DOI QR코드

DOI QR Code

Anti-Inflammatory Activity of Antimicrobial Peptide Allomyrinasin Derived from the Dynastid Beetle, Allomyrina dichotoma

  • Lee, Joon Ha (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Seo, Minchul (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Lee, Hwa Jeong (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Baek, Minhee (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, In-Woo (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Sun Young (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Mi-Ae (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Seong Hyun (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Hwang, Jae Sam (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2018.09.17
  • Accepted : 2019.03.21
  • Published : 2019.05.28

Abstract

In a previous work, we performed de novo RNA sequencing of Allomyrina dichotoma using next generation sequencing and identified several antimicrobial peptide candidates based on transcriptome analysis. Among them, a cationic antimicrobial peptide, allomyrinasin, was selected bioinformatically based on its physicochemical properties. Here, we assessed the antimicrobial and anti-inflammatory activities of allomyrinasin against microorganisms and mouse macrophage Raw264.7 cells. Allomyrinasin showed antimicrobial activities against various microbes and decreased the nitric oxide production of the lipopolysaccharide-induced Raw264.7 cells. Furthermore, quantitative RT-PCR and ELISA revealed that allomyrinasin reduced cytokine expression levels in the Raw264.7 cells. We also identified inducible nitric oxide synthase, cyclooxygenase-2 expression, and $PGE_2$ production through western blot analysis and ELISA. We confirmed that allomyrinasin bound to bacterial cell membranes via a specific interaction with lipopolysaccharides. Taken together, these data indicate that allomyrinasin has antimicrobial and anti-inflammatory activities as exemplified in lipopolysaccharide-induced Raw264.7 cells. We have provided a potentially useful antimicrobial peptide candidate that has both antimicrobial and anti-inflammatory activities.

Keywords

References

  1. Taketa K, Ichikawa E, Umetsu K, Suzuki T. 1986. Allomyrina dichotoma lectin-nonreactive a-fetoprotein in hepatocellular carcinoma and other tumors: comparison with Ricinus communis agglutinin-1. Cancer Lett. 31: 325-331. https://doi.org/10.1016/0304-3835(86)90155-2
  2. Jeune KH, Jung MY, Chol SJ, Lee JW, Park WH, Cho SH, et al. 2001. Immunomodulating effect of the lectin from Allomyrina dichotoma. Korean J. Pharmacognosy 32: 31-38.
  3. Chung MY, Yoon YI, Hwang JS, Goo TW, Yun EY. 2014. Anti-obesity effect of Allomyrina dichotoma (Arthropoda: Insecta) larvae ethanol extract on 3T3-L1 adipocyte differentiation. Entomol. Res. 44: 9-16. https://doi.org/10.1111/1748-5967.12044
  4. Yoon YI, Chung My, Hwang JS, Han MS, Goo TW, Yun EY. 2015. Allomyrina dichotoma (Arthropoda: Insecta) larvae confer resistance to obesity in mice fed a high-fat diet. Nutrients 7: 1978-1991. https://doi.org/10.3390/nu7031978
  5. Kim J, Yun EY, Park SW, Goo TW, Seo M. 2016. Allomyrina dichotoma larvae regulate food intake and body weight in high fat diet-induced obese mice through mTOR and Mapk signaling pathways. Nutrients 8: 100. https://doi.org/10.3390/nu8020100
  6. Kim M, Youn K, Yun EY, Hwang JS, Ahn MR, Jeong WS, et al. 2014. Effects of solvent fractions of Allomyrina dichotoma larvae through the inhibition of in vitro BACE1 and bamyloid(25-35)-induced toxicity in rat pheochromocytoma PC12 cells. Entomol. Res. 44: 23-30. https://doi.org/10.1111/1748-5967.12046
  7. Choi YH, Lee K, Yang KM, Jeong YM, Seo JS. 2006. Effect of larva extract of Allomyrina dichotoma on carbon tetrachlorideinduced hepatotoxicity in mice. J. Korean Soc. Food Sci. Nutr. 35: 1349-1355. https://doi.org/10.3746/jkfn.2006.35.10.1349
  8. Kim D, Huh J, You GC, Chae SC, Lee OS, Lee HB, et al. 2007. Allomyrina dichotoma larva extracts protect streptozotocininduced oxidative cytotoxicity. J. Environ. Toxicol. 22: 349-355.
  9. Lee K, Lee J. 2009. Protective effect of Allomyrina dichotoma larva extract on tert-butyl hydroperoxide-induced oxidative hepatotoxicity. Korean J. Environ. Biol. 27: 230-236.
  10. Suh H, Kim S, Lee K, Park S, Kang S. 2010. Antioxidant activity of various solvent extracts from Allomyrina dichotoma (Arthropoda: Insecta) larvae. J. Photochem. Photobiol. B Biol. 99: 67-73. https://doi.org/10.1016/j.jphotobiol.2010.02.005
  11. Niu L, Gao J, Li H, Liu J, Yin W. 2016. Novel skeleton compound Allomyrinanoid A and two purine alkaloids from the adult of Allomyrina dichotoma L. Bioorg. Med. Chem. Lett. 26: 366-369. https://doi.org/10.1016/j.bmcl.2015.12.012
  12. Miyanoshita A, Hara S, Sugiyama M, Asaoka A, Taniai K, Yukuhiro F, et al. 1996. Isolation and characterization of a new member of the insect defensin family from a beetle, Allomtrina dichotoma. Biochem.Biophy. Res. Commun. 220: 526-531. https://doi.org/10.1006/bbrc.1996.0438
  13. Sagisaka A, Miyanoshita A, Ishibashi J, Yamakawa M. 2001. Purification, characterization and gene expression of a glycine and proline-rich antibacterial protein family from larvae of a beetle, Allomtrina dichotoma. Insect Mol. Biol. 10:293-302. https://doi.org/10.1046/j.0962-1075.2001.00261.x
  14. Yamada M, Nakamura K, Saido-Sakanaka H, Asaoka A, Yamagawa M, Sameshima T, et al. 2004. Effect of modified oligopeptides from the beetle Allomyrina dichotoma on Escherichia coli infection in mice. J. Vet. Med. Sci. 66: 137-142. https://doi.org/10.1292/jvms.66.137
  15. Yamada M, Nakamura K, Saido-Sakanaka H, Asaoka A, Yamagawa M, Yamamoto Y, et al. 2005. Therapeutic effect of modified oligopeptides from the beetle Allomyrina dichotoma on methicillin-resistant Staphylococcus aureus (MRSA) infection in mice. J. Vet. Med. Sci. 67: 1005-1011. https://doi.org/10.1292/jvms.67.1005
  16. Kumar P, Kizhakkedathu JN, Straus SK. 2018. Antimicrobial peptides: diversity, mechanism of action and strategies to improve the activity and biocompatibility in vivo. Biomolecules 8: 4. https://doi.org/10.3390/biom8010004
  17. Karima R, Matsumoto S, Higashi H, Matsushima K. 1999. The molecular pathogenesis of endotoxic shock and organ failure. Mol. Med. Today 5: 123-132. https://doi.org/10.1016/S1357-4310(98)01430-0
  18. Martin GS, Mannino DM, Eaton S, Moss M. 2003. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348: 1546-1554. https://doi.org/10.1056/NEJMoa022139
  19. Ren JD, Gu JS, Gao HF, Xia PY, Xiao GX. 2008. A synthetic cyclic peptide derived from Limulus anti-lipopolysaccharide factor neutralizes endotoxin in vitro and in vivo. Int. Immunopharmacol 8: 775-781. https://doi.org/10.1016/j.intimp.2008.01.015
  20. Koyama Y, Motobu M, Hikosaka K, Yamada M, Nakamura K, Saido-Sakanaka H, et al. 2006. Protective effects of antimicrobial peptides derived from the beetle Allomyrina dichotoma defensin on endotoxic shock in mice. Int. Immunopharmacol 6: 232-240.
  21. Lehrer RI, Rosenman M, Harwig SS, Jackson R, Eisenhauer P. 1991. Designer assays for antimicrobial peptides. J. Immunol. Methods 137: 167-173. https://doi.org/10.1016/0022-1759(91)90021-7
  22. Rosenfeld Y, Shai Y. 2006. Lipopolysaccharide (Endotoxin)-host defense antibacterial peptides interactions: role in bacterial resistance and prevention of sepsis. Biochim. Biophys. Acta 1758: 1513-1522. https://doi.org/10.1016/j.bbamem.2006.05.017
  23. Bhor VM, Thomas CJ, Surolia N, Surolia A. 2005. Polymyxin B: an ode to an old antidote for endotoxic shock. Mol. Biosyst. 1: 213-222. https://doi.org/10.1039/b500756a
  24. Brandenburg K, Andra J, Garidel P, Gutsmann T. 2011. Peptide-based treatment of sepsis. Appl. Microbiol. Biotechnol. 90: 799-808. https://doi.org/10.1007/s00253-011-3185-7
  25. Malmsten M. 2016. Interactions of antimicrobial peptides with bacterial membranes and menbrane components. Curr. Top. Med. Chem. 16: 16-24. https://doi.org/10.2174/1568026615666150703121518
  26. Lee E, Kim JK, Shin S, Jeong KW, Shin A, Lee J, et al. 2013. Insight into the antimicrobial activities of coprisin isolated from the dung beetle, Copris tripatitus, revealed by structureactivity relationships. Biochim. Biophys. Acta 1828: 271-283. https://doi.org/10.1016/j.bbamem.2012.10.028
  27. Nam HJ, Oh AR, Nam ST, Kang JK, Chang JS, Kim DH, et al. 2012. The insect peptide CopA3 inhibits lipopolysaccharideinduced macrophage activation. J. Pept. Sci. 18: 650-656. https://doi.org/10.1002/psc.2437
  28. Qin H, Wilson CA, Lee SJ, Zhao X, Benveniste EN. 2005. LPS induces CD40 gene expression through the activation of NF-kappaB and STAT-1${\alpha}$ in macrophage and microglia. Blood 106: 3114-3122. https://doi.org/10.1182/blood-2005-02-0759
  29. Scott MG, Vreuqdenhil AC, Buurman WA, Hancock RE, Gold MR. 2000. Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS binding protein. J. Immunol. 164: 549-553. https://doi.org/10.4049/jimmunol.164.2.549

Cited by

  1. Allomyrina dichotoma Larva Extract Ameliorates the Hepatic Insulin Resistance of High-Fat Diet-Induced Diabetic Mice vol.11, pp.7, 2019, https://doi.org/10.3390/nu11071522
  2. Anti-Inflammatory Activity of Antimicrobial Peptide Periplanetasin-5 Derived from the Cockroach Periplaneta americana vol.30, pp.9, 2020, https://doi.org/10.4014/jmb.2004.04046
  3. BV-2 미세아교세포에서 왕귀뚜라미 유래 Teleogryllusine의 신경염증 억제 효과 vol.30, pp.11, 2019, https://doi.org/10.5352/jls.2020.30.11.999
  4. A highly efficient hybrid peptide ameliorates intestinal inflammation and mucosal barrier damage by neutralizing lipopolysaccharides and antagonizing the lipopolysaccharide‐receptor interaction vol.34, pp.12, 2019, https://doi.org/10.1096/fj.201903263rrr
  5. Evaluation of Short-Chain Antimicrobial Peptides With Combined Antimicrobial and Anti-inflammatory Bioactivities for the Treatment of Zoonotic Skin Pathogens From Canines vol.12, 2019, https://doi.org/10.3389/fmicb.2021.684650
  6. New Insect Host Defense Peptides (HDP) From Dung Beetle (Coleoptera: Scarabaeidae) Transcriptomes vol.21, pp.4, 2021, https://doi.org/10.1093/jisesa/ieab054
  7. Digestibility of insect meals for Pacific white shrimp (Litopenaeus vannamei) and their performance for growth, feed utilization and immune responses vol.16, pp.11, 2019, https://doi.org/10.1371/journal.pone.0260305
  8. The anti-inflammatory effects of dry-cured ham derived peptides in RAW264.7 macrophage cells vol.87, 2019, https://doi.org/10.1016/j.jff.2021.104827
  9. Antimicrobial peptides: mechanism of action, activity and clinical potential vol.8, pp.1, 2019, https://doi.org/10.1186/s40779-021-00343-2