Lipopolysaccharide neutralization by antimicrobial peptides: A gambit in the innate host defense strategy

Journal of Innate Immunity

Volumn 4, Issue 4, 2012, Pages 327-336

  Pulido, David ^a   Nogús, M Victòria ^a   Boix, Ester ^a   Torrent, Marc ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Antibacterial peptides; Antimicrobial peptides; Endotoxin; Host defense; Immune response; Pathogen associated molecular patterns; Pattern recognition receptors; Peptide design; Peptide structure activity relationship; Sepsis; Septic shock; Toll like receptor

Indexed keywords

CD14 ANTIGEN; ENDOTOXIN; HIGH DENSITY LIPOPROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; LIPID TRANSFER PROTEIN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; NITRIC OXIDE; POLYPEPTIDE ANTIBIOTIC AGENT; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA;

ALPHA HELIX; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG BINDING; GENE EXPRESSION; GRAM NEGATIVE BACTERIUM; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; REVIEW; SEPTIC SHOCK; SEPTICEMIA; TISSUE INJURY;

ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; HUMANS; IMMUNITY, INNATE; INFECTION; LIPOPOLYSACCHARIDES; MODELS, MOLECULAR; NEUTRALIZATION TESTS;

EID: 84863332845     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000336713     Document Type: Review

References (64)

1. Murphy K: Janeway's Immunobiology, ed 8. New York, Garland Science, 2011.
2. Janeway CA Jr, Medzhitov R: Introduction: the role of innate immunity in the adaptive immune response. Semin Immunol 1998; 10: 349-350.
3. Cohen J: The immunopathogenesis of sepsis. Nature 2002; 420: 885-891.
4. Zhang X, Mosser DM: Macrophage activation by endogenous danger signals. J Pathol 2008; 214: 161-178.
5. Israelachvili JN: Intermolecular and Surface Forces, ed 3. London, Academic Press, 2010.
6. Seydel U, Wiese A, Schromm AB, Brandenburg K: A biophysical view in the function and activity of endotoxins; in Brade H, Opal S, Vogel S, Morrison Deds): Endotoxin in Health and Disease. New York, Academic Press, 1999, pp 195-220.
7. Mueller M, Lindner B, Dedrick R, Schromm AB, Seydel U: Endotoxin: physical requirements for cell activation. J Endotoxin Res 2005; 11: 299-303.
8. Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ: Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 1992; 101: 1644-1655.
9. Wimley WC: Describing the mechanism of antimicrobial peptide action with the interfacial activity model. ACS Chem Biol 2010; 5: 905-917.
10. Jenssen H, Hamill P, Hancock RE: Peptide antimicrobial agents. Clin Microbiol Rev 2006; 19: 491-511.
11. Hancock RE, Diamond G: The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol 2000; 8: 402-410.
12. Zaiou M: Multifunctional antimicrobial peptides: therapeutic targets in several human diseases. J Mol MedBerl) 2007; 85: 317-329.
13. Bhunia A, Mohanram H, Bhattacharjya S: Lipopolysaccharide bound structures of the active fragments of fowlicidin-1, a cathelicidin family of antimicrobial and antiendotoxic peptide from chicken, determined by transferred nuclear Overhauser effect spectroscopy. Biopolymers 2009; 92: 9-22.
14. Tack BF, Sawai MV, Kearney WR, Robertson AD, Sherman MA, Wang W, Hong T, Boo LM, Wu H, Waring AJ, Lehrer RI: SMAP-29 has two LPS-binding sites and a central hinge. Eur J Biochem 2002; 269: 1181-1189.
15. 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.
16. Bhunia A, Saravanan R, Mohanram H, Mangoni ML, Bhattacharjya S: NMR structures and interactions of temporin-1Tl and temporin- 1Tb with lipopolysaccharide micelles: mechanistic insights into outer membrane permeabilization and synergistic activity. J Biol Chem 2011; 286: 24394-24406.
17. Bhunia A, Ramamoorthy A, Bhattacharjya S: Helical hairpin structure of a potent antimicrobial peptide MSI-594 in lipopolysaccharide micelles by NMR spectroscopy. Chemistry 2009; 15: 2036-2040.
18. Almeida PF, Pokorny A: Mechanisms of antimicrobial, cytolytic, and cell-penetrating peptides: from kinetics to thermodynamics. Biochemistry 2009; 48: 8083-8093.
19. McKeown AN, Naro JL, Huskins LJ, Almeida PF: A thermodynamic approach to the mechanism of cell-penetrating peptides in model membranes. Biochemistry 2011; 50: 654-662.
20. Majerle A, Pristovsek P, Mancek-Keber M, Jerala R: Interaction of the HIV-1 gp120 viral protein V3 loop with bacterial lipopolysaccharide: a pattern recognition inhibition. J Biol Chem 2011; 286: 26228-26237.
21. Su Y, Waring AJ, Ruchala P, Hong M: Structures of beta-hairpin antimicrobial protegrin peptides in lipopolysaccharide membranes: mechanism of Gram selectivity obtained from solid-state nuclear magnetic resonance. Biochemistry 2011; 50: 2072-2083.
22. Zhang L, Dhillon P, Yan H, Farmer S, Hancock RE: Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrob Agents Chemother 2000; 44: 3317-3321.
23. Moore RA, Hancock RE: Involvement of outer membrane of Pseudomonas cepacia in aminoglycoside and polymyxin resistance. Antimicrob Agents Chemother 1986; 30: 923-926.
24. Rosenfeld Y, Sahl HG, Shai Y: Parameters involved in antimicrobial and endotoxin detoxification activities of antimicrobial peptides. Biochemistry 2008; 47: 6468-6478.
25. Rosenfeld Y, Lev N, Shai Y: Effect of the hydrophobicity to net positive charge ratio on antibacterial and anti-endotoxin activities of structurally similar antimicrobial peptides. Biochemistry 2010; 49: 853-861.
26. Chapple DS, Hussain R, Joannou CL, Hancock RE, Odell E, Evans RW, Siligardi G: Structure and association of human lactoferrin peptides with Escherichia coli lipopolysaccharide. Antimicrob Agents Chemother 2004; 48: 2190-2198.
27. Gough M, Hancock RE, Kelly NM: Antiendotoxin activity of cationic peptide antimicrobial agents. Infect Immun 1996; 64: 4922-4927.
28. Scott MG, Vreugdenhil AC, Buurman WA, Hancock RE, Gold MR: Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharideLPS) to LPS binding protein. J Immunol 2000; 164: 549-553.
29. Bhunia A, Mohanram H, Domadia PN, Torres J, Bhattacharjya S: Designed beta-boomerang antiendotoxic and antimicrobial peptides: structures and activities in lipopolysaccharide. J Biol Chem 2009; 284: 21991-22004.
30. Domadia PN, Bhunia A, Ramamoorthy A, Bhattacharjya S: Structure, interactions, and antibacterial activities of MSI-594 derived mutant peptide MSI-594F5A in lipopolysaccharide micelles: role of the helical hairpin conformation in outer-membrane permeabilization. J Am Chem Soc 2010; 132: 18417-18428.
31. Torrent M, Andreu D, Nogues VM, Boix E: Connecting peptide physicochemical and antimicrobial properties by a rational prediction model. PLoS One 2011; 6:e16968.
32. Torrent M, Valle J, Nogues MV, Boix E, Andreu D: The generation of antimicrobial peptide activity: a trade-off between charge and aggregation? Angew Chem Int Ed Engl 2011; 50: 10686-10689.
33. Kaconis Y, Kowalski I, Howe J, Brauser A, Richter W, Razquin-Olazaran I, Inigo-Pestana M, Garidel P, Rossle M, Martinez de Tejada G, Gutsmann T, Brandenburg K: Biophysical mechanisms of endotoxin neutralization by cationic amphiphilic peptides. Biophys J 2011; 100: 2652-2661.
34. Mares J, Kumaran S, Gobbo M, Zerbe O: Interactions of lipopolysaccharide and polymyxin studied by NMR spectroscopy. J Biol Chem 2009; 284: 11498-11506.
35. Bhunia A, Bhattacharjya S: Mapping residue- specific contacts of polymyxin B with lipopolysaccharide by saturation transfer difference NMR: insights into outer-membrane disruption and endotoxin neutralization. Biopolymers 2011; 96: 273-287.
36. Mangoni ML, Epand RF, Rosenfeld Y, Peleg A, Barra D, Epand RM, Shai Y: Lipopolysaccharide, a key molecule involved in the synergism between temporins in inhibiting bacterial growth and in endotoxin neutralization. J Biol Chem 2008; 283: 22907-22917.
37. Howe J, Andra J, Conde R, Iriarte M, Garidel P, Koch MH, Gutsmann T, Moriyon I, Brandenburg K: Thermodynamic analysis of the lipopolysaccharide- dependent resistance of Gram-negative bacteria against polymyxin B. Biophys J 2007; 92: 2796-2805.
38. Thomas CJ, Surolia N, Surolia A: Kinetic and thermodynamic analysis of the interactions of 23-residue peptides with endotoxin. J Biol Chem 2001; 276: 35701-35706.
39. Corradin SB, Mauel J, Gallay P, Heumann D, Ulevitch RJ, Tobias PS: Enhancement of murine macrophage binding of and response to bacterial lipopolysaccharideLPS) by LPSbinding protein. J Leukoc Biol 1992; 52: 363-368.
40. Gutsmann T, Muller M, Carroll SF, MacKenzie RC, Wiese A, Seydel U: Dual role of lipopolysaccharideLPS)-binding protein in neutralization of LPS and enhancement of LPS-induced activation of mononuclear cells. Infect Immun 2001; 69: 6942-6950.
41. Thompson PA, Kitchens RL: Native highdensity lipoprotein augments monocyte responses to lipopolysaccharideLPS) by suppressing the inhibitory activity of LPS-binding protein. J Immunol 2006; 177: 4880-4887.
42. Wu X, Qian G, Zhao Y, Xu D: LBP inhibitory peptide reduces endotoxin-induced macrophage activation and mortality. Inflamm Res 2005; 54: 451-457.
43. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC: CD14, a receptor for complexes of lipopolysaccharideLPS) and LPS binding protein. Science 1990; 249: 1431-1433.
44. Kim JI, Lee CJ, Jin MS, Lee CH, Paik SG, Lee H, Lee JO: Crystal structure of CD14 and its implications for lipopolysaccharide signaling. J Biol Chem 2005; 280: 11347-11351.
45. Tapping RI, Tobias PS: Cellular binding of soluble CD14 requires lipopolysaccharideLPS) and LPS-binding protein. J Biol Chem 1997; 272: 23157-23164.
46. Kitchens RL, Thompson PA, Viriyakosol S, O'Keefe GE, Munford RS: Plasma CD14 decreases monocyte responses to LPS by transferring cell-bound LPS to plasma lipoproteins. J Clin Invest 2001; 108: 485-493.
47. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ: Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil- derived neurotoxin in host defense. Annu Rev Immunol 2004; 22: 181-215.
48. Bowdish DM, Davidson DJ, Lau YE, Lee K, Scott MG, Hancock RE: Impact of LL-37 on anti-infective immunity. J Leukoc Biol 2005; 77: 451-459.
49. Koyama Y, Motobu M, Hikosaka K, Yamada M, Nakamura K, Saido-Sakanaka H, Asaoka A, Yamakawa M, Sekikawa K, Kitani H, Shimura K, Nakai Y, Hirota Y: Protective effects of antimicrobial peptides derived from the beetle Allomyrina dichotoma defensin on endotoxic shock in mice. Int Immunopharmacol 2006; 6: 234-240.
50. Schultz H, Weiss JP: The bactericidal/permeability- increasing proteinBPI) in infection and inflammatory disease. Clin Chim Acta 2007; 384: 12-23.
51. O'Neill L: The Toll/interleukin-1 receptor domain: a molecular switch for inflammation and host defence. Biochem Soc Trans 2000; 28: 557-563.
52. Lu YC, Yeh WC, Ohashi PS: LPS/TLR4 signal transduction pathway. Cytokine 2008; 42: 145-151.
53. Prohinar P, Re F, Widstrom R, Zhang D, Teghanemt A, Weiss JP, Gioannini TL: Specific high affinity interactions of monomeric endotoxin. Protein complexes with Toll-like receptor 4 ectodomain. J Biol Chem 2007; 282: 1010-1017.
54. Gioannini TL, Teghanemt A, Zhang D, Coussens NP, Dockstader W, Ramaswamy S, Weiss JP: Isolation of an endotoxin-MD-2 complex that produces Toll-like receptor 4-dependent cell activation at picomolar concentrations. Proc Natl Acad Sci USA 2004; 101: 4186-4191.
55. Di Nardo A, Braff MH, Taylor KR, Na C, Granstein RD, McInturff JE, Krutzik S, Modlin RL, Gallo RL: Cathelicidin antimicrobial peptides block dendritic cell TLR4 activation and allergic contact sensitization. J Immunol 2007; 178: 1829-1834.
56. Romano Carratelli C, Mazzola N, Paolillo R, Sorrentino S, Rizzo A: Toll-like receptor-4TLR4) mediates human beta-defensin-2HBD-2) induction in response to chlamydia pneumoniae in mononuclear cells. FEMS Immunol Med Microbiol 2009; 57: 116-124.
57. Mookherjee N, Brown KL, Bowdish DM, Doria S, Falsafi R, Hokamp K, Roche FM, Mu R, Doho GH, Pistolic J, Powers JP, Bryan J, Brinkman FS, Hancock RE: Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J Immunol 2006; 176: 2455-2464.
58. Torrent M, Nogues MV, Boix E: Eosinophil cationic proteinECP) can bind heparin and other glycosaminoglycans through its RNase active site. J Mol Recognit 2011; 24: 90-100.
59. Guo JX, Wood SJ, David SA, Lushington GH: Molecular modeling analysis of the interaction of novel bis-cationic ligands with the lipid A moiety of lipopolysaccharide. Bioorg Med Chem Lett 2006; 16: 714-717.
60. Bahl N, Du R, Winarsih I, Ho B, Tucker-Kellogg L, Tidor B, Ding JL: Delineation of lipopolysaccharideLPS)-binding sites on hemoglobin: from in silico predictions to biophysical characterization. J Biol Chem 2011; 286: 37793-37803.
61. Wasiluk KR, Leslie DB, Vietzen PS, Mayo KH, Dunn DL: Structure/function studies of an endotoxin-neutralizing peptide derived from bactericidal/ permeability-increasing protein. Surgery 2004; 136: 253-260.
62. Bruschi M, Pirri G, Giuliani A, Nicoletto SF, Baster I, Scorciapino MA, Casu M, Rinaldi AC: Synthesis, characterization, antimicrobial activity and LPS-interaction properties of SB041, a novel dendrimeric peptide with antimicrobial properties. Peptides 2010; 31: 1459-1467.
63. Epand RF, Mor A, Epand RM: Lipid complexes with cationic peptides and oaks; their role in antimicrobial action and in the delivery of antimicrobial agents. Cell Mol Life Sci 2011; 68: 2177-2188.
64. Ferguson AD, Kodding J, Walker G, Bos C, Coulton JW, Diederichs K, Braun V, Welte W: Active transport of an antibiotic rifamycin derivative by the outer-membrane protein FhuA. Structure 2001; 9: 707-716.