De novo designed lipopolysaccharide binding peptides: Structure based development of antiendotoxic and antimicrobial drugs

Current Medicinal Chemistry

Volumn 17, Issue 27, 2010, Pages 3080-3093

  Bhattacharjya, S ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Antimicrobial peptide; De novo designed peptide; Endotoxin; Lipopolysaccharide; NMR; Sepsis; STD NMR; tr NOE

Indexed keywords

ALPHA DEFENSIN; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; BETA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CD14 ANTIGEN; DEFB 123; ERITORAN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN GG8WF; PROTEIN MD 2; PROTEIN YI12AA; PROTEIN YI12LL; PROTEIN YI12WF; PROTEIN YI12WW; PROTEIN YI12WY; PROTEIN YW12; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CELL ACTIVATION; HUMAN; IC 50; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; ISOTHERMAL TITRATION CALORIMETRY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERMEABILITY BARRIER; PROTEIN INTERACTION; PROTEIN SYNTHESIS; SEPTIC SHOCK; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

EID: 77955600292     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986710791959756     Document Type: Article

References (139)

1. Mozharov, A.D.; Shchipakin, V.N.; Fishov, I.L.; Evtodienko Y. V. Changes in the composition of membrane phospholipids during the cell cycle of Escherichia coli. FEBS Lett., 1985, 186, 103-106.
2. Zerrouk, Z.; Alexandre, S.; Lafontaine, C.; Norris, V.; Valleton, J.M. Inner membrane lipids of Escherichia coli form domains. Colloids Surf B Biointerfaces, 2008, 63, 306-310.
3. Cronan, J.E. Bacterial membrane lipids: where do we stand? Annu. Rev. Microbiol., 2003, 57, 203-224.
4. Raetz, C.R. Biochemistry of endotoxin. Annu. Rev. Biochem., 1990, 59, 129-170.
5. Raetz, C.R.; Whitfield, C. Lipopolysaccharide endotoxin. Annu. Rev. Biochem., 2002, 71, 635-700.
6. Rietschel, E.T.; Kirikae, T.; Schade, F.U.; Mamat, U.; Schmidt, G.; Loppnow, H.; Ulmer, A. J.; Zahringer, U.; Seydel, U.; Di Padova, F.; et al. Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J., 1994, 8, 217-225.
7. Snyder, S.; Kim, D.; McIntosh, T.J. Lipopolysaccharide bilayer structure: effect of chemotype, core mutations, divalent cations, and temperature. Biochemistry, 1999, 38, 10758-10767.
8. Snyder, D.S.; McIntosh, T.J. The lipopolysaccharide barrier: correlation of antibiotic susceptibility with antibiotic permeability and fluorescent probe binding kinetics. Biochemistry, 2000, 39, 11777-11787.
9. Labischinski, H.; Barnickel, G.; Bradaczek, H.; Naumann, D.; Rietschel, E.T.; Giesbrecht, P. High state of order of isolated bacterial lipopolysaccharide and its possible contribution to the permeation barrier property of the outer membrane. J. Bacteriol., 1985, 162, 9-20.
10. Hancock, R.E. Alterations in outer membrane permeability. Annu. Rev. Microbiol., 1984, 38, 237-264.
11. Stan-Lotter, H.; Gupta, M.; Sanderson, K.E. The influence of cations on the permeability of the outer membrane of Salmonella typhimurium and other gram-negative bacteria. Can. J. Microbiol., 1979, 25, 475-485.
12. Parker, C.T.; Kloser, A.W.; Schnaitman, C.A.; Stein, M.A.; Gottesman, S.; Gibson, B.W. Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12. J Bacteriol., 1992, 174, 2525-2538.
13. Allende, D.; McIntosh, T.J. Lipopolysaccharides in bacterial membranes act like cholesterol in eukaryotic plasma membranes in providing protection against melittininduced bilayer lysis. Biochemistry, 2003, 42, 1101-1108.
14. Ding, L.; Yang, L.; Weiss, T.M.; Waring, A.J.; Lehrer, R.I.; Huang, H.W. Interaction of antimicrobial peptides with lipopolysaccha-rides. Biochemistry, 2003, 42, 12251-12259.
15. Oren, Z.; Shai, Y. Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study. Biochemistry, 1997, 36, 1826-1835.
16. Banemann, A.; Deppisch, H.; Gross, R. The lipopolysaccharide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides. Infect. Immun., 1998, 66, 5607-5612.
17. Nikaido, H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science, 1994, 264, 382-388.
18. Nikaido, H.; Vaara, M. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev., 1985, 49, 1-32.
19. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev., 2003, 67, 593-656.
20. Delcour, A.H. Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta, 2009, 1794, 808-816.
21. Rosenfeld, Y.; Shai, Y. Lipopolysaccharide (Endotoxin)-host defense antibacterial peptides interactions: role in bacterial resistance and prevention of sepsis. Biochim. Biophys. Acta, 2006, 1758, 1513-1522.
22. Brandenburg, K.; Seydel, U. Physical aspects of structure and function of membranes made from lipopolysaccharides and free lipid A. Biochim. Biophys. Acta, 1984, 775, 225-238.
23. Seydel, U.; Koch, M.H.; Brandenburg, K. Structural polymorphisms of rough mutant lipopolysaccharides Rd to Ra from Salmonella Minnesota. J. Struct. Biol., 1993, 110, 232-243.
24. Kastowsky, M.; Gutberlet, T.; Bradaczek, H. Molecular modeling of the three dimensional structure and conformational flexibility of bacterial lipopolysaccharide. J. Bacteriology, 1992, 174, 4798-4806.
25. Kastowsky, M.; Gutberlet, T.; Bradaczek, H. Comparison of X-ray powder-diffraction data of various bacterial lipopolysaccharide structures with theoretical model conformations. Eur. J. Biochem., 1993, 217, 771-779.
26. Westphal, O., Westphal, U.; Sommer, T. The history of pyrogen research. In Microbiology; Schlessinger, D, Ed.; American Society for Microbiology: Washington, D.C, 1977; pp. 221-238.
27. Rietschel, E. T.; Westphal, O. Endotoxin: Historical Perspectives. In Endotoxin in Health and Disease; Brade, H.; Opal, S. M.; Vo-gel, S. N.; Morrison, D. C., Eds.; Marcel Dekker: New York, 1999; pp. 1-29.
28. Fink, P. F. Sepsis Syndrome. In Handbook of Critical Care; Berk, J.L.; Sampliner, J.E., Eds.; Little, Brown and Co: Boston, 1990; pp. 619.
29. Cohen, J. The immunopathogenesis of sepsis. Nature, 2002, 420, 885-891.
30. Martin, G.S.; Mannino, D.M.; Eaton, S.; Moss, M. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med., 2003, 348, 1546-1554.
31. Angus, D.C.; Wax, R.S. Epidemiology of sepsis: an update. Crit. Care Med., 2001, 29, S109-S116.
32. Beutler, B.; Rietschel, E.T. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol., 2003, 3, 169-176.
33. Ward, P. A. The dark side of C5a in sepsis. Nat. Rev. Immunol., 2004, 4, 133-142.
34. Miller, S.I.; Ernst, R.K.; Bader, M.W. LPS, TLR4 and infectious disease diversity. Nat. Rev. Microbiol., 2005, 3, 36-46.
35. Finlay, B.B.; Hancock, R.E. Can innate immunity be enhanced to treat microbial infections? Nat. Rev. Microbiol., 2004, 2, 497-504.
36. Mueller, M.; Lindner, B.; Kusumoto, S.; Fukase, K.; Schromm, A. B.; Seydel, U. Aggregates are the biologically active units of endo-toxin. J. Biol. Chem., 2004, 279, 26307-26313.
37. Gegner, J.A.; Ulevitch, R.J.; Tobias, P.S. Lipopolysaccharide (LPS) signal transduction and clearance. Dual roles for LPS binding protein and membrane CD14. J. Biol. Chem., 1995, 270, 5320-5325.
38. Lamping, N.; Hoess, A.; Yu, B.; Park, T.C.; Kirschning, C.J.; Pfeil, D.; Reuter, D.; Wright, S. D.; Herrmann, F.; Schumann, R.R. Effects of site-directed mutagenesis of basic residues (Arg 94, Lys 95, Lys 99) of lipopolysaccharide (LPS)-binding protein on binding and transfer of LPS and subsequent immune cell activation. J. Immunol., 1996, 157, 4648-4656.
39. Viriyakosol, S.; Tobias, P.S.; Kitchens, R.L.; Kirkland, T.N. MD-2 binds to bacterial lipopolysaccharide. J. Biol. Chem., 2001, 276, 38044-38051.
40. Shimazu, R.; Akashi, S.; Ogata, H.; Nagai, Y.; Fukudome, K.; Miyake, K.; Kimoto, M. MD-2, a molecule that confers lipopoly-saccharide responsiveness on Toll-like receptor 4. J. Exp. Med., 1999, 189, 1777-1782.
41. Re, F.; Strominger, J.L. Monomeric recombinant MD-2 binds tolllike receptor 4 tightly and confers lipopolysaccharide responsiveness. J. Biol. Chem., 2002, 277, 23427-23432.
42. Prohinar, P.; Re, F.; Widstrom, R.; Zhang, D.; Teghanemt, A.; Weiss, J.P.; Gioannini, T.L. Specific high affinity interactions of monomeric endotoxin protein complexes with Toll-like receptor 4 ectodomain. J. Biol. Chem., 2007, 282, 1010-1017
43. Beamer, L.J.; Carroll, S.F.; Eisenberg, D. Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science 1997, 276, 1861-1864.
44. Beamer, L.J.; Carroll, S.F.; Eisenberg, D. The BPI/LBP family of proteins: a structural analysis of conserved regions. Protein Sci., 1998, 7, 906-914.
45. Kim, J.I.; Lee, C.J.; Jin, M.S.; Lee, C.H.; Paik, S.G.; Lee, H.; Lee, J.O. Crystal structure of CD14 and its implications for lipopolysac-charide signaling. J. Biol. Chem., 2005, 280, 11347-11351.
46. Ohto, U.; Fukase, K.; Miyake, K.; Satow, Y. Crystal structures of human MD-2 and its complex with antiendotoxic lipid Iva. Science, 2007, 316, 1632-1634.
47. Kim, H.M.; Park, B.S.; Kim, J.I.; Kim, S.E.; Lee, J.; Oh, S.C.; Enkhbayar, P.; Matsushima, N.; Lee, H.; Yoo, O.J.; Lee, J.O. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 2007, 130, 906-917.
48. Park, B.S.; Song, D.H.; Kim, H.M.; Choi, B.S.; Lee, H.; Lee, J.O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature, 2009, 458, 1191-1195.
49. Taylor, A.H.; Heavner, G.; Nedelman, M.; Sherris, D.; Brunt, E.; Knight, D.; Ghrayeb, J. Lipopolysaccharide (LPS) neutralizing peptides reveal a lipid A binding site of LPS binding protein. J. Biol. Chem., 1995, 270, 17934-17938.
50. Pristovsek, P.; Simcic, S.; Wraber, B.; Urleb, U. Structure of a synthetic fragment of the lipopolysaccharide (LPS) binding protein when bound to LPS and design of a peptidic LPS inhibitor. J. Med. Chem., 2005, 48, 7911-7914.
51. Rietschel, E.T.; Kirikae, T.; Shade, U.F.; Ulmer, A.J.; Holst, O.; Brade, H.; Schmidt, G.; Mamat, U.; Grimmecke, H.D.; Kusumoto, S.; Zahringer, U. The chemical structure of bacterial endotoxin in relation to bioactivity. Immunobiology, 1993, 187, 169-190.
52. Teghanemt, A.; Zhang, D.; Levis, E.N.; Weiss, J.P.; Gioannini, T.L. Molecular basis of reduced potency of underacylated endotox-ins. J. Immuno., 2005, 175, 4669-4676.
53. Rietschel, E.T.; Kirikae, T.; Schade, F.U.; Mamat, U.; Schmidt, G.; Loppnow, H.; Ulmer, A.J.; Zahringer, U.; Seydel, U.; Di Padova, F.; et al. Bacterial endotoxin: molecular relationships of structure to activity and function. F A S E B J., 1994, 8, 217-225.
54. Bochkov, V.N.; Kadl, A.; Huber, J.; Gruber, F.; Binder, B.R.; Leitinger, N. Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature 2002, 419, 77-81.
55. Wang, P.Y.; Kitchens, R.L.; Munford, R.S. Phosphatidylinositides bind to plasma membrane CD14 and can prevent monocyte activation by bacterial lipopolysaccharide. J. Biol. Chem., 1998, 273, 24309-24313.
56. Kuronuma, K.; Mitsuzawa, H.; Takeda, K.; Nishitani, C.; Chan, E.D.; Kuroki, Y.; Nakamura, M.; Voelker, D.R. Anionic pulmonary surfactant phospholipids inhibit inflammatory responses from alveolar macrophages and U937 cells by binding the lipopolysac-charide-interacting proteins CD14 and MD-2. J. Biol. Chem., 2009, 284, 25488-25500.
57. Hawkins, L.D.; Christ, W.J.; Rossignol, D.P. Inhibition of endo-toxin response by synthetic TLR4 antagonists. Curr. Top. Med. Chem., 2004, 4, 1147-1171.
58. Mancek, M.; Pristovsek, P.; Jerala, R. Identification of LPS-binding peptide fragment of MD-2, a toll-receptor accessory protein. Biochem. Biophys. Res. Commun., 2002, 292, 880-885.
59. Verhoef, J. Antibiotic resistance: the pandemic. Adv. Exp. Med. Biol., 2003, 531, 301-313.
60. Hancock, R.E. Peptide antibiotics. Lancet, 1997, 349, 418-422.
61. Overbye, K.M.; Barrett, J.F. Antibiotics: where did we go wrong? Drug Discov. Today, 2005, 10, 45-52.
62. Levy, S.B.; Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med., 2004, 10, S122-129.
63. Walsh, F.M.; Amyes, S.G. Microbiology and drug resistance mechanisms of fully resistant pathogens. Curr. Opin. Microbiol., 2004, 7, 439-444.
64. Weinstein, R.A. Controlling antimicrobial resistance in hospitals: infection control and use of antibiotics. Emerg. Infect. Dis., 2001, 7, 188-192.
65. Fischbach, M.A.; Walsh, C.T. Antibiotics for emerging pathogens. Science, 2009, 325, 1089-1093.
66. Taubes, G. The bacteria fight back. Science, 2008, 321, 356-361.
67. Ganesh, V.; Bodewits, K.; Bartholdson, S.J.; Natale, D.; Campopiano, D.J.; Mareque-Rivas, J.C. Effective binding and sensing of lipopolysaccharide: combining complementary pattern recognition receptors. Angew Chem. Int. Ed. Engl., 2009, 48, 356-360.
68. Chaby, R. Lipopolysaccharide-binding molecules: transporters, blockers and sensors. Cell Mol. Life Sci., 2004, 61, 1697-1713.
69. Hancock, R.E. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis., 2001, 1, 156-164.
70. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415, 389-395.
71. Hancock, R.E.; Scott, M.G. The role of antimicrobial peptides in animal defenses. Proc. Natl. Acad. Sci. U.S.A., 2000, 97, 8856-8861.
72. Brogden, K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3, 238-250.
73. Storm, D.R.; Rosenthal, K.S.; Swanson, P.E. Polymyxin and related peptide antibiotics. Annu. Rev. Biochem., 1977, 46, 723-763.
74. Morrison, D.C.; Jacobs, D.M. Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides. Immunochemistry, 1976, 13, 813-818.
75. Rustici, A.; Velucchi, M.; Faggioni, R.; Sironi, M.; Ghezzi, P.; Quataert, S.; Green, B.; Porro, M. Molecular mapping and detoxification of the lipid A binding site by synthetic peptides. Science, 1993, 259, 361-365.
76. Pristovsek, P.; Kidric, J. Peptides neutralizing lipopolysaccharide -structure and function. Mini. Rev. Med. Chem., 2001, 1, 409-416.
77. Pristovsek, P.; Kidric, J. The search for molecular determinants of LPS inhibition by proteins and peptides. Curr. Top. Med. Chem., 2004, 4, 1185-1201.
78. Jerala, R.; Porro, M. Endotoxin neutralizing peptides. Curr. Top. Med. Chem., 2004, 4, 1173-1184.
79. Bhor, V.M.; Thomas, C.J.; Surolia, N.; Surolia, A. Polymyxin B: an ode to an old antidote for endotoxic shock. Mol. Biosyst., 2005, 1, 213-222.
80. Selsted, M.E.; Ouellette, A.J. Mammalian defensins in the antimicrobial immune response. Nat. Immunol., 2005, 6, 551-557.
81. Dhople, V.; Krukemeyer, A.; Ramamoorthy, A. The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochim. Biophys. Acta, 2006, 1758, 1499-1512.
82. Lehrer, R.I.; Ganz, T. Defensins of vertebrate animals. Curr. Opin. Immunol., 2002, 14, 96-102.
83. Scott, M.G.; Vreugdenhil, A.C.; Buurman, W.A.; Hancock, R.E.; Gold, M.R. Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS binding protein. J. Immunol., 2000, 164, 549-553.
84. Motzkus, D.; Schulz-Maronde, S.; Heitland, A.; Schulz, A.; Forssmann, W.G.; Jubner, M.; Maronde, E. The novel beta-defensin DEFB123 prevents lipopolysaccharide-mediated effects in vitro and in vivo. F A S E B J., 2006, 20, 1701-1702.
85. Kopp, E.; Medzhitov, R. Skin antibiotics get in the loop. Nat. Med., 2002, 8, 1359-1360.
86. 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.; Kwak, L.W. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science, 2002, 298, 1025-1029.
87. Durr, U.H.; Sudheendra, U.S.; Ramamoorthy, A. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta, 2006, 1758, 1408-1425.
88. Gennaro, R.; Zanetti, M. Structural features and biological activities of the cathelicidin-derived antimicrobial peptides. Biopolymers, 2000, 55, 31-49.
89. Hirata, M.; Shimomura, Y.; Yoshida, M.; Wright, S.C.; Larrick, J.W. Endotoxin-binding synthetic peptides with endotoxin-neutralizing, antibacterial and anticoagulant activities. Prog. Clin. Biol. Res., 1994, 388, 147-159.
90. Cowland, J.B.; Johnsen, A.H.; Borregaard, N. hCAP-18, a cathelin/pro-bactenecin-like protein of human neutrophil specific granules. FEBS Lett., 1995, 368, 173-176.
91. Scott, M.G.; Davidson, D.J.; Gold, M.R.; Bowdish, D.; Hancock, R.E. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol., 2002, 169, 3883-3891
92. Di Nardo, A.; Vitiello, A.; Gallo, R.L. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. J. Immunol., 2003, 170, 2274-2278.
93. Zanetti, M. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol., 2004, 75, 39-48.
94. Xiao, Y.; Cai, Y.; Bommineni, Y.R.; Fernando, S.C.; Prakash, O.; Gilliland, S.E.; Zhang, G. Identification and functional characterization of three chicken cathelicidins with potent antimicrobial activity. J. Biol. Chem., 2006, 281, 2858-2867.
95. Xiao, Y.; Dai, H.; Bommineni, Y.R.; Soulages, J.L.; Gong, Y.X.; Prakash, O.; Zhang, G. Structure-activity relationships of fow-licidin-1, a cathelicidin antimicrobial peptide in chicken. FEBS J., 2006, 273, 2581-2593.
96. Bommineni, Y.R.; Dai, H.; Gong, Y.X.; Soulages, J.L.; Fernando, S.C.; Desilva, U.; Prakash, O.; Zhang, G. Fowlicidin-3 is an alpha-helical cationic host defense peptide with potent antibacterial and lipopolysaccharide-neutralizing activities. FEBS J., 2007, 274, 418-428.
97. Goitsuka, R.; Chen, C.L.; Benyon, L.; Asano, Y.; Kitamura, D.; Cooper, M.D. Chicken cathelicidin-B1, an antimicrobial guardian at the mucosal M cell gateway. Proc. Natl. Acad. Sci. U.S.A., 2007, 104, 15063-15068.
98. Chang, C.I.; Zhang, Y.A.; Zou, J.; Nie, P.; Secombes, C.J. Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and atlantic salmon (Salmo salar). Antimicrob. Agents Chemother., 2006, 50, 185-195.
99. Uzzell, T.; Stolzenberg, E.D.; Shinnar, A.E.; Zasloff, M. Hagfish intestinal antimicrobial peptides are ancient cathelicidins. Peptides, 2003, 24, 1655-1667.
100. Scott, M.G.; Hancock, R.E. Cationic antimicrobial peptides and their multifunctional role in the immune system. Crit. Rev. Immunol., 2002, 20, 407-431.
101. Tossi, A.; Scocchi, M.; Skerlavaj, B.; Gennaro, R. Identification and characterization of a primary antibacterial domain in CAP18, a lipopolysaccharide binding protein from rabbit leukocytes. FEBS Lett., 1994, 339, 108-112.
102. Tack, B.F.; Sawai, M.V.; Kearney, W.R.; Robertson, A.D.; Sherman, M.A.; Wang, W.; Hong, T.; Boo, L.M.; Wu, H.; Waring, A.J.; Lehrer, R.I. SMAP-29 has two LPS-binding sites and a central hinge. Eur. J. Biochem., 2002, 269, 1181-1189.
103. Okuda, D.; Yomogida, S.; Tamura, H.; Nagaoka, I. Determination of the antibacterial and lipopolysaccharide-neutralizing regions of guinea pig neutrophil cathelicidin peptide CAP11. Antimicrob. Agents Chemother., 2006, 50, 2602-2607.
104. 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 spec-troscopy. Biopolymers, 2009, 92, 9-22.
105. Nell, M.J.; Tjabringa, G.S.; Wafelman, A.R.; Verrijk, R.; Hiemstra, P.S.; Drijfhout, J.W.; Grote, J. Development of novel LL-37 derived antimicrobial peptides with LPS and LTA neutralizing and antimicrobial activities for therapeutic application. J. Peptides, 2006, 27, 649-660.
106. Ciornei, C.D.; Egesten, A.; Bodelsson, M. Effects of human cathelicidin antimicrobial peptide LL-37 on lipopolysaccharide-induced nitric oxide release from rat aorta in vitro. Acta Anaesthesiol. Scand., 2003, 47, 213-220.
107. Zughaier, S.M.; Shafer, W.M.; Stephens, D.S. Antimicrobial pep-tides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macro-phages. Cell Microbiol., 2005, 7, 1251-1262.
108. Nagaoka, I.; Hirota, S.; Niyonsaba, F.; Hirata, M.; Adachi, Y.; Tamura, H.; Tanaka, S.; Heumann, D. Augmentation of the lipopolysaccharide-neutralizing activities of human cathelicidin CAP18/LL-37-derived antimicrobial peptides by replacement with hydrophobic and cationic amino acid residues. Clin. Diagn. Lab. Immunol., 2002, 9, 972-982.
109. Epand, R.M.; Vogel, H.J. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta, 1999, 1462, 11-28.
110. Haney, E.F.; Vogel, H.J. NMR of antimicrobial peptides. Annu. Rep. NMR Spectrosc., 2009, 65, 1-51.
111. Bhattacharjya, S.; Ramamoorthy, A. Multifunctional host defense peptides: functional and mechanistic insights from NMR structures of potent antimicrobial peptides. FEBS J., 2009, 276, 6465-73.
112. Santos, N.C.; Silva, A.C.; Castanho, M.A.; Martins-Silva, J.; Saldanha, C. Evaluation of lipopolysaccharide aggregation by light scattering spectroscopy. Chembiochem, 2003, 4, 96-100.
113. Yu, L.; Tan, M.; Ho, B.; Ding, J.L.; Wohland, T. Determination of critical micelle concentrations and aggregation numbers by fluorescence correlation spectroscopy: aggregation of a lipopolysaccha-ride. Anal. Chim. Acta, 2006, 556, 216-225.
114. Rajan, R.; Awasthi, S. K.; Bhattacharjya, S.; Balaram, P. Teflon-coated peptides: hexafluoroacetone trihydrate as a structure stabilizer for peptides. Biopolymers, 1997, 42, 125-128.
115. Pristovsek, P.; Kidric, J. Solution structure of polymyxins B and E and effect of binding to lipopolysaccharide: an NMR and molecular modeling study. J. Med. Chem., 1999, 42, 4604-4613.
116. Japelj, B.; Pristovsek, P.; Majerle, A.; Jerala, R. Structural origin of endotoxin neutralization and antimicrobial activity of a lactoferrin-based peptide J. Biol. Chem., 2005, 280, 16955-16961.
117. Pristovsek, P.; Feher, K.; Szilagyi, L.; Kidric, J. Structure of a synthetic fragment of the LALF protein when bound to lipopoly-saccharide. J. Med. Chem., 2005, 48, 1666-1670.
118. Bhunia, A.; Domadia, P.N.; Bhattacharjya, S. Structural and ther-modynamic analyses of the interaction between melittin and lipopolysaccharide. Biochim. Biophys. Acta, 2007, 1768, 3282-3291.
119. Bhunia, A.; Ramamoorthy, A.; Bhattacharjya, S. Helical hairpin structure of a potent antimicrobial peptide MSI-594 in lipopolysac-charide micelles by NMR spectroscopy. Chem. Eur. J., 2009, 15, 2036-2040.
120. Bhunia, A.; Chua, G.L.; Domadia, P.N.; Warshakoon, H.; Cromer, J.R.; David, S.A.; Bhattacharjya, S. Interactions of a designed pep-tide with lipopolysaccharide: Bound conformation and anti-endotoxic activity. Biochem. Biophys. Res. Commun., 2008, 369, 853-857.
121. Clore, G.M.; Gronenborn, A.M. Theory and applications of the transferred nuclear Overhauser effect to the study of the conformations of small ligands bound to proteins. J. Magn. Reson., 1982, 48, 402-417.
122. Post, C.B. Exchange-transferred NOE spectroscopy and bound ligand structure determination. Curr. Opin. Struct. Biol., 2003, 13, 581-588.
123. Meyer, B.; Peters, T. NMR spectroscopy techniques for screening and identifying ligand binding to protein receptors. Angew Chem. Int. Ed. Engl., 2003, 42, 864-890.
124. Mayer, M.; Meyer, B. Characterization of Ligand Binding by Saturation Transfer Difference NMR Spectroscopy. Angew Chem. Int. Ed., 1999, 38, 1784-1788.
125. Bhunia, A.; Domadia, P.N.; Torres, J.; Hallock, K.J.; Ramamoorthy, A.; Bhattacharjya, S. NMR structure of pardaxin, a pore-forming antimicrobial peptide, in lipopolysaccharide Micelles: Mechanism of outer membrane permeabilization. J. Biol. Chem., 2009, In Press.
126. David, S.A.; Awasthi, S.K.; Balaram, P. The role of polar and facial amphipathic character in determining lipopolysaccharide-binding properties in synthetic cationic peptides. J. Endotoxin. Res., 2000, 6, 249-256.
127. David, S.A. Towards a rational development of anti-endotoxin agents: novel approaches to sequestration of bacterial endotoxins with small molecules. J. Mol. Recognit., 2001, 14, 370-387.
128. Rosenfeld, Y.; Papo, N.; Shai, Y. Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. Peptide properties and plausible modes of action. J. Biol. Chem., 2006, 281, 1636-1643.
129. Rosenfeld, Y.; Sahl, H.G.; Shai, Y. Parameters involved in antimicrobial and endotoxin detoxification activities of antimicrobial pep-tides. Biochemistry, 2008, 47, 6468-6478.
130. Gray, B.H.; Haseman, J.R.; Mayo, K.H. B/PI-derived synthetic peptides: synergistic effects in tethered bactericidal and endotoxin neutralizing peptides. Biochim. Biophys. Acta, 1995, 1244, 185-190.
131. Dings, R. P.; Haseman, J. R.; Mayo, K. H. Probing structure-activity relationships in bactericidal peptide betapep-25. Biochem. J., 2008, 414, 143-150.
132. Dings, R.P.; Mayo, K.H. A journey in structure-based drug discovery: from designed peptides to protein surface topomimetics as antibiotic and antiangiogenic agent. Acc. Chem. Res., 2007, 40, 1057-1065.
133. Ilyina, E.; Roongta, V.; Mayo, K.H. NMR structure of a de novo designed, peptide 33mer with two distinct, compact beta-sheet folds. Biochemistry, 1997, 36, 5245-5250.
134. Frecer, V.; Ho, B.; Ding, J.L. De novo design of potent antimicrobial peptides. Antimicrob. Agents Chemother., 2004, 48, 3349-3357.
135. Muhle, S.A.; Tam, J.P. Design of Gram-negative selective antimicrobial peptides. Biochemistry, 2001, 40, 5777-5785.
136. Bhattacharjya, S.; Domadia, P.N.; Bhunia, A.; Malladi, S.; David, S.A. High-resolution solution structure of a designed peptide bound to lipopolysaccharide: transferred nuclear Overhauser effects, micelle selectivity, and anti-endotoxic activity. Biochemistry, 2007, 46, 5864-5874.
137. Bhunia, A.; Mohanram, H.; Domadia, P.N.; Torres, J.; Bhattacharjya, S. Designed beta-boomerang antiendotoxic and antimicrobial peptides: structures and activities in lipopolysaccharide. J. Biol. Chem., 2009, 284, 21991-22004.
138. Ferguson, A.D.; Welte, W.; Hofmann, E.; Lindner, B.; Holst, O.; Coulton, J.W.; Diederichs, K.A. Conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure, 2000, 8, 585-592.
139. Han, X.; Bushweller, J.H.; Cafiso, D.S.; Tamm, L.K. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol., 2001, 8, 715-720.