Transglutaminase 1 and its regulator tazarotene-induced gene 3 localize to neuronal tau inclusions in tauopathies

Journal of Pathology

Volumn 226, Issue 1, 2012, Pages 132-142

  Wilhelmus, Micha M M ^a   De Jager, Mieke ^a   Rozemuller, Annemieke J M ^a   Brevé, John ^a   Bol, John G J M ^a   Eckert, Richard L ^b   Drukarch, Benjamin ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

neurodegeneration; neurofibrillary tangles; tauopathies; tazarotene induced gene 3; transglutaminase 1; transglutaminase 2

Indexed keywords

PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 1; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; TAU PROTEIN; TAZAROTENE INDUCED GENE 3; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ADULT; ALZHEIMER DISEASE; ARTICLE; CATALYSIS; CELL INCLUSION; CONTROLLED STUDY; DENTATE NUCLEUS; ENZYME ACTIVITY; ENZYME MECHANISM; FEMALE; GENE LOCATION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MIDDLE FRONTAL GYRUS; NEOCORTEX; NERVE CELL; NEUROFIBRILLARY TANGLE; PARKINSONISM; PARKINSONISM LINKED TO CHROMOSOME 17; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SUBSTANTIA NIGRA; TAUOPATHY; THALAMUS;

AGED; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; MALE; MIDDLE AGED; NEURONS; RECEPTORS, RETINOIC ACID; TAU PROTEINS; TAUOPATHIES; TRANSGLUTAMINASES;

EID: 82755197141     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2984     Document Type: Article

References (46)

1. Brion JP, Flament-Durand J, Dustin P,. Alzheimer's disease and tau proteins. Lancet 1986; 2: 1098. (Pubitemid 17173976)
2. Grundke-Iqbal I, Iqbal K, Quinlan M, et al., Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 1986; 261: 6084-6089. (Pubitemid 17207447)
3. Mandelkow EM, Mandelkow E,. Tau in Alzheimer's disease. Trends Cell Biol 1998; 8: 425-427. (Pubitemid 28529713)
4. Nukina N, Ihara Y,. One of the antigenic determinants of paired helical filaments is related to tau protein. J Biochem 1986; 99: 1541-1544.
5. Yoshida M,. Cellular tau pathology and immunohistochemical study of tau isoforms in sporadic tauopathies. Neuropathology 2006; 26: 457-470. (Pubitemid 44454419)
6. Goedert M, Spillantini MG, Jakes R, et al., Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989; 3: 519-526.
7. Goedert M,. Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci 1993; 16: 460-465. (Pubitemid 23313524)
8. Biernat J, Mandelkow EM, Schroter C, et al., The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO J 1992; 11: 1593-1597.
9. Trojanowski JQ, Lee VM,. Phosphorylation of paired helical filament tau in Alzheimer's disease neurofibrillary lesions: focusing on phosphatases. FASEB J 1995; 9: 1570-1576. (Pubitemid 26012845)
10. Kowall NW, Kosik KS,. Axonal disruption and aberrant localization of tau protein characterize the neuropil pathology of Alzheimer's disease. Ann Neurol 1987; 22: 639-643. (Pubitemid 17162909)
11. Norlund MA, Lee JM, Zainelli GM, et al., Elevated transglutaminase- induced bonds in PHF tau in Alzheimer's disease. Brain Res 1999; 851: 154-163. (Pubitemid 30038140)
12. Singer SM, Zainelli GM, Norlund MA, et al., Transglutaminase bonds in neurofibrillary tangles and paired helical filament tau early in Alzheimer's disease. Neurochem Int 2002; 40: 17-30. (Pubitemid 34003555)
13. Zainelli GM, Ross CA, Troncoso JC, et al., Transglutaminase cross-links in intranuclear inclusions in Huntington disease. J Neuropathol Exp Neurol 2003; 62: 14-24. (Pubitemid 36068889)
14. Yan SD, Chen X, Schmidt AM, et al., Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc Natl Acad Sci U S A 1994; 91: 7787-7791. (Pubitemid 24238270)
15. Kim SY, Grant P, Lee JH, et al., 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 1999; 274: 30 715-30 721.
16. Eckert RL, Sturniolo MT, Broome AM, et al., Transglutaminase function in epidermis. J Invest Dermatol 2005; 124: 481-492. (Pubitemid 40381569)
17. Fesus L,. Biochemical events in naturally occurring forms of cell death. FEBS Lett 1993; 328: 1-5. (Pubitemid 23234752)
18. Wilhelmus MM, van Dam AM, Drukarch B,. Tissue transglutaminase: a novel pharmacological target in preventing toxic protein aggregation in neurodegenerative diseases. Eur J Pharmacol 2008; 585: 464-472.
19. Lorand L, Conrad SM,. Transglutaminases. Mol Cell Biochem 1984; 58: 9-35.
20. Muma NA,. Transglutaminase is linked to neurodegenerative diseases. J Neuropathol Exp Neurol 2007; 66: 258-263. (Pubitemid 46559018)
21. Segers-Nolten I, Wilhelmus MM, Veldhuis G, et al., Tissue transglutaminase modulates α-synuclein oligomerization. Protein Sci 2008; 17: 1395-1402.
22. Wilhelmus MM, Verhaar R, Andringa G, et al., Presence of tissue transglutaminase in granular endoplasmic reticulum is characteristic of melanized neurons in Parkinson's disease brain. Brain Pathol 2011; 21: 130-139.
23. Wilhelmus MM, Grunberg SC, Bol JG, et al., Transglutaminases and transglutaminase-catalyzed cross-links colocalize with the pathological lesions in Alzheimer's disease brain. Brain Pathol 2008; 19: 612-622.
24. Dudek SM, Johnson GV,. Transglutaminase catalyzes the formation of sodium dodecyl sulfate-insoluble, Alz-50-reactive polymers of tau. J Neurochem 1993; 61: 1159-1162. (Pubitemid 23241261)
25. Dudek SM, Johnson GV,. Transglutaminase facilitates the formation of polymers of the beta-amyloid peptide. Brain Res 1994; 651: 129-133. (Pubitemid 24222858)
26. Wilhelmus MM, Verhaar R, Bol JG, et al., Novel role of transglutaminase 1 in corpora amylacea formation? Neurobiol Aging 2011; 32: 845-856.
27. Verhaar R, Jongenelen CA, Gerard M, et al., Blockade of enzyme activity inhibits tissue transglutaminase-mediated transamidation of alpha-synuclein in a cellular model of Parkinson's disease. Neurochem Int 2011; 58: 785-793.
28. DiSepio D, Ghosn C, Eckert RL, et al., Identification and characterization of a retinoid-induced class II tumor suppressor/growth regulatory gene. Proc Natl Acad Sci U S A 1998; 95: 14 811-14 815.
29. Jans R, Sturniolo MT, Eckert RL,. Localization of the TIG3 transglutaminase interaction domain and demonstration that the amino-terminal region is required for TIG3 function as a keratinocyte differentiation regulator. J Invest Dermatol 2008; 128: 517-529. (Pubitemid 351252649)
30. Sturniolo MT, Dashti SR, Deucher A, et al., A novel tumor suppressor protein promotes keratinocyte terminal differentiation via activation of type I transglutaminase. J Biol Chem 2003; 278: 48 066-48 073.
31. Sturniolo MT, Chandraratna RA, Eckert RL,. A novel transglutaminase activator forms a complex with type 1 transglutaminase. Oncogene 2005; 24: 2963-2972. (Pubitemid 40675527)
32. Mirra SS, Heyman A, McKeel D, et al., The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991; 41: 479-486.
33. Halverson RA, Lewis J, Frausto S, et al., Tau protein is cross-linked by transglutaminase in P301L tau transgenic mice. J Neurosci 2005; 25: 1226-1233. (Pubitemid 40268965)
34. Johnson TS, El-Koraie AF, Skill NJ, et al., Tissue transglutaminase and the progression of human renal scarring. J Am Soc Nephrol 2003; 14: 2052-2062. (Pubitemid 36909913)
35. Sakai M, Austin J, Witmer F, et al., Studies of corpora amylacea. I. Isolation and preliminary characterization by chemical and histochemical techniques. Arch Neurol 1969; 21: 526-544.
36. Zemaitaitis MO, Kim SY, Halverson RA, et al., Transglutaminase activity, protein, and mRNA expression are increased in progressive supranuclear palsy. J Neuropathol Exp Neurol 2003; 62: 173-184. (Pubitemid 36176952)
37. Vandrovcova J, Anaya F, Kay V, et al., Disentangling the role of the tau gene locus in sporadic tauopathies. Curr Alzheimer Res 2010; 7: 726-734.
38. Kovari E,. Neuropathological spectrum of frontal lobe dementias. Front Neurol Neurosci 2009; 24: 149-159.
39. Buee L, Delacourte A,. Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick's disease. Brain Pathol 1999; 9: 681-693. (Pubitemid 29470961)
40. Eckert RL, Sturniolo MT, Jans R, et al., TIG3: a regulator of type I transglutaminase activity in epidermis. Amino Acids 2009; 36: 739-746.
41. Schmidt ML, Huang R, Martin JA, et al., Neurofibrillary tangles in progressive supranuclear palsy contain the same tau epitopes identified in Alzheimer's disease PHFtau. J Neuropathol Exp Neurol 1996; 55: 534-539. (Pubitemid 26140836)
42. Avila J, Lucas JJ, Perez M, et al., Role of tau protein in both physiological and pathological conditions. Physiol Rev 2004; 84: 361-384. (Pubitemid 38365487)
43. Ientile R, Caccamo D, Griffin M,. Tissue transglutaminase and the stress response. Amino Acids 2007; 33: 385-394. (Pubitemid 47222963)
44. Hardy JA, Higgins GA,. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992; 256: 184-185.
45. Cavanagh JB,. Corpora-amylacea and the family of polyglucosan diseases. Brain Res Brain Res Rev 1999; 29: 265-295. (Pubitemid 29191343)
46. Deucher A, Nagpal S, Chandraratna RA, et al., The carboxy-terminal hydrophobic domain of TIG3, a class II tumor suppressor protein, is required for appropriate cellular localization and optimal biological activity. Int J Oncol 2000; 17: 1195-1203.