Tissue transglutaminase catalyzes the deamidation of glutamines in lens βB2- and βB3-crystallins

Experimental Eye Research

Volumn 86, Issue 2, 2008, Pages 383-393

  Boros, Sandor ^a   Wilmarth, Phillip A ^b   Kamps, Bram ^a   de Jong, Wilfried W ^a   Bloemendal, Hans ^a   Lampi, Kirsten ^b   Boelens, Wilbert C ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

calcium; crosslink; crystallin; deamidation; lens; transglutaminase

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; GLUTAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

AGING; ARTICLE; CATALYSIS; CONTROLLED STUDY; CROSS LINKING; DEAMINATION; GUINEA PIG; HUMAN; IN VITRO STUDY; LENS; MACROMOLECULE; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN MODIFICATION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AGING; AMIDES; ANIMALS; BETA-CRYSTALLIN B CHAIN; CATALYSIS; CATTLE; FETUS; GLUTAMINE; GTP-BINDING PROTEINS; HUMANS; LENS, CRYSTALLINE; MIDDLE AGED; PROTEOME; TRANSGLUTAMINASES;

EID: 39149092676     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2007.11.011     Document Type: Article

References (55)

1. Akimov S.S., Krylov D., Fleischman L.F., and Belkin A.M. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J. Cell Biol. 148 (2000) 825-838
2. Berbers G.A., Bentlage H.C., Brans A.M., Bloemendal H., and de Jong W.W. beta-Crystallin: endogenous substrate of lens transglutaminase. Characterization of the acyl-donor site in the beta Bp chain. Eur. J. Biochem. 135 (1983) 315-320
3. Berbers G.A., Feenstra R.W., van den B.R., Hoekman W.A., Bloemendal H., and de Jong W.W. Lens transglutaminase selects specific beta-crystallin sequences as substrate. Proc. Natl. Acad. Sci. U.S.A. 81 (1984) 7017-7020
4. Berry Y., and Truscott R.J. The presence of a human UV filter within the lens represents an oxidative stress. Exp. Eye Res. 72 (2001) 411-421
5. Boros S., Kamps B., Wunderink L., de Bruijn W., de Jong W.W., and Boelens W.C. Transglutaminase catalyzes differential crosslinking of small heat shock proteins and amyloid-beta. FEBS Lett. 576 (2004) 57-62
6. Boros S., Ahrman E., Wunderink L., Kamps B., de Jong W.W., Boelens W.C., and Emanuelsson C.S. Site-specific transamidation and deamidation of the small heat-shock protein Hsp20 by tissue transglutaminase. Proteins 62 (2006) 1044-1052
7. Capasso S. Estimation of the deamidation rate of asparagine side chains. J. Pept. Res. 55 (2000) 224-229
8. Choi Y.C., Park G.T., Kim T.S., Sunwoo I.N., Steinert P.M., and Kim S.Y. Sporadic inclusion body myositis correlates with increased expression and cross-linking by transglutaminases 1 and 2. J. Biol. Chem. 275 (2000) 8703-8710
9. Clement S., Velasco P.T., Murthy S.N., Wilson J.H., Lukas T.J., Goldman R.D., and Lorand L. The intermediate filament protein, vimentin, in the lens is a target for cross-linking by transglutaminase. J. Biol. Chem. 273 (1998) 7604-7609
10. David L.L., Lampi K.J., Lund A.L., and Smith J.B. The sequence of human betaB1-crystallin cDNA allows mass spectrometric detection of betaB1 protein missing portions of its N-terminal extension. J. Biol. Chem. 271 (1996) 4273-4279
11. De Laurenzi V., and Melino G. Gene disruption of tissue transglutaminase. Mol. Cell. Biol. 21 (2001) 148-155
12. Fesus L., and Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci. 27 (2002) 534-539
13. Flaugh S.L., Mills I.A., and King J. Glutamine deamidation destabilizes human gammaD-crystallin and lowers the kinetic barrier to unfolding. J. Biol. Chem. 281 (2006) 30782-30793
14. Fleckenstein B., Molberg O., Qiao S.W., Schmid D.G., von der M.F., Elgstoen K., Jung G., and Sollid L.M. Gliadin T cell epitope selection by tissue transglutaminase in celiac disease. Role of enzyme specificity and pH influence on the transamidation versus deamidation process. J. Biol. Chem. 277 (2002) 34109-34116
15. Folk J.E. Mechanism and basis for specificity of transglutaminase-catalyzed epsilon-(gamma-glutamyl) lysine bond formation. Adv. Enzymol. Relat. Areas Mol. Biol. 54 (1983) 1-56
16. Gentile V., Thomazy V., Piacentini M., Fesus L., and Davies P.J. Expression of tissue transglutaminase in Balb-C 3T3 fibroblasts: effects on cellular morphology and adhesion. J. Cell Biol. 119 (1992) 463-474
17. Gorman J.J., and Folk J.E. Structural features of glutamine substrates for transglutaminases. Role of extended interactions in the specificity of human plasma factor XIIIa and of the guinea pig liver enzyme. J. Biol. Chem. 259 (1984) 9007-9010
18. Griffin M., and Verderio E. Tissue transglutaminase in cell death. Symp. Soc. Exp. Biol. 52 (2000) 223-240
19. Griffin M., Casadio R., and Bergamini C.M. Transglutaminases: nature's biological glues. Biochem. J. 368 (2002) 377-396
20. Groenen P.J., Bloemendal H., and de Jong W.W. The carboxy-terminal lysine of alpha B-crystallin is an amine-donor substrate for tissue transglutaminase. Eur. J. Biochem. 205 (1992) 671-674
21. Groenen P.J., Seccia M., Smulders R.H., Gravela E., Cheeseman K.H., Bloemendal H., and 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. 295 Pt 2 (1993) 399-404
22. Groenen P.J., Grootjans J.J., Lubsen N.H., Bloemendal H., and de Jong W.W. Lys-17 is the amine-donor substrate site for transglutaminase in beta A3-crystallin. J. Biol. Chem. 269 (1994) 831-833
23. Kim S.Y., Grant P., Lee J.H., Pant H.C., and Steinert P.M. Differential expression of multiple transglutaminases in human brain. Increased expression and cross-linking by transglutaminases 1 and 2 in Alzheimer's disease. J. Biol. Chem. 274 (1999) 30715-30721
24. Korlimbinis A., Hains P.G., Truscott R.J., and Aquilina J.A. 3-Hydroxykynurenine oxidizes alpha-crystallin: potential role in cataractogenesis. Biochemistry 45 (2006) 1852-1860
25. Lampi K.J., Ma Z., Shih M., Shearer T.R., Smith J.B., Smith D.L., and David L.L. Sequence analysis of betaA3, betaB3, and betaA4 crystallins completes the identification of the major proteins in young human lens. J. Biol. Chem. 272 (1997) 2268-2275
26. Lampi K.J., Oxford J.T., Bachinger H.P., Shearer T.R., David L.L., and Kapfer D.M. Deamidation of human beta B1 alters the elongated structure of the dimer. Exp. Eye Res. 72 (2001) 279-288
27. Lampi K.J., Amyx K.K., Ahmann P., and Steel E.A. Deamidation in human lens betaB2-crystallin destabilizes the dimer. Biochemistry 45 (2006) 3146-3153
28. Lapko V.N., Purkiss A.G., Smith D.L., and Smith J.B. Deamidation in human gamma S-crystallin from cataractous lenses is influenced by surface exposure. Biochemistry 41 (2002) 8638-8648
29. Lorand L., and Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4 (2003) 140-156
30. Lorand L., Hsu L.K., Siefring Jr. G.E., and Rafferty N.S. Lens transglutaminase and cataract formation. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 1356-1360
31. Lorand L., Conrad S.M., and Velasco P.T. Formation of a 55 000-weight cross-linked beta crystallin dimer in the Ca2+-treated lens. A model for cataract. Biochemistry 24 (1985) 1525-1531
32. Lorand L., Conrad S.M., and Velasco P.T. Inhibition of beta-crystallin cross-linking in the Ca2+-treated lens. Invest. Ophthalmol. Vis. Sci. 28 (1987) 1218-1222
33. Lorand L., Velasco P.T., Murthy S.N., Wilson J., and Parameswaran K.N. Isolation of transglutaminase-reactive sequences from complex biological systems: a prominent lysine donor sequence in bovine lens. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 11161-11163
34. Ma Z., Hanson S.R., Lampi K.J., David L.L., Smith D.L., and Smith J.B. Age-related changes in human lens crystallins identified by HPLC and mass spectrometry. Exp. Eye Res. 67 (1998) 21-30
35. Miesbauer L.R., Smith J.B., and Smith D.L. Amino acid sequence of human lens beta B2-crystallin. Protein Sci. 2 (1993) 290-291
36. Mulders J.W., Hoekman W.A., Bloemendal H., and de Jong W.W. Beta B1 crystallin is an amine-donor substrate for tissue transglutaminase. Exp. Cell Res. 171 (1987) 296-305
37. Murthy S.N.P., Velasco P.T., and Lorand L. Properties of purified lens transglutaminase and regulation of its transamidase/crosslinking activity by GTP. Exp. Eye Res. 67 (1998) 273-281
38. Piacentini M., Farrace M.G., Piredda L., Matarrese P., Ciccosanti F., Falasca L., Rodolfo C., Giammarioli A.M., Verderio E., Griffin M., and Malorni W. Transglutaminase overexpression sensitizes neuronal cell lines to apoptosis by increasing mitochondrial membrane potential and cellular oxidative stress. J. Neurochem. 81 (2002) 1061-1072
39. Robinson N.E., and Robinson A.B. Molecular clocks. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 944-949
40. Robinson N.E., Lampi K.J., Speir J.P., Kruppa G., Easterling M., and Robinson A.B. Quantitative measurement of young human eye lens crystallins by direct injection Fourier transform ion cyclotron resonance mass spectrometry. Mol. Vis. 12 (2006) 704-711
41. Searle B.C., Dasari S., Wilmarth P.A., Turner M., Reddy A.P., David L.L., and Nagalla S.R. Identification of protein modifications using MS/MS de novo sequencing and the OpenSea alignment algorithm. J. Proteome Res. 4 (2005) 546-554
42. Seccia M., Brossa O., Gravela E., Slater T.F., and Cheeseman K.H. Exposure of beta L-crystallin to oxidizing free radicals enhances its susceptibility to transglutaminase activity. Biochem. J. 274 Pt 3 (1991) 869-873
43. Shin D.M., Jeon J.H., Kim C.W., Cho S.Y., Kwon J.C., Lee H.J., Choi K.H., Park S.C., and 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. 279 (2004) 15032-15039
44. Siebinga I., Vrensen G.F., Otto K., Puppels G.J., De Mul F.F., and Greve J. Ageing and changes in protein conformation in the human lens: a Raman microspectroscopic study. Exp. Eye Res. 54 (1992) 759-767
45. Soderberg P.G. Experimental cataract induced by ultraviolet radiation. Acta Ophthalmol. Suppl. 196 (1990) 1-75
46. Takemoto L., and Boyle D. Deamidation of specific glutamine residues from alpha-A crystallin during aging of the human lens. Biochemistry 37 (1998) 13681-13685
47. Takemoto L., Fujii N., and Boyle D. Mechanism of asparagine deamidation during human senile cataractogenesis. Exp. Eye Res. 72 (2001) 559-563
48. Tsur D., Tanner S., Zandi E., Bafna V., and Pevzner P.A. Identification of post-translational modifications by blind search of mass spectra. Nat. Biotechnol. 23 (2005) 1562-1567
49. Vader L.W., de Ru A., van der W.Y., Kooy Y.M., Benckhuijsen W., Mearin M.L., Drijfhout J.W., van Veelen P., and Koning F. Specificity of tissue transglutaminase explains cereal toxicity in celiac disease. J. Exp. Med. 195 (2002) 643-649
50. van de Wal Y., Kooy Y., van Veelen P., Pena S., Mearin L., Papadopoulos G., and Koning F. Selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T cell reactivity. J. Immunol. 161 (1998) 1585-1588
51. Velasco P.T., and Lorand L. Acceptor-donor relationships in the transglutaminase-mediated cross-linking of lens beta-crystallin subunits. Biochemistry 26 (1987) 4629-4634
52. Werten P.J., Carver J.A., Jaenicke R., and de Jong W.W. The elusive role of the N-terminal extension of beta A3- and beta A1-crystallin. Protein Eng. 9 (1996) 1021-1028
53. Wilmarth P.A., Tanner S., Dasari S., Nagalla S.R., Riviere M.A., Bafna V., Pevzner P.A., and David L.L. Age-related changes in human crystallins determined from comparative analysis of post-translational modifications in young and aged lens: does deamidation contribute to crystallin insolubility?. J. Proteome Res. 5 (2006) 2554-2566
54. Wright H.T. Non-enzymatic deamidation of asparaginyl and glutaminyl residues in proteins. Crit. Rev. Biochem. Mol. Biol. 26 (1991) 1-52
55. Zhang Z., Smith D.L., and Smith J.B. Human beta-crystallins modified by backbone cleavage, deamidation and oxidation are prone to associate. Exp. Eye Res. 77 (2003) 259-272