The end product of transglutaminase crosslinking: Simultaneous quantitation of [Nε-(γ-glutamyl) lysine] and lysine by HPLC-MS3

Analytical Biochemistry

Volumn 384, Issue 2, 2009, Pages 296-304

  Hoffner, G ^a   van der Rest, G ^b   Dansette, P M ^c   Djian, P ^a  

^a CNRS   (France)

^b LABORATOIRE HÉTÉROÉLÉMENTS ET COORDINATION   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Huntington disease; Liquid chromatography; Mass spectrometry; Neurodegenerative diseases; Quantitation method; Transglutaminase; N ( Glutamyl) lysine isodipeptide

Indexed keywords

ACETYLATION; AMIDES; LIQUID CHROMATOGRAPHY; LIQUIDS; MASS SPECTROMETERS; MASS SPECTROMETRY; NEURODEGENERATIVE DISEASES; PLANTS (BOTANY);

COEFFICIENTS OF VARIATIONS; CORRELATION COEFFICIENT; HUNTINGTON DISEASE; ION TRAP MASS SPECTROMETER; LIQUID-LIQUID EXTRACTION; MULTIPLE STAGE MASS SPECTROMETRY; QUANTITATION METHOD; TRANSGLUTAMINASES;

AMINO ACIDS;

ACETONITRILE; AMIDE; CARBOXYL GROUP; DIPEPTIDE DERIVATIVE; FIBRIN; LYSINE; N EPSILON (GAMMA GLUTAMYL)LYSINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BUTYLATION; CATALYST; CHEMICAL REACTION; CONTROLLED STUDY; CORRELATION COEFFICIENT; DERIVATIZATION; ELUTION; ENZYME ACTIVITY; ENZYME MECHANISM; EPIDERMIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; ION TRAP MASS SPECTROMETRY; LIQUID LIQUID EXTRACTION; MASS SPECTROMETRY; NEOPLASM; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; TECHNIQUE;

EID: 56749180750     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2008.09.039     Document Type: Article

References (43)

1. Lorand J.B., Urayama T., and Lorand L. Transglutaminase as a blood clotting enzyme. Biochem. Biophys. Res. Commun. 23 (1966) 828-834
2. Esposito C., and Caputo I. Mammalian transglutaminases: identification of substrates as a key to physiological function and physiopathological relevance. FEBS J. 272 (2005) 615-631
3. Rice R.H., and Green H. The cornified envelope of terminally differentiated human epidermal keratinocytes consists of cross-linked protein. Cell 11 (1977) 417-422
4. Green H. Human genetic diseases due to codon reiteration: relationship to an evolutionary mechanism. Cell 74 (1993) 955-956
5. Fuller G.M., and Doolittle R.F. The formation of cross-linked fibrins: evidence for the involvement of lysine ε-amino groups. Biochem. Biophys. Res. Commun. 25 (1966) 694
6. Williams-Ashman H.G. Transglutaminases and the clotting of mammalian seminal fluids. Mol. Cell. Biochem. 58 (1984) 51
7. Fesus L., and Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci. 27 (2002) 534-539
8. Aeschlimann D., and Thomazy V. Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. Connect. Tissue Res. 41 (2000) 1-27
9. Singh U.S., Kunar M.T., Kao Y.L., and Baker K.M. Role of transglutaminase II in retinoic acid-induced activation of RhoA-associated kinase-2. EMBO J. 20 (2001) 2413-2423
10. Janiak A., Zemskov E.A., and Belkin A.M. Cell surface transglutaminase promotes RhoA activation via integrin clustering and suppression of the Src-p190RhoGAP signaling pathway. Mol. Biol. Cell 17 (2006) 1606-1619
11. Kahlem P., Terre C., Green H., and Djian P. Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: relevance to diseases of the nervous system. Proc. Natl. Acad. Sci. USA 93 (1996) 14580-14585
12. Kahlem P., Green H., and Djian P. Transglutaminase action imitates Huntington's disease: selective polymerization of huntingtin containing expanded polyglutamine. Mol. Cell 1 (1998) 595-601
13. Hoffner G., and Djian P. Transglutaminase and diseases of the central nervous system. Front. Biosci. 10 (2005) 3078-3092
14. Hoffner G., Island M.L., and Djian P. Purification of neuronal inclusions of patients with Huntington's disease reveals a broad range of N-terminal fragments of expanded huntingtin and insoluble polymers. J. Neurochem. 95 (2005) 125-136
15. Cooper A.J., Sheu K.F., Burke J.R., Onodera O., Strittmatter W.J., Roses A.D., and Blass J.P. Polyglutamine domains are substrates of tissue transglutaminase: does transglutaminase play a role in expanded CAG/poly-Q neurodegenerative diseases?. J. Neurochem. 69 (1997) 431-434
16. Lesort M., Chun W., Johnson G.V., and Ferrante R.J. Tissue transglutaminase is increased in Huntington's disease brain. J. Neurochem. 73 (1999) 2018-2027
17. Gentile V., Sepe C., Calvani M., Melone M.A., Cotrufo R., Cooper A.J., Blass J.P., and Peluso G. Tissue transglutaminase-catalyzed 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 (1998) 314-321
18. n-expansion diseases?. Neurochem. Intl. 40 (2002) 53-67
19. Zainelli G.M., Dudek N.L., Ross C.A., Kim S.Y., and Muma N.A. Mutant huntingtin protein: a substrate for transglutaminase 1, 2, and 3. J. Neuropathol. Exp. Neurol. 64 (2005) 58-65
20. Selkoe D.J., Abraham C., and Ihara Y. Brain transglutaminase: in vitro crosslinking of human neurofilament proteins into insoluble polymers. Proc. Natl. Acad. Sci. USA 79 (1982) 6070-6074
21. Junn E., Ronchetti R.D., Quezado M.M., Kim S.Y., and Mouradian M.M. Tissue transglutaminase-induced aggregation of α-synuclein: implications for Lewy body formation in Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. USA 100 (2003) 2047-2052
22. Verma A., and Mehta K. Tissue transglutaminase-mediated chemoresistance in cancer cells. Drug Resist. Updat. 10 (2007) 144-151
23. Siegel M., and Khosla C. Transglutaminase 2 inhibitors and their therapeutic role in disease states. Pharmacol. Ther. 115 (2007) 232-245
24. Kotsakis P., and Griffin M. Tissue transglutaminase in tumour progression: friend or foe?. Amino Acids 33 (2007) 373-384
25. Ai L., Kim W.J., Demircan B., Dyer L.M., Bray K.J., Skehan R.R., Massoll N.A., and Brown K.D. The transglutaminase 2 gene (TGM2), a potential molecular marker for chemotherapeutic drug sensitivity, is epigenetically silenced in breast cancer. Carcinogenesis 29 (2008) 510-518
26. Kim S.Y. Transglutaminase 2 in inflammation. Front. Biosci. 11 (2006) 3026-3035
27. Pinkas D.M., Strop P., Brunger A.T., and Khosla C. Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol. 5 (2007) e327
28. Falasca L., Farrace M.G., Rinaldi A., Tuosto L., Melino G., and Piacentini M. Transglutaminase type II is involved in the pathogenesis of endotoxic shock. J. Immunol. 180 (2008) 2616-2624
29. Pruissen D.M.O., Slooter A.J.C., Rosendaal F.R., van der Graaf Y., and Algra A. Coagulation factor XIII gene variation, oral contraceptives, and risk of ischemic stroke. Blood 111 (2008) 1282
30. Nemes Z., Petrovski G., and Fesus L. Tools for the detection and quantitation of protein transglutamination. Anal. Biochem. 342 (2005) 1-10
31. Tarcsa E., and Fesus L. Determination of ε(γ-glutamyl)lysine crosslink in proteins using phenylisothiocyanate derivatization and high-pressure liquid chromatographic separation. Anal. Biochem. 186 (1990) 135-140
32. Miller M.L., and Johnson G.V. Rapid, single-step procedure for the identification of transglutaminase-mediated isopeptide crosslinks in amino acid digests. J. Chromatogr. B 732 (1999) 65-72
33. ε-(γ-l-Glutamyl)-l-lysine (GGEL) is increased in cerebrospinal fluid of patients with Huntington's disease. J. Neurochem. 79 (2001) 1109-1112
34. ε(γ-Glutamyl)lysine in cerebrospinal fluid marks Alzheimer type and vascular dementia. Neurobiol. Aging 22 (2001) 403-406
35. Nemes Z., Devreese B., Steinert P.M., Van Beeumen J., and Fesus L. Cross-linking of ubiquitin, HSP27, parkin, and α-synuclein by γ-glutamyl-ε-lysine bonds in Alzheimer's neurofibrillary tangles. FASEB J. 18 (2004) 1135-1137
36. Jeitner T.M., Matson W.R., Folk J.E., Blass J.P., and Cooper A.J. Increased levels of γ-glutamylamines in Huntington disease CSF. J. Neurochem. 106 (2008) 37-44
37. Schäfer C., Schott M., Brandl F., Neidhart S., and Carle R. Identification and quantification of ε-(γ-glutamyl)lysine in digests of enzymatically cross-linked leguminous proteins by high-performance liquid chromatography-electrospray ionization mass spectrometry (HPLC-ESI-MS). J. Agric. Food Chem. 53 (2005) 2830-2837
38. ε-(γ-Glutamyl) lysine] as a potential biomarker in neurological diseases: new detection method and fragmentation pathways. J. Mass Spectrom. 43 (2008) 456-469
39. Pisano J.J., Finlayson J.S., and Peyton M.P. Cross-link in fibrin polymerized by factor 13: ε-(γ-glutamyl)lysine. Science 160 (1968) 892-893
40. Pisano J.J., Finlayson J.S., Peyton M.P., and Nagai Y. ε-(γ-Glutamyl) lysine in fibrin: lack of crosslink formation in factor 13 deficiency. Proc. Natl. Acad. Sci. USA 68 (1971) 770-772
41. Matacic S., and Loewy A.G. The identification of isopeptide crosslinks in insoluble fibrin. Biochem. Biophys. Res. Commun. 30 (1968) 356-362
42. Lorand L., Downey J., Gotoh T., Jacobsen A., and Tokura S. The transpeptidase system which crosslinks fibrin by γ-glutamyl-ε-lysine bonds. Biochem. Biophys. Res. Commun. 31 (1968) 222-230
43. Dedeoglu A., Kubilus J.K., Jeitner T.M., Matson S.A., Bogdanov M., Kowall N.W., Matson W.R., Cooper A.J., Ratan R.R., Beal M.F., Hersch S.M., and Ferrante R.J. Therapeutic effects of cystamine in a murine model of Huntington's disease. J. Neurosci. 22 (2002) 8942-8950