Determination of total protein, trans- 10-Hydroxy-2-Decenoic Acid (10-HDA) and major royal jelly proteins in royal jelly produced at different harvest times in queenless and queenright colonies

Year 2022, Volume: 26 Issue: 1, 109 - 117, 25.03.2022

Aytül Uçak Koç , Mete Karacaoğlu , Zehra Burcu Bakır , Kadir Kızılkaya

https://doi.org/10.29050/harranziraat.1016909

Cited By: 1

Abstract

Two of the most important ingredients to add functional properties to royal jelly are 10-HDA and major royal jelly proteins (MRJPs). The effect of royal jelly (RJ) production and the effect of royal jelly harvest time (24, 48 and 72 hours) on 10-HDA, the total protein content of RJ, and molecular weights of major proteins in RJ were investigated in queenright and queenless colonies. RJ production colonies were divided into 2 groups as queenless and queenright where the queen was confined with frames. Subgroups were formed within each group (queenless and queenright) according to harvest time (24, 48 and 72 hours). 80 larvae were transferred to each colony. In this study, as the harvest time increased, total protein (TP) ratio decreased (p<0.05); TP ratio in RJs harvested at 24, 48 and 72 hours was determined as 18.4±1.24%, 15.2±0.80%, 10.6±0.27%, respectively. As the harvest time increased, 10-HDA decreased. It was determined 10-HDA rates in RJ harvested at 24, 48 and 72 hours respectively; 2.52±0.109%, 2.20±0.110%, 2.00±0.112%. MRJP1, MRJP2, MRJP3 and MRJP5 were found from the MRJP family, and their molecular weights were determined as 53 kDa, 46.5 kDa, 66.8 kDa, 80.9 kDa, respectively. As a result, the early harvested (24 and 48 hours) RJ had higher values in terms of TP and trans 10-HDA than the royal jelly harvested at 72 hours.

Keywords

Honey bee,, Early harvest royal jelly, Aegean Ecotype of Anatolian bee,, Functional food, MRJP1

Supporting Institution

TUBİTAK

Project Number

213O413

Thanks

We thank the The Scientific and Technological Research Council of Turkey, (Tubitak-219O413) for its financial support and thank TARBIYOMER for its laboratory service support.

Farklı hasat zamanlarında ana arısız ve ana arılı kolonilerde üretilen arı sütlerinde toplam protein, trans 10-HDA ve arı sütü majör proteinlerinin tayini

Abstract

Arı sütüne (AS) fonksiyonel özellik katan en önemli içeriklerinden ikisi 10-HDA ve majör arı sütü proteinleridir. Bu çalışmada, hasat zamanı (24, 48 ve 72 saat) ve AS üretim kolonilerinin ana arılı ve ana arısız olmasının arı sütünün 10-HDA, toplam protein (TP) içeriğine etkisi belirlenmiş ve majör arı sütü proteinlerinin (MASP) molekül ağırlıkları saptanmıştır. Bu amaçla AS üretim kolonileri 2 gruba ayrılmış, birinci grup ana arısız, ikinci grup ise ana arılı grubu oluşturmuştur. Birinci grubun ana arıları kovandan alındığı gün, diğer grubunun ana arıları da 2 çerçeve ile birlikte plastik sınırlandırma kafeslerine yerleştirilmiştir. Her bir koloniye 80 adet larva transfer edilmiştir. Her grup içinde (anasız ve ve ana arılı) 2’şer koloni 24, 48 ve 72 saat hasat zamanı alt gruplarını oluşturmuştur. Bu çalışmada hasat zamanı uzadıkça TP oranı azalmış (P<0.05); 24, 48 ve 72 saatte hasat edilen arı sütlerinde TP oranı sırasıyla; %18.4±1.24, 15.2±0.80, 10.6±0.27 olarak belirlenmiştir. 10-HDA üzerine hasat zamanın etkisi önemli (P<0.05) bulunmuş, hasat zamanı uzadıkça 10-HDA azalmış, 24, 48 ve 72 saatte hasat edilen sütlerde 10-HDA sırasıyla; %2.52±0.109, %2.20±0.110, %2.00±0.112 saptanmış ve 24 saatte hasat edilen arı sütü, 48 ve 72 saatte hasat edilen sütlerden 10-HAD bakımından farklı bulunmuştur (P<0.05). Bu çalışmada MASP ailesinden MASP1, MASP2,  MASP3 ve MASP5 tespit edilmiş ve aynı sırayla molekül ağırlıkları; 53 kDa, 46.5 kDa, 66.8 kDa, 80.9 kDa olarak belirlenmiştir. Sonuçta erken hasat (24 ve 48 saat) arı sütleri 72 saatte hasat edilen arı sütlerinden TP ve 10-HDA bakımından daha yüksek değerlere sahip olmuştur.

Keywords

Bal arısı, Erken hasat arı sütü, Anadolu arısı Ege ekotipi, fonksiyonel gıda, MASP1

Project Number

213O413

References

• Al-Kahtani, S. & Taha, El-K.A. (2020). Effect of harvest time on royal jelly yield and chemical composition. Journal of the Kansas Entomological Society, 93(2):132-139.
• Bilikova, K., Hanes, J., Nordhoff, E., Saenger, W., Klaundny, J., Simuth, J. (2002). Apisimin, a new serine-valine-rich peptide from honeybee (Apis mellifera L.) royal jelly: purification and molecular characterization. FEBS Letters, 528:125-129.
• Blum, M.S., Novak, A.F. & Taber, S. (1959). 10-hydroxy-Δ 2 -decenoic acid, an antibiotic found in royal jelly. Science, 130: 452-453.
• Boselli, E., Caboni, M.F., Sabatini, A.G., Marcazzan, G.L., Lercker, G. (2003). Determination and changes of free amino acids in royal jelly during storage. Apidologie 34 :129–137.
• Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72:248-254.
• Buttstedt, A., Moritz, R.F. & Erler, S. (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.
• Caparica, C., Marcucci S. & Marcucci, M.C. (2007). Quantitative determination of trans- 10-Hydroxy-2-Decenoic Acid (10-HDA) in Brazilian royal jelly and commercial products containing royal jelly. Journal of Apicultural Research and Bee World, 46(3): 149-153.
• Chen, Y.F., Wang, K., Zhang, Y.Z., Zheng, Y.F. & Hu, F.L. (2016). In vitro anti-inflammatory effects of three fatty acids from royal jelly. Mediators Inflamm. 2, 2016.
• Chen., Y.F, You, M.M., Liua, Y.C., Shia, Y.Z., Wang, K., Lua, Y.Y. & Hua, F.L. (2018). Potential protective effect ofTrans-10-hydroxy-2-decenoic acid on theinflammation induced by Lipoteichoic acid. Journal of Functional Foods, 45: 491-498.
• Drapeau, M.D., Albert, S., Kucharski, R., Prusko, C., Maleszka, R. (2006). Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honey bees. Genome Research, 16:1385-1394.
• Erdoğan, A., Uçak Koç, A., Karacaoğlu, M. (2017). Anadolu arısı Ege ekotipi (Apis mellifera anatoliaca) ve İtalyan (Apis mellifera ligustica) X Ege melezi bal arılarının ve farklı yüksük sayılarının arı sütü verimleri üzerine etkileri. Harran Tarım ve Gıda Bilimleri Dergisi, 21(1): 91-98.
• Furusawa, T., Rakwal, R., Nam, H.W., Shibato, J., Agrawal, G.K., Kim, Y.S., Ogawa, Y., Yoshida, Y., Kouzuma, Y. & Masuo, Y. (2008). Comprehensive royal jelly (RJ) proteomics using one-and two-dimensional proteomics platforms reveals novel RJ proteins and potential phospho/glycoproteins. J. Proteome Res., 7, 3194-3229.
• Furusawa, T., Arai, Y., Kato, K. & Ichihara, K. (2016). Quantitative Analysis of Apisin, a Major Protein Unique to Royal Jelly, Hindawi Publishing Corporation. Evidence-Based Complementary and Alternative Medicine, 2016:1-9.
• Garcia, M.C., Finola, M.S. & Marioli, J.M. (2013). Bioassay direct identification of royal jelly’s active compounds against the growth of bacteria capable of infecting cutaneous wounds. Adv. Microbiol., 3: 138–144.
• Imjongjirak, C., Klinbunga, S. & Sittipraneed, S. (2005). Cloning, expression and genomic organization of genes encoding major royal jelly protein 1 and 2 of the honey bee (Apis cerana). BMB Reports, 38: 49-57.
• Isidorov, V.A., Bakier, S. & Grzech, I. (2012). Gas chromatographicmass spectrometric investigation of volatile and extractable compounds of crude royal jelly. Journal of Chromatography B, (885–886): 109–116.
• Kamakura, M., Suenobu, N. & Fukushima, M. (2001). Fifty-seven-kDa protein in royal jelly enhances proliferation of primary cultured rat hepatocytes and increases albumin production in the absence of serum. Biochemical and Biophysical Research Communications, 282(4):865-874.
• Kim, J. & Lee, J. (2010). Quantitative analysis of trans-10hydroxy-2-decenoic acid in royal jelly products purchased in USA by high-performance liquid chromatography. Journal of Apicultural Science, 54(1):77-85.
• Kimura, M., Kimura, Y., Tsumura, K., Okihara, K., Sugimoto, H., Yamada, H., Yonekura, M. (2003). 350-kDa royal jelly glycoprotein (apisin), which stimulates proliferation of human monocytes, bears the β1-3galactosylated N-glycan: Analysis of the N-gly-cosylation site. Bioscience, Biotechnology and Biochemistry, 67: 2055-2058.
• Knecht, D. & Kaatz, H. (1990). Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie, 21: 457-468.
• Kösoğlu, M., Yücel, B., Gökbulut, C., Konak, R. & Bı̇rcan, C. (2013). The effect of harvesting time on some biochemical and trace element compositions of royal jelly. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 19(2), 233-237.
• Kucharski, R., Maleszka J. & Maleszka R. (2008) Nutritional control of reproductive status in honeybees via DNA methylation, Science, 319:1827-1830.
• Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
• Lercker, G., Capella, P., Conte, L.S., Ruini, F. & Giordani, G. (1981). Components of royal jelly: I. Identification of the organic acids. Lipids, 16: 912–919.
• Lercker, G., Caboni M., Vecchi M., Sabatini A., Nanetti A., Piana L. (1985) Composizione della frazione glucidica della gelatina reale e della gelatina delle api operaie in relazione all’età larvale, Apicoltura, 8, 27–37.
• Li, J.K., Feng, M., Begna, D., Fang, Y. & Zheng, A.J. (2010). Proteome comparison of hypopharyngeal gland development between Italian and royal jelly-producing worker honeybees (Apis mellifera L). J. Proteome Res., 9: 6578-6594.
• Li, X., Huang, C. & Xue, Y. (2013). Contribution of lipids in honeybee (Apis mellifera) royal jelly to health. J. Med. Food, 16, 96-102.
• Liu, J. R., Yang, Y.C., Shi, L.S. & Peng C.C. (2008). Antioxidant properties of royal jelly associated with larval age and time of harvest. Journal of Agricultural Food Chemistry, 56: 11447-11452.
• Malecova, B., Ramser, J., O'Brien, J.K., Janitz, M., Judova, J., Lehrach, H. & Simuth, J. (2003). Honey bee (Apis mellifera L.) mrjp gene family: Computational analysis of putative promoters and genomic structure of mrjp1, the gene coding for the most abundant protein of larval food. Gene 303: 165-175.
• Mandacaru, S.C., do Vole, L.H.F., Vahidi, S., Xiao, Y., Skinner, O.S., Ricart, C.A.O., Kelleher, N.L., de Souso, M.V. & Konermann, L. (2017). Characterizing the structure and oligomerization of major royal jelly protein 1 (MRJP1) by mass spectrometry and complementary biophysical tools. Biochemistry, 56: 1645-1655.
• Melliou, E. & Chinou, I. (2014). Chemistry and bioactivities of royal jelly. In Studies in Natural Products Chemistry, 43: 261–290.
• Mureşan, C.I. &Buttstedt, A. (2019). pH-dependent stability of honey bee (Apis mellifera) major royal jelly proteins. Nature, Scientific Reports 9:9014.
• Özbakır Özmen, G., Doğan, Z., Öztokmak, A. (2016). Adıyaman İli Arıcılık Faaliyetlerinin İncelenmesi. Harran Tarım ve Gıda Bilimleri Dergisi (2016) 20(2): 119-126.
• Peixoto, L., G, Calabria, L.K., Garcia, L., Capparelli, F.E., Goulart, L.R., de Sousa MV, & Espindola, F.S. (2009). Identification of major royal jelly proteins in the brain of the honey bee Apis mellifera. Journal of Insect Physiology, 55: 671-677.
• Ramadan, M.F. & Al-Ghamdi, A. (2012). Bioactive compounds and health-promoting properties of royal jelly: A review, Journal of Functional Foods, 4, 39 –52.
• Ramanathan, A.N.K.G., Nair A.J., Sagunan, V.S. (2018). A review on Royal Jelly proteins and peptides. Journal of Functional Foods, 44: 255-264.
• Sabatini, A.G., Marcazzan, G.L., Caboni, M.F., Bogdanov, S. & Almeida-Muradian, L.B. (2009). Quality and standardisation of royal jelly. Journal of ApiProduction ApiMedical Science, 1, 1–6.
• Santos, K.S., dos Santos, L.D., Mendes, M.A., de Souza, B.M., Malaspina, O. & Palma, M.S. (2005). Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honey bees (Apis mellifera L.). Insect Biochemistry and Molecular Biology, 35: 85-91.
• SAS. 1999. Statistical Analsis System for Windows (Relase 8.2). SAS Institute Inc.Raleigh, Caroline, USA.
• Schmitzova, J., Klaudiny, J., Albert, S., Schroder, W., Schreckengost, W., Hanes, J., Judova, J. & Simuth, J. (1998). A family of major royal jelly proteins of the honeybee Apis mellifera L. Cellular and Molecular Life Sciences, 54: 1020-1030.
• Shinkhede, M.M. & Tembhare, D.B. (2009). Royal jelly protein and lipid composition in Apis cerana indica F. International Journal of Industrial Entomology, 18: 139-142.
• Simuth, J. (2001). Some properties of the main protein of honeybee (Apis mellifera) royal jelly. Apidologie, 32: 69-80.
• Sugiyama, T., Takahashi, K. & Mori, H. (2012). Royal jelly acid, 10-hydroxy-trans-2-decenoic acid, as a modulator of the innate immune responses. Endocr. Metab. Immune Disord. Drug Targets, 12: 368–376.
• Tamura, S., Amano, S., Kono, T., Kondoh, J., Yamaguchi, K., Kobayashi, S., Ayabe, T., & Moriyama, T. (2009). Molecular characteristics and physiological functions of major royal jelly protein 1 oligomer. Proteomics, 9: 5534-5543.
• Terada, Y., Narukawa, M., & Watanabe, T. (2011). Specific Hydroxy Fatty Acids in Royal Jelly Activate TRPA1. |J. Agric. Food Chem., 59:2627–2635.
• Ucak Koc, A. Karacaoğlu, M., Uygun, M., Bakır, Z.B. & Keser, B. (2021a). Effect of harvesting time and the number of queen cell cups on royal jelly composition. Journal of Apicultural Research (underpress). https://doi.org/10.1080/00218839.2021.1930956
• Ucak Koc, A. Karacaoğlu, M., Bakır, Z.B. & Keser, B. (2021b). Does the presence and absence of queen bee in the production of royal jelly affect the amount of soluble protein and ratio of 10-Hydroxy-2-Decenoic Acid? Turkish Journal of Agriculture - Food Science and Technology, 9(8): 1443-1447.
• Xue, X., Wu, L. & Wang, K. (2017). Bee Products-Chemical and Biological Properties; Alvarez-Suarez, J.M., Ed.; Springer: Berlin/Heidelberg, Germany, pp. 181–190.
• Yatsunami, K. & Echigo, T. (1985). Antibacterial action of royal jelly. Bull. Fac. Agr. Tamagawa Univ., 25, 13–22.
• You, M., Pan, Y., Liu, Y., Chen, Y. W., Si, J., Wang, K. & Hu, F. (2019). Royal jelly alleviates cognitive deficits and β-Amyloid accumulation in APP/PS1 mouse model via activation of the cAMP/PKA/CREB/BDNF pathway and inhibition of neuronal apoptosis. Frontiers in Aging Neuroscience, 10(428):1-12.
• Zheng, H.Q., Hu, F.L. & Dietemann, V. (2011). Changes in composition of royal jelly harvested at different times: consequences for quality standards. Apidologie, 42:39–47.