Regulation of the activities of the mammalian transglutaminase family of enzymes

Protein Science

Volumn 21, Issue 12, 2012, Pages 1781-1791

  Klöock, Cornelius ^a   Khosla, Chaitan ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

Author keywords

Allostery; Disulfide redox switch; Human mutations; Post translational modification; Transglutaminase

Indexed keywords

ACYLTRANSFERASE INHIBITOR; BLOOD CLOTTING FACTOR 13A; BLOOD CLOTTING FACTOR 13B; CALCIUM ION; CK IV 38; FIBRONECTIN; GLUCOSAMINE PHOSPHATE ACETYLTRANSFERASE; GLUTAMINE; GUANINE NUCLEOTIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; ISOENZYME; LDN 27219; PHOSPHOLIPASE C; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; TRANSGLUTAMINASE 1; TRANSGLUTAMINASE 3; UNCLASSIFIED DRUG;

ALLOSTERISM; ALTERNATIVE RNA SPLICING; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME MECHANISM; ENZYME MODIFICATION; ENZYME REGULATION; ENZYME STRUCTURE; ENZYME SUBUNIT; EXON; GENE MUTATION; GENETIC ASSOCIATION; HOMEOSTASIS; HUMAN; ICHTHYOSIS; KERATINOCYTE; LAMELLAR ICHTHYOSIS; LOSS OF FUNCTION MUTATION; MAMMAL; MISSENSE MUTATION; MUTAGENESIS; MYRISTYLATION; OXIDATION; OXIDATION REDUCTION POTENTIAL; PALMITOYLATION; PHENOTYPE; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW;

ALLOSTERIC REGULATION; ANIMALS; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSGLUTAMINASES;

MAMMALIA;

EID: 84870359579     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2162     Document Type: Review

References (87)

1. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Biol 4:140-156.
2. Iismaa SE, Mearns BM, Lorand L, Graham RM (2009) Transglutaminases and disease: lessons from genetically engineered mouse models and inherited disorders. Physiol Rev 89:991-1023.
3. Mehta K, Eckert R, editors (2005). Transglutaminases family of enzymes with diverse functions. Basel: Karger, pp1-247.
4. Muszbek L, Bereczky Z, Bagoly Z, Komáromi I, Katona É (2011) Factor XIII: a coagulation factor with multipleplasmatic and cellular functions. Physiol Rev 91:931-972.
5. Nurminskaya MV, Belkin AM (2012) Cellular functions of tissue transglutaminase. Int Rev Cell Mol Biol 294:1-97.
6. Liu S, Cerione RA, Clardy J (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc Natl Acad Sci USA 99:2743-2747.
7. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5:2788-2796.
8. Bergamini CM (1988) GTP modulates calcium binding and cation-induced conformational changes in erythrocyte transglutaminase. FEBS Lett 239:255-258.
9. 2+-binding sites of human transglutaminase 2 characterized by site-directed mutagenesis. FEBS J 276:7083-7096.
10. Bergamini CM, Signorini M, Poltronieri L (1987) Inhibition of erythrocyte transglutaminase by GTP. Biochim Biophys Acta 916:149-151.
11. Begg GE, Holman SR, Stokes PH, Matthews JM, Graham RM, Iismaa SE (2006) Mutation of a critical arginine in the GTP-binding site of transglutaminase 2 disinhibits intracellular cross-linking activity. J Biol Chem 281:12603-12609.
12. Bergamini CM, Dondi A, Lanzara V, Squerzanti M, Cervellati C, Montin K, Mischiati C, Tasco G, Collighan R, Griffin M, Casadio R (2010) Thermodynamics of binding of regulatory ligands to tissue transglutaminase. Amino Acids 39:297-304.
13. Siegel M, Strnad P, Watts RE, Choi K, Jabri B, Omary MB, Khosla C (2008) Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS ONE 3:e1861.
14. Folk J, Cole P (1966) Mechanism of action of guinea pig liver transglutaminase. J Biol Chem 241:5518-5525.
15. Boothe R, Folk J (1969) A reversible, calcium-dependent, copper-catalyzed inactivation of guinea pig liver transglutaminase. J Biol Chem 244:399-405.
16. Jin X, Stamnaes J, Klöock C, Diraimondo TR, Sollid LM, Khosla C (2011) Activation of extracellular transglutaminase 2 by thioredoxin. J Biol Chem 286:37866-37873.
17. Stamnaes J, Pinkas DM, Fleckenstein B, Khosla C, Sollid LM (2010) Redox regulation of transglutaminase 2 activity. J Biol Chem 285:25402-25409.
18. Fesus L, Piacentini M (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 27:534-539.
19. Orrenius S, Zhivotovsky B, Nicotera P (2003) Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4:552-565.
20. Wei L, Warburton RR, Preston IR, Roberts KE, Comhair SAA, Erzurum SC, Hill NS, Fanburg BL (2012) Serotonylated fibronectin is elevated in pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 302:L1273-L1279.
21. Zemskov E, Janiak A, Hang J, Waghray A (2006) The role of tissue transglutaminase in cell-matrix interactions. Front Biosci 11:1057-1076.
22. Turner P, Lorand L (1989) Complexation of fibronectin with tissue transglutaminase. Biochemistry 28:628-635.
23. Nakaoka H, Perez DM, Baek KJ, Das T, Husain A, Misono K, Im MJ, Graham RM (1994) Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 264:1593-1596.
24. Lortat-Jacob H, Burhan I, Scarpellini A, Thomas A, Imberty A, Vivès RR, Johnson T, Gutierrez A, Verderio EA (2012) Transglutaminase-2 interaction with heparin: identification of a heparin binding site that regulates cell adhesion to fibronectin-transglutaminase-2 matrix. J Biol Chem 287:18005-18017.
25. Wang Z, Collighan RJ, Pytel K, Rathbone DL, Li X, Griffin M (2012) Characterization of heparin-binding site of tissue transglutaminase: its importance in cell surface targeting, matrix deposition, and cell signaling. J Biol Chem 287:13063-13083.
26. Wang Y, Ande SR, Mishra S (2012) Phosphorylation of transglutaminase 2 (TG2) at serine-216 plays a role in TG2 mediated activation of nuclear factor-kappa B and in the downregulation of PTEN. BMC Cancer 12:277.
27. Fraij BM (2011) Activation of tissue tranglutsaminase by removal of carboxyl-terminal peptides. J Cell Biochem 112:3469-3481.
28. Watts RE, Siegel M, Khosla C (2006) Structure-activity relationship analysis of the selective inhibition of transglutaminase 2 by dihydroisoxazoles. J Med Chem 49:7493-7501.
29. Marrano C, de Macédo P, Keillor JW (2001) Evaluation of novel dipeptide-bound alpha, beta-unsaturated amides and epoxides as irreversible inhibitors of guinea pig liver transglutaminase. Bioorg Med Chem 9:1923-1928.
30. Hausch F, Halttunen T, Möaki M, Khosla C (2003) Design, synthesis, and evaluation of gluten peptide analogs as selective inhibitors of human tissue transglutaminase. Chem Biol 10:225-231.
31. Siegel M, Khosla C (2007) Transglutaminase 2 inhibitors and their therapeutic role in disease states. Pharmacol Ther 115:232-245.
32. Pardin C, Pelletier JN, Lubell WD, Keillor JW (2008) Cinnamoyl inhibitors of tissue transglutaminase. J Org Chem 73:5766-5775.
33. Datta S, Antonyak MA, Cerione RA (2007) GTP-binding-defective forms of tissue transglutaminase trigger cell death. Biochemistry 46:14819-14829.
34. Jeong K-C, Ahn K-O, Lee BI, Lee C-H, Kim S-Y (2010) The mechanism of transglutaminase 2 inhibition with glucosamine: implications of a possible anti-inflammatory effect through transglutaminase inhibition. J Cancer Res Clin Oncol 136:143-150.
35. Case A, Stein RL (2007) Kinetic analysis of the interaction of tissue transglutaminase with a nonpeptidic slow-binding inhibitor. Biochemistry 46:1106-1115.
36. Klöock C, Jin X, Choi K, Khosla C, Madrid PB, Spencer A, Raimundo BC, Boardman P, Lanza G, Griffin JH (2011) Acylideneoxoindoles: a new class of reversible inhibitors of human transglutaminase 2. Bioorg Med Chem Lett 21:2692-2696.
37. Duval E, Case A, Stein RL, Cuny GD (2005) Structureactivity relationship study of novel tissue transglutaminase inhibitors. Bioorg Med Chem Lett 15:1885-1889.
38. Schaertl S, Prime M, Wityak J, Dominguez C, Munoz-Sanjuan I, Pacifici RE, Courtney S, Scheel A, Macdonald D (2010) A profiling platform for the characterization of transglutaminase 2 (TG2) inhibitors. J Biomol Screen 15:478-487.
39. Fraij BM, Birckbichler PJ, Patterson MK, Lee KN, Gonzales RA (1992) A retinoic acid-inducible mRNA from human erythroleukemia cells encodes a novel tissue transglutaminase homologue. J Biol Chem 267:22616-22623.
40. Fraij BM, Gonzales RA (1996) A third human tissue transglutaminase homologue as a result of alternative gene transcripts. Biochim Biophys Acta 1306:63-74.
41. Lai T-S, Liu Y, Li W, Greenberg CS (2007) Identification of two GTP-independent alternatively spliced forms of tissue transglutaminase in human leukocytes, vascular smooth muscle, and endothelial cells. FASEB J 21:4131-4143.
42. Antonyak MA, Jansen JM, Miller AM, Ly TK, Endo M, Cerione RA (2006) Two isoforms of tissue transglutaminase mediate opposing cellular fates. Proc Natl Acad Sci USA 103:18609-18614.
43. Bernassola F, Federici M, Corazzari M, Terrinoni A, Hribal ML, De Laurenzi V, Ranalli M, Massa O, Sesti G, McLean WHI, Citro G, Barbetti F, Melino G (2002) Role of transglutaminase 2 in glucose tolerance: knockout mice studies and a putative mutation in a MODY patient. FASEB J 16:1371-1378.
44. Porzio O, Massa O, Cunsolo V, Colombo C, Malaponti M, Bertuzzi F, Hansen T, Johansen A, Pedersen O, Meschi F, Terrinoni A, Melino G, Federici M, Decarlo N, Menicagli M, Campani D, Marchetti P, Ferdaoussi M, Froguel P, Federici G, Vaxillaire M, Barbetti F (2007) Missense mutations in the TGM2 gene encoding transglutaminase 2 are found in patients with earlyonset type 2 diabetes. Mutation in brief no. 982. Online. Hum Mutat 28:1150.
45. 2+- dependent action of a multifunctional protein. FEBS J 278:4717-4739.
46. Salter NW, Ande SR, Nguyen HK, Nyomba BLG, Mishra S (2012) Functional characterization of naturally occurring transglutaminase 2 mutants implicated in early-onset type 2 diabetes. J Mol Endocrinol 48:203-216.
47. Nanda N, Iismaa SE, Owens WA, Husain A, Mackay F, Graham RM (2001) Targeted inactivation of Gh/tissue transglutaminase II. J Biol Chem 276:20673-20678.
48. De Laurenzi V, Melino G (2001) Gene disruption of tissue transglutaminase. Mol Cell Biol 21:148-155.
49. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a weβ-based environment for protein structure homology modelling. Bioinformatics 22:195-201.
50. Herman ML, Farasat S, Steinbach PJ, Wei M-H, Toure O, Fleckman P, Blake P, Bale SJ, Toro JR (2009) Transglutaminase-1 gene mutations in autosomal recessive congenital ichthyosis: summary of mutations (including 23 novel) and modeling of TGase-1. Hum Mutat 30:537-547.
51. UniProt Consortium (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40:D71-D75.
52. Vollmar M, Krysztofinska E, Krojer T, Yue WW, Cooper C, Kavanagh K, Allerston C, Chaikuad A, Von Delft F, Arrowsmith CH, Weigelt J, Edwards A, Bountra C, Oppermann U. (in press) Crystal structure of the human transglutaminase 1 beta-barrel domain (PDB File 2XZZ).
53. Boeshans KM, Mueser TC, Ahvazi B (2007) A threedimensional model of the human transglutaminase 1: insights into the understanding of lamellar ichthyosis. J Mol Model 13:233-246.
54. Steinert PM, Kim SY, Chung SI, Marekov LN (1996) The transglutaminase 1 enzyme is variably acylated by myristate and palmitate during differentiation in epidermal keratinocytes. J Biol Chem 271:26242-26250.
55. Chakravarty R, Rice RH (1989) Acylation of keratinocyte transglutaminase by palmitic and myristic acids in the membrane Anchorage region. J Biol Chem 264:625-629.
56. Phillips MA, Qin Q, Mehrpouyan M, Rice RH (1993) Keratinocyte transglutaminase membrane anchorage: analysis of site-directed mutants. Biochemistry 32:11057-11063.
57. Steinert PM, Chung SI, Kim SY (1996) Inactive zymogen and highly active proteolytically processed membrane-bound forms of the transglutaminase 1 enzyme in human epidermal keratinocytes. Biochem Biophys Res Commun 221:101-106.
58. Kim SY, Chung SI, Steinert PM (1995) Highly active soluble processed forms of the transglutaminase 1 enzyme in epidermal keratinocytes. J Biol Chem 270:18026-18035.
59. Rice RH, Green H (1979) Presence in human epidermal cells of a soluble protein precursor of the cross-linked envelope: activation of the cross-linking by calcium ions. Cell 18:681-694.
60. Sturniolo MT, Chandraratna RAS, Eckert RL (2005) A novel transglutaminase activator forms a complex with type 1 transglutaminase. Oncogene 24:2963-2972.
61. Eckert RL, Sturniolo MT, Jans R, Kraft CA, Jiang H, Rorke EA (2009) TIG3: a regulator of type I transglutaminase activity in epidermis. Amino Acids 36:739-476.
62. Farasat S, Wei M-H, Herman M, Liewehr DJ, Steinberg SM, Bale SJ, Fleckman P, Toro JR (2009) Novel transglutaminase-1 mutations and genotype-phenotype investigations of 104 patients with autosomal recessive congenital ichthyosis in the USA. J Med Genet 46:103-111.
63. Ahvazi B, Kim HC, Kee S-H, Nemes Z, Steinert PM (2002) Three-dimensional structure of the human transglutaminase 3 enzyme: binding of calcium ions changes structure for activation. EMBO J 21:2055-2067.
64. Ahvazi B, Boeshans KM, Idler W, Baxa U, Steinert PM (2003) Roles of calcium ions in the activation and activity of the transglutaminase 3 enzyme. J Biol Chem 278:23834-23841.
65. Ahvazi B, Boeshans KM, Rastinejad F (2004) The emerging structural understanding of transglutaminase 3. J Struct Biol 147:200-207.
66. Kim IG, Gorman JJ, Park SC, Chung SI, Steinert PM (1993) The deduced sequence of the novel protransglutaminase E (TGase3) of human and mouse. J Biol Chem 268:12682-12690.
67. Kim H, Lewis M, Gorman J, Park SC, Girard J, Folk J, Chung S (1990) Protransglutaminase E from guinea pig skin. Isolation and partial characterization. J Biol Chem 265:21971-21978.
68. Cheng T, Hitomi K, van Vlijmen-Willems IMJJ, de Jongh GJ, Yamamoto K, Nishi K, Watts C, Reinheckel T, Schalkwijk J, Zeeuwen PLJM (2006) Cystatin M/E is a high affinity inhibitor of cathepsin V and cathepsin L by a reactive site that is distinct from the legumainbinding site. A novel clue for the role of cystatin M/E in epidermal cornification. J Biol Chem 281:15893-15899.
69. Hitomi K, Kanehiro S, Ikura K, Maki M (1999) Characterization of recombinant mouse epidermal-type transglutaminase (TGase 3): regulation of its activity by proteolysis and guanine nucleotides. J Biochem 125:1048-1054.
70. Zocchi L, Terrinoni A, Candi E, Ahvazi B, Bagetta G, Corasaniti MT, Lena AM, Melino G (2007)Identification of transglutaminase 3 splicing isoforms. J Invest Dermatol 127:1791-1794.
71. Fox BA, Yee VC, Pedersen LC, Le I, Bishop PD, Stenkamp RE, Teller DC (1999) Identification of the calcium binding site and a novel ytterbium site in blood coagulation factor XIII by X-ray crystallography. J Biol Chem 274:4917-4923.
72. Weiss MS, Metzner HJ, Hilgenfeld R (1998) Two nonproline cis peptide bonds may be important for factor XIII function. FEBS Lett 423:291-296.
73. Yee VC, Pedersen LC, Bishop PD, Stenkamp RE, Teller DC (1995) Structural evidence that the activation peptide is not released upon thrombin cleavage of factor XIII. Thromb Res 78:389-397.
74. Yee VC, Pedersen LC, Le Trong I, Bishop PD, Stenkamp RE, Teller DC (1994) Three-dimensional structure of a transglutaminase: human blood coagulation factor XIII. Proc Natl Acad Sci USA 91:7296-7300.
75. Muszbek L, Yee VC, Hevessy Z (1999) Blood coagulation factor XIII: structure and function. Thromb Res 94:271-305.
76. Lorand L, Jeong JM, Radek JT, Wilson J (1993) Human plasma factor XIII: subunit interactions and activation of zymogen. Meth Enzymol 222:22-35.
77. Radek JT, Jeong JM, Wilson J, Lorand L (1993) Association of the A subunits of recombinant placental factor XIII with the native carrier B subunits from human plasma. Biochemistry 32:3527-3534.
78. Hornyak TJ, Shafer JA (1991) Role of calcium ion in the generation of factor XIII activity. Biochemistry 30:6175-6182.
79. Lewis BA, Freyssinet JM, Holbrook JJ (1978) An equilibrium study of metal ion binding to human plasma coagulation factor XIII. Biochem J 169:397-402.
80. Muszbek L, Haramura G, Polgár J (1995) Transformation of cellular factor XIII into an active zymogen transglutaminase in thrombin-stimulated platelets. Thromb Haemost 73:702-705.
81. Muszbek L, Polgár J, Boda Z (1993) Platelet factor XIII becomes active without the release of activation peptide during platelet activation. Thromb Haemost 69:282-285.
82. Abdalla S, Lother H, Langer A, El Faramawy Y, Quitterer U (2004) Factor XIIIA transglutaminase crosslinks AT1 receptor dimers of monocytes at the onset of atherosclerosis. Cell 119:343-354.
83. Lewis SD, Janus TJ, Lorand L, Shafer JA (1985) Regulation of formation of factor XIIIa by its fibrin substrates. Biochemistry 24:6772-6777.
84. Achyuthan KE, Greenberg CS (1987) Identification of a guanosine triphosphate-binding site on guinea pig liver transglutaminase. Role of GTP and calcium ions in modulating activity. J Biol Chem 262:1901-1906.
85. Iismaa SE, Wu MJ, Nanda N, Church WB, Graham RM (2000) GTP binding and signaling by Gh/transglutaminase II involves distinct residues in a unique GTP-binding pocket. J Biol Chem 275:18259-18265.
86. Ivaskevicius V, Seitz R, Kohler HP, Schroeder V, Muszbek L, Ariens RAS, Seifried E, Oldenburg J (2007) International registry on factor XIII deficiency: a basis formed mostly on European data. Thromb Haemos 97:914-921.
87. Biswas A, Ivaskevicius V, Seitz R, Thomas A, Oldenburg J (2011) An update of the mutation profile of factor 13 A and B genes. Blood Rev 25:193-204.