Home LiteratureArticle Details
PMID: 12651621 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transglutaminase type II plays a protective role in hepatic injury.

The American journal of pathology ·Vol. 162 ·No. 4 ·2003-04-00 ·Pages 1293-303

Nardacci R, Lo Iacono O, Ciccosanti F, Falasca L, Addesso M, Amendola A, Antonucci G, Craxì A, Fimia GM, Iadevaia V, Melino G, Ruco L, Tocci G, Ippolito G, Piacentini M

Abstract

The up-regulation of "tissue" transglutaminase (TG2) gene has been shown to occur in various pathologies and can lead to severe liver injury; however, its role in the onset of liver damage has not yet been clarified. To address this issue, we have used two experimental settings: carbon tetrachloride (CCl(4))-induced liver injury in wild-type and TG2 knockout mice; and liver biopsies obtained from a large cohort of hepatitis C virus (HCV)-infected patients. Mice lacking TG2 failed to clear the hepatic necrotic tissue formed in response to prolonged CCl(4) exposure (5 weeks) and 60% of them died before the end of the treatment. By contrast, wild-type mice were able to recover after the toxic insult. CCl(4)-treated TG2 null mice showed a derangement of the hepatic lobular architecture and a progressive accumulation of extracellular matrix (ECM) components and inflammatory cells which were not observed in the liver of control animals. Consistent with this protective role, we observed that TG2 levels were much higher (up to 15-fold) during the initial stages of liver fibrosis in HCV-infected individuals (METAVIR = F2) compared with uninfected controls, in which the enzyme protein localized in the hepatocytes facing the periportal infiltrate. By contrast, the enzyme levels decreased in the advanced stages (METAVIR = F3 and F4) and their localization was limited to the ECM. Our data demonstrate that TG2 plays a protective role in the liver injury by favoring tissue stability and repair.

MeSH Terms
Adult Animals Carbon Tetrachloride Poisoning/prevention & control GTP-Binding Proteins/deficiency,genetics,metabolism Gene Expression Regulation, Enzymologic Genotype Hepatitis C, Chronic/enzymology,genetics,pathology Humans Liver/injuries,pathology Mice Mice, Inbred C57BL Mice, Knockout Middle Aged Necrosis Protein Glutamine gamma Glutamyltransferase 2 Transglutaminases/deficiency,genetics,metabolism
Chemicals
Protein Glutamine gamma Glutamyltransferase 2 Transglutaminases GTP-Binding Proteins
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Nardacci Roberta
Istituto Nazionale per le Malattie Infettive, IRCCS L. Spallanzani, Rome.
Lo Iacono Oreste
Ciccosanti Fabiola
Falasca Laura
Addesso Maria
Amendola Alessandra
Antonucci Giorgio
Craxì Antonio
Fimia Gian Maria
Iadevaia Valentina
Melino Gerry
Ruco Luigi
Tocci Guido
Ippolito Giuseppe
Piacentini Mauro
References (41)
41 references, click to expand
  1. Requirement for transglutaminase in the activation of latent transforming growth factor-beta in bovine endothelial cells.
    J Cell Biol. 1993 Apr;121(2):439-48 PMID: 8096847
  2. High amount of epsilon-(gamma-glutamyl)lysine cross-links in Mallory bodies.
    Lab Invest. 1992 Jun;66(6):774-7 PMID: 1351114
  3. Transglutaminase-mediated processing of fibronectin by endothelial cell monolayers.
    Biochemistry. 1994 Mar 8;33(9):2538-45 PMID: 7906954
  4. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function.
    Science. 1994 Jun 10;264(5165):1593-6 PMID: 7911253
  5. Tissue transglutaminase: a candidate effector element of physiological cell death.
    Curr Top Microbiol Immunol. 1995;200:163-75 PMID: 7634831
  6. Transglutaminase-catalyzed cross-linking of fibrils of collagen V/XI in A204 rhabdomyosarcoma cells.
    Biochemistry. 1995 Oct 24;34(42):13768-75 PMID: 7577969
  7. The long-term pathological evolution of chronic hepatitis C.
    Hepatology. 1996 Jun;23(6):1334-40 PMID: 8675148
  8. Neurodegenerative diseases and transglutaminase.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14310-3 PMID: 8962045
  9. A role for tissue transglutaminase in hepatic injury and fibrogenesis, and its regulation by NF-kappaB.
    Am J Physiol. 1997 Feb;272(2 Pt 1):G281-8 PMID: 9124352
  10. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups.
    Lancet. 1997 Mar 22;349(9055):825-32 PMID: 9121257
  11. Age and platelet count: a simple index for predicting the presence of histological lesions in patients with antibodies to hepatitis C virus. METAVIR and CLINIVIR Cooperative Study Groups.
    J Viral Hepat. 1997 May;4(3):199-208 PMID: 9181529
  12. The role of transglutaminase in the rat subtotal nephrectomy model of renal fibrosis.
    J Clin Invest. 1997 Jun 15;99(12):2950-60 PMID: 9185519
  13. Tissue transglutaminase-dependent posttranslational modification of the retinoblastoma gene product in promonocytic cells undergoing apoptosis.
    Mol Cell Biol. 1997 Oct;17(10):6040-8 PMID: 9315663
  14. TNF-alpha modulates expression of the tissue transglutaminase gene in liver cells.
    Am J Physiol. 1998 Feb;274(2 Pt 1):G240-5 PMID: 9486175
  15. Interleukin-10 expression and function in experimental murine liver inflammation and fibrosis.
    Hepatology. 1998 Dec;28(6):1597-606 PMID: 9828224
  16. Inhibition of "tissue" transglutaminase increases cell survival by preventing apoptosis.
    J Biol Chem. 1999 Nov 26;274(48):34123-8 PMID: 10567382
  17. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin.
    J Cell Biol. 2000 Feb 21;148(4):825-38 PMID: 10684262
  18. Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases.
    Connect Tissue Res. 2000;41(1):1-27 PMID: 10826705
  19. Gene disruption of tissue transglutaminase.
    Mol Cell Biol. 2001 Jan;21(1):148-55 PMID: 11113189
  20. Hepatitis C virus infection.
    N Engl J Med. 2001 Jul 5;345(1):41-52 PMID: 11439948
  21. Transglutaminase-mediated cross-linking is involved in the stabilization of extracellular matrix in human liver fibrosis.
    J Hepatol. 2001 Sep;35(3):367-75 PMID: 11592598
  22. Transglutaminase overexpression sensitizes neuronal cell lines to apoptosis by increasing mitochondrial membrane potential and cellular oxidative stress.
    J Neurochem. 2002 Jun;81(5):1061-72 PMID: 12065619
  23. 'Tissue' transglutaminase ablation reduces neuronal death and prolongs survival in a mouse model of Huntington's disease.
    Cell Death Differ. 2002 Sep;9(9):873-80 PMID: 12181738
  24. Transglutaminase 2: an enigmatic enzyme with diverse functions.
    Trends Biochem Sci. 2002 Oct;27(10):534-9 PMID: 12368090
  25. The epsilon-(gamma-glutamyl)lysine crosslink and the catalytic role of transglutaminases.
    Adv Protein Chem. 1977;31:1-133 PMID: 73346
  26. Transglutaminases.
    Annu Rev Biochem. 1980;49:517-31 PMID: 6105840
  27. Transglutaminases.
    Mol Cell Biochem. 1984;58(1-2):9-35 PMID: 6143256
  28. Carbon tetrachloride-induced lipid peroxidation dependent on an ethanol-inducible form of rabbit liver microsomal cytochrome P-450.
    FEBS Lett. 1985 Apr 22;183(2):265-9 PMID: 3987892
  29. Differential expression of tissue transglutaminase in human cells. An immunohistochemical study.
    Cell Tissue Res. 1989 Jan;255(1):215-24 PMID: 2567625
  30. Mechanisms of carbon tetrachloride toxicity.
    Pharmacol Ther. 1989;43(1):139-54 PMID: 2675128
  31. 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
  32. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues.
    FASEB J. 1991 Dec;5(15):3071-7 PMID: 1683845
  33. Apoptosis: molecular mechanisms in programmed cell death.
    Eur J Cell Biol. 1991 Dec;56(2):170-7 PMID: 1802705
  34. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death.
    Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):770-4 PMID: 8421714
  35. Prognosis of chronic hepatitis C: results of a large, prospective cohort study.
    Hepatology. 1998 Dec;28(6):1687-95 PMID: 9828236
  36. The role of TGFbeta1 in initiating hepatic stellate cell activation in vivo.
    J Hepatol. 1999 Jan;30(1):77-87 PMID: 9927153
  37. Identification of 'tissue' transglutaminase binding proteins in neural cells committed to apoptosis.
    FASEB J. 1999 Feb;13(2):355-64 PMID: 9973324
  38. Histological damage in chronic hepatitis C is not related to the extent of infection in the liver.
    Am J Pathol. 1999 Jun;154(6):1877-81 PMID: 10362814
  39. 'Tissue' transglutaminase release from apoptotic cells into extracellular matrix during human liver fibrogenesis.
    J Pathol. 1999 Sep;189(1):92-8 PMID: 10451494
  40. Cell surface localization of tissue transglutaminase is dependent on a fibronectin-binding site in its N-terminal beta-sandwich domain.
    J Biol Chem. 1999 Oct 22;274(43):30707-14 PMID: 10521459
  41. The involvement of Kupffer cells in carbon tetrachloride toxicity.
    Toxicol Appl Pharmacol. 1993 Apr;119(2):275-9 PMID: 8480336
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
2003-04-00
Pages
1293-303
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1851212
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: product@genelibs.com