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Molecular Characterization and Expression Analysis of Ribosomal Protein S6 Gene in the Cashmere Goat (Capra hircus)

  • Bao, Wenlei (College of Life Science, Inner Mongolia University) ;
  • Hao, Xiyan (College of Life Science, Inner Mongolia University) ;
  • Zheng, Xu (College of Life Science, Inner Mongolia University) ;
  • Liang, Yan (College of Life Science, Inner Mongolia University) ;
  • Chen, Yuhao (College of Life Science, Inner Mongolia University) ;
  • Wang, Yanfeng (College of Life Science, Inner Mongolia University) ;
  • Wang, Zhigang (College of Life Science, Inner Mongolia University)
  • Received : 2013.03.17
  • Accepted : 2013.05.13
  • Published : 2013.11.01

Abstract

Ribosomal protein (rp) S6 is the substrate of ribosomal protein S6K (S6 kinase) and is involved in protein synthesis by mTOR/S6K/S6 signaling pathway. Some S6 cDNA have been cloned in mammals in recent years but has not been identified in the goat. To facilitate such studies, we cloned the cDNA encoding Cashmere goat (Capra hircus) S6 (GenBank accession GU131122) and then detected mRNA expression in seven tissues by real time PCR and protein expression in testis tissue by immunohistochemisty. Sequence analysis indicated that the obtained goat S6 was a 808 bp product, including a 3' untranslated region of 58 bp and an open reading frame of 750 bp which predicted a protein of 249 amino acids. The predicted amino acid sequence was highly homologous to cattle, human, mouse and rat S6. Expression analysis indicated S6 mRNA was expressed extensively in detected tissues and S6 protein was expressed in testis tissue.

Keywords

References

  1. Arnold, K., L. Bordoli, J. Kopp, and T. Schwede. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201. https://doi.org/10.1093/bioinformatics/bti770
  2. Bartel, D. P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233. https://doi.org/10.1016/j.cell.2009.01.002
  3. Boylan, J. M., P. Anand, and P. A. Gruppuso. 2001. Ribosomal protein S6 phosphorylation and function during late gestation liver development in the rat. J. Biol. Chem. 276:44457-44463. https://doi.org/10.1074/jbc.M103457200
  4. Chen, W. and D. P. Dittmer. 2011. Ribosomal protein S6 interacts with the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 85:9495-9505. https://doi.org/10.1128/JVI.02620-10
  5. Fenton, T. R. and I. T. Gout. 2011. Functions and regulation of the 70kDa ribosomal S6 kinases. Int. J. Biochem. Cell Biol. 43:47-59. https://doi.org/10.1016/j.biocel.2010.09.018
  6. Flotow, H. and G. Thomas. 1992. Substrate recognition determinants of the mitogen-activated 70K S6 kinase from rat liver. J. Biol. Chem. 267:3074-3078.
  7. Guex, N. and M. C. Peitsch. 1997. $SWISS{{\copyright}}$\MODEL and the $Swiss{{\copyright}}$\Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723. https://doi.org/10.1002/elps.1150181505
  8. Hay, N. and N. Sonenberg. 2004. Upstream and downstream of mTOR. Genes Dev. 18:1926-1945. https://doi.org/10.1101/gad.1212704
  9. Hutchinson, M. S., Y. Figenschau, B. Almas, I. Njolstad, and R. Jorde. 2011. Serum 25-hydroxyvitamin D levels in subjects with reduced glucose tolerance and type 2 diabetes - the Tromso OGTT-study. Internationale Zeitschrift fur Vitamin- und Ernahrungsforschung Journal international de vitaminologie et de nutrition. Int. J. Vit. Nutr. Res. 81:317-327. https://doi.org/10.1024/0300-9831/a000079
  10. Iwenofu, O. H., R. D. Lackman, A. P. Staddon, D. G. Goodwin, H. M. Haupt, and J. S. Brooks. 2008. Phospho-S6 ribosomal protein: a potential new predictive sarcoma marker for targeted mTOR therapy. Modern pathology: An official journal of the United States and Canadian Academy of Pathology, Inc. 21:231-237. https://doi.org/10.1038/modpathol.3800995
  11. Jefferies, H. B., S. Fumagalli, P. B. Dennis, C. Reinhard, R. B. Pearson, and G. Thomas. 1997. Rapamycin suppresses 5'TOP mRNA translation through inhibition of p70s6k. EMBO J. 16:3693-3704. https://doi.org/10.1093/emboj/16.12.3693
  12. Kahvejian, A., G. Roy, and N. Sonenberg. 2001. The mRNA closed-loop model: the function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harb. Symp. Quant. Biol. 66:293-300.
  13. Klann, E., M. D. Antion, J. L. Banko, and L. Hou. 2004. Synaptic plasticity and translation initiation. Learn. Mem. 11:365-372. https://doi.org/10.1101/lm.79004
  14. Krieg, J., J. Hofsteenge, and G. Thomas. 1988. Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J. Biol. Chem. 263:11473-11477.
  15. Kundu-Michalik, S., M. A. Bisotti, E. Lipsius, A. Bauche, A. Kruppa, T. Klokow, G. Kammler, and J. Kruppa. 2008. Nucleolar binding sequences of the ribosomal protein S6e family reside in evolutionary highly conserved peptide clusters. Mol. Biol. Evol. 25:580-590. https://doi.org/10.1093/molbev/msn002
  16. Laplante, M. and D. M. Sabatini. 2012. mTOR signaling in growth control and disease. Cell 149:274-293. https://doi.org/10.1016/j.cell.2012.03.017
  17. Ledda, M., M. Di Croce, B. Bedini, F. Wannenes, M. Corvaro, P. P. Boyl, S. Caldarola, F. Loreni, and F. Amaldi. 2005. Effect of 3'UTR length on the translational regulation of 5'-terminal oligopyrimidine mRNAs. Gene 344:213-220. https://doi.org/10.1016/j.gene.2004.09.023
  18. Li, Y., S. Mitsuhashi, M. Ikejo, N. Miura, T. Kawamura, T. Hamakubo, and M. Ubukata. 2012. Relationship between ATM and ribosomal protein S6 revealed by the chemical inhibition of Ser/Thr protein phosphatase type 1. Biosci. Biotechnol. Biochem. 76:486-494. https://doi.org/10.1271/bbb.110774
  19. Magnuson, J., F. Leonessa, and G. S. Ling. 2012. Neuropathology of explosive blast traumatic brain injury. Curr. Neurol. Neurosci. Rep. 12:570-579. https://doi.org/10.1007/s11910-012-0303-6
  20. Mayer, C., J. Zhao, X. Yuan, and I. Grummt. 2004. mTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev. 18:423-434. https://doi.org/10.1101/gad.285504
  21. Mazumder, B., V. Seshadri, and P. L. Fox. 2003. Translational control by the 3'-UTR: the ends specify the means. Trends Biochem. Sci. 28:91-98. https://doi.org/10.1016/S0968-0004(03)00002-1
  22. Parkhitko, C. A., C. O. Favorova, and E. P. Henske. 2011. Rabin8 protein interacts with GTPase Rheb and inhibits phosphorylation of Ser235/Ser236 in small ribosomal subunit protein S6. Acta Nat. 3:71-76.
  23. Pende, M., S. H. Um, V. Mieulet, M. Sticker, V. L. Goss, J. Mestan, M. Mueller, S. Fumagalli, S.C. Kozma, and G. Thomas. 2004. S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5'-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 24:3112-3124. https://doi.org/10.1128/MCB.24.8.3112-3124.2004
  24. Peterson, R. T., B. N. Desai, J. S. Hardwick, and S. L. Schreiber. 1999. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycinassociated protein. Proc. Natl. Acad. Sci. USA. 96:4438-4442. https://doi.org/10.1073/pnas.96.8.4438
  25. Proud, C. G. 2002. Regulation of mammalian translation factors by nutrients. Eur. J. Biochem. 269:5338-5349. https://doi.org/10.1046/j.1432-1033.2002.03292.x
  26. Romeo, S., C. Maglio, M. A. Burza, C. Pirazzi, K. Sjoholm, P. Jacobson, P. A. Svensson, M. Peltonen, L. Sjostrom, and L. M. Carlsson. 2012. Cardiovascular events after bariatric surgery in obese subjects with type 2 diabetes. Diabetes Care. 35:2613-2617. https://doi.org/10.2337/dc12-0193
  27. Rosner, M., C. Fuchs, H. Dolznig, and M. Hengstschlager. 2011. Different cytoplasmic/nuclear distribution of S6 protein phosphorylated at S240/244 and S235/236. Amino Acids 40:595-600. https://doi.org/10.1007/s00726-010-0684-2
  28. Rosner, S., J. Konnerth, B. Plank, D. Salaberger, and C. Hansmann. 2010. Radial shrinkage and ultrasound acoustic emissions of fresh versus pre-dried Norway spruce sapwood. Trees (Berl West). 24:931-940. https://doi.org/10.1007/s00468-010-0464-3
  29. Ruvinsky, I., M. Katz, A. Dreazen, Y. Gielchinsky, A. Saada, N. Freedman, E. Mishani, G. Zimmerman, J. Kasir, and O. Meyuhas. 2009. Mice deficient in ribosomal protein S6 phosphorylation suffer from muscle weakness that reflects a growth defect and energy deficit. PLoS One. 4:e5618. https://doi.org/10.1371/journal.pone.0005618
  30. Ruvinsky, I. and O. Meyuhas. 2006. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem. Sci. 31:342-348. https://doi.org/10.1016/j.tibs.2006.04.003
  31. Schmelzle, T. and M. N. Hall. 2000. TOR, a central controller of cell growth. Cell 103:253-262. https://doi.org/10.1016/S0092-8674(00)00117-3
  32. Schwede, T., J. Kopp, N. Guex, and M.C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucl. Acids Res. 31:3381-3385. https://doi.org/10.1093/nar/gkg520
  33. Stark, A., J. Brennecke, N. Bushati, R. B. Russell, and S. M. Cohen. 2005. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 123:1133-1146. https://doi.org/10.1016/j.cell.2005.11.023
  34. Svitkin, Y. V. and N. Sonenberg. 2004. An efficient system for cap- and poly(A)-dependent translation in vitro. Methods Mol. Biol. 257:155-170.
  35. Tanguay, R. L. and D. R. Gallie. 1996. Translational efficiency is regulated by the length of the 3' untranslated region. Mol. Cell. Biol. 16:146-156.
  36. Wullschleger, S., R. Loewith, and M. N. Hall. 2006. TOR signaling in growth and metabolism. Cell 124:471-484. https://doi.org/10.1016/j.cell.2006.01.016
  37. Zhang, R. and B. Su. 2009. Small but influential: the role of microRNAs on gene regulatory network and 3'UTR evolution. J. Genet. Genomics 36:1-6. https://doi.org/10.1016/S1673-8527(09)60001-1

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