Structural characterization of transglutaminase-catalyzed cross-linking between glyceraldehyde 3-phosphate dehydrogenase and polyglutamine repeats

Protein Science

Volumn 12, Issue 1, 2003, Pages 170-179

  Ruoppolo, Margherita ^a,b   Orrù, Stefania ^a   Francese, Simona ^a   Caputo, Ivana ^b   Esposito, Carla ^a  

^a UNIVERSITY OF SALERNO   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Glyceraldehyde 3 phosphate dehydrogenase; Lysine residues; Mass spectrometry; Qn disease; Transglutaminase

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LYSINE; POLYGLUTAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ANIMAL TISSUE; ARTICLE; CATALYSIS; CHROMATOGRAPHY; CROSS LINKING; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; GUINEA PIG; MASS SPECTROMETRY; MODULATION; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; RABBIT;

ANIMALS; CATALYSIS; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GTP-BINDING PROTEINS; GUINEA PIGS; LIVER; LYSINE; NEURODEGENERATIVE DISEASES; PEPTIDES; RABBITS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY; TRANSGLUTAMINASES; TRINUCLEOTIDE REPEATS;

ANIMALIA; CAVIA PORCELLUS; ORYCTOLAGUS CUNICULUS; SUS SCROFA;

EID: 0037216488     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0216103     Document Type: Article

References (44)

1. Aeschlimann, D. and Paulsson, M. 1994. Transglutaminases: Protein cross-linking enzymes in body fluids. Thromb. Haemost. 71: 402-414.
2. Aeschlimann, D. and Thomazy, V. 2000. Protein cross-linking in assembly and remodeling of extra cellular matrices: The role of transglutaminases. Connect. Tissue Res. 41: 1-27.
3. Altschuler, E.L., Hud, N.V., Mazrimas, J.A., and Rupp, B. 2000. Structure of polyglutamine. FEBS Lett. 472: 166-168.
4. Browne, S.E., Bowling, A.C., MacGarvey, U., Baik, M.J., Berger, S.C., Muqit, M.M., Bird, E.D., and Beal, M.F. 1997. Oxidative damage and metabolic dysfunction in Huntington's disease: Selective vulnerability of the basal ganglia. Ann. Neurol. 41: 646-653.
5. Burke, J.R., Enghild, J.J., Martin, M.E., Jou, Y.-S., Myers, R.M., Roses, A.D., Vance, J.M., and Strittmatter, W.J. 1996. Huntingtin and DRPLA proteins selectively interact with the protein GAPDH. Nat. Med. 2: 347-350.
6. Cha, J.K. 2000. Transcriptional dysregulation in Huntington's disease. Trends Neurosci. 23: 387-392.
7. Chen, S. and Wetzel, R., 2000. Solubilization and disaggregation of polyglutamine peptides. Protein Sci. 10: 887-891.
8. Chen, S., Berthelier, V., Yang, W., and Wetzel, R. 2001. Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity. J. Mol. Biol. 311: 173-182.
9. Citron, B.A., SantaCruz, K.S., Davies, P.J., and Festoff, B.W. 2001. Intronexon swapping of transglutaminase mRNA and neuronal tau aggregation in Alzheimer's disease. J. Biol. Chem. 276: 3295-3301.
10. Cooper, A.J.L., Sheu, K.-F.R., Burke, J.R., Onodera, O., Strittmatter, W.J., Roses, A.D., and Blass, J.P. 1997a. Polyglutamine domain are substrates of tissue transglutaminase. Does transglutaminase play a role in the expanded CAG/poly-Q neurodegenerative diseases? J. Neurochem. 69: 431-434.
11. -, 1997b. Transglutaminase-catalysed inactivation of glyceraldehyde 3-phosphate dehydrogenase and α-ketoglutarate dehydrogenase complex by polyglutamine domains of pathological length. Proc. Natl. Acad. Sci. 94: 12604-12609.
12. n-expansion diseases with special reference to the role of tissue transglutaminase and to selective vulnerability. J. Neurochem. 72: 889-899.
13. n-expansion diseases? Neurochem. Int. 40: 53-67.
14. Davies, S.W., Turmaine, M., Cozens, B.A., DiFiglia, M., Sharp, A.H., Ross, C.A., Scherzinger, E., Wanker, E.E., Mangiarini, L., and Bates, G.P. 1997. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90: 537-548.
15. de Cristofaro, T., Affiatati, A., Cariello, L., Avvedimento, E.V., and Varrone, S. 1999. The length of polyglutamine tract, the rate of degradation, and the transglutaminase activity influence the formation of intracellular aggregates. Biochem. Biophys. Res. Commun. 260: 150-158.
16. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P., and Aronin, N. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993.
17. 5)spermine derivatives of Substance P. J. Neurochem. 65: 420-426.
18. Folk, J.E. and Finlayson, J.S. 1977. The ε-(γ-glutamyl)lysine cross-link and the catalytic role of transglutaminases. Adv. Protein Chem. 31: 1-133.
19. Gentile, V., Sepe, C., Calvani, M., Melone, M.A.B., Cotrufo, R., Cooper, A.J.L., Blass, J.P., and Peluso, G. 1998. Tissue transglutaminase-catalysed formation of high-molecular-weight aggregates in vitro is favored with long polyglutamine domains: A possible mechanism contributing to CAG-triplet diseases. Arch. Biochem. Biophys. 352: 314-321.
20. Green, H. 1993. Human genetic diseases due to codon reiteration: Relationship to an evolutionary mechanism. Cell 74: 955-956.
21. Grenard, P., Bates, M.K., and Aeshlimann, D. 2001. Evolution of transglutaminase genes: Identification of a transglutaminase gene cluster on human chromosome 15q15. J. Biol. Chem. 276: 33066-33078.
22. Groenen, P.J.T.A., Smulders, R.H.P.H., Peters, R.F.R., Grootjans, J.J. Van Den Ijessel, P.R.L.A., Bloemendal, H., and de Jong, W.W. 1994. The amino-donor substrate specificity of tissue-type transglutaminase. Influence of amino acid residues flanking the amino-donor lysine residue. Eur. J. Biochem. 220: 795-799.
23. Grootjans. J.J., Groenen, P.J.T.A., and de Jong, W.W. 1995. Substrate requirements for transglutaminases. Influence of the amino acid residue preceding the amino donor lysine in a native protein. J. Biol. Chem. 270: 22855-22858.
24. Gutekunst, C.A., Li, S.H., Yi, H., Mulroy, J.S., Kuemmerle, S., Jones, R., Rye, D., Ferrante, R.J., Hersch, S.M., and Li, X.J. 1999. Nuclear and neurophil aggregates in Huntington's disease: Relationship to neuropathology. Neuroscience 19: 2522-2534.
25. Jeitner, T.M., Bogdanov, M.B., Matson, W.R., Daikhin, Y., Yudkoff, M., Folk, J.E., Steinman, L., Browne, M.F., Blass, J.P., and Cooper, A.J.L. 2001. N(ε)-(γ-L-glutamyl)-L-lysine (GGEL) is increased in cerebrospinal fluid of patients with Huntington's disease. J. Neurochem. 79: 1109-1112.
26. Kahlem, P., Terré, C., Green, H., and Djian, P. 1996. Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: Relevance to diseases of the nervous system. Proc. Natl. Acad. Sci. 93: 14580-14585.
27. Karpuj, M.V., Becher, M.W., and Steinman, L. 2002a. Evidence for a role for transglutaminase in Huntington's disease and potential therapeutic implications. Neurochem. Int. 40: 31-36.
28. Karpuj, M.V., Becher, M.W., Springer, J.E., Chabas, D., Youssef, S., Pedotti, R., Mitchell, D., and Steinman, L. 2002b. Prolonged survival and decreased abnormal movements in transgenic model of Huntington disease, with administration of the transglutaminase inhibitor cystamine. Nat. Med. 8: 143-149.
29. Kim, S.-Y., Jeitner, T.M., and Steinert, P.M. 2002. Transglutaminases in disease. Neurochem. Int. 40: 85-103.
30. Kosby, B., Matilla, T., Burright, E.N., Merry, D.E., Fischbeck, K.H., Orr, H.T., and Zoghbi, H.Y. 1996. Spinocerebellar ataxia type-1 and spinobulbar muscular atropy gene products interact with glyceraldehyde 3-phosphate dehydrogenase. Hum. Mol. Genet. 5: 1311-1318.
31. Lee, K.N., Birckbichler, P.J., Patterson, Jr., M.K. 1989. GTP hydrolysis by guinea pig liver transglutaminase. Biochem. Biophys. Res. Commun. 162: 1370-1375.
32. Lesort, M., Chun, W., Johnson, G.V.W., and Ferrante, R.J. 1999. Tissue transglutaminase is increased in Huntington's disease brain. J. Neurochem. 73: 2018-2027.
33. Li, H., Li, S.H., Cheng, A.L., Mangiarini, L., Bates, G.P., and Li, X.J. 1999. Ultrastructural localization and progressive formation of neurophil aggregates in Huntington's disease transgenic mice. Hum. Mol. Genet. 8: 1227-1236.
34. Lorand, L. and Conrad, S.M. 1984. Transglutaminases. Mol. Cell. Biochem. 58: 9-35.
35. Masino, L., Kelly, G., Leonard, K., Trottier, Y., and Pastore, A. 2002. Solution structure of polyglutamine tracts in GST-polyglutamine fusion proteins. FEBS Lett. 513: 267-272.
36. Mazzola, J.L. and Sirover, M.A. 2001. Reduction of glyceraldehyde-3-phosphate-dehydrogenase activity in Alzheimer's disease and in Huntington's disease fibroblasts. J. Neurochem. 76: 442-449.
37. Orrù, S., Ruoppolo, M., Francese, S., Vitagliano, L., Marino, G., and Esposito, C. 2002. Identification of tissue transglutaminase-reactive lysine residues in glyceraldehyde-3-phosphate-dehydrogenase. Protein Sci. 11: 137-146.
38. Paulson, H.L. 1999. Human Genetics '99: Trinucleotide repeats. Protein fate in neurodegenerative proteinopathies: Polyglutamine diseases join the (mis) fold. Am. J. Hum. Genet. 64: 339-345.
39. Paulson, H.L., Perez, M.K., Trottier, Y., Trojanowski, J.Q, Subramony, S.H., Das, S.S., Vig, P., Mandel, J.L., Fischbeck, K.H., and Pittman, R.N. 1997. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 19: 333-344.
40. Perutz, M.F. 1999. Glutamine repeats and neurodegenerative diseases: Molecular aspects. Trends Biochem. Sci. 24: 58-63.
41. Perutz, M.F., Johnson, T., Suzuki, M., and Finch, J.T. 1994. Glutamine repeats as polar zippers: Their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. 91: 5355-5358.
42. Sirover, M.A. 1999. New insights into an old protein: The functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochem. Biophys. Acta 1432: 159-184.
43. Stott, K., Blackburn, J.M., Butler, P.J., and Perutz, M. 1995. Incorporation of glutamine repeats makes protein oligomerize: Implications for neurodegenerative diseases. Proc. Natl. Acad. Sci. 92: 6509-6513.
44. Zoghbi, H.Y. and Orr. H.T. 2000. Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23: 217-247.