Methylglyoxal in cells elicits a negative feedback loop entailing transglutaminase 2 and glyoxalase 1

Redox Biology

Volumn 2, Issue 1, 2014, Pages 196-205

  Lee, Der Yen ^a   Chang, Geen Dong ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Glyoxalase 1; Methylglyoxal; Oxidative stress; Transglutaminase 2

Indexed keywords

LACTOYLGLUTATHIONE LYASE; METHYLGLYOXAL; POLYAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; REACTIVE OXYGEN METABOLITE; CALCIUM; GLO1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; PHENYLGLYOXAL; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

AEROBIC GLYCOLYSIS; ARTICLE; ATTENUATION; CONTROLLED STUDY; DEAMINATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DENATURATION; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME SUBSTRATE; GLYCOLYSIS; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; NEGATIVE FEEDBACK; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROCESSING; AEROBIC METABOLISM; CATALYSIS; CELL GROWTH; CONJUGATION; ENZYME REGULATION; ENZYME STABILITY; HELA CELL LINE; PROTEIN PROTEIN INTERACTION; DRUG EFFECTS; FEEDBACK SYSTEM; METABOLISM; PROTEIN STABILITY;

CALCIUM; FEEDBACK, PHYSIOLOGICAL; GTP-BINDING PROTEINS; HELA CELLS; HUMANS; LACTOYLGLUTATHIONE LYASE; PHENYLGLYOXAL; POLYAMINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; REACTIVE OXYGEN SPECIES; TRANSGLUTAMINASES;

EID: 84893160083     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.12.024     Document Type: Article

References (58)

1. Griffin M., Casadio R., Bergamini C.M. Transglutaminases: nature's biological glues. Biochem. J. 2002, 368:377-396.
2. Lorand L., Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nature reviews. Mol. Cell Biol. 2003, 4:140-156.
3. Beninati S., Piacentini M. The transglutaminase family: an overview: minireview article. Amino Acids 2004, 26:367-372.
4. Folk J.E., Park M.H., Chung S.I., Schrode J., Lester E.P., Cooper H.L. Polyamines as physiological substrates for transglutaminases. J. Biol. Chem. 1980, 255:3695-3700.
5. Molberg O., McAdam S.N., Korner R., Quarsten H., Kristiansen C., Madsen L., Fugger L., Scott H., Noren O., Roepstorff P., Lundin K.E., Sjostrom H., Sollid L.M. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat. Med. 1998, 4:713-717.
6. van de Wal Y., Kooy Y., van Veelen P., Pena S., Mearin L., Papadopoulos G., Koning F. Selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T cell reactivity. J. Immunol. 1998, 161:1585-1588.
7. Nakaoka H., Perez D.M., Baek K.J., Das T., Husain A., Misono K., Im M.J., Graham R.M. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 1994, 264:1593-1596.
8. Achyuthan K.E., Greenberg C.S. Identification of a guanosine triphosphate-binding site on guinea pig liver transglutaminase. Role of GTP and calcium ions in modulating activity. J. Biol. Chem. 1987, 262:1901-1906.
9. Hasegawa G., Suwa M., Ichikawa Y., Ohtsuka T., Kumagai S., Kikuchi M., Sato Y., Saito Y. A novel function of tissue-type transglutaminase: protein disulphide isomerase. Biochem. J. 2003, 373:793-803.
10. Mishra S., Murphy L.J. Tissue transglutaminase has intrinsic kinase activity: identification of transglutaminase 2 as an insulin-like growth factor-binding protein-3 kinase. J. Biol. Chem. 2004, 279:23863-23868.
11. Mishra S., Saleh A., Espino P.S., Davie J.R., Murphy L.J. Phosphorylation of histones by tissue transglutaminase. J. Biol. Chem. 2006, 281:5532-5538.
12. Akimov S.S., Krylov D., Fleischman L.F., Belkin A.M. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J. Cell Biol. 2000, 148:825-838.
13. Gentile V., Porta R., Chiosi E., Spina A., Valente F., Pezone R., Davies P.J., Alaadik A., Illiano G. tTGase/G alpha h protein expression inhibits adenylate cyclase activity in Balb-C 3T3 fibroblasts membranes. Biochim. Biophys. Acta 1997, 1357:115-122.
14. Kumar S., Mehta K. Tissue transglutaminase constitutively activates HIF-1alpha promoter and nuclear factor-kappaB via a non-canonical pathway. PloS one 2012, 7:e49321.
15. Tucholski J., Johnson G.V. Tissue transglutaminase directly regulates adenylyl cyclase resulting in enhanced cAMP-response element-binding protein (CREB) activation. J. Biol. Chem. 2003, 278:26838-26843.
16. Phillips S.A., Thornalley P.J. The formation of methylglyoxal from triose phosphates. Investigation using a specific assay for methylglyoxal. Eur. J. Biochem. (FEBS) 1993, 212:101-105.
17. Thornalley P.J., Battah S., Ahmed N., Karachalias N., Agalou S., Babaei-Jadidi R., Dawnay A. Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem. J. 2003, 375:581-592.
18. Abordo E.A., Minhas H.S., Thornalley P.J. Accumulation of alpha-oxoaldehydes during oxidative stress: a role in cytotoxicity. Biochem. Pharmacol. 1999, 58:641-648.
19. Thornalley P.J., Edwards L.G., Kang Y., Wyatt C., Davies N., Ladan M.J., Double J. Antitumour activity of S-p-bromobenzylglutathione cyclopentyl diester in vitro and in vivo. Inhibition of glyoxalase I and induction of apoptosis. Biochem. Pharmacol. 1996, 51:1365-1372.
20. Biswas S., Ray M., Misra S., Dutta D.P., Ray S. Selective inhibition of mitochondrial respiration and glycolysis in human leukaemic leucocytes by methylglyoxal. Biochem. J. 1997, 323(Pt 2):343-348.
21. Chang T., Wang R., Wu L. Methylglyoxal-induced nitric oxide and peroxynitrite production in vascular smooth muscle cells. Free Radic. Biol. Med. 2005, 38:286-293.
22. Rosca M.G., Mustata T.G., Kinter M.T., Ozdemir A.M., Kern T.S., Szweda L.I., Brownlee M., Monnier V.M., Weiss M.F. Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. American journal of physiology. Renal Physiol. 2005, 289:F420-F430.
23. Schlotterer A., Kukudov G., Bozorgmehr F., Hutter H., Du X., Oikonomou D., Ibrahim Y., Pfisterer F., Rabbani N., Thornalley P., Sayed A., Fleming T., Humpert P., Schwenger V., Zeier M., Hamann A., Stern D., Brownlee M., Bierhaus A., Nawroth P., Morcos M. C. elegans as model for the study of high glucose-mediated life span reduction. Diabetes 2009, 58:2450-2456.
24. Brouwers O., Niessen P.M., Ferreira I., Miyata T., Scheffer P.G., Teerlink T., Schrauwen P., Brownlee M., Stehouwer C.D., Schalkwijk C.G. Overexpression of glyoxalase-I reduces hyperglycemia-induced levels of advanced glycation end products and oxidative stress in diabetic rats. J. Biol. Chem. 2011, 286:1374-1380.
25. Lee Z.W., Kwon S.M., Kim S.W., Yi S.J., Kim Y.M., Ha K.S. Activation of in situ tissue transglutaminase by intracellular reactive oxygen species. Biochem. Biophys. Res. Commun. 2003, 305:633-640.
26. Yi S.J., Choi H.J., Yoo J.O., Yuk J.S., Jung H.I., Lee S.H., Han J.A., Kim Y.M., Ha K.S. Arachidonic acid activates tissue transglutaminase and stress fiber formation via intracellular reactive oxygen species. Biochem. Biophys. Res. Commun. 2004, 325:819-826.
27. Ridderstrom M., Mannervik B. Optimized heterologous expression of the human zinc enzyme glyoxalase I. Biochem. J. 1996, 314(Pt 2):463-467.
28. Lee D.Y., Chang G.D. Electrolytic reduction: modification of proteins occurring in isoelectric focusing electrophoresis and in electrolytic reactions in the presence of high salts. Anal. Chem. 2009, 81:3957-3964.
29. Bae N., Yang J.W., Sitte H., Pollak A., Marquez J., Lubec G. An electrophoretic approach to screen for glutamine deamidation. Anal. Biochem. 2012, 428:1-3.
30. Kellum M.W., Oray B., Norton S.J. A convenient quantitative synthesis of methylglyoxal for glyoxalase I assays. Anal. Biochem. 1978, 85:586-590.
31. Mittelmaier S., Funfrocken M., Fenn D., Berlich R., Pischetsrieder M. Quantification of the six major alpha-dicarbonyl contaminants in peritoneal dialysis fluids by UHPLC/DAD/MSMS. Anal. Bioanal. Chem. 2011, 401:1183-1193.
32. Amarzguioui M. Improved siRNA-mediated silencing in refractory adherent cell lines by detachment and transfection in suspension. BioTechniques 2004, 36(766-768):770.
33. Du Y., Wang F., May K., Xu W., Liu H. Determination of deamidation artifacts introduced by sample preparation using 18O-labeling and tandem mass spectrometry analysis. Anal. Chem. 2012, 84:6355-6360.
34. Lesort M., Lee M., Tucholski J., Johnson G.V. Cystamine inhibits caspase activity. Implications for the treatment of polyglutamine disorders. J. Biol. Chem. 2003, 278:3825-3830.
35. Ientile R., Campisi A., Raciti G., Caccamo D., Currò M., Cannavò G., Li Volti G., Macaione S., Vanella A. Cystamine inhibits transglutaminase and caspase-3 cleavage in glutamate-exposed astroglial cells. J. Neurosci. Res. 2003, 74:52-59.
36. Hao P., Ren Y., Alpert A.J., Sze S.K. Detection, evaluation and minimization of nonenzymatic deamidation in proteomic sample preparation. Mol. Cell. Proteomics: (MCP) 2011, 10(O111):009381.
37. Meinwald Y.C., Stimson E.R., Scheraga H.A. Deamidation of the asparaginyl-glycyl sequence. Int. J. Pept. Protein Res. 1986, 28:79-84.
38. Robinson N.E., Robinson A.B. Deamidation of human proteins. Proc. Natl. Acad. Sci. USA 2001, 98:12409-12413.
39. 2+ ligand in the catalytic mechanism of human glyoxalase I. J. Biol. Chem. 1998, 273:21623-21628.
40. Groenen P.J., Seccia M., Smulders R.H., Gravela E., Cheeseman K.H., Bloemendal H., de Jong W.W. Exposure of beta H-crystallin to hydroxyl radicals enhances the transglutaminase-susceptibility of its existing amine-donor and amine-acceptor sites. Biochem. J. 1993, 295(Pt 2):399-404.
41. Shin D.M., Jeon J.H., Kim C.W., Cho S.Y., Kwon J.C., Lee H.J., Choi K.H., Park S.C., Kim I.G. Cell type-specific activation of intracellular transglutaminase 2 by oxidative stress or ultraviolet irradiation: implications of transglutaminase 2 in age-related cataractogenesis. J. Biol. Chem. 2004, 279:15032-15039.
42. Caccamo D., Curro M., Ferlazzo N., Condello S., Ientile R. Monitoring of transglutaminase 2 under different oxidative stress conditions. Amino Acids 2012, 42:1037-1043.
43. Fésüs L., Szondy Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett. 2005, 579:3297-3302.
44. Antonyak M.A., Miller A.M., Jansen J.M., Boehm J.E., Balkman C.E., Wakshlag J.J., Page R.L., Cerione R.A. Augmentation of tissue transglutaminase expression and activation by epidermal growth factor inhibit doxorubicin-induced apoptosis in human breast cancer cells. J. Biol. Chem. 2004, 279:41461-41467.
45. Datta S., Antonyak M.A., Cerione R.A. Importance of Ca(2+)-dependent transamidation activity in the protection afforded by tissue transglutaminase against doxorubicin-induced apoptosis. Biochemistry 2006, 45:13163-13174.
46. Yuan L., Choi K., Khosla C., Zheng X., Higashikubo R., Chicoine M.R., Rich K.M. Tissue transglutaminase 2 inhibition promotes cell death and chemosensitivity in glioblastomas. Mol. Cancer Ther. 2005, 4:1293-1302.
47. Yamaguchi H., Wang H.G. Tissue transglutaminase serves as an inhibitor of apoptosis by cross-linking caspase 3 in thapsigargin-treated cells. Mol. Cell. Biol. 2006, 26:569-579.
48. Kim S.J., Kim K.H., Ahn E.R., Yoo B.C., Kim S.Y. Depletion of cathepsin D by transglutaminase 2 through protein cross-linking promotes cell survival. Amino Acids 2013, 44:73-80.
49. Lunt S.Y., Vander Heiden M.G. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu. Rev. Cell Dev. Biol. 2011, 27:441-464.
50. Thornalley P.J., Rabbani N. Glyoxalase in tumourigenesis and multidrug resistance. Semin. Cell Dev. Biol. 2011, 22:318-325.
51. Santarius T., Bignell G.R., Greenman C.D., Widaa S., Chen L., Mahoney C.L., Butler A., Edkins S., Waris S., Thornalley P.J., Futreal P.A., Stratton M.R. GLO1-A novel amplified gene in human cancer. Genes Chromosomes Cancer 2010, 49:711-725.
52. Young T.W., Mei F.C., Yang G., Thompson-Lanza J.A., Liu J., Cheng X. Activation of antioxidant pathways in ras-mediated oncogenic transformation of human surface ovarian epithelial cells revealed by functional proteomics and mass spectrometry. Cancer Res. 2004, 64:4577-4584.
53. Lin C.Y., Tsai P.H., Kandaswami C.C., Chang G.D., Cheng C.H., Huang C.J., Lee P.P., Hwang J.J., Lee M.T. Role of tissue transglutaminase 2 in the acquisition of a mesenchymal-like phenotype in highly invasive A431 tumor cells. Mol. Cancer 2011, 10:87.
54. Mehta K., Kumar A., Kim H.I. Transglutaminase 2: a multi-tasking protein in the complex circuitry of inflammation and cancer. Biochem. Pharmacol. 2010, 80:1921-1929.
55. Shao M., Cao L., Shen C., Satpathy M., Chelladurai B., Bigsby R.M., Nakshatri H., Matei D. Epithelial-to-mesenchymal transition and ovarian tumor progression induced by tissue transglutaminase. Cancer Res. 2009, 69:9192-9201.
56. Mehta K. High levels of transglutaminase expression in doxorubicin-resistant human breast carcinoma cells. International journal of cancer. J. Int. Cancer 1994, 58:400-406.
57. Herman J.F., Mangala L.S., Mehta K. Implications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells. Oncogene 2006, 25:3049-3058.
58. Singer C.F., Hudelist G., Walter I., Rueckliniger E., Czerwenka K., Kubista E., Huber A.V. Tissue array-based expression of transglutaminase-2 in human breast and ovarian cancer. Clin. Exp. Metastasis 2006, 23:33-39.