Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
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Anti-inflammatory properties of broccoli sprout extract in a lipopolysaccharide-induced testicular dysfunction

  • Hyun-Jung Park (Department of Animal Biotechnology, College of Life Science, Sangji University)
  • Received : 2023.02.24
  • Accepted : 2023.03.05
  • Published : 2023.03.31
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Abstract

Brassica oleracea var. italica (broccoli) is a type of cabbage that contains vitamins, minerals, and phytochemicals. Consequently, it is used as a potential nutraceutical source for improving human health by reducing oxidative stress and inflammatory responses. Here, the effects of broccoli sprout extract (BSE) on the inflammatory response were investigated through lipopolysaccharide (LPS)-induced inflammatory mouse models. First, we found that the BSE obviously reduce NO production in RAW 264.7 cells in response to LPS stimulation in in vitro study. Pretreatment with BSE administration improved sperm motility and testicular cell survivability in LPS-induced endotoxemic mice. Additionally, BSE treatment decreased the levels of the pro-inflammatory cytokines TNF-a, IL-1β, and IL-6, and COX-2 in testis of LPS-induced endotoxemic mice models. In conclusion, BSE could be a potential nutraceutical for preventing the excessive immune related infertility.

Keywords

Acknowledgement

This work was supported by the Regional Specialized Industry Development Plus Program (S3271756), funded by Ministry of SMEs and Startups (MSS, Korea).

References

  1. Azab A, Nassar A, Azab AN. 2016. Anti-inflammatory activity of natural products. Molecules 21:1321.
  2. Bauman JE, Zang Y, Sen M, Li C, Wang L, Egner PA, Fahey JW, Normolle DP, Grandis JR, Kensler TW, Johnson DE. 2016. Prevention of carcinogen-induced oral cancer by sulforaphane. Cancer Prev. Res. (Phila.) 9:547-557. https://doi.org/10.1158/1940-6207.CAPR-15-0290
  3. Bozkurt I and Kilic S. 2014. [Tularemia is spreading from north to south side of Turkey: a small outbreak in Kahramanmaras, Turkey]. Mikrobiyol. Bul. 48:413-419. https://doi.org/10.5578/mb.7789
  4. Fahey JW, Zhang Y, Talalay P. 1997. Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc. Natl. Acad. Sci. U. S. A. 94:10367-10372. https://doi.org/10.1073/pnas.94.19.10367
  5. Gonzalez F, Quintero J, Del Rio R, Mahn A. 2021. Optimization of an extraction process to obtain a food-grade sulforaphane-rich extract from broccoli (Brassica oleracea var. italica). Molecules 26:4042.
  6. Heber D, Li Z, Garcia-Lloret M, Wong AM, Lee TY, Thames G, Krak M, Zhang Y, Nel A. 2014. Sulforaphane-rich broccoli sprout extract attenuates nasal allergic response to diesel exhaust particles. Food Funct. 5:35-41. https://doi.org/10.1039/C3FO60277J
  7. Huo L, Su Y, Xu G, Zhai L, Zhao J. 2019. Sulforaphane protects the male reproductive system of mice from obesity-induced damage: involvement of oxidative stress and autophagy. Int. J. Environ. Res. Public Health 16:3759.
  8. Hwang JS, Kim KH, Park J, Kim SM, Cho H, Lee Y, Han IO. 2019. Glucosamine improves survival in a mouse model of sepsis and attenuates sepsis-induced lung injury and inflammation. J. Biol. Chem. 294:608-622. https://doi.org/10.1074/jbc.RA118.004638
  9. Jayakumar T, Lin KC, Chang CC, Hsia CW, Manubolu M, Huang WC, Sheu JR, Hsia CH. 2021. Targeting MAPK/NF-κB pathways in anti-inflammatory potential of rutaecarpine: impact on Src/FAK-mediated macrophage migration. Int. J. Mol. Sci. 23:92.
  10. 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
  11. Jhun H, Lee WY, Park JK, Hwang SG, Park HJ. 2022. Transcriptomic analysis of testicular gene expression in a dog model of experimentally induced cryptorchidism. Cells 11:2476.
  12. Lafarga T, Bobo G, Vinas I, Collazo C, Aguilo-Aguayo I. 2018. Effects of thermal and non-thermal processing of cruciferous vegetables on glucosinolates and its derived forms. J. Food Sci. Technol. 55:1973-1981. https://doi.org/10.1007/s13197-018-3153-7
  13. Li LS, Chiroma SM, Hashim T, Adam SK, Mohd Moklas MA, Yusuf Z, Rahman SA. 2020. Antioxidant and anti-inflammatory properties of Erythroxylum cuneatum alkaloid leaf extract. Heliyon 6:e04141.
  14. Lippman M. 1989. Growth regulation of breast cancer. Prog. Clin. Biol. Res. 320:111-119.
  15. Menghini L, Ferrante C, Leporini L, Recinella L, Chiavaroli A, Leone S, Pintore G, Vacca M, Orlando G, Brunetti L. 2016. An hydroalcoholic chamomile extract modulates inflammatory and immune response in HT29 cells and isolated rat colon. Phytother. Res. 30:1513-1518. https://doi.org/10.1002/ptr.5655
  16. Nandini DB, Rao RS, Deepak BS, Reddy PB. 2020. Sulforaphane in broccoli: the green chemoprevention!! Role in cancer prevention and therapy. J. Oral Maxillofac. Pathol. 24:405.
  17. Piao CS, Gao S, Lee GH, Kim DS, Park BH, Chae SW, Chae HJ, Kim SH. 2010. Sulforaphane protects ischemic injury of hearts through antioxidant pathway and mitochondrial K(ATP) channels. Pharmacol. Res. 61:342-348. https://doi.org/10.1016/j.phrs.2009.11.009
  18. Prasad S, Tyagi AK, Aggarwal BB. 2016. Detection of inflammatory biomarkers in saliva and urine: potential in diagnosis, prevention, and treatment for chronic diseases. Exp. Biol. Med. (Maywood) 241:783-799. https://doi.org/10.1177/1535370216638770
  19. Qi T, Xu F, Yan X, Li S, Li H. 2016. Sulforaphane exerts antiinflammatory effects against lipopolysaccharide-induced acute lung injury in mice through the Nrf2/ARE pathway. Int. J. Mol. Med. 37:182-188. https://doi.org/10.3892/ijmm.2015.2396
  20. Raeeszadeh M, Shokrollahi B, Khademi N, Akbari A. 2022. Superior effect of broccoli methanolic extract on control of oxidative damage of sperm cryopreservation and reproductive performance in rats: a comparison with vitamin C and E antioxidant. Theriogenology 181:50-58. https://doi.org/10.1016/j.theriogenology.2022.01.010
  21. Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, Hauschildt S. 2011. LPS-induced cytokine production in human monocytes and macrophages. Crit. Rev. Immunol. 31:379-446. https://doi.org/10.1615/CritRevImmunol.v31.i5.20
  22. Rychlik J, Olejnik A, Olkowicz M, Kowalska K, Juzwa W, Myszka K, Dembczynski R, Moyer MP, Grajek W. 2015. Antioxidant capacity of broccoli sprouts subjected to gastrointestinal digestion. J. Sci. Food Agric. 95:1892-1902. https://doi.org/10.1002/jsfa.6895
  23. Saw CL, Huang MT, Liu Y, Khor TO, Conney AH, Kong AN. 2011. Impact of Nrf2 on UVB-induced skin inflammation/ photoprotection and photoprotective effect of sulforaphane. Mol. Carcinog. 50:479-486. https://doi.org/10.1002/mc.20725
  24. Seibert K and Masferrer JL. 1994. Role of inducible cyclooxygenase (COX-2) in inflammation. Receptor 4:17-23.
  25. Sherwood ER and Toliver-Kinsky T. 2004. Mechanisms of the inflammatory response. Best Pract. Res. Clin. Anaesthesiol. 18:385-405. https://doi.org/10.1016/j.bpa.2003.12.002
  26. Song X, Wang T, Zhang Z, Jiang H, Wang W, Cao Y, Zhang N. 2015. Leonurine exerts anti-inflammatory effect by regulating inflammatory signaling pathways and cytokines in LPS-induced mouse mastitis. Inflammation 38:79-88. https://doi.org/10.1007/s10753-014-0009-9
  27. Turner MD, Nedjai B, Hurst T, Pennington DJ. 2014. Cytokines and chemokines: at the crossroads of cell signalling and inflammatory disease. Biochim. Biophys. Acta 1843:2563-2582. https://doi.org/10.1016/j.bbamcr.2014.05.014
  28. Wang J, Cai X, Ma R, Lei D, Pan X, Wang F. 2021. Anti-inflammatory effects of sweroside on LPS-induced ALI in mice via activating SIRT1. Inflammation 44:1961-1968. https://doi.org/10.1007/s10753-021-01473-4
  29. Wang Y, Zhou X, Zhao D, Wang X, Gurley EC, Liu R, Li X, Hylemon PB, Chen W, Zhou H. 2020. Berberine inhibits free fatty acid and LPS-induced inflammation via modulating ER stress response in macrophages and hepatocytes. PLoS One 15:e0232630.
  30. Yang SH, Long M, Yu LH, Li L, Li P, Zhang Y, Guo Y, Gao F, Liu MD, He JB. 2016. Sulforaphane prevents testicular damage in Kunming mice exposed to cadmium via activation of Nrf2/ARE signaling pathways. Int. J. Mol. Sci. 17:1703.