Proteomic analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee

Journal of Proteome Research

Volumn 12, Issue 1, 2013, Pages 404-411

  Fujita, Toshiyuki ^a   Kozuka Hata, Hiroko ^a   Ao Kondo, Hiroko ^a   Kunieda, Takekazu ^a   Oyama, Masaaki ^a   Kubo, Takeo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Age polyethism; Division of labor; Honeybee; Hypopharyngeal gland; Insulin signaling; Polyphenism; Postcerebral gland; Royal jelly; Thoracic gland

Indexed keywords

ALPHA GLUCOSIDASE; DEFENSIN; ROYAL JELLY; ROYAL JELLY PROTEIN; SECRETORY PROTEIN; SOMATOMEDIN BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXOCRINE GLAND; GENE EXPRESSION; HONEYBEE; HYPOPHARYNX; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEOMICS; SIGNAL TRANSDUCTION;

ANIMALS; BEES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FATTY ACIDS; HYPOPHARYNX; INSECT PROTEINS; PROTEOME; SPECIES SPECIFICITY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84874095237     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300700e     Document Type: Article

References (66)

1. Gilbert, S. F.; Epel, D. Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution; Sinauer Associates Inc.: Sunderland, MA, 2008.
2. Waterland, R. A.; Michels, K. B. Epigenetic epidemiology of the developmental origins hypothesis. Annu. Rev. Nutr. 2007, 27, 363-388.
3. Winston, M. The Biology of the Honey Bee; Harvard Univ Press: Cambridge, MA, 1987.
4. Schwander, T.; Lo, N.; Beekman, M.; Oldroyd, B. P.; Keller, L. Nature versus nurture in social insect caste differentiation. Trends Ecol. Evol. 2010, 25 (5), 275-282.
5. Honeybee Genome Sequencing Consortium.. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443, 931-949.
6. Drapeau, M. D.; Albert, S.; Kucharski, R.; Prusko, C.; Maleszka, R. Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honey bees. Genome Res. 2006, 16, 1385-1394.
7. Klaudiny, J.; Kulifajova, J.; Crailsheim, K.; Simuth, J. New approach to the study of division of labour in the honeybee colony (Apis mellifera L.). Apidologie 1994, 25, 596-600.
8. Klaudiny, J.; Hanes, J.; Kulifajova, J.; Albert, S.; Simuth, J. Molecular cloning of two cDNAs from the head of the nurse honey bee (Apis mellifera L.) for coding related proteins of royal jelly. J. Apic. Res. 1994, 33, 105-111.
9. Schmitzova?, J.; Klaudiny, J.; Albert, S.; Schro?der, W.; Schreckengost, W.; Hanes, J.; Ju?dova?, J.; Simu?th, J. A family of major royal jelly proteins of the honeybee Apis mellifera L. Cell. Mol. Life Sci. 1998, 54, 1020-1030.
10. Albert, S.; Klaudiny, J. The MRJP/YELLOW protein family of Apis mellifera: Identification of new members in the EST library. J. Insect Physiol. 2004, 50, 51-59.
11. Kubo, T.; Sasaki, M.; Nakamura, J.; Sasagawa, H.; Ohashi, K.; Takeuchi, H.; Natori, S. Change in the expression of hypopharyngealgland proteins of the worker honeybees (Apis mellifera L.) with age and/or role. J. Biochem. 1996, 119 (2), 291-295.
12. Kamakura, M. Royalactin induces queen differentiation in honeybees. Nature 2011, 473, 478-483.
13. Fujita, T.; Kozuka-Hata, H.; Uno, Y.; Nishikori, K.; Morioka, M.; Oyama, M.; Kubo, T. Functional analysis of the honeybee (Apis mellifera L.) salivary system using proteomics. Biochem. Biophys. Res. Commun. 2010, 397, 740-744.
14. Goodman, L. Form and Function in the Honey Bee; International Bee Research Association: Cardiff, U.K., 2003.
15. Snodgrass, R. E. Anatomy of the Honey Bee; Cornell Univ. Press: Ithaca, NY, 1956.
16. 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.
17. 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.
18. Schoenleben, S.; Sickmann, A.; Mueller, M. J.; Reinders, J. Proteome analysis of Apis mellifera royal jelly. Anal. Bioanal. Chem. 2007, 389, 1087-1093.
19. Qu, N.; Jiang, J.; Sun, L.; Lai, C.; Sun, L.; Wu, X. Proteomic characterization of royal jelly proteins in Chinese (Apis cerana cerana) and European (Apis mellifera) honeybees. Biochemistry (Mosc.) 2008, 73 (6), 676-680.
20. 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. Comprehensive royal jelly (RJ) proteomics using oneand two-dimensional proteomics platforms reveals novel RJ proteins and potential phospho/glycoproteins. J. Proteome Res. 2008, 7, 3194-3229.
21. Yu, F.; Mao, F.; Jianke, L. Royal jelly proteome comparison between A. mellifera ligustica and A. cerana cerana. J. Proteome Res. 2008, 9, 2207-2215.
22. Oyama, M.; Kozuka-Hata, H.; Tasaki, S.; Semba, K.; Hattori, S.; Sugano, S.; Inoue, J.; Yamamoto, T. Temporal perturbation of tyrosine-phosphoproteome dynamics reveals the system-wide regulatory networks. Mol. Cell. Proteomics 2009, 8, 226-231.
23. Hanes, J.; Simuth, J. Identification and partial characterization of the major royal jelly protein of the honey bee (Apis mellifera L.). J. Apic. Res. 1992, 31, 22.
24. Okuda, S.; Yamada, T.; Hamajima, M.; Itoh, M.; Katayama, T.; Bork, P.; Goto, S.; Kanehisa, M. KEGG Atlas mapping for global analysis of metabolic pathways. Nucleic Acids Res. 2008, 36, W423-W426.
25. 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.
26. Horton, P.; Park, K. J.; Obayashi, T.; Fujita, N.; Harada, H.; Adams-Collier, C. J.; Nakai, K. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007, 35, W585-W587.
27. Takeda, K.; Kaisho, T.; Akira, S. Toll-like receptors. Annu. Rev. Immunol. 2003, 21, 335-376.
28. Imler, J. L.; Hoffmann, J. A. Toll receptors in innate immunity. Trends Cell. Biol. 2001, 11, 304-311.
29. Lemaitre, B.; Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25, 697-743.
30. Aronstein, K.; Saldivar, E. Characterization of a honey bee Toll related receptor gene Am18w and its potential involvement in antimicrobial immune defense. Apidologie 2005, 36, 3-14.
31. Evans, J. D.; Aronstein, K.; Chen, Y. P.; Hetru, C.; Imler, J. L.; Jiang, H.; Kanost, M.; Thompson, G. J.; Zou, Z.; Hultmark, D. Immune pathways and defense mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 2006, 15, 645-656.
32. Tabeta, K.; Georgel, P.; Janssen, E.; Du, X.; Hoebe, K.; Crozat, K.; Mudd, S.; Shamel, L.; Sovath, S.; Goode, J.; Alexopoulou, L.; Flavell, R. A.; Beutler, B. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 3516-3521.
33. Shi, Z.; Cai, Z.; Wen, S.; Chen, C.; Gendron, C.; Sanchez, A.; Patterson, K.; Fu, S.; Yang, J.; Wildman, D.; Finnell, R. H.; Zhang, D. Transcriptional regulation of the novel Toll-like receptor Tlr13. J. Biol. Chem. 2009, 284, 20540-20547.
34. Shi, Z.; Cai, Z.; Sanchez, A.; Zhang, T.; Wen, S.; Wang, J.; Yang, J.; Fu, S.; Zhang, D. A novel Toll-like receptor that recognizes vesicular stomatitis virus. J. Biol. Chem. 2011, 286, 4517-4524.
35. So, W. V.; Sarov-Blat, L.; Kotarski, C. K.; McDonald, M. J.; Allada, R.; Rosbash, M. takeout, a novel Drosophila gene under circadian clock transcriptional regulation. Mol. Cell. Biol. 2000, 20, 6935-6944.
36. Sarov-Blat, L.; So, W. V.; Liu, L.; Rosbash, M. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell 2000, 101, 647-656.
37. Dauwalder, B.; Tsujimoto, S.; Moss, J.; Mattox, W. The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Genes Dev. 2002, 16, 2879-2892.
38. Vanaphan, N.; Dauwalder, B.; Zufall, R. A. Diversification of takeout, a male-biased gene family in Drosophila. Gene 2011, 491, 142-148.
39. Hagai, T.; Cohen, M.; Bloch, G. Genes encoding putative Takeout/juvenile hormone binding proteins in the honeybee (Apis mellifera) and modulation by age and juvenile hormone of the takeoutlike gene GB19811. Insect Biochem. Mol. Biol. 2007, 37, 689-701.
40. Reichhart, J. M. Tip of another iceberg: Drosophila serpins. Trends Cell. Biol. 2005, 15, 659-665.
41. Zou, Z.; Lopez, D. L.; Kanost, M. R.; Evans, J. D.; Jiang, H. Comparative analysis of serine protease-related genes in the honey bee genome: possible involvement in embryonic development and innate immunity. Insect Mol. Biol. 2006, 15, 603-614.
42. Holly, J.; Perks, C. The role of insulin-like growth factor binding proteins. Neuroendocrinology 2006, 83, 154-160.
43. Wu, Q.; Brown, M. R. Signaling and function of insulin-like peptides in insects. Annu. Rev. Entomol. 2006, 51, 1-24.
44. Corona, M.; Velarde, R. A.; Remolina, S.; Moran-Lauter, A.; Wang, Y.; Hughes, K. A.; Robinson, G. E. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 7128-7133.
45. Ament, S. A.; Corona, M.; Pollock, H. S.; Robinson, G. E. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 4226-4231.
46. Wheeler, D. E.; Buck, N.; Evans, J. D. Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol. Biol. 2006, 15, 597-602.
47. de Azevedo, S. V.; Hartfelder, K. The insulin signaling pathway in honey bee (Apis mellifera) caste development-differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J. Insect Physiol. 2008, 54, 1064-1071.
48. Dixit, P. K.; Patel, N. G. Insulin-like activity in larval foods of the honeybee. Nature 1964, 202, 189-190.
49. Kramer, K. J.; Tager, H. S.; Childs, C. N.; Speirs, R. D. Insulinlike hypoglycemic and immunological activities in honeybee royal jelly. J. Insect Physiol. 1977, 23, 293-295.
50. O'Connor, K. J.; Baxter, D. The demonstration of insulin-like material in the honey bee, Apis mellifera. Comp. Biochem. Physiol. B 1985, 81, 755-760.
51. Takeuchi, H.; Kage, E.; Sawata, M.; Kamikouchi, A.; Ohashi, K.; Ohara, M.; Fujiyuki, T.; Kunieda, T.; Sekimizu, K.; Natori, S.; Kubo, T. Identification of a novel gene, Mblk-1, that encodes a putative transcription factor expressed preferentially in the large-type Kenyon cells of the honeybee brain. Insect Mol. Biol. 2001, 10, 487-494.
52. Park, J. M.; Kunieda, T.; Takeuchi, H.; Kubo, T. DNA-binding properties of Mblk-1, a putative transcription factor from the honeybee. Biochem. Biophys. Res. Commun. 2002, 291, 23-28.
53. Park, J. M.; Kunieda, T.; Kubo, T. The activity of Mblk-1, a mushroom body-selective transcription factor from the honeybee, is modulated by the ras/MAPK pathway. J. Biol. Chem. 2003, 278, 18689-18694.
54. Baehrecke, E. H.; Thummel, C. S. The Drosophila E93 gene from the 93F early puff displays stage-and tissue-specific regulation by 20-hydroxyecdysone. Dev. Biol. 1995, 171, 85-97.
55. Lee, C. Y.; Wendel, D. P.; Reid, P.; Lam, G.; Thummel, C. S.; Baehrecke, E. H.; et al. E93 directs steroid-triggered programmed cell death in Drosophila. Mol. Cell 2000, 6, 433-443.
56. Mou, X.; Duncan, D. M.; Baehrecke, E. H.; Duncan, I. Control of target gene specificity during metamorphosis by the steroid response gene E93. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 2949-2954.
57. Joliot, A.; Prochiantz, A. Transduction peptides: from technology to physiology. Nat. Cell Biol. 2004, 6, 189-196.
58. Ohashi, K.; Natori, S.; Kubo, T. Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). Eur. J. Biochem. 1999, 265, 127-133.
59. Chan, Q. W.; Howes, C. G.; Foster, L. J. Quantitative comparison of caste differences in honeybee hemolymph. Mol. Cell. Proteomics 2006, 5, 2252-2262.
60. 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 nursehoneybees (Apis mellifera L.). Insect Biochem. Mol. Biol. 2005, 35, 85-91.
61. Deseyn, J.; Billien, J. Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 2005, 36, 49-57.
62. Hrassnigg, N.; Crailsheim, K. Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies. J. Insect Physiol. 1998, 44, 929-939.
63. Feng, M.; Fang, Y.; Li, J. Proteomic analysis of honeybee worker (Apis mellifera) hypopharyngeal gland development. BMC Genomics 2009, 10, 645.
64. Jianke, L.; Mao, F.; Begna, D.; Yu, F.; Aijuan, Z. Proteome comparison of hypopharyngeal gland development between Italian and royal jelly producing worker honeybee (Apis mellifera L.). J. Proteome Res. 2010, 9 (12), 6578-6594.
65. Katzav-Gozansky, T.; Soroker, V.; Ionescu, A.; Robinson, G. E.; Hefetz, A. Task-related chemical analysis of labial gland volatile secretion in workerhoneybees (Apis mellifera ligustica). J. Chem. Ecol. 2001, 27 (5), 919-926.
66. Leoncini, I.; Le Conte, Y.; Costagliola, G.; Plettner, E.; Toth, A. L.; Wang, M.; Huang, Z.; Be?card, J. M.; Crauser, D.; Slessor, K. N.; Robinson, G. E. Regulation of behavioral maturation by a primer pheromone produced by adult worker honeybee. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (50), 17559-17564.