Transglutaminase 2 regulates early chondrogenesis and glycosaminoglycan synthesis

Mechanisms of Development

Volumn 128, Issue 3-4, 2011, Pages 234-245

  Nurminsky, Dmitry ^a   Shanmugasundaram, Shobana ^a   Deasey, Stephanie ^a   Michaud, Claire ^b   Allen, Steven ^c   Hendig, Doris ^d   Dastjerdi, Akbar ^e   Francis West, Philippa ^e   Nurminskaya, Maria ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROYAL VETERINARY COLLEGE   (United Kingdom)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cell differentiation; Chondrocyte; Glycosaminoglycan; Mesenchymal cells; PKA; Transglutaminase 2

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AGGRECAN; ALKALINE PHOSPHATASE; CHONDROITIN SULFATE; COLLAGEN TYPE 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOSAMINOGLYCAN; KT 5720; MITOGEN ACTIVATED PROTEIN KINASE P38; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; PROTEOGLYCAN; TRANSCRIPTION FACTOR SOX9; TRANSFERASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VIRUS DNA; XYLOSYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; CHICKEN; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME REGULATION; GLYCOSAMINOGLYCAN METABOLISM; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RETROVIRUS INFECTION;

EID: 79952899749     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2010.11.007     Document Type: Article

References (51)

1. Aeschlimann D., Wetterwald A., Fleisch H., Paulsson M. Expression of tissue transglutaminase in skeletal tissues correlates with events of terminal differentiation of chondrocytes. J. Cell Biol. 1993, 120:1461-1470.
2. 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.
3. Bobick B.E., Kulyk W.M. Regulation of cartilage formation and maturation by mitogen-activated protein kinase signaling. Birth Defects Res. C Embryo Today 2008, 84:131-154.
4. Carrington J.L., Reddi A.H. Temporal changes in the response of chick limb bud mesodermal cells to transforming growth factor beta-type 1. Exp. Cell Res. 1990, 186:368-373.
5. Cassel D., Selinger Z. Mechanism of adenylate cyclase activation through the beta-adrenergic receptor: catecholamine-induced displacement of bound GDP by GTP. Proc. Natl. Acad. Sci. USA 1978, 75:4155-4159.
6. Chijiwa T., Mishima A., Hagiwara M., Sano M., Hayashi K., Inoue T., Naito K., Toshioka T., Hidaka H. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 1990, 265:5267-5272.
7. Chuang D.M. Beta-adrenergic receptor internalization and processing: role of transglutaminase and lysosomes. Mol. Cell. Biochem. 1984, 58:79-89.
8. Ciarmatori S., Kiepe D., Haarmann A., Huegel U., Tonshoff B. Signaling mechanisms leading to regulation of proliferation and differentiation of the mesenchymal chondrogenic cell line RCJ3.1C5.18 in response to IGF-I. J. Mol. Endocrinol. 2007, 38:493-508.
9. 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.
10. Daumer K.M., Tufan A.C., Tuan R.S. Long-term in vitro analysis of limb cartilage development: involvement of Wnt signaling. J. Cell. Biochem. 2004, 93:526-541.
11. Dierker T., Dreier R., Migone M., Hamer S., Grobe K. Heparan sulfate and transglutaminase activity are required for the formation of covalently cross-linked hedgehog oligomers. J. Biol. Chem. 2009, 284:32562-32571.
12. Ehrbar M., Rizzi S.C., Schoenmakers R.G., Miguel B.S., Hubbell J.A., Weber F.E., Lutolf M.P. Biomolecular hydrogels formed and degraded via site-specific enzymatic reactions. Biomacromolecules 2007, 8:3856-3866.
13. Faverman L., Mikhaylova L., Malmquist J., Nurminskaya M. Extracellular transglutaminase 2 activates beta-catenin signaling in calcifying vascular smooth muscle cells. FEBS Lett. 2008, 582:1552-1557.
14. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. Dev. Dyn. 1951, 195:231-272.
15. Jin E.J., Lee S.Y., Jung J.C., Bang O.S., Kang S.S. TGF-beta3 inhibits chondrogenesis of cultured chick leg bud mesenchymal cells via downregulation of connexin 43 and integrin beta4. J. Cell. Physiol. 2008, 214:345-353.
16. 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.
17. Johnson K.A., Terkeltaub R.A. External GTP-bound transglutaminase 2 is a molecular switch for chondrocyte hypertrophic differentiation and calcification. J. Biol. Chem. 2005, 280:15004-15012.
18. Johnson K.A., Rose D.M., Terkeltaub R.A. Factor XIIIA mobilizes transglutaminase 2 to induce chondrocyte hypertrophic differentiation. J. Cell Sci. 2008, 121(Pt. 13):2256-2264.
19. Jones M.E., Messersmith P.B. Facile coupling of synthetic peptides and peptide-polymer conjugates to cartilage via transglutaminase enzyme. Biomaterials 2007, 28:5215-5224.
20. Juliano R.L. Signal transduction by cell adhesion. Receptors and the cytoskeleton: funtions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 2002, 42:283-323.
21. Kim J.J., Conrad H.E. Properties of cultured chondrocytes obtained from histologically distinct zones of the chick embryo tibiotarsus. J. Biol. Chem. 1977, 252:8292-8299.
22. Koseki-Kuno S., Yamakawa M., Dickneite G., Ichinose A. Factor XIII A subunit-deficient mice developed severe uterine bleeding events and subsequent spontaneous miscarriages. Blood 2003, 102:4410-4412.
23. Koziel L., Kunath M., Kelly O.G., Vortkamp A. Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev. Cell 2004, 6:801-813.
24. Kuhn J., Prante C., Schön S., Götting C., Kleesiek K. Measurement of fibrosis marker xylosyltransferase I activity by HPLC electrospray ionization tandem mass spectrometry. Clin. Chem. 2006, 52:2243-2249.
25. Logan C., Francis-West P. Gene transfer in avian embryos using replication-competent retroviruses. Methods Mol. Biol. 2008, 461:363-376.
26. Lorand L., Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 2003, 4:140-156.
27. Mello M.A., Tuan R.S. Effects of TGF-beta1 and triiodothyronine on cartilage maturation: in vitro analysis using long-term high-density micromass cultures of chick embryonic limb mesenchymal cells. J. Orthop. Res. 2006, 24:2095-2105.
28. McHale M.K., Setton L.A., Chilkoti A. Synthesis and in vitro evaluation of enzymatically cross-linked elastin-like polypeptide gels for cartilaginous tissue repair. Tissue Eng. 2005, 11:1768-1779.
29. McLeod M.J. Differential staining of cartilage and bone in whole mouse fetuses by Alcian Blue and Alizarin Red S. Teratology 1980, 22:299-301.
30. 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.
31. 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.
32. Nunes I., Gleizes P.E., Metz C.N., Rifkin D.B. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J. Cell Biol. 1997, 136:1151-1163.
33. Nurminskaya M., Linsenmayer T.F. Identification and characterization of up-regulated genes during chondrocyte hypertrophy. Dev. Dyn. 1996, 206:60-271.
34. Nurminskaya M.V., Linsenmayer T.F. Immunohistological analysis of transglutaminase factor XIIIA expression in mouse embryonic growth plate. J. Orthop. Res. 2002, 20:575-578.
35. Nurminskaya M., Kaartinen M.T. Transglutaminases in mineralized tissues. Front. Biosci. 2006, 11:1591-1606.
36. Nurminskaya M., Magee C., Nurminsky D., Linsenmayer T.F. Plasma transglutaminase in hypertrophic chondrocytes: expression and cell-specific intracellular activation produce cell death and externalization. J. Cell Biol. 1998, 142:1135-1144.
37. Nurminskaya M., Magee C., Faverman L., Linsenmayer T.F. Chondrocyte-derived transglutaminase promotes maturation of preosteoblasts in periosteal bone. Dev. Biol. 2003, 263:139-152.
38. Oberlender S.A., Tuan R.S. Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 1994, 120:177-187.
39. Ooira A., Kimata K., Suzuki S., Takata K., Suzuki I. A correlation between synthetic activities for matrix macromolecules and specific stages of cyto-differentiation in developing cartilage. J. Biol. Chem. 1974, 249(5):1637-1645.
40. 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 July 3, 284(27):18411-18423.
41. Schmid T.M., Linsenmayer T.F. Developmental acquisition of type X collagen in the embryonic chick tibiotarsus. Dev. Biol. 1985, 107:373-381.
42. Tanaka K., Yokosaki Y., Higashikawa F., Saito Y., Eboshida A., Ochi M. The integrin alpha5beta1 regulates chondrocyte hypertrophic differentiation induced by GTP-bound transglutaminase 2. Matrix Biol. 2007, 26(6):409-418.
43. Tarantino U., Oliva F., Taurisano G., Orlandi A., Pietroni V., Candi E., Melino G., Maffulli N. FXIIIA and TGF-beta over-expression produces normal musculo-skeletal phenotype in TG2-/- mice. Amino Acids 2009, 36:679-684.
44. Thomazy V.A., Davies P.J. Expression of tissue transglutaminase in the developing chicken limb is associated both with apoptosis and endochondral ossification. Cell Death Differ. 1999, 6:146-154.
45. Trigwell S.M., Lynch P.T., Griffin M., Hargreaves A.J., amd Bonner P.L. An improved colorimetric assay for the measurement of transglutaminase (type II)-(gamma-glutamyl) lysine cross-linking activity. Anal. Biochem. 2004, 330:164-166.
46. Watts R.E., Siegel M., Khosla C. Structure-activity relationship analysis of the selective Inhibition of transglutaminase 2 by dihydroisoxazoles. J. Med. Chem. 2006, 49:7493-7501.
47. Woods A., Khan S., Beier F. C-type natriuretic peptide regulates cellular condensation and glycosaminoglycan synthesis during chondrogenesis. Endocrinology 2007, 148:5030-5041.
48. Xu L., Hynes R.O. GPR56 and TG2: possible roles in suppression of tumor growth by the microenvironment. Cell Cycle 2007, 6:160-165.
49. Yoon Y.M., Oh C.D., Kang S.S., Chun J.S. Protein kinase A regulates chondrogenesis of mesenchymal cells at the post-precartilage condensation stage via protein kinase C-alpha signaling. J. Bone Miner. Res. 2000, 15:2197-2205.
50. Za'ka'ny R., Szucs K., Bako' E., Felszeghy S., Czifra G., Bi'ro' T., Mo'dis L., Gergely P. Protein phosphatase 2A is involved in the regulation of protein kinase A signaling pathway during in vitro chondrogenesis. Exp. Cell Res. 2002, 275:1-8.
51. Zhen X., Wei L., Wu Q., Zhang Y., Chen Q. Mitogen-activated protein kinase p38 mediates regulation of chondrocyte differentiation by parathyroid hormone. J. Biol. Chem. 2001, 276:4879-4885.