Blockade of enzyme activity inhibits tissue transglutaminase-mediated transamidation of α-synuclein in a cellular model of Parkinson's disease

Neurochemistry International

Volumn 58, Issue 7, 2011, Pages 785-793

  Verhaar, Robin ^a   Jongenelen, Cornelis A M ^a   Gerard, Melanie ^b   Baekelandt, Veerle ^b   Van Dam, Anne Marie ^a   Wilhelmus, Micha M M ^a   Drukarch, Benjamin ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Synuclein; Neuroblastoma; Parkinson's disease; Tissue transglutaminase

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 5 (BIOTINAMIDO)PENTYLAMINE; ALPHA SYNUCLEIN; B 003; CALCIUM ION; ENZYME INHIBITOR; KCC 009; PENTYLAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; UNCLASSIFIED DRUG; Z 006;

AMIDATION; ARTICLE; CANCER CELL; CONCENTRATION RESPONSE; DRUG EFFICACY; DRUG POTENCY; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; IC 50; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION;

ALPHA-SYNUCLEIN; AMIDES; BLOTTING, WESTERN; CELL LINE, TUMOR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GTP-BINDING PROTEINS; HUMANS; MODELS, BIOLOGICAL; PARKINSON DISEASE; TRANSGLUTAMINASES;

EID: 79955673727     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.03.004     Document Type: Article

References (61)

1. S.S. Akimov, and A.M. Belkin Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin Blood 98 2001 1567 1576
2. S.S. Akimov, D. Krylov, L.F. Fleischman, and A.M. Belkin Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin J. Cell Biol. 148 2000 825 838
3. G. Andringa, K.Y. Lam, M. Chegary, X. Wang, T.N. Chase, and M.C. Bennett Tissue transglutaminase catalyzes the formation of alpha-synuclein crosslinks in Parkinson's disease FASEB J. 18 2004 932 934
4. T. Antony, W. Hoyer, D. Cherny, G. Heim, T.M. Jovin, and V. Subramaniam Cellular polyamines promote the aggregation of alpha-synuclein J. Biol. Chem. 278 2003 3235 3240 (Pubitemid 36801235)
5. +)-induced toxicity in differentiated human SH-SY5Y neuroblastoma cells Neurosci. Lett. 405 2006 46 51 (Pubitemid 44142827)
6. H. Braak, T.K. Del, U. Rub, R.A. de Vos, E.N. Jansen Steur, and E. Braak Staging of brain pathology related to sporadic Parkinson's disease Neurobiol. Aging 24 2003 197 211 (Pubitemid 36007810)
7. J.J. Breve, B. Drukarch, M. van Strien, and A.M. van Dam Validated sandwich ELISA for the quantification of tissue transglutaminase in tissue homogenates and cell lysates of multiple species J. Immunol. Methods 332 2008 142 150
8. R.S. Burns, C.C. Chiueh, S.P. Markey, M.H. Ebert, D.M. Jacobowitz, and I.J. Kopin A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Proc. Natl. Acad. Sci. U.S.A. 80 1983 4546 4550 (Pubitemid 13077876)
9. S. Chandra, G. Gallardo, R. Fernandez-Chacon, O.M. Schluter, and T.C. Sudhof Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration Cell 123 2005 383 396 (Pubitemid 41546670)
10. M.C. Chartier-Harlin, J. Kachergus, C. Roumier, V. Mouroux, X. Douay, S. Lincoln, C. Levecque, L. Larvor, J. Andrieux, M. Hulihan, N. Waucquier, L. Defebvre, P. Amouyel, M. Farrer, and A. Destee Alpha-synuclein locus duplication as a cause of familial Parkinson's disease Lancet 364 2004 1167 1169 (Pubitemid 39296604)
11. K. Choi, M. Siegel, J.L. Piper, L. Yuan, E. Cho, P. Strnad, B. Omary, K.M. Rich, and C. Khosla Chemistry and biology of dihydroisoxazole derivatives: selective inhibitors of human transglutaminase 2 Chem. Biol. 12 2005 469 475 (Pubitemid 40588922)
12. K.A. Conway, J.D. Harper, and P.T. Lansbury Jr. Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid Biochemistry 39 2000 2552 2563 (Pubitemid 30148907)
13. B. Drukarch, C.A. Jongenelen, E. Schepens, C.H. Langeveld, and J.C. Stoof Glutathione is involved in the granular storage of dopamine in rat PC 12 pheochromocytoma cells: implications for the pathogenesis of Parkinson's disease J. Neurosci. 16 1996 6038 6045 (Pubitemid 26313979)
14. D. Eliezer, E. Kutluay, R. Bussell Jr., and G. Browne Conformational properties of alpha-synuclein in its free and lipid-associated states J. Mol. Biol. 307 2001 1061 1073 (Pubitemid 33029953)
15. L. Fesus, A. Falus, A. Erdei, and K. Laki Human beta 2-microglobulin is a substrate of tissue transglutaminase: polymerization in solution and on the cell surface J. Cell Biol. 89 1981 706 710 (Pubitemid 11035981)
16. J.E. Galvin, V.M. Lee, and J.Q. Trojanowski Synucleinopathies: clinical and pathological implications Arch. Neurol. 58 2001 186 190 (Pubitemid 32163154)
17. M. Gerard, A. Deleersnijder, V. Daniels, S. Schreurs, S. Munck, V. Reumers, H. Pottel, Y. Engelborghs, H.C. Van den, J.M. Taymans, Z. Debyser, and V. Baekelandt Inhibition of FK506 binding proteins reduces alpha-synuclein aggregation and Parkinson's disease-like pathology J. Neurosci. 30 2010 2454 2463
18. A.D. Gitler, B.J. Bevis, J. Shorter, K.E. Strathearn, S. Hamamichi, L.J. Su, K.A. Caldwell, G.A. Caldwell, J.C. Rochet, J.M. McCaffery, C. Barlowe, and S. Lindquist The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis Proc. Natl. Acad. Sci. U.S.A. 105 2008 145 150
19. M. Griffin, R. Casadio, and C.M. Bergamini Transglutaminases: nature's biological glues Biochem. J. 368 2002 377 396 (Pubitemid 35454517)
20. M. Griffin, A. Mongeot, R. Collighan, R.E. Saint, R.A. Jones, I.G. Coutts, and D.L. Rathbone Synthesis of potent water-soluble tissue transglutaminase inhibitors Bioorg. Med. Chem. Lett. 18 2008 5559 5562
21. F. Hausch, T. Halttunen, M. Maki, and C. Khosla Design, synthesis, and evaluation of gluten peptide analogs as selective inhibitors of human tissue transglutaminase Chem. Biol. 10 2003 225 231 (Pubitemid 36380279)
22. R.E. Heikkila, A. Hess, and R.C. Duvoisin Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice Science 224 1984 1451 1453 (Pubitemid 14123348)
23. P. Ibanez, A.M. Bonnet, B. Debarges, E. Lohmann, F. Tison, P. Pollak, Y. Agid, A. Durr, and A. Brice Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease Lancet 364 2004 1169 1171 (Pubitemid 39296605)
24. T.M. Jeitner, H.L. Fuchsbauer, J.P. Blass, and A.J. Cooper A sensitive fluorometric assay for tissue transglutaminase Anal. Biochem. 292 2001 198 206 (Pubitemid 32458085)
25. G.V. Johnson, T.M. Cox, J.P. Lockhart, M.D. Zinnerman, M.L. Miller, and R.E. Powers Transglutaminase activity is increased in Alzheimer's disease brain Brain Res. 751 1997 323 329 (Pubitemid 27132565)
26. E. Junn, R.D. Ronchetti, M.M. Quezado, S.Y. Kim, and M.M. Mouradian Tissue transglutaminase-induced aggregation of alpha-synuclein: implications for Lewy body formation in Parkinson's disease and dementia with Lewy bodies Proc. Natl. Acad. Sci. U.S.A. 100 2003 2047 2052 (Pubitemid 36254571)
27. M.V. Karpuj, H. Garren, H. Slunt, D.L. Price, J. Gusella, M.W. Becher, and L. Steinman Transglutaminase aggregates huntingtin into nonamyloidogenic polymers, and its enzymatic activity increases in Huntington's disease brain nuclei Proc. Natl. Acad. Sci. U.S.A. 96 1999 7388 7393 (Pubitemid 29299671)
28. T. Konno, T. Morii, A. Hirata, S. Sato, S. Oiki, and K. Ikura Covalent blocking of fibril formation and aggregation of intracellular amyloidgenic proteins by transglutaminase-catalyzed intramolecular cross-linking Biochemistry 44 2005 2072 2079 (Pubitemid 40223634)
29. R. Kruger, W. Kuhn, T. Muller, D. Woitalla, M. Graeber, S. Kosel, H. Przuntek, J.T. Epplen, L. Schols, and O. Riess Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat. Genet. 18 1998 106 108
30. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
31. K.E. Larsen, Y. Schmitz, M.D. Troyer, E. Mosharov, P. Dietrich, A.Z. Quazi, M. Savalle, V. Nemani, F.A. Chaudhry, R.H. Edwards, L. Stefanis, and D. Sulzer Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis J. Neurosci. 26 2006 11915 11922 (Pubitemid 44772102)
32. H.A. Lashuel, B.M. Petre, J. Wall, M. Simon, R.J. Nowak, T. Walz, and P.T. Lansbury Jr. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils J. Mol. Biol. 322 2002 1089 1102 (Pubitemid 35266514)
33. M. Lesort, W. Chun, G.V. Johnson, and R.J. Ferrante Tissue transglutaminase is increased in Huntington's disease brain J. Neurochem. 73 1999 2018 2027 (Pubitemid 29491816)
34. M. Lesort, M. Lee, J. Tucholski, and G.V. Johnson Cystamine inhibits caspase activity. Implications for the treatment of polyglutamine disorders J. Biol. Chem. 278 2003 3825 3830 (Pubitemid 36801110)
35. L. Lorand, and R.M. Graham Transglutaminases: crosslinking enzymes with pleiotropic functions Nat. Rev. Mol. Cell Biol. 4 2003 140 156 (Pubitemid 36172696)
36. A. Madi, L. Karpati, A. Kovacs, L. Muszbek, and L. Fesus High-throughput scintillation proximity assay for transglutaminase activity measurement Anal. Biochem. 343 2005 256 262 (Pubitemid 41074038)
37. S.J. McConoughey, M. Basso, Z.V. Niatsetskaya, S.F. Sleiman, N.A. Smirnova, B.C. Langley, L. Mahishi, A.J. Cooper, M.A. Antonyak, R.A. Cerione, B. Li, A. Starkov, R.K. Chaturvedi, M.F. Beal, G. Coppola, D.H. Geschwind, H. Ryu, L. Xia, S.E. Iismaa, J. Pallos, R. Pasternack, M. Hils, J. Fan, L.A. Raymond, J.L. Marsh, L.M. Thompson, and R.R. Ratan Inhibition of transglutaminase 2 mitigates transcriptional dysregulation in models of Huntington disease EMBO Mol. Med. 9 2010 335 337
38. Z. Nemes, G. Petrovski, M. Aerts, K. Sergeant, B. Devreese, and L. Fesus Transglutaminase-mediated intramolecular cross-linking of membrane-bound alpha-synuclein promotes amyloid formation in Lewy bodies J. Biol. Chem. 284 2009 27252 27264
39. S. Pahlman, A.I. Ruusala, L. Abrahamsson, M.E. Mattsson, and T. Esscher Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation Cell Differ. 14 1984 135 144 (Pubitemid 14089031)
40. M.H. Polymeropoulos, C. Lavedan, E. Leroy, S.E. Ide, A. Dehejia, A. Dutra, B. Pike, H. Root, J. Rubenstein, R. Boyer, E.S. Stenroos, S. Chandrasekharappa, A. Athanassiadou, T. Papapetropoulos, W.G. Johnson, A.M. Lazzarini, R.C. Duvoisin, I.G. Di, L.I. Golbe, and R.L. Nussbaum Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 1997 2045 2047 (Pubitemid 27443610)
41. S. Schaertl, M. Prime, J. Wityak, C. Dominquez, I. Munoz-Sanjuan, R.E. Pacifici, S. Courtney, A. Scheel, and D. Macdonald A profiling platform for the characterization of transglutaminase 2 (TG2) inhibitors J. Biomol. Screen. 15 5 2010 478 487
42. A.W. Schmid, D. Chiappe, V. Pignat, V. Grimminger, I. Hang, M. Moniatte, and H.A. Lashuel Dissecting the mechanisms of tissue transglutaminase-induced cross-linking of alpha-synuclein: implications for the pathogenesis of Parkinson disease J. Biol. Chem. 284 2009 13128 13142
43. B. Schule, R.A. Pera, and J.W. Langston Can cellular models revolutionize drug discovery in Parkinson's disease? Biochim. Biophys. Acta 1792 2009 1043 1051
44. I.M. Segers-Nolten, M.M. Wilhelmus, G. Veldhuis, B.D. van Rooijen, B. Drukarch, and V. Subramaniam Tissue transglutaminase modulates alpha-synuclein oligomerization Protein Sci. 17 2008 1395 1402
45. M. Siegel, and C. Khosla Transglutaminase 2 inhibitors and their therapeutic role in disease states Pharmacol. Ther. 115 2007 232 245 (Pubitemid 47042912)
46. M. Siegel, P. Strnad, R.E. Watts, K. Choi, B. Jabri, M.B. Omary, and C. Khosla Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury PLoS ONE 3 2008 e1861
47. S.M. Singer, G.M. Zainelli, M.A. Norlund, J.M. Lee, and N.A. Muma Transglutaminase bonds in neurofibrillary tangles and paired helical filament tau early in Alzheimer's disease Neurochem. Int. 40 2002 17 30 (Pubitemid 34003555)
48. U.S. Singh, J. Pan, Y.L. Kao, S. Joshi, K.L. Young, and K.M. Baker Tissue transglutaminase mediates activation of RhoA and MAP kinase pathways during retinoic acid-induced neuronal differentiation of SH-SY5Y cells J. Biol. Chem. 278 2003 391 399 (Pubitemid 36043588)
49. M.G. Spillantini, M.L. Schmidt, V.M. Lee, J.Q. Trojanowski, R. Jakes, and M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
50. P. Strnad, M. Siegel, D.M. Toivola, K. Choi, J.C. Kosek, C. Khosla, and M.B. Omary Pharmacologic transglutaminase inhibition attenuates drug-primed liver hypertrophy but not Mallory body formation FEBS Lett. 580 2006 2351 2357
51. M.D. Suh, C.H. Park, S.S. Kim, M.O. Kil, G.H. Lee, G.V. Johnson, and W. Chun Tissue transglutaminase is not involved in the aggregate formation of stably expressed alpha-synuclein in SH-SY5Y human neuroblastoma cells Arch. Pharm. Res. 27 2004 850 856 (Pubitemid 43073706)
52. T.S. Ulmer, A. Bax, N.B. Cole, and R.L. Nussbaum Structure and dynamics of micelle-bound human alpha-synuclein J. Biol. Chem. 280 2005 9595 9603 (Pubitemid 40409655)
53. V.N. Uversky Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation J. Neurochem. 103 2007 17 37 (Pubitemid 47407730)
54. I. Vermes, E.N. Steur, G.F. Jirikowski, and C. Haanen Elevated concentration of cerebrospinal fluid tissue transglutaminase in Parkinson's disease indicating apoptosis Mov. Disord. 19 2004 1252 1254 (Pubitemid 39429976)
55. R.E. Watts, M. Siegel, and C. Khosla Structure-activity relationship analysis of the selective inhibition of transglutaminase 2 by dihydroisoxazoles J. Med. Chem. 49 2006 7493 7501 (Pubitemid 44913408)
56. P.H. Weinreb, W. Zhen, A.W. Poon, K.A. Conway, and P.T. Lansbury Jr. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded Biochemistry 35 1996 13709 13715 (Pubitemid 26363912)
57. M.M. Wilhelmus, A.M. van Dam, and B. Drukarch Tissue transglutaminase: a novel pharmacological target in preventing toxic protein aggregation in neurodegenerative diseases Eur. J. Pharmacol. 585 2008 464 472
58. L. Yuan, K. Choi, C. Khosla, X. Zheng, R. Higashikubo, M.R. Chicoine, and K.M. Rich Tissue transglutaminase 2 inhibition promotes cell death and chemosensitivity in glioblastomas Mol. Cancer Ther. 4 2005 1293 1302
59. J.J. Zarranz, J. Alegre, J.C. Gomez-Esteban, E. Lezcano, R. Ros, I. Ampuero, L. Vidal, J. Hoenicka, O. Rodriguez, B. Atares, V. Llorens, T.E. Gomez, S.T. del, D.G. Munoz, and J.G. de Yebenes The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia Ann. Neurol. 55 2004 164 173 (Pubitemid 38166992)
60. K. Zatloukal, L. Fesus, H. Denk, E. Tarcsa, G. Spurej, and G. Bock High amount of epsilon-(gamma-glutamyl)lysine cross-links in Mallory bodies Lab Invest 66 1992 774 777
61. J. Zhang, M. Lesort, R.P. Guttmann, and G.V. Johnson Modulation of the in situ activity of tissue transglutaminase by calcium and GTP J. Biol. Chem. 273 1998 2288 2295 (Pubitemid 28069282)