Immunomodulatory and anti-inflammatory activities of chicken cathelicidin-2 derived peptides

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Van Dijk, Albert ^a   Van Eldik, Mandy ^a   Veldhuizen, Edwin J A ^a   Tjeerdsma Van Bokhoven, Hanne L M ^a   De Zoete, Marcel R ^b   Bikker, Floris J ^c   Haagsman, Henk P ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN 2 DERIVED PEPTIDE; INTERLEUKIN 1BETA; INTERLEUKIN 8; LIPID A; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 3; NITRIC OXIDE; PHENYLALANINE; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; RANTES; TRYPTOPHAN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; ANTIINFLAMMATORY AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; AUTACOID; CHEMOKINE; CMAP27 PROTEIN, CHICKEN; CYTOKINE; IMMUNOLOGIC FACTOR; LACTATE DEHYDROGENASE; PEPTIDE FRAGMENT; REACTIVE OXYGEN METABOLITE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL SURVIVAL; BINDING AFFINITY; CAMPYLOBACTER JEJUNI; CHICKEN; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG CYTOTOXICITY; DRUG POTENCY; DRUG STRUCTURE; HOST RESISTANCE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LIMIT OF DETECTION; METABOLIC ACTIVITY ASSAY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SALMONELLA ENTERICA SEROVAR MINNESOTA; ANIMAL; BIOSYNTHESIS; CELL LINE; CHEMISTRY; DRUG EFFECTS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR MODEL; MUTATION; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; CHEMOKINES; CHICKENS; CYTOKINES; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; IMMUNOLOGIC FACTORS; INFLAMMATION MEDIATORS; L-LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDES; MACROPHAGES; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MUTATION; NITRIC OXIDE; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; REACTIVE OXYGEN SPECIES; TRANSCRIPTION, GENETIC;

EID: 84959218661     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147919     Document Type: Article

References (42)

1. Landers TF, Cohen B, Wittum TE, Larson EL. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep. 2012; 127:4-22. PMID: 22298919
2. Shryock TR, Richwine A. The interface between veterinary and human antibiotic use. Ann N Y Acad Sci. 2010; 1213:92-105. doi: 10.1111/j.1749-6632.2010.05788.x PMID: 20946576
3. Li X, Mehrotra M, Ghimire S, Adewoye L. β-Lactam resistance and β-lactamases in bacteria of animal origin. Vet Mic. 2007; 121:197-214.
4. Hancock REW. Mechanisms of action of newer antibiotics for Gram-positive pathogens. Lancet Infect Dis. 2005; 5:209-218. PMID: 15792738
5. Peschel A, Sahl HG. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol. 2006; 4:529-536. PMID: 16778838
6. Scott MG, Vreugdenhil AC, Buurman WA, Hancock RE, Gold MR. Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS binding protein. J Immunol. 2000; 164:549-553. PMID: 10623792
7. Bowdish DM, Davidson DJ, Scott MG, Hancock RE. Immunomodulatory activities of small host defense peptides. Antimicrob Agents Chemother. 2005; 49:1727-1732. PMID: 15855488
8. Scott MG, Davidson DJ, Gold MR, Bowdish D, Hancock REW. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J Immunol. 2002; 169:3883-3891. PMID: 12244186
9. De Y, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, et al. LL-37, the neutrophil granuleand epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med. 2000; 192:1069-1074. PMID: 11015447
10. Davidson DJ, Currie AJ, Reid GSD, Bowdish DME, MacDonald KL, Ma RC, et al. The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J Immunol. 2004; 172:1146-1156. PMID: 14707090
11. Ramanathan B, Wu H, Ross CR, Blecha F. PR-39, a porcine antimicrobial peptide, inhibits apoptosis: involvement of caspase-3. Dev Comp Immunol. 2004; 28:163-169. PMID: 12969801
12. Nagaoka I, Tamura H, Hirata M. An antimicrobial cathelicidin peptide, human CAP18/LL-37, suppresses neutrophil apoptosis via the activation of formyl-peptide receptor-like 1 and P2X7. J Immunol. 2006; 176:3044-3052. PMID: 16493063
13. van Dijk A, Molhoek ME, Veldhuizen EJA, Tjeerdsma-van Bokhoven JLM, Wagendorp E, Bikker F, et al. Identification of chicken cathelicidin-2 core elements involved in antibacterial and immunomodulatory activities. Mol Immunol. 2009; 46:2465-2473. doi: 10.1016/j.molimm.2009.05.019 PMID: 19524300
14. van Dijk A, Tersteeg-Zijderveld MHG, Tjeerdsma-van Bokhoven JLM, Jansman AJM, Veldhuizen EJA, Haagsman HP. Chicken heterophils are recruited to the site of Salmonella infection and release antibacterial mature Cathelicidin-2 upon stimulation with LPS. Mol Immunol. 2009; 46:1517-1526. doi: 10.1016/j.molimm.2008.12.015 PMID: 19187966
15. Westphal O, Jann JK. Bacterial lipopolysaccharide extraction with phenol-water and further application of the procedure. Methods Carbohydr Chem. 1965; 5:83-91.
16. Karkhanis YD, Zeltner JY, Jackson JJ, Carlo DJ. A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gram-negative bacteria. Anal Biochem. 1978; 85:595-601. PMID: 646115
17. Schindler PR, Teuber M. Action of polymyxin B on bacterial membranes: morphological changes in the cytoplasm and in the outer membrane of Salmonella typhimurium and Escherichia coli B. Antimicrob Agents Chemother. 1975; 8:95-104. PMID: 169730
18. Moore RA, Bates NC, Hancock RE. Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin. Antimicrob Agents Chemother. 1986; 29:496-500. PMID: 3013085
19. Beug H, von Kirchbach A, Doderlein G, Conscience JF, Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell. 1979; 18:375-390. PMID: 227607
20. Kaiser P, Poh TY, Rothwell L, Avery S, Balu S, Pathania US, et al. A genomic analysis of chicken cytokines and chemokines. J. Interferon Cytokine Res. 2005; 25:467-484. PMID: 16108730
21. Boscá L, Zeini M, Través PG, Hortelano S. Nitric oxide and cell viability in inflammatory cells: a role for NO in macrophage function and fate. Toxicology. 2005; 208:249-258. PMID: 15691589
22. J. Yang, R. Yan, A. Roy, D. Xu, J. Poisson and Y. Zhang.The I-TASSER Suite: protein structure and function predictionNat.Methods 127-810.1038/nmeth.3213.
23. Japelj B, Pristovsek P, Majerle A, Jerala R. Structural origin of endotoxin neutralization and antimicrobial activity of a lactoferrin-based peptide. J Biol Chem. 2005; 280:16955-16961. PMID: 15687491
24. Bhunia A, Domadia PN, Torres J, Hallock KJ, Ramamoorthy A, Bhattacharjya S. NMR structure of pardaxin, a pore-forming antimicrobial peptide, in lipopolysaccharide micelles: mechanism of outer membrane permeabilization. J. Biol. Chem. 2010; 285:3883-3895. doi: 10.1074/jbc.M109.065672 PMID: 19959835
25. Bommineni YR, Achanta M, Alexander J, Sunkara LT, Ritchey JW, Zhang G. A fowlicidin-1 analog protects mice from lethal infections induced by methicillin-resistant Staphylococcus aureus. Peptides. 2010; 31:1225-1230. doi: 10.1016/j.peptides.2010.03.037 PMID: 20381563
26. Koczulla R, von Degenfeld G, Kupatt C, Krötz F, Zahler S, Gloe T, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest. 2003; 111:1665-1672. PMID: 12782669
27. Scott MG, Dullaghan E, Mookherjee N, Glavas N, Waldbrook M, Thompson A, et al. An anti-infective peptide that selectively modulates the innate immune response. Nat Biotechnol. 2007; 25:465-472. PMID: 17384586
28. Nijnik A, Madera L, Ma S, Waldbrook M, Elliott MR, Easton DM, et al. Synthetic cationic peptide IDR-1002 provides protection against bacterial infections through chemokine induction and enhanced leukocyte recruitment. J Immunol. 2010; 184:2539-2550. doi: 10.4049/jimmunol.0901813 PMID: 20107187
29. Bowdish DM, Davidson DJ, Speert DP, Hancock RE. The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes. J Immunol. 2004; 172:3758-3765. PMID: 15004180
30. Brogden KA, Guthmiller JM, Salzet M, Zasloff M. The nervous system and innate immunity: the neuropeptide connection. Nat Immunol. 2005; 6:558-564. PMID: 15908937
31. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science. 1998; 282:2215-20. PMID: 9856937
32. Molhoek EM, van Dijk A, Veldhuizen EJA, Dijk-Knijnenburg H, Mars-Groenendijk RH, Boele LCL, et al. Chicken cathelicidin-2-derived peptides with enhanced immunomodulatory and antibacterial activities against biological warfare agents. Int J Antimicrob Agents. 2010; 36:271-274. doi: 10.1016/j. ijantimicag.2010.06.001 PMID: 20630709
33. Wimley WC, White SH. Membrane partitioning: distinguishing bilayer effects from the hydrophobic effect. Biochemistry. 1993; 32:6307-12. PMID: 8518274
34. Jacobs RE, White SH. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry. 1989; 28:3421-3437. PMID: 2742845
35. Sanchez KM, Kang G, Wu B, Kim JE. Tryptophan-Lipid Interactions in Membrane Protein Folding Probed by Ultraviolet Resonance Raman and Fluorescence Spectroscopy. Biophys J. 2011; 100:2121-2130. doi: 10.1016/j.bpj.2011.03.018 PMID: 21539779
36. Tsubery H, Ofek I, Cohen S, Eisenstein M, Fridkin M. Modulation of the hydrophobic domain of polymyxin B nonapeptide: effect on outer-membrane permeabilization and lipopolysaccharide neutralization. Mol Pharmacol. 2002; 62:1036-1042. PMID: 12391265
37. Pristovsek P, Kidric J. Solution structure of polymyxins B and E and effect of binding to lipopolysaccharide: an NMR and molecular modeling study. J Med Chem. 1999; 42:4604-4613. PMID: 10579822
38. Ferguson AD, Welte W, Hofmann E, Lindner B, Holst O, Coulton JW, et al. A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure. 2000; 8:585-92. PMID: 10873859
39. Scrutton NS, Raine AR. Cation-π bonding and amino-aromatic interactions in the biomolecular recognition of substituted ammonium ligands. Biochem J. 1996; 319 (Pt 1):1-8. PMID: 8870640
40. Nagaoka I, Hirota S, Niyonsaba F, Hirata M, Adachi Y, Tamura H, et al. Augmentation of the lipopolysaccharide-neutralizing activities of human cathelicidin CAP18/LL-37-derived antimicrobial peptides by replacement with hydrophobic and cationic amino acid residues. Clin Diagn Lab Immunol. 2002; 9:972-982. PMID: 12204946
41. Mookherjee N, Wilson HL, Doria S, Popowych Y, Falsafi R, Yu JJ, et al. Bovine and human cathelicidin cationic host defense peptides similarly suppress transcriptional responses to bacterial lipopolysaccharide. J Leukoc Biol. 2006; 80:1563-1574. PMID: 16943385
42. Wen AY, Sakamoto KM, Miller LS. The role of the transcription factor CREB in immune function. J Immunol. 2010; 185:6413-6419. doi: 10.4049/jimmunol.1001829 PMID: 21084670