Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Anti-Inflammatory Activity of Antimicrobial Peptide Periplanetasin-5 Derived from the Cockroach Periplaneta americana

  • Kim, In-Woo (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • 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, Mi-Ae (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Shin, Yong Pyo (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Sung Hyun (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Iksoo (College of Agriculture and Life Sciences, Chonnam National University) ;
  • Hwang, Jae Sam (Department of Agricultural Biology, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2020.04.22
  • Accepted : 2020.06.02
  • Published : 2020.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

Previously, we performed an in silico analysis of the Periplaneta americana transcriptome. Antimicrobial peptide candidates were selected using an in silico antimicrobial peptide prediction method. It was found that periplanetasin-5 had antimicrobial activity against yeast and gram-positive and gram-negative bacteria. In the present study, we demonstrated the anti-inflammatory activities of periplanetasin-5 in mouse macrophage Raw264.7 cells. No cytotoxicity was observed at 60 ㎍/ml periplanetasin-5, and treatment decreased nitric oxide production in Raw264.7 cells exposed to lipopolysaccharide (LPS). In addition, quantitative RT-PCR and enzyme-linked immunosorbent assay revealed that periplanetasin-5 reduced cytokine (tumor necrosis factor-α, interleukin-6) expression levels in the Raw264.7 cells. Periplanetasin-5 controlled inflammation by inhibiting phosphorylation of MAPKs, an inflammatory signaling element, and reducing the degradation of IκB. Through LAL assay, LPS toxicity was found to decrease in a periplanetasin-5 dose-dependent manner. Collectively, these data showed that periplanetasin-5 had anti-inflammatory activities, exemplified in LPS-exposed Raw264.7 cells. Thus, we have provided a potentially useful antibacterial peptide candidate with anti-inflammatory activities.

Keywords

References

  1. Hultmark D, Steiner H, Rasmuson T, Boman H G. 1980. Insect immunity. purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur. J. Biochem. 106: 7-16. https://doi.org/10.1111/j.1432-1033.1980.tb05991.x
  2. Steiner H, Hultmark D, Engstrom A, Bennich H, Boman H G. 1981. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292: 246-248. https://doi.org/10.1038/292246a0
  3. Bulet P, Stocklin R. 2005. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12: 3-11. https://doi.org/10.2174/0929866053406011
  4. Ganz T, Lehrer R I. 1994. Defensins. Curr. Opin. Immunol. 6: 584-589. https://doi.org/10.1016/0952-7915(94)90145-7
  5. Otvos L Jr. 2000. Antibacterial peptides isolated from insects. J. Pept. Sci. 6: 497-511. https://doi.org/10.1002/1099-1387(200010)6:10<497::AID-PSC277>3.0.CO;2-W
  6. Lee JH, Kim IW, Kim SH, Yun EY, Nam SH, Ahn MY, et al. 2015. Anticancer activity of CopA3 dimer peptide in human gastric cancer cells. BMB Rep. 48: 324-329. https://doi.org/10.5483/BMBRep.2015.48.6.073
  7. Lee JH, Kim IW, Shin YP, Park HJ, Lee YS, Lee IH, et al. 2016. Enantiomeric CopA3 dimer peptide suppresses cell viability and tumor xenograft growth of human gastric cancer cells. Tumor Biol. 37: 3237-3245. https://doi.org/10.1007/s13277-015-4162-z
  8. Lee JH, Kim IW, Kim SH, Kim MA, Yun EY, Nam SH, et al. 2015. Anticancer activity of the antimicrobial peptide scolopendrasin VII derived from the centipede, Scolopendra subspinipes mutilans. J. Microbiol. Biotechnol. 25: 1275-1280. https://doi.org/10.4014/jmb.1503.03091
  9. Kim IW, Lee JH, Subramaniyam S, Yun EY, Kim I, Park J, et al. 2016. De novo transcriptome analysis and detection of antimicrobial peptides of the american cockroach Periplaneta americana (Linnaeus). PLoS One. 11: e0155304. https://doi.org/10.1371/journal.pone.0155304
  10. Chen W, Liu YX, Jiang GF. 2015. De novo assembly and characterization of the testis transcriptome and development of EST-SSR markers in the cockroach Periplaneta americana. Sci. Rep. 5: 11144. https://doi.org/10.1038/srep11144
  11. Ali SM, Siddiqui R, Ong SK, Shah MR, Anwar A, Heard PJ, et al. 2017. Identification and characterization of antibacterial compound(s) of cockroaches (Periplaneta americana). Appl. Microbiol. Biotechnol. 101: 253-286. https://doi.org/10.1007/s00253-016-7872-2
  12. Hong J, Zhang P, Yoon IN, Hwang JS, Kang JK, Kim H. 2017. The American cockroach peptide periplanetasin-2 blocks Clostridium difficile toxin A-induced cell damage and inflammation in the gut. J. Microbiol. Biotechnol. 27: 694-700. https://doi.org/10.4014/jmb.1612.12012
  13. Hawiger J. 2001. Innate immunity and inflammation: A transcriptional paradigm. Immunol. Res. 23: 99-109. https://doi.org/10.1385/IR:23:2-3:099
  14. Hanada T, Yoshimura A. 2002. Regulation of cytokine signaling and inflammation. Cytokine Growth Factor Rev. 13: 413-421. https://doi.org/10.1016/S1359-6101(02)00026-6
  15. Kaminska, B. 2005. MAPK signalling pathways as molecular targets for anti-inflammatory therapy—from molecular mechanisms to therapeutic benefits. Biochim. Biophys. Acta. 1754: 253-262. https://doi.org/10.1016/j.bbapap.2005.08.017
  16. Uwe S. 2008. Anti-inflammatory interventions of NF-kB signaling potential applications and risks. Biochem. Pharmacol. 75: 1567-1579. https://doi.org/10.1016/j.bcp.2007.10.027
  17. Kim MJ, Jeong SM, Kang BK, Kim KB, Ahn DH. 2019. Anti-inflammatory effects of grasshopper ketone from Sargassum fulvellum ethanol extract on lipopolysaccharide-induced inflammatory responses in RAW 264.7 cells. J. Microbiol. Biotechnol. 29: 820-826. https://doi.org/10.4014/jmb.1901.01027
  18. Forstermann U, Sessa WC. 2012. Nitric oxide synthases: regulation and function. Eur. Heart J. 33: 829-837. https://doi.org/10.1093/eurheartj/ehr304
  19. Pacher P, Beckman JS, Liaudet L. 2007. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 1: 315-424. https://doi.org/10.1152/physrev.00029.2006
  20. Botting RM. 2006. Inhibitors of cyclooxygenases: mechanisms, selectivity and uses. J. Physiol. Pharmacol. 5: S113-S124.
  21. Ricciotti E, Fitzgerald GA. 2011. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31: 986-1000. https://doi.org/10.1161/ATVBAHA.110.207449
  22. Yang X, Kang MC, Li Y, Kim EA, Kang SM, Jeon YJ. 2014. Anti-inflammatory activity of Questinol isolated from marine-derived fungus Eurotium amstelodami in lipopolysaccharide-stimulated Raw264.7 macrophages. J. Microbiol. Biotechnol. 24: 1346-1353. https://doi.org/10.4014/jmb.1405.05035
  23. Hu TY, Ju JM, Mo LH, Ma L, Hu WH, You RR, et al. 2019. Anti-inflammation action of xanthones from Swertia chirayita by regulating COX-2/$NF-{\kappa}B$/MAPKs/Akt signaling pathways in RAW 264.7 macrophage cells. Phytomedicine 55: 214-221. https://doi.org/10.1016/j.phymed.2018.08.001
  24. Chen X, Miao J, Wang H, Zhao F, Hu J, Gao P, et al. 2015. The anti-inflammatory activities of Ainsliaea fragrans Champ. extract and its components in lipopolysaccharide stimulated RAW264.7 macrophages through inhibition of $NF-{\kappa}B$ pathway. J. Ethnopharmacol. 170: 72-80. https://doi.org/10.1016/j.jep.2015.05.004
  25. Karin M. 1995. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270: 16483-16486. https://doi.org/10.1074/jbc.270.28.16483
  26. Zhong J, Kyriakis JM. 2007. Dissection of a signaling pathway by which pathogen-associated molecular patterns recruit the JNK and p38 MAPKs and trigger cytokine release. J. Biol. Chem. 282: 24246-24254. https://doi.org/10.1074/jbc.M703422200
  27. Liu T, Zhang L, Joo D, Sun SC. 2017. $NF-{\kappa}B$ signaling in inflammation. Signal Transduct. Target. Ther. 2: 17023. https://doi.org/10.1038/sigtrans.2017.23
  28. Tergaonkar V, Bottero V, Ikawa V, Li Q, Verma IM. 2003. IkB kinase-independent $IkB{\alpha}$ degradation pathway: Functional $NF-{\kappa}B$ activity and implications for cancer therapy. Mol. Cell. Biol. 23: 8070-8083. https://doi.org/10.1128/MCB.23.22.8070-8083.2003
  29. Ahmad B, Hanif Q, Xubiao W, Lulu Z, Shahid M, Dayong S, et al. 2019. Expression and purification of hybrid LL-37Ta1 peptide in Pichia pastoris and evaluation of its immunomodulatory and anti-inflammatory activities by LPS neutralization. Front. Immunol. 10: 1365. https://doi.org/10.3389/fimmu.2019.01365
  30. Mu L, Zhou L, Yang J, Zhuang L, Tang J, Liu T, et al. 2017. The first identified cathelicidin from tree frogs possesses anti-inflammatory and partial LPS neutralization activities. Amino Acids. 49: 1571-1585. https://doi.org/10.1007/s00726-017-2449-7
  31. Walters SM, Dubey VS, Jeffrey NR, Dixon DR. 2010. Antibiotic-induced Porphyromonas gingivalis LPS release and inhibition of LPS-stimulated cytokines by antimicrobial peptides. Peptides 31: 1649-1653. https://doi.org/10.1016/j.peptides.2010.06.001
  32. Schadich E, Mason D, Cole AL. 2013. Neutralization of bacterial endotoxins by frog antimicrobial peptides. Microbiol. Immunol. 57: 159-161. https://doi.org/10.1111/1348-0421.12012
  33. Sun Y, Shang D. 2015. Inhibitory effects of antimicrobial peptides on lipopolysaccharide-induced inflammation. Mediators Inflamm. 2015: 167572.
  34. Nan YH, Jeon YJ, Park IS, Shin SY. 2008. Antimicrobial peptide P18 inhibits inflammatory responses by LPS- but not by IFN-c-stimulated macrophages. Biotechnol. Lett. 30: 1183-1187. https://doi.org/10.1007/s10529-008-9682-9
  35. Lee JH, Seo M, Lee HJ, Baek M, Kim IW, Kim SY, et al. 2019. Anti-inflammatory activity of antimicrobial peptide allomyrinasin derived from the dynastid beetle, Allomyrina dichotoma. J. Microbiol. Biotechnol. 29: 687-695. https://doi.org/10.4014/jmb.1809.09031

Cited by

  1. BV-2 미세아교세포에서 왕귀뚜라미 유래 Teleogryllusine의 신경염증 억제 효과 vol.30, pp.11, 2020, https://doi.org/10.5352/jls.2020.30.11.999
  2. The Effects of Luminescent CdSe Quantum Dot-Functionalized Antimicrobial Peptides Nanoparticles on Antibacterial Activity and Molecular Mechanism vol.16, 2021, https://doi.org/10.2147/ijn.s295928
  3. Periplaneta americana Oligosaccharides Exert Anti-Inflammatory Activity through Immunoregulation and Modulation of Gut Microbiota in Acute Colitis Mice Model vol.26, pp.6, 2020, https://doi.org/10.3390/molecules26061718
  4. Bioinformatic analysis and antiviral effect of Periplaneta americana defensins vol.308, 2020, https://doi.org/10.1016/j.virusres.2021.198627