1887

Abstract

As antibiotic resistance increases worldwide, there is an increasing pressure to develop novel classes of antimicrobial compounds to fight infectious disease. Peptide therapeutics represent a novel class of therapeutic agents. Some, such as cationic antimicrobial peptides and peptidoglycan recognition proteins, have been identified from studies of innate immune effector mechanisms, while others are completely novel compounds generated in biological systems. Currently, only selected cationic antimicrobial peptides have been licensed, and only for topical applications. However, research using new approaches to identify novel antimicrobial peptide therapeutics, and new approaches to delivery and improving stability, will result in an increased range of peptide therapeutics available in the clinic for broader applications.

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2009-08-01
2019-10-19
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References

  1. Allaker, R. P. ( 2008; ). Host defence peptides – a bridge between the innate and adaptive immune responses. Trans R Soc Trop Med Hyg 102, 3–4.[CrossRef]
    [Google Scholar]
  2. Billstein, S. A. ( 1994; ). How the pharmaceutical industry brings an antibiotic drug to market in the United States. Antimicrob Agents Chemother 38, 2679–2682.[CrossRef]
    [Google Scholar]
  3. Bowdish, D. M. E., Davidson, D. J., Lau, Y. E., Lee, K., Scott, M. G. & Hancock, R. E. W. ( 2005; ). Impact of LL-37 on anti-infective immunity. J Leukoc Biol 77, 451–459.
    [Google Scholar]
  4. Brogden, K. A. ( 2005; ). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3, 238–250.[CrossRef]
    [Google Scholar]
  5. Cheng, L., Naumann, T. A., Horswill, A. R., Hong, S. J., Venters, B. J., Tomsho, J. W., Benkovic, S. J. & Keiler, K. C. ( 2007; ). Discovery of antibacterial cyclic peptides that inhibit the ClpXP protease. Protein Sci 16, 1535–1542.[CrossRef]
    [Google Scholar]
  6. Cho, J. H., Fraser, I. P., Fukase, K., Kusumoto, S., Fujimoto, Y., Stahl, G. L. & Ezekowitz, R. A. B. ( 2005; ). Human peptidoglycan recognition protein S is an effector of neutrophil-mediated innate immunity. Blood 106, 2551–2558.[CrossRef]
    [Google Scholar]
  7. Colas, P., Cohen, B., Jessen, T., Grishina, I., Mccoy, J. & Brent, R. ( 1996; ). Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature 380, 548–550.[CrossRef]
    [Google Scholar]
  8. Dartois, V., Sanchez-Quesada, J., Cabezas, E., Chi, E., Dubbelde, C., Dunn, C., Granja, J., Gritzen, C., Weinberger, D. & other authors ( 2005; ). Systemic antibacterial activity of novel synthetic cyclic peptides. Antimicrob Agents Chemother 49, 3302–3310.[CrossRef]
    [Google Scholar]
  9. De Clercq, E. ( 2005; ). Emerging anti-HIV drugs. Expert Opin Emerg Drugs 10, 241–273.[CrossRef]
    [Google Scholar]
  10. Depauw, P., Neyt, C., Vanderwinkel, E., Wattiez, R. & Falmagne, P. ( 1995; ). Characterization of human serum N-acetylmuramyl-l-alanine amidase purified by affinity chromatography. Protein Expr Purif 6, 371–378.[CrossRef]
    [Google Scholar]
  11. Domagk, G. ( 1935; ). A new class of disinfectant. Dtsch Med Wochenschr 61, 829–832.[CrossRef]
    [Google Scholar]
  12. Dziarski, R., Platt, K. A., Gelius, E., Steiner, H. & Gupta, D. ( 2003; ). Defect in neutrophil killing and increased susceptibility to infection with nonpathogenic gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice. Blood 102, 689–697.[CrossRef]
    [Google Scholar]
  13. Eldridge W., Fitzgerald K., Cooley N. & McGregor D. ( 2006; ). Peptide stabilizer compounds and screening methods. Patent Application WO2006097748.
  14. Elvin, S. J., Eyles, J. E., Howard, K. A., Ravichandran, E., Somavarappu, S., Alpar, H. O. & Williamson, E. D. ( 2006; ). Protection against bubonic and pneumonic plague with a single dose microencapsulated sub-unit vaccine. Vaccine 24, 4433–4439.[CrossRef]
    [Google Scholar]
  15. Falciani, C., Lozzi, L., Pini, A. & Bracci, L. ( 2005; ). Bioactive peptides from libraries. Chem Biol 12, 417–426.[CrossRef]
    [Google Scholar]
  16. Fernandez-Lopez, S., Kim, H. S., Choi, E. C., Delgado, M., Granja, J. R., Khasanov, A., Kraehenbuehl, K., Long, G., Weinberger, D. A. & other authors ( 2001; ). Antibacterial agents based on the cyclic D,L-alpha-peptide architecture. Nature 412, 452–455.[CrossRef]
    [Google Scholar]
  17. Flick-Smith, H. C., Eyles, J. E., Hebdon, R., Waters, E. L., Beedham, R. J., Stagg, T. J., Miller, J., Alpar, H. O., Baillie, L. W. J. & Williamson, E. D. ( 2002; ). Mucosal or parenteral administration of microsphere-associated Bacillus anthracis protective antigen protects against anthrax infection in mice. Infect Immun 70, 2022–2028.[CrossRef]
    [Google Scholar]
  18. Flisiak, R., Horban, A., Kierkus, J., Stanczak, J., Cielnak, I., Stanczak, G. P., Wiercinska-Drapalo, A., Siwak, E., Higersberger, J. & other authors ( 2006; ). The cyclophilin inhibitor DEBIO-025 has a potent dual anti-HIV and anti-HCV activity in treatment-naive HIV/HCV co-infected subjects. Hepatology 44, 1130
    [Google Scholar]
  19. Flisiak, R., Horban, A., Gallay, P., Bobardt, M., Selvarajah, S., Wiercinska-Drapalo, A., Siwak, E., Cielniak, I., Higersberger, J. & other authors ( 2008; ). The cyclophilin inhibitor debio-025 shows potent anti-hepatitis C effect in patients coinfected with hepatitis C and human immunodeficiency virus. Hepatology 47, 817–826.[CrossRef]
    [Google Scholar]
  20. Fogueri, L. R. & Singh, S. ( 2009; ). Smart polymers for controlled delivery of proteins and peptides: a review of patents. Recent Pat Drug Deliv Formul 3, 40–48.[CrossRef]
    [Google Scholar]
  21. Ganz, T. & Lehrer, R. I. ( 1994; ). Defensins. Curr Opin Immunol 6, 584–589.[CrossRef]
    [Google Scholar]
  22. Gelius, E., Persson, C., Karlsson, J. & Steiner, H. ( 2003; ). A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-l-alanine amidase activity. Biochem Biophys Res Commun 306, 988–994.[CrossRef]
    [Google Scholar]
  23. Giuliani, A., Pirri, G. & Nicoletto, S. F. ( 2007; ). Antimicrobial peptides: an overview of a promising class of therapeutics. Cent Eur J Biol 2, 1–33.
    [Google Scholar]
  24. Goldberg, A. L., Akopian, T. N., Kisselev, A. F., Lee, D. H. & Rohrwild, M. ( 1997; ). New insights into the mechanisms and importance of the proteasome in intracellular protein degradation. Biol Chem 378, 131–140.
    [Google Scholar]
  25. Goldman, M. J., Anderson, G. M., Stolzenberg, E. D., Kari, U. P., Zasloff, M. & Wilson, J. M. ( 1997; ). Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 88, 553–560.[CrossRef]
    [Google Scholar]
  26. Grace, M. J., Lee, S., Bradshaw, S., Chapman, J., Spond, J., Cox, S., DeLorenzo, M., Brassard, D., Wylie, D. & other authors ( 2005; ). Site of pegylation and polyethylene glycol molecule size attenuate interferon-alpha antiviral and antiproliferative activities through the JAK/STAT signaling pathway. J Biol Chem 280, 6327–6336.[CrossRef]
    [Google Scholar]
  27. Guan, R., Malchiodi, E. L., Wang, Q., Schuck, P. & Mariuzza, R. A. ( 2004a; ). Crystal structure of the C-terminal peptidoglycan-binding domain of human peptidoglycan recognition protein I alpha. J Biol Chem 279, 31873–31882.[CrossRef]
    [Google Scholar]
  28. Guan, R., Roychowdhury, A., Ember, B., Kumar, S., Boons, G.-J. & Mariuzza, R. A. ( 2004b; ). Structural basis for peptidoglycan binding by peptidoglycan recognition proteins. Proc Natl Acad Sci U S A 101, 17168–17173.[CrossRef]
    [Google Scholar]
  29. Guan, R., Wang, Q., Sundberg, E. J. & Mariuzza, R. A. ( 2005; ). Crystal structure of human peptidoglycan recognition protein S (PGRP-S) at 1.70 angstrom resolution. J Mol Biol 347, 683–691.[CrossRef]
    [Google Scholar]
  30. Guan, R., Brown, P. H., Swaminathan, C. P., Roychowdhury, A., Boons, G.-J. & Mariuzza, R. A. ( 2006; ). Crystal structure of human peptidoglycan recognition protein I alpha bound to a muramyl pentapeptide from Gram-positive bacteria. Protein Sci 15, 1199–1206.[CrossRef]
    [Google Scholar]
  31. Gururaja, T. L., Narasimhamurthy, S., Payan, D. G. & Anderson, D. C. ( 2000; ). A novel artificial loop scaffold for the noncovalent constraint of peptides. Chem Biol 7, 515–527.[CrossRef]
    [Google Scholar]
  32. Hancock, R. E. W. ( 1984; ). Alterations in outer-membrane permeability. Annu Rev Microbiol 38, 237–264.[CrossRef]
    [Google Scholar]
  33. Hancock, R. E. W. ( 2001; ). Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect Dis 1, 156–164.[CrossRef]
    [Google Scholar]
  34. Harris, A. G. ( 1994; ). Somatostatin and somatostatin analogs – pharmacokinetics and pharmacodynamic effects. Gut 35, S1–S4.
    [Google Scholar]
  35. Harris, J. M. & Chess, R. B. ( 2003; ). Effect of pegylation on pharmaceuticals. Nat Rev Drug Discov 2, 214–221.[CrossRef]
    [Google Scholar]
  36. Hatziioannou, T., Perez-Caballero, D., Cowan, S. & Bieniasz, P. D. ( 2005; ). Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J Virol 79, 176–183.[CrossRef]
    [Google Scholar]
  37. He, X. H., Shaw, P. C. & Tam, S. C. ( 1999; ). Reducing the immunogenicity and improving the in vivo activity of trichosanthin by site-directed PEGylation. Life Sci 65, 355–368.[CrossRef]
    [Google Scholar]
  38. Heithoff, D. M., Sinsheimer, R. L., Low, D. A. & Mahan, M. J. ( 1999; ). An essential role for DNA adenine methylation in bacterial virulence. Science 284, 967–970.[CrossRef]
    [Google Scholar]
  39. Herrmann, E., Flisiak, R., Horban, A., Crabbe, R., Porchet, H., Nicolas, V., Scalfaro, P. & Zeuzem, S. ( 2007; ). Viral kinetics during 14-day treatment with debio-025 demonstrate efficient blocking of viral replication in different HCV genotypes without signs of emerging viral resistance. J Hepatol 46, 88
    [Google Scholar]
  40. Hilt, W. & Wolf, D. H. ( 1996; ). Proteasomes: destruction as a programme. Trends Biochem Sci 21, 96–102.[CrossRef]
    [Google Scholar]
  41. Hong, S. Y., Oh, J. E. & Lee, K. H. ( 1999; ). Effect of d-amino acid substitution on the stability, the secondary structure, and the activity of membrane-active peptide. Biochem Pharmacol 58, 1775–1780.[CrossRef]
    [Google Scholar]
  42. Horswill, A. R., Savinov, S. N. & Benkovic, S. J. ( 2004; ). A systematic method for identifying small-molecule modulators of protein-protein interactions. Proc Natl Acad Sci U S A 101, 15591–15596.[CrossRef]
    [Google Scholar]
  43. Hühne, R., Koch, F.-T. & Sühnel, J. ( 2007; ). A comparative view at comprehensive information resources on three-dimensional structures of biological macro-molecules. Brief Funct Genomics Proteomics 6, 220–239.[CrossRef]
    [Google Scholar]
  44. Irache, J. M., Salman, H. H., Gamazo, C. & Espuelas, S. ( 2008; ). Mannose-targeted systems for the delivery of therapeutics. Expert Opin Drug Deliv 5, 703–724.[CrossRef]
    [Google Scholar]
  45. Irwin, J. J. ( 2006; ). How good is your screening library? Curr Opin Chem Biol 10, 352–356.[CrossRef]
    [Google Scholar]
  46. Jacob, M. K., Leena, S. & Kumar, K. S. ( 2008; ). Peptide-polymer biotherapeutic synthesis on novel cross-linked beads with “Spatially Tunable” and “Isolated” functional sites. Biopolymers 90, 512–525.[CrossRef]
    [Google Scholar]
  47. Jenssen, H., Hamill, P. & Hancock, R. E. W. ( 2006; ). Peptide antimicrobial agents. Clin Microbiol Rev 19, 491–511.[CrossRef]
    [Google Scholar]
  48. John, H., Maronde, E., Forssmann, W. G., Meyer, M. & Adermann, K. ( 2008; ). N-terminal acetylation protects glucagon-like peptide GLP-1-(7–34)-amide from DPP-IV-mediated degradation retaining cAMP- and insulin-releasing capacity. Eur J Med Res 13, 73–78.
    [Google Scholar]
  49. Julio, S. M., Heithoff, D. M., Provenzano, D., Klose, K. E., Sinsheimer, R. L., Low, D. A. & Mahan, M. J. ( 2001; ). DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69, 7610–7615.[CrossRef]
    [Google Scholar]
  50. Kang, D., Liu, G., Lundstrom, A., Gelius, E. & Steiner, H. ( 1998; ). A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc Natl Acad Sci U S A 95, 10078–10082.[CrossRef]
    [Google Scholar]
  51. Keiler, K. C., Waller, P. R. H. & Sauer, R. T. ( 1996; ). Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271, 990–993.[CrossRef]
    [Google Scholar]
  52. Kemp, S. F., Fielder, P. J., Attie, K. M., Blethen, S. L., Reiter, E. O., Ford, K. M., Marian, M., Dao, L. N., Lee, H. J. & Saenger, P. ( 2004; ). Pharmacokinetic and pharmacodynamic characteristics of a long-acting growth hormone (GH) preparation (nutropin depot) in GH-deficient children. J Clin Endocrinol Metab 89, 3234–3240.[CrossRef]
    [Google Scholar]
  53. Khaksa, G., D'Souza, R., Lewis, S. & Udupa, N. ( 2000; ). Pharmacokinetic study of niosome encapsulated insulin. Indian J Exp Biol 38, 901–905.
    [Google Scholar]
  54. Kumar, S., Roychowdhury, A., Ember, B., Wang, Q., Guan, R. J., Mariuzza, R. A. & Boons, G. J. ( 2005; ). Selective recognition of synthetic lysine and meso-diaminopimelic acid-type peptidoglycan fragments by human peptidoglycan recognition proteins I alpha and S. J Biol Chem 280, 37005–37012.[CrossRef]
    [Google Scholar]
  55. Levchenko, I., Seidel, M., Sauer, R. T. & Baker, T. A. ( 2000; ). A specificity-enhancing factor for the ClpXP degradation machine. Science 289, 2354–2356.[CrossRef]
    [Google Scholar]
  56. Li, M., Yu, D. H. & Cai, H. ( 2008; ). The synthetic antimicrobial peptide KLKL5KLK enhances the protection and efficacy of the combined DNA vaccine against Mycobacterium tuberculosis. DNA Cell Biol 27, 405–413.[CrossRef]
    [Google Scholar]
  57. Liu, C., Xu, Z. J., Gupta, D. & Dziarski, R. ( 2001; ). Peptidoglycan recognition proteins – a novel family of four human innate immunity pattern recognition molecules. J Biol Chem 276, 34686–34694.[CrossRef]
    [Google Scholar]
  58. Llobet, E., Tomas, J. M. & Bengoechea, J. A. ( 2008; ). Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 154, 3877–3886.[CrossRef]
    [Google Scholar]
  59. Lu, X., Wang, M. H., Qi, J., Wang, H. T., Li, X. N., Gupta, D. & Dziarski, R. ( 2006; ). Peptidoglycan recognition proteins are a new class of human bactericidal proteins. J Biol Chem 281, 5895–5907.
    [Google Scholar]
  60. Luban, J., Bossolt, K. L., Franke, E. K., Kalpana, G. V. & Goff, S. P. ( 1993; ). Human-immunodeficiency-virus type-1 Gag protein binds to cyclophilin-A and cyclophilin-B. Cell 73, 1067–1078.[CrossRef]
    [Google Scholar]
  61. Marr, A. K., Gooderham, W. J. & Hancock, R. E. W. ( 2006; ). Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr Opin Pharmacol 6, 468–472.[CrossRef]
    [Google Scholar]
  62. Matsumoto, S., Akashi, H. & Taira, K. ( 2006; ). Screening and determination of gene function using randomized ribozyme and siRNA libraries. Handb Exp Pharmacol 173, 197–221.
    [Google Scholar]
  63. Mellroth, P., Karlsson, J. & Steiner, H. ( 2003; ). A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem 278, 7059–7064.[CrossRef]
    [Google Scholar]
  64. Moore, S. D. & Sauer, R. T. ( 2005; ). Ribosome rescue: tmRNA tagging activity and capacity in Escherichia coli. Mol Microbiol 58, 456–466.[CrossRef]
    [Google Scholar]
  65. Naumann, T. A., Tavassoli, A. & Benkovic, S. J. ( 2008; ). Genetic selection of cyclic peptide dam methyltransferase inhibitors. ChemBioChem 9, 194–197.[CrossRef]
    [Google Scholar]
  66. Neuwald, A. F., Aravind, L., Spouge, J. L. & Koonin, E. V. ( 1999; ). AAA(+): a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9, 27–43.
    [Google Scholar]
  67. Noyer-Weidner, M. & Trautner, T. A. ( 1993; ). Methylation of DNA in prokaryotes. EXS 64, 39–108.
    [Google Scholar]
  68. Odegrip, R., Coomber, D., Eldridge, B., Hederer, R., Kuhlman, P. A., Ullman, C., FitzGerald, K. & McGregor, D. ( 2004; ). CIS display: in vitro selection of peptides from libraries of protein-DNA complexes. Proc Natl Acad Sci U S A 101, 2806–2810.[CrossRef]
    [Google Scholar]
  69. Oren, Z. & Shai, Y. ( 2000; ). Cyclization of a cytolytic amphipathic alpha-helical peptide and its diastereomer: effect on structure, interaction with model membranes, and biological function. Biochemistry 39, 6103–6114.[CrossRef]
    [Google Scholar]
  70. Pakkala, M., Hekim, C., Soininen, P., Leinonen, J., Koistinen, H., Weisell, J., Stenman, U. H., Vepsalainen, J. & Narvanen, A. ( 2007; ). Activity and stability of human kalikrein-2-specific linear and cyclic peptide inhibitors. J Pept Sci 13, 348–353.[CrossRef]
    [Google Scholar]
  71. Papageorgiou, C., Borer, X. & French, R. R. ( 1994; ). Calcineurin has a very tight-binding pocket for the side-chain of residue-4 of cyclosporine. Bioorg Med Chem Lett 4, 267–272.[CrossRef]
    [Google Scholar]
  72. Ptak, R. G., Gallay, P. A., Jochmans, D., Halestrap, A. P., Ruegg, U. T., Pallansch, L. A., Bobardt, M. D., de Bethune, M. P., Neyts, J. & other authors ( 2008; ). Inhibition of human immunodeficiency virus type 1 replication in human cells by Debio-025, a novel cyclophilin binding agent. Antimicrob Agents Chemother 52, 1302–1317.[CrossRef]
    [Google Scholar]
  73. Qiu, D., Eisinger, V. M., Head, N. E., Pier, G. B. & Yu, H. D. ( 2008; ). ClpXP proteases positively regulate alginate overexpression and mucoid conversion in Pseudomonas aeruginosa. Microbiology 154, 2119–2130.[CrossRef]
    [Google Scholar]
  74. Ramon, J., Saez, V., Baez, R., Aldana, R. & Hardy, E. ( 2005; ). PEGylated interferon-alpha 2b: a branched 40K polyethylene glycol derivative. Pharm Res 22, 1374–1386.
    [Google Scholar]
  75. Reichert, J. & Sühnel, J. ( 2002; ). The IMB Jena Image Library of Biological Macromolecules: 2002 update. Nucleic Acids Res 30, 253–254.[CrossRef]
    [Google Scholar]
  76. Robinson, V. L., Oyston, P. C. F. & Titball, R. W. ( 2005; ). A dam mutant of Yersinia pestis is attenuated and induces protection against plague. FEMS Microbiol Lett 252, 251–256.[CrossRef]
    [Google Scholar]
  77. Royet, J. & Dziarski, R. ( 2007; ). Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 5, 264–277.[CrossRef]
    [Google Scholar]
  78. Samad, A., Sultana, Y. & Aqil, M. ( 2007; ). Liposomal drug delivery systems: an update review. Curr Drug Deliv 4, 297–305.[CrossRef]
    [Google Scholar]
  79. Sang, Y., Ramanathan, B., Ross, C. R. & Blecha, F. ( 2005; ). Gene silencing and overexpression of porcine peptidoglycan recognition protein long isoforms: involvement in beta-defensin-1 expression. Infect Immun 73, 7133–7141.[CrossRef]
    [Google Scholar]
  80. Scott, C. P., Abel-Santos, E., Wall, M., Wahnon, D. C. & Benkovic, S. J. ( 1999; ). Production of cyclic peptides and proteins in vivo. Proc Natl Acad Sci U S A 96, 13638–13643.[CrossRef]
    [Google Scholar]
  81. Scott, M. G., Dullaghan, E., Mookherjee, N., Glavas, N., Waldbrook, M., Thompson, A., Wang, A. K., Lee, K., Doria, S. & other authors ( 2007; ). An anti-infective peptide that selectively modulates the innate immune response. Nat Biotechnol 25, 465–472.[CrossRef]
    [Google Scholar]
  82. Simoes, S., Moreira, J. N., Fonseca, C., Duzgunes, N. & de Lima, M. C. P. ( 2004; ). On the formulation of pH-sensitive long circulation times. Adv Drug Deliv Rev 56, 947–965.[CrossRef]
    [Google Scholar]
  83. Sokolskaja, E., Sayah, D. M. & Luban, J. ( 2004; ). Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J Virol 78, 12800–12808.[CrossRef]
    [Google Scholar]
  84. Steinberg, D. A., Hurst, M. A., Fujii, C. A., Kung, A. H. C., Ho, J. F., Cheng, F. C., Loury, D. J. & Fiddes, J. C. ( 1997; ). Protegrin-1: a broad-spectrum, rapidly microbicidal peptide with in vivo activity. Antimicrob Agents Chemother 41, 1738–1742.
    [Google Scholar]
  85. Steiner, H., Hultmark, D., Engstrom, A., Bennich, H. & Boman, H. G. ( 1981; ). Sequence and specificity of two anti-bacterial proteins involved in insect immunity. Nature 292, 246–248.[CrossRef]
    [Google Scholar]
  86. Steinkasserer, A., Harrison, R., Billich, A., Hammerschmid, F., Werner, G., Wolff, B., Peichl, P., Palfi, G., Schnitzel, W. & other authors ( 1995; ). Mode of action of Sdz Nim-811, a nonimmunosuppressive cyclosporine-A analog with activity against human-immunodeficiency-virus type-1 (HIV-1): interference with early and late events in HIV-1 replication. J Virol 69, 814–824.
    [Google Scholar]
  87. Stromstedt, A. A., Pasupuleti, M., Schmidtchen, A. & Malmsten, M. ( 2009; ). Evaluation of strategies for improving proteolytic resistance of antimicrobial peptides by using variants of EFK17, an internal segment of LL-37. Antimicrob Agents Chemother 53, 593–602.[CrossRef]
    [Google Scholar]
  88. Sun, C., Mathur, P., Dupuis, J., Tizard, R., Ticho, B., Crowell, T., Gardner, H., Bowcock, A. M. & Carulli, J. ( 2006; ). Peptidoglycan recognition proteins PGLRP3 and PGLRP4 are encoded from the epidermal differentiation complex and are candidate genes for the Psors4 locus on chromosome 1q21. Hum Genet 119, 113–125.[CrossRef]
    [Google Scholar]
  89. Swaminathan, C. P., Brown, P. H., Roychowdhury, A., Wang, Q., Guan, R. J., Silverman, N., Goldman, W. E., Boons, G. J. & Mariuzza, R. A. ( 2006; ). Dual strategies for peptidoglycan discrimination by peptidoglycan recognition proteins (PGRPs). Proc Natl Acad Sci U S A 103, 684–689.[CrossRef]
    [Google Scholar]
  90. Tan, D. S. ( 2005; ). Diversity-oriented synthesis: exploring the intersections between chemistry and biology. Nat Chem Biol 1, 74–84.[CrossRef]
    [Google Scholar]
  91. Tavassoli, A. & Benkovic, S. J. ( 2007; ). Split-intein mediated circular ligation used in the synthesis of cyclic peptide libraries in E. coli. Nat Protoc 2, 1126–1133.[CrossRef]
    [Google Scholar]
  92. Taylor, V. L., Titball, R. W. & Oyston, P. C. F. ( 2005; ). Oral immunization with a Dam mutant of Yersinia pseudotuberculosis protects against plague. Microbiology 151, 1919–1926.[CrossRef]
    [Google Scholar]
  93. Thongyoo, P., Roque-Rosell, N., Leatherbarrow, R. J. & Tate, E. W. ( 2008; ). Chemical and biomimetic total syntheses of natural and engineered MCoTI cyclotides. Org Biomol Chem 6, 1462–1470.[CrossRef]
    [Google Scholar]
  94. Ulrich, H., Trujillo, C. A., Nery, A. A., Alves, J. M., Majumder, P., Resende, R. R. & Martins, A. H. ( 2006; ). DNA and RNA aptamers: from tools for basic research towards therapeutic applications. Comb Chem High Throughput Screen 9, 619–632.[CrossRef]
    [Google Scholar]
  95. Uttamchandani, M., Wang, J. & Yao, S. Q. ( 2006; ). Protein and small molecule microarrays: powerful tools for high-throughput proteomics. Mol Biosyst 2, 58–68.[CrossRef]
    [Google Scholar]
  96. Vaara, M. ( 1992; ). Agents that increase the permeability of the outer membrane. Microbiol Rev 56, 395–411.
    [Google Scholar]
  97. Vives, E., Schmidt, J. & Pelegrin, A. ( 2008; ). Cell-penetrating and cell-targeting peptides in drug delivery. Biochim Biophys Acta 1786, 126–138.
    [Google Scholar]
  98. Wang, Z. M., Li, X. N., Cocklin, R. R., Wang, M. H., Wang, M., Fukase, K., Inamura, S., Kusumoto, S., Gupta, D. & Dziarski, R. ( 2003; ). Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-l-alanine amidase. J Biol Chem 278, 49044–49052.[CrossRef]
    [Google Scholar]
  99. Wang, M., Liu, L.-H., Wang, S., Li, X., Lu, X., Gupta, D. & Dziarski, R. ( 2007; ). Human peptidoglycan recognition proteins require zinc to kill both Gram-positive and Gram-negative bacteria and are synergistic with antibacterial peptides. J Immunol 178, 3116–3125.[CrossRef]
    [Google Scholar]
  100. Wang, G., Li, X. & Wang, Z. ( 2009; ). APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res 37, D933–D937.[CrossRef]
    [Google Scholar]
  101. Webb, T. R. ( 2005; ). Current directions in the evolution of compound libraries. Curr Opin Drug Discov Devel 8, 303–308.
    [Google Scholar]
  102. Wenger, R. ( 1986; ). Cyclosporine and analogs – structural requirements for immunosuppressive activity. Transplant Proc 18, 213–218.
    [Google Scholar]
  103. Werner, T., Liu, G., Kang, D., Ekengren, S., Steiner, H. & Hultmark, D. ( 2000; ). A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci U S A 97, 13772–13777.[CrossRef]
    [Google Scholar]
  104. Wirsching, F., Keller, M., Hildmann, C., Riester, D. & Schwienhorst, A. ( 2003; ). Directed evolution towards protease-resistant hirudin variants. Mol Genet Metab 80, 451–462.[CrossRef]
    [Google Scholar]
  105. Woodburn, K. W., Wilson, S. D., Fong, K. L., Schatz, P. J., Spainhour, C. B. & Norton, D. ( 2009; ). Chronic pharmacological and safety evaluation of HematideTM, a PEGylated peptidic erythropoiesis-stimulating agent, in rodents. Basic Clin Pharmacol Toxicol 104, 155–163.[CrossRef]
    [Google Scholar]
  106. Wrighton, N. C., Farrell, F. X., Chang, R., Kashyap, A. K., Barbone, F. P., Mulcahy, L. S., Johnson, D. L., Barrett, R. W., Jolliffe, L. K. & Dower, W. J. ( 1996; ). Small peptides as potent mimetics of the protein hormone erythropoietin. Science 273, 458–463.[CrossRef]
    [Google Scholar]
  107. Yoshida, H., Kinoshita, K. & Ashida, M. ( 1996; ). Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J Biol Chem 271, 13854–13860.[CrossRef]
    [Google Scholar]
  108. Yoshioka, M., Fukuishi, N., Ku, Y., Yamanobe, H., Ohsaki, K., Kawasoe, Y., Murata, M., Ishzumi, A., Nishi, Y. & other authors ( 2008; ). Human cathelicidin CAP18/LL-37 changes mast cell function toward innate immunity. Biol Pharm Bull 31, 212–216.[CrossRef]
    [Google Scholar]
  109. Zaiou, M. ( 2007; ). Multifunctional antimicrobial peptides: therapeutic targets in several human diseases. J Mol Med 85, 317–329.[CrossRef]
    [Google Scholar]
  110. Zasloff, M. ( 1987; ). Magainins, a class of antimicrobial peptides from Xenopus skin – isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc Natl Acad Sci U S A 84, 5449–5453.[CrossRef]
    [Google Scholar]
  111. Zenke, G., Baumann, G., Wenger, R., Hiestand, P., Quesniaux, V., Andersen, E. & Schreier, M. H. ( 1993; ). Molecular mechanisms of immunosuppression by cyclosporins. Ann N Y Acad Sci 685, 330–335.[CrossRef]
    [Google Scholar]
  112. Zhang, Y., van der Fits, L., Voerman, J. S., Melief, M.-J., Laman, J. D., Wang, M., Wang, H., Wang, M., Li, X. & other authors ( 2005; ). Identification of serum N-acetylmuramoyl-l-alanine amidase as liver peptidoglycan recognition protein 2. Biochim Biophys Acta 1752, 34–46.[CrossRef]
    [Google Scholar]
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