Absence of in vitro innate immunomodulation by insect-derived short proline-rich antimicrobial peptides points to direct antibacterial action in vivo

Journal of Peptide Science

Volumn 18, Issue 10, 2012, Pages 599-608

  Fritsche, Stefanie ^a   Knappe, Daniel ^a   Berthold, Nicole ^a   Von Buttlar, Heiner ^a   Hoffmann, Ralf ^a   Alber, Gottfried ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Apidaecin; Immunomodulation; Oncocin; Proline rich antimicrobial peptides

Indexed keywords

APIDAECIN DERIVATIVE; CATHELICIDIN; ONCOCIN DERIVATIVE; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; DENDRITIC CELL; IMMUNOMODULATION; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BEES; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; FEMALE; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; PROLINE;

BACTERIA (MICROORGANISMS); HEXAPODA; MURINAE;

EID: 84866444887     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.2440     Document Type: Article

References (65)

1. Fjell CD, Hiss JA, Hancock RE, Schneider G. Designing antimicrobial peptides: form follows function. Nat. Rev. Drug. Discov. 2012; 11: 37-51.
2. Loutet SA, Valvano MA. Extreme antimicrobial Peptide and polymyxin B resistance in the genus burkholderia. Front Microbiol. 2011; 2: 159.
3. Otvos L, Jr. The short proline-rich antibacterial peptide family. Cell. Mol. Life Sci. 2002; 59: 1138-1150.
4. Bulet P, Dimarcq JL, Hetru C, Lagueux M, Charlet M, Hegy G, Van DA, Hoffmann JA. A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J. Biol. Chem. 1993; 268: 14893-14897.
5. Casteels P, Ampe C, Jacobs F, Vaeck M, Tempst P. Apidaecins: antibacterial peptides from honeybees. EMBO J. 1989; 8: 2387-2391.
6. Cociancich S, Dupont A, Hegy G, Lanot R, Holder F, Hetru C, Hoffmann JA, Bulet P. Novel inducible antibacterial peptides from a hemipteran insect, the sap-sucking bug Pyrrhocoris apterus. Biochem. J. 1994; 300(Pt 2): 567-575.
7. Schneider M, Dorn A. Differential infectivity of two Pseudomonas species and the immune response in the milkweed bug, Oncopeltus fasciatus (Insecta: Hemiptera). J. Invertebr. Pathol. 2001; 78: 135-140.
8. Otvos L, Jr., Wade JD, Lin F, Condie BA, Hanrieder J, Hoffmann R. Designer antibacterial peptides kill fluoroquinolone-resistant clinical isolates. J. Med. Chem. 2005; 48: 5349-5359.
9. Giacometti A, Cirioni O, Del Prete MS, Skerlavaj B, Circo R, Zanetti M, Scalise G. In vitro effect on Cryptosporidium parvum of short-term exposure to cathelicidin peptides. J. Antimicrob. Chemother. 2003; 51: 843-847.
10. Knappe D, Piantavigna S, Hansen A, Mechler A, Binas A, Nolte O, Martin LL, Hoffmann R. Oncocin (VDKPPYLPRPRPPRRIYNR-NH2): a novel antibacterial peptide optimized against gram-negative human pathogens. J. Med. Chem. 2010; 53: 5240-5247.
11. Czihal P, Knappe D, Fritsche S, Zahn M, Berthold N, Piantavigna S, Muller U, Van DS, Herth N, Binas A, Kohler G, De SB, Martin LL, Nolte O, Strater N, Alber G, Hoffmann R. Api88 is a novel antibacterial designer peptide to treat systemic infections with multidrug-resistant gram-negative pathogens. ACS Chem. Biol. 2012; 7: 1281-1291.
12. Knappe D, Fritsche S, Alber G, Koehler G, Hoffmann R, Mueller U. Oncocin derivative Onc72 is highly active against Escherichia coli in a systemic septicaemia infection mouse model. J. Antimicrob. Chemother. 2012; doi: 10.1093/jac/dks241.
13. Knappe D, Kabankov N, Hoffmann R. Bactericidal oncocin derivatives with superior serum stabilities. Int. J. Antimicrob. Agents 2011; 37: 166-170.
14. Knappe D, Zahn M, Sauer U, Schiffer G, Strater N, Hoffmann R. Rational design of oncocin derivatives with superior protease stabilities and antibacterial activities based on the high-resolution structure of the oncocin-DnaK complex. Chembiochem 2011; 12: 874-876.
15. Liebscher M, Roujeinikova A. Allosteric coupling between the lid and interdomain linker in DnaK revealed by inhibitor binding studies. J. Bacteriol. 2009; 191: 1456-1462.
16. Otvos L, Jr., O I, Rogers ME, Consolvo PJ, Condie BA, Lovas S, Bulet P, Blaszczyk-Thurin M. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 2000; 39: 14150-14159.
17. Benincasa M, Pelillo C, Zorzet S, Garrovo C, Biffi S, Gennaro R, Scocchi M. The proline-rich peptide Bac7(1-35) reduces mortality from Salmonella typhimurium in a mouse model of infection. BMC Microbiol. 2010; 10: 178.
18. Szabo D, Ostorhazi E, Binas A, Rozgonyi F, Kocsis B, Cassone M, Wade JD, Nolte O, Otvos L, Jr. The designer proline-rich antibacterial peptide A3-APO is effective against systemic Escherichia coli infections in different mouse models. Int. J. Antimicrob. Agents 2010; 35: 357-361.
19. Navid F, Boniotto M, Walker C, Ahrens K, Proksch E, Sparwasser T, Muller W, Schwarz T, Schwarz A. Induction of regulatory T cells by a murine beta-defensin. J. Immunol. 2012; 188: 735-743.
20. Biragyn A, Surenhu M, Yang D, Ruffini PA, Haines BA, Klyushnenkova E, Oppenheim JJ, Kwak LW. Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J. Immunol. 2001; 167: 6644-6653.
21. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schroder JM, Wang JM, Howard OM, Oppenheim JJ. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999; 286: 525-528.
22. Heilborn JD, Nilsson MF, Kratz G, Weber G, Sorensen O, Borregaard N, Stahle-Backdahl M. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J. Invest. Dermatol. 2003; 120: 379-389.
23. Koczulla R, von DG, Kupatt C, Krotz F, Zahler S, Gloe T, Issbrucker K, Unterberger P, Zaiou M, Lebherz C, Karl A, Raake P, Pfosser A, Boekstegers P, Welsch U, Hiemstra PS, Vogelmeier C, Gallo RL, Clauss M, Bals R. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J. Clin. Invest. 2003; 111: 1665-1672.
24. Scott MG, Davidson DJ, Gold MR, Bowdish D, Hancock RE. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol. 2002; 169: 3883-3891.
25. Tjabringa GS, Aarbiou J, Ninaber DK, Drijfhout JW, Sorensen OE, Borregaard N, Rabe KF, Hiemstra PS. The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J. Immunol. 2003; 171: 6690-6696.
26. Yang D, de la RG, Tewary P, Oppenheim JJ. Alarmins link neutrophils and dendritic cells. Trends Immunol. 2009; 30: 531-537.
27. Alalwani SM, Sierigk J, Herr C, Pinkenburg O, Gallo R, Vogelmeier C, Bals R. The antimicrobial peptide LL-37 modulates the inflammatory and host defense response of human neutrophils. Eur. J. Immunol. 2010; 40: 1118-1126.
28. Kandler K, Shaykhiev R, Kleemann P, Klescz F, Lohoff M, Vogelmeier C, Bals R. The anti-microbial peptide LL-37 inhibits the activation of dendritic cells by TLR ligands. Int. Immunol. 2006; 18: 1729-1736.
29. Kandler K. 2006. Cathelizidine als Immunmodulatoren der angeborenen Immunität (Dissertation).
30. Kurosaka K, Chen Q, Yarovinsky F, Oppenheim JJ, Yang D. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J. Immunol. 2005; 174: 6257-6265.
31. Pinheiro da Silva F, Gallo RL, Nizet V. Differing effects of exogenous or endogenous cathelicidin on macrophage toll-like receptor signaling. Immunol. Cell Biol. 2009; 87: 496-500.
32. Tavano R, Segat D, Gobbo M, Papini E. The honeybee antimicrobial Peptide apidaecin differentially immunomodulates human macrophages, monocytes and dendritic cells. J. Innate Immun. 2011; 3: 614-622.
33. Asselin-Paturel C, Boonstra A, Dalod M, Durand I, Yessaad N, Zutter-Dambuyant C, Vicari A, O'Garra A, Biron C, Briere F, Trinchieri G. Mouse type I IFN-producing cells are imature APCs with plasmacytoid morphology. Nat. Immunol. 2001; 2: 1144-1150.
34. Brawand P, Fitzpatrick DR, Greenfield BW, Brasel K, Maliszewski CR, De ST. Murine plasmacytoid pre-dendritic cells generated from Flt3 ligand-supplemented bone marrow cultures are immature APCs. J. Immunol. 2002; 169: 6711-6719.
35. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, Colonna M. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 1999; 5: 919-923.
36. Lembo A, Kalis C, Kirschning CJ, Mitolo V, Jirillo E, Wagner H, Galanos C, Freudenberg MA. Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar Typhimurium and Staphylococcus aureus in mice. Infect. Immun. 2003; 71: 6058-6062.
37. Naik SH, Proietto AI, Wilson NS, Dakic A, Schnorrer P, Fuchsberger M, Lahoud MH, O'Keeffe M, Shao QX, Chen WF, Villadangos JA, Shortman K, Wu L. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 2005; 174: 6592-6597.
38. Caminschi I, Lahoud MH, Shortman K. Enhancing immune responses by targeting antigen to DC. Eur. J. Immunol. 2009; 39: 931-938.
39. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008; 8: 958-969.
40. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011; 11: 723-737.
41. Gausepohl H, Pieles H, Frank RW. In Peptides: Chemistry, Structure and Biology, Smith JA, Rivier JE (eds). ESCOM: Leiden, 1992; 523.
42. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, Chertov O, Shirakawa AK, Farber JM, Segal DM, Oppenheim JJ, Kwak LW. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 2002; 298: 1025-1029.
43. Funderburg N, Lederman MM, Feng Z, Drage MG, Jadlowsky J, Harding CV, Weinberg A, Sieg SF. Human -defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2. Proc. Natl. Acad. Sci. U. S. A. 2007; 104: 18631-18635.
44. Funderburg NT, Jadlowsky JK, Lederman MM, Feng Z, Weinberg A, Sieg SF. The Toll-like receptor 1/2 agonists Pam(3) CSK(4) and human beta-defensin-3 differentially induce interleukin-10 and nuclear factor-kappaB signalling patterns in human monocytes. Immunology 2011; 134: 151-160.
45. Biragyn A, Coscia M, Nagashima K, Sanford M, Young HA, Olkhanud P. Murine beta-defensin 2 promotes TLR-4/MyD88-mediated and NF-kappaB-dependent atypical death of APCs via activation of TNFR2. J. Leukoc. Biol. 2008; 83: 998-1008.
46. Yang Y, Jiang Y, Yin Q, Liang H, She R. Chicken intestine defensins activated murine peripheral blood mononuclear cells through the TLR4-NF-kappaB pathway. Vet. Immunol. Immunopathol. 2010; 133: 59-65.
47. Niyonsaba F, Iwabuchi K, Someya A, Hirata M, Matsuda H, Ogawa H, Nagaoka I. A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis. Immunology 2002; 106: 20-26.
48. Taylor K, Rolfe M, Reynolds N, Kilanowski F, Pathania U, Clarke D, Yang D, Oppenheim J, Samuel K, Howie S, Barran P, Macmillan D, Campopiano D, Dorin J. Defensin-related peptide 1 (Defr1) is allelic to Defb8 and chemoattracts immature DC and CD4+ T cells independently of CCR6. Eur. J. Immunol. 2009; 39: 1353-1360.
49. Tjabringa GS, Ninaber DK, Drijfhout JW, Rabe KF, Hiemstra PS. Human cathelicidin LL-37 is a chemoattractant for eosinophils and neutrophils that acts via formyl-peptide receptors. Int. Arch. Allergy Immunol. 2006; 140: 103-112.
50. Dieu-Nosjean MC, Vicari A, Lebecque S, Caux C. Regulation of dendritic cell trafficking: a process that involves the participation of selective chemokines. J. Leukoc. Biol. 1999; 66: 252-262.
51. Semple F, Webb S, Li HN, Patel HB, Perretti M, Jackson IJ, Gray M, Davidson DJ, Dorin JR. Human beta-defensin 3 has immunosuppressive activity in vitro and in vivo. Eur. J. Immunol. 2010; 40: 1073-1078.
52. Yoshiyama, M. 2008. Innate immune system in the honey bee. In 8th Conference of Science Council of Asia in China, Vol. Shangri-La Hotel Qingdao, China.
53. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 2006; 15: 645-656.
54. Muller U, Vogel P, Alber G, Schaub GA. The innate immune system of mammals and insects. Contrib. Microbiol. 2008; 15: 21-44.
55. Bukau B, Walker GC. Delta dnaK52 mutants of Escherichia coli have defects in chromosome segregation and plasmid maintenance at normal growth temperatures. J. Bacteriol. 1989; 171: 6030-6038.
56. Bardwell JC, Craig EA. Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proc. Natl. Acad. Sci. U. S. A. 1984; 81: 848-852.
57. Kragol G, Hoffmann R, Chattergoon MA, Lovas S, Cudic M, Bulet P, Condie BA, Rosengren KJ, Montaner LJ, Otvos L, Jr. Identification of crucial residues for the antibacterial activity of the proline-rich peptide, pyrrhocoricin. Eur. J. Biochem. 2002; 269: 4226-4237.
58. Otvos L, Jr., Cudic M, Chua BY, Deliyannis G, Jackson DC. An insect antibacterial peptide-based drug delivery system. Mol. Pharm. 2004; 1: 220-232.
59. Tomasinsig L, Skerlavaj B, Papo N, Giabbai B, Shai Y, Zanetti M. Mechanistic and functional studies of the interaction of a proline-rich antimicrobial peptide with mammalian cells. J. Biol. Chem. 2006; 281: 383-391.
60. Gallo RL, Kim KJ, Bernfield M, Kozak CA, Zanetti M, Merluzzi L, Gennaro R. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J. Biol. Chem. 1997; 272: 13088-13093.
61. Gennaro R, Zanetti M. Structural features and biological activities of the cathelicidin-derived antimicrobial peptides. Biopolymers 2000; 55: 31-49.
62. Montreekachon P, Chotjumlong P, Bolscher JG, Nazmi K, Reutrakul V, Krisanaprakornkit S. Involvement of P2X(7) purinergic receptor and MEK1/2 in interleukin-8 up-regulation by LL-37 in human gingival fibroblasts. J. Periodontal Res. 2011; 46: 327-337.
63. Huang HJ, Ross CR, Blecha F. Chemoattractant properties of PR-39, a neutrophil antibacterial peptide. J. Leukoc. Biol. 1997; 61: 624-629.
64. Yu PL, Cross ML, Haverkamp RG. Antimicrobial and immunomodulatory activities of an ovine proline/arginine-rich cathelicidin. Int. J. Antimicrob. Agents 2010; 35: 288-291.
65. Dutta RC, Nagpal S, Salunke DM. Functional mapping of apidaecin through secondary structure correlation. Int. J. Biochem. Cell Biol. 2008; 40: 1005-1015.