Quantification of bee-derived peptide defensin-1 in honey by competitive enzyme-linked immunosorbent assay, a new approach in honey quality control

https://doi.org/10.17221/422/2015-CJFSCitation:Ivana V., Marcela B., Juraj M. (2016): Quantification of bee-derived peptide defensin-1 in honey by competitive enzyme-linked immunosorbent assay, a new approach in honey quality control. Czech J. Food Sci., 34: 233-243.
download PDF
We established and evaluated a polyclonal antibody based competitive enzyme-linked immunosorbent assay for the quantification of defensin-1 in honey. The assay showed an inhibitory concentration (IC50) value of 111.5 ± 15.41 ng/ml with a detection limit of 7.8125 ng/ml. The regaining of defensin-1 in spiked ‘artificial honey’ was between 87.05 and 112.96% with relative standard deviation less than 9.2%. Sensitivity and specificity of the test were experimentally validated on a sample of 20 different honeys. The antibacterial activity of these honey samples showed a significant concentration-dependent correlation with the production of defensin-1 (n = 20; r = −0.6598; P = 0.0016). The assay provides a specific and sensitive method for the screening of defensin-1 in honey. The method to detect honeybee-derived proteins in honey is a promising approach to verifying the authenticity of honey. The defensin-1 ELISA could also be used for the rapid screening of honeys suitable for medicinal purposes.
References:
Adams Christopher. J., Boult Cherie H., Deadman Benjamin J., Farr Judie M., Grainger Megan N.C., Manley-Harris Merilyn, Snow Melanie J. (2008): Isolation by HPLC and characterisation of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey. Carbohydrate Research, 343, 651-659  https://doi.org/10.1016/j.carres.2007.12.011
 
Alvarez-Suarez José M., Giampieri Francesca, González-Paramás Ana M., Damiani Elisabetta, Astolfi Paola, Martinez-Sanchez Gregorio, Bompadre Stefano, Quiles José L., Santos-Buelga Celestino, Battino Maurizio (2012): Phenolics from monofloral honeys protect human erythrocyte membranes against oxidative damage. Food and Chemical Toxicology, 50, 1508-1516  https://doi.org/10.1016/j.fct.2012.01.042
 
Araújo C.A.C., Waniek P.J., Stock P., Mayer C., Jansen A.M., Schaub G.A. (2006): Sequence characterization and expression patterns of defensin and lysozyme encoding genes from the gut of the reduviid bug Triatoma brasiliensis. Insect Biochemistry and Molecular Biology, 36, 547-560  https://doi.org/10.1016/j.ibmb.2006.04.003
 
Bang Lynne M., Buntting Catherine, Molan Peter (2003): The Effect of Dilution on the Rate of Hydrogen Peroxide Production in Honey and Its Implications for Wound Healing. The Journal of Alternative and Complementary Medicine, 9, 267-273  https://doi.org/10.1089/10755530360623383
 
Baroni María V., Chiabrando Gustavo A., Costa Cristina, Fagúndez Guillermina A., Wunderlin Daniel A. (2004): Development of a Competitive ELISA for the Evaluation of Sunflower Pollen in Honey Samples. Journal of Agricultural and Food Chemistry, 52, 7222-7226  https://doi.org/10.1021/jf049068e
 
Bíliková Katarína, Šimúth Jozef (2010): New Criterion for Evaluation of Honey: Quantification of Royal Jelly Protein Apalbumin 1 in Honey by ELISA. Journal of Agricultural and Food Chemistry, 58, 8776-8781  https://doi.org/10.1021/jf101583s
 
Bucekova Marcela, Valachova Ivana, Kohutova Lenka, Prochazka Emanuel, Klaudiny Jaroslav, Majtan Juraj (2014): Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys. Naturwissenschaften, 101, 661-670  https://doi.org/10.1007/s00114-014-1205-z
 
Bulet P., Hetru C., Dimarcq J.L., Hoffmann D. (1999): Antimicrobial peptides in insects; structure and function. Developmental & Comparative Immunology, 23: 329–344.
 
Bulet P., Stocklin R. (2005): Insect antimicrobial peptides: structures, properties and gene regulation. Protein & Peptide Letters, 12: 3–11.
 
Buttstedt Anja, Moritz Robin F. A., Erler Silvio (2014): Origin and function of the major royal jelly proteins of the honeybee ( Apis mellifera ) as members of the yellow gene family. Biological Reviews, 89, 255-269  https://doi.org/10.1111/brv.12052
 
Casteels P. (1998): Immune response in Hymenoptera. In: Brey P.T., Hultmark D. (eds): Molecular Mechanisms of Immune Responses in Insect. London, Chapman & Hall: 92–10.
 
Casteels-Josson K., Zhang W., Capaci T., Casteels P., Tempst P. (1994): Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required posttranslational conversion of the precursor structures. Journal of Biological Chemistry, 269: 28569–28575.
 
Clinical and Laboratory Standards Institute (2003): Methods for dilution of antimicrobial susceptibility tests for bacteria that growth aerobically. Approved Standard, 6th Ed. NCCLS document M7-A6. Wayne, NCCLS.
 
Codex Alimentarius (2001): Codex Standard for Honey, Codex Stan 12-1981, Rev.1 (1987), Rev.2 (2001).
 
DeGrandi-Hoffman G., Hagler J. (2000): The flow of incoming nectar through a honey bee (Apis mellifera L.) colony as revealed by a protein marker. Insectes Sociaux, 47, 302-306  https://doi.org/10.1007/PL00001720
 
Dunford Cheryl, Cooper Rose, Molan Peter, White Richard (2000): The use of honey in wound management. Nursing Standard, 15, 63-68  https://doi.org/10.7748/ns2000.11.15.11.63.c2952
 
Eddy J.J., Gideonsen M.D. (2005): Topical honey for diabetic foot ulcers. Journal of Family Practice, 54: 533–535.
 
Elflein Lutz, Raezke Kurt-Peter (2008): Improved detection of honey adulteration by measuring differences between 13 C/ 12 C stable carbon isotope ratios of protein and sugar compounds with a combination of elemental analyzer - isotope ratio mass spectrometry and liquid chromatography - isotope ratio mass spectrometry (δ 13 C - EA/LC-IRMS). Apidologie, 39, 574-587  https://doi.org/10.1051/apido:2008042
 
Escuredo Olga, Míguez Montserrat, Fernández-González Maria, Carmen Seijo M. (2013): Nutritional value and antioxidant activity of honeys produced in a European Atlantic area. Food Chemistry, 138, 851-856  https://doi.org/10.1016/j.foodchem.2012.11.015
 
EU Council (2002): Council Directive 2001/110/EC of 20 December 2001 relating to honey. Official Journal of the European Communities, L 10: 47–52.
 
Fujiwara S., Imai J., Fujiwara M., Yaeshima T., Kawashima T., Kobayashi K. (1990). A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry, 265: 11333–11337.
 
Di Girolamo Francesco, D'Amato Alfonsina, Righetti Pier Giorgio (2012): Assessment of the floral origin of honey via proteomic tools. Journal of Proteomics, 75, 3688-3693  https://doi.org/10.1016/j.jprot.2012.04.029
 
Hanes Jozef, Šimuth Jozef (2015): Identification and partial characterization of the major royal jelly protein of the honey bee ( Apis mellifera L.). Journal of Apicultural Research, 31, 22-26  https://doi.org/10.1080/00218839.1992.11101256
 
Iglesias M. Teresa, Martín-Álvarez Pedro J., Polo M. Carmen, de Lorenzo Cristina, Pueyo Encarnación (2006): Protein Analysis of Honeys by Fast Protein Liquid Chromatography:  Application to Differentiate Floral and Honeydew Honeys. Journal of Agricultural and Food Chemistry, 54, 8322-8327  https://doi.org/10.1021/jf061900n
 
Kato Yoji, Araki Yukako, Juri Maki, Fujinaka Rie, Ishisaka Akari, Kitamoto Noritoshi, Nitta Yoko, Niwa Toshio, Takimoto Yosuke (2014): Immunochemical Authentication of Manuka Honey Using a Monoclonal Antibody Specific to a Glycoside of Methyl Syringate. Journal of Agricultural and Food Chemistry, 62, 10672-10678  https://doi.org/10.1021/jf503464a
 
Khan F., Hill J., Kaehler S., Allsopp M., van Vuuren S. (2014): Antimicrobial properties and isotope investigations of South African honey. Journal of Applied Microbiology, 117, 366-379  https://doi.org/10.1111/jam.12533
 
Kim Y.-J., Zitnan D., Cho K.-H., Schooley D. A., Mizoguchi A., Adams M. E. (): Central peptidergic ensembles associated with organization of an innate behavior. Proceedings of the National Academy of Sciences, 103, 14211-14216  https://doi.org/10.1073/pnas.0603459103
 
Kingan Timothy G, Zitnan Dusan, Jaffe Howard, Beckage N.E (1997): Identification of neuropeptides in the midgut of parasitized insects: FLRFamides as candidate paracrines. Molecular and Cellular Endocrinology, 133, 19-32  https://doi.org/10.1016/S0303-7207(97)00140-8
 
KLAUDINY J, ALBERT S, BACHANOVA K, KOPERNICKY J, SIMUTH J (2005): Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee. Insect Biochemistry and Molecular Biology, 35, 11-22  https://doi.org/10.1016/j.ibmb.2004.09.007
 
Klaudiny Jaroslav, Bachanová Katarína, Kohútová Lenka, Dzúrová Mária, Kopernický Ján, Majtán Juraj (2012): Expression of larval jelly antimicrobial peptide defensin1 in Apis mellifera colonies. Biologia, 67, 200-211  https://doi.org/10.2478/s11756-011-0153-8
 
Kwakman P. H. S., te Velde A. A., de Boer L., Speijer D., Vandenbroucke-Grauls C. M. J. E., Zaat S. A. J. (): How honey kills bacteria. The FASEB Journal, 24, 2576-2582  https://doi.org/10.1096/fj.09-150789
 
Kwakman Paulus H. S., te Velde Anje A., de Boer Leonie, Vandenbroucke-Grauls Christina M. J. E., Zaat Sebastian A. J., Cardona Pere-Joan (2011): Two Major Medicinal Honeys Have Different Mechanisms of Bactericidal Activity. PLoS ONE, 6, e17709-  https://doi.org/10.1371/journal.pone.0017709
 
Liu Fang, Li Wenfeng, Li Zhiguo, Zhang Shaowu, Chen Shenglu, Su Songkun (2011): High-abundance mRNAs in Apis mellifera: Comparison between nurses and foragers. Journal of Insect Physiology, 57, 274-279  https://doi.org/10.1016/j.jinsphys.2010.11.015
 
Majtan Juraj, Klaudiny Jaroslav, Bohova Jana, Kohutova Lenka, Dzurova Maria, Sediva Maria, Bartosova Maria, Majtan Viktor (2012): Methylglyoxal-induced modifications of significant honeybee proteinous components in manuka honey: Possible therapeutic implications. Fitoterapia, 83, 671-677  https://doi.org/10.1016/j.fitote.2012.02.002
 
Majtan J., Majtan V. (2010): Is manuka honey the best type of honey for wound care? Journal of Hospital Infection, 74: 305–306.
 
Marshall Thomas, Williams Katherine M. (1987): Electrophoresis of honey: Characterization of trace proteins from a complex biological matrix by silver staining. Analytical Biochemistry, 167, 301-303  https://doi.org/10.1016/0003-2697(87)90168-0
 
Mavric E., Wittmann S., Barth G., Henle T. (2008): Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Molecular Nutrition & Food Research, 52: 483–489.
 
Molan Peter C (): The Antibacterial Activity of Honey. Bee World, 73, 5-28  https://doi.org/10.1080/0005772X.1992.11099109
 
Molan P. C. (2006): The Evidence Supporting the Use of Honey as a Wound Dressing. The International Journal of Lower Extremity Wounds, 5, 40-54  https://doi.org/10.1177/1534734605286014
 
Oplatowska Michalina, Elliott Christopher T., Huet Anne-Catherine, McCarthy Mark, Mulder Patrick P. J., Holst Christoph, Delahaut Philippe, Egmond Hans P., Campbell Katrina (2014): Development and validation of a rapid multiplex ELISA for pyrrolizidine alkaloids and their N-oxides in honey and feed. Analytical and Bioanalytical Chemistry, 406, 757-770  https://doi.org/10.1007/s00216-013-7488-7
 
Eteraf-Oskouei T., Najafi M. (2013): Traditional and modern uses of natural honey in human diseases: a review. Iranian Journal of Basic Medical Sciences, 16: 731–742.
 
Sak-Bosnar Milan, Sakač Nikola (2012): Direct potentiometric determination of diastase activity in honey. Food Chemistry, 135, 827-831  https://doi.org/10.1016/j.foodchem.2012.05.006
 
Seeley ThomasD. (1992): The tremble dance of the honey bee: message and meanings. Behavioral Ecology and Sociobiology, 31, -  https://doi.org/10.1007/BF00170604
 
Tosun Murat (2013): Detection of adulteration in honey samples added various sugar syrups with 13C/12C isotope ratio analysis method. Food Chemistry, 138, 1629-1632  https://doi.org/10.1016/j.foodchem.2012.11.068
 
Valachová Ivana, Bohová Jana, Pálošová Zuzana, Takáč Peter, Kozánek Milan, Majtán Juraj (2013): Expression of lucifensin in Lucilia sericata medicinal maggots in infected environments. Cell and Tissue Research, 353, 165-171  https://doi.org/10.1007/s00441-013-1626-6
 
Wang J. -X., Zhao X. -F., Liang Y. -L., Li L., Zhang W., Ren Q., Wang L. -C., Wang L. -Y. (2006): Molecular characterization and expression of the antimicrobial peptide defensin from the housefly (Musca domestica). Cellular and Molecular Life Sciences, 63, 3072-3082  https://doi.org/10.1007/s00018-006-6284-3
 
Wang Sai, Liu Jiahui, Yong Wei, Chen Qilong, Zhang Liya, Dong Yiyang, Su Haijia, Tan Tianwei (2015): A direct competitive assay-based aptasensor for sensitive determination of tetracycline residue in Honey. Talanta, 131, 562-569  https://doi.org/10.1016/j.talanta.2014.08.028
 
Wang Rongmei, Wang Zhonghui, Yang Hong, Wang Yuzheng, Deng Anping (2012): Highly sensitive and specific detection of neonicotinoid insecticide imidacloprid in environmental and food samples by a polyclonal antibody-based enzyme-linked immunosorbent assay. Journal of the Science of Food and Agriculture, 92, 1253-1260  https://doi.org/10.1002/jsfa.4691
 
White Jonathan W., Subers Mary H., Schepartz Abner I. (1963): The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochimica et Biophysica Acta (BBA) - Specialized Section on Enzymological Subjects, 73, 57-70  https://doi.org/10.1016/0926-6569(63)90108-1
 
YAMAGUCHI Kikuji, HE Shaoyu, LI Zhengyue, MURATA Kiyoshi, HITOMI Nobuyuki, MOZUMI Manaho, ARIGA Risa, ENOMOTO Toshiki (): Quantification of Major Royal Jelly Protein 1 in Fresh Royal Jelly by Indirect Enzyme-Linked Immunosorbent Assay. Bioscience, Biotechnology and Biochemistry, 77, 1310-1312  https://doi.org/10.1271/bbb.130013
 
Yu F., Yu S., Yu L., Li Y., Wu Y., Zhang H., Qu L., Harrington P.B. (2013): Determination of residual enrofloxacin in food samples by a sensitive method of chemiluminescence enzyme immunoassay. Food Chemistry, 149: 71–75.
 
Zitnanova I., Adams M.E., Zitnan D. (2001): Dual ecdysteroid action on epitracheal glands and the central nervous system preceding ecdysis of Manduca sexta. Journal of Experimental Biology, 204: 3483–3495.
 
Adams Christopher. J., Boult Cherie H., Deadman Benjamin J., Farr Judie M., Grainger Megan N.C., Manley-Harris Merilyn, Snow Melanie J. (2008): Isolation by HPLC and characterisation of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey. Carbohydrate Research, 343, 651-659  https://doi.org/10.1016/j.carres.2007.12.011
 
Alvarez-Suarez José M., Giampieri Francesca, González-Paramás Ana M., Damiani Elisabetta, Astolfi Paola, Martinez-Sanchez Gregorio, Bompadre Stefano, Quiles José L., Santos-Buelga Celestino, Battino Maurizio (2012): Phenolics from monofloral honeys protect human erythrocyte membranes against oxidative damage. Food and Chemical Toxicology, 50, 1508-1516  https://doi.org/10.1016/j.fct.2012.01.042
 
Araújo C.A.C., Waniek P.J., Stock P., Mayer C., Jansen A.M., Schaub G.A. (2006): Sequence characterization and expression patterns of defensin and lysozyme encoding genes from the gut of the reduviid bug Triatoma brasiliensis. Insect Biochemistry and Molecular Biology, 36, 547-560  https://doi.org/10.1016/j.ibmb.2006.04.003
 
Bang Lynne M., Buntting Catherine, Molan Peter (2003): The Effect of Dilution on the Rate of Hydrogen Peroxide Production in Honey and Its Implications for Wound Healing. The Journal of Alternative and Complementary Medicine, 9, 267-273  https://doi.org/10.1089/10755530360623383
 
Baroni María V., Chiabrando Gustavo A., Costa Cristina, Fagúndez Guillermina A., Wunderlin Daniel A. (2004): Development of a Competitive ELISA for the Evaluation of Sunflower Pollen in Honey Samples. Journal of Agricultural and Food Chemistry, 52, 7222-7226  https://doi.org/10.1021/jf049068e
 
Bíliková Katarína, Šimúth Jozef (2010): New Criterion for Evaluation of Honey: Quantification of Royal Jelly Protein Apalbumin 1 in Honey by ELISA. Journal of Agricultural and Food Chemistry, 58, 8776-8781  https://doi.org/10.1021/jf101583s
 
Bucekova Marcela, Valachova Ivana, Kohutova Lenka, Prochazka Emanuel, Klaudiny Jaroslav, Majtan Juraj (2014): Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys. Naturwissenschaften, 101, 661-670  https://doi.org/10.1007/s00114-014-1205-z
 
Bulet P., Hetru C., Dimarcq J.L., Hoffmann D. (1999): Antimicrobial peptides in insects; structure and function. Developmental & Comparative Immunology, 23: 329–344.
 
Bulet P., Stocklin R. (2005): Insect antimicrobial peptides: structures, properties and gene regulation. Protein & Peptide Letters, 12: 3–11.
 
Buttstedt Anja, Moritz Robin F. A., Erler Silvio (2014): Origin and function of the major royal jelly proteins of the honeybee ( Apis mellifera ) as members of the yellow gene family. Biological Reviews, 89, 255-269  https://doi.org/10.1111/brv.12052
 
Casteels P. (1998): Immune response in Hymenoptera. In: Brey P.T., Hultmark D. (eds): Molecular Mechanisms of Immune Responses in Insect. London, Chapman & Hall: 92–10.
 
Casteels-Josson K., Zhang W., Capaci T., Casteels P., Tempst P. (1994): Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required posttranslational conversion of the precursor structures. Journal of Biological Chemistry, 269: 28569–28575.
 
Clinical and Laboratory Standards Institute (2003): Methods for dilution of antimicrobial susceptibility tests for bacteria that growth aerobically. Approved Standard, 6th Ed. NCCLS document M7-A6. Wayne, NCCLS.
 
Codex Alimentarius (2001): Codex Standard for Honey, Codex Stan 12-1981, Rev.1 (1987), Rev.2 (2001).
 
DeGrandi-Hoffman G., Hagler J. (2000): The flow of incoming nectar through a honey bee (Apis mellifera L.) colony as revealed by a protein marker. Insectes Sociaux, 47, 302-306  https://doi.org/10.1007/PL00001720
 
Dunford Cheryl, Cooper Rose, Molan Peter, White Richard (2000): The use of honey in wound management. Nursing Standard, 15, 63-68  https://doi.org/10.7748/ns2000.11.15.11.63.c2952
 
Eddy J.J., Gideonsen M.D. (2005): Topical honey for diabetic foot ulcers. Journal of Family Practice, 54: 533–535.
 
Elflein Lutz, Raezke Kurt-Peter (2008): Improved detection of honey adulteration by measuring differences between 13 C/ 12 C stable carbon isotope ratios of protein and sugar compounds with a combination of elemental analyzer - isotope ratio mass spectrometry and liquid chromatography - isotope ratio mass spectrometry (δ 13 C - EA/LC-IRMS). Apidologie, 39, 574-587  https://doi.org/10.1051/apido:2008042
 
Escuredo Olga, Míguez Montserrat, Fernández-González Maria, Carmen Seijo M. (2013): Nutritional value and antioxidant activity of honeys produced in a European Atlantic area. Food Chemistry, 138, 851-856  https://doi.org/10.1016/j.foodchem.2012.11.015
 
EU Council (2002): Council Directive 2001/110/EC of 20 December 2001 relating to honey. Official Journal of the European Communities, L 10: 47–52.
 
Fujiwara S., Imai J., Fujiwara M., Yaeshima T., Kawashima T., Kobayashi K. (1990). A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry, 265: 11333–11337.
 
Di Girolamo Francesco, D'Amato Alfonsina, Righetti Pier Giorgio (2012): Assessment of the floral origin of honey via proteomic tools. Journal of Proteomics, 75, 3688-3693  https://doi.org/10.1016/j.jprot.2012.04.029
 
Hanes Jozef, Šimuth Jozef (2015): Identification and partial characterization of the major royal jelly protein of the honey bee ( Apis mellifera L.). Journal of Apicultural Research, 31, 22-26  https://doi.org/10.1080/00218839.1992.11101256
 
Iglesias M. Teresa, Martín-Álvarez Pedro J., Polo M. Carmen, de Lorenzo Cristina, Pueyo Encarnación (2006): Protein Analysis of Honeys by Fast Protein Liquid Chromatography:  Application to Differentiate Floral and Honeydew Honeys. Journal of Agricultural and Food Chemistry, 54, 8322-8327  https://doi.org/10.1021/jf061900n
 
Kato Yoji, Araki Yukako, Juri Maki, Fujinaka Rie, Ishisaka Akari, Kitamoto Noritoshi, Nitta Yoko, Niwa Toshio, Takimoto Yosuke (2014): Immunochemical Authentication of Manuka Honey Using a Monoclonal Antibody Specific to a Glycoside of Methyl Syringate. Journal of Agricultural and Food Chemistry, 62, 10672-10678  https://doi.org/10.1021/jf503464a
 
Khan F., Hill J., Kaehler S., Allsopp M., van Vuuren S. (2014): Antimicrobial properties and isotope investigations of South African honey. Journal of Applied Microbiology, 117, 366-379  https://doi.org/10.1111/jam.12533
 
Kim Y.-J., Zitnan D., Cho K.-H., Schooley D. A., Mizoguchi A., Adams M. E. (): Central peptidergic ensembles associated with organization of an innate behavior. Proceedings of the National Academy of Sciences, 103, 14211-14216  https://doi.org/10.1073/pnas.0603459103
 
Kingan Timothy G, Zitnan Dusan, Jaffe Howard, Beckage N.E (1997): Identification of neuropeptides in the midgut of parasitized insects: FLRFamides as candidate paracrines. Molecular and Cellular Endocrinology, 133, 19-32  https://doi.org/10.1016/S0303-7207(97)00140-8
 
KLAUDINY J, ALBERT S, BACHANOVA K, KOPERNICKY J, SIMUTH J (2005): Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee. Insect Biochemistry and Molecular Biology, 35, 11-22  https://doi.org/10.1016/j.ibmb.2004.09.007
 
Klaudiny Jaroslav, Bachanová Katarína, Kohútová Lenka, Dzúrová Mária, Kopernický Ján, Majtán Juraj (2012): Expression of larval jelly antimicrobial peptide defensin1 in Apis mellifera colonies. Biologia, 67, 200-211  https://doi.org/10.2478/s11756-011-0153-8
 
Kwakman P. H. S., te Velde A. A., de Boer L., Speijer D., Vandenbroucke-Grauls C. M. J. E., Zaat S. A. J. (): How honey kills bacteria. The FASEB Journal, 24, 2576-2582  https://doi.org/10.1096/fj.09-150789
 
Kwakman Paulus H. S., te Velde Anje A., de Boer Leonie, Vandenbroucke-Grauls Christina M. J. E., Zaat Sebastian A. J., Cardona Pere-Joan (2011): Two Major Medicinal Honeys Have Different Mechanisms of Bactericidal Activity. PLoS ONE, 6, e17709-  https://doi.org/10.1371/journal.pone.0017709
 
Liu Fang, Li Wenfeng, Li Zhiguo, Zhang Shaowu, Chen Shenglu, Su Songkun (2011): High-abundance mRNAs in Apis mellifera: Comparison between nurses and foragers. Journal of Insect Physiology, 57, 274-279  https://doi.org/10.1016/j.jinsphys.2010.11.015
 
Majtan Juraj, Klaudiny Jaroslav, Bohova Jana, Kohutova Lenka, Dzurova Maria, Sediva Maria, Bartosova Maria, Majtan Viktor (2012): Methylglyoxal-induced modifications of significant honeybee proteinous components in manuka honey: Possible therapeutic implications. Fitoterapia, 83, 671-677  https://doi.org/10.1016/j.fitote.2012.02.002
 
Majtan J., Majtan V. (2010): Is manuka honey the best type of honey for wound care? Journal of Hospital Infection, 74: 305–306.
 
Marshall Thomas, Williams Katherine M. (1987): Electrophoresis of honey: Characterization of trace proteins from a complex biological matrix by silver staining. Analytical Biochemistry, 167, 301-303  https://doi.org/10.1016/0003-2697(87)90168-0
 
Mavric E., Wittmann S., Barth G., Henle T. (2008): Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Molecular Nutrition & Food Research, 52: 483–489.
 
Molan Peter C (): The Antibacterial Activity of Honey. Bee World, 73, 5-28  https://doi.org/10.1080/0005772X.1992.11099109
 
Molan P. C. (2006): The Evidence Supporting the Use of Honey as a Wound Dressing. The International Journal of Lower Extremity Wounds, 5, 40-54  https://doi.org/10.1177/1534734605286014
 
Oplatowska Michalina, Elliott Christopher T., Huet Anne-Catherine, McCarthy Mark, Mulder Patrick P. J., Holst Christoph, Delahaut Philippe, Egmond Hans P., Campbell Katrina (2014): Development and validation of a rapid multiplex ELISA for pyrrolizidine alkaloids and their N-oxides in honey and feed. Analytical and Bioanalytical Chemistry, 406, 757-770  https://doi.org/10.1007/s00216-013-7488-7
 
Eteraf-Oskouei T., Najafi M. (2013): Traditional and modern uses of natural honey in human diseases: a review. Iranian Journal of Basic Medical Sciences, 16: 731–742.
 
Sak-Bosnar Milan, Sakač Nikola (2012): Direct potentiometric determination of diastase activity in honey. Food Chemistry, 135, 827-831  https://doi.org/10.1016/j.foodchem.2012.05.006
 
Seeley ThomasD. (1992): The tremble dance of the honey bee: message and meanings. Behavioral Ecology and Sociobiology, 31, -  https://doi.org/10.1007/BF00170604
 
Tosun Murat (2013): Detection of adulteration in honey samples added various sugar syrups with 13C/12C isotope ratio analysis method. Food Chemistry, 138, 1629-1632  https://doi.org/10.1016/j.foodchem.2012.11.068
 
Valachová Ivana, Bohová Jana, Pálošová Zuzana, Takáč Peter, Kozánek Milan, Majtán Juraj (2013): Expression of lucifensin in Lucilia sericata medicinal maggots in infected environments. Cell and Tissue Research, 353, 165-171  https://doi.org/10.1007/s00441-013-1626-6
 
Wang J. -X., Zhao X. -F., Liang Y. -L., Li L., Zhang W., Ren Q., Wang L. -C., Wang L. -Y. (2006): Molecular characterization and expression of the antimicrobial peptide defensin from the housefly (Musca domestica). Cellular and Molecular Life Sciences, 63, 3072-3082  https://doi.org/10.1007/s00018-006-6284-3
 
Wang Sai, Liu Jiahui, Yong Wei, Chen Qilong, Zhang Liya, Dong Yiyang, Su Haijia, Tan Tianwei (2015): A direct competitive assay-based aptasensor for sensitive determination of tetracycline residue in Honey. Talanta, 131, 562-569  https://doi.org/10.1016/j.talanta.2014.08.028
 
Wang Rongmei, Wang Zhonghui, Yang Hong, Wang Yuzheng, Deng Anping (2012): Highly sensitive and specific detection of neonicotinoid insecticide imidacloprid in environmental and food samples by a polyclonal antibody-based enzyme-linked immunosorbent assay. Journal of the Science of Food and Agriculture, 92, 1253-1260  https://doi.org/10.1002/jsfa.4691
 
White Jonathan W., Subers Mary H., Schepartz Abner I. (1963): The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochimica et Biophysica Acta (BBA) - Specialized Section on Enzymological Subjects, 73, 57-70  https://doi.org/10.1016/0926-6569(63)90108-1
 
YAMAGUCHI Kikuji, HE Shaoyu, LI Zhengyue, MURATA Kiyoshi, HITOMI Nobuyuki, MOZUMI Manaho, ARIGA Risa, ENOMOTO Toshiki (): Quantification of Major Royal Jelly Protein 1 in Fresh Royal Jelly by Indirect Enzyme-Linked Immunosorbent Assay. Bioscience, Biotechnology and Biochemistry, 77, 1310-1312  https://doi.org/10.1271/bbb.130013
 
Yu F., Yu S., Yu L., Li Y., Wu Y., Zhang H., Qu L., Harrington P.B. (2013): Determination of residual enrofloxacin in food samples by a sensitive method of chemiluminescence enzyme immunoassay. Food Chemistry, 149: 71–75.
 
Zitnanova I., Adams M.E., Zitnan D. (2001): Dual ecdysteroid action on epitracheal glands and the central nervous system preceding ecdysis of Manduca sexta. Journal of Experimental Biology, 204: 3483–3495.
 
download PDF

© 2020 Czech Academy of Agricultural Sciences