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The FASEB Journal, Vol 5, 3071-3077, Copyright © 1991 by The Federation of American Societies for Experimental Biology

REVIEWS

Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues

CS Greenberg, PJ Birckbichler and RH Rice
Duke University Medical Center, Durham, North Carolina 27710.

Transglutaminases catalyze the posttranslational modification of proteins by transamidation of available glutamine residues. This action results primarily in the formation of epsilon-(gamma-glutamyl)lysine cross-links but includes the incorporation of polyamines into suitable protein substrates as well. The covalent isopeptide crosslink is stable and resistant to proteolysis, thereby increasing the resistance of tissue to chemical, enzymatic, and mechanical disruption. The plasma transglutaminase, factor XIIIa, is formed at sites of blood coagulation and impedes blood loss by stabilizing the fibrin clot. The squamous epithelium constituting the protective callus layer of skin is formed by the action of keratinocyte transglutaminase (TGK) and epidermal transglutaminase (TGE). The tissue transglutaminase (TGC) is a cytoplasmic enzyme present in many cells including those in the blood vessel wall. TGC function is unknown, although it could function to stabilize intra- and extra-cellular molecules in a wide variety of physiologic or pathologic processes. The amino acid sequences of factor XIII, TGC, and TGK establish them as a homologous gene family and also reveal a striking homology to the erythrocyte membrane protein, band 4.2. This review summarizes the current information on structures, functions, and evolution of the most prominent members of this gene family.


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A. Di Venere, A. Rossi, F. De Matteis, N. Rosato, A. F. Agro, and G. Mei
Opposite Effects of Ca2+ and GTP Binding on Tissue Transglutaminase Tertiary Structure
J. Biol. Chem., February 11, 2000; 275(6): 3915 - 3921.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Nemes, M. Demeny, L. N. Marekov, L. Fesus, and P. M. Steinert
Cholesterol 3-Sulfate Interferes with Cornified Envelope Assembly by Diverting Transglutaminase 1 Activity from the Formation of Cross-links and Esters to the Hydrolysis of Glutamine
J. Biol. Chem., January 28, 2000; 275(4): 2636 - 2646.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
N. D. Lazo and D. T. Downing
A Mixture of alpha -Helical and 310-Helical Conformations for Involucrin in the Human Epidermal Corneocyte Envelope Provides a Scaffold for the Attachment of Both Lipids and Proteins
J. Biol. Chem., December 24, 1999; 274(52): 37340 - 37344.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
P. M. Steinert and L. N. Marekov
Initiation of Assembly of the Cell Envelope Barrier Structure of Stratified Squamous Epithelia
Mol. Biol. Cell, December 1, 1999; 10(12): 4247 - 4261.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
S. Oliverio, A. Amendola, C. Rodolfo, A. Spinedi, and M. Piacentini
Inhibition of "Tissue" Transglutaminase Increases Cell Survival by Preventing Apoptosis
J. Biol. Chem., November 26, 1999; 274(48): 34123 - 34128.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Hiiragi, H. Sasaki, A. Nagafuchi, H. Sabe, S. C. Shen, M. Matsuki, K. Yamanishi, and S. Tsukita
Transglutaminase Type 1 and Its Cross-linking Activity Are Concentrated at Adherens Junctions in Simple Epithelial Cells
J. Biol. Chem., November 26, 1999; 274(48): 34148 - 34154.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. A. Gaudry, E. Verderio, D. Aeschlimann, A. Cox, C. Smith, and M. Griffin
Cell Surface Localization of Tissue Transglutaminase Is Dependent on a Fibronectin-binding Site in Its N-terminal beta -Sandwich Domain
J. Biol. Chem., October 22, 1999; 274(43): 30707 - 30714.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S.-Y. Kim, P. Grant, J.-H. Lee, H. C. Pant, and P. M. Steinert
Differential Expression of Multiple Transglutaminases in Human Brain. INCREASED EXPRESSION AND CROSS-LINKING BY TRANSGLUTAMINASES 1 AND 2 IN ALZHEIMER'S DISEASE
J. Biol. Chem., October 22, 1999; 274(43): 30715 - 30721.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. N. P. Murthy, J. W. Lomasney, E. C. Mak, and L. Lorand
Interactions of Gh/transglutaminase with phospholipase Cdelta 1 and with GTP
PNAS, October 12, 1999; 96(21): 11815 - 11819.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
Z. A. HAROON, J. M. HETTASCH, T.-S. LAI, M. W. DEWHIRST, and C. S. GREENBERG
Tissue transglutaminase is expressed, active, and directly involved in rat dermal wound healing and angiogenesis
FASEB J, October 1, 1999; 13(13): 1787 - 1795.
[Abstract] [Full Text]

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 J. Am. Soc. Nephrol.Home page
T. S. JOHNSON, N. J. SKILL, A. M. EL NAHAS, S. D. OLDROYD, G. L. THOMAS, J. A. DOUTHWAITE, J. L. HAYLOR, and M. GRIFFIN
Transglutaminase Transcription and Antigen Translocation in Experimental Renal Scarring
J. Am. Soc. Nephrol., October 1, 1999; 10(10): 2146 - 2157.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
J. Hildesheim, R. A. Foster, M. E. Chamberlin, and J. C. Vogel
Characterization of the Regulatory Domains of the Human Skn-1a/Epoc-1/Oct-11 POU Transcription Factor
J. Biol. Chem., September 10, 1999; 274(37): 26399 - 26406.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T.-S. Lai, T. F. Slaughter, K. A. Peoples, and C. S. Greenberg
Site-directed Mutagenesis of the Calcium-binding Site of Blood Coagulation Factor XIIIa
J. Biol. Chem., August 27, 1999; 274(35): 24953 - 24958.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Small, J.-F. Feng, J. Lorenz, E. T. Donnelly, A. Yu, M.-J. Im, G. W. Dorn II, and S. B. Liggett
Cardiac Specific Overexpression of Transglutaminase II (Gh) Results in a Unique Hypertrophy Phenotype Independent of Phospholipase C Activation
J. Biol. Chem., July 23, 1999; 274(30): 21291 - 21296.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Z. Nemes, L. N. Marekov, L. Fesus, and P. M. Steinert
A novel function for transglutaminase 1: Attachment of long-chain omega -hydroxyceramides to involucrin by ester bond formation
PNAS, July 20, 1999; 96(15): 8402 - 8407.
[Abstract] [Full Text] [PDF]

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 JEMHome page
T. Noll, G. Wozniak, K. McCarson, A. Hajimohammad, H. J. Metzner, J. Inserte, W. Kummer, F. W. Hehrlein, and H. M. Piper
Effect of Factor XIII on Endothelial Barrier Function
J. Exp. Med., May 3, 1999; 189(9): 1373 - 1382.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Nemes, L. N. Marekov, and P. M. Steinert
Involucrin Cross-linking by Transglutaminase 1. BINDING TO MEMBRANES DIRECTS RESIDUE SPECIFICITY
J. Biol. Chem., April 16, 1999; 274(16): 11013 - 11021.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Kida, M. Souri, M. Yamamoto, H. Saito, and A. Ichinose
Transcriptional Regulation of Cell Type-specific Expression of the TATA-less A Subunit Gene for Human Coagulation Factor XIII
J. Biol. Chem., March 5, 1999; 274(10): 6138 - 6147.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Hall, R. Wang, R. van Antwerpen, L. Sottrup-Jensen, and K. Soderhall
The crayfish plasma clotting protein: A vitellogenin-related protein responsible for clot formation in crustacean blood
PNAS, March 2, 1999; 96(5): 1965 - 1970.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B. A. Fox, V. C. Yee, L. C. Pedersen, I. Le Trong, P. D. Bishop, R. E. Stenkamp, and D. C. Teller
Identification of the Calcium Binding Site and a Novel Ytterbium Site in Blood Coagulation Factor XIII by X-ray Crystallography
J. Biol. Chem., February 19, 1999; 274(8): 4917 - 4923.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Medvedev, N. A. Saunders, H. Matsuura, A. Chistokhina, and A. M. Jetten
Regulation of the Transglutaminase I Gene. IDENTIFICATION OF DNA ELEMENTS INVOLVED IN ITS TRANSCRIPTIONAL CONTROL IN TRACHEOBRONCHIAL EPITHELIAL CELLS
J. Biol. Chem., February 5, 1999; 274(6): 3887 - 3896.
[Abstract] [Full Text] [PDF]

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 QJMHome page
H.P. Kohler and P.J. Grant
The role of factor XIIIVal34Leu in cardiovascular disease
QJM, February 1, 1999; 92(2): 67 - 72.
[Full Text] [PDF]

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 FASEB J.Home page
L. PIREDDA, M. GRAZIA FARRACE, M. LO BELLO, W. MALORNI, G. MELINO, R. PETRUZZELLI, and M. PIACENTINI
Identification of `tissue' transglutaminase binding proteins in neural cells committed to apoptosis
FASEB J, February 1, 1999; 13(2): 355 - 364.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
M. T. Kaartinen, A. Pirhonen, A. Linnala-Kankkunen, and P. H. Maenpaa
Cross-linking of Osteopontin by Tissue Transglutaminase Increases Its Collagen Binding Properties
J. Biol. Chem., January 15, 1999; 274(3): 1729 - 1735.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
M. K. Magnusson and D. F. Mosher
Fibronectin : Structure, Assembly, and Cardiovascular Implications
Arterioscler Thromb Vasc Biol, September 1, 1998; 18(9): 1363 - 1370.
[Full Text] [PDF]

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 FASEB J.Home page
A. Monsonego, T. Mizrahi, S. Eitan, G. Moalem, H. Bárdos, R. Ádány, and M. Schwartz
Factor XIIIa as a nerve-associated transglutaminase
FASEB J, September 1, 1998; 12(12): 1163 - 1171.
[Abstract] [Full Text]

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 JCBHome page
M. Nurminskaya, C. Magee, D. Nurminsky, and T. F. Linsenmayer
Plasma Transglutaminase in Hypertrophic Chondrocytes: Expression and Cell-specific Intracellular Activation Produce Cell Death and Externalization
J. Cell Biol., August 24, 1998; 142(4): 1135 - 1144.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
Y. van de Wal, Y. Kooy, P. van Veelen, S. Pena, L. Mearin, G. Papadopoulos, and F. Koning
Cutting Edge: Selective Deamidation by Tissue Transglutaminase Strongly Enhances Gliadin-Specific T Cell Reactivity
J. Immunol., August 15, 1998; 161(4): 1585 - 1588.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. N. Marekov and P. M. Steinert
Ceramides Are Bound to Structural Proteins of the Human Foreskin Epidermal Cornified Cell Envelope
J. Biol. Chem., July 10, 1998; 273(28): 17763 - 17770.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. Schmidt, J. Selzer, M. Lerm, and K. Aktories
The Rho-deamidating Cytotoxic Necrotizing Factor 1 from Escherichia coli Possesses Transglutaminase Activity. CYSTEINE 866 AND HISTIDINE 881 ARE ESSENTIAL FOR ENZYME ACTIVITY
J. Biol. Chem., May 29, 1998; 273(22): 13669 - 13674.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. Candi, G. Melino, A. Lahm, R. Ceci, A. Rossi, I. G. Kim, B. Ciani, and P. M. Steinert
Transglutaminase 1 Mutations in Lamellar Ichthyosis. LOSS OF ACTIVITY DUE TO FAILURE OF ACTIVATION BY PROTEOLYTIC PROCESSING
J. Biol. Chem., May 29, 1998; 273(22): 13693 - 13702.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. J. Ritter and P. J. A. Davies
Identification of a Transforming Growth Factor-beta 1/Bone Morphogenetic Protein 4 (TGF-beta 1/BMP4) Response Element within the Mouse Tissue Transglutaminase Gene Promoter
J. Biol. Chem., May 22, 1998; 273(21): 12798 - 12806.
[Abstract] [Full Text] [PDF]


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