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Antibacterial and Antioxidant Activity of Spermidine, a Natural Polyamine, on Fish Pathogenic Bacteria and C2C12 Myoblast Cells

어류병원성 세균 및 C2C12 근원세포에 대한 polyamine 계열 물질인 spermidine의 항균 및 항산화 활성

  • Hwang-Bo, Hyun (Department of Biochemistry, Dong-eui University College of Korean Medicine, Dong-eui University) ;
  • Choi, Eun-Ok (Department of Biochemistry, Dong-eui University College of Korean Medicine, Dong-eui University) ;
  • Kim, Min Young (Department of Biochemistry, Dong-eui University College of Korean Medicine, Dong-eui University) ;
  • Ji, Seon Yeong (Department of Biochemistry, Dong-eui University College of Korean Medicine, Dong-eui University) ;
  • Hong, Su Hyun (Department of Biochemistry, Dong-eui University College of Korean Medicine, Dong-eui University) ;
  • Park, Cheol (Department of Molecular Biology, College of Natural Sciences, Dong-eui University) ;
  • Cha, Hee-Jae (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Kim, Suhkmann (Department of Chemistry, Pusan National University) ;
  • Kim, Heui-Soo (Department of Biological Sciences, Pusan National University) ;
  • Hwang, Hye-Jin (Department of Food and Nutrition, College of Nursing, Healthcare Sciences & Human Ecology, Dong-eui University) ;
  • Choi, Yung Hyun (Department of Biochemistry, Dong-eui University College of Korean Medicine, Dong-eui University)
  • 황보현 (동의대학교 한의과대학 생화학교실 및 항노화연구소) ;
  • 최은옥 (동의대학교 한의과대학 생화학교실 및 항노화연구소) ;
  • 김민영 (동의대학교 한의과대학 생화학교실 및 항노화연구소) ;
  • 지선영 (동의대학교 한의과대학 생화학교실 및 항노화연구소) ;
  • 홍수현 (동의대학교 한의과대학 생화학교실 및 항노화연구소) ;
  • 박철 (동의대학교 자연과학대학 분자생물학과) ;
  • 차희재 (고신대학교 의과대학 기생충학 및 유전학교실) ;
  • 김석만 (부산대학교 자연과학대학 화학과) ;
  • 김희수 (부산대학교 자연과학대학 생명과학과) ;
  • 황혜진 (동의대학교 의료보건생활대학 식품영양학과) ;
  • 최영현 (동의대학교 한의과대학 생화학교실 및 항노화연구소)
  • Received : 2019.11.19
  • Accepted : 2019.11.25
  • Published : 2019.12.31

Abstract

We compared the antibacterial activities of spermidine and astaxanthin against two gram-positive bacteria such as Streptococcus parauberis and S. iniae to find new antibacterial candidates. We also evaluated the preventive effects of spermidine against oxidative stress-induced cytotoxicity in C2C12 myoblasts. Our results indicated that spermidine has more significant antibacterial activities than astaxanthin against both two fish pathogenic bacteria as well as gram-negative bacteria Escherichia coli used as a control group. Minimum inhibitory concentration and minimum bactericidal concentration of spermidine were 0.25 mM and 1 mM against S. parauberis, 1 mM and 3 mM against S. iniae, and 0.5 mM and 1.5 mM against E. coli, respectively. In addition, the postantibiotic effect lasted from 7 h, 5 h and 6 h for S. parauberis, S. iniae and E. coli, respectively. The results also showed that the decreased C2C12 cell viability by H2O2 could be attributed to the induction of DNA damage and apoptosis accompanied by the increased production of reactive oxygen species, which was remarkably protected by spermidine. Additionally, the antioxidant effect of spermidine was associated with the activation of Nrf2 signaling pathway. According to the data, spermidine may be a potential lead compound which can be further optimized to discover novel antibacterial and antioxidant agents.

Keywords

References

  1. Kang, S. Y. 2005. The antimicrobial compound of Rhus verniciflua barks against fish pathogenic gram-negative bacteria, Edwardsiella tarda and Vivrio anguillarum. J. Fish Pathol. 18, 227-237.
  2. Kim, N. K., Kweon, D. H. and Kim, S. K. 2012. Effects of natural compounds from various plant eradicate the persister cell of Edwardsiella tarda treated with antibiotics of florfenicol and amoxicillin. J. Life Sci. 22, 788-793. https://doi.org/10.5352/JLS.2012.22.6.788
  3. Lee, N. S., Jeong, S. H. and Jee, B. Y. 2010. Anti-fish pathogenic efficacy of hot water extracts obtained from 5 herbs in vitro, and efficacy and toxicity in flounder of the one selected herb, skullcap. J. Fish Pathol. 23, 137-143.
  4. Berridge, B. R., Fuller, J. D., Azavedo, J., Low, D. E., Bercovier, H. and Frelier, P. E. 1998. Development of specific nested oilgonucleotide PCR primers for the Streptococcus iniae 16S-23S ribosomal DNA intergenic spacer. J. Clin. Microbiol. 36, 2778-2781. https://doi.org/10.1128/JCM.36.9.2778-2781.1998
  5. Bragg, R. R., Todd, J. M., Lordan, S. M. and Combrink, M. E. 1989. A selective procedure for the field isolation of pathogenic Streptococcus spp. of rainbow trout (Salmo gairdneri). Onderstepoort. J. Vet. Res. 56, 179-184.
  6. La Frentz, B. R., Shoemaker, C. A. and Klesius, P. H. 2011. Immunoproteomic analysis of the antibody response obtained in Nile tilapia following vaccination with a Streptococcus iniae vaccine. Vet. Microbiol. 152, 346-352. https://doi.org/10.1016/j.vetmic.2011.04.033
  7. Kim, H. J., Woo, S. H., Kim, J. W. and Park, S. I. 2005. Morphological characteristics and pathogenicity of Streptococcus iniae. J. Kor. Fish Soc. 18, 167-178.
  8. Cowan, M. M. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12, 564-582. https://doi.org/10.1128/CMR.12.4.564
  9. Sculley, D. V. 2014. Periodontal disease: modulation of the inflammatory cascade by dietary n-3 polyunsaturated fatty acids. J. Periodontal Res. 49, 277-281. https://doi.org/10.1111/jre.12116
  10. Wiegertjes, G. F. and Forlenza, M. 2010. Nitrosative stress during infection-induced inflammation in fish: lessons from a host-parasite infection model. Curr. Pharm. Des. 16, 4194-4202. https://doi.org/10.2174/138161210794519138
  11. Moloney, J. N. and Cotter, T. G. 2018. ROS signalling in the biology of cancer. Semin. Cell Dev. Biol. 80, 50-64. https://doi.org/10.1016/j.semcdb.2017.05.023
  12. Pizzino, G., Irrera, N., Cucinotta, M,, Pallio, G., Mannino, F., Arcoraci, V., Squadrito, F., Altavilla, D. and Bitto, A. 2017. Oxidative stress: Harms and benefits for human health. Oxid. Med. Cell. Longev. 2017, 8416763.
  13. Zimmermann, M. and Reichert, A. S. 2017. How to get rid of mitochondria: crosstalk and regulation of multiple mitophagy pathways. Biol. Chem. 399, 29-45. https://doi.org/10.1515/hsz-2017-0206
  14. Rigoulet, M., Yoboue, E. D. and Devin, A. 2011. Mitochondrial ROS generation and its regulation: mechanisms involved in $H_2O_2$ signaling. Antioxid. Redox. Signal. 14, 459-68. https://doi.org/10.1089/ars.2010.3363
  15. Wu, M. and Hancock, R. E. 1999. Interaction of the cyclic antimicrobial cationic peptide bactenecin with the outer and cytoplasmic membrane. J. Biol. Chem. 274, 29-35. https://doi.org/10.1074/jbc.274.1.29
  16. Matthew, E. and Levison, M. D. 2004. Pharmacodynamics of antimicrobial drugs. Infect. Dis. Clin. N. Am. 18, 451-465. https://doi.org/10.1016/j.idc.2004.04.012
  17. Kim, M. S., Seo, J. S., Park, M. A., Cho, J. Y., Hwang, J. Y., Kwon, M. G. and Jung, S. H. 2010. Antimicrobial resistance of Edwardsiella tarda, Vibrio spp., and Streptococcus spp. isolated from olive flounder Paralichthys olivaceus. J. Fish Pathol. 23, 37-45.
  18. Bjelakovic, G., Stojanovic, I., Jevtovic Stoimenov, T., Pavlovic, D., Kocic, G., Rossi, S., Tabolacci, C., Nikolic, J., Sokolovic, D. and Bjelakovic, L. 2010. Metabolic correlations of glucocorticoids and polyamines in inflammation and apoptosis. Amino Acids 39, 29-43. https://doi.org/10.1007/s00726-010-0489-3
  19. Chattopadhyay, M. K., Keembiyehetty, C. N., Chen, W. and Tabor, H. 2015. Polyamines stimulate the level of the ${\sigma}38$ subunit (RpoS) of Escherichia coli RNA polymerase, resulting in the induction of the glutamate decarboxylase-dependent acid response system via the gadE regulon. J. Biol. Chem. 290, 17809-17821. https://doi.org/10.1074/jbc.M115.655688
  20. Ozogul, F., Tabanelli, G., Toy, N. and Gardini, F. 2015. Impact of cell-free supernatant of lactic acid bacteria on putrescine and other polyamine formation by foodborne pathogens in ornithine decarboxylase broth. J. Agric. Food Chem. 63, 5828-5835. https://doi.org/10.1021/acs.jafc.5b02410
  21. Choi, Y. H. and Park, H. Y. 2012. Anti-inflammatory effects of spermidine in lipopolysaccharide-stimulated BV2 microglial cells. J. Biomed. Sci. 19, 1-8. https://doi.org/10.1186/1423-0127-19-1
  22. Shimidzu, N., Goto, M. and Miki, W. 1996. Carotenoids as singlet oxygen quenchers in marine organisms. Fish. Sci. 62, 134-137. https://doi.org/10.2331/fishsci.62.134
  23. Stahl, W. and Sies, H. 2003. Antioxidant activity of carotenoids. Mol. Aspects Med. 24, 345-351. https://doi.org/10.1016/S0098-2997(03)00030-X
  24. Nakagawa, K., Kang, S. D., Park, D. K., Handelman, G. J. and Miyazawa, T. 1997. Inhibition of ${\beta}$-carotene and astaxanthin of NADPH-dependent microsomal phospholipid peroxidation. J. Nutr. Sci. Vitaminol. (Tokyo) 43, 345-355. https://doi.org/10.3177/jnsv.43.345
  25. Chew, B. P. and Park, J. S. 2004. Carotenoid action on the immue presponse. J. Nutr. 134, 257S-261S. https://doi.org/10.1093/jn/134.1.257S
  26. Naguib, Y. M. 2000. Antioxidant activities of astaxanthin and related carotenoids. J. Agric. Food Chem. 48, 1150-1154. https://doi.org/10.1021/jf991106k
  27. Jung, S. H. and Kim, J. W. 2000. In vitro antimicrobial activity in combination of antibacterials against fish pathogenic bacteria. J. Fish Pathol. 13, 45-51.
  28. Ost, M., Keipert, S. and Klaus, S. 2017. Targeted mitochondrial uncoupling beyond UCP1 - The fine line between death and metabolic health. Biochimie 134, 77-85. https://doi.org/10.1016/j.biochi.2016.11.013
  29. Auger, C., Alhasawi A, Contavadoo M and Appanna VD. 2015. Dysfunctional mitochondrial bioenergetics and the pathogenesis of hepatic disorders. Front. Cell Dev. Biol. 3, 40.
  30. Deepika, M. S., Thangam, R., Vijayakumar, T. S., Sasirekha, R., Vimala, R. T. V., Sivasubramanian, S., Arun, S., Babu, M. D. and Thirumurugan, R. 2019. Antibacterial synergy between rutin and florfenicol enhances therapeutic spectrum against drug resistant Aeromonas hydrophila. Microb. Pathog. 135. 103612. https://doi.org/10.1016/j.micpath.2019.103612
  31. Wang, C., Pan, X., Fan, Y., Chen, Y. and Mu, W. 2017. The oxidative stress response of oxytetracycline in the ciliate Pseudocohnilembus persalinus. Environ. Toxicol. Pharmacol. 56, 35-42. https://doi.org/10.1016/j.etap.2017.08.019
  32. Cardaci, S., Filomeni, G. and Ciriolo, M. R. 2012. Redox implications of AMPK-mediated signal transduction beyond energetic clues. J. Cell. Sci. 125, 2115-2125. https://doi.org/10.1242/jcs.095216
  33. Mammucari, C. and Rizzuto, R. 2010. Signaling pathways in mitochondrial dysfunction and aging. Mech. Ageing Dev. 131, 536-543. https://doi.org/10.1016/j.mad.2010.07.003
  34. Li, Z., Dong, X., Liu, H., Chen, X., Shi, H., Fan, Y., Hou, D. and Zhang, X. 2013. Astaxanthin protects ARPE-19 cells from oxidative stress via upregulation of Nrf2-regulated phase II enzymes through activation of PI3K/Akt. Mol. Vis. 19, 1656-1666.
  35. Zhang, D. D. 2006. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab. Rev. 38, 769-789. https://doi.org/10.1080/03602530600971974
  36. Kaspar, J. W., Niture, S. K. and Jaiswal, A. K. 2009. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic. Biol. Med. 47, 1304-1309. https://doi.org/10.1016/j.freeradbiomed.2009.07.035
  37. Xie, J., Fang, H., Liao, S., Guo, T., Yin, P., Liu, Y., Tian, L. and Niu, J. 2019. Study on Schizochytrium sp. improving the growth performance and non-specific immunity of golden pompano (Trachinotus ovatus) while not affecting the antioxidant capacity. Fish Shellfish Immunol. S1050-4648, 30987-30988.
  38. Zhang, D. M., Guo, Z. X., Zhao, Y. L., Wang, Q. J., Gao, Y. S., Yu, T., Chen, Y. K., Chen, X. M. and Wang, G. Q. 2019. L-carnitine regulated Nrf2/Keap1 activation in vitro and in vivo and protected oxidized fish oil-induced inflammation response by inhibiting the NF-${\kappa}B$ signaling pathway in Rhynchocypris lagowski Dybowski. Fish Shellfish Immunol. 93, 1100-1110. https://doi.org/10.1016/j.fsi.2019.08.041
  39. Wang, H., Pan, L., Xu, R., Si, L. and Zhang, X. 2019. The molecular mechanism of Nrf2-Keap1 signaling pathway in the antioxidant defense response induced by BaP in the scallop Chlamys farreri. Fish Shellfish Immunol. 92, 489-499. https://doi.org/10.1016/j.fsi.2019.06.006
  40. Liu, P., de la Vega, M. R., Dodson, M., Yue, F., Shi, B., Fang, D., Chapman, E., Liu, L. and Zhang, D. D. 2019. Spermidine confers liver protection by enhancing NRF2 signaling through a MAP1S-mediated noncanonical mechanism. Hepatology 70, 372-388.