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Research Article

Qiangjing tablets ameliorate asthenozoospermia via mitochondrial ubiquitination and mitophagy mediated by LKB1/AMPK/ULK1 signaling

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Pages 271-280 | Received 26 Aug 2022, Accepted 09 Jan 2023, Published online: 19 Jan 2023

References

  • Agostini F, Monti F, Andrei F, Paterlini M, Palomba S, La Sala GB. 2017. Assisted reproductive technology treatments and quality of life: a longitudinal study among subfertile women and men. J Assist Reprod Genet. 34(10):1307–1315.
  • Anand SK, Sharma A, Singh N, Kakkar P. 2020. Activation of autophagic flux via LKB1/AMPK/mTOR axis against xenoestrogen Bisphenol-A exposure in primary rat hepatocytes. Food Chem Toxicol. 141:111314.
  • Balkan M, Tekes S, Gedik A. 2008. Cytogenetic and Y chromosome microdeletion screening studies in infertile males with oligozoospermia and azoospermia in southeast Turkey. J Assist Reprod Genet. 25(11–12):559–565.
  • Berruti G. 2021. Destruction or reconstruction: a subtle liaison between the proteolytic and signaling role of protein ubiquitination in spermatogenesis. Adv Exp Med Biol. 1288:215–240.
  • Chehab M, Madala A, Trussell JC. 2015. On-label and off-label drugs used in the treatment of male infertility. Fertil Steril. 103(3):595–604.
  • Chen X, Li X, Zhang W, He J, Xu B, Lei B, Wang Z, Cates C, Rousselle T, Li J. 2018. Activation of AMPK inhibits inflammatory response during hypoxia and reoxygenation through modulating JNK-mediated NF-κB pathway. Metabolism. 83:256–270.
  • Cordero-Martínez J, Aguirre-Alvarado C, Wong C, Rodríguez-Páez L. 2014. Effect of oxamic analogues on functional mice sperm parameters. Syst Biol Reprod Med. 60(4):189–198.
  • Du Y, Liu H, Zhang M, Zhang S, Hu J, Wu G, Yang J. 2019. Taurine increases spermatozoa quality and function in asthenospermia rats impaired by ornidazole. Adv Exp Med Biol. 1155:507–520.
  • Duan P, Quan C, Huang WT, Yang KD. 2016. PI3K-Akt/LKB1-AMPK-mTOR-p70S6K/4EBP1 signaling pathways participate in the regulation of testis development and spermatogenesis: an update. Zhonghua Nan Ke Xue. 22(11):1016–1020. (Chinese)
  • Eddy EM, Toshimori K, O'Brien DA. 2003. Fibrous sheath of mammalian spermatozoa. Microsc Res Tech. 61(1):103–115.
  • Egan D, Kim J, Shaw RJ, Guan KL. 2011. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy. 7(6):643–644.
  • Eid N, Ito Y, Horibe A, Otsuki Y, Kondo Y. 2019. Ethanol-induced mitochondrial damage in Sertoli cells is associated with Parkin overexpression and activation of mitophagy. Cells. 8(3):283.
  • Eid N, Kondo Y. 2018. Ethanol-induced mitophagy in rat Sertoli cells: implications for male fertility. Andrologia. 50(1):e12820.
  • Galluzzi L, Bravo-San Pedro JM, Kroemer G. 2017. Mitophagy: permitted by prohibitin. Curr Biol. 27(2):R73–R76.
  • He L, Zhou H, Liu H, Qu H. 2017. Prohibitin 2/PHB2 in Parkin-mediated mitophagy: a potential therapeutic target for mitochondrial diseases. Acta Biochim Biophys Sin. 49(8):750–751.
  • He W, Liu H, Hu L, Wang Y, Huang L, Liang A, Wang X, Zhang Q, Chen Y, Cao Y, et al. 2021. Icariin improves testicular dysfunction via enhancing proliferation and inhibiting mitochondria-dependent apoptosis pathway in high-fat diet and streptozotocin-induced diabetic rats. Reprod Biol Endocrinol. 19(1):168.
  • He Y, Li Y, Zhao T, Wang Y, Sun C. 2013. Ursolic acid inhibits adipogenesis in 3T3-L1 adipocytes through LKB1/AMPK pathway. PLoS One. 8(7):e70135.
  • Huang Y, Zhu X, Chen K, Lang H, Zhang Y, Hou P, Ran L, Zhou M, Zheng J, Yi L, et al. 2019. Resveratrol prevents sarcopenic obesity by reversing mitochondrial dysfunction and oxidative stress via the PKA/LKB1/AMPK pathway. Aging. 11(8):2217–2240.
  • Hwang K, Walters RC, Lipshultz LI. 2011. Contemporary concepts in the evaluation and management of male infertility. Nat Rev Urol. 8(2):86–94.
  • Jia J, Abudu YP, Claude-Taupin A, Gu Y, Kumar S, Choi SW, Peters R, Mudd MH, Allers L, Salemi M, et al. 2019. Galectins control MTOR and AMPK in response to lysosomal damage to induce autophagy. Autophagy. 15(1):169–171.
  • Jiang S, Wang Y, Luo L, Shi F, Zou J, Lin H, Ying Y, Luo Y, Zhan Z, Liu P, et al. 2019. AMP-activated protein kinase regulates cancer cell growth and metabolism via nuclear and mitochondria events. J Cell Mol Med. 23(6):3951–3961.
  • Jin C, Xue W, Liu Q, Han J, Luo R, Feng J, Liu J, Guo T, Peng X, Hu T. 2021. LKB1/AMPKα signaling pathway and mitochondrial fission/fusion dynamics regulate apoptosis induced by 3-chlorpropane-1,2-diol in HEK293 cells. Food Chem Toxicol. 154(112350):112350.
  • Jin SM, Youle RJ. 2012. PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci. 125(4):795–799.
  • Killackey SA, Philpott DJ, Girardin SE. 2020. Mitophagy pathways in health and disease. J Cell Biol. 219:e202004029.
  • Li G, Zhang P, You Y, Chen D, Cai J, Ma Z, Huang X, Chang D. 2021. Qiangjing tablets regulate apoptosis and oxidative stress via Keap/Nrf2 pathway to improve the reproductive function in asthenospermia rats. Front Pharmacol. 12:714892.
  • Li GS, Zhang PH, Cai J, Huang XP, Yu XJ, Dong L, You YD, Chen DA, Zhang L, Chang DG. 2018. Effect of Qiangjing tablets on the MAPK signaling pathway in SD rats with asthenospermia. Zhonghua Nan Ke Xue. 24(5):436–441. (Chinese).
  • Li J, Shao ZH, Xie JT, Wang CZ, Ramachandran S, Yin JJ, Aung H, Li CQ, Qin G, Vanden Hoek T, et al. 2012. The effects of ginsenoside Rb1 on JNK in oxidative injury in cardiomyocytes. Arch Pharm Res. 35(7):1259–1267.
  • Li L, Chen B, An T, Zhang H, Xia B, Li R, Zhu R, Tian Y, Wang L, Zhao D, et al. 2021. BaZiBuShen alleviates altered testicular morphology and spermatogenesis and modulates Sirt6/P53 and Sirt6/NF-κB pathways in aging mice induced by d-galactose and NaNO2. J Ethnopharmacol. 271(113810):113810.
  • Liu FJ, Liu X, Han JL, Wang YW, Jin SH, Liu XX, Liu J, Wang WT, Wang WJ. 2015. Aged men share the sperm protein PATE1 defect with young asthenozoospermia patients. Hum Reprod. 30(4):861–869.
  • Loh KP, Qi J, Tan BK, Liu XH, Wei BG, Zhu YZ. 2010. Leonurine protects middle cerebral artery occluded rats through antioxidant effect and regulation of mitochondrial function. Stroke. 41(11):2661–2668.
  • McWilliams TG, Muqit MM. 2017. PINK1 and Parkin: emerging themes in mitochondrial homeostasis. Curr Opin Cell Biol. 45:83–91.
  • Mizushima N. 2004. Methods for monitoring autophagy. Int J Biochem Cell Biol. 36(12):2491–2502.
  • Moore FL, Reijo-Pera RA. 2000. Male sperm motility dictated by mother’s mtDNA. Am J Hum Genet. 67(3):543–548.
  • Narendra DP. 2021. Managing risky assets - mitophagy in vivo. J Cell Sci. 134:jcs240465.
  • Nowicka-Bauer K, Lepczynski A, Ozgo M, Kamieniczna M, Fraczek M, Stanski L, Olszewska M, Malcher A, Skrzypczak W, Kurpisz MK. 2018. Sperm mitochondrial dysfunction and oxidative stress as possible reasons for isolated asthenozoospermia. J Physiol Pharmacol. 69:403–417.
  • Pan T, Huang YH. 2015. Ouabain and asthenospermia. Zhonghua Nan Ke Xue. 21(12):1129–1133. (Chinese).
  • Pang J, Li F, Feng X, Yang H, Han L, Fan Y, Nie H, Wang Z, Wang F, Zhang Y. 2018. Influences of different dietary energy level on sheep testicular development associated with AMPK/ULK1/autophagy pathway. Theriogenology. 108:362–370.
  • Punjani N, Kang C, Lee RK, Goldstein M, Li PS. 2021. Technological advancements in male infertility microsurgery. JCM. 10(18):4259.
  • Shay JW, Homma N, Zhou R, Naseer MI, Chaudhary AG, Al-Qahtani M, Hirokawa N, Goudarzi M, Fornace AJ, Jr., Baeesa S, et al. 2016. Abstracts from the 3rd international genomic medicine conference (3rd IGMC 2015). BMC Genomics. 17(S6):487.
  • Shen Y, You Y, Zhu K, Li G, Huang X, Chen D, Yang F, Dong L, Li J, Yu X. 2022. The traditional Chinese medicine Qiangjing tablet prevents blood-testis barrier injury induced by CdCl2 through the PI3K/Akt/Rictor signaling pathway. Environ Toxicol. 1–13. doi:10.1002/tox.23706
  • Shin S, Lee YJ, Kim EJ, Lee AS, Kang DG, Lee HS. 2011. Effect of Cuscuta chinensis on renal function in ischemia/reperfusion-induced acute renal failure rats. Am J Chin Med. 39(5):889–902.
  • Sikka SC. 2001. Relative impact of oxidative stress on male reproductive function. Curr Med Chem. 8(7):851–862.
  • Song WH, Yi YJ, Sutovsky M, Meyers S, Sutovsky P. 2016. The ART and science of sperm mitophagy. Autophagy. 12(12):2510–2511.
  • Staropoli JF, McDermott C, Martinat C, Schulman B, Demireva E, Abeliovich A. 2003. Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron. 37(5):735–749.
  • Thakur M, Chauhan NS, Sharma V, Dixit VK, Bhargava S. 2012. Effect of Curculigo orchioides on hyperglycemia-induced oligospermia and sexual dysfunction in male rats. Int J Impot Res. 24(1):31–37.
  • Thirupathi A, de Souza CT. 2017. Multi-regulatory network of ROS: the interconnection of ROS, PGC-1 alpha, and AMPK-SIRT1 during exercise. J Physiol Biochem. 73(4):487–494.
  • Vander Borght M, Wyns C. 2018. Fertility and infertility: definition and epidemiology. Clin Biochem. 62:2–10.
  • Villanueva-Paz M, Cotán D, Garrido-Maraver J, Oropesa-Ávila M, de la Mata M, Delgado-Pavón A, de Lavera I, Alcocer-Gómez E, Álvarez-Córdoba M, Sánchez-Alcázar JA. 2016. AMPK regulation of cell growth, apoptosis, autophagy, and bioenergetics. Exp Suppl. 107:45–71.
  • Wang SC, Wang SC, Li CJ, Lin CH, Huang HL, Tsai LM, Chang CH. 2018. The therapeutic effects of traditional Chinese medicine for poor semen quality in infertile males. JCM. 7(9):239.
  • Wang SQ, Cui SX, Qu XJ. 2019. Metformin inhibited colitis and colitis-associated cancer (CAC) through protecting mitochondrial structures of colorectal epithelial cells in mice. Cancer Biol Ther. 20(3):338–348.
  • Wang SQ, Yang XY, Cui SX, Gao ZH, Qu XJ. 2019. Heterozygous knockout insulin-like growth factor-1 receptor (IGF-1R) regulates mitochondrial functions and prevents colitis and colorectal cancer. Free Radic Biol Med. 134:87–98.
  • Wang Y, Nartiss Y, Steipe B, McQuibban GA, Kim PK. 2012. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy. 8(10):1462–1476.
  • Xiong GB, Yao WL, Wu FH. 2009. Shenfu Qiangjing decoction improves non-inflammatory and non-liquefied semen in kidney-yang deficiency men. Zhonghua Nan Ke Xue. 15(12):1138–1141. (Chinese).
  • Yin JY, Nie SP, Zhou C, Wan Y, Xie MY. 2010. Chemical characteristics and antioxidant activities of polysaccharide purified from the seeds of Plantago asiatica L. J Sci Food Agric. 90(2):210–217.
  • Yoshida Y, Yasuda S, Fujita T, Hamasaki M, Murakami A, Kawawaki J, Iwai K, Saeki Y, Yoshimori T, Matsuda N, et al. 2017. Ubiquitination of exposed glycoproteins by SCF(FBXO27) directs damaged lysosomes for autophagy. Proc Natl Acad Sci U S A. 114(32):8574–8579.
  • You YD, Zhang L, Yu XJ, Li GS, Huang XP, Chang DG. 2020. Inhibitory effect of Qiangjing tablets on the secretion of IL-1β and TNF-ɑ from mouse sertoli cells: a study based on the microenvironment of spermatogenesis. Zhonghua Nan Ke Xue. 26(8):740–744. (Chinese).
  • Youle RJ, Narendra DP. 2011. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 12(1):9–14.
  • Yu XJ, Li JJ, Shen YF, Huang XP, Li GS, Zhang PH, You YD, Chang DG. 2021. Qiangjing tablets improves reproductive function in oligospermia rats through toll like signaling pathway. Chinese J Sci Techl Periodicals. 41:1365–1371.
  • Zhang P, Li JJ, Yang F, Dong L, Yu XJ, Chang DG, Chen D. 2018. Clinical study of Qiangjing tablets on sperm DNA integrity and ICSI outcomes of asthenoteratospermia patient with kidney deficiency and blood stasis. Chin J Androl. 32:51–54. (Chinese).
  • Zhang PH, Chen DA, Dong L, Li GS, Yin J, Qu XW, You YD, Chang DG. 2016. Inhibitory effect of Qiangjing tablets on the Fas/FasL pathway of cell apoptosis in male SD rats with infertility. Zhonghua Nan Ke Xue. 22(3):246–251. (Chinese).
  • Zhang R, Dong H, Zhao P, Shang C, Qi H, Ma Y, Gao C, Zhang D, Shen J, Lei Y, et al. 2022. Resveratrol and Lycium barbarum polysaccharide improve Qinling giant panda (Ailuropoda melanoleuca Qinlingensis) sperm quality during cryopreservation. BMC Vet Res. 18(1):23.
  • Zhou P, Xie W, Sun Y, Dai Z, Li G, Sun G, Sun X. 2019. Ginsenoside Rb1 and mitochondria: a short review of the literature. Mol Cell Probes. 43:1–5.
  • Zhuang C, Ni S, Yang ZC, Liu RP. 2020. Oxidative stress induces chondrocyte apoptosis through caspase-dependent and caspase-independent mitochondrial pathways and the antioxidant mechanism of Angelica sinensis polysaccharide. Oxid Med Cell Longev. 2020:3240820.