한국동물생명공학회지 (Journal of Animal Reproduction and Biotechnology)

  • 제38권4호
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  • Pages.189-198
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  • 2023
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  • 2671-4639(pISSN)
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  • 2671-4663(eISSN)
한국동물생명공학회 (The Korean Society of Animal Reproduction and Biotechnology)
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Anti-oxidative effects of broccoli (Brassica oleracea var. italica) sprout extract in RAW 264.7 cell and cisplatin-induced testicular damage

  • Won-Young Lee (Department of Livestock, Korea National University of Agriculture and Fisheries) ;
  • Hyun-Woo Shim (Department of Animal Biotechnology, College of Life Science, Sangji University) ;
  • Hyun-Jung Park (Department of Animal Biotechnology, College of Life Science, Sangji University)
  • 투고 : 2023.09.20
  • 심사 : 2023.10.17
  • 발행 : 2023.12.31
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초록

Background: Brassica oleracea var. italica (broccoli), a rich source of antioxidants, can prevent various diseases and improve human health. In this study, we investigated the antioxidative effects of broccoli sprout extract on oxidative stress induced by lipopolysaccharide and cisplatin in cell and organ tissue models. Methods: Antioxidative effect of BSE was evaluated using DPPH and ABTS in RAW 364.7 cells, and effects of BSE on testes were investigated using Cisplatin-induced testicular damage model with an in vitro organ culture system. Results: The DPPH assay showed that the antioxidant activity of the alcoholic broccoli sprout extract was higher than that of the water extract. Additionally, the expression levels of antioxidation-related genes, Nrf2, Gsr, HO-1, and catalase, were significantly increased in broccoli sprout extract-treated RAW 264.7 cells, and the extract suppressed lipopolysaccharide-induced mitochondrial dysfunction. Based on the results in the RAW 264.7 cell culture, the antioxidative effects of the extracts were investigated in a mouse testis fragment culture. The expression of Nrf2, HO-1, and Ddx4 was clearly decreased in cisplatin-treated mouse testis fragments and not in both broccoli sprout extract- and cisplatin-treated mouse testis fragments. In addition, the oxidative marker O-HdG was strongly detected in cisplatin-treated mouse testis fragments, and these signals were reduced by broccoli sprout extract treatment. Conclusions: The results of this study show that broccoli sprout extracts could serve as potential nutraceutical agents as they possess antioxidant effects in the testes.

키워드

과제정보

This research was supported by Sangji university Research Fund, 2022. This study was supported by the graduate school of Sangji University. This Research was also supported by "Regional Innovation Strategy (RIS)" through the National Research Foundation of Korea (NRF), Funded by the Ministry of Education (MOE) (2022RIS-005).

참고문헌

  1. Al Talebi Z, Karhib MM, Taki MM, Salaam Abood E, Mubarak HA, Sahar Ahmed Ibrahim C. 2023. Chemical analysis, antioxidant, and antibacterial potential of aqueous extract of broccoli (Brassica oleracea var. italica) using GC-ms. Arch. Razi Inst. 78:593-599.
  2. Ashrafi G and Schwarz TL. 2013. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 20:31-42. https://doi.org/10.1038/cdd.2012.81
  3. Atessahin A, Karahan I, Turk G, Gur S, Yilmaz S, Ceribasi AO. 2006. Protective role of lycopene on cisplatin-induced changes in sperm characteristics, testicular damage and oxidative stress in rats. Reprod. Toxicol. 21:42-47. https://doi.org/10.1016/j.reprotox.2005.05.003
  4. Azab A, Nassar A, Azab AN. 2016. Anti-inflammatory activity of natural products. Molecules 21:1321.
  5. Becker TM, Jeffery EH, Juvik JA. 2017. Proposed method for estimating health-promoting glucosinolates and hydrolysis products in broccoli (Brassica oleracea var. italica) using relative transcript abundance. J. Agric. Food Chem. 65:301-308. https://doi.org/10.1021/acs.jafc.6b04668
  6. Cui W, Leng B, Wang G. 2019. Klotho protein inhibits H2O2-induced oxidative injury in endothelial cells via regulation of PI3K/AKT/Nrf2/HO-1 pathways. Can. J. Physiol. Pharmacol. 97:370-376. https://doi.org/10.1139/cjpp-2018-0277
  7. Dai X, Yan X, Wintergerst KA, Cai L, Keller BB, Tan Y. 2020. Nrf2: redox and metabolic regulator of stem cell state and function. Trends Mol. Med. 26:185-200. https://doi.org/10.1016/j.molmed.2019.09.007
  8. Droge W. 2002. Free radicals in the physiological control of cell function. Physiol. Rev. 82:47-95. https://doi.org/10.1152/physrev.00018.2001
  9. Duan X, Li J, Cui J, Dong Y, Xin X, Aisa HA. 2022. Anti-inflammatory activity of Anchusa italica Retz. in LPS-stimulated RAW264.7 cells mediated by the Nrf2/HO-1, MAPK and NFκB signaling pathways. J. Ethnopharmacol. 286:114899.
  10. Gandin V, Hoeschele JD, Margiotta N. 2023. Special issue "cisplatin in cancer therapy: molecular mechanisms of action 3.0". Int. J. Mol. Sci. 24:7917.
  11. Hossain MN, De Leo V, Tamborra R, Laselva O, Ingrosso C, Daniello V, Catucci L, Losito I, Sollitto F, Loizzi D, Conese M, Di Gioia S. 2022. Characterization of anti-proliferative and anti-oxidant effects of nano-sized vesicles from Brassica oleracea var. italica (Broccoli). Sci. Rep. 12:14362.
  12. Jazayeri O, Farahmand Araghi S, Aghajanzadeh TA, Mir Moammadrezaei F. 2021. Up-regulation of Arl4a gene expression by broccoli aqueous extract is associated with improved spermatogenesis in mouse testes. Biomedica 41:706-720. https://doi.org/10.7705/biomedica.5962
  13. Karimi S, Hosseinimehr SJ, Mohammadi HR, Khalatbary AR, Amiri FT. 2018. Zatariamultiflora ameliorates cisplatin-induced testicular damage via suppression of oxidative stress and apoptosis in a mice model. Iran. J. Basic Med. Sci. 21:607-614.
  14. Laskin DL, Sunil VR, Gardner CR, Laskin JD. 2011. Macrophages and tissue injury: agents of defense or destruction? Annu. Rev. Pharmacol. Toxicol. 51:267-288. https://doi.org/10.1146/annurev.pharmtox.010909.105812
  15. Lin PS, Kwock L, Butterfield CE. 1979. Diethyldithiocarbamate enhancement of radiation and hyperthermic effects on Chinese hamster cells in vitro. Radiat. Res. 77:501-511. https://doi.org/10.2307/3575161
  16. Lv X, Meng G, Li W, Fan D, Wang X, Espinoza-Pinochet CA, Cespedes-Acuna CL. 2020. Sulforaphane and its antioxidative effects in broccoli seeds and sprouts of different cultivars. Food Chem. 316:126216.
  17. Mantilla-Rojas C, Velasquez FC, Morton JE, Clemente LC, Parra ER, Torres-Cabala C, Sevick-Muraca EM. 2022. Enhanced Tcell priming and improved anti-tumor immunity through lymphatic delivery of checkpoint blockade immunotherapy. Cancers (Basel) 14:1823.
  18. Mohamed SS, Ibrahim GS, Ghoneim MAM, Hassan AI. 2023. Evaluating the role of polysaccharide extracted from Pleurotus columbinus on cisplatin-induced oxidative renal injury. Sci. Rep. 13:835.
  19. Mohanta O, Ray A, Jena S, Sahoo A, Panda SS, Das PK, Nayak S, Panda PC. 2023. Mesosphaerum suaveolens essential oil attenuates inflammatory response and oxidative stress in LPSstimulated RAW 264.7 macrophages by regulating NF-κB signaling pathway. Molecules 28:5817.
  20. Mokuno K, Ohtani K, Suzumura A, Kiyosawa K, Hirose Y, Kawai K, Kato K. 1994. Induction of manganese superoxide dismutase by cytokines and lipopolysaccharide in cultured mouse astrocytes. J. Neurochem. 63:612-616. https://doi.org/10.1046/j.1471-4159.1994.63020612.x
  21. Niu T, Xuan R, Jiang L, Wu W, Zhen Z, Song Y, Hong L, Zheng K, Zhang J, Xu Q, Tan Y, Yan X, Chen H. 2018. Astaxanthin induces the Nrf2/HO-1 antioxidant pathway in human umbilical vein endothelial cells by generating trace amounts of ROS. J. Agric. Food Chem. 66:1551-1559. https://doi.org/10.1021/acs.jafc.7b05493
  22. Nizami ZN, Aburawi HE, Semlali A, Muhammad K, Iratni R. 2023. Oxidative stress inducers in cancer therapy: preclinical and clinical evidence. Antioxidants (Basel) 12:1159.
  23. Obrenovich ME, Li Y, Parvathaneni K, Yendluri BB, Palacios HH, Leszek J, Aliev G. 2011. Antioxidants in health, disease and aging. CNS Neurol. Disord. Drug Targets 10:192-207. https://doi.org/10.2174/187152711794480375
  24. Park HJ, Kim JS, Lee R, Song H. 2022. Cisplatin induces apoptosis in mouse neonatal testes organ culture. Int. J. Mol. Sci. 23:13360.
  25. Park HJ, Lee R, Yoo H, Hong K, Song H. 2020a. Nonylphenol induces apoptosis through ROS/JNK signaling in a spermatogonia cell line. Int. J. Mol. Sci. 22:307.
  26. Park HJ, Lee WY, Zhang M, Hong KH, Park C, Kim JH, Song H. 2020b. Evaluation of resmethrin toxicity to neonatal testes in organ culture. Toxicol. Sci. 173:53-64. https://doi.org/10.1093/toxsci/kfz212
  27. Park HJ. 2023. Anti-inflammatory properties of broccoli sprout extract in a lipopolysaccharide-induced testicular dysfunction. J. Anim. Reprod. Biotechnol. 38:17-25. https://doi.org/10.12750/JARB.38.1.17
  28. Raza H, John A, Shafarin J. 2016. Potentiation of LPS-induced apoptotic cell death in human hepatoma HepG2 cells by aspirin via ROS and mitochondrial dysfunction: protection by N-acetyl cysteine. PLoS One 11:e0159750.
  29. Rotimi DE, Elebiyo TC, Ojo OA. 2023. Therapeutic potential of rutin in male infertility: a mini review. J. Integr. Med. 21:130-135. https://doi.org/10.1016/j.joim.2023.01.004
  30. Santos NA, Catao CS, Martins NM, Curti C, Bianchi ML, Santos AC. 2007. Cisplatin-induced nephrotoxicity is associated with oxidative stress, redox state unbalance, impairment of energetic metabolism and apoptosis in rat kidney mitochondria. Arch. Toxicol. 81:495-504. https://doi.org/10.1007/s00204-006-0173-2
  31. Shimizu S, Kasai S, Yamazaki H, Tatara Y, Mimura J, Engler MJ, Tanji K, Nikaido Y, Inoue T, Suganuma H, Wakabayashi K, Itoh K. 2022. Sulforaphane increase mitochondrial biogenesis-related gene expression in the hippocampus and suppresses age-related cognitive decline in mice. Int. J. Mol. Sci. 23:8433.
  32. Sobuj MKA, Islam MA, Islam MS, Islam MM, Mahmud Y, Rafiquzzaman SM. 2021. Effect of solvents on bioactive compounds and antioxidant activity of Padina tetrastromatica and Gracilaria tenuistipitata seaweeds collected from Bangladesh. Sci. Rep. 11:19082.
  33. Sul OJ and Ra SW. 2021. Quercetin prevents LPS-induced oxidative stress and inflammation by modulating NOX2/ROS/NF-kB in lung epithelial cells. Molecules 26:6949.
  34. Sun F, Xu K, Zhou J, Zhang W, Duan G, Lei M. 2023. Allicin protects against LPS-induced cardiomyocyte injury by activating Nrf2-HO-1 and inhibiting NLRP3 pathways. BMC Cardiovasc. Disord. 23:410.
  35. Syed RU, Moni SS, Break MKB, Khojali WMA, Jafar M, Alshammari MD, Abdelsalam K, Taymour S, Alreshidi KSM, Elhassan Taha MM, Mohan S. 2023. Broccoli: a multi-faceted vegetable for health: an in-depth review of its nutritional attributes, antimicrobial abilities, and anti-inflammatory properties. Antibiotics (Basel) 12:1157.
  36. Tian En L, Brougham MFH, Wallace WHB, Mitchell RT. 2020. Impacts of platinum-based chemotherapy on subsequent testicular function and fertility in boys with cancer. Hum. Reprod. Update 26:874-885. https://doi.org/10.1093/humupd/dmaa041
  37. Venkatesan T, Choi YW, Kim YK. 2019a. Impact of different extraction solvents on phenolic content and antioxidant potential of Pinus densiflora bark extract. Biomed Res. Int. 2019:3520675.
  38. Venkatesan T, Choi YW, Kim YK. 2019b. Effect of an extraction solvent on the antioxidant quality of Pinus densiflora needle extract. J. Pharm. Anal. 9:193-200. https://doi.org/10.1016/j.jpha.2019.03.005
  39. Vomhof-Dekrey EE and Picklo MJ Sr. 2012. The Nrf2-antioxidant response element pathway: a target for regulating energy metabolism. J. Nutr. Biochem. 23:1201-1206. https://doi.org/10.1016/j.jnutbio.2012.03.005
  40. Yu W, Zhang X, Wu H, Zhou Q, Wang Z, Liu R, Liu J, Wang X, Hai C. 2017. HO-1 is essential for tetrahydroxystilbene glucoside mediated mitochondrial biogenesis and anti-inflammation process in LPS-treated RAW264.7 macrophages. Oxid. Med. Cell. Longev. 2017:1818575.
  41. Zare S, Karbasforooshan H, Hayes AW, Karimi G. 2023. The modulation of sirtuins by natural compounds in the management of cisplatin-induced nephrotoxicity. Naunyn Schmiedebergs Arch. Pharmacol. 396:693-703.