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Defect of SIRT1-FoxO3a axis is associated with the production of reactive oxygen species during protein kinase CK2 downregulation-mediated cellular senescence and nematode aging

  • Ham, Hye-Jun (School of Life Sciences, BK21 Plus KNU Creative BioResearch Group, Kyungpook National University) ;
  • Park, Jeong-Woo (School of Life Sciences, BK21 Plus KNU Creative BioResearch Group, Kyungpook National University) ;
  • Bae, Young-Seuk (School of Life Sciences, BK21 Plus KNU Creative BioResearch Group, Kyungpook National University)
  • Received : 2018.07.12
  • Accepted : 2018.08.10
  • Published : 2019.04.30

Abstract

We investigated whether SIRT1 is associated with reactive oxygen species (ROS) accumulation during CK2 downregulation-mediated senescence. SIRT1 overexpression suppressed ROS accumulation, reduced transcription of FoxO3a target genes, and nuclear export and acetylation of FoxO3a, which were induced by CK2 downregulation in HCT116 and MCF-7 cells. Conversely, overexpression of a dominant-negative mutant SIRT1 (H363Y) counteracted decreased ROS levels, increased transcriptional activity of FoxO3a, and increased nuclear import and decreased acetylation of FoxO3a, which were induced by CK2 upregulation. CK2 downregulation destabilized SIRT1 protein via an ubiquitin-proteasome pathway in human cells, whereas CK2 overexpression reduced ubiquitination of SIRT1. Finally, the SIRT1 activator resveratrol attenuated the accumulation of ROS and lipofuscin as well as lifespan shortening, and reduced expression of the DAF-16 target gene sod-3, which were induced by CK2 downregulation in nematodes. Altogether, this study demonstrates that inactivation of the SIRT1-FoxO3a axis, at least in part, is involved in ROS generation during CK2 downregulation-mediated cellular senescence and nematode aging.

Keywords

References

  1. Campisi J (2013) Aging, cellular senescence, and cancer. Annu Rev Physiol 75, 685-705 https://doi.org/10.1146/annurev-physiol-030212-183653
  2. Rodier F and Campisi J (2011) Four faces of cellular senescence. J Cell Biol 192, 547-556 https://doi.org/10.1083/jcb.201009094
  3. Kuilman T, Michaloglou C, Mooi WJ and Peeper DS (2010) The essence of senescence. Genes Dev 24, 2463-2479 https://doi.org/10.1101/gad.1971610
  4. Liou GY and Storz P (2010) Reactive oxygen species in cancer. Free Radic Res 44, 479-496 https://doi.org/10.3109/10715761003667554
  5. Kang JY, Kim JJ, Jang SY and Bae YS (2009) The $p53-p21^{Cip1/WAF1}$ pathway is necessary for cellular senescence induced by the inhibition of protein kinase CKII in human colon cancer cells. Mol Cells 28, 489-494 https://doi.org/10.1007/s10059-009-0141-9
  6. Jeon SM, Lee SJ, Kwon TK et al (2010) NADPH oxidase is involved in protein kinase CKII down-regulation-mediated senescence through elevation of the level of reactive oxygen species in human colon cancer cells. FEBS Lett 584, 3137-3142 https://doi.org/10.1016/j.febslet.2010.05.054
  7. Park JH, Kim JJ and Bae YS (2013) Involvement of PI3K-AKT-mTOR pathway in protein kinase CKII inhibition-mediated senescence in human colon cancer cells. Biochem Biophys Res Commun 433, 420-425 https://doi.org/10.1016/j.bbrc.2013.02.108
  8. Park SY and Bae YS (2016) Inactivation of the FoxO3a transcription factor is associated with the production of reactive oxygen species during protein kinase CK2 downregulation-mediated senescence in human colon cancer and breast cancer cells. Biochem Biophys Res Commun 478, 18-24 https://doi.org/10.1016/j.bbrc.2016.07.106
  9. Park JH, Lee JH, Park JW et al (2017) Downregulation of protein kinase CK2 activity induces age-related biomarkers in C. elegans. Oncotarget 8, 36950-36963 https://doi.org/10.18632/oncotarget.16939
  10. Storz P (2011) Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid Redox Signal 14, 593-605 https://doi.org/10.1089/ars.2010.3405
  11. Brunet A, Bonni A, Zigmond MJ et al (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 https://doi.org/10.1016/S0092-8674(00)80595-4
  12. Senf SM, Sandesara PB, Reed SA and Judge AR (2011) p300 Acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol 300, 1490-1501 https://doi.org/10.1152/ajpcell.00255.2010
  13. Motta MC, Divecha N, Lemieux M et al (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell 116, 551-563 https://doi.org/10.1016/S0092-8674(04)00126-6
  14. Ferguson D, Shao N, Heller E et al (2015) SIRT1-FOXO3a regulate cocaine actions in the nucleus accumbens. J Neurosci 35, 3100-3111 https://doi.org/10.1523/JNEUROSCI.4012-14.2015
  15. Vaziri H, Dessain SK, Ng Eaton E et al (2001) hSIR2 (SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107, 149-159 https://doi.org/10.1016/S0092-8674(01)00527-X
  16. van der Veer E, Ho C, O'Neil C et al (2007) Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J Biol Chem 282, 10841-1085 https://doi.org/10.1074/jbc.C700018200
  17. Kang H, Jung JW, Kim MK and Chung JH (2009) CK2 is the regulator of SIRT1 substrate-binding affinity, deacetylase activity and cellular response to DNA-damage. PLoS One 4, e6611 https://doi.org/10.1371/journal.pone.0006611
  18. Jang SY, Kim SY and Bae YS (2011) p53 deacetylation by SIRT1 decreases during protein kinase CK2 downregulationmediated cellular senescence. FEBS Lett 585, 3360-3366 https://doi.org/10.1016/j.febslet.2011.09.027
  19. Wood JG, Rogina B, Lavu S et al (2004) Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430, 686-689 https://doi.org/10.1038/nature02789
  20. Viswanathan M, Kim SK, Berdichevsky A and Guarente L (2005) A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev Cell 9, 605-615 https://doi.org/10.1016/j.devcel.2005.09.017
  21. Murphy CT, McCarroll SA, Bargmann CI et al (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283 https://doi.org/10.1038/nature01789
  22. Ogg S, Paradis S, Gottlieb S et al (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999 https://doi.org/10.1038/40194
  23. Ryu SW, Woo JH, Kim YH et al (2006) Downregulation of protein kinase CKII is associated with cellular senescence. FEBS Lett 580, 988-994 https://doi.org/10.1016/j.febslet.2006.01.028
  24. Lee YH, Yuk HJ, Park KH and Bae YS (2013) Coumestrol induces senescence through protein kinase CKII inhibition-mediated reactive oxygen species production in human breast cancer and colon cancer cells. Food Chem 141, 381-388 https://doi.org/10.1016/j.foodchem.2013.03.053
  25. Hwang JS, Ham SA, Yoo T et al (2016) Upregulation of MKP-7 in response to rosiglitazone treatment ameliorates lipopolysaccharide-induced destabilization of SIRT1 by inactivating JNK. Pharmacol Res 114, 47-55 https://doi.org/10.1016/j.phrs.2016.10.014
  26. Cheng J, Liu C, Liu L et al (2016) MEK1 signaling promotes self-renewal and tumorigenicity of liver cancer stem cells via maintaining SIRT1 protein stabilization. Oncotarget 7, 20597-20611. https://doi.org/10.18632/oncotarget.7972
  27. Peng L, Yuan Z, Li Y et al (2015) Ubiquitinated sirtuin 1 (SIRT1) function is modulated during DNA damageinduced cell death and survival. J Biol Chem 290, 8904-8912 https://doi.org/10.1074/jbc.M114.612796
  28. Allende-Vega N, Dias S, Milne D and Meek D (2005) Phosphorylation of the acidic domain of Mdm2 by protein kinase CK2. Mol Cell Biochem 274, 85-90 https://doi.org/10.1007/s11010-005-3074-4
  29. Lee A, Rayner SL, De Luca A et al (2017) Casein kinase II phosphorylation of cyclin F at serine 621 regulates the Lys48-ubiquitylation E3 ligase activity of the $SCF^{(cyclin F)}$ complex. Open Biol 7, 170058 https://doi.org/10.1098/rsob.170058
  30. Lee SJ, Hwang AB and Kenyon C (2010) Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr Biol 20, 2131-2136 https://doi.org/10.1016/j.cub.2010.10.057