Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family

Biological Reviews

Volumn 89, Issue 2, 2014, Pages 255-269

  Buttstedt, Anja ^a,b   Moritz, Robin F A ^a,b,c   Erler, Silvio ^a,b  

^a Departamentul de Apiculturǎ şi Sericiculturǎ Facultatea de Zootehnie şi Biotehnologii Universitatea de Ştiinţe Agricole şi Medicinǎ Veterinarǎ ^*  (Romania)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Apalbumin; Apis mellifera; Caste differentiation; Genome organisation; Hymenoptera; Major royal jelly protein; MRJP; Royal jelly; Royalactin; Social insect

Indexed keywords

APIS MELLIFERA; APOIDEA; HEXAPODA; HYMENOPTERA;

FATTY ACID; INSECT PROTEIN; ROYAL JELLY;

ANIMAL; BEE; CHEMISTRY; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; PHYSIOLOGY;

ANIMALS; BEES; FATTY ACIDS; GENE EXPRESSION REGULATION; INSECT PROTEINS; LARVA;

EID: 84898493871     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12052     Document Type: Article

References (121)

1. Albert, Š., Bhattacharya, D., Klaudiny, J., Schmitzová, J. & Šimúth, J. (1999a). The family of major royal jelly proteins and its evolution. Journal of Molecular Evolution 49, 290-297.
2. Albert, Š. & Klaudiny, J. (2004). The MRJP/YELLOW protein family of Apis mellifera: identification of new members in the EST library. Journal of Insect Physiology 50, 51-59.
3. Albert, Š., Klaudiny, J. & Šimúth, J. (1996). Newly discovered features of the updated sequence of royal jelly protein RJP571; longer repetitive region on C-terminus and homology to Drosophila melanogaster yellow protein. Journal of Apicultural Research 35, 63-68.
4. Albert, Š., Klaudiny, J. & Šimúth, J. (1999b). Molecular characterization of MRJP3, highly polymorphic protein of honeybee (Apis mellifera) royal jelly. Insect Biochemistry and Molecular Biology 29, 427-434.
5. Albert, Š. & Schmitz, J. (2002). Characterization of major royal jelly protein-like DNA sequences in Apis dorsata. Journal of Apicultural Research 41, 75-82.
6. Albertová, V., Su, S., Brockmann, A., Gadau, J. & Albert, Š. (2005). Organization and potential function of the mrjp3 locus in four honeybee species. Journal of Agricultural and Food Chemistry 53, 8075-8081.
7. Amdam, G. V., Simões, Z. L., Guidugli, K. R., Norberg, K. & Omholt, S. W. (2003). Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. BMC Biotechnology 3, 1.
8. Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, G., De Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E., Grosdidier, A., Hernandez, C., Ioannidis, V., Kuznetsov, D., Liechti, R., et al. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Research 40, W597-W603.
9. Asencot, M. & Lensky, Y. (1976). The effect of sugars and juvenile hormone on the differentiation of the female honeybee larvae (Apis mellifera L.) to queens. Life Sciences 18, 693-699.
10. Baitala, T. V., Faquinello, P., Toledo, V. A. A., Mangolin, C. A., Martins, E. N. & Ruvolo-Takasusuki, M. C. C. (2010). Potential use of major royal jelly proteins (MRJPs) as molecular markers for royal jelly production in Africanized honeybee colonies. Apidologie 41, 160-168.
11. Barchuk, A. R., Maleszka, R. & Simões, Z. L. (2004). Apis mellifera ultraspiracle: cDNA sequence and rapid up-regulation by juvenile hormone. Insect Molecular Biology 13, 459-467.
12. Bergem, M., Norberg, K. & Aamodt, R. M. (2006). Long-term maintenance of in vitro cultured honeybee (Apis mellifera) embryonic cells. BMC Developmental Biology 6, 17.
13. Beye, M., Härtel, S., Hagen, A., Hasselmann, M. & Omholt, S. W. (2002). Specific developmental gene silencing in the honey bee using a homeobox motif. Insect Molecular Biology 11, 527-532.
14. Beye, M., Neumann, P., Schmitzová, J., Klaudiny, J., Albert, Š., Šimúth, J., Felder, M. & Moritz, R. F. A. (1998). A simple, non-radioactive DNA fingerprinting method for identifying patrilines in honeybee colonies. Apidologie 29, 255-263.
15. Bíliková, K., Hanes, J., Nordhoff, E., Saenger, W., Klaudiny, J. & Šimúth, 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.
16. Bíliková, K., Mirgorodskaya, E., Bukovská, G., Gobom, J., Lehrach, H. & Šimúth, J. (2009). Towards functional proteomics of minority component of honeybee royal jelly: the effect of post-translational modifications on the antimicrobial activity of apalbumin 2. Proteomics 9, 2131-2138.
17. Bíliková, K. & Šimúth, J. (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.
18. Blank, S., Bantleon, F. I., McIntyre, M., Ollert, M. & Spillner, E. (2012). The major royal jelly proteins 8 and 9 (Api m 11) are glycosylated components of Apis mellifera venom with allergenic potential beyond carbohydrate-based reactivity. Clinical and Experimental Allergy 42, 976-985.
19. Blom, N., Gammeltoft, S. & Brunak, S. (1999). Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of Molecular Biology 294, 1351-1362.
20. Bonasio, R., Zhang, G., Ye, C., Mutti, N. S., Fang, X., Qin, N., Donahue, G., Yang, P., Li, Q., Li, C., Zhang, P., Huang, Z., Berger, S. L., Reinberg, D., Wang, J. & Liebig, J. (2010). Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329, 1068-1071.
21. Calábria, L. K., Garcia Hernandez, L., Teixeira, R. R., Valle de Sousa, M. & Espindola, F. S. (2008). Identification of calmodulin-binding proteins in brain of worker honeybees. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 151, 41-45.
22. Casteel, D. B. (1912). The Behavior of the Honey Bee in Pollen Collection. Government Printing Office, Washington.
23. Chan, Q. W., Melathopoulos, A. P., Pernal, S. F. & Foster, L. J. (2009). The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics 10, 387.
24. Charlab, R., Valenzuela, J. G., Rowton, E. D. & Ribeiro, J. M. (1999). Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proceedings of the National Academy of Sciences of the United States of America 96, 15155-15160.
25. Cruz, G. C. N., Garcia, L., Silva, A. J., Barbosa, J. A. R. G., Ricart, C. A. O., Freitas, S. M. & Sousa, M. V. (2011). Calcium effect and pH-dependence on self-association and structural stability of the Apis mellifera major royal jelly protein. Apidologie 42, 252-269.
26. Davis, R. B., Baldauf, S. L. & Mayhew, P. J. (2010). The origins of species richness in the Hymenoptera: insights from a family-level supertree. BMC Evolutionary Biology 10, 109.
27. De Groot, A. P. (1953). Protein and amino acid requirements of the honeybee (Apis mellifica L.). Physiologia Comparata et Oecologia 3, 197-285.
28. Di Girolamo, F., D'Amato, A. & Righetti, P. G. (2012). Assessment of the floral origin of honey via proteomic tools. Journal of Proteomics 75, 3688-3693.
29. Drapeau, M. M. (2003). A novel hypothesis on the biochemical role of the Drosophila Yellow protein. Biochemical and Biophysical Research Communications 311, 1-3.
30. Drapeau, M. D., Albert, Š., 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.
31. Feng, M., Fang, Y. & Li, J. (2009). Proteomic analysis of honeybee worker (Apis mellifera) hypopharyngeal gland development. BMC Genomics 10, 645.
32. Ferguson, L. C., Green, J., Surridge, A. & Jiggins, C. D. (2011). Evolution of the insect yellow gene family. Molecular Biology and Evolution 28, 257-272.
33. Fontana, R., Mendes, M. A., De Souza, B. M., Konno, K., César, L. M., Malaspina, O. & Palma, M. S. (2004). Jelleines: a family of antimicrobial peptides from the Royal Jelly of honeybees (Apis mellifera). Peptides 25, 919-928.
34. Furusawa, T., Rakwal, R., Nam, H. W., Shibato, J., Agrawal, G. K., Kim, Y. S., Ogawa, Y., Yoshida, Y., Kouzuma, Y., Masuo, Y. & Yonekura, M. (2008). Comprehensive royal jelly (RJ) proteomics using one- and two-dimensional proteomics platforms reveals novel RJ proteins and potential phospho/glycoproteins. Journal of Proteome Research 7, 3194-3229.
35. Garcia, L., Saraiva Garcia, C. H., Calábria, L. K., Costa Nunes da Cruz, G., Sánchez Puentes, A., Báo, S. N., Fontes, W., Ricart, C. A., Salmen Espindola, F. & Valle de Sousa, M. (2009). Proteomic analysis of honey bee brain upon ontogenetic and behavioral development. Journal of Proteome Research 8, 1464-1473.
36. Goulet, H. & Huber, J. (1993). Hymenoptera of the World: An Identification Guide to Families. Agriculture Canada Publication, Ottawa.
37. Han, B., Li, C., Zhang, L., Fang, Y., Feng, M. & Li, J. (2011). Novel royal jelly proteins identified by gel-based and gel-free proteomics. Journal of Agricultural and Food Chemistry 59, 10346-10355.
38. Hanes, J. & Šimúth, J. (1992). Identification and partial characterization of the major royal jelly protein of the honey bee (Apis mellifera L.). Journal of Apicultural Research 31, 22-26.
39. Hayashi, T., Takamatsu, N., Nakashima, T. & Arita, T. (2011). Immunological characterization of honey proteins and identification of MRJP 1 as an IgE-binding protein. Bioscience, Biotechnology, and Biochemistry 75, 556-560.
40. Hojo, M., Kagami, T., Sasaki, T., Nakamura, J. & Sasaki, M. (2010). Reduced expression of major royal jelly protein 1 gene in the mushroom bodies of worker honeybees with reduced learning ability. Apidologie 41, 194-202.
41. Honeybee Genome Sequencing Consortium (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949.
42. Huang, C. Y., Chi, L. L., Huang, W. J., Chen, Y. W., Chen, W. J., Kuo, Y. C., Yuan, C. M. & Chen, C. N. (2012). Growth stimulating effect on queen bee larvae of histone deacetylase inhibitors. Journal of Agricultural and Food Chemistry 60, 6139-6149.
43. Ichikawa, N. & Sasaki, M. (2003). Importance of social stimuli for the development of learning capability in honeybees. Applied Entomology and Zoology 38, 203-209.
44. Ito, K., Katsuma, S., Yamamoto, K., Kadono-Okuda, K., Mita, K. & Shimada, T. (2010). Yellow-e determines the color pattern of larval head and tail spots of the silkworm Bombyx mori. Journal of Biological Chemistry 285, 5624-5629.
45. Jarosch, A., Stolle, E., Crewe, R. M. & Moritz, R. F. (2011). Alternative splicing of a single transcription factor drives selfish reproductive behavior in honeybee workers (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America 108, 15282-15287.
46. Jones, G. & Sharp, P. A. (1997). Ultraspiracle: an invertebrate nuclear receptor for juvenile hormones. Proceedings of the National Academy of Sciences of the United States of America 94, 13499-13503.
47. Kaftanoglu, O., Linksvayer, T. A. & Page, R. E. (2011). Rearing honey bees, Apis mellifera, in vitro 1: effects of sugar concentrations on survival and development. Journal of Insect Science 11, 1-10.
48. Kamakura, M. (2011). Royalactin induces queen differentiation in honeybees. Nature 473, 478-483.
49. Kamakura, M., Fukuda, T., Fukushima, M. & Yonekura, M. (2001a). Storage-dependent degradation of 57-kDa protein in royal jelly: a possible marker for freshness. Bioscience, Biotechnology, and Biochemistry 65, 277-284.
50. Kamakura, M. & Sakaki, T. (2006). A hypopharyngeal gland protein of the worker honeybee Apis mellifera L. enhances proliferation of primary-cultured rat hepatocytes and suppresses apoptosis in the absence of serum. Protein Expression and Purification 45, 307-314.
51. Kamakura, M., Suenobu, N. & Fukushima, M. (2001b). 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, 865-874.
52. Kimura, Y., Kajiyama, S., Kanaeda, J., Izukawa, T. & Yonekura, M. (1996). N-linked sugar chain of 55-kDa royal jelly glycoprotein. Bioscience, Biotechnology, and Biochemistry 60, 2099-2102.
53. Kimura, Y., Miyagi, C., Kimura, M., Nitoda, T., Kawai, N. & Sugimoto, H. (2000). Structural features of N-glycans linked to royal jelly glycoproteins: structures of high-mannose type, hybrid type, and biantennary type glycans. Bioscience, Biotechnology, and Biochemistry 64, 2109-2120.
54. Kimura, Y., Nagai, H., Miyamoto, M., Kimura, M. & Yonekura, M. (2010). Identification of a royal jelly glycoprotein that carries unique complex-type N-glycans harboring the T-antigen (Galβ1-3GalNAc) unit. Bioscience, Biotechnology, and Biochemistry 74, 2148-2150.
55. Klaudiny, J., Hanes, J., Kulifajová, J., Albert, Š. & Šimúth, J. (1994a). Molecular cloning of two cDNAs from the head of the nurse honey bee (Apis mellifera L.) for coding related proteins of royal jelly. Journal of Apicultural Research 33, 105-111.
56. Klaudiny, J., Kulifajová, J., Crailsheim, K. & Šimúth, J. (1994b). New approach to the study of division of labour in the honeybee colony (Apis mellifera L). Apidologie 25, 596-600.
57. Kohno, K., Okamoto, I., Sano, O., Arai, N., Iwaki, K., Ikeda, M. & Kurimoto, M. (2004). Royal jelly inhibits the production of proinflammatory cytokines by activated macrophages. Bioscience, Biotechnology, and Biochemistry 68, 138-145.
58. Kubo, T., Sasaki, M., Nakamura, J., Sasagawa, H., Ohashi, K., Takeuchi, H. & Natori, S. (1996). Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera L.) with age and/or role. Journal of Biochemistry 119, 291-295.
59. Kucharski, R., Maleszka, J., Foret, S. & Maleszka, R. (2008). Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827-1830.
60. Kucharski, R., Maleszka, R., Hayward, D. C. & Ball, E. E. (1998). A royal jelly protein is expressed in a subset of Kenyon cells in the mushroom bodies of the honey bee brain. Naturwissenschaften 85, 343-346.
61. Kupke, J., Spaethe, J., Mueller, M. J., Rössler, W. & Albert, Š. (2012). Molecular and biochemical characterization of the major royal jelly protein in bumblebees suggest a non-nutritive function. Insect Biochemistry and Molecular Biology 42, 647-654.
62. Leimar, O., Hartfelder, K., Laubichler, M. D. & Page, R. E. (2012). Development and evolution of caste dimorphism in honeybees-a modeling approach. Ecology and Evolution 2, 3098-3109.
63. Li, J., Feng, M., Zhang, L., Zhang, Z. & Pan, Y. (2008). Proteomics analysis of major royal jelly protein changes under different storage conditions. Journal of Proteome Research 7, 3339-3353.
64. Li, J., Wang, T., Zhang, Z. & Pan, Y. (2007). Proteomic analysis of royal jelly from three strains of western honeybees (Apis mellifera). Journal of Agricultural and Food Chemistry 55, 8411-8422.
65. Majtán, J., Kováčová, E., Bíliková, K. & Šimúth, J. (2006). The immunostimulatory effect of the recombinant apalbumin 1-major honeybee royal jelly protein-on TNFα release. International Immunopharmacology 6, 269-278.
66. Malecová, B., Ramser, J., O'Brien, J. K., Janitz, M., Júdová, J., Lehrach, H. & Šimúth, J. (2003). Honeybee (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.
67. Nakaoka, T., Takeuchi, H. & Kubo, T. (2008). Laying workers in queenless honeybee (Apis mellifera L.) colonies have physiological states similar to that of nurse bees but opposite that of foragers. Journal of Insect Physiology 54, 806-812.
68. Nash, W. G. (1976). Patterns of pigmentation color states regulated by the y locus in Drosophila melanogaster. Developmental Biology 48, 336-343.
69. Neumann, P. & Moritz, R. F. A. (2002). The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? Behavioral Ecology and Sociobiology 52, 271-281.
70. Nygaard, S., Zhang, G., Schiøtt, M., LI, C., Wurm, Y., Hu, H., Zhou, J., Ji, L., Qiu, F., Rasmussen, M., Pan, H., Hauser, F., Krogh, A., Grimmelikhuijzen, C. J., Wang, J. & Boomsma, J. J. (2011). The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Research 21, 1339-1348.
71. Ohashi, K., Natori, S. & Kubo, T. (1997). Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L. European Journal of Biochemistry 249, 797-802.
72. Ohashi, K., Sasaki, M., Sasagawa, H., Nakamura, J., Natori, S. & Kubo, T. (2000). Functional flexibility of the honey bee hypopharyngeal gland in a dequeened colony. Zoological Science 17, 1089-1094.
73. Okamoto, I., Taniguchi, Y., Kunikata, T., Kohno, K., Iwaki, K., Ikeda, M. & Kurimoto, M. (2003). Major royal jelly protein 3 modulates immune responses in vitro and in vivo. Life Sciences 73, 2029-2045.
74. Patel, N. G., Haydak, M. H. & Gochnauer, T. A. (1960). Electrophoretic components of the proteins in honeybee larval food. Nature 186, 633-634.
75. Peiren, N., De Graaf, D. C., Vanrobaeys, F., Danneels, E. L., Devreese, B., Van Beeumen, J. & Jacobs, F. J. (2008). Proteomic analysis of the honey bee worker venom gland focusing on the mechanisms of protection against tissue damage. Toxicon 52, 72-83.
76. Peiren, N., Vanrobaeys, F., De Graaf, D. C., Devreese, B., Van Beeumen, J. & Jacobs, F. J. (2005). The protein composition of honeybee venom reconsidered by a proteomic approach. Biochimica et Biophysica Acta 1752, 1-5.
77. Peixoto, L. G., Calábria, L. K., Garcia, L., Capparelli, F. E., Goulart, L. R., De Sousa, M. V. & Espindola, F. S. (2009). Identification of major royal jelly proteins in the brain of the honeybee Apis mellifera. Journal of Insect Physiology 55, 671-677.
78. Petersen, T. N., Brunak, S., Von Heijne, G. & Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8, 785-786.
79. Rachinsky, A., Strambi, C., Strambi, A. & Hartfelder, K. (1990). Caste and metamorphosis: hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. General and Comparative Endocrinology 79, 31-38.
80. Randolt, K., Gimple, O., Geissendörfer, J., Reinders, J., Prusko, C., Mueller, M. J., Albert, Š., Tautz, J. & Beier, H. (2008). Immune-related proteins induced in the hemolymph after aseptic and septic injury differ in honey bee worker larvae and adults. Archives of Insect Biochemistry and Physiology 69, 155-167.
81. Rembold, H. (1983). Royal Jelly. In Queen Rearing: Biological Basis and Technical Instruction Chapter 2 (ed. F. Ruttner ), pp. 35-42. Apimondia Publishing House, Bucharest.
82. Rembold, H., Lackner, B. & Geistbeck, I. (1974). The chemical basis of honeybee, Apis mellifera, caste formation. Partial purification of queen bee determinator from royal jelly. Journal of Insect Physiology 20, 307-314.
83. Rösch, G. A. (1930). Untersuchungen über die Arbeitsteilung im Bienenstaat. 2. Teil: die Tätigkeiten der Arbeitsbienen unter experimentell veränderten Bedingungen. Zeitschrift für Vergleichende Physiologie 12, 1-71(only in German).
84. Rosmilah, M., Shahnaz, M., Patel, G., Lock, J., Rahman, D., Masita, A. & Noormalin, A. (2008). Characterization of major allergens of royal jelly Apis mellifera. Tropical Biomedicine 25, 243-251.
85. Rossano, R., Larocca, M., Polito, T., Perna, A. M., Padula, M. C., Martelli, G. & Riccio, P. (2012). What are the proteolytic enzymes of honey and what they do tell us? A fingerprint analysis by 2-D zymography of unifloral honeys. PLoS One 7, e49164.
86. Sano, O., Kunikata, T., Kohno, K., Iwaki, K., Ikeda, M. & Kurimoto, M. (2004). Characterization of royal jelly proteins in both Africanized and European honeybees (Apis mellifera) by two-dimensional gel electrophoresis. Journal of Agricultural and Food Chemistry 52, 15-20.
87. 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-honeybees (Apis mellifera L.). Insect Biochemistry and Molecular Biology 35, 85-91.
88. Scarselli, R., Donadio, E., Giuffrida, M. G., Fortunato, D., Conti, A., Balestreri, E., Felicioli, R., Pinzauti, M., Sabatini, A. G. & Felicioli, A. (2005). Towards royal jelly proteome. Proteomics 5, 769-776.
89. Scharlaken, B., De Graaf, D. C., Memmi, S., Devreese, B., Van Beeumen, J. & Jacobs, F. J. (2007). Differential protein expression in the honey bee head after a bacterial challenge. Archives of Insect Biochemistry and Physiology 65, 223-237.
90. Schmitzová, J., Klaudiny, J., Albert, Š., Schröder, W., Schreckengost, W., Hanes, J., Júdová, J. & Šimúth, J. (1998). A family of major royal jelly proteins of the honeybee Apis mellifera L. Cellular and Molecular Life Sciences 54, 1020-1030.
91. Schönleben, S., Sickmann, A., Mueller, M. J. & Reinders, J. (2007). Proteome analysis of Apis mellifera royal jelly. Analytical and Bioanalytical Chemistry 389, 1087-1093.
92. Seeley, T. D. (1982). Adaptive significance of the age polyethism schedule in honeybee colonies. Behavioral Ecology and Sociobiology 11, 287-293.
93. Segraves, W. A. (1991). Something old, some things new: the steroid receptor superfamily in Drosophila. Cell 67, 225-228.
94. Ševčik, V. (1950). Mikrobiologie pylového kvašení. Přírodovědecká fakulta Masarykova Univerzita 323, 103-130(only in Czech).
95. Shen, L., Zhang, W., Jin, F., Zhang, L., Chen, Z., Liu, L., Parnell, L. D., Lai, C. Q. & Li, D. (2010). Expression of recombinant AccMRJP1 protein from royal jelly of Chinese honeybee in Pichia pastoris and its proliferation activity in an insect cell line. Journal of Agricultural and Food Chemistry 58, 9190-9197.
96. Šimúth, J. (2001). Some properties of the main protein of honeybee (Apis mellifera) royal jelly. Apidologie 32, 69-80.
97. Šimúth, J., Bíliková, K., Kováčová, E., Kuzmová, Z. & Schröder, W. (2004). Immunochemical approach to detection of adulteration in honey: physiologically active royal jelly protein stimulating TNF-α release is a regular component of honey. Journal of Agricultural and Food Chemistry 52, 2154-2158.
98. Smith, C. D., Zimin, A., Holt, C., Abouheif, E., Benton, R., Cash, E., Croset, V., Currie, C. R., Elhaik, E., Elsik, C. G., Favé, M. J., Fernandes, V., Gadau, J., Gibson, J. D., Graur, D., et al. (2011a). Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proceedings of the National Academy of Sciences of the United States of America 108, 5673-5678.
99. Smith, C. R., Smith, C. D., Robertson, H. M., Helmkampf, M., Zimin, A., Yandell, M., Holt, C., Hu, H., Abouheif, E., Benton, R., Cash, E., Croset, V., Currie, C. R., Elhaik, E., Elsik, C. G., et al. (2011b). Draft genome of the red harvester ant Pogonomyrmex barbatus. Proceedings of the National Academy of Sciences of the United States of America 108, 5667-5672.
100. Snodgrass, R. E. (1925). Anatomy and Physiology of the Honey Bee. McGraw-Hill Book Company, New York.
101. Spannhoff, A., Kim, Y. K., Raynal, N. J., Gharibyan, V., Su, M. B., Zhou, Y. Y., Li, J., Castellano, S., Sbardella, G., Issa, J. P. & Bedford, M. T. (2011). Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Reports 12, 238-243.
102. Srisuparbh, D., Klinbunga, S., Wongsiri, S. & Sittipraneed, S. (2003). Isolation and characterization of major royal jelly cDNAs and proteins of the honey bee (Apis cerana). Journal of Biochemistry and Molecular Biology 36, 572-579.
103. Su, S., Albert, Š., Chen, S. & Zhong, B. (2005). Molecular cloning and analysis of four cDNAs from the heads of Apis cerana cerana nurse honeybees coding for major royal jelly proteins. Apidologie 36, 389-401.
104. Suen, G., Teiling, C., Li, L., Holt, C., Abouheif, E., Bornberg-Bauer, E., Bouffard, P., Caldera, E. J., Cash, E., Cavanaugh, A., Denas, O., Elhaik, E., Favé, M. J., Gadau, J., Gibson, J. D., et al. (2011). The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics 7, e1002007.
105. Tamura, S., Amano, S., Kono, T., Kondoh, J., Yamaguchi, K., Kobayashi, S., Ayabe, T. & Moriyama, T. (2009a). Molecular characteristics and physiological functions of major royal jelly protein 1 oligomer. Proteomics 9, 5534-5543.
106. Tamura, S., Kono, T., Harada, C., Yamaguchi, K. & Moriyama, T. (2009b). Estimation and characterisation of major royal jelly proteins obtained from the honeybee Apis merifera. Food Chemistry 114, 1491-1497.
107. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731-2739.
108. Tao, T., Su, S. K., Miao, Y. G., Yue, W. F., Du, H. H., Chen, S. L., Liu, F. & Zhan, Y. (2008). Expression of apalbumin1 of Apis cerana cerana in the larvae of silkworm, Bombyx mori. Journal of Agricultural and Food Chemistry 56, 9464-9468.
109. Thien, F. C., Leung, R., Baldo, B. A., Weiner, J. A., Plomley, R. & Czarny, D. (1996). Asthma and anaphylaxis induced by royal jelly. Clinical and Experimental Allergy 26, 216-222.
110. Thompson, G. J., Kucharski, R., Maleszka, R. & Oldroyd, B. P. (2006). Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees. Insect Molecular Biology 15, 637-644.
111. Ueno, T., Nakaoka, T., Takeuchi, H. & Kubo, T. (2009). Differential gene expression in the hypopharyngeal glands of worker honeybees (Apis mellifera L.) associated with an age-dependent role change. Zoological Science 26, 557-563.
112. Valenzuela, J. G., Belkaid, Y., Garfield, M. K., Mendez, S., Kamhawi, S., Rowton, E. D., Sacks, D. L. & Ribeiro, J. M. (2001). Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. The Journal of Experimental Medicine 194, 331-342.
113. Volf, P., Skarupová, S. & Man, P. (2002). Characterization of the lectin from females of Phlebotomus duboscqi sand flies. European Journal of Biochemistry 269, 6294-6301.
114. Von Planta, A. (1888). Ueber den Futtersaft der Bienen. Hoppe-Seyler's Zeitschrift für Physiologische Chemie 12, 327-354(only in German).
115. Watanabe, K., Shinmoto, H., Kobori, M., Tsushida, T., Shinohara, K., Kanaeda, J. & Yonekura, M. (1996). Growth stimulation with honey royal jelly DIII protein of human lymphocytic cell lines in a serum-free medium. Biotechnology Techniques 10, 959-962.
116. Watanabe, K., Shinmoto, H., Kobori, M., Tsushida, T., Shinohara, K., Kanaeda, J. & Yonekura, M. (1998). Stimulation of cell growth in the U-937 human myeloid cell line by honey royal jelly protein. Cytotechnology 26, 23-27.
117. Werren, J. H., Richards, S., Desjardins, C. A., Niehuis, O., Gadau, J., Colbourne, J. K., Beukeboom, L. W., Desplan, C., Elsik, C. G., Grimmelikhuijzen, C. J., Kitts, P., Lynch, J. A., Murphy, T., Oliveira, D. C., Smith, C. D., et al. (2010). Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343-348.
118. Whitfield, C. W., Band, M. R., Bonaldo, M. F., Kumar, C. G., Liu, L., Pardinas, J. R., Robertson, H. M., Soares, M. B. & Robinson, G. E. (2002). Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Research 12, 555-566.
119. Xu, X., Oliveira, F., Chang, B. W., Collin, N., Gomes, R., Teixeira, C., Reynoso, D., My Pham, V., Elnaiem, D. E., Kamhawi, S., Ribeiro, J. M., Valenzuela, J. G. & Andersen, J. F. (2011). Structure and function of a "yellow" protein from saliva of the sand fly Lutzomyia longipalpis that confers protective immunity against Leishmania major infection. Journal of Biological Chemistry 286, 32383-32393.
120. Yu, F., Mao, F. & Jianke, L. (2010). Royal jelly proteome comparison between A. mellifera ligustica and A. cerana cerana. Journal of Proteome Research 9, 2207-2215.
121. Zhang, L., Fang, Y., Li, R., Feng, M., Han, B., Zhou, T. & Li, J. (2012). Towards posttranslational modification proteome of royal jelly. Journal of Proteomics 75, 5327-5341.