SIRT2 regulates tumour hypoxia response by promoting HIF-1α hydroxylation

Oncogene

Volumn 34, Issue 11, 2015, Pages 1354-1362

  Seo, K S ^a   Park, J H ^a   Heo, J Y ^a   Jing, K ^a   Han, J ^a   Min, K N ^b   Kim, C ^c   Koh, G Y ^c   Lim, K ^a   Kang, G Y ^d   Uee Lee, J ^e   Yim, Y H ^f   Shong, M ^a   Kwak, T H ^b   Kweon, G R ^a  

^a Chungnam National University   (South Korea)

^b R and D Center KT and G Life Sciences Corp   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^d Diatech Korea Co Ltd   (South Korea)

^e The Catholic University of Korea   (South Korea)

^f Korea Research Institute of Standards and Science   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN BINDING; SIRT2 PROTEIN, HUMAN; SIRTUIN 2; SMALL INTERFERING RNA;

ANIMAL; BAGG ALBINO MOUSE; CELL HYPOXIA; ENERGY METABOLISM; FEMALE; GENETICS; HELA CELL LINE; HUMAN; HYDROXYLATION; METABOLISM; MOUSE; NUDE MOUSE; PROTEIN STABILITY; RNA INTERFERENCE; TUMOR CELL LINE; UBIQUITINATION;

ANIMALS; CELL HYPOXIA; CELL LINE, TUMOR; ENERGY METABOLISM; FEMALE; HELA CELLS; HUMANS; HYDROXYLATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED BALB C; MICE, NUDE; NAD; PROLYL HYDROXYLASES; PROTEIN BINDING; PROTEIN STABILITY; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIRTUIN 2; UBIQUITINATION;

EID: 84896690461     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.76     Document Type: Article

References (45)

1. Weidemann A, Johnson RS. Biology of HIF-1alpha. Cell Death Differ 2008; 15: 621-627.
2. Melillo G. Inhibiting hypoxia-inducible factor 1 for cancer therapy. Mol Cancer Res 2006; 4: 601-605.
3. Zhang D, Li J, Costa M, Gao J, Huang C. JNK1 mediates degradation HIF-1alpha by a VHL-independent mechanism that involves the chaperones Hsp90/Hsp70. Cancer Res 2010; 70: 813-823.
4. Papadakis AI, Paraskeva E, Peidis P, Muaddi H, Li S, Raptis L et al. eIF2{alpha} Kinase PKR modulates the hypoxic response by Stat3-dependent transcriptional suppression of HIF-1{alpha}. Cancer Res 2010; 70: 7820-7829.
5. Semenza GL. HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 2009; 20: 51-56.
6. Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 2008; 8: 705-713.
7. Berra E, Ginouves A, Pouyssegur J. The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep 2006; 7: 41-45.
8. Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 2010; 40: 294-309.
9. Kwon SJ, Song JJ, Lee YJ. Signal pathway of hypoxia-inducible factor-1alpha phosphorylation and its interaction with von Hippel-Lindau tumor suppressor protein during ischemia in MiaPaCa-2 pancreatic cancer cells. Clin Cancer Res 2005; 11: 7607-7613.
10. Cheng J, Kang X, Zhang S, Yeh ET. SUMO-speci fic protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 2007; 131: 584-595.
11. Jeong JW, Bae MK, Ahn MY, Kim SH, Sohn TK, Bae MH et al. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 2002; 111: 709-720.
12. Houtkooper RH, Pirinen E, Auwerx J. Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 2012; 13: 225-238.
13. Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J et al. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 2011; 19: 416-428.
14. Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol Cell 2010; 38: 864-878.
15. Dioum EM, Chen R, Alexander MS, Zhang Q, Hogg RT, Gerard RD et al. Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science 2009; 324: 1289-1293.
16. Chen R, Dioum EM, Hogg RT, Gerard RD, Garcia JA. Hypoxia increases sirtuin 1 expression in a hypoxia-inducible factor-dependent manner. J Biol Chem 2011; 286: 13869-13878.
17. Laemmle A, Lechleiter A, Roh V, Schwarz C, Portmann S, Furer C et al. Inhibition of SIRT1 impairs the accumulation and transcriptional activity of HIF-1alpha protein under hypoxic conditions. PLoS One 2012; 7: e33433.
18. Krishnan J, Danzer C, Simka T, Ukropec J, Walter KM, Kumpf S et al. Dietary obesity-associated Hif1alpha activation in adipocytes restricts fatty acid oxidation and energy expenditure via suppression of the Sirt2-NAD+ system. Genes Dev 2012; 26: 259-270.
19. Luthi-Carter R, Taylor DM, Pallos J, Lambert E, Amore A, Parker A et al. SIRT2 inhibition achieves neuroprotection by decreasing sterol biosynthesis. Proc Natl Acad Sci USA 2010; 107: 7927-7932.
20. Jiang W, Wang S, Xiao M, Lin Y, Zhou L, Lei Q et al. Acetylation regulates gluconeogenesis by promoting PEPCK1 degradation via recruiting the UBR5 ubiquitin ligase. Mol Cell 2011; 43: 33-44.
21. North BJ, Verdin E. Mitotic regulation of SIRT2 by cyclin-dependent kinase 1-dependent phosphorylation. J Biol Chem 2007; 282: 19546-19555.
22. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 2004; 19: 176-182.
23. Miettinen M, Lindenmayer AE, Chaubal A. Endothelial cell markers CD31, CD34, and BNH9 antibody to H- and Y-antigens - evaluation of their specificity and sensitivity in the diagnosis of vascular tumors and comparison with von Willebrand factor. Mod Pathol 1994; 7: 82-90.
24. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 2005; 16: 4623-4635.
25. Geng H, Liu Q, Xue C, David LL, Beer TM, Thomas GV et al. HIF1alpha protein stability is increased by acetylation at lysine 709. J Biol Chem 2012; 287: 35496-35505.
26. Wang F, Chan CH, Chen K, Guan X, Lin HK, Tong Q. Deacetylation of FOXO3 by SIRT1 or SIRT2 leads to Skp2-mediated FOXO3 ubiquitination and degradation. Oncogene 2012; 31: 1546-1557.
27. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, Pouyssegur J. HIF prolylhydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J 2003; 22: 4082-4090.
28. Outeiro TF, Kontopoulos E, Altmann SM, Kufareva I, Strathearn KE, Amore AM et al. Sirtuin 2 inhibitors rescue alpha-synuclein-mediated toxicity in models of Parkinson's disease. Science 2007; 317: 516-519.
29. Kim HS, Vassilopoulos A, Wang RH, Lahusen T, Xiao Z, Xu X et al. SIRT2 maintains genome integrity and suppresses tumorigenesis through regulating APC/C activity. Cancer Cell 2011; 20: 487-499.
30. Hwang JH, Kim DW, Jo EJ, Kim YK, Jo YS, Park JH et al. Pharmacological stimulation of NADH oxidation ameliorates obesity and related phenotypes in mice. Diabetes 2009; 58: 965-974.
31. North BJ, Marshall BL, Borra MT, Denu JM, Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 2003; 11: 437-444.
32. Terzuoli E, Puppo M, Rapisarda A, Uranchimeg B, Cao L, Burger AM et al. Aminoflavone, a ligand of the aryl hydrocarbon receptor, inhibits HIF-1alpha expression in an AhR-independent fashion. Cancer Res 2010; 70: 6837-6848.
33. Hiratsuka M, Inoue T, Toda T, Kimura N, Shirayoshi Y, Kamitani H et al. Proteomics-based identification of differentially expressed genes in human gliomas: down-regulation of SIRT2 gene. Biochem Biophys Res Commun 2003; 309: 558-566.
34. Page EL, Robitaille GA, Pouyssegur J, Richard DE. Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms. J Biol Chem 2002; 277: 48403-48409.
35. Jin Y, Wu J, Song X, Song Q, Cully BL, Messmer-Blust A et al. RTEF-1, an upstream gene of hypoxia-inducible factor-1alpha, accelerates recovery from ischemia. J Biol Chem 2011; 286: 22699-22705.
36. van Uden P, Kenneth NS, Rocha S. Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem J 2008; 412: 477-484.
37. Kaelin WG Jr., Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008; 30: 393-402.
38. Tanaka H, Li Z, Ikuta K, Addo L, Akutsu H, Nakamura M et al. Iron facilitator LS081 reduces hypoxia-inducible factor-1alpha protein and functions as anticancer agent in hepatocellular carcinoma. Cancer Sci 2012; 103: 767-774.
39. Choi HJ, Song BJ, Gong YD, Gwak WJ, Soh Y. Rapid degradation of hypoxia-inducible factor-1alpha by KRH102053, a new activator of prolyl hydroxylase 2. Br J Pharmacol 2008; 154: 114-125.
40. Schwer B, Schumacher B, Lombard DB, Xiao C, Kurtev MV, Gao J et al. Neural sirtuin 6 (Sirt6) ablation attenuates somatic growth and causes obesity. Proc Natl Acad Sci USA 2010; 107: 21790-21794.
41. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD et al. SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 2010; 17: 41-52.
42. Massudi H, Grant R, Braidy N, Guest J, Farnsworth B, Guillemin GJ. Age-associated changes in oxidative stress and NAD+ metabolism in human tissue. PLoS One 2012; 7: e42357.
43. Kim SY, Jeoung NH, Oh CJ, Choi YK, Lee HJ, Kim HJ et al. Activation of NAD(P)H: quinone oxidoreductase 1 prevents arterial restenosis by suppressing vascular smooth muscle cell proliferation. Circ Res 2009; 104: 842-850.
44. Kim YH, Hwang JH, Noh JR, Gang GT, Tadi S, Yim YH et al. Prevention of salt-induced renal injury by activation of NAD(P)H:quinone oxidoreductase 1, associated with NADPH oxidase. Free Radic Biol Med 2012; 52: 880-888.
45. Zhang Q, Wang SY, Nottke AC, Rocheleau JV, Piston DW, Goodman RH. Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proc Natl Acad Sci USA 2006; 103: 9029-9033.