Transglutaminases and neurodegeneration

Journal of Neurochemistry

Volumn 109, Issue SUPPL. 1, 2009, Pages 160-166

  Jeitner, Thomas M ^b   Pinto, John T ^a   Krasnikov, Boris F ^a   Horswill, Mark ^c   Cooper, Arthur J L ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b Red Anvil LLC   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

glutamyl lysine; glutamylpolyamines; Cystamine; Neurodegeneration; Polyamines; Transglutaminase

Indexed keywords

1,2,4 THIADIAZOLE DERIVATIVE; AMIDE; CYSTAMINE; DOPAMINE; EPOXIDE; ISOXAZOLE DERIVATIVE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ALZHEIMER DISEASE; BRAIN; CONFERENCE PAPER; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUNTINGTON CHOREA; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BRAIN; HUMANS; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; TRANSGLUTAMINASES;

ANIMALIA;

EID: 64349083615     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.05843.x     Document Type: Conference Paper

References (89)

1. Andringa G., Lam K. Y., Chegary M., Wang X., Chase T. N. Bennett M. C. (2004) Tissue transglutaminase catalyzes the formation of α-synuclein crosslinks in Parkinson's disease. FASEB J. 18, 932 934.
2. Appelt D. M. Balin B. J. (1997) The association of tissue transglutaminase with human recombinant tau results in the formation of insoluble filamentous structures. Brain Res. 745, 21 31.
3. Bennett E. J., Shaler T. A., Woodman B., Ryu K. Y., Zaitseva T. S., Becker C. H., Bates G. P., Schulman H. Kopito R. R. (2007) Global changes to the ubiquitin system in Huntington's disease. Nature 448, 704 708.
4. Bergamini C. M., Signorini M. Poltronieri L. (1987) Inhibition of erythrocyte transglutaminase by GTP. Biochim. Biophys. Acta 916, 149 151.
5. Bonelli R. M., Aschoff A., Niederwieser G., Heuberger C. Jirikowski G. (2002) Cerebrospinal fluid tissue transglutaminase as a biochemical marker for Alzheimer's disease. Neurobiol. Dis. 11, 106 110.
6. Borrell-Pages M., Canals J. M., Cordelieres F. P. et al. (2006) Cystamine and cysteamine increase brain levels of BDNF in Huntington disease via HSJ1b and transglutaminase. J. Clin. Invest. 116, 1410 1424.
7. Caccamo D., Campisi A., Curro M., Li Volti G., Vanella A. Ientile R. (2004) Excitotoxic and post-ischemic neurodegeneration: involvement of transglutaminases. Amino Acids 27, 373 379.
8. Campisi A., Caccamo D., Li Volti G., Curro M., Parisi G., Avola R., Vanella A. Ientile R. (2004) Glutamate-evoked redox state alterations are involved in tissue transglutaminase upregulation in primary astrocyte cultures. FEBS Lett. 578, 80 84.
9. Case A. Stein R. L. (2007) Kinetic analysis of the interaction of tissue transglutaminase with a nonpeptidic slow-binding inhibitor. Biochemistry 46, 1106 1115.
10. Cooper A. J. L., Sheu K. F., Burke J. R., Onodera O., Strittmatter W. J., Roses A. D. Blass J. P. (1997a) Polyglutamine domains are substrates of tissue transglutaminase: does transglutaminase play a role in expanded CAG/poly-Q neurodegenerative diseases? J. Neurochem. 69, 431 434.
11. Cooper A. J. L., Sheu K. R., Burke J. R., Onodera O., Strittmatter W. J., Roses A. D. Blass J. P. (1997b) Transglutaminase-catalyzed inactivation of glyceraldehyde 3-phosphate dehydrogenase and α-ketoglutarate dehydrogenase complex by polyglutamine domains∼of pathological length. Proc. Natl Acad. Sci. USA 94, 12604 12609.
12. n expansion diseases. Dev. Neurosci. 22, 404 417.
13. n-expansion diseases? Neurochem. Int. 40, 53 67.
14. Cordella-Miele E., Miele L., Beninati S. Mukherjee A. B. (1993) Transglutaminase-catalyzed incorporation of polyamines into phospholipase A2. J. Biochem. 113, 164 173.
15. 2+-dependent transamidation activity in the protection afforded by tissue transglutaminase against doxorubicin-induced apoptosis. Biochemistry 45, 13163 13174.
16. Dedeoglu A., Kubilus J. K., Jeitner T. M. et al. (2002) Therapeutic effects of cystamine in a murine model of Huntington's disease. J. Neurosci. 22, 8942 8950.
17. DiFiglia M., Sapp E., Chase K. et al. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14, 1075 1081.
18. Dudek S. M. Johnson G. V. W. (1993) Transglutaminase catalyzes the formation of sodium dodecyl sulfate-insoluble, Alz-50-reactive polymers of tau. J. Neurochem. 61, 1159 1162.
19. Dudek S. M. Johnson G. V. W. (1994) Transglutaminase facilitates the formation of polymers of the beta-amyloid peptide. Brain Res. 651, 129 133.
20. Duval E., Case A., Stein R. L. Cuny G. D. (2005) Structure-activity relationship study of novel tissue transglutaminase inhibitors. Bioorg. Med. Chem. Lett. 15, 1885 1889.
21. Festoff B. W., SantaCruz K., Arnold P. M., Sebastian C. T., Davies P. J. A. Citron B. A. (2002) Injury-induced "switch" from GTP-regulated to novel GTP-independent isoform of tissue transglutaminase in the rat spinal cord. J. Neurochem. 81, 708 718.
22. Fink M. L. Folk J. E. (1981) γ-Glutamylamine cyclotransferase. An enzyme involved in the catabolism of ε-(γ-glutamyl)lysine and other gamma-glutamylamines. Mol. Cell. Biochem. 38 Spec. No., 59 67.
23. Fox J. H., Barber D. S., Singh B. et al. (2004) Cystamine increases L-cysteine levels in Huntington's disease transgenic mouse brain and in a PC12 model of polyglutamine aggregation. J. Neurochem. 91, 413 422.
24. Frankel D. Schipper H. M. (1999) Cysteamine pretreatment of the astroglial substratum (mitochondrial iron sequestration) enhances PC12 cell vulnerability to oxidative injury. Exp. Neurol. 160, 376 385.
25. Gentile V. Cooper A. J. L. (2004) Transglutaminases - possible drug targets in human diseases. Curr. Drug Targets CNS Neurol. Disord. 3, 99 104.
26. Gentile V., Sepe C., Calvani M., Melone M. A., Cotrufo R., Cooper A. J. L., Blass J. P. Peluso G. (1998) 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, 314 321.
27. Gillet S. M., Chica R. A., Keillor J. W. Pelletier J. N. (2004) Expression and rapid purification of highly active hexahistidine-tagged guinea pig liver transglutaminase. Protein. Expr. Purif. 33, 256 264.
28. Goldstone S. D., Fragonas J. C., Jeitner T. M. Hunt N. H. (1995) Transcription factors as targets for oxidative signalling during lymphocyte activation. Biochim. Biophys. Acta 1263, 114 122.
29. Gomez-Santos C., Ferrer I., Santidrian A. F., Barrachina M., Gil J. Ambrosio S. (2003) Dopamine induces autophagic cell death and alpha-synuclein increase in human neuroblastoma SH-SY5Y cells. J. Neurosci. Res. 73, 341 350.
30. Green H. (1993) Human genetic diseases due to codon reiteration: relationship to an evolutionary mechanism. Cell 74, 955 956.
31. Hadjivassiliou M., Aeschlimann P., Strigun A., Sanders D. S., Woodroofe N Acshlimann D. (2008) Autoantibodies in gluten ataxia recognize a novel neural transglutaminase. Ann Neurol. 64, 332 343.
32. Hartley D. M., Zhao C., Speier A. C., Woodard G. A., Li S., Li Z. Walz T. (2008) Transglutaminase induces protofibril-like amyloid beta-protein assemblies that are protease-resistant and inhibit long-term potentiation. J. Biol. Chem. 283, 16790 16800.
33. Ho G. J., Gregory E. J., Smirnova I. V., Zoubine M. N. Festoff B. W. (1994) Cross-linking of beta-amyloid protein precursor catalyzed by tissue transglutaminase. FEBS Lett. 349, 151 154.
34. Ikura K., Takahata K. Sasaki R. (1993) Cross-linking of a synthetic partial-length (1-28) peptide of the Alzheimer beta/A4 amyloid protein by transglutaminase. FEBS Lett. 326, 109 111.
35. ε-(γ-L-Glutamyl)-L-lysine (GGEL) is increased in cerebrospinal fluid of patients with Huntington's disease. J. Neurochem. 79, 1109 1112.
36. Jeitner T. M., Delikatny E. J., Ahlqvist J., Capper H. Cooper A. J. L. (2005) Mechanism for the inhibition of transglutaminase 2 by cystamine. Biochem. Pharmacol. 69, 961 970.
37. Jeitner T. M., Matson W. R., Folk J. E., Blass J. P. Cooper A. J. L. (2008) Increased levels of gamma-glutamylamines in Huntington disease CSF. J. Neurochem. 106, 37 44.
38. Jensen P. H., Sorensen E. S., Petersen T. E., Gliemann J. Rasmussen L. K. (1995) Residues in the synuclein consensus motif of the alpha-synuclein fragment, NAC, participate in transglutaminase-catalysed cross-linking to Alzheimer-disease amyloid β A4 peptide. Biochem. J. 310, 91 94.
39. Johnson G. V. W. LeShoure R. Jr. (2004) Immunoblot analysis reveals that isopeptide antibodies do not specifically recognize the ε-(γ- glutamyl)lysine bonds formed by transglutaminase activity. J. Neurosci. Methods 134, 151 158.
40. Johnson G. V. W., Cox T. M., Lockhart J. P., Zinnerman M. D., Miller M. L. Powers R. E. (1997) Transglutaminase activity is increased in Alzheimer's disease brain. Brain Res. 751, 323 329.
41. Kahlem P., Terre C., Green H. 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. USA 93, 14580 14585.
42. Karpuj M. V., Garren H., Slunt H., Price D. L., Gusella J., Becher M. W. Steinman L. (1999) Transglutaminase aggregates huntingtin into nonamyloidogenic polymers, and its enzymatic activity increases in Huntington's disease brain nuclei. Proc. Natl Acad. Sci. USA 96, 7388 7393.
43. Kawabe S., Ikuta T., Ohba M., Chida K., Ueda E., Yamanishi K. Kuroki T. (1998) Cholesterol sulfate activates transcription of transglutaminase 1 gene in normal human keratinocytes. J. Invest. Dermatol. 111, 1098 1102.
44. Kim S. Y., Grant P., Lee J. H., Pant H. C. Steinert P. M. (1999) 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, 30715 30721.
45. Kim Y., Park Y. W., Lee Y. S. Jeoung D. (2008) Hyaluronic acid induces transglutaminase II to enhance cell motility; role of Rac1 and FAK in the induction of transglutaminase II. Biotechnol. Lett. 30, 31 39.
46. Konno T., Morii T., Shimizu H., Oiki S. Ikura K. (2005) Paradoxical inhibition of protein aggregation and precipitation by transglutaminase- catalyzed intermolecular cross-linking. J. Biol. Chem. 280, 17520 17525.
47. Krasnikov B. F., Kim S. Y., McConoughey S. J. et al. (2005) Transglutaminase activity is present in highly purified nonsynaptosomal mouse brain and liver mitochondria. Biochemistry 44, 7830 7843.
48. Kuemmerle S., Gutekunst C. A., Klein A. M., Li X. J., Li S. H., Beal M. F., Hersch S. M. Ferrante R. J. (1999) Huntington aggregates may not predict neuronal death in Huntington's disease. Ann. Neurol. 46, 842 849.
49. Kuncio G. S., Tsyganskaya M., Zhu J., Liu S. L., Nagy L., Thomazy V., Davies P. J. A. Zern M. A. (1998) TNF-α modulates expression of the tissue transglutaminase gene in liver cells. Am. J. Physiol. 274, G240 G245.
50. Lai T. S., Tucker T., Burke J. R., Strittmatter W. J. Greenberg C. S. (2004) Effect of tissue transglutaminase on the solubility of proteins containing expanded polyglutamine repeats. J. Neurochem. 88, 1253 1260.
51. Lesort M., Attanavanich K., Zhang J. Johnson G. V. W. (1998) Distinct nuclear localization and activity of tissue transglutaminase. J. Biol. Chem. 273, 11991 11994.
52. Lesort M., Chun W., Johnson G. V. W. Ferrante R. J. (1999) Tissue transglutaminase is increased in Huntington's disease brain. J. Neurochem. 73, 2018 2027.
53. Lesort M., Lee M., Tucholski J. Johnson G. V. W. (2003) Cystamine inhibits caspase activity. Implications for the treatment of polyglutamine disorders. J. Biol. Chem. 278, 3825 3830.
54. Lin M. T. Beal M. F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787 795.
55. Lorand L. Graham R. M. (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140 156.
56. Mastroberardino P. G., Iannicola C., Nardacci R. et al. (2002) 'Tissue' transglutaminase ablation reduces neuronal death and prolongs survival in a mouse model of Huntington's disease. Cell Death Differ. 9, 873 880.
57. Mattson M. P. (2007) Calcium and neurodegeneration. Aging Cell 6, 337 350.
58. Medvedev A., Saunders N. A., Matsuura H., Chistokhina A. Jetten A. M. (1999) Regulation of the transglutaminase I gene. Identification of DNA elements involved in its transcriptional control in tracheobronchial epithelial cells. J. Biol. Chem. 274, 3887 3896.
59. Miller C. C. Anderton B. H. (1986) Transglutaminase and the neuronal cytoskeleton in Alzheimer's disease. J. Neurochem. 46, 1912 1922.
60. Miller M. L. Johnson G. V. W. (1995) Transglutaminase cross-linking of the tau protein. J. Neurochem. 65, 1760 1770.
61. Murthy S. N., Wilson J. H., Lukas T. J., Kuret J. Lorand L. (1998) Cross-linking sites of the human tau protein, probed by reactions with human transglutaminase. J. Neurochem. 71, 2607 2614.
62. Nagy L., Saydak M., Shipley N. et al. (1996) Identification and characterization of a versatile retinoid response element (retinoic acid receptor response element-retinoid X receptor response element) in the mouse tissue transglutaminase gene promoter. J. Biol. Chem. 271, 4355 4365.
63. Nemes Z., Devreese B., Steinert P. M., Van Beeumen J. Fesus L. (2004) Cross-linking of ubiquitin, HSP27, parkin, and alpha-synuclein by γ-glutamyl-ε-lysine bonds in Alzheimer's neurofibrillary tangles. FASEB J. 18, 1135 1137.
64. Pardin C., Pelletier J. N., Lubell W. D. Keillor J. W. (2008a) Cinnamoyl inhibitors of tissue transglutaminase. J. Org. Chem. 73, 5766 5775.
65. Pardin C., Roy I., Lubell W. D. Keillor J. W. (2008b) Reversible and Competitive Cinnamoyl Triazole Inhibitors of Tissue Transglutaminase. Chem. Biol. Drug Des. 72, 189 196.
66. Park K. C., Chung K. C., Kim Y. S., Lee J., Joh T. H. Kim S. Y. (2004) Transglutaminase 2 induces nitric oxide synthesis in BV-2 microglia. Biochem. Biophys. Res. Commun. 323, 1055 1062.
67. Pastuszko A., Wilson D. F. Erecińska M. (1986) A role for transglutaminase in neurotransmitter release by rat brain synaptosomes. J. Neurochem. 46, 499 508.
68. Perry M. J., Mahoney S. A. Haynes L. W. (1995) Transglutaminase C in cerebellar granule neurons: regulation and localization of substrate cross-linking. Neuroscience 65, 1063 1076.
69. Piacentini M., Martinet N., Beninati S. Folk J. E. (1988) Free and protein-conjugated polyamines in mouse epidermal cells. Effect of high calcium and retinoic acid. J. Biol. Chem. 263, 3790 3794.
70. Pinto J. T., Van Raamsdonk J. M., Leavitt B. R., Hayden M. R., Jeitner T. M., Thaler H. T., Krasnikov B. F. Cooper A. J. L. (2005) Treatment of YAC128 mice and their wild-type littermates with cystamine does not lead to its accumulation in plasma or brain: implications for the treatment of Huntington disease. J. Neurochem. 94, 1087 1101.
71. Polakowska R. R., Graf B. A., Falciano V. LaCelle P. (1999) Transcription regulatory elements of the first intron control human transglutaminase type I gene expression in epidermal keratinocytes. J. Cell. Biochem. 73, 355 369.
72. Rasmussen L. K., Sorensen E. S., Petersen T. E., Gliemann J. Jensen P. H. (1994) Identification of glutamine and lysine residues in Alzheimer amyloid beta A4 peptide responsible for transglutaminase-catalysed homopolymerization and cross-linking to α 2M receptor. FEBS Lett. 338, 161 166.
73. Ritter S. J. Davies P. J. A. (1998) Identification of a transforming growth factor-beta1/bone morphogenetic protein 4 (TGF-beta1/BMP4) response element within the mouse tissue transglutaminase gene promoter. J. Biol. Chem. 273, 12798 12806.
74. Sárvari M., Karpati L., Fésüs L., Deli L., Muszbek L. Nemes Z. (2002) Competitive enzyme-linked immunosorbent assay for N εγ-glutamyl lysine. Anal. Biochem. 311, 187 190.
75. Selkoe D. J., Abraham C. Ihara Y. (1982a) Brain transglutaminase: in vitro crosslinking of human neurofilament proteins into insoluble polymers. Proc. Natl Acad. Sci. USA 79, 6070 6074.
76. Selkoe D. J., Ihara Y. Salazar F. J. (1982b) Alzheimer's disease: insolubility of partially purified paired helical filaments in sodium dodecyl sulfate and urea. Science 215, 1243 1245.
77. Sieradzan K. A. Mann D. M. (2001) The selective vulnerability of nerve cells in Huntington's disease. Neuropathol. Appl. Neurobiol. 27, 1 21.
78. Sohn J., Kim T. I., Yoon Y. H., Kim J. Y. Kim S. Y. (2003) Novel transglutaminase inhibitors reverse the inflammation of allergic conjunctivitis. J. Clin. Invest. 111, 121 128.
79. Stack E. C., Ferro J. L., Kim J. et al. (2008) Therapeutic attenuation of mitochondrial dysfunction and oxidative stress in neurotoxin models of Parkinson's disease. Biochim. Biophys. Acta 1782, 151 162.
80. Tucholski J., Kuret J. Johnson G. V. W. (1999) Tau is modified by tissue transglutaminase in situ: possible functional and metabolic effects of polyamination. J. Neurochem. 73, 1871 1880.
81. Van Raamsdonk J. M., Pearson J., Bailey C. D., Rogers D. A., Johnson G. V. W., Hayden M. R. Leavitt B. R. (2005) Cystamine treatment is neuroprotective in the YAC128 mouse model of Huntington disease. J. Neurochem. 95, 210 220.
82. Vermes I., Steur E. N., Jirikowski G. F. Haanen C. (2004) Elevated concentration of cerebrospinal fluid tissue transglutaminase in Parkinson's disease indicating apoptosis. Mov. Disord. 19, 1252 1254.
83. Wang J., Wang C. E., Orr A., Tydlacka S., Li S. H. Li X. J. (2008) Impaired ubiquitin-proteasome system activity in the synapses of Huntington's disease mice. J. Cell Biol. 180, 1177 1189.
84. Yan Z. H., Noonan S., Nagy L., Davies P. J. A. Stein J. P. (1996) Retinoic acid induction of the tissue transglutaminase promoter is mediated by a novel response element. Mol. Cell. Endocrinol. 120, 203 212.
85. Zainelli G. M., Ross C. A., Troncoso J. C. Muma N. A. (2003) Transglutaminase cross-links in intranuclear inclusions in Huntington disease. J. Neuropathol. Exp. Neurol. 62, 14 24.
86. Zainelli G. M., Dudek N. L., Ross C. A., Kim S. Y. Muma N. A. (2005) Mutant huntingtin protein: a substrate for transglutaminase 1, 2, and 3. J. Neuropathol. Exp. Neurol. 64, 58 65.
87. Zemaitaitis M. O., Lee J. M., Troncoso J. C. Muma N. A. (2000) Transglutaminase-induced cross-linking of tau proteins in progressive supranuclear palsy. J. Neuropathol. Exp. Neurol. 59, 983 989.
88. Zemaitaitis M. O., Kim S. Y., Halverson R. A., Troncoso J. C., Lee J. M. Muma N. A. (2003) Transglutaminase activity, protein, and mRNA expression are increased in progressive supranuclear palsy. J. Neuropathol. Exp. Neurol. 62, 173 184.
89. Zhang W., Johnson B. R., Suri D. E., Martinez J. Bjornsson T. D. (1998) Immunohistochemical demonstration of tissue transglutaminase in amyloid plaques. Acta Neuropathol. 96, 395 400.