Intracellular localization of microbial transglutaminase and its influence on the transport of gliadin in enterocytes

Journal of Pediatric Gastroenterology and Nutrition

Volumn 68, Issue 3, 2019, Pages E43-E50

  Stricker, Sebastian ^a   De Laffolie, Jan ^a   Rudloff, Silvia ^a   Komorowski, Lars ^b   Zimmer, Klaus Peter ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b Institute of Experimental Immunology   (Germany)

Author keywords

celiac disease; cross presentation; enterocyte transport; gliadin peptides; Rapid uptake of Antigen into the Cytosol of Enterocytes cells

Indexed keywords

GLIADIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

CD8+ T LYMPHOCYTE; CELIAC DISEASE; DUODENUM; HUMAN; IMMUNOLOGY; INTESTINE CELL; INTESTINE FLORA; METABOLISM; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CD8-POSITIVE T-LYMPHOCYTES; CELIAC DISEASE; DUODENUM; ENTEROCYTES; GASTROINTESTINAL MICROBIOME; GLIADIN; GTP-BINDING PROTEINS; HUMANS; TRANSGLUTAMINASES;

EID: 85059760156     PISSN: 02772116     EISSN: 15364801     Source Type: Journal    
DOI: 10.1097/MPG.0000000000002171     Document Type: Article

References (50)

1. Gianfrani C, Troncone R, Mugione P,. Celiac disease association with CD8+ T cell responses. J Immunol 2003; 170: 2719-2726.
2. Mazzarella G, Stefanile R, Camarca A,. Gliadin activates HLA class I-restricted CD8+ T cells in celiac disease intestinal mucosa and induces the enterocyte apoptosis. Gastroenterology 2008; 134: 1017-1027.
3. Kovacsovics-Bankowski M, Rock KL,. A phagosome-To-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 1995; 267: 243-246.
4. Den Haan JM, Lehar SM, Bevan MJ,. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 2000; 192: 1685-1695.
5. Grommé M, Neefjes J,. Antigen degradation or presentation by MHC class I molecules via classical and non-classical pathways. Mol Immunol 2002; 39: 181-202.
6. Kersting S, Bruewer M, Schuermann G,. Antigen transport and cytoskeletal characteristics of a distinct enterocyte population in inflammatory bowel diseases. Am J Pathol 2004; 165: 425-437.
7. Schürmann G, Brüwer M, Klotz A,. Transepithelial transport processes at the intestinal mucosa in inflammatory bowel disease. Int J Colorectal Dis 1999; 14: 41-46.
8. Yokoyama K, Nio N, Kikuchi Y,. Properties and applications of microbial transglutaminase. Appl Microbiol Biotechnol 2004; 64: 447-454.
9. Richtlinie 2000/13/EG des Europäischen Parlaments und des Rates vom 20.03.2000 zur Angleichung der Rechtsvorschriften der Mitgliedstaaten über die Etikettierung und Aufmachung von Lebensmitteln sowie die Werbung hierfür. www.eur-lex.europa.eu/legal-content/de/ALL/?uri=CELEX%3A32000L0013. Accessed September 14, 2016.
10. Zhu Y, Rinzema A, Tramper J,. Microbial transglutaminase-A review of its production and application in food processing. Appl Microbiol Biotechnol 1995; 44: 277-282.
11. Kaufmann A, Köppel R, Widmer M,. Determination of microbial transglutaminase in meat and meat products. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2012; 29: 1364-1373.
12. Dekking EHA, Van Veelen PA, De Ru A,. Microbial transglutaminases generate T cell stimulatory epitopes involved in celiac disease. J Cereal Sci 2008; 47: 339-346.
13. Skovbjerg H, Koch C, Anthonsen D,. Deamidation and cross-linking of gliadin peptides by transglutaminases and the relation to celiac disease. Biochim Biophys Acta 2004; 1690: 220-230.
14. Lerner A, Matthias T,. Changes in intestinal tight junction permeability associated with industrial food additives explain the rising incidence of autoimmune disease. Autoimmun Rev 2015; 14: 479-489.
15. Lerner A, Aminov R, Matthias T,. Transglutaminases in dysbiosis as potential environmental drivers of autoimmunity. Front Microbiol 2017; 8: 66.
16. Lerner A, Matthias T,. Possible association between celiac disease and bacterial transglutaminase in food processing: A hypothesis. Nutr Rev 2015; 73: 544-552.
17. Matthias T, Jeremias P, Neidhofer S,. The industrial food additive, microbial transglutaminase, mimics tissue transglutaminase and is immunogenic in celiac disease patients. Autoimmun Rev 2016; 15: 1111-1119.
18. Frazer AC, Fletcher RF, Ross CA,. Gluten-induced enteropathy: The effect of partially digested gluten. Lancet 1959; 2: 252-255.
19. Hase K, Kawano K, Nochi T,. Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 2009; 462: 226-230.
20. Ohno H,. Intestinal M cells. J Biochem 2016; 159: 151-160.
21. Griffiths G, Simons K, Warren G,. Immunoelectron microscopy using thin, frozen sections: Application to studies of the intracellular transport of Semliki Forest virus spike glycoproteins. Methods Enzymol 1983; 96: 466-485.
22. Tokuyasu KT,. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 1973; 57: 551-565.
23. Yu J, Pian Y, Ge J,. Functional and structural characterization of the antiphagocytic properties of a novel transglutaminase from Streptococcus suis. J Biol Chem 2015; 290: 19081-19092.
24. Skovbjerg H, Norén O, Anthonsen D,. Coeliac disease gliadin is a good substrate of several transglutaminases: possible implication in the pathogenesis of coeliac disease. Scand J Gastroenterol 2002; 37: 812-817.
25. Lerner A, Matthias T, Aminov R,. Potential effects of horizontal gene exchange in the human gut. Front Immunol 2017; 8: 1630.
26. Barone MV, Zimmer KP,. Endocytosis and transcytosis of gliadin peptides. Mol Cell Pediatr 2016; 3: 8.
27. Zimmer KP, Buning J, Weber P,. Modulation of antigen trafficking to MHC class II-positive late endosomes of enterocytes. Gastroenterology 2000; 118: 128-137.
28. Zimmer K-P, Fischer I, Mothes T,. Endocytotic segregation of gliadin peptide 31-49 in enterocytes. Gut 2010; 59: 300-310.
29. Melcher CA, Schmitz M, Hildebrand R,. Targeting of gliadin peptide alpha 31-49 to late endosomes of enterocytes of infantile mice by conjugation to cholera toxin B subunit (CTB). J Pediatr Gastroenterol Nutr 2010; 50: 26-27.
30. Lubbing N, Barone M-V, Rudloff S,. Correction of gliadin transport within enterocytes through celiac disease serum. Pediatr Res 2011; 70: 357-362.
31. Davies PJA, Davies DR, Levitzki A,. Transglutaminase is essential in receptor-mediated endocytosis of alpha2-makroglobulin and polypeptide hormones. Nature 1980; 283: 162-167.
32. Reinke Y, Behrendt M, Schmidt S,. Impairment of protein trafficking by direct interaction of gliadin peptides with actin. Exp Cell Res 2011; 317: 2124-2135.
33. Barone MV, Gimigliano A, Castoria G,. Growth factor-like activity of gliadin, an alimentary protein: implications for coeliac disease. Gut 2007; 56: 480-488.
34. Horiguchi Y, Inoue N, Masuda M,. Bordetella bronchiseptica dermonecrotizing toxin induces reorganization of actin stress fibers through deamidation of Gln-63 of the GTP-binding protein Rho. Proc Natl Acad Sci USA 1997; 94: 11623-11626.
35. Schmidt G, Selzer J, Lerm M,. 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 1998; 273: 13669-13674.
36. Rouch JD, Scott A, Lei NY,. Development of functional microfold (M) cells from intestinal stem cells in primary human enteroids. PLoS One 2016; 11: e0148216.
37. De Lau W, Kujala P, Schneeberger K,. Peyer's patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured "miniguts". Mol Cell Biol 2012; 32: 3639-3647.
38. Kernéis S, Bogdanova A, Kraehenbuhl JP,. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 1997; 277: 949-952.
39. Hundorfean G, Zimmer K-P, Strobel S,. Luminal antigens access late endosomes of intestinal epithelial cells enriched in MHC I and MHC II molecules: in vivo study in Crohn's ileitis. Am J Physiol Gastrointest Liver Physiol 2007; 293: 798-808.
40. Gonnella PA, Wilmore DW,. Co-localization of class II antigen and exogenous antigen in the rat enterocyte. J Cell Sci 1993; 106: 937-940.
41. Korponay-Szabo IR, Halttunen T, Szalai Z,. In vivo targeting of intestinal and extraintestinal transglutaminase 2 by coeliac autoantibodies. Gut 2004; 53: 641-648.
42. Mazumdar K, Alvarez X, Borda JT,. Visualization of transepithelial passage of the immunogenic 33-residue peptide from alpha-2 gliadin in gluten-sensitive macaques. PLoS One 2010; 5: e10228.
43. Skovbjerg H, Anthonsen D, Knudsen E,. Deamidation of gliadin peptides in lamina propria: implications for celiac disease. Dig Dis Sci 2008; 53: 2917-2924.
44. Heil A, Ohsam J, Büchold C,. Microbial transglutaminase has a lower deamidation preference than human tissue transglutaminase on a celiac disease relevant wheat gliadin T-cell epitope. J Cereal Sci 2016; 70: 47-56.
45. Lombardi E, Bergamo P, Maurano F,. Selective inhibition of the gliadin-specific, cell-mediated immune response by transamidation with microbial transglutaminase. J Leukoc Biol 2013; 93: 479-488.
46. Heredia-Sandoval NG, Islas-Rubio AR, Cabrera-Chavez F,. Transamidation of gluten proteins during the bread-making process of wheat flour to produce breads with less immunoreactive gluten. Food Funct 2014; 5: 1813-1818.
47. Zhou L, Kooy-Winkelaar YMC, Cordfunke RA,. Abrogation of immunogenic properties of gliadin peptides through transamidation by microbial transglutaminase is acyl-Acceptor dependent. J Agric Food Chem 2017; 65: 7542-7552.
48. Berti C, Roncoroni L, Falini ML,. Celiac-related properties of chemically and enzymatically modified gluten proteins. J Agric Food Chem 2007; 55: 2482-2488.
49. Falini ML, Elli L, Caramanico R,. Immunoreactivity of antibodies against transglutaminase-deamidated gliadins in adult celiac disease. Dig Dis Sci 2008; 53: 2697-2701.
50. Schuppan D, Ciccocioppo R,. Coeliac disease and secondary autoimmunity. Dig Liver Dis 2002; 34: 13-15.