Api88 is a novel antibacterial designer peptide to treat systemic infections with multidrug-resistant gram-negative pathogens

ACS Chemical Biology

Volumn 7, Issue 7, 2012, Pages 1281-1291

  Czihal, Patricia ^a   Knappe, Daniel ^a   Fritsche, Stefanie ^a   Zahn, Michael ^a   Berthold, Nicole ^a   Piantavigna, Stefania ^b   Müller, Uwe ^a   Van Dorpe, Sylvia ^c   Herth, Nicole ^a   Binas, Annegret ^d   Köhler, Gabriele ^e   De Spiegeleer, Bart ^c   Martin, Lisandra L ^b   Nolte, Oliver ^d   Sträter, Norbert ^a   Alber, Gottfried ^a   Hoffmann, Ralf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b MONASH UNIVERSITY   (Australia)

^c GHENT UNIVERSITY   (Belgium)

^d AiCuris GmbH   (Germany)

^e UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; PEPTIDE DERIVATIVE; PROTEIN DNAK;

ACINETOBACTER BAUMANNII; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BRAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYTOTOXICITY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INFECTION; ISOTOPE LABELING; KIDNEY; KLEBSIELLA PNEUMONIAE; LIVER; LYSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SEPSIS; SYSTEMIC INFECTION;

AMINO ACID SEQUENCE; ANIMALS; ANTI-BACTERIAL AGENTS; DRUG DESIGN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; TREATMENT OUTCOME;

ACINETOBACTER BAUMANNII; ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; KLEBSIELLA PNEUMONIAE; MUS; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84864148170     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300063v     Document Type: Article

References (56)

1. Kotra, L. P., Golemi, D., Vakulenko, S., and Mobashery, S. (2000) Bacteria fight back Chem. Ind. 341-344
2. DßCosta, V. M., King, C. E., Kalan, L., Morar, M., Sung, W. W. L., Schwarz, C., Froese, D., Zazula, G., Calmels, F., Debruyne, R., Golding, G. B., Poinar, H. N., and Wright, G. D. (2011) Antibiotic resistance is ancient Nature 477, 457-461
3. Michalopoulos, A. and Falagas, M. E. (2010) Treatment of Acinetobacter infections Expert Opin. Pharmacother. 11, 779-788
4. Kumarasamy, K. K., Toleman, M. A., Walsh, T. R., Bagaria, J., Butt, F., Balakrishnan, R., Chaudhary, U., Doumith, M., Giske, C. G., Irfan, S., Krishnan, P., Kumar, A. V., Maharjan, S., Mushtaq, S., Noorie, T., Paterson, D. L., Pearson, A., Perry, C., Pike, R., Rao, B., Ray, U., Sarma, J. B., Sharma, M., Sheridan, E., Thirunarayan, M. A., Turton, J., Upadhyay, S., Warner, M., Welfare, W., Livermore, D. M., and Woodford, N. (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study Lancet Infect. Dis. 10, 597-602
5. Kumarasamy, K. and Kalyanasundaram, A. (2012) Emergence of Klebsiella pneumoniae isolate co-producing NDM-1 with KPC-2 from India J. Antimicrob. Chemother. 67, 243-244
6. Khan, N. A. (2008) Acanthamoeba and the blood-brain barrier: the breakthrough J. Med. Microbiol. 57, 1051-1057
7. Mariani, M. M. and Kielian, T. (2009) Microglia in infectious diseases of the central nervous system J. Neuroimmune Pharmacol. 4, 448-461
8. Rock, R. B., Gekker, G., Hu, S. X., Sheng, W. S., Cheeran, M., Lokensgard, J. R., and Peterson, P. K. (2004) Role of microglia in central nervous system infections Clin. Microbiol. Rev. 17, 942-964
9. Brogden, K. A. (2005) Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250
10. Otvos, L. (2002) The short proline-rich antibacterial peptide family Cell. Mol. Life Sci. 59, 1138-1150
11. Casteels, P., Ampe, C., Jacobs, F., Vaeck, M., and Tempst, P. (1989) Apidaecins-Antibacterial peptides from honeybees EMBO J. 8, 2387-2391
12. Casteels, P. and Tempst, P. (1994) Apidaecin-type peptide antibiotics function through a non-poreforming mechanism involving stereospecificity Biochem. Biophys. Res. Commun. 199, 339-345
13. Piantavigna, S., Czihal, P., Mechler, A., Richter, M., Hoffmann, R., and Martin, L. L. (2009) Cell penetrating apidaecin peptide interactions with biomimetic phospholipid membranes Int. J. Pept. Res. Ther. 15, 139-146
14. Casteels, P., Romagnolo, J., Castle, M., Casteelsjosson, K., Erdjumentbromage, H., and Tempst, P. (1994) Biodiversity of apidaecin-type peptide antibiotics-prospects of manipulating the antibacterial spectrum and combating acquired-resistance J. Biol. Chem. 269, 26107-26115
15. Ostorhazi, E., Holub, M. C., Rozgonyi, F., Harmos, F., Cassone, M., Wade, J. D., and Otvos, L., Jr. (2011) Broad-spectrum antimicrobial efficacy of peptide A3-APO in mouse models of multidrug-resistant wound and lung infections cannot be explained by in vitro activity against the pathogens involved Int. J. Antimicrob. Agents 37, 480-484
16. Szabo, D., Ostorhazi, E., Binas, A., Rozgonyi, F., Kocsis, B., Cassone, M., Wade, J. D., Nolte, O., and Otvos, L. (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
17. Benincasa, M., Pelillo, C., Zorzet, S., Garrovo, C., Biffi, S., Gennaro, R., and Scocchi, M. (2010) The proline-rich peptide Bac7(1-35) reduces mortality from Salmonella typhimurium in a mouse model of infection BMC Microbiol. 10, 178
18. Knappe, D., Kabankov, N., and Hoffmann, R. (2011) Bactericidal oncocin derivatives with superior serum stabilities Int. J. Antimicrob. Agents 37, 166-170
19. Scocchi, M., Tossi, A., and Gennaro, R. (2011) Proline-rich antimicrobial peptides: converging to a non-lytic mechanism of action Cell. Mol. Life Sci. 68, 2317-2330
20. Otvos, L., O, I., Rogers, M. E., Consolvo, P. J., Condie, B. A., Lovas, S., Bulet, P., and Blaszczyk-Thurin, M. (2000) Interaction between heat shock proteins and antimicrobial peptides Biochemistry 39, 14150-14159
21. Morell, M., Czihal, P., Hoffmann, R., Otvos, L., Aviles, F. X., and Ventura, S. (2008) Monitoring the interference of protein-protein interactions in vivo by bimolecular fluorescence complementation: the DnaK case Proteomics 8, 3433-3442
22. Bukau, B. and Walker, G. C. (1989) Delta-Dnak52 mutants of Escherichia coli have defects in chromosome segregation and plasmid maintenance at normal growth temperatures J. Bacteriol. 171, 6030-6038
23. Knappe, D., Piantavigna, S., Hansen, A., Mechler, A., Binas, A., Nolte, O., Martin, L. L., and Hoffmann, R. (2010) Oncocin (VDKPPYLPRPRPPRRIYNR-NH2): A novel antibacterial peptide optimized against Gram-negative human pathogens J. Med. Chem. 53, 5240-5247
24. Mechler, A., Praporski, S., Atmuri, K., Boland, M., Separovic, F., and Martin, L. L. (2007) Specific and selective peptide-membrane interactions revealed using quartz crystal microbalance Biophys. J. 93, 3907-3916
25. McCubbin, G. A., Praporski, S., Piantavigna, S., Knappe, D., Hoffmann, R., Bowie, J. H., Separovic, F., and Martin, L. L. (2011) QCM-D fingerprinting of membrane-active peptides Eur. Biophys. J. Biophys. Lett. 40, 437-446
26. Sauerbrey, G. (1959) Verwendung Von Schwingquarzen Zur Wagung Dunner Schichten und Zur Mikrowagung Z. Phys. 155, 206-222
27. Knappe, D., Zahn, M., Sauer, U., Schiffer, G., Strater, N., and Hoffmann, R. (2011) Rational design of oncocin derivatives with superior protease stabilities and antibacterial activities based on the high-resolution structure of the oncocin-DnaK complex ChemBioChem 12, 874-876
28. Liebscher, M. and Roujeinikova, A. (2009) Allosteric coupling between the lid and interdomain linker in DnaK revealed by inhibitor binding studies J. Bacteriol. 191, 1456-1462
29. Tapley, T. L., Cupp-Vickery, J. R., and Vickery, L. E. (2005) Sequence-dependent peptide binding orientation by the molecular chaperone DnaK Biochemistry 44, 12307-12315
30. Zhou, Y. S. and Chen, W. N. (2011) iTRAQ-coupled 2-D LC-MS/MS analysis of cytoplasmic protein profile in Escherichia coli incubated with apidaecin IB J. Proteomics 75, 511-516
31. Zhou, Y. S. and Chen, W. N. (2011) iTRAQ-coupled 2-D LC-MS/MS analysis of membrane protein profile in Escherichia coli incubated with apidaecin IB Plos ONE 6, e20442
32. Van Dorpe, S., Bronselaer, A., Nielandt, J., Stalmans, S., Wynendaele, E., Audenaert, K., Van De Wiele, C., Burvenich, C., Peremans, K., Hsuchou, H., De Tre, G., and De Spiegeleer, B. (2011) Brainpeps: the blood-brain barrier peptide database Brain Struct. Funct. 10.1007/s00429-011-0375-0
33. Tavano, R., Segat, D., Gobbo, M., and Papini, E. (2011) The honeybee antimicrobial peptide apidaecin differentially immunomodulates human macrophages, monocytes and dendritic cells J. Innate Immun. 3, 614-622
34. van Ogtrop, M. L., Andes, D., Stamstad, T. J., Conklin, B., Weiss, W. J., Craig, W. A., and Vesga, O. (2000) In vivo pharmacodynamic activities of two glycylcyclines (GAR-936 and WAY 152,288) against various gram-positive and gram-negative bacteria Antimicrob. Agents Chemother. 44, 943-949
35. Andes, D. and Craig, W. A. (2006) Pharmacodynamics of a new cephalosporin, PPI-0903 (TAK-599), active against methicillin-resistant Staphylococcus aureus in murine thigh and lung infection models: Identification of an in vivo pharmacokinetic-pharmacodynamic target Antimicrob. Agents Chemother. 50, 1376-1383
36. Biragyn, A., Surenhu, M., Yang, D., Ruffini, P. A., Haines, B. A., Klyushnenkova, E., Oppenheim, J. J., and Kwak, L. W. (2001) Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens J. Immunol. 167, 6644-6653
37. Biragyn, A., Ruffini, P. A., Leifer, C. A., Klyushnenkova, E., Shakhov, A., Chertov, O., Shirakawa, A. K., Farber, J. M., Segal, D. M., Oppenheim, J. J., and Kwak, L. W. (2002) Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2 Science 298, 1025-1029
38. Biragyn, A., Coscia, M., Nagashima, K., Sanford, M., Young, H. A., and Olkhanud, P. (2008) Murine beta-defensin 2 promotes TLR-4/MyD88-mediated and NF-kappa B-dependent atypical death of APCs via activation of TNFR2 J. Leukocyte Biol. 83, 998-1008
39. Funderburg, N., Lederman, M. M., Feng, Z., Drage, M. G., Jacllowsky, J., Harding, C. V., Weinberg, A., and Sieg, S. F. (2007) Human beta-defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2 Proc. Natl. Acad. Sci. U.S.A. 104, 18631-18635
40. Kandler, K., Shaykhiev, R., Kleemann, P., Klescz, F., Lohoff, M., Vogelmeier, C., and Bals, R. (2006) The anti-microbial peptide LL-37 inhibits the activation of dendritic cells by TLR ligands Int. Immunol. 18, 1729-1736
41. Semple, F., Webb, S., Li, H. N., Patel, H. B., Perretti, M., Jackson, I. J., Gray, M., Davidson, D. J., and Dorin, J. R. (2010) Human beta-defensin 3 has immunosuppressive activity in vitro and in vivo Eur. J. Immunol. 40, 1073-1078
42. Singer, D., Zauner, T., Genz, M., Hoffmann, R., and Zuchner, T. (2010) Synthesis of pathological and nonpathological human exon 1 huntingtin J. Pept. Sci. 16, 358-363
43. Gausepohl, H., Pieles, U., and Frank, R. W. (1992) in Peptides-Chemistry and Biology: Proceedings of the 12th American Peptide Symposium (Smith, J. A. and Rivier, J. E., Eds.) pp 523-524, ESCOM Science, Leiden.
44. Zhu, X. T., Zhao, X., Burkholder, W. F., Gragerov, A., Ogata, C. M., Gottesman, M. E., and Hendrickson, W. A. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK Science 272, 1606-1614
45. Kabsch, W. (2010) XDS Acta Crystallogr., Sect. D: Biol. Crystallogr 66, 125-132
46. Bailey, S. (1994) The Ccp4 suite-programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763
47. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025
48. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
49. Murshudov, G. N., Skubak, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 355-367
50. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival-application to proliferation and cyto-toxicity assays J. Immunol. Methods 65, 55-63
51. Cook, J. A. and Mitchell, J. B. (1989) Viability measurements in mammalian-cell systems Anal. Biochem. 179, 1-7
52. Gobbo, M., Benincasa, M., Bertoloni, G., Biondi, B., Dosselli, R., Papini, E., Reddi, E., Rocchi, R., Tavano, R., and Gennaro, R. (2009) Substitution of the arginine/leucine residues in apidaecin Ib with peptoid residues: Effect on antimicrobial activity, cellular uptake, and proteolytic degradation J. Med. Chem. 52, 5197-5206
53. Gjedde, A. (1981) High-affinity and low-affinity transport of d -glucose from blood to brain J. Neurochem. 36, 1463-1471
54. Triguero, D., Buciak, J., and Pardridge, W. M. (1990) Capillary depletion method for quantification of blood-brain-barrier transport of circulating peptides and plasma-proteins J. Neurochem. 54, 1882-1888
55. Gutierrez, E. G., Banks, W. A., and Kastin, A. J. (1993) Murine tumor-necrosis-factor-alpha is transported from blood to brain in the mouse J. Neuroimmunol. 47, 169-176
56. Frimodt-Moller, N., Knudsen, J. D., and Espersen, F. (1999) Handbook of Animal Models of Infection, Academic Press, London.