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Effects of immune-challenged domestic silkworm hemolymph on the regulation of SIRT5 and PRDx1 expression

  • Jin Ha Yun (Department of Biomedical Science, Daegu Catholic University) ;
  • Seong Ryul Kim (Sericultural and Apicultural Materials Division, National Academy of Agricultural Science, RDA) ;
  • Seung-Won Park (Department of Biomedical Science, Daegu Catholic University)
  • Received : 2023.10.31
  • Accepted : 2023.12.04
  • Published : 2023.12.31

Abstract

SIRT5 and PRDx1 play crucial roles in cancer and are involved in the basic mechanisms of reactive oxygen species detoxification. In our previous studies, we showed that hemolymph extracts of immune-challenged Bombyx mori have antioxidant properties. Following H2O2 stimulation, immune-challenged B. mori hemolymph extracts elicited SIRT5 downregulation activity, reaching effective activity at the highest concentration of 100 ppm. Additionally, cells treated with immune-challenged B. mori hemolymph extracts demonstrated increased PRDx1 mRNA expression compared to that of PBS-treated cells. Therefore, immune-challenged B. mori hemolymph extracts offer a potential auxiliary means of treating drug-resistant tumors through downregulation of SIRT5 and upregulation of PRDx1 expression. Nevertheless, further studies on the effects of B. mori hemolymph on SIRT5 and PRDx1 regulation are pertinent for using it as a food or pharmaceutical material and understanding its therapeutic effect on tumors, including those that are drug-resistant.

Keywords

Acknowledgement

I express sincerely my former research assistants from the Department of Biomedical Science, at the Daegu Catholic University and gratitude to the participants who were involved in the study. This work was supported by the National Research Foundation of Korea (NRF) grant founded by the Korea Government (MSIT) (No. 2021R1F1A1062456).

References

  1. Balakrishnan D, Kandasamy D, Nithyanand P (2014) A review on antioxidant activity of marine organisms. Int J ChemTech Res 6, 3431-3436.
  2. Baynes JW (1991) Role of oxidative stress in development of complications in diabetes. Diabetes 40, 405-412. https://doi.org/10.2337/diab.40.4.405
  3. Chang L, Xi L, Liu Y, Liu R, Wu Z, Jian Z (2018) SIRT5 promotes cell proliferation and invasion in hepatocellular carcinoma by targeting E2F1. Mol Med Rep 17, 342-349. https://doi.org/10.3892/mmr.2017.7875
  4. Chen X, Wang KW, Chen YQ (2019) Cisplatin induces apoptosis of A549 cells by downregulating peroxidase V. Eur Rev Med Pharmacol Sci 23, 3718-3718. https://doi.org/10.26355/eurrev_201905_17795
  5. Ding C, Fan X, Wu G (2017) Peroxiredoxin 1 - an antioxidant enzyme in cancer. J Cell Mol Med 21, 193-202. https://doi.org/10.1111/jcmm.12955
  6. Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29, 187-197. https://doi.org/10.1002/arch.940290208
  7. Goncalves K, Sullivan K, Phelan S (2012) Differential expression and function of peroxiredoxin 1 and peroxiredoxin 6 in cancerous MCF-7 and noncancerous MCF-10A breast epithelial cells. Cancer Investing 30, 38-47. https://doi.org/10.3109/07357907.2011.629382
  8. Kalinina EV, Berezov TT, Shtil' AA, Chernov NN, Glazunova VA, Novichkova MD et al. (2012) Expression of peroxiredoxin 1, 2, 3, and 6 genes in cancer cells during drug resistance formation. Bull Exp Biol Med 153, 878-881. https://doi.org/10.1007/s10517-012-1849-7
  9. Kim SR, Hong SJ, Choi K, Kim SW, Jeong ST, Park SW (2020) Antibacterial and anti-inflammatory activities of the immune-challenged silkworm (Bombyx mori) hemolymph with Lactobacillus cell wall extracts. Entomol Res 49, 354-362. http://dx.doi.org/10.1111/1748-5967.12369
  10. Kim SR, Park SW (2021) Papiliocin, an antimicrobial peptide, rescues hyperoxia-induced intestinal injury. Int J Indust Entomol 43, 86-90. http://dx.doi.org/10.7852/ijie.2021.43.2.94
  11. Li F, He X, Ye D, Lin Y, Yu H, Yao C, et al. (2015) NADP+-IDH mutations promote hypersuccinylation that impairs mitochondria respiration and induces apoptosis resistance. Mol Cell 60, 661-675. http://dx.doi.org/10.1016/j.molcel.2015.10.017
  12. Liang F, Wang X, Ow SH, Chen W, Ong WC (2017) Sirtuin 5 is anti-apoptotic and anti-oxidative in cultured SH-EP neuroblastoma cells. Neurotox Res 31, 63-76. https://doi.org/10.1007/s12640-016-9664-y
  13. Liu B, Che W, Zheng C, Liu W, Wen J, Fu H, et al. (2013) SIRT5: a safeguard against oxidative stress-induced apoptosis in cardiomyocytes. Cell Physiol Biochem 32, 1050-1059. https://doi.org/10.1159/000354505
  14. Liu Y, Li Q, Zhou L, Xie N, Nice EC, Zhang H, et al. (2016) Cancer drug resistance: redox resetting renders a way. Oncotarget 7, 42740-42761. https://doi.org/10.18632/oncotarget.8600
  15. Lu W, Zuo Y, Feng Y, Zhang M (2014) SIRT5 facilitates cancer cell growth and drug resistance in non-small cell lung cancer. Tumor Biol 35, 10699-10705. https://doi.org/10.1007/s13277-014-2372-4
  16. Luo H, Yang A, Schulte BA, Wargovich MJ, Wang GY (2013) Resveratrol induces premature senescence in lung cancer cells via ROS-mediated DNA damage. PLoS ONE 8, e60065. https://doi.org/10.1371/journal.pone.0060065
  17. Lv XB, Liu L, Cheng C, Yu B, Xiong L, Hu K, et al. (2015) SUN2 exerts tumor suppressor functions by suppressing the Warburg effect in lung cancer. Sci Rep 5, 1-12. https://doi.org/10.1038/srep17940
  18. Marullo R, Werner E, Degtyareva N, Moore B, Altavilla G, Ramalingam SS, et al. (2013) Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PLoS ONE 8, e81162. https://doi.org/10.1371/journal.pone.0081162
  19. McDonald C, Muhlbauer J, Perlmutter G, Taparra K, Phelan SA (2014) Peroxiredoxin proteins protect MCF-7 breast cancer cells from doxorubicin-induced toxicity. Int J Oncol 45, 219-226. https://doi.org/10.3892/ijo.2014.2398
  20. Nakagawa T, Lomb DJ, Haigis MC, Guarente L (2009) SIRT5 Deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 137, 560-570. https://doi.org/10.1016/j.cell.2009.02.026
  21. Oghenesuvwe EE, Paul C (2019) Edible insects bio-actives as antioxidants: Current status and perspectives. J Complement Med Res 10, 89-102. https://dx.doi.org/10.5455/jcmr.20190130100319
  22. Park SW (2022) A preliminary study of the anti-inflammatory activities of the Japanese oak silk moth, Antheraea yamamai. Int J Indust Entomol 45, 17-21. https://doi.org/10.7852/ijie.2022.45.1.17
  23. Pardini RS (1995) Toxicity of oxygen from naturally occurring redox-active pro-oxidants. Arch Insect Biochem Physiol 29, 101-118. https://doi.org/10.1002/arch.940290203
  24. Polletta L, Vernucci E, Carnevale I, Arcangeli T, Rotili D, Palmerio S, et al. (2015) SIRT5 regulation of ammonia-induced autophagy and mitophagy. Autophagy 11, 253-270. https://doi.org/10.1080/15548627.2015.1009778
  25. Ren P, Ye H, Dai L, Liu M, Liu X, Chai Y, et al. (2013) Peroxiredoxin 1 is a tumor-associated antigen in esophageal squamous cell carcinoma. Oncol Rep 30, 2297-2303. https://doi.org/10.3892/or.2013.2714
  26. Shi L, Yan H, An S, Shen M, Jia W, Zhang R, et al. (2019) SIRT5-mediated deacetylation of LDHB promotes autophagy and tumorigenesis in colorectal cancer. Mol Oncol 13, 358-375. https://doi.org/10.1002/1878-0261.12408
  27. Singh CK, Chhabra G, Ndiaye MA, Garcia-Peterson LM, Mack NJ, Ahmad N (2018) The Role of Sirtuins in antioxidant and redox signaling. Antoxid Redox Signal 28, 643-661. https://doi.org/10.1089/ars.2017.7290
  28. Sosa V, Moline T, Somoza R, Paciucci R, Kondoh H, LLeonart ME (2013) Oxidative stress and cancer: an overview. Ageing Res Rev 12, 376-390. http://dx.doi.org/10.1016/j.arr.2012.10.004
  29. Srinivas US, Tan BWQ, Vellayappan BA, Jeyasekharan AD (2019) ROS and the DNA damage response in cancer. Redox Biol 21, 101084. https://doi.org/10.1016/j.redox.2018.101084
  30. Sun JY, Xu L, Tseng H, Ciccarelli B, Fulciniti M, Hunter ZR, et al. (2011) Histone deacetylase inhibitors demonstrate significant preclinical activity as single agents, and in combination with bortezomib in Waldenstrom's macroglobulinemia. Clin Lymphoma Myeloma Leuk 11, 152-156. https://doi.org/10.3816/CLML.2011.n.036
  31. Sun X, Wang S, Gai J, Guan J, Li J, Li Y, et al. (2019) SIRT5 promotes cisplatin resistance in ovarian cancer by suppressing DNA damage in a ROS-dependent manner via regulation of the Nrf2/HO-1 pathway. Front Oncol 9, 754. https://doi.org/10.3389/fonc.2019.00754
  32. Turner-Ivey B, Manevich Y, Schulte J, Kistner-Griffin E, Jezierska-Drutel A, Liu Y, et al. (2013) Role for Prdx1 as a specific sensor in redox-regulated senescence in breast cancer. Oncogene 32, 5302-5314. https://doi.org/10.1038/onc.2012.624
  33. Wang Y, Liu Q, Huan Y, Li R, Li C, Sun S, et al. (2018a) Sirtuin 5 overexpression attenuates glucolipotoxicity-induced pancreatic β cells apoptosis and dysfunction. Exp Cell Res 371, 205-213. https://doi.org/10.1016/j.yexcr.2018.08.011
  34. Wang YQ, Wang HL, Xu J, Tan J, Fu LN, Wang JL, et al. (2018b) Sirtuin5 contributes to colorectal carcinogenesis by enhancing glutaminolysis in a deglutarylation-dependent manner. Nat Commun 9, 1-15. https://doi.org/10.1038/s41467-018-02951-4
  35. Zhang Y, Yang F, Jamali MA, Peng Z (2016) Antioxidant enzyme activities and lipid oxidation in Rape (Brassica campestris L.) Bee pollen added to salami during processing. Molecules 21, 1439. https://doi.org/10.3390/molecules21111439
  36. Zielinska E, Karas M, Jakubczyk A (2017) Antioxidant activity of predigested protein obtained from a range of farmed edible insects. Int J Food Sci Tech 52, 306-312. https://doi.org/10.1111/ijfs.13282