Anovel chemosynthetic peptide with β-sheet motif efficiently kills Klebsiella pneumoniae in a mouse model

International Journal of Nanomedicine

Volumn 10, Issue , 2015, Pages 1045-1059

  Tan, Shirui ^a,b   Gan, Changpei ^a,c   Li, Rongpeng ^a   Ye, Yan ^a   Zhang, Shuang ^a,c   Wu, Xu ^a   Yang, Yi Yan ^d   Fan, Weimin ^e   Wu, Min ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b YUNNAN UNIVERSITY   (China)

^c SICHUAN UNIVERSITY   (China)

^d INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

Antimicrobial peptides; Bacterial pathogenesis; Bactericidal activity; Infectious diseases; Inflammatory cytokines; STAT3 JAK signaling transduction

Indexed keywords

ANTIBIOTIC AGENT; IK8L PEPTIDE; INTERLEUKIN 6; JANUS KINASE; STAT3 PROTEIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BETA SHEET; BIOFILM; CONTROLLED STUDY; CYTOTOXICITY TEST; DISEASE SEVERITY; DOWN REGULATION; DRUG EFFECT; DRUG SCREENING; IN VITRO STUDY; KLEBSIELLA PNEUMONIAE; KLEBSIELLA PNEUMONIAE INFECTION; LUNG INJURY; MORTALITY; MOUSE; NONHUMAN; PROTEIN MOTIF; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; KLEBSIELLA INFECTIONS; MICROBIOLOGY; PROTEIN SECONDARY STRUCTURE;

ANIMALIA; BACTERIA (MICROORGANISMS); KLEBSIELLA PNEUMONIAE; MUS;

ANIMALS; ANTI-BACTERIAL AGENTS; DISEASE MODELS, ANIMAL; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MICE; PEPTIDES; PROTEIN STRUCTURE, SECONDARY;

EID: 84922756485     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S73303     Document Type: Article

References (59)

1. Lee JK, Park SC, Hahm KS, Park Y. A helix-PXXP-helix peptide with antibacterial activity without cytotoxicity against MDRPA-infected mice. Biomaterials. 2014;35 (3):1025-1039.
2. Peters BM, Shirtliff ME, Jabra-Rizk MA. Antimicrobial peptides: primeval molecules or future drugs? PLoS Pathog. 2010;6 (10):e1001067.
3. Pompilio A, Crocetta V, Scocchi M, et al. Potential novel therapeutic strategies in cystic fibrosis: antimicrobial and anti-biofilm activity of natural and designed α-helical peptides against Staphylococcus aureus, Pseudomonas aeruginosa, and Stenotrophomonas maltophilia. BMC Microbiol. 2012;12:145.
4. Adachi R, Suzuki K. Lyn, one of the Src-family tyrosine kinases expressed in phagocytes, plays an important role in beta2 integrin-signalling pathways in opsonized zymosan-activated macrophage-like U937 cells. Cell Biochem Funct. 2007;25 (3):323-333.
5. Lopes SP, Ceri H, Azevedo NF, Pereira MO. Antibiotic resistance of mixed biofilms in cystic fibrosis: impact of emerging microorganisms on treatment of infection. Int J Antimicrob Agents. 2012;40 (3):260-263.
6. Lech M, Römmele C, Kulkarni OP, et al. Lack of the long pentraxin PTX3 promotes autoimmune lung disease but not glomerulonephritis in murine systemic lupus erythematosus. PLoS One. 2011;6 (5):e20118.
7. van Zoelen MA, Verstege MI, Draing C, et al. Endogenous MCP-1 promotes lung inflammation induced by LPS and LTA. Mol Immunol. 2011;48 (12-13):1468-1476.
8. Izbicka E, Streeper RT, Michalek JE, Louden CL, Diaz A, Campos DR. Plasma biomarkers distinguish non-small cell lung cancer from asthma and differ in men and women. Cancer Genomics Proteomics. 2012;9 (1):27-35.
9. Thornton MM, Chung-Esaki HM, Irvin CB, Bortz DM, Solomon MJ, Younger JG. Multicellularity and antibiotic resistance in Klebsiella pneumoniae grown under bloodstream-mimicking fluid dynamic conditions. J Infect Dis. 2012;206 (4):588-595.
10. Orsi GB, García-Fernández A, Giordano A, et al. Risk factors and clinical significance of ertapenem-resistant Klebsiella pneumoniae in hospitalised patients. J Hosp Infect. 2011;78 (1):54-58.
11. O’Neill AJ. New antibacterial agents for treating infections caused by multi-drug resistant Gram-negative bacteria. Expert Opin Investig Drugs. 2008;17 (3):297-302.
12. Jenssen H, Hamill P, Hancock RE. Peptide antimicrobial agents. Clin Microbiol Rev. 2006;19 (3):491-511.
13. Wiesner J, Vilcinskas A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence. 2010;1 (5):440-464.
14. Cederlund A, Gudmundsson GH, Agerberth B. Antimicrobial peptides important in innate immunity. FEBS J. 2011;278 (20):3942-3951.
15. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol. 2004;2 (1):43-56.
16. Rajanbabu V, Chen JY. Applications of antimicrobial peptides from fish and perspectives for the future. Peptides. 2011;32 (2):415-420.
17. Cudic M, Bulet P, Hoffmann R, Craik DJ, Otvos L. Chemical synthesis, antibacterial activity and conformation of diptericin, an 82-mer peptide originally isolated from insects. Eur J Biochem. 1999;266 (2):549-558.
18. Yuan K, Huang C, Fox J, et al. Elevated inflammatory response in caveolin-1-deficient mice with Pseudomonas aeruginosa infection is mediated by STAT3 protein and nuclear factor kappaB (NF-kappaB). J Biol Chem. 2011;286 (24):21814-21825.
19. Li X, Zhou X, Ye Y, et al. Lyn regulates inflammatory responses in Klebsiella pneumoniae infection via the p38/NF-κB pathway. Eur J Immunol. 2014;44 (3):763-773.
20. Guo Q, Shen N, Yuan K, et al. Caveolin-1 plays a critical role in host immunity against Klebsiella pneumoniae by regulating STAT5 and Akt activity. Eur J Immunol. 2012;42 (6):1500-1511.
21. Ong ZY, Cheng J, Huang Y, et al. Effect of stereochemistry, chain length and sequence pattern on antimicrobial properties of short synthetic β-sheet forming peptide amphiphiles. Biomaterials. 2014;35 (4):1315-1325.
22. Zhou X, Li X, Ye Y, et al. MicroRNA-302b augments host defense to bacteria by regulating inflammatory responses via feedback to TLR/IRAK4 circuits. Nat Commun. 2014;5:3619.
23. O’toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R. Genetic approaches to study of biofilms. Methods Enzymol. 1999;310:91-109.
24. Deng X, Weerapana E, Ulanovskaya O, et al. Proteome-wide quantification and characterization of oxidation-sensitive cysteines in pathogenic bacteria. Cell Host Microbe. 2013;13 (3):358-370.
25. Wu M, Kelley MR, Hansen WK, Martin WJ. Reduction of BCNU toxicity to lung cells by high-level expression of O (6)-methylguanine-DNA methyltransferase. Am J Physiol Lung Cell Mol Physiol. 2001;280 (4):L755-L761.
26. Kannan S, Huang H, Seeger D, et al. Alveolar epithelial type II cells activate alveolar macrophages and mitigate P. aeruginosa infection. PLoS One. 2009;4 (3):e4891.
27. Wu M, Audet A, Cusic J, Seeger D, Cochran R, Ghribi O. Broad DNA repair responses in neural injury are associated with activation of the IL-6 pathway in cholesterol-fed rabbits. J Neurochem. 2009;111 (4):1011-1021.
28. Wu M, Huang H, Zhang W, et al. Host DNA repair proteins in response to Pseudomonas aeruginosa in lung epithelial cells and in mice. Infect Immun. 2011;79 (1):75-87.
29. Long Q, Huang W, Yao Y, et al. Virus-like particles presenting interleukin-33 molecules: Immunization characteristics and potentials of blocking IL-33/ST2 pathway in allergic airway inflammation. Hum Vaccin Immunother. 2014;10 (8):2303-2311.
30. Gast A, Anderson W, Probst A, et al. Pharmacokinetics and distribution of recombinant secretory leukocyte proteinase inhibitor in rats. Am Rev Respir Dis. 1990;141 (4 Pt 1):889-894.
31. Wu M, Stockley PG, Martin WJ. An improved western blotting technique effectively reduces background. Electrophoresis. 2002;23 (15):2373-2376.
32. Yuan K, Huang C, Fox J, et al. Autophagy plays an essential role in the clearance of Pseudomonas aeruginosa by alveolar macrophages. J Cell Sci. 2012;125 (Pt 2):507-515.
33. Li G, Yuan K, Yan C, et al. 8-Oxoguanine-DNA glycosylase 1 deficiency modifies allergic airway inflammation by regulating STAT6 and IL-4 in cells and in mice. Free Radic Biol Med. 2012;52 (2):392-401.
34. Ye Y, Wang H, Chu JH, et al. Atractylenolide II induces G1 cell-cycle arrest and apoptosis in B16 melanoma cells. J Ethnopharmacol. 2011;136 (1):279-282.
35. Kannan S, Pang H, Foster DC, Rao Z, Wu M. Human 8-oxoguanine DNA glycosylase increases resistance to hyperoxic cytotoxicity in lung epithelial cells and involvement with altered MAPK activity. Cell Death Differ. 2006;13 (2):311-323.
36. He YH, Wu M, Kobune M, Xu Y, Kelley MR, Martin WJ. Expression of yeast apurinic/apyrimidinic endonuclease (APN1) protects lung epithelial cells from bleomycin toxicity. Am J Respir Cell Mol Biol. 2001;25 (6):692-698.
37. Lu Z, Dai T, Huang L, et al. Photodynamic therapy with a cationic functionalized fullerene rescues mice from fatal wound infections. Nanomedicine (Lond). 2010;5 (10):1525-1533.
38. Ong ZY, Gao SJ, Yang YY. Short synthetic β-sheet forming peptide amphiphiles as broad spectrum antimicrobials with antibiofilm and endotoxin neutralizing capabilities. Adv Funct Mater. 2013;23 (29):3682-3692.
39. Reino DC, Palange D, Feketeova E, et al. Activation of toll-like receptor 4 is necessary for trauma hemorrhagic shock-induced gut injury and polymorphonuclear neutrophil priming. Shock. 2012;38 (1):107-114.
40. Gonzalez RJ, Weening EH, Frothingham R, Sempowski GD, Miller VL. Bioluminescence imaging to track bacterial dissemination of Yersinia pestis using different routes of infection in mice. BMC Microbiol. 2012;12:147.
41. Feyler A, Voho A, Bouchardy C, et al. Point: myeloperoxidase-463G-. a polymorphism and lung cancer risk. Cancer Epidemiol Biomarkers Prev. 2002;11 (12):1550-1554.
42. Regueiro V, Moranta D, Frank CG, et al. Klebsiella pneumoniae subverts the activation of inflammatory responses in a NOD1-dependent manner. Cell Microbiol. 2011;13 (1):135-153.
43. Kannan S, Audet A, Huang H, Chen LJ, Wu M. Cholesterol-rich membrane rafts and Lyn are involved in phagocytosis during Pseudomonas aeruginosa infection. J Immunol. 2008;180 (4):2396-2408.
44. Simons K, Ikonen E. How cells handle cholesterol. Science. 2000;290 (5497):1721-1726.
45. Davies J. Origins and evolution of antibiotic resistance. Microbiologia. 1996;12 (1):9-16.
46. Chiavolini D, Pozzi G, Ricci S. Animal models of Streptococcus pneumoniae disease. Clin Microbiol Rev. 2008;21 (4):666-685.
47. Mbawuike IN, Herscowitz HB. MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics. J Leukoc Biol. 1989;46 (2):119-127.
48. Coque TM, Baquero F, Canton R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill. 2008;13 (47):1-11.
49. Wu G, Li X, Deng X, et al. Protective effects of antimicrobial peptide S-thanatin against endotoxic shock in mice introduced by LPS. Peptides. 2011;32 (2):353-357.
50. Wu G, Wu P, Xue X, et al. Application of S-thanatin, an antimicrobial peptide derived from thanatin, in mouse model of Klebsiella pneumoniae infection. Peptides. 2013;45:73-77.
51. Ye P, Garvey PB, Zhang P, et al. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am J Respir Cell Mol Biol. 2001;25 (3):335-340.
52. Kannan S, Wu M. Respiratory stem cells and progenitors: overview, derivation, differentiation, carcinogenesis, regeneration and therapeutic application. Curr Stem Cell Res Ther. 2006;1 (1):37-46.
53. Wu M. DNA repair proteins as molecular therapeutics for oxidative and alkylating lung injury. Curr Gene Ther. 2005;5 (2):225-236.
54. Wang P, Wang X, Yang X, Liu Z, Wu M, Li G. Budesonide suppresses pulmonary antibacterial host defense by down-regulating cathelicidin-related antimicrobial peptide in allergic inflammation mice and in lung epithelial cells. BMC Immunol. 2013;14:7.
55. Priebe GP, Goldberg JB. Vaccines for Pseudomonas aeruginosa: a long and winding road. Expert Rev Vaccines. 2014;13 (4):507-519.
56. Yan J, Liu X, Wang Y, et al. Enhancing the potency of HBV DNA vaccines using fusion genes of HBV-specific antigens and the N-terminal fragment of gp96. J Gene Med. 2007;9 (2):107-121.
57. Zhao K, Deng X, He C, Yue B, Wu M. Pseudomonas aeruginosa outer membrane vesicles modulate host immune responses by targeting the Toll-like receptor 4 signaling pathway. Infect Immun. 2013;81 (12):4509-4518.
58. Wu M, Pasula R, Smith PA, Martin WJ. Mapping alveolar binding sites in vivo using phage peptide libraries. Gene Ther. 2003;10 (17):1429-1436.
59. Zhang D, Wu M, Nelson DE, Pasula R, Martin WJ. Alpha-1-antitrypsin expression in the lung is increased by airway delivery of gene-transfected macrophages. Gene Ther. 2003;10 (26):2148-2152.