SIRT6 regulates Ras-related protein R-Ras2 by lysine defatty-acylation

eLife

Volumn 6, Issue , 2017, Pages

  Zhang, Xiaoyu ^a   Spiegelman, Nicole A ^a   Nelson, Ornella D ^a   Jing, Hui ^a   Lin, Hening ^a  

^a Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; LYSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PUROMYCIN; RAS PROTEIN; RAS RELATED PROTEIN R RAS2; SIRTUIN 6; STREPTAVIDIN; UNCLASSIFIED DRUG; RRAS PROTEIN, MOUSE; SIRT6 PROTEIN, MOUSE; SIRTUIN;

ACYLATION; ANIMAL CELL; ARTICLE; CELL CLONING; CELL FRACTIONATION; CELL MEMBRANE; CELL PROLIFERATION ASSAY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEFATTY ACYLATION; ESCHERICHIA COLI; FIBROBLAST; FLUORESCENCE; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; IN GEL FLUORESCENCE; MOUSE; NONHUMAN; PALMITOYLATION; PROTEIN PROCESSING; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ANIMAL; KNOCKOUT MOUSE; METABOLISM;

ACYLATION; ANIMALS; FIBROBLASTS; LYSINE; MICE; MICE, KNOCKOUT; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAS PROTEINS; SIRTUINS;

EID: 85018497337     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.25158     Document Type: Article

References (40)

1. Ahearn IM, Haigis K, Bar-Sagi D, Philips MR. 2011. Regulating the regulator: post-translational modification of RAS. Nature Reviews Molecular Cell Biology 13:39–51. doi: 10.1038/nrm3255, PMID: 22189424
2. Burnaevskiy N, Fox TG, Plymire DA, Ertelt JM, Weigele BA, Selyunin AS, Way SS, Patrie SM, Alto NM. 2013. Proteolytic elimination of N-myristoyl modifications by the shigella virulence factor IpaJ. Nature 496:106–109. doi: 10.1038/nature12004, PMID: 23535599
3. Charron G, Zhang MM, Yount JS, Wilson J, Raghavan AS, Shamir E, Hang HC. 2009. Robust fluorescent detection of protein fatty-acylation with chemical reporters. Journal of the American Chemical Society 131: 4967–4975. doi: 10.1021/ja810122f, PMID: 19281244
4. Clark GJ, Kinch MS, Gilmer TM, Burridge K, Der CJ. 1996. Overexpression of the Ras-related TC21/R-Ras2 protein may contribute to the development of human breast cancers. Oncogene 12:169–176. PMID: 8552388
5. Cox AD, Fesik SW, Kimmelman AC, Luo J, Der CJ. 2014. Drugging the undruggable RAS: mission possible? Nature Reviews Drug Discovery 13:828–851. doi: 10.1038/nrd4389, PMID: 25323927
6. Drivas GT, Shih A, Coutavas E, Rush MG, D’Eustachio P. 1990. Characterization of four novel ras-like genes expressed in a human teratocarcinoma cell line. Molecular and Cellular Biology 10:1793–1798. doi: 10.1128/MCB.10.4.1793, PMID: 2108320
7. Du J, Zhou Y, Su X, Yu JJ, Khan S, Jiang H, Kim J, Woo J, Kim JH, Choi BH, He B, Chen W, Zhang S, Cerione RA, Auwerx J, Hao Q, Lin H. 2011. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 334:806–809. doi: 10.1126/science.1207861, PMID: 22076378
8. Erdogan M, Pozzi A, Bhowmick N, Moses HL, Zent R. 2007. Signaling pathways regulating TC21-induced tumorigenesis. Journal of Biological Chemistry 282:27713–27720. doi: 10.1074/jbc.M703037200, PMID: 17656362
9. Gutierrez-Erlandsson S, Herrero-Vidal P, Fernandez-Alfara M, Hernandez-Garcia S, Gonzalo-Flores S, Mudarra-Rubio A, Fresno M, Cubelos B. 2013. R-RAS2 overexpression in tumors of the human central nervous system. Molecular Cancer 12:127. doi: 10.1186/1476-4598-12-127, PMID: 24148564
10. Hancock JF. 2003. Ras proteins: different signals from different locations. Nature Reviews Molecular Cell Biology 4:373–385. doi: 10.1038/nrm1105, PMID: 12728271
11. He B, Hu J, Zhang X, Lin H. 2014. Thiomyristoyl peptides as cell-permeable Sirt6 inhibitors. Organic & Biomolecular Chemistry 12:7498–7502. doi: 10.1039/C4OB00860J, PMID: 25163004
12. Huang Z, Cheng Y, Chiu PM, Cheung FM, Nicholls JM, Kwong DL, Lee AW, Zabarovsky ER, Stanbridge EJ, Lung HL, Lung ML. 2012. Tumor suppressor alpha B-crystallin (CRYAB) associates with the cadherin/catenin adherens junction and impairs NPC progression-associated properties. Oncogene 31:3709–3720. doi: 10.1038/onc.2011.529, PMID: 22158051
13. Jiang H, Khan S, Wang Y, Charron G, He B, Sebastian C, Du J, Kim R, Ge E, Mostoslavsky R, Hang HC, Hao Q, Lin H. 2013. SIRT6 regulates TNF-a secretion through hydrolysis of long-chain fatty acyl lysine. Nature 496:110– 113. doi: 10.1038/nature12038, PMID: 23552949
14. Jiang H, Zhang X, Lin H. 2016. Lysine fatty acylation promotes lysosomal targeting of TNF-a. Scientific Reports 6: 24371. doi: 10.1038/srep24371, PMID: 27079798
15. Kaidi A, Weinert BT, Choudhary C, Jackson SP. 2010. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329:1348–1353. doi: 10.1126/science.1192049, PMID: 20829486
16. Karnoub AE, Weinberg RA. 2008. Ras oncogenes: split personalities. Nature Reviews Molecular Cell Biology 9: 517–531. doi: 10.1038/nrm2438, PMID: 18568040
17. Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, Lin M, McCord RA, Ongaigui KC, Boxer LD, Chang HY, Chua KF. 2009. SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136:62–74. doi: 10.1016/j.cell.2008.10.052, PMID: 19135889
18. Lee JH, Pyon JK, Lee SH, Lee YJ, Kang SG, Kim CH, Kim DW, Nam HS, Park YH, Jeong DJ, Cho MK. 2011. Greater expression of TC21/R-ras2 in highly aggressive malignant skin cancer. International Journal of Dermatology 50:956–960. doi: 10.1111/j.1365-4632.2010.04846.x, PMID: 21781067
19. Linder ME, Deschenes RJ. 2007. Palmitoylation: policing protein stability and traffic. Nature Reviews Molecular Cell Biology 8:74–84. doi: 10.1038/nrm2084, PMID: 17183362
20. Liszt G, Ford E, Kurtev M, Guarente L. 2005. Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. Journal of Biological Chemistry 280:21313–21320. doi: 10.1074/jbc.M413296200, PMID: 15795229
21. Mao Z, Hine C, Tian X, Van Meter M, Au M, Vaidya A, Seluanov A, Gorbunova V. 2011. SIRT6 promotes DNA repair under stress by activating PARP1. Science 332:1443–1446. doi: 10.1126/science.1202723, PMID: 21680 843
22. Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, Damian M, Cheung P, Kusumoto R, Kawahara TL, Barrett JC, Chang HY, Bohr VA, Ried T, Gozani O, Chua KF. 2008. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452:492–496. doi: 10.1038/nature06736, PMID: 18337721
23. Michishita E, McCord RA, Boxer LD, Barber MF, Hong T, Gozani O, Chua KF. 2009. Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 8:2664–2666. doi: 10.4161/cc.8.16.9367, PMID: 19625767
24. Mostoslavsky R, Chua KF, Lombard DB, Pang WW, Fischer MR, Gellon L, Liu P, Mostoslavsky G, Franco S, Murphy MM, Mills KD, Patel P, Hsu JT, Hong AL, Ford E, Cheng HL, Kennedy C, Nunez N, Bronson R, Frendewey D, et al. 2006. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124:315–329. doi: 10.1016/j.cell.2005.11.044, PMID: 16439206
25. Murphy GA, Graham SM, Morita S, Reks SE, Rogers-Graham K, Vojtek A, Kelley GG, Der CJ. 2002. Involvement of phosphatidylinositol 3-kinase, but not RalGDS, in TC21/R-Ras2-mediated transformation. Journal of Biological Chemistry 277:9966–9975. doi: 10.1074/jbc.M109059200, PMID: 11788587
26. Rodriguez-Viciana P, Sabatier C, McCormick F. 2004. Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Molecular and Cellular Biology 24:4943–4954. doi: 10.1128/MCB.24.11.4943-4954.2004, PMID: 15143186
27. Rong R, He Q, Liu Y, Sheikh MS, Huang Y. 2002. TC21 mediates transformation and cell survival via activation of phosphatidylinositol 3-kinase/Akt and NF-kappaB signaling pathway. Oncogene 21:1062–1070. doi: 10.1038/sj.onc.1205154, PMID: 11850823
28. Rosário M, Paterson HF, Marshall CJ. 1999. Activation of the Raf/MAP kinase cascade by the Ras-related protein TC21 is required for the TC21-mediated transformation of NIH 3T3 cells. The EMBO Journal 18:1270–1279. doi: 10.1093/emboj/18.5.1270, PMID: 10064593
29. Rosário M, Paterson HF, Marshall CJ. 2001. Activation of the Ral and phosphatidylinositol 3’ kinase signaling pathways by the ras-related protein TC21. Molecular and Cellular Biology 21:3750–3762. doi: 10.1128/MCB.21.11.3750-3762.2001, PMID: 11340168
30. Sebastián C, Zwaans BM, Silberman DM, Gymrek M, Goren A, Zhong L, Ram O, Truelove J, Guimaraes AR, Toiber D, Cosentino C, Greenson JK, MacDonald AI, McGlynn L, Maxwell F, Edwards J, Giacosa S, Guccione E, Weissleder R, Bernstein BE, et al. 2012. The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism. Cell 151:1185–1199. doi: 10.1016/j.cell.2012.10.047, PMID: 23217706
31. Stevenson FT, Bursten SL, Locksley RM, Lovett DH. 1992. Myristyl acylation of the tumor necrosis factor alpha precursor on specific lysine residues. Journal of Experimental Medicine 176:1053–1062. doi: 10.1084/jem.176.4.1053, PMID: 1402651
32. Sundaresan NR, Vasudevan P, Zhong L, Kim G, Samant S, Parekh V, Pillai VB, Ravindra PV, Gupta M, Jeevanandam V, Cunningham JM, Deng CX, Lombard DB, Mostoslavsky R, Gupta MP. 2012. The sirtuin SIRT6 blocks IGF-Akt signaling and development of cardiac hypertrophy by targeting c-Jun. Nature Medicine 18: 1643–1650. doi: 10.1038/nm.2961, PMID: 23086477
33. Tasselli L, Xi Y, Zheng W, Tennen RI, Odrowaz Z, Simeoni F, Li W, Chua KF. 2016. SIRT6 deacetylates H3K18ac at pericentric chromatin to prevent mitotic errors and cellular senescence. Nature Structural & Molecular Biology 23:434–440. doi: 10.1038/nsmb.3202, PMID: 27043296
34. Toiber D, Erdel F, Bouazoune K, Silberman DM, Zhong L, Mulligan P, Sebastian C, Cosentino C, Martinez-Pastor B, Giacosa S, D’Urso A, Näär AM, Kingston R, Rippe K, Mostoslavsky R. 2013. SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling. Molecular Cell 51:454–468. doi: 10.1016/j.molcel.2013.06.018, PMID: 23911928
35. Wennerberg K, Rossman KL, Der CJ. 2005. The Ras superfamily at a glance. Journal of Cell Science 118:843– 846. doi: 10.1242/jcs.01660, PMID: 15731001
36. Yang B, Zwaans BM, Eckersdorff M, Lombard DB. 2009. The sirtuin SIRT6 deacetylates H3 K56Ac in vivo to promote genomic stability. Cell Cycle 8:2662–2663. doi: 10.4161/cc.8.16.9329, PMID: 19597350
37. Zhang X, Khan S, Jiang H, Antonyak MA, Chen X, Spiegelman NA, Shrimp JH, Cerione RA, Lin H. 2016. Identifying the functional contribution of the defatty-acylase activity of SIRT6. Nature Chemical Biology 12:614– 620. doi: 10.1038/nchembio.2106, PMID: 27322069
38. Zhong L, D’Urso A, Toiber D, Sebastian C, Henry RE, Vadysirisack DD, Guimaraes A, Marinelli B, Wikstrom JD, Nir T, Clish CB, Vaitheesvaran B, Iliopoulos O, Kurland I, Dor Y, Weissleder R, Shirihai OS, Ellisen LW, Espinosa JM, Mostoslavsky R. 2010. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140: 280–293. doi: 10.1016/j.cell.2009.12.041, PMID: 20141841
39. Zhou Y, Prakash P, Liang H, Cho KJ, Gorfe AA, Hancock JF. 2017. Lipid-Sorting specificity encoded in K-Ras membrane anchor regulates signal output. Cell 168:239–251. doi: 10.1016/j.cell.2016.11.059, PMID: 28041850
40. Zhu AY, Zhou Y, Khan S, Deitsch KW, Hao Q, Lin H. 2012. Plasmodium falciparum Sir2A preferentially hydrolyzes medium and long chain fatty acyl lysine. ACS Chemical Biology 7:155–159. doi: 10.1021/cb200230x, PMID: 21 992006