Methylglyoxal suppresses TNF-α-induced NF-κB activation by inhibiting NF-κB DNA-binding

Biochemical Pharmacology

Volumn 74, Issue 4, 2007, Pages 579-589

  Laga, Mathias ^a,b   Cottyn, Anneleen ^a,b   Van Herreweghe, Franky ^a,b   Berghe, Wim Vanden ^b   Haegeman, Guy ^b   Van Oostveldt, Patrick ^b   Vandekerckhove, Joël ^a,b   Vancompernolle, Katia ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Cell death; Methylglyoxal; Necrosis; NF B; Tumor necrosis factor

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CYSTEINE; DNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYLGLYOXAL; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BINDING AFFINITY; CELL DEATH; CELL STRAIN L 929; CONTROLLED STUDY; DEGENERATIVE DISEASE; DIABETES MELLITUS; GENE EXPRESSION; GENE OVEREXPRESSION; GLYCOLYSIS; HUMAN; HUMAN CELL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; REPORTER GENE;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CELL NUCLEUS; CYSTEINE; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; L CELLS (CELL LINE); LUCIFERASES; MICE; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; PROTEIN BINDING; PYRUVALDEHYDE; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA; UMBILICAL VEINS;

EID: 34447252547     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2007.05.026     Document Type: Article

References (62)

1. Ray S., and Ray M. Isolation of methylglyoxal synthase from goat liver. J Biol Chem 256 (1981) 6230-6233
2. Kalapos M.P. On the promine/retine theory of cell division: now and then. Biochim Biophys Acta 1426 (1999) 1-16
3. Thornalley P.J., Edwards L.G., Kang Y., Wyatt C., Davies N., Ladan M.J., et al. Antitumour activity of S-p-bromobenzylglutathione cyclopentyl diester in vitro and in vivo. Inhibition of glyoxalase I and induction of apoptosis. Biochem Pharmacol 51 (1996) 1365-1372
4. Vince R., and Wadd W.B. Glyoxalase inhibitors as potential anticancer agents. Biochem Biophys Res Commun 34 (1969) 593-598
5. Chen F., Wollmer M.A., Hoerndli F., Munch G., Kuhla B., Rogaev E.I., et al. Role for glyoxalase I in Alzheimer's disease. Proc Natl Acad Sci USA 101 (2004) 7687-7692
6. Ranganathan S., Walsh E.S., Godwin A.K., and Tew K.D. Cloning and characterization of human colon glyoxalase-I. J Biol Chem 268 (1993) 5661-5667
7. Rulli A., Carli L., Romani R., Baroni T., Giovannini E., Rosi G., et al. Expression of glyoxalase I and II in normal and breast cancer tissues. Breast Cancer Res Treat 66 (2001) 67-72
8. Davidson S.D., Cherry J.P., Choudhury M.S., Tazaki H., Mallouh C., and Konno S. Glyoxalase I activity in human prostate cancer: a potential marker and importance in chemotherapy. J Urol 161 (1999) 690-691
9. Jones M.B., Krutzsch H., Shu H., Zhao Y., Liotta L.A., Kohn E.C., et al. Proteomic analysis and identification of new biomarkers and therapeutic targets for invasive ovarian cancer. Proteomics 2 (2002) 76-84
10. Zhang D.H., Tai L.K., Wong L.L., Chiu L.L., Sethi S.K., and Koay E.S. Proteomics study reveals that proteins involved in metabolic and detoxification pathways are highly expressed in HER-2/neu positive breast cancer. Mol Cell Proteomics (2005)
11. Sakamoto H., Mashima T., Kizaki A., Dan S., Hashimoto Y., Naito M., et al. Glyoxalase I is involved in resistance of human leukemia cells to antitumor agent-induced apoptosis. Blood 95 (2000) 3214-3218
12. Van Herreweghe F., Mao J., Chaplen F.W., Grooten J., Gevaert K., Vandekerckhove J., et al. 2000 Tumor necrosis factor-induced modulation of glyoxalase I activities through phosphorylation by PKA results in cell death and is accompanied by the formation of a specific methylglyoxal-derived AGE. Proc Natl Acad Sci USA 99 (2002) 949-954
13. Godbout J.P., Pesavento J., Hartman M.E., Manson S.R., and Freund G.G. 2002 Methylglyoxal enhances cisplatin-induced cytotoxicity by activating protein kinase Cdelta. J Biol Chem 277 (2002) 2554-2561
14. Shinohara M., Thornalley P.J., Giardino I., Beisswenger P., Thorpe S.R., Onorato J., et al. Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J Clin Invest 101 (1998) 1142-1147
15. van Heijst J.W., Niessen H.W., Musters R.J., van Hinsbergh V.W., Hoekman K., and Schalkwijk C.G. Argpyrimidine-modified Heat shock protein 27 in human non-small cell lung cancer: a possible mechanism for evasion of apoptosis. Cancer Lett 241 (2006) 309-319
16. Tracey K.J., and Cerami A. Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annu Rev Med 45 (1994) 491-503
17. Balkwill F., and Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 357 (2001) 539-545
18. Wajant H., Pfizenmaier K., and Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 10 (2003) 45-65
19. Chen G., and Goeddel D.V. TNF-R1 signaling: a beautiful pathway. Science 296 (2002) 1634-1635
20. Beg A.A., and Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274 (1996) 782-784
21. Wang C.Y., Mayo M.W., and Baldwin Jr. A.S. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274 (1996) 784-787
22. Tergaonkar V., Bottero V., Ikawa M., Li Q., and Verma I.M. IkappaB kinase-independent IkappaBalpha degradation pathway: functional NF-kappaB activity and implications for cancer therapy. Mol Cell Biol 23 (2003) 8070-8083
23. Vancompernolle K., Boonefaes T., Mann M., Fiers W., and Grooten J. Tumor necrosis factor-induced microtubule stabilization mediated by hyperphosphorylated oncoprotein 18 promotes cell death [In Process Citation]. J Biol Chem 275 (2000) 33876-33882
24. Plaisance S., Vanden Berghe W., Boone E., Fiers W., and Haegeman G. Recombination signal sequence binding protein Jkappa is constitutively bound to the NF-kappaB site of the interleukin-6 promoter and acts as a negative regulatory factor. Mol Cell Biol 17 (1997) 3733-3743
25. Nasuhara Y., Adcock I.M., Catley M., Barnes P.J., and Newton R. Differential IkappaB kinase activation and IkappaBalpha degradation by interleukin-1beta and tumor necrosis factor-alpha in human U937 monocytic cells. Evidence for additional regulatory steps in kappaB-dependent transcription. J Biol Chem 274 (1999) 19965-19972
26. Vanden Berghe W., Plaisance S., Boone E., De Bosscher K., Schmitz M.L., Fiers W., et al. p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-kappaB p65 transactivation mediated by tumor necrosis factor. J Biol Chem 273 (1998) 3285-3290
27. Lin A., and Karin M. NF-kappaB in cancer: a marked target. Semin Cancer Biol 13 (2003) 107-114
28. Baeuerle P.A., and Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12 (1994) 141-179
29. Siebenlist U., Franzoso G., and Brown K. Structure, regulation and function of NF-kappa B. Annu Rev Cell Biol 10 (1994) 405-455
30. Lo T.W., Westwood M.E., McLellan A.C., Selwood T., and Thornalley P.J. Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N alpha- acetylarginine, N alpha-acetylcysteine, and N alpha-acetyllysine, and bovine serum albumin. J Biol Chem 269 (1994) 32299-32305
31. Peng H.B., Libby P., and Liao J.K. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J Biol Chem 270 (1995) 14214-14219
32. Arenzana-Seisdedos F., Thompson J., Rodriguez M.S., Bachelerie F., Thomas D., and Hay R.T. Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNA-binding and transcriptional activities of NF-kappa B. Mol Cell Biol 15 (1995) 2689-2696
33. Mahon T.M., and O'Neill L.A. Evidence for direct modification of NF kappa B by the tyrosine kinase inhibitor, herbimycin A. Biochem Soc Trans 23 (1995) 111S
34. Natarajan K., Singh S., Burke Jr. T.R., Grunberger D., and Aggarwal B.B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci USA 93 (1996) 9090-9095
35. Viatour P., Merville M.P., Bours V., and Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30 (2005) 43-52
36. Vermeulen L., De Wilde G., Van Damme P., Vanden Berghe W., and Haegeman G. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 22 (2003) 1313-1324
37. Ghosh S., Gifford A.M., Riviere L.R., Tempst P., Nolan G.P., and Baltimore D. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell 62 (1990) 1019-1029
38. Liang M.C., Bardhan S., Pace E.A., Rosman D., Beutler J.A., Porco Jr. J.A., et al. Inhibition of transcription factor NF-kappaB signaling proteins IKKbeta and p65 through specific cysteine residues by epoxyquinone A monomer: correlation with its anti-cancer cell growth activity. Biochem Pharmacol 71 (2006) 634-645
39. Garcia-Pineres A.J., Castro V., Mora G., Schmidt T.J., Strunck E., Pahl H.L., et al. Cysteine 38 in p65/NF-kappaB plays a crucial role in DNA binding inhibition by sesquiterpene lactones. J Biol Chem 276 (2001) 39713-39720
40. Matthews J.R., Kaszubska W., Turcatti G., Wells T.N., and Hay R.T. Role of cysteine62 in DNA recognition by the P50 subunit of NF-kappa B. Nucleic Acids Res 21 (1993) 1727-1734
41. Ghosh G., van Duyne G., Ghosh S., and Sigler P.B. Structure of NF-kappa B p50 homodimer bound to a kappa B site. Nature 373 (1995) 303-310
42. Muller C.W., Rey F.A., Sodeoka M., Verdine G.L., and Harrison S.C. Structure of the NF-kappaB p50 homodimer bound to DNA. Nature 373 (1995) 311-317
43. Maeta K., Izawa S., Okazaki S., Kuge S., and Inoue Y. Activity of the Yap1 transcription factor in Saccharomyces cerevisiae is modulated by methylglyoxal, a metabolite derived from glycolysis. Mol Cell Biol 24 (2004) 8753-8764
44. Schmitz M.L., and Baeuerle P.A. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J 10 (1991) 3805-3817
45. Lleonart R., Naf D., Browning H., Weissmann C., and novel A. quantitative bioassay for type I interferon using a recombinant indicator cell line. Biotechnology (NY) 8 (1990) 1263-1267
46. Grooten J., Goossens V., Vanhaesebroeck B., and Fiers W. Cell membrane permeabilization and cellular collapse, followed by loss of dehydrogenase activity: early events in tumour necrosis factor- induced cytotoxicity. Cytokine 5 (1993) 546-555
47. Liu Z.G., Hsu H., Goeddel D.V., and Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87 (1996) 565-576
48. Van Antwerp D.J., Martin S.J., Kafri T., Green D.R., and Verma I.M. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274 (1996) 787-789
49. Reynaert N.L., Ckless K., Korn S.H., Vos N., Guala A.S., Wouters E.F., et al. Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc Natl Acad Sci USA 101 (2004) 8945-8950
50. Matthews J.R., and Hay R.T. Regulation of the DNA binding activity of NF-kappa B. Int J Biochem Cell Biol 27 (1995) 865-879
51. Matthews J.R., Botting C.H., Panico M., Morris H.R., and Hay R.T. Inhibition of NF-kappaB DNA binding by nitric oxide. Nucleic Acids Res 24 (1996) 2236-2242
52. Matthews J.R., Wakasugi N., Virelizier J.L., Yodoi J., and Hay R.T. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 20 (1992) 3821-3830
53. Sandur S.K., Ichikawa H., Sethi G., Ahn K.S., and Aggarwal B.B. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and IkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J Biol Chem 281 (2006) 17023-17033
54. Zuin A., Vivancos A.P., Sanso M., Takatsume Y., Ayte J., Inoue Y., et al. The glycolytic metabolite methylglyoxal activates Pap1 and Sty1 stress responses in Schizosaccharomyces pombe. J Biol Chem 280 (2005) 36708-36713
55. Abate C., Patel L., Rauscher III F.J., and Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science 249 (1990) 1157-1161
56. Yao D., Taguchi T., Matsumura T., Pestell R., Edelstein D., Giardino I., et al. Methylglyoxal Modification of mSin3A Links Glycolysis to Angiopoietin-2 Transcription. Cell (2006)
57. Ranganathan S., Ciaccio P.J., Walsh E.S., and Tew K.D. Genomic sequence of human glyoxalase-I: analysis of promoter activity and its regulation. Gene 240 (1999) 149-155
58. Chaplen F.W., Fahl W.E., and Cameron D.C. Evidence of high levels of methylglyoxal in cultured Chinese hamster ovary cells. Proc Natl Acad Sci USA 95 (1998) 5533-5538
59. Lapolla A., Flamini R., Dalla V.A., Senesi A., Reitano R., Fedele D., et al. Glyoxal and methylglyoxal levels in diabetic patients: quantitative determination by a new GC/MS method. Clin Chem Lab Med 41 (2003) 1166-1173
60. Greten F.R., and Karin M. The IKK/NF-kappaB activation pathway-a target for prevention and treatment of cancer. Cancer Lett 206 (2004) 193-199
61. Karin M., and Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5 (2005) 749-759
62. Baldwin A.S. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J Clin Invest 107 (2001) 241-246