Anti-inflammatory action of an antimicrobial model peptide that suppresses the TRIF-Dependent signaling pathway via inhibition of toll-like receptor 4 endocytosis in lipopolysaccharide-stimulated macrophages

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Shim, Do Wan ^a   Heo, Kang Hyuck ^a   Kim, Young Kyu ^a   Sim, Eun Jeong ^a   Kang, Tae Bong ^a   Choi, Jae Wan ^a   Sim, Dae Won ^a   Cheong, Sun Hee ^a   Lee, Seung Hong ^a   Bang, Jeong Kyu ^b   Won, Hyung Sik ^a   Lee, Kwang Ho ^a  

^a Konkuk University   (South Korea)

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; BETA INTERFERON; CD14 ANTIGEN; CYCLOOXYGENASE 2; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; NITRIC OXIDE; POLYPEPTIDE ANTIBIOTIC AGENT; STAT1 PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WALK11.3; ANTIINFECTIVE AGENT; AUTACOID; NONSTEROID ANTIINFLAMMATORY AGENT; PEPTIDE; PTGS2 PROTEIN, MOUSE; TICAM-1 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; DRUG SCREENING; ENDOCYTOSIS; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CHEMISTRY; DRUG EFFECTS; METABOLISM; PRECLINICAL STUDY; PROCEDURES;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTI-INFECTIVE AGENTS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIGENS, CD14; CELL LINE; CYCLOOXYGENASE 2; DRUG EVALUATION, PRECLINICAL; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NITRIC OXIDE; PEPTIDES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84957571033     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126871     Document Type: Article

References (34)

1. Conlon JM, Mechkarska M, Lukic ML, Flatt PR (2014) Potential therapeutic applications of multifunctional host-defense peptides from frog skin as anti-cancer, anti-viral, immunomodulatory, and anti-diabetic agents. Peptides 57: 67-77. doi: 10.1016/j.peptides.2014.04.019 PMID: 24793775
2. Hilchie AL, Wuerth K, Hancock RE (2013) Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nature Chem Biol 9: 761-768. doi: 10.1038/nchembio.1393 PMID: 24231617
3. Fjell CD, Hiss JA, Hancock RE, Schneider G (2011) Designing antimicrobial peptides: Form follows function. Nature Rev Drug Discov 11: 37-51.
4. Nakatsuji T, Gallo RL (2012) Antimicrobial peptides: Old molecules with new ideas. J Invest Dermatol 132: 887-895. doi: 10.1038/jid.2011.387 PMID: 22158560
5. Nguyen LT, Haney EF, Vogel HJ (2011) The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol 29: 464-472. doi: 10.1016/j.tibtech.2011.05.001 PMID: 21680034
6. Ge L, Lyu P, Zhou M, Zhang H, Wan Y, Li B (2014) AcT-2: A novel myotropic and antimicrobial type 2 tryptophyllin from the skin secretion of the central american red-eyed leaf frog, agalychnis callidryas. Scientific World Journal 2014.
7. Meng P, Wei L, Yang S, Liu H, Liu R, Lai R (2012) A novel frog skin peptide containing function to induce muscle relaxation. Biochimie 94: 2508-2513. doi: 10.1016/j.biochi.2012.06.029 PMID: 22771463
8. Kim S, Kim J, Lee Y, Sim D, Lee S, Bank YY (2013) Structural characterization of de novo designed L5K5W model peptide isomers with potent antimicrobial and varied hemolytic activities. Molecules 18: 859-876. doi: 10.3390/molecules18010859 PMID: 23344198
9. Lee S, Kim S, Lee Y, Song M, Kim I, Won H (2011) De novo generation of short antimicrobial peptides with simple amino acid composition. Regul Pept 166: 36-41. doi: 10.1016/j.regpep.2010.08.010 PMID: 20736034
10. Nathan C, Ding A (2010) Nonresolving inflammation. Cell 140: 871-882. doi: 10.1016/j.cell.2010.02. 029 PMID: 20303877
11. Tabas I, Glass CK (2013) Anti-inflammatory therapy in chronic disease: Challenges and opportunities. Science 339: 166-172. doi: 10.1126/science.1230720 PMID: 23307734
12. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969. doi: 10.1038/nri2448 PMID: 19029990
13. Moynagh PN (2005) TLR signalling and activation of IRFs: Revisiting old friends from the NF-êB pathway. Trends Immunol 26: 469-476. PMID: 16006187
14. Beutler B, Rietschel ET (2003) Innate immune sensing and its roots: The story of endotoxin. Nat Rev Immunol 3: 169-176. PMID: 12563300
15. Aderem A, Ulevitch RJ (2000) Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787. PMID: 10963608
16. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17: 1-14. PMID: 15585605
17. Zanoni I, Ostuni R, Marek LR, Barresi S, Barbalat R, Barton GM (2011) CD14 controls the LPS-induced endocytosis of toll-like receptor 4. Cell 147: 868-880. doi: 10.1016/j.cell.2011.09.051 PMID: 22078883
18. Jacob B, Kim Y, Hyun J, Park I, Bang J, Shin S (2014) Bacterial killing mechanism of sheep myeloid antimicrobial peptide-18 (SMAP-18) and its trp-substituted analog with improved cell selectivity and reduced mammalian cell toxicity. Amino Acids 46: 187-198. doi: 10.1007/s00726-013-1616-8 PMID: 24221355
19. Lee S, Shin HJ, Kim D, Shim D, Kim T, Ye S (2013) Streptochlorin suppresses allergic dermatitis and mast cell activation via regulation of lyn/fyn and syk signaling pathways in cellular and mouse models. PloS one 8: e74194. doi: 10.1371/journal.pone.0074194 PMID: 24086321
20. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216. PMID: 11861602
21. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511. PMID: 15229469
22. Wang J, Hou L, Yang Y, Tang W, Li Y, Zuo J (2009) SM905, an artemisinin derivative, inhibited NO and pro-inflammatory cytokine production by suppressing MAPK and NF-êB pathways in RAW 264.7 macrophages. Acta Pharmacol Sin 30: 1428-1435. doi: 10.1038/aps.2009.138 PMID: 19801997
23. Kawai T, Takeuchi O, Fujita T, Inoue J, Muhlradt PF, Sato S (2001) Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167: 5887-5894. PMID: 11698465
24. Toshchakov V, Jones BW, Perera P, Thomas K, Cody MJ, Zhang S (2002) TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β-dependent gene expression in macrophages. Nat Immunol 3: 392-398. PMID: 11896392
25. Kawai T, Akira S (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650. doi: 10.1016/j.immuni.2011.05.006 PMID: 21616434
26. Husebye H, Halaas Ø, Stenmark H, Tunheim G, Sandanger Ø, Bogen B (2006) Endocytic pathways regulate toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J 25: 683-692. PMID: 16467847
27. Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R (2008) TRAM couples endocytosis of toll-like receptor 4 to the induction of interferon-β. Nat Immunol 9: 361-368. doi: 10.1038/ni1569 PMID: 18297073
28. Rosenfeld Y, Papo N, Shai Y (2006) Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. peptide properties and plausible modes of action. J Biol Chem 281: 1636-1643. PMID: 16293630
29. Nagaoka I, Hirota S, Niyonsaba F, Hirata M, Adachi Y, Tamura H (2001) Cathelicidin family of antibacterial peptides CAP18 and CAP11 inhibit the expression of TNF-alpha by blocking the binding of LPS to CD14(+) cells. J Immunol 167: 3329-3338. PMID: 11544322
30. Lee E, Kim J, Shin S, Jeong K, Shin A, Lee J (2013) Insight into the antimicrobial activities of coprisin isolated from the dung beetle, copris tripartitus, revealed by structure-activity relationships. Biochimica et Biophysica Acta (BBA)-Biomembranes 1828: 271-283. doi: 10.1016/j.bbamem.2012.10.028 PMID: 23137439
31. Wei L, Yang J, He X, Mo G, Hong J, Yan X (2013) Structure and function of a potent lipopolysaccharide-binding antimicrobial and anti-inflammatory peptide. J Med Chem 56: 3546-3556. doi: 10.1021/ jm4004158 PMID: 23594231
32. Jacobs AT, Ignarro LJ (2001) Lipopolysaccharide-induced expression of interferon-beta mediates the timing of inducible nitric-oxide synthase induction in RAW 264.7 macrophages. J Biol Chem 276: 47950-47957. PMID: 11602590
33. Moore KJ, Andersson LP, Ingalls RR, Monks BG, Li R, Arnaout MA (2000) Divergent response to LPS and bacteria in CD14-deficient murine macrophages. J Immunol 165: 4272-4280. PMID: 11035061
34. Shim DW, Han JW, Sun X, Jang CH, Koppula S, Kim TJ (2013) Lysimachia clethroides duby extract attenuates inflammatory response in raw 264.7 macrophages stimulated with lipopolysaccharide and in acute lung injury mouse model. J Ethnopharmacol 150: 1007-1015. doi: 10.1016/j.jep.2013.09.056 PMID: 24145006