Antioxidant Nanoparticles Restore Cisplatin-Induced Male Fertility Defects by Promoting MDC1-53bp1-Associated Non-Homologous DNA Repair Mechanism and Sperm Intracellular Calcium Influx

References

• Clark GF. Molecular models for mouse sperm-oocyte binding. Glycobiology. 2011;21(1):3–5. doi:10.1093/glycob/cwq159
   PubMed Web of Science ®Google Scholar
• Tosti E, Menezo Y. Gamete activation: basic knowledge and clinical applications. Hum Reprod Update. 2016;22(4):420–439. doi:10.1093/humupd/dmw014
   PubMed Web of Science ®Google Scholar
• Finkelstein M, Etkovitz N, Breitbart H. Ca(2+) signaling in mammalian spermatozoa. Mol Cell Endocrinol. 2020;516:110953. doi:10.1016/j.mce.2020.110953
   PubMed Web of Science ®Google Scholar
• Wang H, McGoldrick LL, Chung JJ. Sperm ion channels and transporters in male fertility and infertility. Nat Rev Urol. 2021;18(1):46–66. doi:10.1038/s41585-020-00390-9
   PubMed Web of Science ®Google Scholar
• Lishko PV, Kirichok Y, Ren D, et al. The control of male fertility by spermatozoan ion channels. Annu Rev Physiol. 2012;74(1):453–475. doi:10.1146/annurev-physiol-020911-153258
   PubMedGoogle Scholar
• Ren D, Navarro B, Perez G, et al. A sperm ion channel required for sperm motility and male fertility. Nature. 2001;413(6856):603–609. doi:10.1038/35098027
   PubMed Web of Science ®Google Scholar
• Lefievre L, Nash K, Mansell S, et al. 2-APB-potentiated channels amplify CatSper-induced Ca(2+) signals in human sperm. Biochem J. 2012;448(2):189–200. doi:10.1042/BJ20120339
   PubMedGoogle Scholar
• Hirohashi N, Yanagimachi R. Sperm acrosome reaction: its site and role in fertilization. Biol Reprod. 2018;99(1):127–133. doi:10.1093/biolre/ioy045
   PubMed Web of Science ®Google Scholar
• Tsai PS, Garcia-Gil N, van Haeften T, et al. How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane. PLoS One. 2010;5(6):e11204. doi:10.1371/journal.pone.0011204
   PubMed Web of Science ®Google Scholar
• Boguenet M, Bouet P-E, Spiers A, et al. Mitochondria: their role in spermatozoa and in male infertility. Hum Reprod Update. 2021;27(4):697–719. doi:10.1093/humupd/dmab001
   PubMed Web of Science ®Google Scholar
• Losano JDA, Angrimani DDSR, Ferreira Leite R, et al. Spermatic mitochondria: role in oxidative homeostasis, sperm function and possible tools for their assessment. Zygote. 2018;26(4):251–260. doi:10.1017/S0967199418000242
   PubMed Web of Science ®Google Scholar
• Vertika S, Singh KK, Rajender S. Mitochondria, spermatogenesis, and male infertility - An update. Mitochondrion. 2020;54:26–40. doi:10.1016/j.mito.2020.06.003
   PubMed Web of Science ®Google Scholar
• Choi Y-M, Kim H-K, Shim W, et al. Mechanism of cisplatin-induced cytotoxicity is correlated to impaired metabolism due to mitochondrial ROS generation. PLoS One. 2015;10(8):e0135083. doi:10.1371/journal.pone.0135083
   PubMed Web of Science ®Google Scholar
• Liu HT, Wang T-E, Hsu Y-T, et al. Nanoparticulated honokiol mitigates cisplatin-induced chronic kidney injury by maintaining mitochondria antioxidant capacity and reducing caspase 3-associated cellular apoptosis. Antioxidants. 2019;8(10):466. doi:10.3390/antiox8100466
   Web of Science ®Google Scholar
• Wang TE, Lai Y-H, Yang K-C, et al. Counteracting cisplatin-induced testicular damages by natural polyphenol constituent honokiol. Antioxidants. 2020;9(8):723. doi:10.3390/antiox9080723
   Web of Science ®Google Scholar
• Sharma P, Sampath H. Mitochondrial DNA integrity: role in health and disease. Cells. 2019;8(2):100. doi:10.3390/cells8020100
   PubMed Web of Science ®Google Scholar
• Chainy GBN, Sahoo DK. Hormones and oxidative stress: an overview. Free Radic Res. 2020;54(1):1–26. doi:10.1080/10715762.2019.1702656
   PubMed Web of Science ®Google Scholar
• Poprac P, Jomova K, Simunkova M, et al. Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci. 2017;38(7):592–607. doi:10.1016/j.tips.2017.04.005
   PubMed Web of Science ®Google Scholar
• Aitken RJ. Impact of oxidative stress on male and female germ cells: implications for fertility. Reproduction. 2020;159(4):R189–R201. doi:10.1530/REP-19-0452
   PubMed Web of Science ®Google Scholar
• Alahmar AT. Role of oxidative stress in male infertility: an updated review. J Hum Reprod Sci. 2019;12(1):4–18. doi:10.4103/jhrs.JHRS_150_18
   PubMedGoogle Scholar
• Bansal AK, Bilaspuri GS. Impacts of oxidative stress and antioxidants on semen functions. Vet Med Int. 2010;2010. doi:10.4061/2011/686137
   PubMedGoogle Scholar
• Takeshima T, Usui K, Mori K, et al. Oxidative stress and male infertility. Reprod Med Biol. 2021;20(1):41–52. doi:10.1002/rmb2.12353
   PubMed Web of Science ®Google Scholar
• Gupta S, Finelli R, Agarwal A, et al. Total antioxidant capacity-Relevance, methods and clinical implications. Andrologia. 2021;53(2):e13624. doi:10.1111/and.13624
   PubMed Web of Science ®Google Scholar
• Miyamoto Y, Koh YH, Park YS, et al. Oxidative stress caused by inactivation of glutathione peroxidase and adaptive responses. Biol Chem. 2003;384(4):567–574. doi:10.1515/BC.2003.064
   PubMed Web of Science ®Google Scholar
• Mruk DD, Silvestrini B, Mo M-Y, et al. Antioxidant superoxide dismutase - a review: its function, regulation in the testis, and role in male fertility. Contraception. 2002;65(4):305–311. doi:10.1016/S0010-7824(01)00320-1
   PubMed Web of Science ®Google Scholar
• O’Flaherty C. Orchestrating the antioxidant defenses in the epididymis. Andrology. 2019;7(5):662–668. doi:10.1111/andr.12630
   PubMed Web of Science ®Google Scholar
• O’Flaherty C, Boisvert A, Manku G, et al. Protective role of peroxiredoxins against reactive oxygen species in neonatal rat testicular gonocytes. Antioxidants. 2019;9(1):32. doi:10.3390/antiox9010032
   Web of Science ®Google Scholar
• Rahman SU, Huang Y, Zhu L, et al. Therapeutic role of green tea polyphenols in improving fertility: a review. Nutrients. 2018;10(7):834. doi:10.3390/nu10070834
   PubMed Web of Science ®Google Scholar
• Shaito A, Posadino AM, Younes N, et al. Potential adverse effects of resveratrol: a literature review. Int J Mol Sci. 2020;21(6):2084. doi:10.3390/ijms21062084
   PubMed Web of Science ®Google Scholar
• Wang TJ, Liu H-T, Lai Y-H, et al. Honokiol, a polyphenol natural compound, attenuates cisplatin-induced acute cytotoxicity in renal epithelial cells through cellular oxidative stress and cytoskeleton modulations. Front Pharmacol. 2018;9:357. doi:10.3389/fphar.2018.00357
   PubMed Web of Science ®Google Scholar
• Ijaz MU, Tahir A, Ahmed H, et al. Chemoprotective effect of vitexin against cisplatin-induced biochemical, spermatological, steroidogenic, hormonal, apoptotic and histopathological damages in the testes of Sprague-Dawley rats. Saudi Pharm J. 2022;30(5):519–526. doi:10.1016/j.jsps.2022.03.001
   PubMed Web of Science ®Google Scholar
• Hsiao YP, Chen H-T, Liang Y-C, et al. Development of nanosome-encapsulated honokiol for intravenous therapy against experimental autoimmune encephalomyelitis. Int J Nanomedicine. 2020;15:17–29. doi:10.2147/IJN.S214349
   PubMed Web of Science ®Google Scholar
• Wang TE, Li S-H, Minabe S, et al. Mouse quiescin sulfhydryl oxidases exhibit distinct epididymal luminal distribution with segment-specific sperm surface associations. Biol Reprod. 2018;99(5):1022–1033. doi:10.1093/biolre/ioy125
   PubMed Web of Science ®Google Scholar
• Wang TE, Minabe S, Matsuda F, et al. Testosterone regulation on quiescin sulfhydryl oxidase 2 synthesis in the epididymis. Reproduction. 2021;161(5):593–602. doi:10.1530/REP-20-0629
   PubMed Web of Science ®Google Scholar
• Hara-Yokoyama M, Kurihara H, Ichinose S, et al. KIF11 as a potential marker of spermatogenesis within mouse seminiferous tubule cross-sections. J Histochem Cytochem. 2019;67(11):813–824. doi:10.1369/0022155419871027
   PubMed Web of Science ®Google Scholar
• Balbach M, Beckert V, Hansen JN, et al. Shedding light on the role of cAMP in mammalian sperm physiology. Mol Cell Endocrinol. 2018;468:111–120. doi:10.1016/j.mce.2017.11.008
   PubMed Web of Science ®Google Scholar
• Sampaio B, Ortiz I, Resende H, et al. Factors affecting intracellular calcium influx in response to calcium ionophore A23187 in equine sperm. Andrology. 2021;9(5):1631–1651. doi:10.1111/andr.13036
   PubMed Web of Science ®Google Scholar
• Ciarimboli G, Deuster D, Knief A, et al. Organic cation transporter 2 mediates cisplatin-induced oto- and nephrotoxicity and is a target for protective interventions. Am J Pathol. 2010;176(3):1169–1180. doi:10.2353/ajpath.2010.090610
   PubMed Web of Science ®Google Scholar
• Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740:364–378. doi:10.1016/j.ejphar.2014.07.025
   PubMed Web of Science ®Google Scholar
• Zhu S, Pabla N, Tang C, et al. DNA damage response in cisplatin-induced nephrotoxicity. Arch Toxicol. 2015;89(12):2197–2205. doi:10.1007/s00204-015-1633-3
   PubMed Web of Science ®Google Scholar
• Dugbartey GJ, Peppone LJ, de Graaf IAM. An integrative view of cisplatin-induced renal and cardiac toxicities: molecular mechanisms, current treatment challenges and potential protective measures. Toxicology. 2016;371:58–66. doi:10.1016/j.tox.2016.10.001
   PubMed Web of Science ®Google Scholar
• Ozkok A, Edelstein CL. Pathophysiology of cisplatin-induced acute kidney injury. Biomed Res Int. 2014;2014:967826. doi:10.1155/2014/967826
   PubMed Web of Science ®Google Scholar
• Garcia Sar D, Montes-Bayón M, Blanco González E, et al. Speciation studies of cisplatin adducts with DNA nucleotides via elemental specific detection (P and Pt) using liquid chromatography-inductively coupled plasma-mass spectrometry and structural characterization by electrospray mass spectrometry. J Anal At Spectrom. 2006;21(9):861–868. doi:10.1039/B603434A
   Web of Science ®Google Scholar
• Cullen KJ, Yang Z, Schumaker L, et al. Mitochondria as a critical target of the chemotherapeutic agent cisplatin in head and neck cancer. J Bioenerg Biomembr. 2007;39(1):43–50. doi:10.1007/s10863-006-9059-5
   PubMed Web of Science ®Google Scholar
• Marullo R, Werner E, Degtyareva N, et al. Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PLoS One. 2013;8(11):e81162. doi:10.1371/journal.pone.0081162
   PubMed Web of Science ®Google Scholar
• Santos NA, Bezerra CSC, Martins NM, et al. Hydroxyl radical scavenger ameliorates cisplatin-induced nephrotoxicity by preventing oxidative stress, redox state unbalance, impairment of energetic metabolism and apoptosis in rat kidney mitochondria. Cancer Chemother Pharmacol. 2008;61(1):145–155. doi:10.1007/s00280-007-0459-y
   PubMed Web of Science ®Google Scholar
• Wang FY, Tang X-M, Wang X, et al. Mitochondria-targeted platinum(II) complexes induce apoptosis-dependent autophagic cell death mediated by ER-stress in A549 cancer cells. Eur J Med Chem. 2018;155:639–650. doi:10.1016/j.ejmech.2018.06.018
   PubMed Web of Science ®Google Scholar
• Miller RP, Tadagavadi RK, Ramesh G, et al. Mechanisms of cisplatin nephrotoxicity. Toxins. 2010;2(11):2490–2518. doi:10.3390/toxins2112490
   PubMed Web of Science ®Google Scholar
• Zhang X, Chen H, Zhang Y, et al. HA-DOPE-modified honokiol-loaded liposomes targeted therapy for osteosarcoma. Int J Nanomedicine. 2022;17:5137–5151. doi:10.2147/IJN.S371934
   PubMed Web of Science ®Google Scholar
• Zhang Q, Li D, Guan S, et al. Tumor-targeted delivery of honokiol via polysialic acid modified zein nanoparticles prevents breast cancer progression and metastasis. Int J Biol Macromol. 2022;203:280–291. doi:10.1016/j.ijbiomac.2022.01.148
   PubMed Web of Science ®Google Scholar
• Weng Y, Zhang H, Xu S, et al. Preparation and quality evaluation of honokiol nanoparticles using a new polysaccharide polymer as its carrier. Curr Drug Deliv. 2023;20(2):183–191. doi:10.2174/1567201819666220607153457
   PubMed Web of Science ®Google Scholar
• Li X, Guan S, Li H, et al. Polysialic acid-functionalized liposomes for efficient honokiol delivery to inhibit breast cancer growth and metastasis. Drug Deliv. 2023;30(1):2181746. doi:10.1080/10717544.2023.2181746
   PubMed Web of Science ®Google Scholar
• Huang RX, Zhou PK. DNA damage response signaling pathways and targets for radiotherapy sensitization in cancer. Signal Transduct Target Therc. 2020;5(1):60.
   PubMed Web of Science ®Google Scholar
• Noordermeer SM, Adam S, Setiaputra D, et al. The shieldin complex mediates 53BP1-dependent DNA repair. Nature. 2018;560(7716):117–121. doi:10.1038/s41586-018-0340-7
   PubMed Web of Science ®Google Scholar
• Mata-Martinez E, Sánchez-Cárdenas C, Chávez JC, et al. Role of calcium oscillations in sperm physiology. Biosystems. 2021;209:104524. doi:10.1016/j.biosystems.2021.104524
   PubMed Web of Science ®Google Scholar
• Lishko PV, Mannowetz N. CatSper: a unique calcium channel of the sperm flagellum. Curr Opin Physiol. 2018;2:109–113. doi:10.1016/j.cophys.2018.02.004
   PubMed Web of Science ®Google Scholar
• Nowicka-Bauer K, Szymczak-Cendlak M. Structure and function of ion channels regulating sperm motility-an overview. Int J Mol Sci. 2021;22(6):3259. doi:10.3390/ijms22063259
   PubMed Web of Science ®Google Scholar
• Miyata H, Satouh Y, Mashiko D, et al. Sperm calcineurin inhibition prevents mouse fertility with implications for male contraceptive. Science. 2015;350(6259):442–445. doi:10.1126/science.aad0836
   PubMed Web of Science ®Google Scholar