Journal of Marine Bioscience and Biotechnology (한국해양바이오학회지)

The Korean Society for Marine Biotechnology (한국해양바이오학회)
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Inhibitory effect of luthione on tacrolimus-induced DNA damage, apoptosis and inflammatory response in olive flounder natural embryo cells

넙치 배아세포에서 tacrolimus에 의한 DNA 손상, 세포사멸 및 염증성 반응에 대한 luthione의 억제 효과

  • Park, Sang Eun (Department of Korean internal medicine, College of Korean Medicine, Dong-eui University) ;
  • Choi, Yung Hyun (Department of Biochemistry, College of Korean Medicine, Dong-eui University)
  • 박상은 (동의대학교 한의과대학 간계내과학교실) ;
  • 최영현 (동의대학교 한의과대학 생화학교실)
  • Received : 2022.03.30
  • Accepted : 2022.05.06
  • Published : 2022.06.30
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Abstract

Tacrolimus, a type of macrolide produced by Streptomyces tsukubaensis, is widely used as an immunosuppressant. However, continuous exposure to tacrolimus causes oxidative stress in normal cells, ultimately inducing cell injury. Therefore, this study investigated whether luthione, a reduced glutathione, could inhibit tacrolimus-induced cytotoxicity in olive flounder (hirame) natural embryo (HINAE) cells. According to the results, luthione significantly inhibited tacrolimus-induced reduction in cell viability in a concentration-dependent manner. Additinally, although luthione unaffected autophagy by tacrolimus, tacrolimus-induced apoptosis was significantly suppressed in the presence of luthione. Luthione also markedly blocked DNA damage in tacrolimus-treated HINAE cells, associated with the inhibition of reactive oxygen species (ROS) generation. Additionally, tacrolimus cytotoxicity in HINAE cells was correlated with increased inflammatory response, also attenuated by luthione. Collectively, these results show that at least luthione protects HINAE cells against tacrolimus-induced DNA damage, apoptosis, and inflammation, but not autophagy, by scavenging ROS. Although additional in-vivo studies are required, this study's results can be used as a basis for utilizing luthione to reduce the toxicity of fish cells caused by excessive immune responses.

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References

  1. Diaz Vivancos, P., Wolff, T., Markovic, J., Pallardo, F. V. and Foyer, C. H. 2010. A nuclear glutathione cycle within the cell cycle. Biochem. J. 431, 169-178. https://doi.org/10.1042/BJ20100409
  2. Pastore, A., Federici, G., Bertini, E. and Piemonte, F. 2003. Analysis of glutathione: Implication in redox and detoxification. Clin. Chim. Acta 333, 19-39. https://doi.org/10.1016/S0009-8981(03)00200-6
  3. Monostori, P., Wittmann, G., Karg, E. and Tri, S. 2009. Determination of glutathione and glutathione disulfide in biological samples: An in-depth review. J. Chromatogr. B 877, 3331-3346. https://doi.org/10.1016/j.jchromb.2009.06.016
  4. Perricone, C., De Carolis, C. and Perricone, R. 2009. Glutathione: A key player in autoimmunity. Autoimmun. Rev. 8, 697-701. https://doi.org/10.1016/j.autrev.2009.02.020
  5. Kerksick, C. and Willoughby, D. 2005. The antioxidant role of glutathione and N-acetyl-cysteine supplements and exercise-induced oxidative stress. J. Int. Soc. Sports Nutr. 2, 38-44. https://doi.org/10.1186/1550-2783-2-2-38
  6. Filomeni, G., Rotilio, G. and Ciriolo, M. R. 2005. Disulfide relays and phosphorylative cascades: Partners in redoxmediated signaling pathways. Cell Death Dier. 12, 1555-1563. https://doi.org/10.1038/sj.cdd.4401754
  7. Lei, C. X., Xie, Y. J., Li, S. J., Jiang, P., Du, J. X. and Tian, J. J. 2002. Fabp4 contributes toward regulating inflammatory gene expression and oxidative stress in Ctenopharyngodon idella. Comp. Biochem. Physiol. B Bioche m. Mol. Biol. 259, 110715.
  8. Li, D., Li, Z., Zhang, T., Peng, B., Zhang, Y., Sun, H. and Wang, S. 2021. 2-amino-3-methylimidazo[4,5-f]quinoline triggering liver damage by inhibiting autophagy and inducing endoplasmic reticulum stress in zebrafish (Danio rerio). Toxins (Basel) 13, 826. https://doi.org/10.3390/toxins13110826
  9. Han, J., Dong, J., Zhang, R., Zhang, X., Chen, M., Fan, X., Li, M., Li, J., Zhu, J., Shang, J. and Yue, Y. 2021. Dendrobium catenatum Lindl. water extracts attenuate atherosclerosis. Mediators Inflamm. 2021, 9951946.
  10. Wang, Y., Zhao, H., Liu, Y., Nie, X. and Xing, M. 2020. Zinc exerts its renal protection effect on arsenic-exposed common carp: A signaling network comprising Nrf2, NF-κB and MAPK pathways. Fish Shellfish Immunol. 104, 383-390. https://doi.org/10.1016/j.fsi.2020.06.031
  11. Liu, J., Pan, M., Liu, Y., Huang, D., Luo, K., Wu, Z., Zhang, W. and Mai, K. 2022. Taurine alleviates endoplasmic reticulum stress, inflammatory cytokine expression and mitochondrial oxidative stress induced by high glucose in the muscle cells of olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 123, 358-368. https://doi.org/10.1016/j.fsi.2022.03.021
  12. Klintmalm, G. B. 1994. FK 506: An update. Clin. Transplant. 8, 207-210.
  13. Wallemacq, P. E. and Reding, R. 1993. FK506 (tacrolimus), a novel immunosuppressant in organ transplantation: Clinical, biomedical, and analytical aspects. Clin. Chem. 39, 2219-2228. https://doi.org/10.1093/clinchem/39.11.2219
  14. Kitamura, N. and Kaminuma, O. 2021. Isoform-selective NFAT inhibitor: Potential usefulness and development. Int. J. Mol. Sci. 22, 2725. https://doi.org/10.3390/ijms22052725
  15. Bonner, J. M. and Boulianne, G. L. 2017. Diverse structures, functions and uses of FK506 binding proteins. Cell. Signal. 38, 97-105. https://doi.org/10.1016/j.cellsig.2017.06.013
  16. Wimmer, C. D., Angele, M. K., Schwarz, B., Pratschke, S., Rentsch, A. M., Khandoga, Guba, M., Jauch, K. W., Bruns, C. and Graeb, C. 2013. Impact of cyclosporine versus tacrolimus on the incidence of de novo malignancy following liver transplantation: A single center experience with 609 patients. Transpl. Int. 26, 999-1006. https://doi.org/10.1111/tri.12165
  17. Sommerer, C. and Giese, T. 2016. Nuclear factor of activated T cells-regulated gene expression as predictive biomarker of personal response to calcineurin inhibitors. Ther. Drug Monit. 38, S50-56. https://doi.org/10.1097/FTD.0000000000000234
  18. Noble, J., Terrec, F., Malvezzi, P. and Rostaing, L. 2021. Adverse effects of immunosuppression after liver transplantation. Best Pract. Res. Clin. Gastroenterol. 54-55, 101762. https://doi.org/10.1016/j.bpg.2021.101762
  19. Amorese, G., Lombardo, C., Tudisco, A., Iacopi, S., Men onna, F., Marchetti, P., Vistoli, F. and Boggi, U. 2020. Induction and immunosuppressive management of pancreas transplant recipients. Curr. Pharm. Des. 26, 3425-3439. https://doi.org/10.2174/1381612826666200430111620
  20. Hissong, E., Mostyka, M. and Yantiss, R. K. 2022. Histologic features of tacrolimus-induced colonic injury. Am. J. Surg. Pathol. 46, 118-123. https://doi.org/10.1097/PAS.0000000000001761
  21. Kim, H. S., Lim, S. W., Jin, L., Jin, J., Chung, B. H. and Yang, C. W. 2017. The protective effect of febuxostat on chronic tacrolimus-induced nephrotoxicity in rats. Nephron 135, 61-71. https://doi.org/10.1159/000449289
  22. Park, C., Kwon, D. H., Hwang, S. J., Han, M. H., Jeong, J. W., Hong, S. H., Cha, H. J., Hong, S. H., Kim, G. Y., Lee, H. J., Kim, S., Kim, H. S. and Choi, Y. H. 2019. Protective effects of nargenicin A1 against tacrolimus-induced oxidative stress in hirame natural embryo cells. Int. J. Environ. Res. Public Health 16, 1044. https://doi.org/10.3390/ijerph16061044
  23. Liu, G., Fan, G., Guo, G., Kang, W., Wang, D., Xu, B. and Zhao, J. 2017. FK506 attenuates the inflammation in rat spinal cord injury by inhibiting the activation of NF-κB in microglia cells. Cell. Mol. Neurobiol. 37, 843-855. https://doi.org/10.1007/s10571-016-0422-8
  24. Yu, Y., Zhong, J., Peng, L., Wang, B., Li, S., Huang, H., Deng, Y., Zhang, H., Yang, R., Wang, C. and Yuan, J. 2017. Tacrolimus downregulates inflammation by regulating pro-/anti-inflammatory responses in LPS-induced keratitis. Mol. Med. Rep. 16, 5855-5862. https://doi.org/10.3892/mmr.2017.7353
  25. Wang, L., Chang, J. H., Paik, S. Y., Tang, Y., Eisner, W. and Spurney, R. F. 2011. Calcineurin (CN) activation promotes apoptosis of glomerular podocytes both in vitro and in vivo. Mol. Endocrinol. 25, 1376-1386. https://doi.org/10.1210/me.2011-0029
  26. Gurkan, A., Afacan, B., Emingil, G., Toz, H., Baskesen, A. and Atilla, G. 2008. Gingival crevicular fluid transforming growth factor-β1 in cyclosporine and tacrolimus treated renal transplant patients without gingival overgrowth. Arch. Oral Biol. 53, 723-728. https://doi.org/10.1016/j.archoralbio.2008.02.003
  27. Lim, S. W., Jin, L., Luo, K., Jin, J. and Yang, C. W. 2017. Ginseng extract reduces tacrolimus-induced oxidative stress by modulating autophagy in pancreatic β cells. Lab. Investig. 97, 1271-1281. https://doi.org/10.1038/labinvest.2017.75
  28. Jeon, S. H., Park, H. M., Kim, S. J., Lee, M. Y., Kim, G. B., Rahman, M. M., Woo, J. N., Kim, I. S., Kim, J. S. and Kang, H. S. 2010. Taurine reduces FK506-induced generation of ROS and activation of JNK and Bax in Madin Darby canine kidney cells. Hum. Exp. Toxicol. 2010, 29, 627-633. https://doi.org/10.1177/0960327109359019
  29. Kwon, D. H., Cha, H. J., Lee, H., Hong, S. H., Park, C., Park, S. H., Kim, G. Y., Kim, S., Kim, H. S., Hwang, H. J. and Choi, Y. H. 2019. Protective effect of glutathione against oxidative stress-induced cytotoxicity in RAW 264.7 macrophages through activating the nuclear factor erythroid 2-related factor-2/heme oxygenase-1 pathway. Antioxidants (Basel) 8, 82. https://doi.org/10.3390/antiox8040082
  30. Ding, J., Jin, J., Lei, Y.N., Cui, S., Li, H. Y., Zheng, H. L., Piao, S. G., Jiang, Y. J., Xuan, M. Y., Jin, J. Z., Jin, Y. S., Lee, J. P., Chung B. H., Choi, B. S., Yang, C. W. and Li, C. 2022. Exogenous pancreatic kininogenase protects against tacrolimus-induced renal injury by inhibiting PI3K/AKT signaling: The role of bradykinin receptors. Int. Immunopharmacol. 105, 108547. https://doi.org/10.1016/j.intimp.2022.108547
  31. Jiang, Y. J., Cui, S., Luo, K., Ding, J., Nan, Q. Y., Piao, S. G., Xuan, M. Y., Zheng, H. L., Jin, Y. J., Jin, J. Z., Lee, J. P., Chung, B. H., Choi, B. S., Yang, C. W. and Li, C. 2021. Nicotine exacerbates tacrolimus-induce d renal injury by programmed cell death. Korean J. Inter n. Med. 36, 1437-1449. https://doi.org/10.3904/kjim.2021.326
  32. Xu, X. S., Shao, N., Duan, X. T., Zhang, X. and Zhang, Y. F. 2018. Tacrolimus alleviates Ox-LDL damage through inducing vascular endothelial autophagy. Eur. Rev. Med. Pharmacol. Sci. 22, 3199-3206.
  33. Babaeenezhad, E., Hadipour Moradi, F., Rahimi Monfared, S., Fattahi, M. D., Nasri, M., Amini, A., Dezfoulian, O. and Ahmadvand, H. 2021. D-limonene alleviates acute kidney injury following gentamicin administration in rats: Role of NF-κB pathway, mitochondrial apoptosis, oxidative stress, and PCNA. Oxid. Med. Cell. Longev. 2021, 6670007.
  34. Ren, J., Li, S., Wang, C., Hao, Y., Liu, Z., Ma, Y., Liu, G. and Dai, Y. 2021. Glutathione protects against the meiotic defects of ovine oocytes induced by arsenic exposure via the inhibition of mitochondrial dysfunctions. Ecotoxicol. Environ. Saf. 230, 113135.
  35. Jie, J., Li, W., Wang, G. and Xu, X. 2021. FK506 ameliorates osteoporosis caused by osteoblast apoptosis via suppressing the activated CaN/NFAT pathway during oxidative stress. Inflamm. Res. 70, 789-797. https://doi.org/10.1007/s00011-021-01452-3
  36. Kowalczyk, P., Sulejczak, D., Kleczkowska, P., Bukowska-Osko, I., Kucia, M., Popiel, M., Wietrak, E., Kramkowski, K., Wrzosek, K. and Kaczynska, K. 2021. Mitochondrial oxidative stress-A causative factor and therapeutic target in many diseases. Int. J. Mol. Sci. 22, 13384. https://doi.org/10.3390/ijms222413384
  37. Shi, T. and Dansen, T. B. 2020. Reactive oxygen species induced p53 activation: DNA damage, redox signaling, or both? Antioxid. Redox Signal. 33, 839-859. https://doi.org/10.1089/ars.2020.8074
  38. Ferjani, H., Timoumi, R., Amara, I., Abid, S., Achour, A., Bacha, H. and Boussema-Ayed, I. 2017. Beneficial effects of mycophenolate mofetil on cardiotoxicity induced by tacrolimus in wistar rats. Exp. Biol. Med. (Maywood) 242, 448-455. https://doi.org/10.1177/1535370215616709
  39. Cordelli, E., Bignami, M. and Pacchierotti, F. 2021. Comet assay: a versatile but complex tool in genotoxicity testing. Toxicol. Res. (Camb) 10, 68-78. https://doi.org/10.1093/toxres/tfaa093
  40. Liu, Z., Ren, Z., Zhang, J., Chuang, C. C., Kandaswamy, E., Zhou, T. and Zuo, L. 2018. Role of ROS and nutritional antioxidants in human diseases. Front. Physiol. 9, 477. https://doi.org/10.3389/fphys.2018.00477
  41. Aksentijevich, M., Lateef, S. S., Anzenberg, P., Dey, A. K. and Mehta, N. N. 2020. Chronic inflammation, cardiometabolic diseases and effects of treatment: psoriasis as a human model. Trends Cardiovasc. Med. 30, 472-478. https://doi.org/10.1016/j.tcm.2019.11.001
  42. Picca, A., Calvani, R., Coelho-Junior, H. J. and Marzetti, E. 2021. Cell death and inflammation: The role of mitochondria in health and disease. Cells 10, 537. https://doi.org/10.3390/cells10030537
  43. Mailey, B., O'Shea, G., Romanelli, M. and West, B. 2021. Systemic imunosuppression for prevention of recurrent tendon adhesions. Plast. Reconstr. Surg. Glob. Open 9, e3834. https://doi.org/10.1097/GOX.0000000000003834
  44. Meyer, N., Brodowski, L., von Kaisenberg, C., SchroderHeurich, B. and von Versen-Hoynck, F. 2021. Cyclosporine A and tacrolimus induce functional impairment and inflammatory reactions in endothelial progenitor cells. Int. J. Mol. Sci. 22, 9696. https://doi.org/10.3390/ijms22189696
  45. Wang, F., Wei, F., Liu, H., Wang, X., Wang, W., Ouyang, Y., Liu, J., Chen, D. and Zang, Y. 2021. Association of the IL-6 Rs1800796 SNP with concentration/dose ratios of tacrolimus and donor liver function after transplantation. Immunol. Invest. 50, 939-948. https://doi.org/10.1080/08820139.2020.1793775
  46. Ibrahim, S. A., Eltahawy, N. F., Abdalla, A. M. and Khalaf, H. M. 2021. Protective effects of selenium in tacrolimus-induced lung toxicity: potential role of hemeoxygenase 1. Can. J. Physiol. Pharmacol. 99, 1069-1078. https://doi.org/10.1139/cjpp-2020-0547
  47. Soufli, I., Toumi, R., Rafa, H. and Touil-Boukoffa, C. 2016. Overview of cytokines and nitric oxide involvement in immuno-pathogenesis of inflammatory bowel diseases. World J. Gastrointest. Pharmacol. Ther. 7, 353-360. https://doi.org/10.4292/wjgpt.v7.i3.353
  48. Aleem, D. and Tohid, H. 2018 Pro-inflammatory cytokines, biomarkers, genetics and the immune system: a mechanistic approach of depression and psoriasis. Rev. Colomb. Psiquiatr. 47, 177-186. https://doi.org/10.1016/j.rcp.2017.03.002