular leptin signal transduction and testosterone biosynthesis in male mice. Am J Physiol Regulatory, Integr Compar Physiol. 312:R501–R510. Apr 1. Epub 2017/01/20.
   PubMed Web of Science ®Google Scholar
• Yoshimoto H, Takeo T, Nakagata N. 2017. Dimethyl sulfoxide and quercetin prolong the survival, motility, and fertility of cold-stored mouse sperm for 10 days. Biol Reprod. 97:883–891. Jan 1. Epub 2017/11/11.
   PubMed Web of Science ®Google Scholar
• Zhan XX, Qing XR, Shang XJ, Huang YF. 2013. [Lipopolysaccharide affects male reproductive function through toll-like receptors]. Zhonghua nan ke xue = National Journal of Andrology. 19:163–168. Feb. Epub 2013/02/28.
   Google Scholar
• Zhang W, Tao Q, Guo Z, Fu Y, Chen X, Shar PA, Shahen M, Zhu J, Xue J, Bai Y, et al. 2016. Systems pharmacology dissection of the integrated treatment for cardiovascular and gastrointestinal disorders by traditional Chinese medicine. Sci Rep. 6:32400. Sep 6. Epub 2016/09/07.
   PubMed Web of Science ®Google Scholar
• Zhang X, Wang T, Deng T, Xiong W, Lui P, Li N, Chen Y, Han D. 2013. Damaged spermatogenic cells induce inflammatory gene expression in mouse sertoli cells through the activation of toll-like receptors 2 and 4. Mol Cell Endocrinol. 365:162–173. Jan 30. Epub 2012/11/06.
   Web of Science ®Google Scholar
• Zhang W, Wang Y, Yang Z, Qiu J, Ma J, Zhao Z, Bao T. 2011. Antioxidant treatment with quercetin ameliorates erectile dysfunction in streptozotocin-induced diabetic rats. J Biosci Bioeng. 112:215–218. Sep. Epub 2011/06/15.
   PubMed Web of Science ®Google Scholar
• Zhang R, Zhu X, Bai H, Ning K. 2019. Network pharmacology databases for traditional Chinese Medicine: review and assessment. Front Pharmacol. 10:123. Epub 2019/03/09.
   PubMed Web of Science ®Google Scholar
• Zhou SH, Deng YF, Weng ZW, Weng HW, Liu ZD. 2019. Traditional Chinese Medicine as a remedy for male infertility: A review. World J Mens Health. Jan 10. Epub 2019/01/16.
   Google Scholar
• Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, Benner C, Chanda SK. 2019. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 10:1523. Apr 3. Epub 2019/04/05.
   PubMed Web of Science ®Google Scholar