Transglutaminase 2 is secreted from smooth muscle cells by transamidation-dependent microparticle formation

Amino Acids

Volumn 42, Issue 2-3, 2012, Pages 961-973

  Van Den Akker, Jeroen ^a   Van Weert, Angela ^a   Afink, Gijs ^a   Bakker, Erik N T P ^a   Van Der Pol, Edwin ^a,b   Böing, Anita N ^b   Nieuwland, Rienk ^b   VanBavel, Ed ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Flow cytometry; GFP; Microparticle; Smooth muscle cell; Transglutaminase

Indexed keywords

FIBRONECTIN; GREEN FLUORESCENT PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; AMIDE; FLUORESCENT DYE; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ARTICLE; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CHEMICAL MODIFICATION; CONTROLLED STUDY; ENZYME RELEASE; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MEMBRANE MICROPARTICLE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SMOOTH MUSCLE FIBER; TRANSAMIDATION; CELL FRACTIONATION; CELL LINE; CYTOLOGY; ENZYMOLOGY; METABOLISM; SECRETION; SMOOTH MUSCLE;

AMIDES; CELL LINE; FIBRONECTINS; FLOW CYTOMETRY; FLUORESCENT DYES; GTP-BINDING PROTEINS; HUMANS; MUSCLE, SMOOTH; SUBCELLULAR FRACTIONS; TRANSGLUTAMINASES;

EID: 84860478831     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-1010-3     Document Type: Article

References (65)

1. Aeschlimann D, Thomazy V (2000) Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. Connect Tissue Res 41:1-27 (Pubitemid 30246155)
2. Akimov SS, Belkin AM (2001a) Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 98:1567-1576
3. Akimov SS, Belkin AM (2001b) Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatinbinding domain of fibronectin: a role in TGFbeta-dependent matrix deposition. J Cell Sci 114:2989-3000 (Pubitemid 32821537)
4. Akimov SS, Krylov D, Fleischman LF, Belkin AM (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 148:825-838
5. Antonyak MA, Li B, Regan AD, Feng Q, Dusaban SS, Cerione RA (2009) Tissue transglutaminase is an essential participant in the epidermal growth factor-stimulated signaling pathway leading to cancer cell migration and invasion. J Biol Chem 284:17914-17925
6. Aras O, Shet A, Bach RR, Hysjulien JL, Slungaard A, Hebbel RP, Escolar G, Jilma B, Key NS (2004) Induction of microparticleand cell-associated intravascular tissue factor in human endotoxemia. Blood 103:4545-4553 (Pubitemid 38745982)
7. Bakker EN, Buus CL, Spaan JA, Perree J, Ganga A, Rolf TM, Sorop O, Bramsen LH, Mulvany MJ, VanBavel E (2005) Small artery remodeling depends on tissue-type transglutaminase. Circ Res 96:119-126 (Pubitemid 40095761)
8. Bakker EN, Pistea A, Spaan JA, Rolf T, de Vries CJ, van Rooijen N, Candi E, VanBavel E (2006) Flow-dependent remodeling of small arteries in mice deficient for tissue-type transglutaminase: possible compensation by macrophage-derived factor XIII. Circ Res 99:86-92 (Pubitemid 44297059)
9. Bakker EN, Pistea A, VanBavel E (2008) Transglutaminases in vascular biology: relevance for vascular remodeling and atherosclerosis. J Vasc Res 45:271-278 (Pubitemid 351793730)
10. Balklava Z, Verderio E, Collighan R, Gross S, Adams J, Griffin M (2002) 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 277:16567-16575 (Pubitemid 34967673)
11. Bobik A (2010) Circulating microparticles. Markers or participants in carotid artery remodelling? J Hypertens 28:673-675
12. Brisset AC, Terrisse AD, Dupouy D, Tellier L, Pech S, Navarro C, Sie P (2003) Shedding of active tissue factor by aortic smooth muscle cells (SMCs) undergoing apoptosis. Thromb Haemost 90:511-518 (Pubitemid 37138777)
13. Burnier L, Fontana P, Kwak BR, Angelillo-Scherrer A (2009) Cellderived microparticles in haemostasis and vascular medicine. Thromb Haemost 101:439-451
14. Carson SD, Perry GA, Pirruccello SJ (1994) Fibroblast tissue factor: calcium and ionophore induce shape changes, release of membrane vesicles, and redistribution of tissue factor antigen in addition to increased procoagulant activity. Blood 84: 526-534 (Pubitemid 24215953)
15. Chen JS, Mehta K (1999) Tissue transglutaminase: an enzyme with a split personality. Int J Biochem Cell Biol 31:817-836 (Pubitemid 29354079)
16. Chironi GN, Simon A, Boulanger CM, Dignat-George F, Hugel B, Megnien JL, Lefort M, Freyssinet JM, Tedgui A (2010) Circulating microparticles may influence early carotid artery remodeling. J Hypertens 28:789-796
17. Collighan RJ, Griffin M (2009) Transglutaminase 2 cross-linking of matrix proteins: biological significance and medical applications. Amino Acids 36:659-670
18. Di Pierro P, Mariniello L, Sorrentino A, Villalonga R, Chico B, Porta R (2010) Putrescine-polysaccharide conjugates as transglutaminase substrates and their possible use in producing crosslinked films. Amino Acids 38:669-675
19. el Alaoui S, Legastelois S, Roch AM, Chantepie J, Quash G (1991) Transglutaminase activity and N epsilon (gamma glutamyl) lysine isopeptide levels during cell growth: an enzymic and immunological study. Int J Cancer 48:221-226
20. Essayagh S, Brisset AC, Terrisse AD, Dupouy D, Tellier L, Navarro C, Arnal JF, Sie P (2005) Microparticles from apoptotic vascular smooth muscle cells induce endothelial dysfunction, a phenomenon prevented by beta3-integrin antagonists. Thromb Haemost 94:853-858 (Pubitemid 41489249)
21. Fesus L, Szondy Z (2005) Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 579:3297-3302 (Pubitemid 40804677)
22. Forsprecher J, Wang Z, Nelea V, Kaartinen MT (2009) Enhanced osteoblast adhesion on transglutaminase 2-crosslinked fibronectin. Amino Acids 36:747-753
23. Gaudry CA, Verderio E, Aeschlimann D, Cox A, Smith C, Griffin M (1999a) Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal betasandwich domain. J Biol Chem 274:30707-30714
24. Gaudry CA, Verderio E, Jones RA, Smith C, Griffin M (1999b) 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 252: 104-113 (Pubitemid 29485130)
25. Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: nature's biological glues. Biochem J 368:377-396 (Pubitemid 35454517)
26. Gundemir S, Johnson GV (2009) Intracellular localization and conformational state of transglutaminase 2: implications for cell death. PLoS ONE 4:e6123
27. Jayo A, Conde I, Lastres P, Jimenez-Yuste V, Gonzalez-Manchon C (2009) Possible role for cellular FXIII in monocyte-derived dendritic cell motility. Eur J Cell Biol 88:423-431
28. Jeong EM, Kim CW, Cho SY, Jang GY, Shin DM, Jeon JH, Kim IG (2009) Degradation of transglutaminase 2 by calcium-mediated ubiquitination responding to high oxidative stress. FEBS Lett 583:648-654
29. Johnson KA, Terkeltaub RA (2005) External GTP-bound transglutaminase 2 is a molecular switch for chondrocyte hypertrophic differentiation and calcification. J Biol Chem 280:15004-15012 (Pubitemid 40562853)
30. Jones RA, Nicholas B, Mian S, Davies PJ, Griffin M (1997) 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 110(Pt 19):2461-2472 (Pubitemid 127699160)
31. Kawai Y, Wada F, Sugimura Y, Maki M, Hitomi K (2008) Transglutaminase 2 activity promotes membrane resealing after mechanical damage in the lung cancer cell line A549. Cell Biol Int 32:928-934
32. Krawczyk PM, Stap J, Hoebe RA, van Oven CH, Kanaar R, Aten JA (2008) Analysis of the mobility of DNA double-strand breakcontaining chromosome domains in living mammalian cells. Methods Mol Biol 463:309-320
33. Leroyer AS, Isobe H, Leseche G, Castier Y, Wassef M, Mallat Z, Binder BR, Tedgui A, Boulanger CM (2007) Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J Am Coll Cardiol 49:772-777 (Pubitemid 46240708)
34. Leung CL, Green KJ, Liem RK (2002) Plakins: a family of versatile cytolinker proteins. Trends Cell Biol 12:37-45 (Pubitemid 34164155)
35. 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 (Pubitemid 34240531)
36. Liu Y, Wei L, Laskin DL, Fanburg BL (2010) Role of protein transamidation in serotonin-induced proliferation and migration of pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol (epub ahead of print)
37. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4:140-156 (Pubitemid 36172696)
38. Martinez MC, Tesse A, Zobairi F, Andriantsitohaina R (2005) Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol 288:H1004-H1009 (Pubitemid 40269999)
39. Medhat M, El-Zaiat SY, Radi Amr, Omar MF (2002) Application of fringes of equal chromatic order for investigating the effect of temperature on optical parameters of a GRIN optical fibre. J Opt A Pure Appl Opt 4:174-179 (Pubitemid 34272001)
40. Muesch A, Hartmann E, Rohde K, Rubartelli A, Sitia R, Rapoport TA (1990) A novel pathway for secretory proteins? Trends Biochem Sci 15:86-88 (Pubitemid 20067984)
41. Murthy SN, Iismaa S, Begg G, Freymann DM, Graham RM, Lorand L (2002) Conserved tryptophan in the core domain of transglutaminase is essential for catalytic activity. Proc Natl Acad Sci USA 99:2738-2742 (Pubitemid 34240530)
42. Nguyen M, Arkell J, Jackson CJ (1998) Active and tissue inhibitor of matrix metalloproteinase-free gelatinase B accumulates within human microvascular endothelial vesicles. J Biol Chem 273: 5400-5404 (Pubitemid 28108709)
43. Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC, Maquelin KN, Roozendaal KJ, Jansen PG, ten Have K, Eijsman L, Hack CE, Sturk A (1997) Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 96:3534-3541 (Pubitemid 27513430)
44. Park D, Choi SS, Ha KS (2010) Transglutaminase 2: a multifunctional protein in multiple subcellular compartments. Amino Acids 39:619-631
45. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5:e327
46. Ruan Q, Tucholski J, Gundemir S, Johnson Voll GV (2008) The differential effects of R580A mutation on transamidation and GTP binding activity of rat and human type 2 transglutaminase. Int J Clin Exp Med 1:248-259
47. Scarpellini A, Germack R, Lortat-Jacob H, Muramtsu T, Johnson TS, Billett E, Verderio EA (2009) Heparan sulphate proteoglycans are receptors for the cell-surface trafficking and biological activity of transglutaminase-2. J Biol Chem 284:18411-18423
48. Schecter AD, Spirn B, Rossikhina M, Giesen PL, Bogdanov V, Fallon JT, Fisher EA, Schnapp LM, Nemerson Y, Taubman MB (2000) Release of active tissue factor by human arterial smooth muscle cells. Circ Res 87:126-132 (Pubitemid 30616908)
49. Serrano K, Devine DV (2002) Intracellular factor XIII crosslinks platelet cytoskeletal elements upon platelet activation. Thromb Haemost 88:315-320 (Pubitemid 34873715)
50. Shah MD, Bergeron AL, Dong JF, Lopez JA (2008) Flow cytometric measurement of microparticles: pitfalls and protocol modifications. Platelets 19:365-372
51. Shirk RA, Church FC, Wagner WD (1996) Arterial smooth muscle cell heparan sulfate proteoglycans accelerate thrombin inhibition by heparin cofactor II. Arterioscler Thromb Vasc Biol 16:1138-1146 (Pubitemid 26299286)
52. Stampfuss JJ, Censarek P, Fischer JW, Schror K, Weber AA (2006) Rapid release of active tissue factor from human arterial smooth muscle cells under flow conditions. Arterioscler Thromb Vasc Biol 26:e34-e37 (Pubitemid 43732093)
53. Stap J, Krawczyk PM, van Oven CH, Barendsen GW, Essers J, Kanaar R, Aten JA (2008) Induction of linear tracks of DNA double-strand breaks by alpha-particle irradiation of cells. Nat Methods 5:261-266 (Pubitemid 351325651)
54. Sun Z, Martinez-Lemus LA, Hill MA, Meininger GA (2008) Extracellular matrix-specific focal adhesions in vascular smooth muscle produce mechanically active adhesion sites. Am J Physiol Cell Physiol 295:C268-C278 (Pubitemid 352755818)
55. Telci D, Wang Z, Li X, Verderio EA, Humphries MJ, Baccarini M, Basaga H, Griffin M (2008) Fibronectin-tissue transglutaminase matrix rescues RGD-impaired cell adhesion through syndecan-4 and beta1 integrin co-signaling. J Biol Chem 283:20937-20947
56. Tucholski J, Johnson GV (2002) Tissue transglutaminase differentially modulates apoptosis in a stimuli-dependent manner. J Neurochem 81:780-791 (Pubitemid 34809306)
57. van den Akker J, Schoorl MJ, Bakker EN, VanBavel E (2009) Small artery remodeling: current concepts and questions. J Vasc Res 47:183-202
58. Van Der Pol E, Hoekstra AG, Sturk A, Otto C, Van Leeuwen TG, Nieuwland R (2010) Optical and non-optical methods for detection and characterisation of microparticles and exosomes. J Thromb Haemost 8:2596-2607
59. VanWijk MJ, VanBavel E, Sturk A, Nieuwland R (2003) Microparticles in cardiovascular diseases. Cardiovasc Res 59:277-287 (Pubitemid 37272022)
60. Verderio EA, Telci D, Okoye A, Melino G, Griffin M (2003) A novel RGD-independent cel adhesion pathway mediated by fibronectin- bound tissue transglutaminase rescues cells from anoikis. J Biol Chem 278:42604-42614 (Pubitemid 37310534)
61. Verderio EA, Scarpellini A, Johnson TS (2009) Novel interactions of TG2 with heparan sulfate proteoglycans: reflection on physiological implications. Amino Acids 36:671-677
62. Yuan L, Siegel M, Choi K, Khosla C, Miller CR, Jackson EN, Piwnica-Worms D, Rich KM (2007) Transglutaminase 2 inhibitor, KCC009, disrupts fibronectin assembly in the extracellular matrix and sensitizes orthotopic glioblastomas to chemotherapy. Oncogene 26:2563-2573 (Pubitemid 46632005)
63. Zainelli GM, Dudek NL, Ross CA, Kim SY, Muma NA (2005) Mutant huntingtin protein: a substrate for transglutaminase 1, 2, and 3. J Neuropathol Exp Neurol 64:58-65 (Pubitemid 40189479)
64. Zemskov EA, Janiak A, Hang J, Waghray A, Belkin AM (2006) The role of tissue transglutaminase in cell-matrix interactions. Front Biosci 11:1057-1076 (Pubitemid 43253460)
65. Zemskov EA, Mikhailenko I, Hsia RC, Zaritskaya L, Belkin AM (2011) Unconventional secretion of tissue transglutaminase involves phospholipid-dependent delivery into recycling endosomes. PLoS ONE 6:e19414