Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Molecular Characterization and Expression Analysis of S6K1 in Cashmere Goats (Capra hircus)

  • Wu, Manlin (College of Life Science, Inner Mongolia University) ;
  • 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) ;
  • Wang, Yanfeng (College of Life Science, Inner Mongolia University) ;
  • Wang, Zhigang (College of Life Science, Inner Mongolia University)
  • Received : 2012.12.21
  • Accepted : 2013.02.17
  • Published : 2013.08.01
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Abstract

p70 ribosomal S6 kinase (p70S6K) can integrate nutrient and growth factor signals to promote cell growth and survival. We report our molecular characterization of the complementary DNA (cDNA) that encodes the goat p70S6K gene 40S ribosomal S6 kinase 1 (S6K1) (GenBank accession GU144017) and its 3' noncoding sequence in Inner Mongolia Cashmere goats (Capra hircus). Goat S6K1 cDNA was 2,272 bp and include an open reading frame (ORF) of 1,578 bp, corresponding to a polypeptide of 525 amino acids, and a 694-residue 3' noncoding sequence with a polyadenylation signal at nucleotides 2,218 to 2,223. The relative abundance of S6K1 mRNA was measured by real-time PCR in 6 tissues, and p70S6K expression was examined by immunohistochemistry in heart and testis. The phosphorylation of p70S6K is regulated by mitogen-activated protein kinase (MAPK) signaling in fetal fibroblasts.

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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. Brian, M., E. Bilgen, and C. F. Diane. 2012. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem. J. 441:1-21. https://doi.org/10.1042/BJ20110892
  3. Carnevalli, L. S., K. Masuda, F. Frigerio, O. Le Bacquer, S. H. Um, V. Gandin, I. Topisirovic, N. Sonenberg, G. Thomas, and S. C. Kozma. 2010. S6K1 plays a critical role in early adipocyte differentiation. Dev. Cell 18:763-774. https://doi.org/10.1016/j.devcel.2010.02.018
  4. Casas-Terradellas, E., I. Tato, R. Bartrons, F. Ventura, and J. L. Rosa. 2008. ERK and p38 pathways regulate amino acid signalling. Biochim.Biophys.Acta 1783:2241-2254. https://doi.org/10.1016/j.bbamcr.2008.08.011
  5. Castaneda, T. R., W. Abplanalp, S. H. Um, P. T. Pfluger, B. Schrott, K. Brown, E. Grant, L. Carnevalli, S. C. Benoit, and D. A. Morgan. 2012. Metabolic control by S6 kinases depends on dietary lipids. PloS One 7:e32631. doi: 10.1371/journal.pone.0032631
  6. Charron, J., V. Bissonauth, and V. Nadeau. 2012. Implication of MEK1 and MEK2 in the establishment of the blood-placenta barrier during placentogenesis in mouse. Reprod. BioMed. Online 25:58-67. https://doi.org/10.1016/j.rbmo.2012.02.012
  7. Chung, J., C. J. Kuo, G. R. Crabtree, and J. Blenis. 1992. Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell 69:1227-1236. https://doi.org/10.1016/0092-8674(92)90643-Q
  8. Coffer, P. J., and J. R. Woodgett. 1994. Differential subcellular localization of two isoforms of p70 S6 protein kinase. Biochem. Biophys. Res. Commun. 198:780-786. https://doi.org/10.1006/bbrc.1994.1112
  9. Duvel, K., J. L. Yecies, S. Menon, P. Raman, A. I. Lipovsky, A. L. Souza, E. Triantafellow, Q. Ma, R. Gorski, and S. Cleaver. 2010. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol.cell 39:171-183. https://doi.org/10.1016/j.molcel.2010.06.022
  10. Dibble, C. C., J. M. Asara, and B. D. Manning. 2009. Characterization of Rictor phosphorylation sites reveals direct regulation of mTOR complex 2 by S6K1. Mol. Cell. Biol. 29:5657-5670. https://doi.org/10.1128/MCB.00735-09
  11. Duchene, S., E. Audouin, S. Crochet, M. J. Duclos, J. Dupont, and S. Tesseraud. 2008. Involvement of the ERK1/2 MAPK pathway in insulin-induced S6K1 activation in avian cells. Domest. Anim. Endocrinol. 34:63-73. https://doi.org/10.1016/j.domaniend.2006.11.001
  12. Favata, M. F., K. Y. Horiuchi, E. J. Manos, A. J. Daulerio, D. A. Stradley, W. S. Feeser, D. E. Van Dyk, W. J. Pitts, R. A. Earl, and F. Hobbs. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273:18623-18632. https://doi.org/10.1074/jbc.273.29.18623
  13. 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
  14. Gout, I., T. Minami, K. Hara, Y. Tsujishita, V. Filonenko, M. D. Waterfield, and K. Yonezawa. 1998. Molecular cloning and characterization of a novel p70 S6 kinase, p70 S6 kinase ${\beta}$ containing a proline-rich region. J. Biol.Chem. 273:30061-30064. https://doi.org/10.1074/jbc.273.46.30061
  15. Grove, J. R., P. Banerjee, A. Balasubramanyam, P. Coffer, D. Price, J. Avruch, and J. Woodgett. 1991. Cloning and expression of two human p70 S6 kinase polypeptides differing only at their amino termini. Mol. Cell. Biol. 11:5541-5550.
  16. Guex, N., and M. C. Peitsch. 1997. SWISS(c)\MODEL and the Swiss(c)\Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723. https://doi.org/10.1002/elps.1150181505
  17. Hamilton, D. L., A. Philp, M. MacKenzie, and K. Baar. 2010. Prolonged activation of S6K1 does not suppress IRS or PI-3 kinase signaling during muscle cell differentiation. BMC Cell Biol. 11:37. doi: 10.1186/1471-2121-11-37.
  18. Hannan, K. M., Y. Brandenburger, A. Jenkins, K. Sharkey, A. Cavanaugh, L. Rothblum, T. Moss, G. Poortinga, G. A. McArthur, and R. B. Pearson. 2003. mTOR-Dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol. Cell. Biol. 23:8862-8877. https://doi.org/10.1128/MCB.23.23.8862-8877.2003
  19. Hannan, K. M., G. Thomas, and R. B. Pearson. 2003. Activation of S6K1 (p70 ribosomal protein S6 kinase 1) requires an initial calcium-dependent priming event involving formation of a high-molecular-mass signalling complex. Biochem. J. 370:469-477. https://doi.org/10.1042/BJ20021709
  20. Hay, N., and N. Sonenberg. 2004. Upstream and downstream of mTOR. Genes Dev. 18:1926-1945. https://doi.org/10.1101/gad.1212704
  21. Julien, L. A., A. Carriere, J. Moreau, and P. P. Roux. 2010. mTORC1-activated S6K1 phosphorylates Rictor on threonine 1135 and regulates mTORC2 signaling. Mol. Cell. Biol. 30:908-921. https://doi.org/10.1128/MCB.00601-09
  22. Karapetsas, A., A. Giannakakis, M. Pavlaki, M. Panayiotidis, R. Sandaltzopoulos, and A. Galanis. 2011. Biochemical and molecular analysis of the interaction between ERK2 MAP kinase and hypoxia inducible factor-1alpha. Int. J. Biochem. Cell. Biol. 43:1582-1590. https://doi.org/10.1016/j.biocel.2011.07.007
  23. Kim, D., A. Akcakanat, G. Singh, C. Sharma, and F. Meric-Bernstam. 2009. Regulation and localization of ribosomal protein S6 kinase 1 isoforms. Growth Factors 27:12-21. https://doi.org/10.1080/08977190802556986
  24. 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
  25. Li, S., W. Ogawa, A. Emi, K. Hayashi, Y. Senga, K. Nomura, K. Hara, D. Yu, and M. Kasuga. 2011. Role of S6K1 in regulation of SREBP1c expression in the liver. Biochem. Biophys. Res. Commun. 412:197-202. https://doi.org/10.1016/j.bbrc.2011.07.038
  26. Medeiros, C., M. J. Frederico, G. da Luz, J. R. Pauli, A. S. Silva, R. A. Pinho, L. A. Velloso, E. R. Ropelle, and C. T. De Souza. 2011. Exercise training reduces insulin resistance and upregulates the mTOR/p70S6k pathway in cardiac muscle of diet-induced obesity rats. J. Cell. Physiol. 226:666-674. https://doi.org/10.1002/jcp.22387
  27. Melnik, B. C. 2012. Leucine signaling in the pathogenesis of type 2 diabetes and obesity. World J. Diabetes 3:38-53. https://doi.org/10.4239/wjd.v3.i3.38
  28. Moreno-Navarrete, J. M., F. Ortega, M. A. Sanchez-Garrido, M. Sabater, W. Ricart, A. Zorzano, M. Tena-Sempere, and J. M. Fernandez-Real. 2013. Phosphorylated S6K1 (Thr389) is a molecular adipose tissue marker of altered glucose tolerance. J. Nutr. Biochem. 24:32-38. doi:10.1016/j.jnutbio.2012.01.005
  29. Nawroth, R., F. Stellwagen, W. A. Schulz, R. Stoehr, A. Hartmann, B. J. Krause, J. E. Gschwend, and M. Retz. 2011. S6K1 and 4E-BP1 are independent regulated and control cellular growth in bladder cancer. PLoS One 6:e27509. doi: 10.1371/ journal.pone.0027509
  30. 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
  31. Pullen, N., P. B. Dennis, M. Andjelkovic, A. Dufner, S. C. Kozma, B. A. Hemmings, and G. Thomas. 1998. Phosphorylation and activation of p70s6k by PDK1. Science 279:707-710. https://doi.org/10.1126/science.279.5351.707
  32. Ragan, T. J., D. B. Ross, M. M. Keshwani, and T. K. Harris. 2008. Expression, purification, and characterization of a structurally disordered and functional C-terminal autoinhibitory domain (AID) of the 70 kDa 40S ribosomal protein S6 kinase-1 (S6K1). Protein Expr. Purif. 57:271-279. https://doi.org/10.1016/j.pep.2007.09.014
  33. Reinhard, C., A. Fernandez, N. Lamb, and G. Thomas. 1994. Nuclear localization of p85s6k: functional requirement for entry into S phase. EMBO J. 13:1557-1565.
  34. Rolfe, M., L. E. McLEOD, P. F. Pratt, and C. G. Proud,. 2005. Activation of protein synthesis in cardiomyocytes by the hypertrophic agent phenylephrine requires the activation of ERK and involves phosphorylation of tuberous sclerosis complex 2 (TSC2). Biochem. J. 388:973-984. https://doi.org/10.1042/BJ20041888
  35. Rosner, M., and M. Hengstschlager. 2011. Nucleocytoplasmic localization of p70 S6K1, but not of its isoforms p85 and p31, is regulated by TSC2/mTOR. pncogene 30:4509-4522.
  36. Rosner, M., K. Schipany, and M. Hengstschlager. 2012. p70 S6K1 nuclear localization depends on its mTOR-mediated phosphorylation at T389, but not on its kinase activity towards S6. Amino Acids 42:2251-2256. https://doi.org/10.1007/s00726-011-0965-4
  37. Saitoh, M., N. Pullen, P. Brennan, D. Cantrell, P. B. Dennis, and G. Thomas. 2002. Regulation of an activated S6 kinase 1 variant reveals a novel mammalian target of rapamycin phosphorylation site. J.Biol. Chem. 277:20104-20112. https://doi.org/10.1074/jbc.M201745200
  38. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385. https://doi.org/10.1093/nar/gkg520
  39. Selman, C., J. Tullet, D. Wieser, E. Irvine, S. J. Lingard, A. I. Choudhury, M. Claret, H. Al-Qassab, D. Carmignac, and F. Ramadani. 2009. Ribosomal Protein S6 kinase 1 signaling regulates mammalian life span. Science 326:140-144. https://doi.org/10.1126/science.1177221
  40. Tandon, P., C. A. Gallo, S. Khatri, J. F. Barger, H. Yepiskoposyan, and D. R. Plas. 2011. Requirement for ribosomal protein S6 kinase 1 to mediate glycolysis and apoptosis resistance induced by Pten deficiency. Proc. Natl. Acad.Sci. 108:2361-2365. https://doi.org/10.1073/pnas.1013629108
  41. Valovka, T., F. Verdier, R. Cramer, A. Zhyvoloup, T. Fenton, H. Rebholz, M. L. Wang, M. Gzhegotsky, A. Lutsyk, G. Matsuka, V. Filonenko, L. Wang, C. G. Proud, P. J. Parker, and I. T. Gout. 2003. Protein kinase C phosphorylates ribosomal protein S6 kinase betaII and regulates its subcellular localization. Mol. Cell. Biol. 23:852-863. https://doi.org/10.1128/MCB.23.3.852-863.2003
  42. Wang, P., Y. F. Guan, H. Du, Q. W. Zhai, D. F. Su, and C. Y. Miao. 2012. Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 8:77-87. https://doi.org/10.4161/auto.8.1.18274
  43. Wang, Y., Q. Ding, C. J. Yen, W. Xia, J. G. Izzo, J. Y. Lang, C. W. Li, J. L. Hsu, S. A. Miller, and X. Wang. 2012. The crosstalk of mTOR/S6K1 and hedgehog pathways. Cancer cell 21:374-387. https://doi.org/10.1016/j.ccr.2011.12.028
  44. Wang, Z., T. Liu, Y. Chen, X. Zhang, M. Liu, H. Fu, and D. Liu. 2012. Inhibition of mammalian target of rapamycin signaling by CCI-779 (Temsirolimus) induces growth inhibition and cell cycle arrest in Cashmere goat fetal fibroblasts (Capra hircus). DNA Cell Biol. 31:1095-1099. https://doi.org/10.1089/dna.2011.1559
  45. Wang Z., T. Fukazawa, T. Nishikawa, N. Watanabe, K. Sakurama, T. Motoki, S. Hatakeyama, O. Omori, T. Ohara, S. Tanabe, Y. Fujiwara, M. Takaoka, Y. Shirakawa, T. Yamatsuji, N. Tanaka, and Y. Naomoto. 2010. RAD001 offers a therapeutic intervention through inhibition of mTOR as a potential strategy for esophageal cancer. Oncol.Rep. 23:1167-1172.
  46. 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
  47. Xu, X., K. Chen, S. Kobayashi, D. Timm, and D. Liang. 2012. Resveratrol attenuates doxorubicin-induced cardiomyocyte death via inhibition of p70 S6 kinase 1-mediated autophagy. J. Pharmacol. Exp. Ther. 341:183-195. https://doi.org/10.1124/jpet.111.189589
  48. Zoncu, R., A. Efeyan, and D. M. Sabatini. 2011. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12:21-35. https://doi.org/10.1038/nrm3025