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Avian antimicrobial proteins: structure, distribution and activity

Published online by Cambridge University Press:  21 September 2007

O. WELLMAN-LABADIE ,
J. PICMAN  and
M.T. HINCKE
O. WELLMAN-LABADIE
Affiliation:
Department of Biology, University of Ottawa, 30 Marie Curie, Ottawa, Ontario, Canada, K1N 6N5
J. PICMAN
Affiliation:
Department of Biology, University of Ottawa, 30 Marie Curie, Ottawa, Ontario, Canada, K1N 6N5
M.T. HINCKE*
Affiliation:
Department of Cellular and Molecular Medicine, University of Ottawa, 451 Smyth Road, Ottawa, Ontario, Canada, K1H 8M5
*
*Corresponding author: mhincke@uottawa.ca
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Abstract

Antimicrobial proteins are active against protozoans, fungi, viruses as well as gram-positive and gram-negative bacteria. In many cases, antimicrobial proteins are present as components of innate immunity and are capable of evading bacterial resistance mechanisms. Due to these characteristics, these proteins represent an appealing alternative to conventional antibiotic drugs. Considerable research has been conducted on antimicrobial proteins from invertebrate and mammalian sources. Within the last decade, over 20 novel antimicrobial proteins have been isolated from avian systems. The majority of these proteins has been isolated from the domestic chicken and therefore represents a minuscule fraction of the avian antimicrobial proteins that are potentially awaiting discovery. In this review, we elaborate on these discoveries and on the future of avian antimicrobial protein research.

Keywords

antimicrobialavianβ-defensincathelicidinlysozymetransferrin
Type
Review Article
Information
World's Poultry Science Journal , Volume 63 , Issue 3 , September 2007 , pp. 421 - 438
Copyright
Copyright © World's Poultry Science Association 2007

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References

AGUILERA, O., QUIROS, L.M. and FIERRO, J.F. (2003) Transferrins selectively cause ion efflux through bacterial and artificial membranes. FEBS Letter 548: 5–10.CrossRefGoogle ScholarPubMed
ANDREU, D. and RIVAS, L. (1998) Animal antimicrobial peptides: an overview. Biopolymers 47: 415–433.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
BANDYOPADHYAY, A. and BHATTACHARYYA, S.P. (1996) Influence of fowl uropygial gland and its secretory lipid components on growth of skin surface bacteria of fowl. Indian Journal of Experimental Biology 34(1): 48–52.Google ScholarPubMed
BANDYOPADHYAY, A. and BHATTACHARYYA, S.P. (1999) Influence of fowl uropygial gland and its secretory lipid components on the growth of skin surface fungi of fowl. Indian Journal of Experimental Biology 37(12): 1218–1222.Google ScholarPubMed
BERA, A., HERBERT, S., JAKOB, A., VOLLMER, W. and GOTZ, F. (2005) Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Molecular Microbiology 55(3): 778–787.CrossRefGoogle ScholarPubMed
BIRK, Y., KHALEF, S. and JIBSON, M.D. (1983) Purification and properties of protease F, a bacterial enzyme with chymotrypsin and elastase specificities. Archives of Biochemistry and Biophysics 225(2): 451–457.CrossRefGoogle ScholarPubMed
BROCKUS, C.W., JACKWOOD, M.W. and HARMON, B.G. (1998) Characterisation of β-defensin prepropeptide mRNA from chicken and turkey bone marrow. Animal Genetics 29: 283–289.CrossRefGoogle ScholarPubMed
BROQUIST, H.P. and SNELL, E.E. (1951) Biotin and bacterial growth. Relation to aspartate, oleata and carbon dioxide. Journal of Biological Chemistry 188(1): 431–444.CrossRefGoogle Scholar
BULET, P., STOCKLIN, R. and MENIN, L. (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunological Reviews 198: 169–184.CrossRefGoogle ScholarPubMed
BURLEY, R.W. and VADEHRA, D.V. (1989) The avian egg chemistry and biology. John Wiley and Sons Inc, New York.Google Scholar
CANFIELD, R.E. and MCMURRY, S. (1967) Purification and characterisation of a lysozyme from goose egg white. Biochemical and Biophysical research communications 26: 38–42.CrossRefGoogle ScholarPubMed
DAVIES, E.A., BEVIS, H.E. and DELVES-BROUGHTON, J. (1997) The use of the bacteriocin, nisin, as a preservative in ricotta-type cheeses to control the food-borne pathogen Listeria monocytogenes. Letters in Applied Microbiology 24: 343–346.CrossRefGoogle ScholarPubMed
DIANOUX, A-C. and JOLLES, P. (1967) A study of a lysozyme poor in cystine and tryptophan: the lysozyme of goose egg white. Biochimical et Biophysical Acta 133(3): 472–479.CrossRefGoogle ScholarPubMed
DEEMING, D.C. (1987) Effect of cuticle removal on the water vapour conductance of egg shells of several species of domestic bird. British Poultry Science 28: 231–237.CrossRefGoogle Scholar
EVANS, E.W., BEACH, G.G., WUNDERLICH, J. and HARMON, B.G. (1994) Isolation of antimicrobial peptides from avian heterophils. Journal of Leukocyte Biology 56: 661–665.CrossRefGoogle ScholarPubMed
EVANS, E.W., BEACH, G.G., MOORE, K.M., JACKWOOD, M.W., GLISSON, J.R. and HARMON, B.G. (1995) Antimicrobial activity of chicken and turkey heterophil peptides CHP1, CHP2, THP1 and THP3. Veterinary Microbiology 47: 295–303.CrossRefGoogle ScholarPubMed
FLORKIN, M., SCHEER, B.T. and BRUSH, A.H. (1978) Chemical zoology. Volume 10. Aves. Academic Press, New York, 436p.Google Scholar
GANZ, T. (2003) Defensins: antimicrobial peptides of innate immunity. Nature Reviews Immunology 3(9): 710–720.CrossRefGoogle ScholarPubMed
GAUTRON, J., HINCKE, M.T., PANHELEUX, M., BAIN, M., MCKEE, M.D., SOLOMON, S.E. and NYS, Y. (2001) Ovocalyxin-32, a novel chicken eggshell matrix protein. Isolation, amino acid sequencing, cloning, and immunocytochemical localization. Journal of Biological Chemistry 276(42): 39243–39252.CrossRefGoogle ScholarPubMed
GAUTRON, J., MURAYAMA, E., VIGNAL, A., MORISSON, M., MCKEE, M.D., REHAULT, S., VIDAL, M.L., NYS, Y. and HINCKE, M.T. (2007) Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins (LPB) bactericidal permeability-increasing proteins (BPI), and Plunc family proteins. Journal of Biological Chemistry 282(8): 5273–5286.CrossRefGoogle Scholar
GIANSANTI, F., ROSSI, P., MASSUCCI, M. T., BOTTI, D., ANTONINI, G., VALENTI, P. and SEGANTI, L. (2002) Antiviral activity of ovotransferrin discloses an evolutionary strategy for the defensive activities of lactoferrin. Biochemistry and Cell Biology 80: 125–130.CrossRefGoogle ScholarPubMed
GRAHAM, I. and WILLIAMS, J. (1975) A comparison of glycopeptides from the transferrins of several species. Biochemical Journal 145: 263–279.CrossRefGoogle Scholar
GREENGARD, O., SENTENAC, A. and MENDELSOHN, N. (1964) Phosvitin, the iron carrier of egg yolk. Biochimica et Biophysica Acta 90: 406–407.CrossRefGoogle ScholarPubMed
GUERIN-DUBIARD, C., PASCO, M., MOLLE, D., DESERT, C., CROGUENNEC, T. and NAU, F. (2006) Proteomic analysis of hen egg white. Journal of Agricultural and Food Chemistry 54: 3901–3910.CrossRefGoogle ScholarPubMed
HARMON, B.G. (1998) Avian heterophils in inflammation and disease resistance. Poultry Science 77: 972–977.CrossRefGoogle ScholarPubMed
HANCOCK, R.E.W. and CHAPPLE, D.S. (1999) Peptide Antibiotics. Antimicrobial Agents and Chemotherapy 43(6): 1317–1323.CrossRefGoogle ScholarPubMed
HARWIG, S.S.L., SWIDEREK, K.M., KOKRYAKOV, V.N., TAN, L., LEE, T.D., PANYUTICH, E.A., ALESHINA, G.A., SHAMOVA, O.V. and LEHRER, R.I. (1994) Gallinacins: cysteine-rich antimicrobial peptides of chicken leukocytes. FEBS Letters 342: 281–285.CrossRefGoogle ScholarPubMed
HEMMEN, F., MAHANA, W., JOLLES, P. and PARAF, A. (1992) Common antigenic properties of a g-type (goose) and a c-type (duck) egg white lysozyme: antibody response in rabbits and mice. Experientia 48: 79–84.Google Scholar
HERMANN, J., JOLLES, J. and JOLLES, P. (1971) Multiple forms of duck-egg white lysozyme. Primary structure of two duck lysozymes. European Journal of Biochemistry 24(1): 12–17.CrossRefGoogle ScholarPubMed
HIGGS, R., LYNN, D.J., GAINES, S., MCMAHON, J., TIERNEY, J., JAMES, T., LLOYD, A.T., MULCAHY, G. and O'FARRELLY, C. (2005) The synthetic form of a novel chicken β-defensin identified in silico is predominantly active against intestinal pathogens. Immunogenetics 57: 90–98.CrossRefGoogle ScholarPubMed
HINCKE, M.T., GAUTRON, J., PANHELEUX, M., GARCIA-RUIZ, J., MCKEE, M.D. and NYS, Y. (2000) Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biology 19: 443–453.CrossRefGoogle ScholarPubMed
HINCKE, M.T., GAUTRON, J., MANN, K., PANHÉLEUX, M., MCKEE, M.D., BAIN, M., SOLOMON, S.E. and NYS, Y. (2003) Purification of ovocalyxin-32, a novel chicken eggshell matrix protein. Connective Tissue Research 44(suppl. 1): 16–19.CrossRefGoogle ScholarPubMed
HINDENBURG, A., SPITZNAGEL, J. and ARNHEIM, N. (1974) Isozymes of lysozyme in leukocytes and egg white: evidence for the species-species control of egg-white lysozyme synthesis. Proceedings of the National Academy of Science 71(5): 1653–1657.CrossRefGoogle Scholar
HUMPHREY, T.J. and WHITEHEAD, A. (1993) Egg age and the growth of Salmonella enteritidis PT4 in egg contents. Epidemiology and Infection 111(2): 209–219.CrossRefGoogle ScholarPubMed
HUMPHREY, T.J., WHITEHEAD, A., GAWLER, A.H., HENLEY, A. and ROWE, B. (1991) Numbers of Salmonella enteritidis in the contents of naturally contaminated hen's eggs. Epidemiology and Infection 106(3): 489–496.CrossRefGoogle Scholar
IBRAHIM, H.R., HIGASHIGUCHI, S., JUNEJA, L.R., KIM, M. and YAMAMOTO, T. (1996) Astructural phase of heat-denatured lysozyme with novel antimicrobial action. Journal of Agriculture and Food Chemistry 44: 1416–1423.CrossRefGoogle Scholar
IBRAHIM, H.R., IWAMORI, E., SUGIMOTO, Y. and AOKI, T. (1998) Identification of a distinct antibacterial domain within the N-lobe of ovotransferrin. Biochimica et Biophysica Acta 1401: 289–303.CrossRefGoogle ScholarPubMed
IBRAHIM, H.R., SUGIMOTO, Y. and AOKI, T. (2000) Ovotransferrin antimicrobial peptide (OTAP-92) kills bacteria through a membrane damage mechanism. Biochimica et Biophysica Acta 1523: 196–205.CrossRefGoogle ScholarPubMed
IBRAHIM, H.R., MATSUZAKI, T. and AOKI, T. (2001a) Genetic evidence that antibacterial activity of lysozyme is independent of its catalytic function. FEBS Letters 506: 27–32.CrossRefGoogle ScholarPubMed
IBRAHIM, H.R., THOMAS, U. and PELLEGRINI, A. (2001b) A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action. Journal of Biological Chemistry 276(47): 43767–43774.CrossRefGoogle ScholarPubMed
IRWIN, D.M. and GONG, Z. (2003) Molecular evolution of vertebrate goose-type lysozyme genes. Journal of Molecular Evolution 56: 234–242.CrossRefGoogle ScholarPubMed
KAMYSZ, W. (2005) Are antimicrobial peptides an alternative for conventional antibiotics? Nuclear Medicine Review 8(1): 78–86.Google ScholarPubMed
KASSAIFY, Z.G. and MINE, Y. (2004) Effect of food protein supplements on Salmonella enteritidis infection and prevention in laying hens. Poultry Science 83: 753–760.CrossRefGoogle ScholarPubMed
KONDO, K., FUJIO, H. and AMANO, T. (1982) Chemical and immunological properties and amino acid sequences of three lysozymes from Peking-duck egg white. Journal of Biochemistry (Tokyo) 91(2): 571–587.CrossRefGoogle ScholarPubMed
KORANT, B.D., BRZIN, J. and TURK, V. (1985) Cystatin, a protein inhibitor of cysteine proteases alters viral protein cleavages in infected human cells. Biochemical and Biophysical Research Communications 127(3): 1072–1076.CrossRefGoogle ScholarPubMed
LANDON, C., THOUZEAU, C., LABBE, H., BULET, P. and VOVELLE, F. (2004) Solution structure of spheniscin, a β-defensin from the penguin stomach. Journal of Biological Chemistry 279(29): 30422–30439.CrossRefGoogle ScholarPubMed
LEE-HUANG, S., HUANG, P.L., SUN, Y., HUANG, P.L., KUMG, H.F., BITHE, D.L. and CHEN, H.C. (1999) Lysozyme RNases as anti-HIV components in beta-core preparations of human chorionic gonadotropin. Proceedings of the National Academy of Sciences of the United States of America 96: 2678–2681.CrossRefGoogle ScholarPubMed
LESNIEROWSKI, G., CEGIELSKA-RADZIEJEWSKA, R. and KIJOWSKI, J. (2004) Thermally and chemical-thermally modified lysozyme and its bacteriostatic activity. World's Poultry Science Journal 60: 303–309.CrossRefGoogle Scholar
LYNN, D.J., HIGGS, R., GAINES, S., TIERNEY, J., JAMES, T., LLOYD, A.T., FARES, M.A., MULCAHY, G. and O'FARRELLY, C. (2004) Bioinformatics discovery and initial characterisation of nine novel antimicrobial peptide genes in the chicken. Immunogenetics 56: 170–177.CrossRefGoogle ScholarPubMed
LYNN, D.J., HIGGS, R., LLOYD, A.T., O'FARRELLY, C., HERVE-GREPINET, V., NYS, Y., BRINKMAN, F.S., YU, P.L., SOULIER, A., KAISER, P., ZHANG, G. and LEHRER, R.I. (2007) Avian beta-defensin nomenclature: a community proposed update. Immunology Letters 110(1): 86–9.CrossRefGoogle ScholarPubMed
MANN, K., MACEK, B. and OLSEN, J. (2006) Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 6: 3801–3810.CrossRefGoogle ScholarPubMed
MARTENS, J-H., BARG, H., WARREN, M.J. and JAHN, D. (2002) Microbial production of vitamin B12. Applied Microbiology and Biotechnology 58: 275–285.CrossRefGoogle ScholarPubMed
MARTIN-PLATERO, A.M., VALDIVIA, E., RUIZ-RODRIGUEZ, M., SOLER, J.J., MARTIN-VIVALDI, M., MAQUEDA, M. and MARTINEZ-BUENO, M. (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10–3, isolated from the uropygial gland of the hoopoe (Upupoe epops). Applied and Environmental Microbiology 72(6): 4245–4249.CrossRefGoogle ScholarPubMed
MATSUZAKI, K. (2001) Why and how are peptide-lipid interactions utilized for self defence? Biochemical Society Transactions 29(3): 598–601.CrossRefGoogle ScholarPubMed
MINE, Y., OBERLE, C. and KASSAIFY, Z. (2003) Eggshell matrix proteins as defense mechanism of avian eggs. Journal of Agriculture and Food Chemistry 51(1): 249–253.CrossRefGoogle ScholarPubMed
MINE, Y., MA, F. and LAURIAU, S. (2004) Antimicrobial peptides released by enzymatic hydrolysis of hen egg white lysozyme. Journal of Agricultural and Food Chemistry 52: 1088–1094.CrossRefGoogle ScholarPubMed
MIYAGAWA, S., MATSUMOTO, K., KAMATA, R., OKAMURA, R. and MAEDA, H. (1991a) Spreading of Serratia marcescens in experimental keratitis and growth suppression by chicken egg white ovomacroglobulin. Japanese Journal of Ophthalmology 35(3): 402–410.Google ScholarPubMed
MIYAGAWA, S., KAMATA, R., MATSUMOTO, K., OKAMURA, R. and MAEDA, H. (1991b) Inhibitory effects of ovomacroglobulin on bacterial kerititis in rabbits. Graefe's Archive for Clinical and Experimental Opthalmology 229(3): 281–286.CrossRefGoogle ScholarPubMed
MOLLA, A., MATSUMURA, Y., YAMAMOTO, T., OKAMURA, R. and MAEDA, H. (1987) Pathogenic capacity of proteases from Serratia marcescens and Pseudomonas aeruginosa and their suppression by chicken egg white ovomacroglobulin. Infection and Immunity 55(10): 2509–2517.CrossRefGoogle ScholarPubMed
MUNIYAPPA, K. and ADIGA, P.R. (1979) Isolation and characterization of thiamine-binding protein chicken egg white. Biochemistry Journal 177: 887–894.CrossRefGoogle Scholar
NAKANO, T. and GRAF, T. (1991) Goose-type lysozyme gene of the chicken: sequence, genomic organisation and expression reveals major differences to chicken-type lysozyme gene. Biochimica et Biophysica Acta 1090: 273–276.CrossRefGoogle ScholarPubMed
NAKIMBUGWE, D., MASSCHALCK, B., ATANASSOVA, M., ZEWDIE-BOSUNER, A. and MICHIELS, C.W. (2006) Comparison of bactericidal activity of six lysozymes at atmospheric pressure and under high hydrostatic pressure. International Journal of Food Microbiology 108(3): 355–363.Google ScholarPubMed
NILE, C.J., TOWNES, C.L., HIRST, B.H. and HALL, J. (2006) The novel avian protein, AWAK, contains multiple domains with homology to protease inhibitory modules. Molecular Immunology 43: 388–394.CrossRefGoogle ScholarPubMed
OHASHI, H., SUBEDI, K., NISHIBORI, M., ISOBE, N. and YOSHIMURA, Y. (2005) Expressions of antimicrobial peptide gallinacin-1,-2 and -3 mRNA in the oviduct of laying hens. The Journal of Poultry Science 42: 337–345.CrossRefGoogle Scholar
PELLEGRINI, A., HULSMEIER, A.J., HUNZIKER, P. and THOMAS, U. (2004) Proteolytic fragments of ovalbumin display antimicrobial activity. Biochimica et Biophysica Acta 1672: 76–85.CrossRefGoogle ScholarPubMed
PHELPS, C.F. and ANTONINI, E. (1975) A study of the kinetics of iron and copper binding to hen ovotransferrin. Biochemical Journal 147: 385–391.CrossRefGoogle ScholarPubMed
POOART, J., TORIKATA, T. and ARAKI, T. (2004) The primary structure of a novel goose-type lysozyme from rhea egg white. Bioscience Biotechnology and Biochemistry 68(1): 159–169.CrossRefGoogle ScholarPubMed
POOART, J., TORIKATA, T. and ARAKI, T. (2005) Enzymatic properties of rhea lysozyme. Bioscience Biotechnology and Biochemistry 69(1): 103–112.CrossRefGoogle ScholarPubMed
PRAGER, E.M. and JOLLES, P. (1996) Animal lysozymes c and g: an overview. EXS 75: 9–31.Google Scholar
PRAGER, E.M. and WILSON, A.C. (1974) Widespread distribution of lysozyme g in egg white of birds. Journal of Biological Chemistry 249(22): 7295–7297.CrossRefGoogle ScholarPubMed
RAMANATHAN, B., DAVIS, E.G., ROSS, C.R. and BLECHA, F. (2002) Cathelicidins: microbicidal activity, mechanisms of action, and roles in innate immunity. Microbes and Infection 4: 361–372.CrossRefGoogle ScholarPubMed
RAWAS, A., MORETON, K., MUIRHEAD, H. and WILLIAMS, J. (1989) Preliminary crystallographic studies on duck ovotransferrin. Journal of Molecular Biology 208: 213–214.CrossRefGoogle ScholarPubMed
READ, R.J., FUJINAGA, M., SIELECKI, A.R. and JAMES, M.N. (1983) Structure of the complex of Streptomyces griseus protease B and the third domain of the turkey ovomucoid inhibitor at 1.8-A resolution. Biochemistry 22(19): 4420–4233.CrossRefGoogle Scholar
REDDY, K.V.R., ARANHA, C., GUPTA, S.M. and YEDERY, R.D. (2004) Evaluation of antimicrobial peptide nisin as a safe vaginal contraceptive agent in rabbits: in vitro and in vivo studies. Reproduction 128: 117–126.CrossRefGoogle ScholarPubMed
RICHARDS, M.P. (1997) Trace mineral metabolism in the avian embryo. Poultry Science 76: 152–164.CrossRefGoogle ScholarPubMed
ROSE, E.M. and ORLANS, E. (1981) Immunoglobulins in the egg, embryo and young chick. Developmental and Comparative Immunology 5(1): 15–20.CrossRefGoogle ScholarPubMed
ROSE, E.M., ORLANS, E. and BUTTRESS, N. (1974) Immunoglobulin classes in the hen's egg: their segregation in yolk and white. European Journal of Immunology 4(7): 521–523.CrossRefGoogle ScholarPubMed
SATTAR KHAN, M.A., NAKAMURA, S., OGAWA, M., AKITA, E., AZAKAMI, H. and KATO, A. (2000) Bactericidal action of egg yolk phosvitin against Escherichia coli under thermal stress. Journal of Agricultural and Food Chemistry 48(5): 1503–1506.CrossRefGoogle ScholarPubMed
SAVA, G. (1996) Pharmacological aspects and therapeutic applications of lysozymes. Experimental Science 75: 433–449.Google ScholarPubMed
SEVIOUR, E.M. and BOARD, R.G. (1972) Bacterial growth in albumin taken from the eggs of domestic hens and waterfowl. British Poultry Science 13: 557–575.CrossRefGoogle ScholarPubMed
SHAWKEY, M.D., PILLAI, S.R. and HILL, G.E. (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. Journal of Avian Biology 34(3): 345–349.CrossRefGoogle Scholar
SHELBURNE, C.E., AN, F.Y., DHOLPE, V., RAMAMOORTHY, A., LOPATIN, D.E. and LANTZ, M.S. (2007) The spectrum of antimicrobial activity of the bacteriocin subtilosin A. Journal of Antimicrobial Chemotherapy 59(2): 297–300.CrossRefGoogle ScholarPubMed
SILPHADUANG, U., HINCKE, M.T., NYS, Y. and MINE, Y. (2006) Antimicrobial proteins in chicken reproductive system. Biochemical and Biophysical Research Communications 340: 648–655.CrossRefGoogle ScholarPubMed
SUGIARTO, H. and YU, P-L. (2004) Avian antimicrobial peptides: the defense role of β-defensins. Biochemical and Biophysical Research Communications 323: 721–727.CrossRefGoogle ScholarPubMed
SUGIARTO, H. and YU, P-L. (2006) Identification of three novel ostricacins: an update on the phylogenetic perspective of β-defensins. International Journal of Antimicrobial Agents 27: 229–235.CrossRefGoogle ScholarPubMed
SUPURAN, C.T., SCOZZAFAVA, A. and CLARE, B.W. (2002) Bacterial Protease Inhibitors. Medical Research Reviews 22: 329–372.CrossRefGoogle ScholarPubMed
TABORSKY, G. (1980) Iron binding by phosvitin and its conformational consequences. Journal of Biological Chemistry 255(7): 2976–2985.CrossRefGoogle ScholarPubMed
TENNESSEN, J.A. (2005) Molecular evolution of animal antimicrobial peptides: widespread moderate positive selection. Journal of Evolutionary Biology 18: 1387–1394.CrossRefGoogle ScholarPubMed
THAMMASIRIRAK, S., TORIKATA, T., TAKAMI, K., MURATA, K. and ARAKI, T. (2001) Purification and characterisation of goose type lysozyme from cassowary (Casuarius casuarius) egg white. Bioscience Biotechnology and Biochemistry 65(3): 584–592.CrossRefGoogle ScholarPubMed
THOUZEAU, C., LE MAHO, Y., FROGET, G., SABATIER, L., LE BOHEC, C., HOFFMANN, J.A. and BULET, P. (2003) Spheniscins, avian β-defensins in preserved stomach contents of the king penguin, Aptenodytes patagonicus. Journal of Biological Chemistry 278(51): 51053–51058.CrossRefGoogle ScholarPubMed
TOWNES, C.L., MICHAILIDIS, G., NILE, C.J. and HALL, J. (2004) Induction of cationic chicken liver-expressed antimicrobial peptide 2 in response to salmonella enterica infection. Infection and Immunity: 6987–6993.CrossRefGoogle ScholarPubMed
TOWNES, C.L., MILONA, P. and HALL, J. (2006) Characterization of AWAP IV, the C-terminal domain of the avian protein AWAK. Biochemical Society Transactions 34(2): 267–269.CrossRefGoogle ScholarPubMed
TSUGE, Y., SHIMOYAMADA, M. and WATANABE, K. (1996a) Binding of egg white proteins to viruses. Bioscience, Biotechnology and Biochemistry 60: 1503–1504.CrossRefGoogle ScholarPubMed
TSUGE, Y., SHIMOYAMADA, M. and WATANABE, K. (1996b) Differences in hemagglutination inhibition activity against bovine rotavirus and hen Newcastle disease virus based on the subunits in hen egg white ovomucin. Bioscience, Biotechnology and Biochemistry 60: 1505–1506.CrossRefGoogle ScholarPubMed
TSUGE, Y., SHIMOYAMADA, M. and WATANABE, K. (1997a) Structural features of Newcastle disease virus- and anti-ovomucin antibody-binding glycopeptides from pronase-treated ovomucin. Journal of Agricultural and Food Chemistry 45: 2393–2398.CrossRefGoogle Scholar
TSUGE, Y., SHIMOYAMADA, M. and WATANABE, K. (1997b) Bindings of ovomucin to Newcastle disease virus and anti-ovomucin antibodies and its heat stability based on binding abilities. Journal of Agricultural and Food Chemistry 45: 4629–4634.CrossRefGoogle Scholar
VALENTI, P., DE STASIO, A., MASTROMERINO, P., SEGANTI, L., SINIBALDI, L. and ORSI, N. (1981a) Influence of bicarbonate and citrate on the bacteriostatic action of ovotransferrin towards staphylococci. FEMS Microbiology Letters 10: 77–79.CrossRefGoogle Scholar
VALENTI, P., GUARINO, M., VISCA, P., VON HUNOLSTEIN, , ANTONINI, G., DE STASIO, A. and ORSI, N. (1981b) Resistance of genus proteus to ovotransferrin. Bollettino dell'Istituto sieroterapico Milanese 60(3): 284–287.Google ScholarPubMed
VALENTI, P., ANTONINI, G., ROSSI FANELLI, M.R., ORSI, N. and ANTONINI, E. (1982) Antibacterial activity of matrix-bound ovotransferrin. Antimicrobial Agents and Chemotherapy 21(5): 840–841.CrossRefGoogle ScholarPubMed
VALENTI, P., ANTONINI, G., VON HUNOLSTEIN, C., VISCA, P., ORSI, N. and ANTONINI, E. (1983) Studies on the antimicrobial activity of ovotransferrin. International Journal of Tissue Reactions V(1): 97–105.Google Scholar
VALENTI, P., VISCA, P., ANTONINI, G. and ORSI, N. (1985) Antifungal activity of ovotransferrin towards genus candida. Mycopathologia 89: 169–175.CrossRefGoogle ScholarPubMed
VALENTI, P., VISCA, P., ANTONINI, G., ORSI, N. and ANTONINI, E. (1987) The effect of saturation with Zn2+ and other metal ions on the antibacterial activity of ovotransferrin. Medical Microbiology and Immunology 176: 123–130.CrossRefGoogle ScholarPubMed
VAN DIJK, A., VELDHUIZEN, E.J.A., VAN ASTEN, A.J.A.M. and HAAGSMAN, H.P. (2005) CMAP27, a novel chicken cathelicidin-like antimicrobial protein. Veterinary Immunology and Immunopathology 106: 321–327.CrossRefGoogle ScholarPubMed
VON HUNOLSTEIN, C., RICCI, M.L., VALENTI, P. and OREFICI, G. (1992) Lack of activity of transferrins towards streptococcus spp. Medical Microbiology Immunology 181: 351–357.CrossRefGoogle ScholarPubMed
WATANABE, K., YSUGE, Y., SHIMOYAMADA, M., OGAMA, N. and EBINA, T. (1998) Antitumor effects of pronase-treated fragments, glycopeptides, from ovomucin in hen egg white in a double grafted tumor system. Journal of Agriculture and Food Chemistry 46: 3033–3038.CrossRefGoogle Scholar
XIAO, Y., HUGHES, A.L., ANDO, J., MATSUDA, Y., CHENG, J-F., SKINNER-NOBLE, D. and ZHANG, G. (2004) A genome-wide screen identifies a single β-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genomics 5: 56.CrossRefGoogle ScholarPubMed
XIAO, Y., CAI, Y., BOMMINENI, Y.R., FERNANDO, S.C., PRAKASH, O., GILLILAND, S.E. and ZHANG, G. (2006a) Identification and functional characterisation of three chicken cathelicidins with potent antimicrobial activity. Journal of Biological Chemistry 281(5): 2858–2867.CrossRefGoogle ScholarPubMed
XIAO, Y., DAI, H., BOMMINENI, Y.R., SOULAGES, J.L., GONG, Y-X., PRAKASH, O. and ZHANG, G. (2006b) Structure-activity relationships of fowlicidin-1, a cathelicidin antimicrobial peptide in the chicken. FEBS Journal 273: 2581–2593.CrossRefGoogle Scholar
XING, J., WELLMAN-LABADIE, O., GAUTRON, J. and HINCKE, M.T. (2007) Recombinant eggshell ovocalyxin-32: expression, purification and biological activity of the glutathione S-transferase fusion protein. Comparative Biochemistry and Physiology B 147: 172–177.CrossRefGoogle ScholarPubMed
YU, P-L., CHOUDHURY, S.D. and AHRENS, K. (2001) Purification and characterisation of the antimicrobial peptide, ostricacin. Biotechnology Letters 23: 207–210.CrossRefGoogle Scholar
YOSHIMURA, Y., OHASHI, H., SUBEDI, K., NISHIBORI, M. and ISOBE, N. (2006) Effects of age, egg-laying activity, and salmonella-inoculation on the expressions of gallinacin mRNA in the vagina of the hen oviduct. Journal of Reproduction and Development 52(2): 211–218.CrossRefGoogle ScholarPubMed
ZHAO, C., NGUYEN, T., LIU, L., SACCO, R.E., BROGDEN, K.A. and LEHRER, R.I. (2001) Gallinacin-3, an inducible epithelial β-defensin in the chicken. Infection and Immunity: 2684–2691.CrossRefGoogle ScholarPubMed