Transglutaminase 2 is central to induction of the arterial calcification program by smooth muscle cells

Circulation Research

Volumn 102, Issue 5, 2008, Pages 529-537

  Johnson, Kristen A ^a   Polewski, Monika ^a   Terkeltaub, Robert A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Atherosclerosis; Laminin; Matrix Gla protein; Osteopontin; Osteoprotegerin; Smooth muscle cells

Indexed keywords

LAMININ; OSTEOCALCIN; OSTEOPONTIN; OSTEOPROTEGERIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; SODIUM PHOSPHATE COTRANSPORTER 1; TRANSFERASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTERY CALCIFICATION; ARTICLE; CARTILAGE CELL; CATALYSIS; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER;

ANIMALS; AORTA; ARTERIES; ATHEROSCLEROSIS; CALCINOSIS; CALCIUM-BINDING PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; EXTRACELLULAR MATRIX PROTEINS; GTP-BINDING PROTEINS; HUMANS; LAMININ; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; ORGAN CULTURE TECHNIQUES; OSTEOPONTIN; OSTEOPROTEGERIN; PHOSPHATES; TRANSGLUTAMINASES;

EID: 40949152051     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.154260     Document Type: Article

References (56)

1. Bakker EN, Buus CL, Spaan JA, Perree J, Ganga A, Rolf TM, Sorop O, Bramsen LH, Mulvany MJ, Vanbavel E. Small artery remodeling depends on tissue-type transglutaminase. Circ Res. 2005;96:119-126.
2. Raines EW. PDGF and cardiovascular disease. Cytokine Growth Factor Rev. 2004;15:237-254.
3. Raines EW, Koyama H, Carragher NO. The extracellular matrix dynamically regulates smooth muscle cell responsiveness to PDGF. Ann N Y Acad Sci. 2000;902:39-51.
4. Steitz SA, Speer MY, Curinga G, Yang HY, Haynes P, Aebersold R, Schinke T, Karsenty G, Giachelli CM. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ Res. 2001;89:1147-1154.
5. Abedin M, Tintut Y, Demer LL. Vascular calcification: mechanisms and clinical ramifications. Arterioscler Thromb Vasc Biol. 2004;24:1161-1170.
6. Speer MY, Chien YC, Quan M, Yang HY, Vali H, McKee MD, Giachelli CM. Smooth muscle cells deficient in osteopontin have enhanced susceptibility to calcification in vitro. Cardiovasc Res. 2005;66:324-333.
7. Yang H, Curinga G, Giachelli CM. Elevated extracellular calcium levels induce smooth muscle cell matrix mineralization in vitro. Kidney Int. 2004;66:2293-2299.
8. i depletion promotes spontaneous aortic calcification in NPP1-/- mice. Arterioscler Thromb Vasc Biol. 2005;25:686-691.
9. Tintut Y, Alfonso Z, Saini T, Radcliff K, Watson K, Bostrom K, Demer LL. Multilineage potential of cells from the artery wall. Circulation. 2003;108:2505-2510.
10. Shao JS, Cheng SL, Pingsterhaus JM, Charlton-Kachigian N, Loewy AP, Towler DA. Msx2 promotes cardiovascular calcification by activating paracrine Wnt signals. J Clin Invest. 2005;115:1210-1220.
11. Towler DA, Bidder M, Latifi T, Coleman T, Semenkovich CF. Diet-induced diabetes activates an osteogenic gene regulatory program in the aortas of low density lipoprotein receptor-deficient mice. J Biol Chem. 1998;273:30427-30434.
12. Alexander MY, Wilkinson FL, Kirton JP, Rock CF, Collett GD, Jeziorska M, Smyth JV, Heagerty AM, Canfield AE. Identification and characterization of vascular calcification-associated factor, a novel gene upregulated during vascular calcification in vitro and in vivo. Arterioscler Thromb Vasc Biol. 2005;25:1851-1857.
13. Rutsch F, Ruf N, Vaingankar S, Toliat MR, Suk A, Hohne W, Schauer G, Lehmann M, Roscioli T, Schnabel D, Epplen JT, Knisely A, Superti-Furga A, McGill J, Filippone M, Sinaiko AR, Vallance H, Hinrichs B, Smith W, Ferre M, Terkeltaub R, Nurnberg P. Mutations in ENPP1 are associated with 'idiopathic' infantile arterial calcification. Nat Genet. 2003;34:379-381.
14. Speer MY, McKee MD, Guldberg RE, Liaw L, Yang HY, Tung E, Karsenty G, Giachelli CM. Inactivation of the osteopontin gene enhances vascular calcification of matrix Gla protein-deficient mice: evidence for osteopontin as an inducible inhibitor of vascular calcification in vivo. J Exp Med. 2002;196:1047-1055.
15. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, Boyle WJ, Simonet WS. Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998;12:1260-1268.
16. Bennett BJ, Scatena M, Kirk EA, Rattazzi M, Varon RM, Averill M, Schwartz SM, Giachelli CM, Rosenfeld ME. Osteoprotegerin inactivation accelerates advanced atherosclerotic lesion progression and calcification in older ApoE-/- mice. Arterioscler Thromb Vasc Biol. 2006;26:2117-2124.
17. Johnson KA, van Etten D, Nanda N, Graham RM, Terkeltaub RA. Distinct transglutaminase 2-independent and transglutaminase 2-dependent pathways mediate articular chondrocyte hypertrophy. J Biol Chem. 2003;278:18824-18832.
18. Johnson KA, Terkeltaub RA. External GTP-bound transglutaminase 2 is a molecular switch for chondrocyte hypertrophic differentiation and calcification. J Biol Chem. 2005;280:15004-15012.
19. Nurminskaya M, Kaartinen MT. Transglutaminases in mineralized tissues. Front Biosci. 2006;11:1591-1606.
20. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol. 2003;4:140-156.
21. Merz D, Liu R, Johnson K, Terkeltaub R. IL-8/CXCL8 and growth-related oncogene alpha/CXCL1 induce chondrocyte hypertrophic differentiation. J Immunol. 2003;171:4406-4415.
22. Zemskov EA, Janiak A, Hang J, Waghray A, Belkin AM. The role of tissue transglutaminase in cell-matrix interactions. Front Biosci. 2006;11:1057-1076.
23. 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.
24. Auld GC, Ritchie H, Robbie LA, Booth NA. Thrombin upregulates tissue transglutaminase in endothelial cells: a potential role for tissue transglutaminase in stability of atherosclerotic plaque. Arterioscler Thromb Vasc Biol. 2001;21:1689-1694.
25. Boisvert WA, Rose DM, Boullier A, Quehenberger O, Sydlaske A, Johnson KA, Curtiss LK, Terkeltaub R. Leukocyte Transglutaminase 2 Expression Limits Atherosclerotic Lesion Size. Arterioscler Thromb Vasc Biol. 2006;26:563-569.
26. Haroon ZA, Wannenburg T, Gupta M, Greenberg CS, Wallin R, Sane DC. Localization of tissue transglutaminase in human carotid and coronary artery atherosclerosis: implications for plaque stability and progression. Lab Invest. 2001;81:83-93.
27. Nanda N, Iismaa SE, Owens WA, Husain A, Mackay F, Graham RM. Targeted inactivation of Gh/tissue transglutaminase II. J Biol Chem. 2001;276:20673-20678.
28. Bakker EN, Pistea A, Spaan JA, Rolf T, de Vries CJ, van Rooijen N, Candi E, VanBavel E. Flow-dependent remodeling of small arteries in mice deficient for tissue-type transglutaminase: possible compensation by macrophage-derived factor XIII. Circ Res. 2006;99:86-92.
29. Jono S, McKee MD, Murry CE, Shioi A, Nishizawa Y, Mori K, Morii H, Giachelli CM. Phosphate regulation of vascular smooth muscle cell calcification. Circ Res. 2000;87:e10-e17.
30. Thyberg J, Hultgardh-Nilsson A, Kallin B. Inhibitors of ADP-ribosylation suppress phenotypic modulation and proliferation of smooth muscle cells cultured from rat aorta. Differentiation. 1995;59:243-252.
31. Bonin LR, Madden K, Shera K, Ihle J, Matthews C, Aziz S, Perez-Reyes N, McDougall JK, Conroy SC. Generation and characterization of human smooth muscle cell lines derived from atherosclerotic plaque. Arterioscler Thromb Vasc Biol. 1999;19:575-587.
32. Thyberg J. Differentiated properties and proliferation of arterial smooth muscle cells in culture. Int Rev Cytol. 1996;169:183-265.
33. Lomashvili KA, Cobbs S, Hennigar RA, Hardcastle KI, O'Neill WC. Phosphate-induced vascular calcification: role of pyrophosphate and osteopontin. J Am Soc Nephrol. 2004;15:1392-1401.
34. Madi A, Karpati L, Kovacs A, Muszbek L, Fesus L. High-throughput scintillation proximity assay for transglutaminase activity measurement. Anal Biochem. 2005;343:256-262.
35. Murshed M, Harmey D, Millan JL, McKee MD, Karsenty G. Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev. 2005;19:1093-1104.
36. Li X, Yang HY, Giachelli CM. Role of the sodium-dependent phosphate cotransporter, Pit-1, in vascular smooth muscle cell calcification. Circ Res. 2006;98:905-912.
37. Villa-Bellosta R, Bogaert YE, Levi M, Sorribas V. Characterization of phosphate transport in rat vascular smooth muscle cells. Implications for vascular calcification. Arterioscler Thromb Vasc Biol. 2007;27:1030-1036.
38. Beck GR Jr. Inorganic phosphate as a signaling molecule in osteoblast differentiation. J Cell Biochem. 2003;90:234-243.
39. Bostrom K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 1993;91:1800-1809.
40. Suzuki A, Ghayor C, Guicheux J, Magne D, Quillard S, Kakita A, Ono Y, Miura Y, Oiso Y, Itoh M, Caverzasio J. Enhanced expression of the inorganic phosphate transporter Pit-1 is involved in BMP-2-induced matrix mineralization in osteoblast-like cells. J Bone Miner Res. 2006;21:674-683.
41. Chau DY, Collighan RJ, Verderio EA, Addy VL, Griffin M. The cellular response to transglutaminase-cross-linked collagen. Biomaterials. 2005;26:6518-6529.
42. Kaartinen MT, Pirhonen A, Linnala-Kankkunen A, Maenpaa PH. Cross-linking of osteopontin by tissue transglutaminase increases its collagen binding properties. J Biol Chem. 1999;274:1729-1735.
43. Rosenthal AK, Gohr CM, Uzuki M, Masuda I. Osteopontin promotes pathologic mineralization in articular cartilage. Matrix Biol. 2007;26:96-105.
44. Kaartinen MT, Murshed M, Karsenty G, McKee MD. Osteopontin upregulation and polymerization by transglutaminase 2 in calcified arteries of matrix Gla protein-deficient mice. J Histochem Cytochem. 2007;55:375-386.
45. Guilluy C, Rolli-Derkinderen M, Tharaux PL, Melino G, Pacaud P, Loirand G. Transglutaminase-dependent RhoA activation and depletion by serotonin in vascular smooth muscle cells. J Biol Chem. 2007;282:2918-2928.
46. Collett GD, Sage AP, Kirton JP, Alexander MY, Gilmore AP, Canfield AE. Axl/phosphatidylinositol 3-kinase signaling inhibits mineral deposition by vascular smooth muscle cells. Circ Res. 2007;100:502-509.
47. Kang SK, Yi KS, Kwon NS, Park KH, Kim UH, Baek KJ, Im MJ. Alpha1B-adrenoceptor signaling and cell motility: GTPase function of Gh/transglutaminase 2 inhibits cell migration through interaction with cytoplasmic tail of integrin alpha subunits. J Biol Chem. 2004;279:36593-36600.
48. Janiak A, Zemskov EA, Belkin AM. Cell surface transglutaminase promotes RhoA activation via integrin clustering and suppression of the Src-p190RhoGAP signaling pathway. Mol Biol Cell. 2006;17:1606-1619.
49. Woods A, Beier F. RhoA/ROCK signaling regulates chondrogenesis in a context-dependent manner. J Biol Chem. 2006;281:13134-13140.
50. Aeschlimann D, Koeller MK, Allen-Hoffmann BL, Mosher DF. Isolation of a cDNA encoding a novel member of the transglutaminase gene family from human keratinocytes. Detection and identification of transglutaminase gene products based on reverse transcription-polymerase chain reaction with degenerate primers. J Biol Chem. 1998;273:3452-3460.
51. Lai CF, Seshadri V, Huang K, Shao JS, Cai J, Vattikuti R, Schumacher A, Loewy AP, Denhardt DT, Rittling SR, Towler DA. An osteopontin-NADPH oxidase signaling cascade promotes pro-matrix metalloproteinase 9 activation in aortic mesenchymal cells. Circ Res. 2006;98:1479-1489.
52. Akimov SS, Belkin AM. Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood. 2001;98:1567-1576.
53. 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.
54. Soehnlein O, Eskafi S, Schmeisser A, Kloos H, Daniel WG, Garlichs CD. Atorvastatin induces tissue transglutaminase in human endothelial cells. Biochem Biophys Res Commun. 2004;322:105-109.
55. Adams LD, Geary RL, Li J, Rossini A, Schwartz SM. Expression profiling identifies smooth muscle cell diversity within human intima and plaque fibrous cap: loss of RGS5 distinguishes the cap. Arterioscler Thromb Vasc Biol. 2006;26:319-325.
56. Mahoney WM, Schwartz SM. Defining smooth muscle cells and smooth muscle injury. J Clin Invest. 2005;115:221-224.