Modification of RelA by O-linked N-acetylglucosamine links glucose metabolism to NF-κB acetylation and transcription

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 42, 2012, Pages 16888-16893

  Allison, David F ^a   Wamsley, J Jacob ^a   Kumar, Manish ^a   Li, Duo ^a   Gray, Lisa G ^a   Hart, Gerald W ^b   Jones, David R ^a   Mayo, Marty W ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; NF kappa B; p65

Indexed keywords

BCL2 RELATED PROTEIN A1; E1A ASSOCIATED P300 PROTEIN; ETOPOSIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; N ACETYLGLUCOSAMINE; O LINKED N ACETYLGLUCOSAMINE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BIOSYNTHESIS; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME LOCALIZATION; GENE EXPRESSION; GLUCOSE METABOLISM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN PROCESSING; UPREGULATION;

ACETYLATION; ACETYLGLUCOSAMINE; CHROMATIN IMMUNOPRECIPITATION; DNA, COMPLEMENTARY; ENZYME-LINKED IMMUNOSORBENT ASSAY; ETOPOSIDE; GENE EXPRESSION REGULATION; GLUCOSE; HEK293 CELLS; HEXOSAMINES; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LUCIFERASES; METABOLIC NETWORKS AND PATHWAYS; NF-KAPPA B; PLASMIDS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84867650919     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1208468109     Document Type: Article

References (48)

1. Dennis JW, Nabi IR, Demetriou M (2009) Metabolism, cell surface organization, and disease. Cell 139:1229-1241.
2. Wellen KE, et al. (2010) The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism. Genes Dev 24:2784-2799.
3. Hanover JA, Krause MW, Love DC (2010) The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim Biophys Acta 1800:80-95.
4. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O (2011) Cross talk between O-GlcNAcylation and phosphorylation: Roles in signaling, transcription, and chronic disease. Annu Rev Biochem 80:825-858.
5. Shafi R, et al. (2000) The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc Natl Acad Sci USA 97:5735-5739. (Pubitemid 30367467)
6. Yang YR, et al. (2012) O-GlcNAcase is essential for embryonic development and maintenance of genomic stability. Aging Cell 11:439-448.
7. Hanover JA, Krause MW, Love DC (2012) Bittersweet memories: Linking metabolism to epigenetics through O-GlcNAcylation. Nat Rev Mol Cell Biol 13:312-321.
8. Love DC, Krause MW, Hanover JA (2010) O-GlcNAc cycling: Emerging roles in development and epigenetics. Semin Cell Dev Biol 21:646-654.
9. Schwartz YB, Pirrotta V (2009) A little bit of sugar makes polycomb better. J Mol Cell Biol 1:11-12.
10. Slawson C, Hart GW (2011) O-GlcNAc signalling: Implications for cancer cell biology. Nat Rev Cancer 11:678-684.
11. Golks A, Tran TT, Goetschy JF, Guerini D (2007) Requirement for O-linked N-acetylglucosaminyltransferase in lymphocytes activation. EMBO J 26:4368-4379. (Pubitemid 47587656)
12. Kawauchi K, Araki K, Tobiume K, Tanaka N (2009) Loss of p53 enhances catalytic activity of IKKbeta through O-linked beta-N-acetyl glucosamine modification. Proc Natl Acad Sci USA 106:3431-3436.
13. Ozcan S, Andrali SS, Cantrell JE (2010) Modulation of transcription factor function by O-GlcNAc modification. Biochim Biophys Acta 1799:353-364.
14. Xing D, et al. (2011) O-GlcNAc modification of NFκB p65 inhibits TNF-α-induced inflammatorymediator expression in rat aortic smooth muscle cells. PLoS ONE 6: e24021.
15. Yang WH, et al. (2008) NFkappaB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions. Proc Natl Acad Sci USA 105:17345-17350.
16. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362.
17. Siebel AL, Fernandez AZ, El-Osta A (2010) Glycemic memory associated epigenetic changes. Biochem Pharmacol 80:1853-1859.
18. Lee SK, Kim JH, Lee YC, Cheong J, Lee JW (2000) Silencing mediator of retinoic acid and thyroid hormone receptors, as a novel transcriptional corepressor molecule of activating protein-1, nuclear factor-kappaB, and serum response factor. J Biol Chem 275:12470-12474. (Pubitemid 30241389)
19. Baek SH, et al. (2002) Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110: 55-67. (Pubitemid 34874606)
20. Zhong H, May MJ, Jimi E, Ghosh S (2002) The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 9:625-636. (Pubitemid 34273792)
21. Hoberg JE, Yeung F, Mayo MW (2004) SMRT derepression by the IkappaB kinase alpha: A prerequisite to NF-kappaB transcription and survival. Mol Cell 16:245-255. (Pubitemid 39388839)
22. Ashburner BP, Westerheide SD, Baldwin AS, Jr. (2001) The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol 21:7065-7077. (Pubitemid 32916079)
23. Hoberg JE, Popko AE, Ramsey CS, Mayo MW (2006) IkappaB kinase alpha-mediated derepression of SMRT potentiates acetylation of RelA/p65 by p300. Mol Cell Biol 26: 457-471. (Pubitemid 43090920)
24. Kawahara TL, et al. (2009) SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136:62-74.
25. Yeung F, et al. (2004) Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23:2369-2380. (Pubitemid 38954844)
26. Gerritsen ME, et al. (1997) CREB-binding protein/p300 are transcriptional coactivators of p65. Proc Natl Acad Sci USA 94:2927-2932. (Pubitemid 27157241)
27. Sheppard KA, et al. (1998) Nuclear integration of glucocorticoid receptor and nuclear factor-kappaB signaling by CREB-binding protein and steroid receptor coactivator-1. J Biol Chem 273:29291-29294.
28. Paal K, Baeuerle PA, Schmitz ML (1997) Basal transcription factors TBP and TFIIB and the viral coactivator E1A 13S bind with distinct affinities and kinetics to the transactivation domain of NF-kappaB p65. Nucleic Acids Res 25:1050-1055. (Pubitemid 27298276)
29. Schmitz ML, Stelzer G, Altmann H, Meisterernst M, Baeuerle PA (1995) Interaction of the COOH-terminal transactivation domain of p65 NF-kappa B with TATA-binding protein, transcription factor IIB, and coactivators. J Biol Chem 270:7219-7226.
30. Buerki C, et al. (2008) Functional relevance of novel p300-mediated lysine 314 and 315 acetylation of RelA/p65. Nucleic Acids Res 36:1665-1680. (Pubitemid 351426117)
31. Chen LF, Mu Y, Greene WC (2002) Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 21:6539-6548. (Pubitemid 35448431)
32. Rothgiesser KM, Fey M, Hottiger MO (2010) Acetylation of p65 at lysine 314 is important for late NF-kappaB-dependent gene expression. BMC Genomics 11:22.
33. Huxford T, Huang DB, Malek S, Ghosh G (1998) The crystal structure of the IkappaBalpha/NF-kappaB complex reveals mechanisms of NF-kappaB inactivation. Cell 95: 759-770. (Pubitemid 29014456)
34. Zhong H, Voll RE, Ghosh S (1998) Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1:661-671. (Pubitemid 128379244)
35. Bergqvist S, et al. (2006) Thermodynamics reveal that helix four in the NLS of NF-kappaB p65 anchors IkappaBalpha, forming a very stable complex. J Mol Biol 360: 421-434. (Pubitemid 43927832)
36. Jacobs MD, Harrison SC (1998) Structure of an IkappaBalpha/NF-kappaB complex. Cell 95:749-758.
37. Beg AA, Baltimore D (1996) An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274:782-784. (Pubitemid 26398258)
38. Wang CY, Mayo MW, Baldwin AS, Jr. (1996) TNF- and cancer therapy-induced apoptosis: Potentiation by inhibition of NF-kappaB. Science 274:784-787. (Pubitemid 26398259)
39. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM (1996) Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274:787-789.
40. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS, Jr. (1998) NF-kappaB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680-1683.
41. Wang CY, Guttridge DC, Mayo MW, Baldwin AS, Jr. (1999) NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol Cell Biol 19:5923-5929. (Pubitemid 29399297)
42. Levy D, et al. (2011) Lysine methylation of the NF-κB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-κB signaling. Nat Immunol 12:29-36.
43. Liu X, et al. (2008) The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451:846-850. (Pubitemid 351253165)
44. Dey A, et al. (2012) Loss of the tumor suppressor BAP1 causes myeloid transformation. Science 337:1541-1546.
45. Ruan HB, et al. (2012) O-GlcNAc Transferase/Host cell factor C1 complex regulates gluconeogenesis by modulating PGC-1alpha stability. Cell Metab 16:226-237.
46. Wysocka J, Myers MP, Laherty CD, Eisenman RN, Herr W (2003) Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev 17:896-911. (Pubitemid 36397377)
47. Fujiki R, et al. (2009) GlcNAcylation of a histone methyltransferase in retinoic-acid-induced granulopoiesis. Nature 459:455-459.
48. Ramsey CS, et al. (2008) Copine-I represses NF-kappaB transcription by endoproteolysis of p65. Oncogene 27:3516-3526. (Pubitemid 351793807)