Functions of antimicrobial peptides in gut homeostasis

Current Protein and Peptide Science

Volumn 16, Issue 7, 2015, Pages 582-591

  Wang, Shuai ^a   Thacker, Philip A ^b   Watford, Malcolm ^c   Qiao, Shiyan ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c the State University of New Jersey   (United States)

Author keywords

Antimicrobial peptides; Biology; Epithelial barrier; Gut homeostasis; Immune; Mechanisms

Indexed keywords

BACTERIOCIN; POLYPEPTIDE ANTIBIOTIC AGENT; ANTIMICROBIAL CATIONIC PEPTIDE;

ANTIMICROBIAL ACTIVITY; ARTICLE; CELL PERMEABILIZATION; CHEMICAL PHENOMENA; DRUG POTENTIATION; GUT HOMEOSTASIS; HOMEOSTASIS; HUMAN; IMMUNOMODULATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SYNTHESIS; ANIMAL; GASTROINTESTINAL TRACT; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PERMEABILITY; PHYSIOLOGY;

AMPHIBIA; BACTERIA (MICROORGANISMS); HEXAPODA; MAMMALIA;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INTESTINAL MUCOSA; PERMEABILITY;

EID: 84939816489     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/1389203716666150630135847     Document Type: Article

References (116)

1. Ganz, T. Defensins: Antimicrobial peptides of innate immunity. Nat. Rev. Immunol., 2003, 3(9), 710-720.
2. Lai, Y.; Gallo, R.L. AMPed up immunity: How antimicrobial peptides have multiple roles in immune defense. Trends Immunol., 2009, 30(3), 131-141.
3. Territo, M.C.; Ganz, T.; Selsted, M.E.; Lehrer, R. Monocytechemotactic activity of defensins from human neutrophils. J. Clin. Invest., 1989, 84(6), 2017-2020.
4. Mookherjee, N.; Brown, K.L.; Bowdish, D.M.; Doria, S.; Falsafi, R.; Hokamp, K.; Roche, F.M.; Mu, R.; Doho, G.H.; Pistolic, J.; Powers, J.P.; Bryan, J.; Brinkman, F.S.; Hancock, R.E. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J. Immunol., 2006, 176(4), 2455-2464.
5. Gracia, A.; Polewicz, M.; Halperin, S.A.; Hancock, R.E.; Potter, A.A.; Babiuk, L.A.; Gerdts, V. Antibody responses in adult and neonatal BALB/c mice to immunization with novel Bordetella pertussis vaccine formulations. Vaccine, 2011, 29(8), 1595-1604.
6. Klaenhammer, T.R. Genetics of bacteriocins produced by lactic acid bacteria. Fems. Microbiol. Rev., 1993, 12(1-3), 39-85.
7. Donini, M.; Lico, C.; Baschieri, S.; Conti, S.; Magliani, W.; Polonelli, L.; Benvenuto, E. Production of an engineered killer peptide in Nicotiana benthamiana by using a potato virus X expression system. Appl. Environ. Microbiol., 2005, 71(10), 6360-6367.
8. Liu, H.; Zhang, J.; Zhang, S.; Yang, F.; Thacker, P.A.; Zhang, G.; Qiao, S.; Ma, X. Oral administration of Lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets. J. Agric. Food Chem., 2014, 62(4), 860-866.
9. Bowdish, D.M.; Davidson, D.J.; Hancock, R.E. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr. Protein Pept. Sci., 2005, 6(1), 35-51.
10. Cotter, P.D.; Hill, C.; Ross, R.P. Bacteriocins: Developing innate immunity for food. Nat. Rev. Microbiol., 2005, 3(10), 777-788.
11. Kuipers, O.P.; Beerthuyzen, M.M.; Siezen, R.J.; Devos, W.M. Characterization of the nisin gene-cluster nisABTCIPR of lactococcus- lactis-requirement of expression of the nisa and nisi genes for development of immunity. Eur. J. Biochem., 1993, 216(1), 281- 291.
12. Siegers, K.; Heinzmann, S.; Entian, K.D. Biosynthesis of lantibiotic nisin. Posttranslational modification of its prepeptide occurs at a multimeric membrane-associated lanthionine synthetase complex. J. Biol. Chem., 1996, 271(21), 12294-12301.
13. Meyer, C.; Bierbaum, G.; Heidrich, C.; Reis, M.; Suling, J.; Iglesias- Wind, M.I.; Kempter, C.; Molitor, E.; Sahl, H.G. Nucleotide sequence of the lantibiotic Pep5 biosynthetic gene cluster and functional analysis of PepP and PepC. Evidence for a role of PepC in thioether formation. Eur. J. Biochem., 1995, 232(2), 478-489.
14. Peschel, A.; Gotz, F. Analysis of the Staphylococcus epidermidis genes epiF, -E, and -G involved in epidermin immunity. J. Bacteriol., 1996, 178(2), 531-536.
15. Chatterjee, S.; Chatterjee, S.; Lad, S.J.; Phansalkar, M.S.; Rupp, R.H.; Ganguli, B.N.; Fehlhaber, H.W.; Kogler, H. Mersacidin, a new antibiotic from Bacillus. Fermentation, isolation, purification and chemical characterization. J. Antibiot. (Tokyo), 1992, 45(6), 832-838.
16. Fredenhagen, A.; Fendrich, G.; Marki, F.; Marki, W.; Gruner, J.; Raschdorf, F.; Peter, H.H. Duramycins B and C, two new lanthionine containing antibiotics as inhibitors of phospholipase A2. Structural revision of duramycin and cinnamycin. J. Antibiot. (Tokyo), 1990, 43(11), 1403-1412.
17. Montville, T.J.; Chen, Y. Mechanistic action of pediocin and nisin: recent progress and unresolved questions. Appl. Microbiol. Biotechnol., 1998, 50(5), 511-519.
18. Parisien, A.; Allain, B.; Zhang, J.; Mandeville, R.; Lan, C.Q. Novel alternatives to antibiotics: Bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. J. Appl. Microbiol., 2008, 104(1), 1-13.
19. Boman, H.G. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol., 1995, 13, 61-92.
20. Steiner, H.; Hultmark, D.; Engstrom, A.; Bennich, H.; Boman, H.G. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature, 1981, 292(5820), 246-248.
21. Andreu, D.; Merrifield, R.B.; Steiner, H.; Boman, H.G. N-terminal analogues of cecropin A: Synthesis, antibacterial activity, and conformational properties. Biochemistry-US, 1985, 24(7), 1683-1688.
22. Cornet, B.; Bonmatin, J.M.; Hetru, C.; Hoffmann, J.A.; Ptak, M.; Vovelle, F. Refined three-dimensional solution structure of insect defensin A. Structure, 1995, 3(5), 435-448.
23. Maget-Dana, R.; Ptak, M. Penetration of the insect defensin A into phospholipid monolayers and formation of defensin A-lipid complexes. Biophys. J., 1997, 73(5), 2527-2533.
24. Simmaco, M.; Mignogna, G.; Barra, D. Antimicrobial peptides from amphibian skin: What do they tell us?. Biopolymers, 1998, 47(6), 435-450.
25. Papagianni, M. Ribosomally synthesized peptides with antimicrobial properties: Biosynthesis, structure, function, and applications. Biotechnol. Adv., 2003, 21 (6), 465-499.
26. Zasloff, M. 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., 1987, 84(15), 5449-5453.
27. Marion, D.; Zasloff, M.; Bax, A. A two-dimensional NMR study of the antimicrobial peptide magainin 2. FEBS Lett., 1988, 227(1), 21- 26.
28. Mor, A.; Nguyen, V.H.; Delfour, A.; Migliore-Samour, D.; Nicolas, P. Isolation, amino acid sequence, and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry- US, 1991, 30(36), 8824-8830.
29. Hernandez, C.; Mor, A.; Dagger, F.; Nicolas, P.; Hernandez, A.; Benedetti, E.L.; Dunia, I. Functional and structural damage in Leishmania mexicana exposed to the cationic peptide dermaseptin. Eur. J. Cell Biol., 1992, 59(2), 414-424.
30. Mor, A.; Hani, K.; Nicolas, P. The vertebrate peptide antibiotics dermaseptins have overlapping structural features but target specific microorganisms. J. Biol. Chem., 1994, 269(50), 31635-31641.
31. De Lucca, A.J.; Bland, J.M.; Jacks, T.J.; Grimm, C.; Walsh, T.J. Fungicidal and binding properties of the natural peptides cecropin B and dermaseptin. Med. Mycol., 1998, 36(5), 291-298.
32. Coote, P.J.; Holyoak, C.D.; Bracey, D.; Ferdinando, D.P.; Pearce, J.A. Inhibitory action of a truncated derivative of the amphibian skin peptide dermaseptin s3 on Saccharomyces cerevisiae. Antimicrob. Agents Chemother., 1998, 42(9), 2160-2170.
33. Martin, E.; Ganz, T.; Lehrer, R.I. Defensins and other endogenous peptide antibiotics of vertebrates. J. Leukoc. Biol., 1995, 58(2), 128-136.
34. Lehrer, R.I.; Ganz, T.; Selsted, M.E. Defensins: Endogenous antibiotic peptides of animal cells. Cell, 1991, 64(2), 229-230.
35. Bowdish, D.M.; Davidson, D.J.; Hancock, R.E. Immunomodulatory properties of defensins and cathelicidins. Curr. Top Microbiol. Immunol., 2006, 306, 27-66.
36. Lehrer, R.I.; Jung, G.; Ruchala, P.; Andre, S.; Gabius, H.J.; Lu, W. Multivalent binding of carbohydrates by the human alpha-defensin, HD5. J. Immunol., 2009, 183(1), 480-490.
37. Harder, J.; Bartels, J.; Christophers, E.; Schroder, J.M. Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. J. Biol. Chem., 2001, 276(8), 5707-5713.
38. Zanetti, M.; Gennaro, R.; Skerlavaj, B.; Tomasinsig, L.; Circo, R. Cathelicidin peptides as candidates for a novel class of antimicrobials. Curr. Pharm. Des., 2002, 8(9), 779-793.
39. 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(9), 1408-1425.
40. Frohm, N.M.; Sandstedt, B.; Sorensen, O.; Weber, G.; Borregaard, N.; Stahle-Backdahl, M. The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6. Infect. Immun., 1999, 67(5), 2561-2566.
41. Sochacki, K.A.; Barns, K.J.; Bucki, R.; Weisshaar, J.C. Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37. Proc. Natl. Acad. Sci. U. S. A., 2011, 108(16), E77- E81.
42. De Yang; Chen, Q.; Schmidt, A.P.; Anderson, G.M.; Wang, J.M.; Wooters, J.; Oppenheim, J.J.; Chertov, O. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med., 2000, 192(7), 1069-1074.
43. Boman, H.G.; Wade, D.; Boman, I.A.; Wahlin, B.; Merrifield, R.B. Antibacterial and antimalarial properties of peptides that are cecropin- melittin hybrids. Febs. Lett., 1989, 259(1), 103-106.
44. Chen, Y.; Mant, C.T.; Farmer, S.W.; Hancock, R.E.; Vasil, M.L.; Hodges, R.S. Rational design of alpha-helical antimicrobial peptides with enhanced activities and specificity/therapeutic index. J. Biol. Chem., 2005, 280(13), 12316-12329.
45. Hancock, R.E. Peptide antibiotics. Lancet, 1997, 349(9049), 418- 422.
46. Feng, X.; Liu, C.; Guo, J.; Bi, C.; Cheng, B.; Li, Z.; Shan, A.; Li, Z. Expression and purification of an antimicrobial peptide, bovine lactoferricin derivative LfcinB-W10 in Escherichia coli. Curr. Microbiol., 2010, 60(3), 179-184.
47. Wu, S.; Zhang, F.; Huang, Z.; Liu, H.; Xie, C.; Zhang, J.; Thacker, P.A.; Qiao, S. Effects of the antimicrobial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli. Peptides, 2012, 35(2), 225-230.
48. Mowat, A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol., 2003, 3(4), 331-341.
49. Johansson, M.E.; Phillipson, M.; Petersson, J.; Velcich, A.; Holm, L.; Hansson, G.C. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U. S. A., 2008, 105(39), 15064-15069.
50. Balda, M.S.; Matter, K. Tight junctions at a glance. J. Cell Sci., 2008, 121(Pt 22), 3677-3682.
51. Krause, G.; Winkler, L.; Mueller, S.L.; Haseloff, R.F.; Piontek, J.; Blasig, I.E. Structure and function of claudins. Biochim. Biophys. Acta, 2008, 1778(3), 631-645.
52. Turner, J.R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol., 2009, 9(11), 799-809.
53. Furuse, M.; Hirase, T.; Itoh, M.; Nagafuchi, A.; Yonemura, S.; Tsukita, S.; Tsukita, S. Occludin: A novel integral membrane protein localizing at tight junctions. J. Cell Biol., 1993, 123(6 Pt 2), 1777-1788.
54. Song, P.; Zhang, R.; Wang, X.; He, P.; Tan, L.; Ma, X. Dietary grape-seed procyanidins decreased post-weaning diarrhea by modulating intestinal permeability and suppressing oxidative stress in rats. J. Agric. Food Chem., 2011, 59(11), 6227-6232.
55. Ikenouchi, J.; Furuse, M.; Furuse, K.; Sasaki, H.; Tsukita, S.; Tsukita, S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J. Cell Biol., 2005, 171(6), 939-945.
56. Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell, 2010, 140(6), 805-820.
57. Lavelle, E.C.; Murphy, C.; O'Neill, L.A.; Creagh, E.M. The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol., 2010, 3(1), 17-28.
58. Kawai, T.; Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity, 2011, 34(5), 637-650.
59. Kawai, T.; Akira, S. TLR signaling. Cell Death Differ., 2006, 13(5), 816-825.
60. Chung, H.; Kasper, D.L. Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr. Opin. Immunol., 2010, 22(4), 455-460.
61. Rakoff-Nahoum, S.; Paglino, J.; Eslami-Varzaneh, F.; Edberg, S.; Medzhitov, R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell, 2004, 118(2), 229-241.
62. Yeretssian, G. Effector functions of NLRs in the intestine: Innate sensing, cell death, and disease. Immunol. Res., 2012, 54(1-3), 25- 36.
63. Podolsky, D.K. Review article: Healing after inflammatory injury-- coordination of a regulatory peptide network. Aliment. Pharmacol. Ther., 2000, 14(Suppl. 1), 87-93.
64. Yang, L.; Harroun, T.A.; Weiss, T.M.; Ding, L.; Huang, H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J., 2001, 81(3), 1475-1485.
65. Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta, 1999, 1462(1-2), 55-70.
66. Brotz, H.; Bierbaum, G.; Leopold, K.; Reynolds, P.E.; Sahl, H.G. The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob. Agents Chemother., 1998, 42(1), 154- 160.
67. Lehrer, R.I.; Barton, A.; Daher, K.A.; Harwig, S.S.; Ganz, T.; Selsted, M.E. Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity. J. Clin. Invest., 1989, 84(2), 553-561.
68. Bierbaum, G.; Sahl, H.G. Autolytic system of Staphylococcus simulans 22: Influence of cationic peptides on activity of Nacetylmuramoyl- L-alanine amidase. J. Bacteriol., 1987, 169(12), 5452-5458.
69. Zhao, H.; Kinnunen, P.K. Modulation of the activity of secretory phospholipase A2 by antimicrobial peptides. Antimicrob. Agents Chemother., 2003, 47(3), 965-971.
70. Matsuzaki, K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta, 1999, 1462(1-2), 1-10.
71. Tollin, M.; Bergman, P.; Svenberg, T.; Jornvall, H.; Gudmundsson, G.H.; Agerberth, B. Antimicrobial peptides in the first line defence of human colon mucosa. Peptides, 2003, 24(4), 523-530.
72. Iimura, M.; Gallo, R.L.; Hase, K.; Miyamoto, Y.; Eckmann, L.; Kagnoff, M.F. Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J. Immunol., 2005, 174(8), 4901-4907.
73. Ma, X.; Fan, P.X.; Li, L.S.; Qiao, S.Y.; Zhang, G.L.; Li, D.F. Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. J. Anim. Sci., 2012, 90 (Suppl 4), 266-268.
74. Tai, E.K.; Wu, W.K.; Wong, H.P.; Lam, E.K.; Yu, L.; Cho, C.H. A new role for cathelicidin in ulcerative colitis in mice. Exp. Biol. Med. (Maywood), 2007, 232(6), 799-808.
75. Tai, E.K.; Wong, H.P.; Lam, E.K.; Wu, W.K.; Yu, L.; Koo, M.W.; Cho, C.H. Cathelicidin stimulates colonic mucus synthesis by upregulating MUC1 and MUC2 expression through a mitogenactivated protein kinase pathway. J. Cell Biochem., 2008, 104(1), 251-258.
76. Tang, Z.R.; Deng, H.; Zhang, X.L.; Zen, Y.; Xiao, D.F.; Sun, W.Z.; Zhang, Z. Effects of orally administering the antimicrobial peptide buforin II on small intestinal mucosal membrane integrity, the expression of tight junction proteins and protective factors in weaned piglets challenged by enterotoxigenic Escherichia coli. Anim. Feed Sci. Tech., 2013, 186(3-4), 177-185.
77. Kiatsurayanon, C.; Niyonsaba, F.; Smithrithee, R.; Akiyama, T.; Ushio, H.; Hara, M.; Okumura, K.; Ikeda, S.; Ogawa, H. Host defense (Antimicrobial) peptide, human beta-defensin-3, improves the function of the epithelial tight-junction barrier in human keratinocytes. J. Invest. Dermatol., 2014, 134(8), 2163-2173.
78. Maher, S.; Feighery, L.; Brayden, D.J.; McClean, S. Melittin as an epithelial permeability enhancer I: Investigation of its mechanism of action in Caco-2 monolayers. Pharm. Res., 2007, 24(7), 1336- 1345.
79. Murphy, C.J.; Foster, B.A.; Mannis, M.J.; Selsted, M.E.; Reid, T.W. Defensins are mitogenic for epithelial cells and fibroblasts. J. Cell Physiol., 1993, 155(2), 408-413.
80. Gallo, R.L.; Ono, M.; Povsic, T.; Page, C.; Eriksson, E.; Klagsbrun, M.; Bernfield, M. Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc. Natl. Acad. Sci. U. S. A., 1994, 91(23), 11035- 11039.
81. Koczulla, R.; von Degenfeld, G.; Kupatt, C.; Krotz, F.; Zahler, S.; Gloe, T.; Issbruicker, K.; Unterberger, P.; Zaiou, M.; Lebherz, C.; Karl, A.; Raake, P.; Pfosser, A.; Boekstegers, P.; Welsch, U.; Hiemstra, P.S.; Vogelmeier, C.; Gallo, R.L.; Clauss, M.; Bals, R. An angiogenic role for the human peptide antibiotic LL-37/hCAP- 18. J. Clin. Invest., 2003, 111(11), 1665-1672.
82. Heilborn, J.D.; Nilsson, M.F.; Kratz, G.; Weber, G.; Sorensen, O.; Borregaard, N.; Stahle-Backdahl, M. The cathelicidin antimicrobial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J. Invest. Dermatol., 2003, 120(3), 379-389.
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(2), 549-553.
84. Yang, D.; Biragyn, A.; Kwak, L.W.; Oppenheim, J.J. Mammalian defensins in immunity: more than just microbicidal. Trends Immunol., 2002, 23(6), 291-296.
85. Niyonsaba, F.; Iwabuchi, K.; Matsuda, H.; Ogawa, H.; Nagaoka, I. Epithelial cell-derived human beta-defensin-2 acts as a chemotaxin for mast cells through a pertussis toxin-sensitive and phospholipase C-dependent pathway. Int. Immunol., 2002, 14(4), 421-426.
86. Yang, D.; Chertov, O.; Oppenheim, J.J. Participation of mammalian defensins and cathelicidins in anti-microbial immunity: receptors and activities of human defensins and cathelicidin (LL-37). J. Leukoc. Biol., 2001, 69(5), 691-697.
87. Yang, D.; Chertov, O.; Bykovskaia, S.N.; Chen, Q.; Buffo, M.J.; Shogan, J.; Anderson, M.; Schroder, J.M.; Wang, J.M.; Howard, O.M.; Oppenheim, J.J. Beta-defensins: Linking innate and adaptive immunity through dendritic and T cell CCR6. Science, 1999, 286(5439), 525-528.
88. Kurosaka, K.; Chen, Q.; Yarovinsky, F.; Oppenheim, J.J.; 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(10), 6257-6265.
89. Funderburg, N.; Lederman, M.M.; Feng, Z.; Drage, M.G.; Jadlowsky, J.; Harding, C.V.; Weinberg, A.; Sieg, S.F. Humandefensin- 3 activates professional antigen-presenting cells via Tolllike receptors 1 and 2. Proc. Natl. Acad. Sci. U. S. A., 2007, 104(47), 18631-18635.
90. Yu, J.; Mookherjee, N.; Wee, K.; Bowdish, D.M.; Pistolic, J.; Li, Y.; Rehaume, L.; Hancock, R.E. Host defense peptide LL-37, in synergy with inflammatory mediator IL-1beta, augments immune responses by multiple pathways. J. Immunol., 2007, 179(11), 7684- 7691.
91. Hurtado, P.; Peh, C.A. LL-37 promotes rapid sensing of CpG oligodeoxynucleotides by B lymphocytes and plasmacytoid dendritic cells. J. Immunol., 2010, 184(3), 1425-1435.
92. Brown, T.H.; David, J.; Acosta-Ramirez, E.; Moore, J.M.; Lee, S.; Zhong, G.; Hancock, R.E.; Xing, Z.; Halperin, S.A.; Wang, J. Comparison of immune responses and protective efficacy of intranasal prime-boost immunization regimens using adenovirus-based and CpG/HH2 adjuvanted-subunit vaccines against genital Chlamydia muridarum infection. Vaccine, 2012, 30(2), 350-360.
93. Zhang, L.; Falla, T.J. Antimicrobial peptides: Therapeutic potential. Expert. Opin. Pharmacother., 2006, 7(6), 653-663.
94. Hancock, R.E.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol., 2006, 24(12), 1551-1557.
95. Guell, I.; Cabrefiga, J.; Badosa, E.; Ferre, R.; Talleda, M.; Bardaji, E.; Planas, M.; Feliu, L.; Montesinos, E. Improvement of the efficacy of linear undecapeptides against plant-pathogenic bacteria by incorporation of D-amino acids. Appl. Environ. Microbiol., 2011, 77(8), 2667-2675.
96. Wade, D.; Boman, A.; Wahlin, B.; Drain, C.M.; Andreu, D.; Boman, H.G.; Merrifield, R.B. All-D amino acid-containing channel- forming antibiotic peptides. Proc. Natl. Acad. Sci. U. S. A., 1990, 87(12), 4761-4765.
97. Dean, S.N.; Bishop, B.M.; van Hoek, M.L. Natural and synthetic cathelicidin peptides with anti-microbial and anti-biofilm activity against Staphylococcus aureus. BMC Microbiol., 2011, 11, 114.
98. Wei, G.; de Leeuw, E.; Pazgier, M.; Yuan, W.; Zou, G.; Wang, J.; Ericksen, B.; Lu, W.Y.; Lehrer, R.I.; Lu, W. Through the looking glass, mechanistic insights from enantiomeric human defensins. J. Biol. Chem., 2009, 284(42), 29180-29192.
99. Yoon, J.H.; Ingale, S.L.; Kim, J.S.; Kim, K.H.; Lee, S.H.; Park, Y.K.; Kwon, I.K.; Chae, B.J. Effects of dietary supplementation of antimicrobial peptide-A3 on growth performance, nutrient digestibility, intestinal and fecal microflora and intestinal morphology in weanling pigs. Anim. Feed Sci. Tech., 2012, 177(1-2), 98-107.
100. Choi, S.C.; Ingale, S.L.; Kim, J.S.; Park, Y.K.; Kwon, I.K.; Chae, B.J. An antimicrobial peptide-A3: Effects on growth performance, nutrient retention, intestinal and faecal microflora and intestinal morphology of broilers. Brit. Poultry Sci., 2013, 54(6), 738-746.
101. Xiao, H.; Wu, M.M.; Tan, B.E.; Yin, Y.L.; Li, T.J.; Xiao, D.F.; Li, L. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: I. Growth performance, immune function, and antioxidation capacity. J. Anim. Sci., 2013, 91(10), 4772-4780.
102. Xiao, H.; Tan, B.E.; Wu, M.M.; Yin, Y.L.; Li, T.J.; Yuan, D.X.; Li, L. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: II. Intestinal morphology and function. J. Anim. Sci., 2013, 91(10), 4750-4756.
103. Wang, Q.; Zeng, X.; Wang, S.; Hou, C.; Yang, F.; Ma, X.; Thacker, P.; Qiao, S. The bacteriocin sublancin attenuates intestinal injury in young mice infected with Staphylococcus aureus. Anat. Rec. (Hoboken), 2014, 297(8), 1454-1461.
104. Chen, X.; Zhu, F.; Cao, Y.; Qiao, S. Novel expression vector for secretion of cecropin AD in Bacillus subtilis with enhanced antimicrobial activity. Antimicrob. Agents Chemother., 2009, 53(9), 3683-3689.
105. Yang, L.; Harroun, T.A.; Heller, W.T.; Weiss, T.M.; Huang, H.W. Neutron off-plane scattering of aligned membranes. I. Method Of measurement. Biophys. J., 1998, 75(2), 641-645.
106. Yamaguchi, S.; Hong, T.; Waring, A.; Lehrer, R.I.; Hong, M. Solid-state NMR investigations of peptide-lipid interaction and orientation of a beta-sheet antimicrobial peptide, protegrin. Biochemistry- Us, 2002, 41(31), 9852-9862.
107. Robinson, W.J.; McDougall, B.; Tran, D.; Selsted, M.E. Anti-HIV- 1 activity of indolicidin, an antimicrobial peptide from neutrophils. J. Leukoc. Biol., 1998, 63(1), 94-100.
108. Wachinger, M.; Kleinschmidt, A.; Winder, D.; von Pechmann, N.; Ludvigsen, A.; Neumann, M.; Holle, R.; Salmons, B.; Erfle, V.; Brack-Werner, R. Antimicrobial peptides melittin and cecropin inhibit replication of human immunodeficiency virus 1 by suppressing viral gene expression. J. Gen. Virol., 1998, 79(Pt 4), 731-740.
109. Garcia, J.R.; Jaumann, F.; Schulz, S.; Krause, A.; Rodriguez- Jimenez, J.; Forssmann, U.; Adermann, K.; Kluver, E.; Vogelmeier, C.; Becker, D.; Hedrich, R.; Forssmann, W.G.; Bals, R. Identification of a novel, multifunctional beta-defensin (human beta-defensin 3) with specific antimicrobial activity. Its interaction with plasma membranes of Xenopus oocytes and the induction of macrophage chemoattraction. Cell Tissue Res., 2001, 306(2), 257- 264.
110. Garcia, J.R.; Krause, A.; Schulz, S.; Rodriguez-Jimenez, F.J.; Kluver, E.; Adermann, K.; Forssmann, U.; Frimpong-Boateng, A.; Bals, R.; Forssmann, W.G. Human beta-defensin 4: A novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. Faseb. J., 2001, 15(10), 1819-1821.
111. Chertov, O.; Michiel, D.F.; Xu, L.; Wang, J.M.; Tani, K.; Murphy, W.J.; Longo, D.L.; Taub, D.D.; Oppenheim, J.J. Identification of defensin-1, defensin-2, and CAP37/azurocidin as T-cell chemoattractant proteins released from interleukin-8-stimulated neutrophils. J. Biol. Chem., 1996, 271(6), 2935-2940.
112. 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(3), 1636-1643.
113. Yoon, J.H.; Ingale, S.L.; Kim, J.S.; Kim, K.H.; Lohakare, J.; Park, Y.K.; Park, J.C.; Kwon, I.K.; Chae, B.J. Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J. Sci. Food Agr., 2013, 93(3), 587-592.
114. Choi, S.C.; Ingale, S.L.; Kim, J.S.; Park, Y.K.; Kwon, I.K.; Chae, B.J. Effects of dietary supplementation with an antimicrobial peptide- P5 on growth performance, nutrient retention, excreta and intestinal microflora and intestinal morphology of broilers. Anim. Feed Sci. Tech., 2013, 185(1-2), 78-84.
115. Gough, M.; Hancock, R.E.; Kelly, N.M. Antiendotoxin activity of cationic peptide antimicrobial agents. Infect. Immun., 1996, 64(12), 4922-4927.
116. Peng, Z.; Wang, A.; Feng, Q.; Wang, Z.; Ivanova, I.V.; He, X.; Zhang, B.; Song, W. High-level expression, purification and characterisation of porcine beta-defensin 2 in Pichia pastoris and its potential as a cost-efficient growth promoter in porcine feed. Appl. Microbiol. Biotechnol., 2014, 98(12), 5487-5497.