Toxic peptides in Frazer's fraction interact with the actin cytoskeleton and affect the targeting and function of intestinal proteins

Experimental Cell Research

Volumn 315, Issue 19, 2009, Pages 3442-3452

  Reinke, Yvonne ^a   Zimmer, Klaus Peter ^b   Naim, Hassan Y ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Actin cytoskeleton; Aminopeptidase N; Brush border membrane; Celiac disease; Dipeptidylpeptidase IV; Endocytosis; Gliadin toxic peptides; Lactase phlorizin hydrolase; Protein trafficking; Sucrase isomaltase

Indexed keywords

ACTIN; CHOLESTEROL; DISACCHARIDE; GLIADIN; GLYCOSYLCERAMIDASE; LACTASE; SPHINGOMYELIN; SUCRASE ISOMALTASE;

APICAL MEMBRANE; ARTICLE; CARBOHYDRATE INTOLERANCE; CELIAC DISEASE; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTESTINE BRUSH BORDER; LIPID COMPOSITION; LIPID STORAGE; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANSCYTOSIS;

TRITICUM AESTIVUM;

EID: 70350426216     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.06.026     Document Type: Article

References (44)

1. Ciclitira P.J., and Moodie S.J. Transition of care between paediatric and adult gastroenterology. Coeliac disease. Best Pract. Res. Clin. Gastroenterol. 17 (2003) 181-195
2. Marsh M.N. Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity ('celiac sprue'). Gastroenterology 102 (1992) 330-354
3. Sollid L.M. Coeliac disease: dissecting a complex inflammatory disorder. Nat. Rev. Immunol. 2 (2002) 647-655
4. Sollid L.M. Molecular basis of celiac disease. Annu. Rev. Immunol. 18 (2000) 53-81
5. Snoeck V., Goddeeris B., and Cox E. The role of enterocytes in the intestinal barrier function and antigen uptake. Microbes Infect. 7 (2005) 997-1004
6. Buono C., Li Y., Waldo S.W., and Kruth H.S. Liver X receptors inhibit human monocyte-derived macrophage foam cell formation by inhibiting fluid-phase pinocytosis of LDL. J. Lipid Res. 48 (2007) 2411-2418
7. Lamaze C., and Schmid S.L. The emergence of clathrin-independent pinocytic pathways. Curr. Opin. Cell Biol. 7 (1995) 573-580
8. Matysiak-Budnik T., Moura I.C., Arcos-Fajardo M., Lebreton C., Menard S., Candalh C., Ben-Khalifa K., Dugave C., Tamouza H., van Niel G., Bouhnik Y., Lamarque D., Chaussade S., Malamut G., Cellier C., Cerf-Bensussan N., Monteiro R.C., and Heyman M. Secretory IgA mediates retrotranscytosis of intact gliadin peptides via the transferrin receptor in celiac disease. J. Exp. Med. 205 (2008) 143-154
9. Lammers K.M., Lu R., Brownley J., Lu B., Gerard C., Thomas K., Rallabhandi P., Shea-Donohue T., Tamiz A., Alkan S., Netzel-Arnett S., Antalis T., Vogel S.N., and Fasano A. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology 135 (2008) 194-204 e3
10. Alpers D. Digestion and Absorption of Carbohydrates and Protein. 2nd ed. (1987), Raven Press, New York
11. Le Bivic A., Quaroni A., Nichols B., and Rodriguez-Boulan E. Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line. J. Cell Biol. 111 (1990) 1351-1361
12. Matter K., Brauchbar M., Bucher K., and Hauri H.P. Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2). Cell 60 (1990) 429-437
13. Jacob R., Heine M., Alfalah M., and Naim H.Y. Distinct cytoskeletal tracks direct individual vesicle populations to the apical membrane of epithelial cells. Curr. Biol. 13 (2003) 607-612
14. Holmgren Peterson K., Magnusson K.E., Stenhammar L., and Falth-Magnusson K. Confocal laser scanning microscopy of small-intestinal mucosa in celiac disease. Scand. J. Gastroenterol. 30 (1995) 228-234
15. Sander G.R., Cummins A.G., Henshall T., and Powell B.C. Rapid disruption of intestinal barrier function by gliadin involves altered expression of apical junctional proteins. FEBS Lett. 579 (2005) 4851-4855
16. Frazer A.C., Fletcher R.F., Ross C.A., Shaw B., Sammons H.G., and Schneider R. Gluten-induced enteropathy: the effect of partially digested gluten. Lancet 2 (1959) 252-255
17. Schmitz J., Preiser H., Maestracci D., Ghosh B.K., Cerda J.J., and Crane R.K. Purification of the human intestinal brush border membrane. Biochim. Biophys. Acta 323 (1973) 98-112
18. Hauri H.P., Sterchi E.E., Bienz D., Fransen J.A., and Marxer A. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells. J. Cell Biol. 101 (1985) 838-851
19. Danielsen E.M., Sjostrom H., Noren O., and Dabelsteen E. Immunoelectrophoretic studies on pig intestinal brush border proteins. Biochim. Biophys. Acta 494 (1977) 332-342
20. Maiuri L., Raia V., Potter J., Swallow D., Ho M.W., Fiocca R., Finzi G., Cornaggia M., Capella C., Quaroni A., et al. Mosaic pattern of lactase expression by villous enterocytes in human adult-type hypolactasia. Gastroenterology 100 (1991) 359-369
21. Leitner K., Ellinger I., Grill M., Brabec M., and Fuchs R. Efficient apical IgG recycling and apical-to-basolateral transcytosis in polarized BeWo cells overexpressing hFcRn. Placenta 27 (2006) 799-811
22. Beaulieu J.F., Nichols B., and Quaroni A. Posttranslational regulation of sucrase-isomaltase expression in intestinal crypt and villus cells. J. Biol. Chem. 264 (1989) 20000-20011
23. Jacob R., and Naim H.Y. Apical membrane proteins are transported in distinct vesicular carriers. Curr. Biol. 11 (2001) 1444-1450
24. Bligh E.G., and Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37 (1959) 911-917
25. Takadate A., Ohkubo Y., Irikura M., Goya S., Otagiri M., and Uekama K. Interaction of the fluorescent probe 7-anilino-4-methylcoumarin-3-acetic acid with alpha-globulin. Chem. Pharm. Bull. (Tokyo) 33 (1985) 1522-1527
26. Bailey D.S., Freedman A.R., Price S.C., Chescoe D., and Ciclitira P.J. Early biochemical responses of the small intestine of coeliac patients to wheat gluten. Gut 30 (1989) 78-85
27. Kersting S., Bruewer M., Schuermann G., Klotz A., Utech M., Hansmerten M., Krieglstein C.F., Senninger N., Schulzke J.D., Naim H.Y., and Zimmer K.P. Antigen transport and cytoskeletal characteristics of a distinct enterocyte population in inflammatory bowel diseases. Am. J. Pathol. 165 (2004) 425-437
28. Fujiwara I., Takahashi S., Tadakuma H., Funatsu T., and Ishiwata S. Microscopic analysis of polymerization dynamics with individual actin filaments. Nat. Cell Biol. 4 (2002) 666-673
29. Weber A. Actin binding proteins that change extent and rate of actin monomer-polymer distribution by different mechanisms. Mol. Cell Biochem. 190 (1999) 67-74
30. Draaijer M., Koninkx J., Hendriks H., Kik M., Van Dijk J., and Mouwen J. Actin cytoskeletal lesions in differentiated human colon carcinoma Caco-2 cells after exposure to soybean agglutinin. Biol. Cell 65 (1989) 29-35
31. Dudley M.A., Hachey D.L., Quaroni A., Hutchens T.W., Nichols B.L., Rosenberger J., Perkinson J.S., Cook G., and Reeds P.J. In vivo sucrase-isomaltase and lactase-phlorizin hydrolase turnover in the fed adult rat. J. Biol. Chem. 268 (1993) 13609-13616
32. Coluccio L.M., and Myosin I. Am. J. Physiol. 273 (1997) C347-C359
33. Mooseker M.S., and Tilney L.G. Organization of an actin filament-membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J. Cell Biol. 67 (1975) 725-743
34. Louvard D., Kedinger M., and Hauri H.P. The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Annu. Rev. Cell Biol. 8 (1992) 157-195
35. Cooper J.A., and Schafer D.A. Control of actin assembly and disassembly at filament ends. Curr. Opin. Cell Biol. 12 (2000) 97-103
36. Hunziker W., Male P., and Mellman I. Differential microtubule requirements for transcytosis in MDCK cells. EMBO J. 9 (1990) 3515-3525
37. Breitfeld P.P., McKinnon W.C., and Mostov K.E. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells. J. Cell Biol. 111 (1990) 2365-2373
38. Ojetti V., Nucera G., Migneco A., Gabrielli M., Lauritano C., Danese S., Zocco M.A., Nista E.C., Cammarota G., De Lorenzo A., Gasbarrini G., and Gasbarrini A. High prevalence of celiac disease in patients with lactose intolerance. Digestion 71 (2005) 106-110
39. Radlovic N., Mladenovic M., Lekovic Z., Ristic D., Pavlovic M., Stojsic Z., Vuletic B., Radlovic V., Nikolic D., Djurdjevid J., and Gaji M. Lactose intolerance in infants with gluten-sensitive enteropathy: frequency and clinical characteristics. Srp. Arh. Celok. Lek. 137 (2009) 33-37
40. Prasad K.K., Thapa B.R., Nain C.K., Sharma A.K., and Singh K. Brush border enzyme activities in relation to histological lesion in pediatric celiac disease. J. Gastroenterol. Hepatol. 23 (2008) e348-52
41. Mukherjee S., Ghosh R.N., and Maxfield F.R. Endocytosis. Physiol. Rev. 77 (1997) 759-803
42. Gottlieb T.A., Ivanov I.E., Adesnik M., and Sabatini D.D. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120 (1993) 695-710
43. Costa de Beauregard M.A., Pringault E., Robine S., and Louvard D. Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO J. 14 (1995) 409-421
44. Muller T., Hess M.W., Schiefermeier N., Pfaller K., Ebner H.L., Heinz-Erian P., Ponstingl H., Partsch J., Rollinghoff B., Kohler H., Berger T., Lenhartz H., Schlenck B., Houwen R.J., Taylor C.J., Zoller H., Lechner S., Goulet O., Utermann G., Ruemmele F.M., Huber L.A., and Janecke A.R. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet. 40 (2008) 1163-1165