Tissue transglutaminase colocalizes with extracellular matrix proteins in cerebral amyloid angiopathy

Neurobiology of Aging

Volumn 34, Issue 4, 2013, Pages 1159-1169

  De Jager, Mieke ^a   van der Wildt, Berend ^a   Schul, Emma ^a   Bol, John G J M ^a   van Duinen, Sjoerd G ^b   Drukarch, Benjamin ^a   Wilhelmus, Micha M M ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Alzheimer's disease; Cerebral amyloid angiopathy; Extracellular matrix proteins; Hereditary cerebral hemorrhages with amyloidosis of the Dutch type; Tissue transglutaminase

Indexed keywords

AMYLOID BETA PROTEIN; FIBRONECTIN; LAMININ; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOIDOSIS; ARTICLE; ASTROCYTE; BRAIN HEMORRHAGE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ENDOTHELIUM; ENZYME ACTIVITY; FEMALE; HEREDITARY CEREBRAL HEMORRHAGE WITH AMYLOIDOSIS OF THE DUTCH TYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; LEPTOMENINX; MALE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TISSUE LEVEL; VASCULAR AMYLOIDOSIS;

AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOIDOSIS, FAMILIAL; CEREBRAL AMYLOID ANGIOPATHY; CEREBRAL ARTERIES; CEREBRAL HEMORRHAGE; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GTP-BINDING PROTEINS; HUMANS; MALE; MIDDLE AGED; TISSUE DISTRIBUTION; TRANSGLUTAMINASES;

EID: 84872335309     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.10.005     Document Type: Article

References (67)

1. Appelt D.M., Kopen G.C., Boyne L.J., Balin B.J. Localization of transglutaminase in hippocampal neurons: implications for Alzheimer's disease. J. Histochem. Cytochem. 1996, 44:1421-1427.
2. Attems J., Jellinger K., Thal D.R., Van Nostrand W. Review: sporadic cerebral amyloid angiopathy. Neuropathol. Appl. Neurobiol. 2011, 37:75-93.
3. Bakker E.N., Buus C.L., Spaan J.A., Perree J., Ganga A., Rolf T.M., Sorop O., Bramsen L.H., Mulvany M.J., VanBavel E. Small artery remodeling depends on tissue-type transglutaminase. Circ. Res. 2005, 96:119-126.
4. Bakker E.N., Pistea A., VanBavel E. Transglutaminases in vascular biology: relevance for vascular remodeling and atherosclerosis. J. Vasc. Res. 2008, 45:271-278.
5. Boros S., Ahrman E., Wunderink L., Kamps B., de Jong W.W., Boelens W.C., Emanuelsson C.S. Site-specific transamidation and deamidation of the small heat-shock protein Hsp20 by tissue transglutaminase. Proteins 2006, 62:1044-1052.
6. Braak H., Alafuzoff I., Arzberger T., Kretzschmar H., Del T.K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006, 112:389-404.
7. Colognato H., Yurchenco P.D. Form and function: the laminin family of heterotrimers. Dev. Dyn. 2000, 218:213-234.
8. Curro M., Ferlazzo N., Condello S., Caccamo D., Ientile R. Transglutaminase 2 silencing reduced the beta-amyloid-effects on the activation of human THP-1 cells. Amino Acids 2010, 39:1427-1433.
9. Dudek S.M., Johnson G.V. Transglutaminase facilitates the formation of polymers of the beta-amyloid peptide. Brain Res. 1994, 651:129-133.
10. Fesus L., Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci. 2002, 27:534-539.
11. Franke W.W., Schmid E., Osborn M., Weber K. Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc. Natl. Acad. Sci. U. S. A. 1978, 75:5034-5038.
12. Girma J.P., Meyer D., Verweij C.L., Pannekoek H., Sixma J.J. Structure-function relationship of human von Willebrand factor. Blood 1987, 70:605-611.
13. Greenberg C.S., Birckbichler P.J., Rice R.H. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J. 1991, 5:3071-3077.
14. Greenberg S.M., Gurol M.E., Rosand J., Smith E.E. Amyloid angiopathy-related vascular cognitive impairment. Stroke 2004, 35:2616-2619.
15. Griffin M., Casadio R., Bergamini C.M. Transglutaminases: nature's biological glues. Biochem. J. 2002, 368:377-396.
16. Hartley D.M., Zhao C., Speier A.C., Woodard G.A., Li S., Li Z., Walz T. Transglutaminase induces protofibril-like amyloid beta-protein assemblies that are protease-resistant and inhibit long-term potentiation. J. Biol. Chem. 2008, 283:16790-16800.
17. Heneka M.T., O'Banion M.K., Terwel D., Kummer M.P. Neuroinflammatory processes in Alzheimer's disease. J. Neural Transm. 2010, 117:919-947.
18. Ientile R., Caccamo D., Griffin M. Tissue transglutaminase and the stress response. Amino Acids 2007, 33:385-394.
19. Ikura K., Takahata K., Sasaki R. Cross-linking of a synthetic partial-length (1-28) peptide of the Alzheimer beta/A4 amyloid protein by transglutaminase. FEBS Lett. 1993, 326:109-111.
20. Jaffe E.A., Hoyer L.W., Nachman R.L. Synthesis of von Willebrand factor by cultured human endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 1974, 71:1906-1909.
21. Jellinger K.A., Attems J. Prevalence and pathogenic role of cerebrovascular lesions in Alzheimer disease. J. Neurol. Sci. 2005, 229-230:37-41.
22. Jeon W.M., Lee K.N., Birckbichler P.J., Conway E., Patterson M.K. Colorimetric assay for cellular transglutaminase. Anal. Biochem. 1989, 182:170-175.
23. Jin X., Stamnaes J., Klock C., DiRaimondo T.R., Sollid L.M., Khosla C. Activation of extracellular transglutaminase 2 by thioredoxin. J. Biol. Chem. 2011, 286:37866-37873.
24. Johnson G.V., Cox T.M., Lockhart J.P., Zinnerman M.D., Miller M.L., Powers R.E. Transglutaminase activity is increased in Alzheimer's disease brain. Brain Res. 1997, 751:323-329.
25. Kalaria R.N. Cerebral vessels in ageing and Alzheimer's disease. Pharmacol. Ther. 1996, 72:193-214.
26. Kim S.Y., Grant P., Lee J.H., Pant H.C., 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. 1999, 274:30715-30721.
27. Lee K.N., Birckbichler P.J., Patterson M.K. Colorimetric assay of blood coagulation factor XIII in plasma. Clin. Chem. 1988, 34:906-910.
28. Lorand L., Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 2003, 4:140-156.
29. Maat-Schieman M., Roos R., van Duinen S. Hereditary cerebral hemorrhage with amyloidosis-Dutch type. Neuropathology 2005, 25:288-297.
30. Miners J.S., Ashby E., Van H.Z., Chalmers K.A., Palmer L.E., Love S., Kehoe P.G. Angiotensin-converting enzyme (ACE) levels and activity in Alzheimer's disease, and relationship of perivascular ACE-1 to cerebral amyloid angiopathy. Neuropathol. Appl. Neurobiol. 2008, 34:181-193.
31. Nurminskaya M.V., Belkin A.M. Cellular functions of tissue transglutaminase. Int. Rev. Cell Mol. Biol. 2012, 294:1-97.
32. Perlmutter L.S. Microvascular pathology and vascular basement membrane components in Alzheimer's disease. Mol. Neurobiol. 1994, 9:33-40.
33. Perlmutter L.S., Chui H.C. Microangiopathy, the vascular basement membrane and Alzheimer's disease: a review. Brain Res. Bull. 1990, 24:677-686.
34. Pinkas D.M., Strop P., Brunger A.T., Khosla C. Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol. 2007, 5:e327.
35. Rasmussen L.K., Sorensen E.S., Petersen T.E., Gliemann J., Jensen P.H. Identification of glutamine and lysine residues in Alzheimer amyloid beta A4 peptide responsible for transglutaminase-catalysed homopolymerization and cross-linking to alpha 2M receptor. FEBS Lett. 1994, 338:161-166.
36. Santhanam L., Tuday E.C., Webb A.K., Dowzicky P., Kim J.H., Oh Y.J., Sikka G., Kuo M., Halushka M.K., Macgregor A.M., Dunn J., Gutbrod S., Yin D., Shoukas A., Nyhan D., Flavahan N.A., Belkin A.M., Berkowitz D.E. Decreased S-nitrosylation of tissue transglutaminase contributes to age-related increases in vascular stiffness. Circ. Res. 2010, 107:117-125.
37. Sárvári M.á., Fésüs L.á., Nemes Z. Transglutaminase-mediated crosslinking of neural proteins in Alzheimer's disease and other primary dementias. Drug Dev. Res. 2002, 56:458-472.
38. Schaertl S., Prime M., Wityak J., Dominguez C., Munoz-Sanjuan I., Pacifici R.E., Courtney S., Scheel A., Macdonald D. A profiling platform for the characterization of transglutaminase 2 (TG2) inhibitors. J. Biomol. Screen 2010, 15:478-487.
39. Schley D., Carare-Nnadi R., Please C.P., Perry V.H., Weller R.O. Mechanisms to explain the reverse perivascular transport of solutes out of the brain. J. Theor. Biol. 2006, 238:962-974.
40. Schmid A.W., Condemi E., Tuchscherer G., Chiappe D., Mutter M., Vogel H., Moniatte M., Tsybin Y.O. Tissue transglutaminase-mediated glutamine deamidation of beta-amyloid peptide increases peptide solubility, whereas enzymatic cross-linking and peptide fragmentation may serve as molecular triggers for rapid peptide aggregation. J. Biol. Chem. 2011, 286:12172-12188.
41. Selkoe D.J. Cell biology of the amyloid beta-protein precursor and the mechanism of Alzheimer's disease. Annu. Rev. Cell Biol. 1994, 10:373-403.
42. Skalli O., Vandekerckhove J., Gabbiani G. Actin-isoform pattern as a marker of normal or pathological smooth-muscle and fibroblastic tissues. Differentiation 1987, 33:232-238.
43. Skill N.J., Johnson T.S., Coutts I.G., Saint R.E., Fisher M., Huang L., El Nahas A.M., Collighan R.J., Griffin M. Inhibition of transglutaminase activity reduces extracellular matrix accumulation induced by high glucose levels in proximal tubular epithelial cells. J. Biol. Chem. 2004, 279:47754-47762.
44. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
45. Stenman S., Vaheri A. Distribution of a major connective tissue protein, fibronectin, in normal human tissues. J. Exp. Med. 1978, 147:1054-1064.
46. Thal D.R., Ghebremedhin E., Rub U., Yamaguchi H., Del T.K., Braak H. Two types of sporadic cerebral amyloid angiopathy. J. Neuropathol. Exp. Neurol. 2002, 61:282-293.
47. Thal D.R., Rub U., Orantes M., Braak H. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 2002, 58:1791-1800.
48. Thomazy V., Fesus L. Differential expression of tissue transglutaminase in human cells. An immunohistochemical study. Cell Tissue Res. 1989, 255:215-224.
49. van den Akker J., van Weert A., Afink G., Bakker E.N., van der Pol E., Boing A.N., Nieuwland R., VanBavel E. Transglutaminase 2 is secreted from smooth muscle cells by transamidation-dependent microparticle formation. Amino Acids 2012, 42:961-973.
50. van Duinen S.G., Maat-Schieman M.L., Bruijn J.A., Haan J., Roos R.A. Cortical tissue of patients with hereditary cerebral hemorrhage with amyloidosis (Dutch) contains various extracellular matrix deposits. Lab. Invest. 1995, 73:183-189.
51. Verderio E.A., Scarpellini A., Johnson T.S. Novel interactions of TG2 with heparan sulfate proteoglycans: reflection on physiological implications. Amino Acids 2009, 36:671-677.
52. Walsh D.M., Hartley D.M., Kusumoto Y., Fezoui Y., Condron M.M., Lomakin A., Benedek G.B., Selkoe D.J., Teplow D.B. Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 1999, 274:25945-25952.
53. Wang D.S., Dickson D.W., Malter J.S. Tissue transglutaminase, protein cross-linking and Alzheimer's disease: review and views. Int. J. Clin. Exp. Pathol. 2008, 1:5-18.
54. Wang D.S., Uchikado H., Bennett D.A., Schneider J.A., Mufson E.J., Wu J., Dickson D.W. Cognitive performance correlates with cortical isopeptide immunoreactivity as well as Alzheimer type pathology. J. Alzheimers Dis. 2008, 13:53-66.
55. Weller R.O., Preston S.D., Subash M., Carare R.O. Cerebral amyloid angiopathy in the aetiology and immunotherapy of Alzheimer disease. Alzheimers Res. Ther. 2009, 1:6.
56. Wilhelmus M.M., de Jager M., Drukarch B. Tissue transglutaminase: a novel therapeutic target in cerebral amyloid angiopathy. Neurodegener. Dis. 2012, 10:317-319.
57. Wilhelmus M.M., de Waal R.M., Verbeek M.M. Heat shock proteins and amateur chaperones in amyloid-beta accumulation and clearance in Alzheimer's disease. Mol. Neurobiol. 2007, 35:203-216.
58. Wilhelmus M.M., Grunberg S.C., Bol J.G., van Dam A.M., Hoozemans J.J., Rozemuller A.J., Drukarch B. Transglutaminases and transglutaminase-catalyzed cross-links colocalize with the pathological lesions in Alzheimer's disease brain. Brain Pathol. 2009, 19:612-622.
59. Wilhelmus M.M., Otte-Holler I., Wesseling P., de Waal R.M., Boelens W.C., Verbeek M.M. Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer's disease brains. Neuropathol. Appl. Neurobiol. 2006, 32:119-130.
60. Wilhelmus M.M., van Dam A.M., Drukarch B. Tissue transglutaminase: a novel pharmacological target in preventing toxic protein aggregation in neurodegenerative diseases. Eur. J. Pharmacol. 2008, 585:464-472.
61. Wilhelmus M.M., Verhaar R., Andringa G., Bol J.G., Cras P., Shan L., Hoozemans J.J., Drukarch B. Presence of tissue transglutaminase in granular endoplasmic reticulum is characteristic of melanized neurons in Parkinson's disease brain. Brain Pathol. 2011, 21:130-139.
62. Wilhelmus M.M., Verhaar R., Bol J.G., van Dam A.M., Hoozemans J.J., Rozemuller A.J., Drukarch B. Novel role of transglutaminase 1 in corpora amylacea formation?. Neurobiol. Aging 2011, 32:845-856.
63. Wisniewski H.M., Vorbrodt A.W., Wegiel J. Amyloid angiopathy and blood-brain barrier changes in Alzheimer's disease. Ann. N. Y. Acad. Sci. 1997, 826:161-172.
64. Yamada T., Yoshiyama Y., Kawaguchi N., Ichinose A., Iwaki T., Hirose S., Jefferies W.A. Possible roles of transglutaminases in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 1998, 9:103-110.
65. Zemskov E.A., Janiak A., Hang J., Waghray A., Belkin A.M. The role of tissue transglutaminase in cell-matrix interactions. Front. Biosci. 2006, 11:1057-1076.
66. Zhang W.W., Lempessi H., Olsson Y. Amyloid angiopathy of the human brain: immunohistochemical studies using markers for components of extracellular matrix, smooth muscle actin and endothelial cells. Acta Neuropathol. 1998, 96:558-563.
67. Zipfel G.J., Han H., Ford A.L., Lee J.M. Cerebral amyloid angiopathy: progressive disruption of the neurovascular unit. Stroke 2009, 40:S16-S19.