Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Review Article

Bioinformatics and Therapeutic Insights on Proteins in Royal Jelly

Author(s): Md. Sakib Hossen, Taebun Nahar, Siew Hua Gan* and Md. Ibrahim Khalil*

Volume 16, Issue 2, 2019

Page: [84 - 101] Pages: 18

DOI: 10.2174/1570164615666181012113130

Price: $65

Abstract

Background: To date, there is no x-ray crystallography or structures from nuclear magnetic resonance (NMR) on royal jelly proteins available in the online data banks. In addition, characterization of proteins in royal jelly is not fully accomplished to date. Although new investigations unravel novel proteins in royal jelly, the majority of a protein family is present in high amounts (80-90%).

Objective: In this review, we attempted to predict the three-dimensional structure of royal jelly proteins (especially the major royal jelly proteins) to allow visualization of the four protein surface properties (aromaticity, hydrophobicity, ionizability and (hydrogen (H)-bond) by using bioinformatics tools. Furthermore, we gathered the information on available therapeutic activities of crude royal jelly and its proteins.

Methods: For protein modeling, prediction and analysis, the Phyre2 web portal systematically browsed in which the modeling mode was intensive. On the other side, to build visualized understanding of surface aromaticity, hydrophobicity, ionizability and H-bond of royal jelly proteins, the Discovery Studio 4.1 (Accelrys Software Inc.) was used.

Results: Our in silico study confirmed that all proteins treasure these properties, including aromaticity, hydrophobicity, ionizability and (hydrogen (H)-bond. Another finding was that newly discovered proteins in royal jelly do not belong to the major royal jelly protein group.

Conclusion: In conclusion, the three dimensional structure of royal jelly proteins along with its major characteristics were successfully elucidated in this review. Further studies are warranted to elucidate the detailed physiochemical properties and pharmacotherapeutics of royal jelly proteins.

Keywords: Royal jelly, proteins, bioinformatics, in silico, pharmacology, crystallography.

Graphical Abstract

[1]
Schmitzova, J.; Klaudiny, J.; Albert, Š.; Schröder, W.; Schreckengost, W.; Hanes, J.; Judova, J.; Šimúth, J. A family of major royal jelly proteins of the honeybee Apis mellifera L. Cell. Mol. Life Sci., 1998, 54, 1020-1030.
[2]
Furusawa, T.; Rakwal, R.; Nam, H.W.; Shibato, J.; Agrawal, G.K.; Kim, Y.S.; Ogawa, Y.; Yoshida, Y.; Kouzuma, Y.; Masuo, Y. Comprehensive Royal Jelly (RJ) proteomics using one-and two-dimensional proteomics platforms reveals novel RJ proteins and potential phospho/glycoproteins. J. Proteome Res., 2008, 7, 3194-3229.
[3]
Zhang, L.; Han, B.; Li, R.; Lu, X.; Nie, A.; Guo, L.; Fang, Y.; Feng, M.; Li, J. Comprehensive identification of novel proteins and N-glycosylation sites in royal jelly. BMC Genomics, 2014, 15, 135.
[4]
Bogdanov, S. Royal jelly, bee brood: Composition, health, medicine: A review. Lipids, 2011, 3, 8-19.
[5]
Pavel, C.I.; Mărghitaş, L.A.; Bobiş, O.; Dezmirean, D.S.; Şapcaliu, A.; Radoi, I.; Mădaş, M.N. Biological activities of royal jelly-review. Sci. Papers Anim. Sci. Biotech., 2011, 44, 108-118.
[6]
Mărghitaş, L. Produsele apicole şi principalele lor însuşiri terapeutice. Albinele şi produsele lor LA Mărghitaş, 2nd ed; Ceres: Bucharest, Romania, 2008, pp. 280-378.
[7]
Knecht, D.; Kaatz, H. Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie , 1990, 21, 457-468.
[8]
Fujita, T.; Kozuka-Hata, H.; Ao-Kondo, H.; Kunieda, T.; Oyama, M.; Kubo, T. Proteomic analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee. J. Proteome Res., 2012, 12, 404-411.
[9]
Šimúth, J. Some properties of the main protein of honeybee (Apis mellifera) royal jelly. Apidologie , 2001, 32, 69-80.
[10]
Zhang, L.; Fang, Y.; Li, R.; Feng, M.; Han, B.; Zhou, T.; Li, J. Towards posttranslational modification proteome of royal jelly. J. Proteomics, 2012, 75, 5327-5341.
[11]
Li, J.; Wang, T.; Zhang, Z.; Pan, Y. Proteomic analysis of royal jelly from three strains of western honeybees (Apis mellifera). J. Agric. Food Chem., 2007, 55, 8411-8422.
[12]
Yu, F.; Mao, F.; Jianke, L. Royal jelly proteome comparison between A. mellifera ligustica and A. cerana cerana. J. Proteomics Res., 2010, 9, 2207-2215.
[13]
Scarselli, R.; Donadio, E.; Giuffrida, M.G.; Fortunato, D.; Conti, A.; Balestreri, E.; Felicioli, R.; Pinzauti, M.; Sabatini, A.G.; Felicioli, A. Towards royal jelly proteome. Proteomics, 2005, 5, 769-776.
[14]
Santos, K.S.; dos Santos, L.D.; Mendes, M.A.; de Souza, B.M.; Malaspina, O.; Palma, M.S. Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honeybees (Apis mellifera L.). Insect Biochem. Mol. Biol., 2005, 35, 85-91.
[15]
Schönleben, S.; Sickmann, A.; Mueller, M.J.; Reinders, J. Proteome analysis of Apis mellifera royal jelly. Anal. Bioanal. Chem., 2007, 389, 1087.
[16]
Han, B.; Li, C.; Zhang, L.; Fang, Y.; Feng, M.; Li, J. Novel royal jelly proteins identified by gel-based and gel-free proteomics. J. Agric. Food Chem., 2011, 59, 10346-10355.
[17]
Fujita, T.; Kozuka-Hata, H.; Ao-Kondo, H.; Kunieda, T.; Oyama, M.; Kubo, T. Proteomic Analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee. J. Proteome Res., 2013, 12, 404-411.
[18]
Jones, D.T.; Taylor, W.R.; Thornton, J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci., 1992, 8, 275-282.
[19]
Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 1985, 39(4), 783-791.
[20]
Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol., 2016, 33(7), 1870-1874.
[21]
Kelley, L.A.; Mezulis, S.; Yates, C.M.; Wass, M.N.; Sternberg, M.J.E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc., 2015, 10, 845-858.
[22]
Thien, F.C.; Leung, R.; Plomley, R.; Weiner, J.; Czarny, D. Royal jelly-induced asthma. Med. J. Aust., 1993, 159, 639.
[23]
Bullock, R.J.; Rohan, A.; Straatmans, J.A. Fatal royal jelly-induced asthma. Med. J. Aust., 1994, 160, 44.
[24]
Roger, A.; Rubira, N.; Nogueiras, C.; Guspi, R.; Baltasar, M.; Cadahia, A. Anaphylaxis caused by royal jelly. Allergol. Immunopathol. , 1994, 23, 133-135.
[25]
Thien, F.; Leung, R.; Baldo, B.; Weinbr, J.; Plomley, R.; Czarny, D. Asthma and anaphylaxis induced by royal jelly. Clin. Experimen. Allergy, 1996, 26, 216-222.
[26]
Paola, F.; Pantalea, D.D.; Gianfranco, C.; Antonio, F.; Angelo, V.; Eustachio, N.; Elisabetta, D.L. Oral allergy syndrome in a child provoked by royal jelly. Case Rep. Med., 2014, 2014, 941248.
[27]
Li, L.; Guan, K. P136 occupational asthma caused by inhalable royal jelly in a Chinese woman. Ann. Allergy Asthma Immunol., 2016, 117, S61.
[28]
Takahama, H.; Shimazu, T. Food-induced anaphylaxis caused by ingestion of royal jelly. J. Dermatol., 2006, 33, 424-426.
[29]
Laporte, J.R.; Ibaanez, L.; Vendrell, L.; Ballarin, E. Bronchospasm induced by royal jelly. Allergy, 1996, 51, 440.
[30]
Peacock, S.; Murray, V.; Turton, C. Respiratory distress and royal jelly. BMJ, 1995, 311, 1472.
[31]
Yang, A.; Zhou, M.; Zhang, L.; Xie, G.; Chen, H.; Liu, Z.; Ma, W. Influence of royal jelly on the reproductive function of puberty male rats. Food Chem. Toxicol., 2012, 50, 1834-1840.
[32]
Takahashi, M.; Matsuo, I.; Ohkido, M. Contact dermatitis due to honeybee royal jelly. Contact Dermat., 1983, 9, 452-455.
[33]
Rosmilah, M.; Shahnaz, M.; Patel, G.; Lock, J.; Rahman, D.; Masita, A.; Noormalin, A. Characterization of major allergens of royal jelly Apis mellifera. Trop. Biomed., 2008, 25, 243-251.
[34]
Kamakura, M.; Fukuda, T.; Fukushima, M.; Yonekura, M. Storage-dependent degradation of 57-kDa protein in royal jelly: A possible marker for freshness. Biosci. Biotechnol. Biochem., 2001, 65, 277-284.
[35]
Kamakura, M. Royalactin induces queen differentiation in honeybees. Nature, 2011, 473, 478-483.
[36]
Sabatini, A.G.; Marcazzan, G.L.; Caboni, M.F.; Bogdanov, S.; Almeida-Muradian, L. Quality and standardisation of royal jelly. J. ApiProduct ApiMed. Sci., 2009, 1, 1-6.
[37]
Marconi, E.; Caboni, M.F.; Messia, M.C.; Panfili, G. Furosine: A suitable marker for assessing the freshness of royal jelly. J. Agric. Food Chem., 2002, 50, 2825-2829.
[38]
Zheng, H.Q.; Wei, W.T.; Wu, L.M.; Hu, F.L.; Dietemann, V. Fast determination of royal jelly freshness by a chromogenic reaction. J. Food Sci., 2012, 77, S247-S252.
[39]
Chiu, H.F.; Chen, B.K.; Lu, Y.Y.; Han, Y.C.; Shen, Y.C.; Venkatakrishnan, K.; Golovinskaia, O.; Wang, C.K. Hypocholesterolemic efficacy of royal jelly in healthy mild hypercholesterolemic adults. Pharm. Biol., 2017, 55, 497-502.
[40]
Zargar, H.R.; Hemmati, A.A.; Ghafourian, M.; Arzi, A.; Rezaie, A.; Javad-Moosavi, S.A. Long-term treatment with royal jelly improves bleomycin-induced pulmonary fibrosis in rats. Can. J. Physiol. Pharmacol., 2017, 95, 23-31.
[41]
Pajovic, B.; Radojevic, N.; Dimitrovski, A.; Tomovic, S.; Vukovic, M. The therapeutic potential of royal jelly in benign prostatic hyperplasia. Comparison with contemporary literature. Aging Male, 2016, 19, 192-196.
[42]
Yoshida, M.; Hayashi, K.; Watadani, R.; Okano, Y.; Tanimura, K.; Kotoh, J.; Sasaki, D.; Matsumoto, K.; Maeda, A. Royal jelly improves hyperglycemia in obese/diabetic KK-Ay mice. J. Vet. Med. Sci., 2016, 79(2), 299-307.
[43]
Zahran, A.M.; Elsayh, K.I.; Saad, K.; Eloseily, E.M.; Osman, N.S.; Alblihed, M.A.; Badr, G.; Mahmoud, M.H. Effects of royal jelly supplementation on regulatory T cells in children with SLE. Food Nutr. Res., 2016, 60, 32963.
[44]
Ghanbari, E.; Nejati, V.; Khazaei, M. Improvement in serum biochemical alterations and oxidative stress of liver and pancreas following use of royal jelly in streptozotocin-induced diabetic rats. Cell J., 2016, 18, 362-370.
[45]
Saral, O.; Yildiz, O.; Aliyazicioglu, R.; Yulug, E.; Canpolat, S.; Ozturk, F.; Kolayli, S. Apitherapy products enhance the recovery of CCL4-induced hepatic damages in rats. Turk. J. Med. Sci., 2016, 46(1), 194-202.
[46]
Mofid, B.; Rezaeizadeh, H.; Termos, A.; Rakhsha, A.; Mafi, A.R.; Taheripanah, T.; Ardakani, M.M.; Taghavi, S.M.; Moravveji, S.A.; Kashi, A.S. Effect of processed honey and royal jelly on cancer-related fatigue: A double-blind randomized clinical trial. Electron Phys., 2016, 8, 2475-2482.
[47]
Lambrinoudaki, I.; Augoulea, A.; Rizos, D.; Politi, M.; Tsoltos, N.; Moros, M.; Chinou, I.; Graikou, K.; Kouskouni, E.; Kambani, S.; Panoulis, K.; Moutsatsou, P. Greek-origin royal jelly improves the lipid profile of postmenopausal women. Gynecol. Endocrinol., 2016, 32, 835-839.
[48]
Malekinejad, H.; Ahsan, S.; Delkhosh-Kasmaie, F.; Cheraghi, H.; Rezaei-Golmisheh, A.; Janbaz-Acyabar, H. Cardioprotective effect of royal jelly on paclitaxel-induced cardio-toxicity in rats. Iran. J. Basic Med. Sci., 2016, 19, 221-227.
[49]
Khoshpey, B.; Djazayeri, S.; Amiri, F.; Malek, M.; Hosseini, A.F.; Hosseini, S.; Shidfar, S.; Shidfar, F. Effect of royal jelly intake on serum glucose, apolipoprotein A-I (ApoA-I), apolipoprotein B (ApoB) and ApoB/ApoA-I ratios in patients with type 2 diabetes: A randomized, double-blind clinical trial study. Can. J. Diab., 2016, 40, 324-328.
[50]
Ibrahim, A.; Eldaim, M.A.; Abdel-Daim, M.M. Nephroprotective effect of bee honey and royal jelly against subchronic cisplatin toxicity in rats. Cytotechnology, 2016, 68, 1039-1048.
[51]
Manzo, L.P.; de-Faria, F.M.; Dunder, R.J.; Rabelo-Socca, E.A.; Consonni, S.R.; de Almeida, A.C.; Souza-Brito, A.R.; Luiz-Ferreira, A. Royal Jelly and its dual role in TNBS colitis in mice. Sci. World J., 2015, 2015, 956235.
[52]
Ozan, F.; Corekci, B.; Toptas, O.; Halicioglu, K.; Irgin, C.; Yilmaz, F.; Hezenci, Y. Effect of royal jelly on new bone formation in rapid maxillary expansion in rats. Med. Oral Patol. Oral Cir. Bucal, 2015, 20(6), e651-e656.
[53]
Jeon, S.; Cho, Y. Epidermal hydration is improved by enhanced ceramide metabolism in aged C57BL/6J mice after dietary supplementation of royal jelly. J. Med. Food, 2015, 18, 999-1006.
[54]
Hashemipour, M.A.; Tavakolineghad, Z.; Arabzadeh, S.A.; Iranmanesh, Z.; Nassab, S.A. Antiviral activities of honey, royal jelly, and acyclovir against HSV-1. Wounds, 2014, 26, 47-54.
[55]
Pourmoradian, S.; Mahdavi, R.; Mobasseri, M.; Faramarzi, E.; Mobasseri, M. Effects of royal jelly supplementation on glycemic control and oxidative stress factors in type 2 diabetic female: A randomized clinical trial. Chin. J. Integr. Med., 2014, 20, 347-352.
[56]
Zamani, Z.; Reisi, P.; Alaei, H.; Pilehvarian, A.A. Effect of Royal Jelly on spatial learning and memory in rat model of streptozotocin-induced sporadic Alzheimer’s disease. Adv. Biomed. Res., 2012, 1, 26.
[57]
Shen, L.; Liu, D.; Li, M.; Jin, F.; Din, M.; Parnell, L.D.; Lai, C.Q. Mechanism of action of recombinant acc-royalisin from royal jelly of Asian honeybee against gram-positive bacteria. PLoS One, 2012, 7, e47194.
[58]
Ito, S.; Nitta, Y.; Fukumitsu, H.; Soumiya, H.; Ikeno, K.; Nakamura, T.; Furukawa, S. Antidepressant-like activity of 10-hydroxy-trans-2-decenoic acid, a unique unsaturated fatty acid of royal jelly, in stress-inducible depression-like mouse model. Evid. Based Complement. Alternat. Med., 2012, 2012, 139140.
[59]
Han, S.M.; Yeo, J.H.; Cho, Y.H.; Pak, S.C. Royal jelly reduces melanin synthesis through down-regulation of tyrosinase expression. Am. J. Chin. Med., 2011, 39, 1253-1260.
[60]
Gannabathula, S.; Krissansen, G.W.; Skinner, M.; Steinhorn, G.; Schlothauer, R. Honeybee apisimin and plant arabinogalactans in honey costimulate monocytes. Food Chem., 2015, 168, 34-40.
[61]
Kashima, Y.; Kanematsu, S.; Asai, S.; Kusada, M.; Watanabe, S.; Kawashima, T.; Nakamura, T.; Shimada, M.; Goto, T.; Nagaoka, S. Identification of a novel hypocholesterolemic protein, major royal jelly protein 1, derived from royal jelly. PLoS One, 2014, 9, e105073.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy