Epinecidin-1 has immunomodulatory effects, facilitating its therapeutic use in a mouse model of pseudomonas aeruginosa sepsis

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 8, 2014, Pages 4264-4274

  Pan, Chieh Yu ^a   Chen, Jian Chyi ^b   Sheen, Jenn Feng ^c   Lin, Tai Lang ^d   Chen, Jyh Yih ^d  

^a NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^b SOUTHERN TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^c NATIONAL FORMOSA UNIVERSITY   (Taiwan)

^d INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; EPINECIDIN-1, EPINEPHELUS COIOIDES; FISH PROTEIN; IMIPENEM; IMMUNOLOGIC FACTOR;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; MALE; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOLECULAR GENETICS; MORTALITY; MOUSE; MULTIDRUG RESISTANCE; PATHOGENICITY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SEPSIS; SURVIVAL; SYNTHESIS; TOXICITY TESTING;

AMINO ACID SEQUENCE; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FISH PROTEINS; HUMANS; IMIPENEM; IMMUNOLOGIC FACTORS; MALE; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SEPSIS; SURVIVAL ANALYSIS; TOXICITY TESTS, ACUTE;

EID: 84905366007     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02958-14     Document Type: Article

References (45)

1. Toufekoula C, Papadakis V, Tsaganos T, Routsi C, Orfanos SE, Kotanidou A, Carrer DP, Raftogiannis M, Baziaka F, Giamarellos-Bourboulis EJ. 2013. Compartmentalization of lipid peroxidation in sepsis by multidrug-resistant gram-negative bacteria: experimental and clinical evidence. Crit. Care 17:R6. http://dx.doi.org/10.1186/cc11930.
2. Van Delden C. 2007. Pseudomonas aeruginosa bloodstream infections: how should we treat them? Int. J. Antimicrob. Agents 30:S71-S75. http://dx.doi.org/10.1016/j.ijantimicag.2007.06.015.
3. Page MG, Heim J. 2009. Prospects for the next anti-Pseudomonas drug. Curr. Opin. Pharmacol. 9:558-565. http://dx.doi.org/10.1016/j.coph.2009.08.006.
4. Senati M, Polacco M, Grassi VM, Carbone A, De-Giorgio F. 2013. Child abuse followed by fatal systemic Pseudomonas aeruginosa infection. Leg. Med. (Tokyo) 15:28-31. http://dx.doi.org/10.1016/j.legalmed.2012.08.001.
5. Haja Mydin H, Corris PA, Nicholson A, Perry JD, Meachery G, Marrs EC, Peart S, Fagan C, Lordan JL, Fisher AJ, Gould FK. 2012. Targeted antibiotic prophylaxis for lung transplantation in cystic fibrosis patients colonised with Pseudomonas aeruginosa using multiple combination bactericidal testing. J. Transplant. 2012:135738. http://dx.doi.org/10.1155/2012/135738.
6. Hsueh PR, Tseng SP, Teng LJ, Ho SW. 2005. Pan-drug-resistant Pseudomonas aeruginosa causing nosocomial infection at a university hospital in Taiwan. Clin. Microbiol. Infect. 11:670-681. http://dx.doi.org/10.1111/j.1469-0691.2005. 01196.x.
7. Barnea Y, Carmeli Y, Kuzmenko B, Gur E, Hammer-Munz O, Navon-Venezia S. 2006. The establishment of a Pseudomonas aeruginosainfected burn-wound sepsis model and the effect of imipenem treatment. Ann. Plast. Surg. 56:674-679. http://dx.doi.org/10.1097/01.sap. 0000203984.62284.7a.
8. Ahn JY, Song JY, Yun YS, Jeong G, Choi IS. 2006. Protection of Staphylococcus aureus-infected septic mice by suppression of early acute inflammation and enhanced antimicrobial activity by ginsan. FEMS Immunol. Med. Microbiol. 46:187-197. http://dx.doi.org/10.1111/j.1574-695X.2005.00021.x.
9. Armand-Lefèvre L, Angebault C, Barbier F, Hamelet E, Defrance G, Ruppé E, Bronchard R, Lepeule R, Lucet JC, El Mniai A, Wolff M, Montravers P, Plésiat P, Andremont A. 2013. Emergence of imipenemresistant gram-negative bacilli in intestinal flora of intensive care patients. Antimicrob. Agents Chemother. 57:1488-1495. http://dx.doi.org/10.1128/ AAC.01823-12.
10. Saugar JM, Alarcón T, López-Hernández S, López-Brea M, Andreu D, Rivas L. 2002. Activities of polymyxin B and cecropin A-melittin peptide CA (1-8) M (1-18) against a multiresistant strain of Acinetobacter baumannii. Antimicrob. Agents Chemother. 46:875-878. http://dx.doi.org/10.1128/AAC.46.3.875-878.2002.
11. Saugar JM, Rodríguez-Hernández MJ, De La Torre BG, Pachón-Ibañez ME, Fernández-Reyes M, Andreu D, Pachón J, Rivas L. 2006. Activity of cecropin A-melittin hybrid peptides against colistin-resistant clinical strains of Acinetobacter baumannii: molecular basis for the differential mechanisms of action. Antimicrob. Agents Chemother. 50:1251-1256. http://dx.doi.org/10.1128/AAC.50.4.1251-1256.2006.
12. Bowdish DM, Davidson DJ, Hancock RE. 2005. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr. Protein Pept. Sci. 6:35-51. http://dx.doi.org/10.2174/1389203053027494.
13. Reddy KV, Yedery RD, Aranha C. 2004. Antimicrobial peptides: premises and promises. Int. J. Antimicrob. Agents 24:536-547. http://dx.doi.org/10.1016/j. ijantimicag.2004.09.005.
14. Bobone S, Roversi D, Giordano L, De Zotti M, Formaggio F, Toniolo C, Park Y, Stella L. 2012. The lipid dependence of antimicrobial peptide activity is an unreliable experimental test for different pore models. Biochemistry 51:10124-10126. http://dx.doi.org/10.1021/bi3015086.
15. Wu M, Maier E, Benz R, Hancock RE. 1999. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38:7235-7242. http://dx.doi.org/10.1021/bi9826299.
16. Yang L, Weiss TM, Lehrer RI, Huang HW. 2000. Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys. J. 79:2002-2009. http://dx.doi.org/10.1016/S0006-3495 (00) 76448-4.
17. Hallock KJ, Lee DK, Ramamoorthy A. 2003. MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. Biophys. J. 84:3052-3060. http://dx.doi.org/10.1016/S0006-3495 (03) 70031-9.
18. Yeung AT, Gellatly SL, Hancock RE. 2011. Multifunctional cationic host defence peptides and their clinical applications. Cell. Mol. Life Sci. 68:2161-2176. http://dx.doi.org/10.1007/s00018-011-0710-x.
19. Hancock RE, Lehrer R. 1998. Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16:82-88. http://dx.doi.org/10.1016/S0167-7799 (97) 01156-6.
20. David SA, Awasthi SK, Balaram P. 2000. The role of polar and facial amphipathic character in determining lipopolysaccharide-binding properties in synthetic cationic peptides. J. Endotoxin Res. 6:249-256. http://dx.doi.org/10. 1179/096805100101532117.
21. Sainath Rao S, Mohan KV, Atreya CD. 2013. A peptide derived from phage display library exhibits antibacterial activity against E. coli and Pseudomonas aeruginosa. PLoS One 8:e56081. http://dx.doi.org/10.1371/journal.pone.0056081.
22. Hancock RE, Sahl HG. 2006. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24:1551-1557. http://dx.doi.org/10.1038/nbt1267.
23. Pan CY, Chen JY, Cheng YS, Chen CY, Ni IH, Sheen JF, Pan YL, Kuo CM. 2007. Gene expression and localization of the epinecidin-1 antimicrobial peptide in the grouper (Epinephelus coioides), and its role in protecting fish against pathogenic infection. DNACell Biol. 26:403-413. http://dx.doi.org/10.1089/dna. 2006.0564.
24. Nijnik A, Madera L, Ma S, Waldbrook M, Elliott MR, Easton DM, Mayer ML, Mullaly SC, Kindrachuk J, Jenssen H, Hancock RE. 2010. Synthetic cationic peptide IDR-1002 provides protection against bacterial infections through chemokine induction and enhanced leukocyte recruitment. J. Immunol. 184:2539-2550. http://dx.doi.org/10.4049/jimmunol.0901813.
25. Wang YD, Kung CW, Chi SC, Chen JY. 2010. Inactivation of nervous necrosis virus infecting grouper (Epinephelus coioides) by epinecidin-1 and hepcidin 1-5 antimicrobial peptides, and downregulation of Mx2 and Mx3 gene expressions. Fish Shellfish Immunol. 28:113-120. http://dx.doi.org/10.1016/j.fsi.2009.10.001.
26. Huang HN, Pan CY, Rajanbabu V, Chan YL, Wu CJ, Chen JY. 2011. Modulation of immune responses by the antimicrobial peptide, epinecidin (Epi)-1, and establishment of an Epi-1-based inactivated vaccine. Biomaterials 32:3627-3636. http://dx.doi.org/10.1016/j.biomaterials.2011.01.061.
27. Lee SC, Pan CY, Chen JY. 2012. The antimicrobial peptide, epinecidin-1, mediates secretionofcytokinesintheimmuneresponsetobacterial infectioninmice. Peptides 36:100-108. http://dx.doi.org/10.1016/j.peptides.2012.04.002.
28. Pan CY, Wu JL, Hui CF, Lin CH, Chen JY. 2011. Insights into the antibacterial and immunomodulatory functions of the antimicrobial peptide, epinecidin-1, against Vibrio vulnificus infection in zebrafish. Fish Shellfish Immunol. 31:1019-1025. http://dx.doi.org/10.1016/j.fsi.2011.09.001.
29. Cirioni O, Silvestri C, Ghiselli R, Orlando F, Riva A, Gabrielli E, Mocchegiani F, Cianforlini N, Trombettoni MM, Saba V, Scalise G, Giacometti A. 2009. Therapeutic efficacy of buforin II and rifampin in a rat model of Acinetobacter baumannii sepsis. Crit. Care Med. 37:1403-1407. http://dx.doi.org/10.1097/CCM.0b013e31819c3e22.
30. Pan CY, Lee SC, Rajanbabu V, Lin CH, Chen JY. 2012. Insights into the antibacterial and immunomodulatory functions of tilapia hepcidin (TH) 2-3 against Vibrio vulnificus infection in mice. Dev. Comp. Immunol. 36:166-173. http://dx.doi.org/10.1016/j.dci.2011.06.013.
31. Huang TC, Chen JY. 2013. Proteomic and functional analysis of zebrafish after administration of antimicrobial peptide epinecidin-1. Fish Shellfish Immunol. 34:593-598. http://dx.doi.org/10.1016/j.fsi.2012.11.032.
32. Lin WJ, Chien YL, Pan CY, Lin TL, Chen JY, Chiu SJ, Hui CF. 2009. Epinecidin-1, an antimicrobial peptide from fish (Epinephelus coioides) which has an antitumor effect like lytic peptides in human fibrosarcoma cells. Peptides 30:283-290. http://dx.doi.org/10.1016/j.peptides.2008.10.007.
33. Cirioni O, Wu G, Li L, Orlando F, Silvestri C, Ghiselli R, Shen Z, Gabrielli E, Brescini L, Lezoche G, Provinciali M, Guerrieri M, Giacometti A. 2011. S-thanatin in vitro prevents colistin resistance and improves its efficacy in an animal model of Pseudomonas aeruginosa sepsis. Peptides 32:697-701. http://dx.doi.org/10.1016/j.peptides.2011.01.016.
34. Ostorhazi E, Rozgonyi F, Sztodola A, Harmos F, Kovalszky I, Szabo D, Knappe D, Hoffmann R, Cassone M, Wade JD, Bonomo RA, Otvos L, Jr. 2010. Preclinical advantages of intramuscularly administered peptide A3-APO over existing therapies in Acinetobacter baumannii wound infections. J. Antimicrob. Chemother. 65:2416-2422. http://dx.doi.org/10.1093/jac/dkq337.
35. Qu H, Chen B, Peng H, Wang K. 2013. Molecular cloning, recombinant expression, and antimicrobial activity of EC-hepcidin3, a new fourcysteine hepcidin isoform from Epinephelus coioides. Biosci. Biotechnol. Biochem. 77:103-110. http://dx.doi.org/10.1271/bbb.120600.
36. Szabo D, Ostorhazi E, Binas A, Rozgonyi F, Kocsis B, Cassone M, Wade JD, Nolte O, Otvos L, Jr. 2010. The designer proline-rich antibacterial peptide A3-APO is effective against systemic Escherichia coli infections in different mouse models. Int. J. Antimicrob. Agents 35:357-361. http://dx.doi.org/10.1016/ j.ijantimicag.2009.10.015.
37. Noto PB, Abbadessa G, Cassone M, Mateo GD, Agelan A, Wade JD, Szabo D, Kocsis B, Nagy K, Rozgonyi F, Otvos L, Jr. 2008. Alternative stabilities of a proline-rich antibacterial peptide in vitro and in vivo. Protein Sci. 17:1249-1255. http://dx.doi.org/10.1110/ps.034330.108.
38. Warszawska JM, Gawish R, Sharif O, Sigel S, Doninger B, Lakovits K, Mesteri I, Nairz M, Boon L, Spiel A, Fuhrmann V, Strobl B, Müller M, Schenk P, Weiss G, Knapp S. 2013. Lipocalin 2 deactivates macrophages and worsens pneumococcal pneumonia outcomes. J. Clin. Invest. 123:3363-3372. http://dx.doi.org/10.1172/JCI67911.
39. Peng KC, Lee SH, Hour AL, Pan CY, Lee LH, Chen JY. 2012. Five different piscidins from Nile tilapia, Oreochromis niloticus: analysis of their expressions and biological functions. PLoS One 7:e50263. http://dx.doi.org/10. 1371/journal.pone.0050263.
40. López-Rojas R, Docobo-Pérez F, Pachón- Ibáñez ME, De La Torre BG, Fernández-Reyes M, March C, Bengoechea JA, Andreu D, Rivas L, Pachón J. 2011. Efficacy of cecropin A-melittin peptides on a sepsis model of infection by pan-resistant Acinetobacter baumannii. Eur. J. Clin. Microbiol. Infect. Dis. 30:1391-1398. http://dx.doi.org/10.1007/s10096-011-1233-y.
41. Pan CY, Chow TY, Yu CY, Yu CY, Chen JC, Chen JY. 2010. Antimicrobial peptides of an anti-lipopolysaccharide factor, epinecidin-1, and hepcidin reduce the lethality of Riemerella anatipestifer sepsis in ducks. Peptides 31:806-815. http://dx.doi.org/10.1016/j.peptides.2010.01.013.
42. 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. http://dx.doi.org/10.1016/j. bbamem.2006.05.017.
43. Mandard N, Sodano P, Labbe H, Bonmatin JM, Bulet P, Hetru C, Ptak M, Vovelle F. 1998. Solution structure of thanatin, a potent bactericidal and fungicidal insect peptide, determined from proton two-dimensional nuclear magnetic resonance data. Eur. J. Biochem. 256:404-410. http://dx.doi.org/10. 1046/j.1432-1327.1998.2560404.x.
44. Moore DF, Rosenfeld MR, Gribbon PM, Winlove CP, Tsai CM. 1997. Alpha-1-acid (AAG, orosomucoid) glycoprotein: interaction with bacterial lipopolysaccharide and protection from sepsis. Inflammation 21:69-82. http://dx.doi.org/10.1023/A:1027342909423.
45. Tkalčević VI, Hrvačić B, Paš alić I, Eraković-Haber V, Glojnarić I. 2011. Immunomodulatory effects of azithromycin on serum amyloid A production in lipopolysaccharide-induced endotoxemia in mice. J. Antibiot. (Tokyo) 64:515-517. http://dx.doi.org/10.1038/ja.2011.14.