Eur. J. Entomol. 110 (1): 21-30, 2013 | DOI: 10.14411/eje.2013.003

Molecular cloning and characterization of the S6K-p70 gene in Chinese honeybees, Apis cerana cerana (Hymenoptera: Apidae)

Yingqi CAI1, Taobo AI1, Xiaoli YU1, Baohua XU2, Xingqi GUO1
1 College of Life Sciences, Shandong Agricultural University, Taian, Shandong, 271018, P. R. China; e-mails: caiyingq@sdau.edu.cn (Y. Cai), crazywolf119.-@163.com (T. Ai), dos-888@163.com (X. Yu), and xqguo@sdau.edu.cn (X. Guo)
2 College of Animal Science and Technology, Shandong Agricultural University, Taian, Shandong, 271018, P. R. China; e-mail: bhxu@sdau.edu.cn

The ribosomal protein S6 kinase (S6K) plays a pivotal role in developmental processes and cell survival by participating in protein synthesis relevant signaling pathways. In the present study, an S6K gene (AccS6K-p70) was isolated and characterized from the Chinese honeybee, Apis cerana cerana (Fabricius) (Hymenoptera: Apidae), an important economic insect in the agricultural industry. The cDNA of AccS6K-p70 was 1683 bp in length and predicted to encode a protein of 467 amino acid residues. Sequence and structure analysis showed that there was a conserved catalytic domain in AccS6K-p70, whilst a phosphorylation site was found in the conserved part of the catalytic domain. Development relevant transcription factor binding sites found in the 5'-flanking region of AccS6K-p70 suggest that AccS6K-p70 might be involved in A. c. cerana development. Furthermore, quantitative PCR revealed that the expression levels of AccS6K-p70 were higher in head and thorax than in other tissues. The AccS6K-p70 was highly expressed in both larvae and adults compared with that in pupae, whilst expression of the gene was significantly down-regulated by hydrogen peroxide (H2O2) (although initially and slightly increased by it) and pyriproxyfen (a juvenile hormone analogue insecticide) stresses. These results suggest that AccS6K-p70 may play critical roles in developmental processes and cell survival in A. c. cerana, whilst both oxidative stress and pyriproxyfen may impair S6K-p70 mediated developmental processes by down-regulation of AccS6K-p70 expression.

Keywords: Apidae, ribosomal protein S6 kinase, Apis cerana cerana, development, environmental stresses, expression pattern

Received: May 28, 2012; Revised: July 9, 2012; Accepted: July 9, 2012; Published: January 2, 2013  Show citation

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CAI, Y., AI, T., YU, X., XU, B., & GUO, X. (2013). Molecular cloning and characterization of the S6K-p70 gene in Chinese honeybees, Apis cerana cerana (Hymenoptera: Apidae). EJE, 110(1), 21-30. doi: 10.14411/eje.2013.003
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    References

    1. ARNOLD K., BORDOLI L., KOPP J. & SCHWEDE T. 2006: The SWISS-MODEL Workspace: A web-based environment for protein structure homology modelling. - Bioinformatics 22: 195-201 Go to original source...
    2. AZEVEDO S.V., CARANTON O.A.M., OLIVEIRA T.L. & HARTFELDER K. 2011: Differential expression of hypoxia pathway genes in honeybee (Apis mellifera L.) caste development. - J. Insect Physiol. 57: 38-45 Go to original source...
    3. CHANG M.V., CHANG J.L., GANGOPADHYAY A., SHEARER A. & CADIGAN K. 2008: Activation of wingless targets requires bipartite recognition of DNA by TCF. - Curr. Biol. 18: 1877-1881 Go to original source...
    4. CHIANG G.G. & ABRAHAM R.T. 2007: Targeting the mTOR signaling network in cancer. - Trends Mol. Med. 13: 433-422 Go to original source...
    5. CHO I., HORN L., FELIX T.M., FOSTER L., GREGORY G., STARZGAIANO M., CHAMBERS M.M., LUCA M.D. & LEIPS J. 2010: Age- and diet-specific effects of variation at S6 Kinase on life history, metabolic, and immune response traits in Drosophila melanogaster. - DNA Cell Biol. 29: 473-485 Go to original source...
    6. CONSOULAS C., LEVINE R.B. & RESTIFO L.L. 2005: The steroid hormone-regulated gene broad complex is required for dendritic growth of motorneurons during metamorphosis of Drosophila. - J. Compar. Neurol. 485: 321-337 Go to original source...
    7. DISTEFANO G., BOCA M., ROWE I., WODARCZYK C., MA L., PIONTEK K.B., GERMINO G.G., PANDOLFI P.P. & BOLETTA A. 2009: Polycystin-1 regulates extracellular signal-regulated kinase-dependent phosphorylation of tuberin to control cell size through mTOR and its downstream effectors S6K and 4EBP1. - Mol. Cell. Biol. 29: 2359-2371 Go to original source...
    8. FERRARI S. & THOMAS G. 1994: S6 phosphorylation and the p70s6k/p85s6k. - Critic. Rev. Biochem. Mol. Biol. 29: 385-413 Go to original source...
    9. FOSTER D.A. 2004: Targeting mTOR-mediated survival signals in anticancer therapeutic strategies. - Expert Rev. Anti-Infect. Ther. 4: 691-701 Go to original source...
    10. GEOURJON C. & DELEAGE G. 1995: SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. - Comput. Appl. Biosci. 11: 681-684 Go to original source...
    11. GRIMALDI D. & ENGEL E.S. 2005: Evolution of the Insects. Cambridge University Press, Cambridge, 772 pp
    12. GUEX N. & PEITSCH M.C. 1997: SWISS-MODEL and the SwissPdbViewer: An environment for comparative protein modelling. - Electrophoresis 18: 2714-2723 Go to original source...
    13. HARADA H., ANDERSEN J.S., MANN M., TERADA N. & KORSMEYER S.J. 2001: p70S6 kinase signals cell survival as well as growth, in activating the pro-apoptotic molecule BAD. - Proc. Nat. Acad. Sci. U. S. A. 98: 9666-9670 Go to original source...
    14. KAMAKURA M. 2011: Royalactin induces queen differentiation in honeybees. - Nature 26: 478-483 Go to original source...
    15. KESHWANI M.M., DAAKE S., NEWTON A.C., HARRIS T.K. & TAYLOR S.S. 2011: Hydrophobic motif phosphorylation is not required for activation loop phosphorylation of p70 Ribosomal protein S6 kinase 1 (S6K1). - J. Biol. Chem. 286: 23552-23558 Go to original source...
    16. KRAB L.C., GOORDEN S.M.I. & ELGERSMA Y. 2008: Oncogenes on my mind: ERK and MTOR signaling in cognitive diseases. - Cell 24: 498-510. Go to original source...
    17. LANE H.A., FERNANDEZ A., LAMB N.J.C. & THOMAS G. 1993: p70s6k function is essential for G1 progression. - Nature 363: 170-172 Go to original source...
    18. LIVAK K.J. & SCHMITTGEN T.D. 2001: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). - Methods 25: 402-408 Go to original source...
    19. MIRON M., LASKO P. & SONENBERG N. 2003: Signaling from Akt to FRAP/TOR targets both 4E-BP and S6K in Drosophila melanogaster. - Mol. Cell. Biol. 23: 9117-9126 Go to original source...
    20. PEI J. & HUGON J. 2008: mTOR-dependent signalling in Alzheimer's disease. - J. Cell. Mol. Med. 12: 2525-2532 Go to original source...
    21. PROUD C.G. 2004: The multifaceted role of mTOR in cellular stress responses. - DNA Repair 3: 927-934 Go to original source...
    22. REINHARD C., THOMAS G. & KOZMA S.C. 1992: A single gene encodes two isoforms of the p70 S6 kinase: Activation upon mitogenic stimulation. - Proc. Nat. Acad. Sci. U. S. A. 89: 4052-4056 Go to original source...
    23. REINHARD C., FERNANADEZ A., LAMB N.J.C. & THOMAS G. 1994: Nuclear localization of p85s6k: functional requirement for entry into S phase. - EMBO J. 13: 1557-1565 Go to original source...
    24. RINTELEN F., STOCKER H., THOMAS G. & HAFEN E. 2001: PDK1 regulates growth through Akt and S6K in Drosophila. - Proc. Nat. Acad. Sci. U. S. A. 98: 15020-15025 Go to original source...
    25. SCHAEFER C.H. & MULLIGAN F.S. 1991: Potential for resistance to pyriproxyfen: A promising new mosquito larvicide. - J. Am. Mosq. Contr. Assoc. 7: 409-411
    26. SCHEPER M.A., CHAISUPARAT R., NIKITAKIS N.G. & SAUK J.J. 2008: Expression and alterations of the PTEN/AKT/mTOR pathway in ameloblastomas. - Oral Dis. 14: 561-568 Go to original source...
    27. SCHWEDE T., KOPP J., GUEX N. & PEITSCH M.C. 2003: SWISSMODEL: an automated protein homology-modeling server. - Nucl. Acids Res. 31: 3381-3385 Go to original source...
    28. SHANDALA T., KORTSCHAK R.D., GREGORY S. & SAINT R. 1999: The Drosophila dead ringer gene is required for early embryonic patterning through regulation of argos and buttonhead expression. - Development 126: 4341-4349 Go to original source...
    29. SONG Q. & GILBERT L.I. 1997: Molecular cloning, developmental expression, and phosphorylation of ribosomal protein S6 in the endocrine gland responsible for insect molting. - J. Biol. Chem. 272: 4429-4435 Go to original source...
    30. STEWART M.J., BERRY C.A., ZILBERMAN F., THOMAS G. & KOZMA S.C. 1996: The Drosophila p70s6k homolog exhibits conserved regulatory elements and rapamycin sensitivity. - Proc. Nat. Acad. Sci. U. S. A. 93: 10791-10796 Go to original source...
    31. SWIECH L., PERYCZ M., MALIK A. & JAWORSKI J. 2008: Role of mTOR in physiology and pathology of the nervous system. - Biochim. Biophys. Acta 1784: 116-132 Go to original source...
    32. TAGA M., MOUTON-LIGER F., PAQUET C. & HUGON J. 2011: Modulation of oxidative stress and tau phosphorylation by the mTOR activator phosphatidic acid in SH-SY5Y cells. - FEBS Letters 585: 1801-1806 Go to original source...
    33. TANAKA K.K., BRYANTSEV A.L. & CRIPPS R.M. 2008: Myocyte enhancer factor 2 and chorion factor 2 collaborate in activation of the myogenic program in Drosophila. - Mol. Cell. Biol. 28: 1616-1629 Go to original source...
    34. WATSON K.L., CHOU M.M., BLENIS J., GELBART W.M. & ERIKSON R.L. 1996: A Drosophila gene structurally and functionally homologous to the mammalian 70-kDa S6 kinase gene. - Proc. Nat. Acad. Sci. U. S. A. 93: 13694-13698 Go to original source...
    35. WENG Q.P., KOZLOWSKI M., BELHAM C., ZHANG A., COMB M.J. & AVRUCH J. 1998: Regulation of the p70 S6 Kinase by phosphorylation in vivo. - J. Biol. Chem. 273: 16621-16629 Go to original source...
    36. XU P., SHI M. & CHEN X.X. 2009: Antimicrobial peptide evolution in the Asiatic honeybee Apis cerana. - PLoS One 4: e4239 Go to original source...
    37. YU F., KANG M., MENG F., GUO X. & XU B. 2011: Molecular cloning and characterization of a thioredoxin peroxidase gene from Apis cerana cerana. - Insect Mol. Biol. 20: 367-378 Go to original source...

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