Home LiteratureArticle Details
PMID: 8095503 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Expression of tissue transglutaminase in skeletal tissues correlates with events of terminal differentiation of chondrocytes.

The Journal of cell biology ·Vol. 120 ·No. 6 ·1993-03-00 ·Pages 1461-70

Aeschlimann D, Wetterwald A, Fleisch H, Paulsson M

Abstract

Calcifying cartilages show a restricted expression of tissue transglutaminase. Immunostaining of newborn rat paw bones reveals expression only in the epiphyseal growth plate. Tissue transglutaminase appears first intracellularly in the proliferation/maturation zone and remains until calcification of the tissue in the lower hypertrophic zone. Externalization occurs before mineralization. Subsequently, the enzyme is present in the interterritorial matrix during provisional calcification and in the calcified cartilage cores of bone trabeculae. In trachea, mineralization occurring with maturation in the center of the cartilage is accompanied by expression of tissue transglutaminase at the border of the hydroxyapatite deposits. Transglutaminase activity also shows a restricted distribution in cartilage, similar to the one observed for tissue transglutaminase protein. Analysis of tissue homogenates showed that the enzyme is present in growth plate cartilage, but not in articular cartilage, and recognizes a limited set of substrate proteins. Osteonectin is coexpressed with tissue transglutaminase both in the growth plate and in calcifying tracheal cartilage and is a specific substrate for tissue transglutaminase in vitro. Tissue transglutaminase expression in skeletal tissues is strictly regulated, correlates with chondrocyte differentiation, precedes cartilage calcification, and could lead to cross-linking of the mineralizing matrix.

MeSH Terms
Animals Animals, Newborn Bone Development Bone and Bones/cytology,enzymology Calcification, Physiologic Cartilage, Articular/cytology,enzymology Cattle Cell Differentiation Electrophoresis, Polyacrylamide Gel Growth Plate/cytology,enzymology Molecular Weight Osteonectin/analysis Rats Trachea Transglutaminases/analysis,metabolism
Chemicals
Osteonectin Transglutaminases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Aeschlimann D
M. E. Müller-Institute for Biomechanics, University of Bern, Switzerland.
Wetterwald A
Fleisch H
Paulsson M
References (43)
43 references, click to expand
  1. Identification of Gln726 in nidogen as the amine acceptor in transglutaminase-catalyzed cross-linking of laminin-nidogen complexes.
    J Biol Chem. 1992 Jun 5;267(16):11316-21 PMID: 1350783
  2. High-affinity and low-affinity calcium binding and stability of the multidomain extracellular 40-kDa basement membrane glycoprotein (BM-40/SPARC/osteonectin).
    Eur J Biochem. 1992 Apr 1;205(1):233-40 PMID: 1555584
  3. Investigations of ageing in costal and tracheal cartilage of rats.
    Z Zellforsch Mikrosk Anat. 1974 Mar 21;147(4):505-27 PMID: 4135295
  4. Fluorescent labeling of proteins and a plasma membrane using cycloheptaamylose-dansyl chloride complex.
    Anal Biochem. 1974 Oct;61(2):632-7 PMID: 4423747
  5. Catalytic formation of epsilon-(gamma-glutamyl)lysine in guinea pig liver transglutaminase.
    Biochem Biophys Res Commun. 1977 Sep 9;78(1):1-7 PMID: 20879
  6. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  7. Mineral and collagen-binding proteins of fetal calf bone.
    J Biol Chem. 1981 Oct 25;256(20):10403-8 PMID: 6793579
  8. Osteonectin, a bone-specific protein linking mineral to collagen.
    Cell. 1981 Oct;26(1 Pt 1):99-105 PMID: 7034958
  9. Transglutaminases.
    Mol Cell Biochem. 1984;58(1-2):9-35 PMID: 6143256
  10. Keratinocyte-specific transglutaminase of cultured human epidermal cells: relation to cross-linked envelope formation and terminal differentiation.
    Cell. 1985 Mar;40(3):685-95 PMID: 2578891
  11. Developmental acquisition of type X collagen in the embryonic chick tibiotarsus.
    Dev Biol. 1985 Feb;107(2):373-81 PMID: 3882482
  12. Transglutaminase-sensitive glutamine residues of human plasma fibronectin revealed by studying its proteolytic fragments.
    Eur J Biochem. 1986 Jan 15;154(2):371-4 PMID: 2867902
  13. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  14. Structural properties of guinea pig liver transglutaminase.
    J Biol Chem. 1971 Feb 25;246(4):1093-8 PMID: 5543674
  15. Isolation and characterization of a collagen from chick cartilage containing three identical alpha chains.
    Biochemistry. 1971 Apr 27;10(9):1652-9 PMID: 4325605
  16. Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell 'culture shock' glycoprotein of Mr 43,000.
    EMBO J. 1986 Jul;5(7):1465-72 PMID: 3755680
  17. Purification and tissue distribution of a small protein (BM-40) extracted from a basement membrane tumor.
    Eur J Biochem. 1986 Dec 1;161(2):455-64 PMID: 3536514
  18. Identification of a substrate site for liver transglutaminase on the aminopropeptide of type III collagen.
    J Biol Chem. 1987 Jan 25;262(3):1022-4 PMID: 2879837
  19. The calcification of cartilage matrix in chondrocyte culture: studies of the C-propeptide of type II collagen (chondrocalcin).
    J Cell Biol. 1987 May;104(5):1435-41 PMID: 3494735
  20. Purification and partial characterization of small proteoglycans I and II, bone sialoproteins I and II, and osteonectin from the mineral compartment of developing human bone.
    J Biol Chem. 1987 Jul 15;262(20):9702-8 PMID: 3597437
  21. Calcium binding domains and calcium-induced conformational transition of SPARC/BM-40/osteonectin, an extracellular glycoprotein expressed in mineralized and nonmineralized tissues.
    Biochemistry. 1987 Nov 3;26(22):6958-65 PMID: 3427055
  22. Developmental expression of 2ar (osteopontin) and SPARC (osteonectin) RNA as revealed by in situ hybridization.
    J Cell Biol. 1988 Feb;106(2):441-50 PMID: 3339096
  23. Osteonectin cDNA sequence reveals potential binding regions for calcium and hydroxyapatite and shows homologies with both a basement membrane protein (SPARC) and a serine proteinase inhibitor (ovomucoid).
    Proc Natl Acad Sci U S A. 1988 May;85(9):2919-23 PMID: 2834720
  24. The binding sites on fibrin(ogen) for guinea pig liver transglutaminase are similar to those of blood coagulation factor XIII. Characterization of the binding of liver transglutaminase to fibrin.
    J Biol Chem. 1988 Oct 5;263(28):14296-301 PMID: 2902081
  25. The glutamine residues reactive in transglutaminase-catalyzed cross-linking of involucrin.
    J Biol Chem. 1988 Dec 5;263(34):18093-8 PMID: 2461365
  26. Vitronectin is a substrate for transglutaminases.
    Biochem Biophys Res Commun. 1988 Nov 30;157(1):115-20 PMID: 2461707
  27. Structure and biology of cartilage and bone matrix noncollagenous macromolecules.
    FASEB J. 1989 Jul;3(9):2042-51 PMID: 2663581
  28. Localization of osteonectin expression in human fetal skeletal tissues by in situ hybridization.
    Calcif Tissue Int. 1989 Sep;45(3):146-52 PMID: 2505905
  29. Physiological mechanisms adopted by chondrocytes in regulating longitudinal bone growth in rats.
    J Physiol. 1989 Jul;414:55-71 PMID: 2607442
  30. Sequence location of a putative transglutaminase cross-linking site in human vitronectin.
    FEBS Lett. 1990 Mar 26;262(2):269-74 PMID: 1692291
  31. Structure of transglutaminases.
    J Biol Chem. 1990 Aug 15;265(23):13411-4 PMID: 1974250
  32. Human bone contains type III collagen, type VI collagen, and fibrillin: type III collagen is present on specific fibers that may mediate attachment of tendons, ligaments, and periosteum to calcified bone cortex.
    J Histochem Cytochem. 1991 Jan;39(1):59-69 PMID: 1983874
  33. Association between proteoglycans and matrix vesicles in the extracellular matrix of growth plate cartilage.
    J Biol Chem. 1991 Jan 15;266(2):1187-94 PMID: 1985942
  34. Immunoelectrophoretic characterizations of the cross-linking of fibrinogen and fibrin by factor XIIIa and tissue transglutaminase. Identification of a rapid mode of hybrid alpha-/gamma-chain cross-linking that is promoted by the gamma-chain cross-linking.
    J Biol Chem. 1991 Apr 5;266(10):6429-37 PMID: 1672529
  35. Characterization of human loricrin. Structure and function of a new class of epidermal cell envelope proteins.
    J Biol Chem. 1991 Apr 5;266(10):6626-36 PMID: 2007607
  36. Osteopontin, a substrate for transglutaminase and factor XIII activity.
    Biochem Biophys Res Commun. 1991 Jun 28;177(3):1205-10 PMID: 1676261
  37. Extravascular fibrin formation and dissolution in synovial tissue of patients with osteoarthritis and rheumatoid arthritis.
    Arthritis Rheum. 1991 Aug;34(8):996-1005 PMID: 1677574
  38. Cross-linking of laminin-nidogen complexes by tissue transglutaminase. A novel mechanism for basement membrane stabilization.
    J Biol Chem. 1991 Aug 15;266(23):15308-17 PMID: 1678389
  39. Recombinant expression and properties of the human calcium-binding extracellular matrix protein BM-40.
    Eur J Biochem. 1991 Sep 1;200(2):529-36 PMID: 1653704
  40. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues.
    FASEB J. 1991 Dec;5(15):3071-7 PMID: 1683845
  41. Localization of cellular transglutaminase on the extracellular matrix after wounding: characteristics of the matrix bound enzyme.
    J Cell Physiol. 1991 Dec;149(3):375-82 PMID: 1683874
  42. Apoptosis: molecular mechanisms in programmed cell death.
    Eur J Cell Biol. 1991 Dec;56(2):170-7 PMID: 1802705
  43. Increased transglutaminase in the aortas of cholesterol-fed rabbits: occurrence of buffer soluble and insoluble forms and an inhibitor.
    Biochem Cell Biol. 1991 Dec;69(12):821-7 PMID: 1687845
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1993-03-00
Pages
1461-70
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119748
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]