Insect proteins as a potential source of antimicrobial peptides in livestock production. A review

• Autorzy: Jozefiak A. , Engberg R.M.
• Języki publikacji: EN

Abstrakty

EN

Together with the extraction of first insect antimicrobial protein (AMP) from the pupae of the giant silk moths Hyalophora cecropia the antibacterial activity of insects was observed for the first time in 1980. Practically, AMPs are small, cationic proteins that exhibit activity against bacteria, fungi as well as certain parasites and viruses. It is known that in addition to their antimicrobial effect, they boost host specific innate immune responses and exert selective immunomodulatory effects involved in angiogenesis and wound healing. More than 1,500 proteins with antimicrobial activity have been identified in different organisms, including plants, fungi, bacteria and animals. Insects are a primary source of AMPs which are considered as not resulting in the development of natural bacterial resistance. In general, they are characterized as heat-stable with no adverse effects on eukaryotic cells. These characteristics contribute to the potential use of these proteins in human and veterinary medicine and in animal nutrition. Depending on their mode of action, insect AMPs may be applied as single peptides, as a complex of different AMPs and as an active fraction of insect proteins in the nutrition of different livestock. The great potential for the use of AMPs in animal production is primarily associated with the growing problem of antibiotics resistance, which has triggered the search for alternatives to antibiotics in livestock production. The review presents the current knowledge of insect AMPs, their chemical structure and mode of action with focus on their potential use in agriculture and livestock production.

• Wydawca: -
• Czasopismo: Journal of Animal and Feed Sciences
• Rocznik: 2017
• Tom: 26
• Numer: 2
• Opis fizyczny: P.87–99,fig.

Twórcy

autor

Jozefiak A.

• Poznan University of Life Sciences, Institute of Veterinary Sciences, Wolynska 35, 60-637 Poznan, Poland

autor

Engberg R.M.

• Aarhus University, Department of Animal Science Blichers Alle 20, 8830 Tjele, Denmark

Bibliografia

• Aerts A.M., François I.E.J.A., Cammue B.P.A., Thevissen K., 2008. The mode of antifungal action of plant, insect and human defensins. Cell. Mol. Life Sci. 65, 2069–2079, https://doi.org/10.1007/s00018-008-8035-0
• Andersen A.S., Sandvang D., Schnorr K.M., Kruse T., Neve S., Joergensen B., Karlsmark T., Krogfelt K.A., 2010. A novel approach to the antimicrobial activity of maggot debridementtherapy. J. Antimicrob. Chemother. 65, 1646–1654, https://doi.org/10.1093/jac/dkq165
• Andersson D.I., Hughes D., Kubicek-Sutherland J.Z., 2016. Mechanisms and consequences of bacterial resistance to antimicrobial peptides. Drug Resist. Updates 26, 43–57, https://doi.org/10.1016/j.drup.2016.04.002
• BagnickaE., JóźwikA.,StrzałkowskaN.,Krzyżewski J.,ZwierzchowskiL., 2011. Antimicrobial peptides – outline of the history of studies and mode of action (in Polish). Med. Wet. 67, 444–448
• Bengoechea J.A., SkurnikM., 2000. Temperature-regulated efflux pump/ potassium antiporter system mediates resistance to cationic antimicrobial peptides in Yersinia. Mol. Microbiol. 37, 67–80, https://doi.org/10.1046/j.1365-2958.2000.01956.x
• Boman H.G., Nilsson-Faye I., Paul K., Rasmuson T. Jr, 1974. Insect immunity. I. Characteristics of an inducible cell-free antibacterial reaction in hemolymph of Samia cynthia pupae. Infect. Immun. 10, 136–145
• Bovera F., Loponte R., Marono S., Piccolo G., Parisi G., Iaconisi V., Gasco L., Nizza A., 2016. Use of Tenebrio molitor larvae meal as protein source in broiler diet: Effect on growth performance, nutrient digestibility, and carcass and meat traits. J. Anim. Sci. 94, 639–647, https://doi.org/10.2527/jas.2015-9201
• Buchon N., Silverman N., Cherry S., 2014. Immunity in Drosophila melanogaster – from microbial recognition to whole-organism physiology. Nat. Rev. Immunol. 14, 796–810, https://doi.org/10.1038/nri3763
• Bulet P., Stöcklin R., 2005. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12, 3–11, https://doi.org/10.2174/0929866053406011
• Bulet P., Stöcklin R., Menin L., 2004. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 198, 169–184, https://doi.org/10.1111/j.0105-2896.2004.0124.x
• Cheng J.-x., Liu Y.-g., Suo W.-l., Zhao R.-j., Fan H.-y., 2010. Effects of the antimicrobial peptide of Tenebrio molitor Linnaeus on cell cycle of K562 and inhibitory effects of that on cell proliferation compared with hydroxyurea. Chin. J. Vector Biol. Control 21, 324–326
• Chernysh S., Gordya N., Suborova T., 2015. Insect antimicrobial peptide complexes prevent resistance development in bacteria. PLoS ONE 10, e0130788, https://doi.org/10.1371/journal.pone.0130788
• Choi S.C., Ingale S.L., Kim J.S., Park Y.K., Kwon I.K., Chae B.J., 2013a. 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. Technol. 185, 78–84, https://doi.org/10.1016/j.anifeedsci.2013.07.005
• Choi S.C., Ingale S.L., Kim J.S., Park Y.K., Kwon I.K., Chae B.J., 2013b. An antimicrobial peptide-A3: effects on growth performance, nutrient retention, intestinal and faecal microflora and intestinal morphology of broilers. Br. Poult. Sci. 54, 738–746, https://doi.org/10.1080/00071668.2013.838746
• Choi W.-H., Yun J.-H., Chu J.-P., Chu K.-B., 2012. Antibacterial effect of extracts of Hermetia illucens (Diptera: Stratiomyidae) larvae against Gram-negative bacteria. Entomol. Res. 42, 219–226, https://doi.org/10.1111/j.1748-5967.2012.00465.x
• Coyne L.A., Latham S.M., Williams N.J., Dawson S., Donald I.J., Pearson R.B., Smith R.F., Pinchbeck G.L., 2016. Understanding the culture of antimicrobial prescribing in agriculture: a qualitative study of UK pig veterinary surgeons. J. Antimicrob.Chemother. 71, 3300–3312, https://doi.org/10.1093/jac/dkw300
• Dang X.L., Wang Y.S., Huang Y.D., Yu X.Q., Zhang W.Q., 2010. Purification and characterization of an antimicrobial peptide, insect defensin, from immunized house fly (Diptera: Muscidae). J. Med. Entomol. 47, 1141–1145, https://doi.org/10.1603/ME10016
• Duclohier H., 2002. How do channel- and pore-forming helical peptides interact with lipid membranes and how does this account for their antimicrobial activity? Mini-Rev. Med. Chem. 2, 331–342, https://doi.org/10.2174/1389557023405963
• El-Tantawy N.L., 2015. Helminthes and insects: maladies or therapies. Parasitol. Res. 114, 359–377, https://doi.org/10.1007/s00436-014-4260-7
• Erickson M.C., Islam M., Sheppard C., Liao J., Doyle M.P., 2004. Reduction of Escherichia coli O157:H7 and Salmonella enterica serovar Enteritidis in chicken manure by larvae of the black soldier fly. J. Food Prot. 67, 685–690, https://doi.org/10.4315/0362-028X-67.4.685
• Faye I., Pye A., Rasmuson T., Boman H.G., Boman I.A., 1975. Insect immunity: II. Simultaneous induction of antibacterial activity and selective synthesis of some haemolymph proteins in diapausing pupae of Hyalophora cecropia and Samia cynthia. Infect. Immun. 12, 1426–1438
• Frick I.-M., Åkesson P., Rasmussen M., Schmidtchen A., Björck L., 2003. SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J. Biol. Chem. 278, 16561–16566, https://doi.org/10.1074/jbc.M301995200
• Fu P., Wu J., Guo G., 2009. Purification and molecular identification of an antifungal peptide from the hemolymph of Musca domestica (housefly). Cell. Mol. Immunol. 6, 245–251, https://doi.org/10.1038/cmi.2009.33
• Groisman E.A., Parra-Lopez C., Salcedo M., Lipps C.J., Heffron F., 1992. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc. Natl. Acad. Sci. USA 89, 11939–11943, https://doi.org/10.1073/pnas.89.24.11939
• Guina T., Yi E.C., Wang H., Hackett M., Miller S.I., 2000. A PhoPregulated outer membrane protease of Salmonella enterica serovar typhimurium promotes resistance to alpha-helical antimicrobial peptides. J. Bacteriol. 182, 4077–4086, https://doi.org/10.1128/JB.182.14.4077-4086.2000
• Hancock R.E.W., Chapple D.S., 1999. Peptide antibiotics. Antimicrob. Agents Chemother. 43, 1317–1323
• Hansen A., Schäfer I., Knappe D., Seibel P., Hoffmann R., 2012. Intracellular toxicity of proline-rich antimicrobial peptides shuttled into mammalian cells by the cell-penetrating peptide penetration. Antimicrob. Agents Chemother. 56, 5194–5201, https://doi.org/10.1128/AAC.00585-12
• Hull R., Katete R., Ntwasa M., 2012. Therapeutic potential of antimicrobial peptides from insects. Biotechnol. Mol. Biol. Rev. 7, 31–47
• Hultmark D., Steiner H., Rasmuson T., Boman H.G., 1980. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur. J. Biochem. 106, 7–16, https://doi.org/10.1111/j.1432-1033.1980.tb05991.x
• Imler J.-L., Hoffmann J.A., 2000. Signaling mechanisms in the antimicrobial host defense of Drosophila. Curr. Opin. Microbiol. 3, 16–22, https://doi.org/10.1016/S1369-5274(99)00045-4
• Jin T., Bokarewa M., Foster T., Mitchell J., Higgins J., Tarkowski A., 2004. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172, 1169–1176, https://doi.org/10.4049/jimmunol.172.2.1169
• 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
• Jones D.E., Bevins C.L., 1992. Paneth cells of the human small intestine express an antimicrobial peptide gene. J. Biol. Chem. 267, 23216–23225
• Joo H.-S., Fu C.-I., Otto M., 2016. Bacterial strategies of resistance to antimicrobial peptides. Philos. Trans. R. Soc. B-Biol. Sci. 371, 20150292, https://doi.org/10.1098/rstb.2015.0292
• Józefiak D., Józefiak A., Kierończyk B., Rawski M., Świątkiewicz S., Długosz J., Engberg R.M., 2016. Insects – a natural nutrient source for poultry – a review. Ann. Anim. Sci. 16, 297–313, https://doi.org/10.1515/aoas-2016-0010
• Józefiak D., Kierończyk B., Juśkiewicz J., Zduńczyk Z., Rawski M., Długosz J., Sip A., Højberg O., 2013. Dietary nisin modulates the gastrointestinal microbial ecology and enhances growth performance of the broiler chickens. PLoS ONE 8, e85347, https://doi.org/10.1371/journal.pone.0085347
• Kierończyk B., Pruszyńska-Oszmałek E., Świątkiewicz S., Rawski M., Długosz J., Engberg R.M., Józefiak D., 2016. The nisin improves broiler chicken growth performance and interacts with salinomycin in terms of gastrointestinal tract microbiota composition. J. Anim. Feed Sci. 25, 309–316, https://doi.org/10.22358/jafs/67802/2016
• Kim I.-W., Lee J.H., Subramaniyam S., Yun E.-Y., Kim I., Park J., Hwang J.S., 2016. De novo transcriptome analysis and detection of antimicrobial peptides of the American cockroach Periplaneta americana (Linnaeus). PLoS ONE, 11, e0155304, https://doi.org/10.1371/journal.pone.0155304
• Kragol G., Hoffmann R., Chattergoon M.A., Lovas S., Cudic M., Bulet P., Condie B.A., Rosengren K.J., Montaner L.J., Otvos L. Jr, 2002. Identification of crucial residues for the antibacterial activity of the proline-rich peptide, pyrrhocoricin. Eur. J. Biochem. 269, 4226–4237, https://doi.org/10.1046/j.1432-1033.2002.03119.x
• Lamberty M., Zachary D., Lanot R., Bordereau C., Robert A., Hoffmann J.A., Bulet P., 2001. Inect immunity. Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J. Biol. Chem. 276, 4085–4092, https://doi.org/10.1074/jbc.M002998200
• Landers T.F., Cohen B., Wittum T.E., Larson E.L., 2012. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep. 127, 4–22
• Lee K.H., Hong S.Y., Oh J.E., 1998. Synthesis and structure-function study about tenecin 1, an antibacterial protein from larvae of Tenebrio molitor. FEBS Lett. 439, 41–45, https://doi.org/10.1016/S0014-5793(98)01333-7
• Lee S., Siddiqui R., Khan N.A., 2012. Animals living in polluted environments are potential source of antimicrobials against infectious agents. Pathog. Glob. Health 106, 218–223, https://doi.org/10.1179/2047773212Y.0000000033
• Lee Y.-T., Kim D.-H., Suh J.-Y., Chung J.H., Lee B.L., Lee Y., Choi B.-S., 1999. Structural characteristics of tenecin 3, an insect antifungal protein. IUBMB Life 47, 369–376, https://doi.org/10.1080/15216549900201393
• Lehrer R.I., Ganz T., 1990.polypeptides of human neutrophils. Blood 76, 2169–2181
• Li W.-F., Ma G.-X., Zhou X.-X., 2006. Apidaecin-type peptides: Biodiversity, structure–function relationships and mode of action. Peptides 27, 2350–2359, https://doi.org/10.1016/j.peptides.2006.03.016
• Li Y., Xiang Q., Zhang Q., Huang Y., Su Z., 2012. Overview on the recent study of antimicrobial peptides: Origins, functions, relative mechanisms and application. Peptides 37, 207–215, https://doi.org/10.1016/j.peptides.2012.07.001
• Luenser K., Ludwig A., 2005. Variability and evolution of bovine β-defensin genes. Genes Immun. 6, 115–122, https://doi.org/10.1038/sj.gene.6364153
• Makkar H.P.S., Tran G., Heuzé V., Ankers P., 2014. State-of-the-art on use of insects as animal feed. Anim. Feed Sci. Technol. 197, 1–33, https://doi.org/10.1016/j.anifeedsci.2014.07.008
• Mattiuzzo M., Bandiera A., Gennaro R., Benincasa M., Pacor S., Antcheva N., Scocchi M., 2007. Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides. Mol. Microbiol. 66, 151–163, https://doi.org/10.1111/j.1365-2958.2007.05903.x
• McCoy A.J., Liu H., Falla T.J., Gunn J.S., 2001. Identification of Proteus mirabilis mutants with increased sensitivity to antimicrobial peptides. Antimicrob. Agents Chemother. 45, 2030–2037, https://doi.org/10.1128/AAC.45.7.2030-2037.2001
• McPhee J.B., Scott M.G., Hancock R.E.W., 2005. Design of host defence peptides for antimicrobial and immunity enhancing activities. Comb. Chem. High Throughput Screen 8, 257–272, https://doi.org/10.2174/1386207053764558
• Narayanan S., Modak J.K., Ryan C.S., Garcia-Bustos J., Davies J.K., Roujeinikova A., 2014. Mechanism of Escherichia coli resistance to pyrrhocoricin. Antimicrob. Agents Chemother. 58, 2754–2762, https://doi.org/10.1128/AAC.02565-13
• Nicolas P., 2009. Multifunctional host defence peptides: intracellulartargeting antimicrobial peptides. FEBS J. 276, 6483–6496, https://doi.org/10.1111/j.1742-4658.2009.07359.x
• OuelletteA.J., Darmoul D., Tran D., Huttner K.M., Yuan J., Selsted M.E., 1999. Peptide localization and gene structure of cryptdin 4, a differentially expressed mouse paneth cell α-defensin. Infect. Immun. 67, 6643–6651
• Park S.-I., Chang B.S., Yoe S.M., 2014. Detection of antimicrobial substances from larvae of the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae). Entomol. Res. 44, 58–64, https://doi.org/10.1111/1748-5967.12050
• Park S.-I., Kim J.-W., Yoe S.M., 2015. Purification and characterization of a novel antibacterial peptide from black soldier fly (Hermetia illucens) larvae. Dev. Comp. Immunol. 52, 98–106, https://doi.org/10.1016/j.dci.2015.04.018
• Park Y., Hahm K.-S., 2005. Antimicrobial peptides (AMPs): peptide structure and mode of action. J. Biochem. Mol. Biol. 38, 507–516, https://doi.org/10.5483/bmbrep.2005.38.5.507
• Peschel A., Vuong C., Otto M., Götz F., 2000. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antomicrob. Agents Chemother. 44, 2845–2847, https://doi.org/10.1128/AAC.44.10.2845-2847.2000
• Ratcliffe N.A., Mello C.B., Garcia E.S., Butt T.M., Azambuja P., 2011. Insect natural products and processes: New treatments for human disease. Insect Biochem. Mol. Biol. 41, 747–769, https://doi.org/10.1016/j.ibmb.2011.05.007
• Rodríguez-Rojas A., Makarova O., Rolff J., 2014. Antimicrobials, stress and mutagenesis. PLoS Pathog. 10, e1004445, https://doi.org/10.1371/journal.ppat.1004445
• RotemS., MorA., 2009. Antimicrobial peptide mimics for improved therapeutic properties. Biochim. Biophys. Acta-Biomembr. 178, 1582–1592, https://doi.org/10.1016/j.bbamem.2008.10.020
• Sánchez-Muros M.J., Barroso F.G., Manzano-Agugliaro F., 2014. Insect meal as renewable source of food for animal feeding: a review. J. Clean. Prod. 65, 16–27, https://doi.org/10.1016/j.jclepro.2013.11.068
• Schiappa J., Van Hee R., 2012. From ants to staples: history and ideas concerning suturing techniques. Acta Chir. Belg. 2012, 112, 395–402, https://doi.org/10.1080/00015458.2012.11680861
• Seo M.-D., Won H.-S., Kim J.-H., Mishig-Ochir T., Lee B.-J., 2012. Antimicrobial peptides for therapeutic applications: a review. Molecules 17, 12276–12286, https://doi.org/10.3390/molecules171012276
• Shafer W.M., Qu X.-D., Waring A.J., Lehrer R.I., 1998. Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc. Natl. Acad. Sci. USA 95, 1829–1833, https://doi.org/10.1073/pnas.95.4.1829
• Steiner H., Hultmark D., Engström A., Bennich H., Boman H.G., 1981. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292, 246–248, https://doi.org/10.1038/292246a0
• Stumpe S., Schmid R., Stephens D.L., Georgiou G., Bakker E.P., 1998. Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J. Bacteriol. 180, 4002–4006
• Sun H.-X., Chen L.-Q., Zhang J., Chen F.-Y., 2014. Anti-tumor and immunomodulatory activity of peptide fraction from the larvae of Musca domestica. J. Ethnopharmacol. 153, 831–839, https://doi.org/10.1016/j.jep.2014.03.052
• Tang X., Fatufe A.A., Yin Y., Tang Z., Wang S., Liu Z., Xinwu, Li T.-J., 2012. Dietary supplementation with recombinant lactoferrampin-lactoferricin improves growth performance and affects serum parameters in piglets. J. Anim. Vet. Adv. 11, 2548–2555, https://doi.org/10.3923/javaa.2012.2548.2555
• Tang Z., Yin Y., Zhang Y. et al., 2009. Effects of dietary supplementation with an expressed fusion peptide bovine lactoferricin-lactoferrampin on performance, immune function and intestinal mucosal morphology in piglets weaned at age 21 d. Br. J. Nutr. 101, 998–1005, https://doi.org/10.1017/S0007114508055633
• Uvell H., Engström Y., 2007. A multilayed defense against infection: combinatorial control of insect immune genes. Trends Genet. 23, 342–349, https://doi.org/10.1016/j.tig.2007.05.003
• Wang S., Zeng X., Yang Q., Qiao S., 2016. Antimicrobial peptides as potential alternatives to antibiotics in food animal industry. Int. J. Mol. Sci. 17, 603–614, https://doi.org/10.3390/ijms17050603
• Wang Y.-Z., Shan T.-Z., Xu Z.-R., Feng J., Wang Z.-Q., 2007. Effects of the lactoferrin (LF) on the growth performance, intestinal microflora and morphology of weanling pigs. Anim. Feed Sci. Technol. 135, 263–272, https://doi.org/10.1016/j.anifeedsci.2006.07.013
• Wen L.-F., He J.-G., 2012. Dose-response effects of an antimicrobial peptide, a cecropin hybrid, on growth performance, nutrient utilisation, bacterial counts in the digesta and intestinal morphology in broilers. Br. J. Nutr. 108, 1756–1763, https://doi.org/10.1017/S0007114511007240
• Wu S., Zhang F., Huang Z., Liu H., Xie C., Zhang J., Thacker P.A., Qiao S., 2012. Effects of the antimicrobial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli. Peptides 35, 225–230, https://doi.org/10.1016/j.peptides.2012.03.030
• Xiao H., Shao F., Wu M., Ren W., Xiong X., Tan B., Yin Y., 2015a. The application of antimicrobial peptides as growth and health promoters for swine. J. Anim. Sci. Biotechnol. 6, 19, https://doi.org/10.1186/s40104-015-0018-z
• Xiao H., Tan B.E., Wu M.M., Yin Y.L., Li T.J., Yuan D.X., Li L., 2013a. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: II. Intestinal morphology and function. J. Anim. Sci. 91, 4750–4756, https://doi.org/10.2527/jas.2013-6427
• Xiao H., Wu M.M., Shao F.Y. et al., 2015b. Metabolic profiles in the response to supplementation with composite antimicrobial peptides in piglets challenged with deoxynivalenol. J. Anim. Sci. 93, 1114–1123, https://doi.org/10.2527/jas.2014-8229
• Xiao H., Wu M.M., Tan B.E., Yin Y.L., Li T.J., Xiao D.F., Li L., 2013b. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: I. Growth performance, immune function, and antioxidation capacity. J. Anim. Sci. 91, 4772–4780, https://doi.org/10.2527/jas.2013-6426
• Xiong X., Yang H.S., Li L., Wang Y.F., Huang R.L., Li F.N., Wang S.P., Qiu W., 2014. Effects of antimicrobial peptides in nursery diets on growth performance of pigs reared on five different farms. Livest. Sci. 167, 206–210, https://doi.org/10.1016/j.livsci.2014.04.024
• Yi H.-Y., Chowdhury M., Huang Y.-D., Yu X.-Q., 2014. Insect antimicrobial peptides and their applications. Appl. Microbiol. Biotechnol. 98, 5807–5822, https://doi.org/10.1007/s00253-014-5792-6
• Yoon J.H., Ingale S.L., Kim J.S., Kim K.H., Lee S.H., Park Y.K., Kwon I.K., Chae B.J., 2012. 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. Technol. 177, 98–107, https://doi.org/10.1016/j.anifeedsci.2012.06.009
• Yoon J.H., Ingale S.L., KimJ.S., KimK.H., Lee S.H., Park Y.K., Lee S.C., Kwon I.K., Chae B.J., 2014. Effects of dietary supplementation of synthetic antimicrobial peptide-A3 and P5 on growth performance, apparent total tract digestibility of nutrients, fecal and intestinal microflora and intestinal morphology in weanling pigs. Livest. Sci. 159, 53–60, https://doi.org/10.1016/j.livsci.2013.10.025
• 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., 2013. 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 Agric. 93, 587–592, https://doi.org/10.1002/jsfa.5840
• Żyłowska M., Wyszyńska A., Jagusztyn-Krynicka E.K., 2011. Antimicrobial peptides – defensins (in Polish). Post. Mikrobiol. 50, 223–234

Identyfikatory

DOI

10.22358/jafs/69998/2017