Transglutaminase 2: A molecular Swiss army knife

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 2, 2012, Pages 406-419

  Gundemir, Soner ^a   Colak, Gozde ^a   Tucholski, Janusz ^b   Johnson, Gail V W ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Calcium; Cell death; GTP; Transamidase; Transcription regulation; Transglutaminase 2

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; CYCLOSPORIN A; CYSTEINE; FOCAL ADHESION KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; NITRIC OXIDE; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN DISULFIDE ISOMERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN BINDING PROTEIN 3;

CALCIUM BINDING; CATALYST; CELL ADHESION; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL SURFACE; CELL SURVIVAL; CRYSTALLOGRAPHY; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUNTINGTON CHOREA; IC 50; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; UPREGULATION; WILD TYPE;

ANIMALS; CATALYTIC DOMAIN; CELL PROLIFERATION; CELL SURVIVAL; GENE DUPLICATION; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION, GENETIC; TRANSGLUTAMINASES;

EID: 84855787788     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.09.012     Document Type: Review

References (172)

1. Griffin M., Casadio R., Bergamini C.M. Transglutaminases: nature's biological glues. Biochem. J. 2002, 368:377-396.
2. Lai T.S., Slaughter T.F., Peoples K.A., Hettasch J.M., Greenberg C.S. Regulation of human tissue transglutaminase function by magnesium-nucleotide complexes. Identification of distinct binding sites for Mg-GTP and Mg-ATP. J. Biol. Chem. 1998, 273:1776-1781.
3. Begg G.E., Carrington L., Stokes P.H., Matthews J.M., Wouters M.A., Husain A., Lorand L., Iismaa S.E., Graham R.M. Mechanism of allosteric regulation of transglutaminase 2 by GTP. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:19683-19688.
4. Chen J.S., Mehta K. Tissue transglutaminase: an enzyme with a split personality. Int. J. Biochem. Cell Biol. 1999, 31:817-836.
5. Baek K.J., Kwon N.S., Lee H.S., Kim M.S., Muralidhar P., Im M.J. Oxytocin receptor couples to the 80 kDa Gh alpha family protein in human myometrium. Biochem. J. 1996, 315(Pt 3):739-744.
6. Nakaoka H., Perez D.M., Baek K.J., Das T., Husain A., Misono K., Im M.J., Graham R.M. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 1994, 264:1593-1596.
7. Vezza R., Habib A., FitzGerald G.A. Differential signaling by the thromboxane receptor isoforms via the novel GTP-binding protein, Gh. J. Biol. Chem. 1999, 274:12774-12779.
8. Hasegawa G., Suwa M., Ichikawa Y., Ohtsuka T., Kumagai S., Kikuchi M., Sato Y., Saito Y. A novel function of tissue-type transglutaminase: protein disulphide isomerase. Biochem. J. 2003, 373:793-803.
9. Mastroberardino P.G., Farrace M.G., Viti I., Pavone F., Fimia G.M., Melino G., Rodolfo C., Piacentini M. "Tissue" transglutaminase contributes to the formation of disulphide bridges in proteins of mitochondrial respiratory complexes. Biochim. Biophys. Acta 2006, 1757:1357-1365.
10. Mishra S., Murphy L.J. Tissue transglutaminase has intrinsic kinase activity: identification of transglutaminase 2 as an insulin-like growth factor-binding protein-3 kinase. J. Biol. Chem. 2004, 279:23863-23868.
11. Mishra S., Saleh A., Espino P.S., Davie J.R., Murphy L.J. Phosphorylation of histones by tissue transglutaminase. J. Biol. Chem. 2006, 281:5532-5538.
12. Akimov S.S., Belkin A.M. Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatin-binding domain of fibronectin: a role in TGFbeta-dependent matrix deposition. J. Cell Sci. 2001, 114:2989-3000.
13. Akimov S.S., Belkin A.M. Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 2001, 98:1567-1576.
14. Takeuchi Y., Ohashi H., Birckbichler P.J., Ikejima T. Nuclear translocation of tissue type transglutaminase during sphingosine-induced cell death: a novel aspect of the enzyme with DNA hydrolytic activity. Z. Naturforsch. C 1998, 53:352-358.
15. Satchwell T.J., Shoemark D.K., Sessions R.B., Toye A.M. Protein 4.2: a complex linker. Blood Cells Mol. Dis. 2009, 42:201-210.
16. Lorand L., Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 2003, 4:140-156.
17. Grenard P., Bates M.K., Aeschlimann D. Evolution of transglutaminase genes: identification of a transglutaminase gene cluster on human chromosome 15q15. Structure of the gene encoding transglutaminase X and a novel gene family member, transglutaminase Z. J. Biol. Chem. 2001, 276:33066-33078.
18. Polakowska R.R., Eickbush T., Falciano V., Razvi F., Goldsmith L.A. Organization and evolution of the human epidermal keratinocyte transglutaminase I gene. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:4476-4480.
19. Yokoyama K., Nio N., Kikuchi Y. Properties and applications of microbial transglutaminase. Appl. Microbiol. Biotechnol. 2004, 64:447-454.
20. Vogel C., Morea V. Duplication, divergence and formation of novel protein topologies. Bioessays 2006, 28:973-978.
21. Soskine M., Tawfik D.S. Mutational effects and the evolution of new protein functions. Nat. Rev. Genet. 2010, 11:572-582.
22. Sarkar N.K., Clarke D.D., Waelsch H. An enzymically catalyzed incorporation of amines into proteins. Biochim. Biophys. Acta 1957, 25:451-452.
23. Lichti U., Ben T., Yuspa S.H. Retinoic acid-induced transglutaminase in mouse epidermal cells is distinct from epidermal transglutaminase. J. Biol. Chem. 1985, 260:1422-1426.
24. Folk J.E. Mechanism and basis for specificity of transglutaminase-catalyzed epsilon-(gamma-glutamyl) lysine bond formation. Adv. Enzymol. Relat. Areas Mol. Biol. 1983, 54:1-56.
25. Nicholas B., Smethurst P., Verderio E., Jones R., Griffin M. Cross-linking of cellular proteins by tissue transglutaminase during necrotic cell death: a mechanism for maintaining tissue integrity. Biochem. J. 2003, 371:413-422.
26. Fesus L., Madi A., Balajthy Z., Nemes Z., Szondy Z. Transglutaminase induction by various cell death and apoptosis pathways. Experientia 1996, 52:942-949.
27. Fleckenstein B., Molberg O., Qiao S.W., Schmid D.G., von der Mulbe F., Elgstoen K., Jung G., 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. 2002, 277:34109-34116.
28. 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.
29. Stamnaes J., Fleckenstein B., Sollid L.M. The propensity for deamidation and transamidation of peptides by transglutaminase 2 is dependent on substrate affinity and reaction conditions. Biochim. Biophys. Acta 2008, 1784:1804-1811.
30. Pinkas D.M., Strop P., Brunger A.T., Khosla C. Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol. 2007, 5:e327.
31. Achyuthan K.E., Greenberg C.S. Identification of a guanosine triphosphate-binding site on guinea pig liver transglutaminase. Role of GTP and calcium ions in modulating activity. J. Biol. Chem. 1987, 262:1901-1906.
32. Zhang J., Tucholski J., Lesort M., Jope R.S., Johnson G.V. Novel bimodal effects of the G-protein tissue transglutaminase on adrenoreceptor signalling. Biochem. J. 1999, 343(Pt 3):541-549.
33. Nanda N., Iismaa S.E., Owens W.A., Husain A., Mackay F., Graham R.M. Targeted inactivation of Gh/tissue transglutaminase II. J. Biol. Chem. 2001, 276:20673-20678.
34. Lai T.S., Liu Y., Li W., Greenberg C.S. Identification of two GTP-independent alternatively spliced forms of tissue transglutaminase in human leukocytes, vascular smooth muscle, and endothelial cells. FASEB J. 2007, 21:4131-4143.
35. Datta S., Antonyak M.A., Cerione R.A. Importance of Ca(2+)-dependent transamidation activity in the protection afforded by tissue transglutaminase against doxorubicin-induced apoptosis. Biochemistry 2006, 45:13163-13174.
36. Gundemir S., Johnson G.V. Intracellular localization and conformational state of transglutaminase 2: implications for cell death. PLoS One 2009, 4:e6123.
37. Antonyak M.A., Jansen J.M., Miller A.M., Ly T.K., Endo M., Cerione R.A. Two isoforms of tissue transglutaminase mediate opposing cellular fates. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18609-18614.
38. Datta S., Antonyak M.A., Cerione R.A. GTP-binding-defective forms of tissue transglutaminase trigger cell death. Biochemistry 2007, 46:14819-14829.
39. Tee A.E., Marshall G.M., Liu P.Y., Xu N., Haber M., Norris M.D., Iismaa S.E., Liu T. Opposing effects of two tissue transglutaminase protein isoforms in neuroblastoma cell differentiation. J. Biol. Chem. 2010, 285:3561-3567.
40. Tucholski J., Lesort M., Johnson G.V. Tissue transglutaminase is essential for neurite outgrowth in human neuroblastoma SH-SY5Y cells. Neuroscience 2001, 102:481-491.
41. Mishra S., Murphy L.J. Phosphorylation of transglutaminase 2 by PKA at Ser216 creates 14-3-3 binding sites. Biochem. Biophys. Res. Commun. 2006, 347:1166-1170.
42. Mishra S., Murphy L.J. The p53 oncoprotein is a substrate for tissue transglutaminase kinase activity. Biochem. Biophys. Res. Commun. 2006, 339:726-730.
43. Mishra S., Melino G., Murphy L.J. Transglutaminase 2 kinase activity facilitates protein kinase A-induced phosphorylation of retinoblastoma protein. J. Biol. Chem. 2007, 282:18108-18115.
44. Cohen I., Blankenberg T.A., Borden D., Kahn D.R., Veis A. Factor XIIIa-catalyzed cross-linking of platelet and muscle actin. Regulation by nucleotides. Biochim. Biophys. Acta 1980, 628:365-375.
45. Chandrashekar R., Tsuji N., Morales T., Ozols V., Mehta K. An ERp60-like protein from the filarial parasite Dirofilaria immitis has both transglutaminase and protein disulfide isomerase activity. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:531-536.
46. Knodler L.A., Noiva R., Mehta K., McCaffery J.M., Aley S.B., Svard S.G., Nystul T.G., Reiner D.S., Silberman J.D., Gillin F.D. Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J. Biol. Chem. 1999, 274:29805-29811.
47. Natsuka S., Takubo R., Seki R., Ikura K. Molecular cloning and expression of Caenorhabditis elegans ERp57-homologue with transglutaminase activity. J. Biochem. 2001, 130:731-735.
48. Lahav J., Karniel E., Bagoly Z., Sheptovitsky V., Dardik R., Inbal A. Coagulation factor XIII serves as protein disulfide isomerase. Thromb. Haemost. 2009, 101:840-844.
49. Szondy Z., Mastroberardino P.G., Varadi J., Farrace M.G., Nagy N., Bak I., Viti I., Wieckowski M.R., Melino G., Rizzuto R., Tosaki A., Fesus L., Piacentini M. Tissue transglutaminase (TG2) protects cardiomyocytes against ischemia/reperfusion injury by regulating ATP synthesis. Cell Death Differ. 2006, 13:1827-1829.
50. Malorni W., Farrace M.G., Matarrese P., Tinari A., Ciarlo L., Mousavi-Shafaei P., D'Eletto M., Di Giacomo G., Melino G., Palmieri L., Rodolfo C., Piacentini M. The adenine nucleotide translocator 1 acts as a type 2 transglutaminase substrate: implications for mitochondrial-dependent apoptosis. Cell Death Differ. 2009, 16:1480-1492.
51. Piacentini M., Farrace M.G., Piredda L., Matarrese P., Ciccosanti F., Falasca L., Rodolfo C., Giammarioli A.M., Verderio E., Griffin M., Malorni W. Transglutaminase overexpression sensitizes neuronal cell lines to apoptosis by increasing mitochondrial membrane potential and cellular oxidative stress. J. Neurochem. 2002, 81:1061-1072.
52. Ruan Q., Quintanilla R.A., Johnson G.V. Type 2 transglutaminase differentially modulates striatal cell death in the presence of wild type or mutant huntingtin. J. Neurochem. 2007, 102:25-36.
53. Rodolfo C., Mormone E., Matarrese P., Ciccosanti F., Farrace M.G., Garofano E., Piredda L., Fimia G.M., Malorni W., Piacentini M. Tissue transglutaminase is a multifunctional BH3-only protein. J. Biol. Chem. 2004, 279:54783-54792.
54. Krasnikov B.F., Kim S.Y., McConoughey S.J., Ryu H., Xu H., Stavrovskaya I., Iismaa S.E., Mearns B.M., Ratan R.R., Blass J.P., Gibson G.E., Cooper A.J. Transglutaminase activity is present in highly purified nonsynaptosomal mouse brain and liver mitochondria. Biochemistry 2005, 44:7830-7843.
55. Liu S., Cerione R.A., Clardy J. Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2743-2747.
56. Han B.G., Cho J.W., Cho Y.D., Jeong K.C., Kim S.Y., Lee B.I. Crystal structure of human transglutaminase 2 in complex with adenosine triphosphate. Int. J. Biol. Macromol. 2010, 47:190-195.
57. Murthy S.N., Iismaa S., Begg G., Freymann D.M., Graham R.M., Lorand L. Conserved tryptophan in the core domain of transglutaminase is essential for catalytic activity. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2738-2742.
58. Begg G.E., Holman S.R., Stokes P.H., Matthews J.M., Graham R.M., Iismaa S.E. Mutation of a critical arginine in the GTP-binding site of transglutaminase 2 disinhibits intracellular cross-linking activity. J. Biol. Chem. 2006, 281:12603-12609.
59. Iismaa S.E., Wu M.J., Nanda N., Church W.B., Graham R.M. GTP binding and signaling by Gh/transglutaminase II involves distinct residues in a unique GTP-binding pocket. J. Biol. Chem. 2000, 275:18259-18265.
60. Fox B.A., Yee V.C., Pedersen L.C., Le Trong I., Bishop P.D., Stenkamp R.E., Teller D.C. Identification of the calcium binding site and a novel ytterbium site in blood coagulation factor XIII by X-ray crystallography. J. Biol. Chem. 1999, 274:4917-4923.
61. Ahvazi B., Boeshans K.M., Idler W., Baxa U., Steinert P.M. Roles of calcium ions in the activation and activity of the transglutaminase 3 enzyme. J. Biol. Chem. 2003, 278:23834-23841.
62. Ahvazi B., Boeshans K.M., Idler W., Baxa U., Steinert P.M., Rastinejad F. Structural basis for the coordinated regulation of transglutaminase 3 by guanine nucleotides and calcium/magnesium. J. Biol. Chem. 2004, 279:7180-7192.
63. Casadio R., Polverini E., Mariani P., Spinozzi F., Carsughi F., Fontana A., Polverino de Laureto P., Matteucci G., Bergamini C.M. The structural basis for the regulation of tissue transglutaminase by calcium ions. Eur. J. Biochem. 1999, 262:672-679.
64. Bergamini C.M. GTP modulates calcium binding and cation-induced conformational changes in erythrocyte transglutaminase. FEBS Lett. 1988, 239:255-258.
65. Kiraly R., Csosz E., Kurtan T., Antus S., Szigeti K., Simon-Vecsei Z., Korponay-Szabo I.R., Keresztessy Z., Fesus L. Functional significance of five noncanonical Ca2+- binding sites of human transglutaminase 2 characterized by site-directed mutagenesis. FEBS J. 2009, 276:7083-7096.
66. Siegel M., Strnad P., Watts R.E., Choi K., Jabri B., Omary M.B., Khosla C. Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS One 2008, 3:e1861.
67. Stamnaes J., Pinkas D.M., Fleckenstein B., Khosla C., Sollid L.M. Redox regulation of transglutaminase 2 activity. J. Biol. Chem. 2010, 285:25402-25409.
68. Ohashi H., Itoh Y., Birckbichler P.J., Takeuchi Y. Purification and characterization of rat brain transglutaminase. J. Biochem. 1995, 118:1271-1278.
69. Luciani A., Villella V.R., Vasaturo A., Giardino I., Raia V., Pettoello-Mantovani M., D'Apolito M., Guido S., Leal T., Quaratino S., Maiuri L. SUMOylation of tissue transglutaminase as link between oxidative stress and inflammation. J. Immunol. 2009, 183:2775-2784.
70. 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.
71. Lesort M., Attanavanich K., Zhang J., Johnson G.V. Distinct nuclear localization and activity of tissue transglutaminase. J. Biol. Chem. 1998, 273:11991-11994.
72. Singh U.S., Erickson J.W., Cerione R.A. Identification and biochemical characterization of an 80 kilodalton GTP-binding/transglutaminase from rabbit liver nuclei. Biochemistry 1995, 34:15863-15871.
73. Janiak A., Zemskov E.A., Belkin A.M. Cell surface transglutaminase promotes RhoA activation via integrin clustering and suppression of the Src-p190RhoGAP signaling pathway. Mol. Biol. Cell 2006, 17:1606-1619.
74. 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.
75. Balklava Z., Verderio E., Collighan R., Gross S., Adams J., Griffin M. Analysis of tissue transglutaminase function in the migration of Swiss 3T3 fibroblasts: the active-state conformation of the enzyme does not affect cell motility but is important for its secretion. J. Biol. Chem. 2002, 277:16567-16575.
76. Antonyak M.A., Li B., Boroughs L.K., Johnson J.L., Druso J.E., Bryant K.L., Holowka D.A., Cerione R.A. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4852-4857.
77. Zemskov E.A., Mikhailenko I., Hsia R.C., Zaritskaya L., Belkin A.M. Unconventional secretion of tissue transglutaminase involves phospholipid-dependent delivery into recycling endosomes. PLoS One 2011, 6:e19414.
78. McConoughey S.J., Basso M., Niatsetskaya Z.V., Sleiman S.F., Smirnova N.A., Langley B.C., Mahishi L., Cooper A.J., Antonyak M.A., Cerione R.A., Li B., Starkov A., Chaturvedi R.K., Beal M.F., Coppola G., Geschwind D.H., Ryu H., Xia L., Iismaa S.E., Pallos J., Pasternack R., Hils M., Fan J., Raymond L.A., Marsh J.L., Thompson L.M., Ratan R.R. Inhibition of transglutaminase 2 mitigates transcriptional dysregulation in models of Huntington disease. EMBO Mol. Med. 2010, 2:349-370.
79. Lu S., Saydak M., Gentile V., Stein J.P., Davies P.J. Isolation and characterization of the human tissue transglutaminase gene promoter. J. Biol. Chem. 1995, 270:9748-9756.
80. Shimada J., Suzuki Y., Kim S.J., Wang P.C., Matsumura M., Kojima S. Transactivation via RAR/RXR-Sp1 interaction: characterization of binding between Sp1 and GC box motif. Mol. Endocrinol. 2001, 15:1677-1692.
81. Nagy L., Saydak M., Shipley N., Lu S., Basilion J.P., Yan Z.H., Syka P., Chandraratna R.A., Stein J.P., Heyman R.A., Davies P.J. 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. 1996, 271:4355-4365.
82. Ritter S.J., Davies P.J. 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. 1998, 273:12798-12806.
83. Mirza A., Liu S.L., Frizell E., Zhu J., Maddukuri S., Martinez J., Davies P., Schwarting R., Norton P., Zern M.A. A role for tissue transglutaminase in hepatic injury and fibrogenesis, and its regulation by NF-kappaB. Am. J. Physiol. 1997, 272:G281-G288.
84. Jang G.Y., Jeon J.H., Cho S.Y., Shin D.M., Kim C.W., Jeong E.M., Bae H.C., Kim T.W., Lee S.H., Choi Y., Lee D.S., Park S.C., Kim I.G. Transglutaminase 2 suppresses apoptosis by modulating caspase 3 and NF-kappaB activity in hypoxic tumor cells. Oncogene 2010, 29:356-367.
85. Suto N., Ikura K., Sasaki R. Expression induced by interleukin-6 of tissue-type transglutaminase in human hepatoblastoma HepG2 cells. J. Biol. Chem. 1993, 268:7469-7473.
86. Johnson K., Hashimoto S., Lotz M., Pritzker K., Terkeltaub R. Interleukin-1 induces pro-mineralizing activity of cartilage tissue transglutaminase and factor XIIIa. Am. J. Pathol. 2001, 159:149-163.
87. Kuncio G.S., Tsyganskaya M., Zhu J., Liu S.L., Nagy L., Thomazy V., Davies P.J., Zern M.A. TNF-alpha modulates expression of the tissue transglutaminase gene in liver cells. Am. J. Physiol. 1998, 274:G240-G245.
88. Chen R., Gao B., Huang C., Olsen B., Rotundo R.F., Blumenstock F., Saba T.M. Transglutaminase-mediated fibronectin multimerization in lung endothelial matrix in response to TNF-alpha. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279:L161-L174.
89. Mehta K., Fok J.Y., Mangala L.S. Tissue transglutaminase: from biological glue to cell survival cues. Front. Biosci. 2006, 11:173-185.
90. Ai L., Kim W.J., Demircan B., Dyer L.M., Bray K.J., Skehan R.R., Massoll N.A., Brown K.D. The transglutaminase 2 gene (TGM2), a potential molecular marker for chemotherapeutic drug sensitivity, is epigenetically silenced in breast cancer. Carcinogenesis 2008, 29:510-518.
91. Park K.S., Kim H.K., Lee J.H., Choi Y.B., Park S.Y., Yang S.H., Kim S.Y., Hong K.M. Transglutaminase 2 as a cisplatin resistance marker in non-small cell lung cancer. J. Cancer Res. Clin. Oncol. 2010, 136:493-502.
92. Dyer L.M., Schooler K.P., Ai L., Klop C., Qiu J., Robertson K.D., Brown K.D. The transglutaminase 2 gene is aberrantly hypermethylated in glioma. J. Neurooncol. 2011, 101:429-440.
93. Liu T., Tee A.E., Porro A., Smith S.A., Dwarte T., Liu P.Y., Iraci N., Sekyere E., Haber M., Norris M.D., Diolaiti D., Della Valle G., Perini G., Marshall G.M. Activation of tissue transglutaminase transcription by histone deacetylase inhibition as a therapeutic approach for Myc oncogenesis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18682-18687.
94. Ientile R., Caccamo D., Griffin M. Tissue transglutaminase and the stress response. Amino Acids 2007, 33:385-394.
95. Fraij B.M., Birckbichler P.J., Patterson M.K., Lee K.N., Gonzales R.A. A retinoic acid-inducible mRNA from human erythroleukemia cells encodes a novel tissue transglutaminase homologue. J. Biol. Chem. 1992, 267:22616-22623.
96. Fraij B.M., Gonzales R.A. A third human tissue transglutaminase homologue as a result of alternative gene transcripts. Biochim. Biophys. Acta 1996, 1306:63-74.
97. Citron B.A., SantaCruz K.S., Davies P.J., Festoff B.W. Intron-exon swapping of transglutaminase mRNA and neuronal Tau aggregation in Alzheimer's disease. J. Biol. Chem. 2001, 276:3295-3301.
98. Festoff B.W., SantaCruz K., Arnold P.M., Sebastian C.T., Davies P.J., Citron B.A. Injury-induced "switch" from GTP-regulated to novel GTP-independent isoform of tissue transglutaminase in the rat spinal cord. J. Neurochem. 2002, 81:708-718.
99. Monsonego A., Shani Y., Friedmann I., Paas Y., Eizenberg O., Schwartz M. Expression of GTP-dependent and GTP-independent tissue-type transglutaminase in cytokine-treated rat brain astrocytes. J. Biol. Chem. 1997, 272:3724-3732.
100. Milakovic T., Tucholski J., McCoy E., Johnson G.V. Intracellular localization and activity state of tissue transglutaminase differentially impacts cell death. J. Biol. Chem. 2004, 279:8715-8722.
101. Tucholski J., Johnson G.V. Tissue transglutaminase differentially modulates apoptosis in a stimuli-dependent manner. J. Neurochem. 2002, 81:780-791.
102. Fok J.Y., Mehta K. Tissue transglutaminase induces the release of apoptosis inducing factor and results in apoptotic death of pancreatic cancer cells. Apoptosis 2007, 12:1455-1463.
103. Akar U., Ozpolat B., Mehta K., Fok J., Kondo Y., Lopez-Berestein G. Tissue transglutaminase inhibits autophagy in pancreatic cancer cells. Mol. Cancer Res. 2007, 5:241-249.
104. D'Eletto M., Farrace M.G., Falasca L., Reali V., Oliverio S., Melino G., Griffin M., Fimia G.M., Piacentini M. Transglutaminase 2 is involved in autophagosome maturation. Autophagy 2009, 5:1145-1154.
105. Rossin F., D'Eletto M., Macdonald D., Farrace M.G., Piacentini M. TG2 transamidating activity acts as a reostat controlling the interplay between apoptosis and autophagy. Amino Acids 2011.
106. 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.
107. Lesort M., Chun W., Johnson G.V., Ferrante R.J. Tissue transglutaminase is increased in Huntington's disease brain. J. Neurochem. 1999, 73:2018-2027.
108. Maggio N., Sellitti S., Capano C.P., Papa M. Tissue-transglutaminase in rat and human brain: light and electron immunocytochemical analysis and in situ hybridization study. Brain Res. Bull. 2001, 56:173-182.
109. Ruan Q., Johnson G.V. Transglutaminase 2 in neurodegenerative disorders. Front. Biosci. 2007, 12:891-904.
110. Bailey C.D., Johnson G.V. Tissue transglutaminase contributes to disease progression in the R6/2 Huntington's disease mouse model via aggregate-independent mechanisms. J. Neurochem. 2005, 92:83-92.
111. Mastroberardino P.G., Iannicola C., Nardacci R., Bernassola F., De Laurenzi V., Melino G., Moreno S., Pavone F., Oliverio S., Fesus L., Piacentini M. 'Tissue' transglutaminase ablation reduces neuronal death and prolongs survival in a mouse model of Huntington's disease. Cell Death Differ. 2002, 9:873-880.
112. De Laurenzi V., Melino G. Gene disruption of tissue transglutaminase. Mol. Cell. Biol. 2001, 21:148-155.
113. Tucholski J., Roth K.A., Johnson G.V. Tissue transglutaminase overexpression in the brain potentiates calcium-induced hippocampal damage. J. Neurochem. 2006, 97:582-594.
114. Filiano A.J., Bailey C.D., Tucholski J., Gundemir S., Johnson G.V. Transglutaminase 2 protects against ischemic insult, interacts with HIF1beta, and attenuates HIF1 signaling. FASEB J. 2008, 22:2662-2675.
115. Filiano A.J., Tucholski J., Dolan P.J., Colak G., Johnson G.V. Transglutaminase 2 protects against ischemic stroke. Neurobiol. Dis. 2010, 39:334-343.
116. Aeschlimann D., Thomazy V. Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. Connect. Tissue Res. 2000, 41:1-27.
117. Aeschlimann D., Mosher D., Paulsson M. Tissue transglutaminase and factor XIII in cartilage and bone remodeling. Semin. Thromb. Hemost. 1996, 22:437-443.
118. Jones R.A., Nicholas B., Mian S., Davies P.J., Griffin M. Reduced expression of tissue transglutaminase in a human endothelial cell line leads to changes in cell spreading, cell adhesion and reduced polymerisation of fibronectin. J. Cell Sci. 1997, 110(Pt 19):2461-2472.
119. Gentile V., Thomazy V., Piacentini M., Fesus L., Davies P.J. Expression of tissue transglutaminase in Balb-C 3T3 fibroblasts: effects on cellular morphology and adhesion. J. Cell Biol. 1992, 119:463-474.
120. Gaudry C.A., Verderio E., Jones R.A., Smith C., Griffin M. Tissue transglutaminase is an important player at the surface of human endothelial cells: evidence for its externalization and its colocalization with the beta(1) integrin. Exp. Cell Res. 1999, 252:104-113.
121. Lorand L., Dailey J.E., Turner P.M. Fibronectin as a carrier for the transglutaminase from human erythrocytes. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:1057-1059.
122. Gaudry C.A., Verderio E., Aeschlimann D., Cox A., Smith C., Griffin M. Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal beta-sandwich domain. J. Biol. Chem. 1999, 274:30707-30714.
123. Akimov S.S., Krylov D., Fleischman L.F., Belkin A.M. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J. Cell Biol. 2000, 148:825-838.
124. Verma A., Mehta K. Tissue transglutaminase-mediated chemoresistance in cancer cells. Drug Resist. Updat. 2007, 10:144-151.
125. Verderio E.A., Telci D., Okoye A., Melino G., Griffin M. A novel RGD-independent cel adhesion pathway mediated by fibronectin-bound tissue transglutaminase rescues cells from anoikis. J. Biol. Chem. 2003, 278:42604-42614.
126. Kojima S., Nara K., Rifkin D.B. Requirement for transglutaminase in the activation of latent transforming growth factor-beta in bovine endothelial cells. J. Cell Biol. 1993, 121:439-448.
127. Telci D., Collighan R.J., Basaga H., Griffin M. Increased TG2 expression can result in induction of transforming growth factor beta1, causing increased synthesis and deposition of matrix proteins, which can be regulated by nitric oxide. J. Biol. Chem. 2009, 284:29547-29558.
128. Shweke N., Boulos N., Jouanneau C., Vandermeersch S., Melino G., Dussaule J.C., Chatziantoniou C., Ronco P., Boffa J.J. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am. J. Pathol. 2008, 173:631-642.
129. Olsen K.C., Sapinoro R.E., Kottmann R.M., Kulkarni A.A., Iismaa S.E., Johnson G.V., Thatcher T.H., Phipps R.P., Sime P.J. Transglutaminase 2 and its role in pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 2011, 184:699-707.
130. Gambetti S., Dondi A., Cervellati C., Squerzanti M., Pansini F.S., Bergamini C.M. Interaction with heparin protects tissue transglutaminase against inactivation by heating and by proteolysis. Biochimie 2005, 87:551-555.
131. Scarpellini A., Germack R., Lortat-Jacob H., Muramatsu T., Billett E., Johnson T., Verderio E.A. Heparan sulfate proteoglycans are receptors for the cell-surface trafficking and biological activity of transglutaminase-2. J. Biol. Chem. 2009, 284:18411-18423.
132. Boros S., Kamps B., Wunderink L., de Bruijn W., de Jong W.W., Boelens W.C. Transglutaminase catalyzes differential crosslinking of small heat shock proteins and amyloid-beta. FEBS Lett. 2004, 576:57-62.
133. Wakshlag J.J., Antonyak M.A., Boehm J.E., Boehm K., Cerione R.A. Effects of tissue transglutaminase on beta -amyloid1-42-induced apoptosis. Protein J. 2006, 25:83-94.
134. Belkin A.M., Zemskov E.A., Hang J., Akimov S.S., Sikora S., Strongin A.Y. Cell-surface-associated tissue transglutaminase is a target of MMP-2 proteolysis. Biochemistry 2004, 43:11760-11769.
135. Dardik R., Inbal A. Complex formation between tissue transglutaminase II (tTG) and vascular endothelial growth factor receptor 2 (VEGFR-2): proposed mechanism for modulation of endothelial cell response to VEGF. Exp. Cell Res. 2006, 312:2973-2982.
136. Joshi S., Guleria R., Pan J., DiPette D., Singh U.S. Retinoic acid receptors and tissue-transglutaminase mediate short-term effect of retinoic acid on migration and invasion of neuroblastoma SH-SY5Y cells. Oncogene 2006, 25:240-247.
137. Mangala L.S., Fok J.Y., Zorrilla-Calancha I.R., Verma A., Mehta K. Tissue transglutaminase expression promotes cell attachment, invasion and survival in breast cancer cells. Oncogene 2007, 26:2459-2470.
138. Herman J.F., Mangala L.S., Mehta K. Implications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells. Oncogene 2006, 25:3049-3058.
139. Mangala L.S., Arun B., Sahin A.A., Mehta K. Tissue transglutaminase-induced alterations in extracellular matrix inhibit tumor invasion. Mol. Cancer 2005, 4:33.
140. Lentini A., Provenzano B., Caraglia M., Shevchenko A., Abbruzzese A., Beninati S. Impairment of the metastatic activity of melanoma cells by transglutaminase-catalyzed incorporation of polyamines into laminin and Matrigel. Amino Acids 2008, 34:251-256.
141. Mohan K., Pinto D., Issekutz T.B. Identification of tissue transglutaminase as a novel molecule involved in human CD8+ T cell transendothelial migration. J. Immunol. 2003, 171:3179-3186.
142. 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.
143. van Strien M.E., Drukarch B., Bol J.G., van der Valk P., van Horssen J., Gerritsen W.H., Breve J.J., van Dam A.M. Appearance of tissue transglutaminase in astrocytes in multiple sclerosis lesions: a role in cell adhesion and migration?. Brain Pathol. 2011, 21:44-54.
144. Szondy Z., Sarang Z., Molnar P., Nemeth T., Piacentini M., Mastroberardino P.G., Falasca L., Aeschlimann D., Kovacs J., Kiss I., Szegezdi E., Lakos G., Rajnavolgyi E., Birckbichler P.J., Melino G., Fesus L. Transglutaminase 2-/- mice reveal a phagocytosis-associated crosstalk between macrophages and apoptotic cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:7812-7817.
145. Falasca L., Iadevaia V., Ciccosanti F., Melino G., Serafino A., Piacentini M. Transglutaminase type II is a key element in the regulation of the anti-inflammatory response elicited by apoptotic cell engulfment. J. Immunol. 2005, 174:7330-7340.
146. Toth B., Garabuczi E., Sarang Z., Vereb G., Vamosi G., Aeschlimann D., Blasko B., Becsi B., Erdodi F., Lacy-Hulbert A., Zhang A., Falasca L., Birge R.B., Balajthy Z., Melino G., Fesus L., Szondy Z. Transglutaminase 2 is needed for the formation of an efficient phagocyte portal in macrophages engulfing apoptotic cells. J. Immunol. 2009, 182:2084-2092.
147. Toth B., Sarang Z., Vereb G., Zhang A., Tanaka S., Melino G., Fesus L., Szondy Z. Over-expression of integrin beta3 can partially overcome the defect of integrin beta3 signaling in transglutaminase 2 null macrophages. Immunol. Lett. 2009, 126:22-28.
148. Michlewska S., McColl A., Rossi A.G., Megson I.L., Dransfield I. Clearance of dying cells and autoimmunity. Autoimmunity 2007, 40:267-273.
149. Rebe C., Raveneau M., Chevriaux A., Lakomy D., Sberna A.L., Costa A., Bessede G., Athias A., Steinmetz E., Lobaccaro J.M., Alves G., Menicacci A., Vachenc S., Solary E., Gambert P., Masson D. Induction of transglutaminase 2 by a liver X receptor/retinoic acid receptor alpha pathway increases the clearance of apoptotic cells by human macrophages. Circ. Res. 2009, 105:393-401.
150. Xu L., Begum S., Hearn J.D., Hynes R.O. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:9023-9028.
151. Xu L., Hynes R.O. GPR56 and TG2: possible roles in suppression of tumor growth by the microenvironment. Cell Cycle 2007, 6:160-165.
152. Chiarugi P., Giannoni E. Anoikis: a necessary death program for anchorage-dependent cells. Biochem. Pharmacol. 2008, 76:1352-1364.
153. Yuan L., Siegel M., Choi K., Khosla C., Miller C.R., Jackson E.N., Piwnica-Worms D., Rich K.M. Transglutaminase 2 inhibitor, KCC009, disrupts fibronectin assembly in the extracellular matrix and sensitizes orthotopic glioblastomas to chemotherapy. Oncogene 2007, 26:2563-2573.
154. Yuan L., Holmes T.C., Watts R.E., Khosla C., Broekelmann T.J., Mecham R., Zheng H., Izaguirre E.W., Rich K.M. Novel chemo-sensitizing agent, ERW1227B, impairs cellular motility and enhances cell death in glioblastomas. J. Neurooncol. 2010, 103:207-219.
155. Campisi A., Caccamo D., Li Volti G., Curro M., Parisi G., Avola R., Vanella A., Ientile R. Glutamate-evoked redox state alterations are involved in tissue transglutaminase upregulation in primary astrocyte cultures. FEBS Lett. 2004, 578:80-84.
156. Mann A.P., Verma A., Sethi G., Manavathi B., Wang H., Fok J.Y., Kunnumakkara A.B., Kumar R., Aggarwal B.B., Mehta K. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-kappaB in cancer cells: delineation of a novel pathway. Cancer Res. 2006, 66:8788-8795.
157. Tatsukawa H., Fukaya Y., Frampton G., Martinez-Fuentes A., Suzuki K., Kuo T.F., Nagatsuma K., Shimokado K., Okuno M., Wu J., Iismaa S., Matsuura T., Tsukamoto H., Zern M.A., Graham R.M., Kojima S. Role of transglutaminase 2 in liver injury via cross-linking and silencing of transcription factor Sp1. Gastroenterology 2009, 136. 1783-1795 e1710.
158. Balajthy Z., Csomos K., Vamosi G., Szanto A., Lanotte M., Fesus L. Tissue-transglutaminase contributes to neutrophil granulocyte differentiation and functions. Blood 2006, 108:2045-2054.
159. Ahn J.S., Kim M.K., Hahn J.H., Park J.H., Park K.H., Cho B.R., Park S.B., Kim D.J. Tissue transglutaminase-induced down-regulation of matrix metalloproteinase-9. Biochem. Biophys. Res. Commun. 2008, 376:743-747.
160. Lesort M., Tucholski J., Miller M.L., Johnson G.V. Tissue transglutaminase: a possible role in neurodegenerative diseases. Prog. Neurobiol. 2000, 61:439-463.
161. Zuccato C., Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 2009, 5:311-322.
162. Mehta K., Kumar A., Kim H.I. Transglutaminase 2: a multi-tasking protein in the complex circuitry of inflammation and cancer. Biochem. Pharmacol. 2010, 80:1921-1929.
163. Lee J., Kim Y.S., Choi D.H., Bang M.S., Han T.R., Joh T.H., Kim S.Y. Transglutaminase 2 induces nuclear factor-kappaB activation via a novel pathway in BV-2 microglia. J. Biol. Chem. 2004, 279:53725-53735.
164. Kim D.S., Park S.S., Nam B.H., Kim I.H., Kim S.Y. Reversal of drug resistance in breast cancer cells by transglutaminase 2 inhibition and nuclear factor-kappaB inactivation. Cancer Res. 2006, 66:10936-10943.
165. Cao L., Petrusca D.N., Satpathy M., Nakshatri H., Petrache I., Matei D. Tissue transglutaminase protects epithelial ovarian cancer cells from cisplatin-induced apoptosis by promoting cell survival signaling. Carcinogenesis 2008, 29:1893-1900.
166. Tucholski J., Johnson G.V. Tissue transglutaminase directly regulates adenylyl cyclase resulting in enhanced cAMP-response element-binding protein (CREB) activation. J. Biol. Chem. 2003, 278:26838-26843.
167. Satpathy M., Shao M., Emerson R., Donner D.B., Matei D. Tissue transglutaminase regulates matrix metalloproteinase-2 in ovarian cancer by modulating cAMP-response element-binding protein activity. J. Biol. Chem. 2009, 284:15390-15399.
168. Kang S.K., Lee J.Y., Chung T.W., Kim C.H. Overexpression of transglutaminase 2 accelerates the erythroid differentiation of human chronic myelogenous leukemia K562 cell line through PI3K/Akt signaling pathway. FEBS Lett. 2004, 577:361-366.
169. Oliverio S., Amendola A., Rodolfo C., Spinedi A., Piacentini M. Inhibition of "tissue" transglutaminase increases cell survival by preventing apoptosis. J. Biol. Chem. 1999, 274:34123-34128.
170. Tolentino P.J., DeFord S.M., Notterpek L., Glenn C.C., Pike B.R., Wang K.K., Hayes R.L. Up-regulation of tissue-type transglutaminase after traumatic brain injury. J. Neurochem. 2002, 80:579-588.
171. Tolentino P.J., Waghray A., Wang K.K., Hayes R.L. Increased expression of tissue-type transglutaminase following middle cerebral artery occlusion in rats. J. Neurochem. 2004, 89:1301-1307.
172. Sarang Z., Molnar P., Nemeth T., Gomba S., Kardon T., Melino G., Cotecchia S., Fesus L., Szondy Z. Tissue transglutaminase (TG2) acting as G protein protects hepatocytes against Fas-mediated cell death in mice. Hepatology 2005, 42:578-587.