European Journal of Internal Medicine
Volume 19, Issue 2 , Pages 83-91 , March 2008

Transglutaminase and the pathogenesis of coeliac disease

  • Pål Stenberg

      Affiliations

    • Hospital Pharmacy, Malmö University Hospital, S-205 02 Malmö, Sweden
    • Corresponding Author InformationCorresponding author. Tel.: +46 40 33 37 85; fax: +46 40 33 62 32.
    • ,
  • E. Bodil Roth

      Affiliations

    • Hospital Pharmacy, Malmö University Hospital, S-205 02 Malmö, Sweden
    • Department of Medicine, Lund University, Malmö University Hospital, Malmö, Sweden
    • ,
  • Klas Sjöberg

      Affiliations

    • Department of Medicine, Lund University, Malmö University Hospital, Malmö, Sweden

Received 8 December 2006 ,Revised 9 May 2007 ,Accepted 10 May 2007.

References 

  1. Dieterich W, Ehnis T, Bauer M, et al. Identification of tissue transglutaminase as the autoantigen of coeliac disease. Nat Med. 1997;3:797–801
  2. Beninati S, Piacentini M. The transglutaminase family: an overview: minireview article. Amino Acids. 2004;26:367–372
  3. Korsgren C, Lawler J, Lambert S, et al. Complete amino acid sequence and homologies of human erythrocyte membrane protein band 4.2. Proc Natl Acad Sci U S A. 1990;87:613–617
  4. Aeschlimann D, Paulsson M. Transglutaminases: protein cross-linking enzymes in tissues and body fluids. Thromb Haemost. 1994;71:402–415
  5. Lorand L. Factor XIII and the clotting of fibrinogen: from basic research to medicine. J Thromb Haemost. 2005;3:1337–1348
  6. Hitomi K. Transglutaminases in skin epidermis. Eur J Dermatol. 2005;15:313–319
  7. Im MJ, Russell MA, Feng JF. Transglutaminase II: a new class of GTP-binding protein with new biological functions. Cell Signal. 1997;9:477–482
  8. Murthy SN, Iismaa S, Begg G, et al. Conserved tryptophan in the core domain of transglutaminase is essential for catalytic activity. Proc Natl Acad Sci U S A. 2002;99:2738–2742
  9. Lesort M, Attanavanich K, Zhang J, Johnson GV. Distinct nuclear localization and activity of tissue transglutaminase. J Biol Chem. 1998;273:11991–11994
  10. Martinez J, Chalupowicz DG, Roush RK, et al. Transglutaminase-mediated processing of fibronectin by endothelial cell monolayers. Biochemistry. 1994;33:2538–2545
  11. Upchurch HF, Conway E, Patterson MK, Maxwell MD. Localization of cellular transglutaminase on the extracellular matrix after wounding: characteristics of the matrix bound enzyme. J Cell Physiol. 1991;149:375–382
  12. De Laurenzi V, Melino G. Gene disruption of tissue transglutaminase. Mol Cell Biol. 2001;21:148–155
  13. Bernassola F, Federici M, Corazzari M, et al. Role of transglutaminase 2 in glucose tolerance: knockout mice studies and a putative mutation in a MODY patient. Faseb J. 2002;16:1371–1378
  14. Falasca L, Iadevaia V, Ciccosanti F, et al. Transglutaminase type II is a key element in the regulation of the anti-inflammatory response elicited by apoptotic cell engulfment. J Immunol. 2005;174:7330–7340
  15. Seiving B, Ohlsson K, Linder C, Stenberg P. Transglutaminase differentiation during maturation of human blood monocytes to macrophages. Eur J Haematol. 1991;46:263–271
  16. Laki K, Tyler HM, Yancey ST. Clot forming and clot stabilizing enzymes from the mouse tumor YPC-1. Biochem Biophys Res Commun. 1966;22:776–781
  17. Mann AP, Verma A, Sethi G, et al. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-{kappa}b in cancer cells: delineation of a novel pathway. Cancer Res. 2006;66:8788–8795
  18. Skill NJ, Griffin M, El Nahas AM, et al. Increases in renal epsilon-(gamma-glutamyl)-lysine crosslinks result from compartment-specific changes in tissue transglutaminase in early experimental diabetic nephropathy: pathologic implications. Lab Invest. 2001;81:705–716
  19. Skill NJ, Johnson TS, Coutts IG, et al. Inhibition of transglutaminase activity reduces extracellular matrix accumulation induced by high glucose levels in proximal tubular epithelial cells. J Biol Chem. 2004;279:47754–47762
  20. Lorand L, Hsu LK, Siefring GE, Rafferty NS. Lens transglutaminase and cataract formation. Proc Natl Acad Sci U S A. 1981;78:1356–1360
  21. Samuelsson B, Stenberg P, Pandolfi M. Localization and characteristics of transglutaminase in the rabbit and human eye. Graefes Arch Clin Exp Ophthalmol. 1982;218:233–236
  22. Karpuj MV, Becher MW, Springer JE, et al. Prolonged survival and decreased abnormal movements in transgenic model of Huntington disease, with administration of the transglutaminase inhibitor cystamine. Nat Med. 2002;8:143–149
  23. Stenberg P, Curtis CG, Wing D, et al. Transamidase kinetics. Amide formation in the enzymic reactions of thiol esters with amines. Biochem J. 1975;147:155–163
  24. Curtis CG, Stenberg P, Brown KL, et al. Kinetics of transamidating enzymes. Production of thiol in the reactions of thiol esters with fibrinoligase. Biochemistry. 1974;13:3257–3262
  25. Lorand L, Gray AJ, Brown K, et al. Dissociation of the subunit structure of fibrin stabilizing factor during activation of the zymogen. Biochem Biophys Res Commun. 1974;56:914–922
  26. Credo RB, Stenberg P, Tong YS, Lorand L. Inhibition of fibrinoligase and transglutaminase by zinc ions. In: Fed. Proc. San Fransisco. 1976;
  27. Marsh MN. Coeliac Disease. Oxford: Blackwell Scientific Publications; 1992;1–16 pp.
  28. Dicke WK, Weijers HA, Van De Kamer JH. Coeliac disease. II. The presence in wheat of a factor having a deleterious effect in cases of coeliac disease. Acta Paediatr. 1953;42:34–42
  29. Marsh MN. Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity (‘coeliac sprue’). Gastroenterology. 1992;102:330–354
  30. Frazer AC. Discussion of some problems of steatorrhea and reduced stature. Proc R Soc Med. 1956;49:1009–1013
  31. Booth CC. The enterocyte in coeliac disease. Br Med J. 1970;4:14–17
  32. Van De Kamer JH, Weijers HA. Coeliac disease. V. Some experiments on the cause of the harmful effect of wheat gliadin. Acta Paediatr. 1955;44:465–469
  33. Bruce SE, Bjarnason I, Peters TJ. Human jejunal transglutaminase: demonstration of activity, enzyme kinetics and substrate specificity with special relation to gliadin and coeliac disease. Clin Sci (Lond). 1985;68:573–579
  34. Skovbjerg H, Hansen GH, Niels-Christiansen LL, et al. Intestinal tissue transglutaminase in coeliac disease of children and adults: ultrastructural localization and variation in expression. Scand J Gastroenterol. 2004;39:1219–1227
  35. Hansson T, Ulfgren AK, Lindroos E, et al. Transforming growth factor-beta (TGF-beta) and tissue transglutaminase expression in the small intestine in children with coeliac disease. Scand J Immunol. 2002;56:530–537
  36. Sjostrom H, Lundin KE, Molberg O, et al. Identification of a gliadin T-cell epitope in coeliac disease: general importance of gliadin deamidation for intestinal T-cell recognition. Scand J Immunol. 1998;48:111–115
  37. Molberg O, McAdam SN, Korner R, et al. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in coeliac disease. Nat Med. 1998;4:713–717
  38. Shan L, Molberg O, Parrot I, et al. Structural basis for gluten intolerance in coeliac sprue. Science. 2002;297:2275–2279
  39. Vader LW, de Ru A, van der Wal Y, et al. Specificity of tissue transglutaminase explains cereal toxicity in coeliac disease. J Exp Med. 2002;195:643–649
  40. Wong RC, Wilson RJ, Steele RH, et al. A comparison of 13 guinea pig and human anti-tissue transglutaminase antibody ELISA kits. J Clin Pathol. 2002;55:488–494
  41. Roth EB, Sjoberg K, Stenberg P. Biochemical and immuno-pathological aspects of tissue transglutaminase in coeliac disease. Autoimmunity. 2003;36:221–226
  42. Stenberg P, Stenflo J. A rapid and specific fluorescent activity staining procedure for transamidating enzymes. Anal Biochem. 1979;93:445–452
  43. Nakachi K, Swift G, Wilmot D, et al. Antibodies to tissue transglutaminase: comparison of ELISA and immunoprecipitation assay in the presence and in the absence of calcium ions. Clin Chim Acta. 2001;304:75–84
  44. Agardh D, Roth B, Lernmark A, Stenberg P. Calcium activation of tissue transglutaminase in radioligand binding and enzyme-linked autoantibody immunoassays in childhood coeliac disease. Clin Chim Acta. 2005;358:95–103
  45. Prasad AS. Zinc deficiency. BMJ. 2003;326:409–410
  46. Srinivas U, Ohlsson T, Hallstadius L, et al. Organ sequestration of (65)Zn during experimental sepsis. Clin Nutr. 1989;8:263–267
  47. Dieterich W, Esslinger B, Trapp D, et al. Cross linking to tissue transglutaminase and collagen favours gliadin toxicity in coeliac disease. Gut. 2006;55:478–484
  48. Esposito C, Paparo F, Caputo I, et al. Anti-tissue transglutaminase antibodies from coeliac patients inhibit transglutaminase activity both in vitro and in situ. Gut. 2002;51:177–181
  49. Dieterich W, Trapp D, Esslinger B, et al. Autoantibodies of patients with coeliac disease are insufficient to block tissue transglutaminase activity. Gut. 2003;52:1562–1566
  50. Byrne G, Ryan F, Jackson J, et al. Mutagenesis of the catalytic triad of tissue transglutaminase abrogates coeliac disease serum IgA autoantibody binding. Gut. 2006;
  51. van Heel DA, West J. Recent advances in coeliac disease. Gut. 2006;55:1037–1046
  52. Green PH, Jabri B. Coeliac disease. Lancet. 2003;362:383–391
  53. Ivarsson A. The Swedish epidemic of coeliac disease explored using an epidemiological approach—some lessons to be learnt. Best Pract Res Clin Gastroenterol. 2005;19:425–440
  54. Sardy M, Karpati S, Merkl B, et al. Epidermal transglutaminase (TGase 3) is the autoantigen of dermatitis herpetiformis. J Exp Med. 2002;195:747–757
  55. Roth EB, Stenberg P, Book C, Sjoberg K. Antibodies against transglutaminases, peptidylarginine deiminase and citrulline in rheumatoid arthritis—new pathways to epitope spreading. Clin Exp Rheumatol. 2006;24:12–18
  56. Kearney PL, Bhatia M, Jones NG, et al. Kinetic characterization of protein arginine deiminase 4: a transcriptional corepressor implicated in the onset and progression of rheumatoid arthritis. Biochemistry. 2005;44:10570–10582
  57. Lorand JB, Pilkington TR, Lorand L. Inhibitors of fibrin cross-linking: relevance for thrombolysis. Nature. 1966;210:1273–1274
  58. Lorand L, Parameswaran KN, Stenberg P, et al. Specificity of guinea pig liver transglutaminase for amine substrates. Biochemistry. 1979;18:1756–1765
  59. Ljunggren C, Hoffmann KJ, Stenberg P, Nilsson JL. Fibrin-stabilizing factor inhibitors. 10. Thiol esters as potent enzyme inhibitors. J Med Chem. 1973;16:1186–1188
  60. Agardh CD, Cilio CM, Lethagen A, et al. Clinical evidence for the safety of GAD65 immunomodulation in adult-onset autoimmune diabetes. J Diabetes Complications. 2005;19:238–246

☆ We hereby certify that there are no financial or other relationships that might lead to a conflict of interest. The manuscript has been read and approved by all authors.

PII: S0953-6205(07)00256-7

doi: 10.1016/j.ejim.2007.05.012

European Journal of Internal Medicine
Volume 19, Issue 2 , Pages 83-91 , March 2008

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