Noninflammatory Gluten Peptide Analogs as Biomarkers for Celiac Sprue

Chemistry and Biology

Volumn 16, Issue 8, 2009, Pages 868-881

  Bethune, Michael T ^a   Crespo Bosque, Mónica ^a   Bergseng, Elin ^b   Mazumdar, Kaushiki ^c   Doyle, Lara ^c   Sestak, Karol ^c,d   Sollid, Ludvig M ^d   Khosla, Chaitan ^a,e  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF OSLO   (Norway)

^c TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Stanford University   (United States)

Author keywords

CHEMBIO; HUMDISEASE

Indexed keywords

BIOLOGICAL MARKER; GLUTEN; PEPTIDE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELIAC DISEASE; CHEMISTRY; HUMAN; IMMUNOLOGY; ISOTOPE LABELING; MALE; METABOLISM; MOLECULAR GENETICS; RAT; T LYMPHOCYTE; WISTAR RAT;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; CELIAC DISEASE; GLUTENS; HUMANS; ISOTOPE LABELING; MALE; MOLECULAR SEQUENCE DATA; PEPTIDES; RATS; RATS, WISTAR; T-LYMPHOCYTES; TRANSGLUTAMINASES;

ANIMALIA;

EID: 69049113890     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2009.07.009     Document Type: Article

References (68)

1. Alaedini A., and Green P.H. Narrative review: celiac disease: understanding a complex autoimmune disorder. Ann. Intern. Med. 142 (2005) 289-298
2. Anderson R.P., van Heel D.A., Tye-Din J.A., Barnardo M., Salio M., Jewell D.P., and Hill A.V. T cells in peripheral blood after gluten challenge in coeliac disease. Gut 54 (2005) 1217-1223
3. Arentz-Hansen H., Korner R., Molberg O., Quarsten H., Vader W., Kooy Y.M., Lundin K.E., Koning F., Roepstorff P., Sollid L.M., and McAdam S.N. The intestinal T cell response to alpha-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J. Exp. Med. 191 (2000) 603-612
4. Baert F.J., D'Haens G.R., Peeters M., Hiele M.I., Schaible T.F., Shealy D., Geboes K., and Rutgeerts P.J. Tumor necrosis factor alpha antibody (infliximab) therapy profoundly down-regulates the inflammation in Crohn's ileocolitis. Gastroenterology 116 (1999) 22-28
5. Bethune M.T., and Khosla C. Parallels between pathogens and gluten peptides in celiac sprue. PLoS Pathog. 4 (2008) e34
6. Bethune M.T., Strop P., Tang Y., Sollid L.M., and Khosla C. Heterologous expression, purification, refolding, and structural-functional characterization of EP-B2, a self-activating barley cysteine endoprotease. Chem. Biol. 13 (2006) 637-647
7. Bethune M.T., Borda J.T., Ribka E., Liu M.X., Phillippi-Falkenstein K., Jandacek R.J., Doxiadis G.G., Gray G.M., Khosla C., and Sestak K. A non-human primate model for gluten sensitivity. PLoS ONE 3 (2008) e1614
8. Bethune M.T., Ribka E., Khosla C., and Sestak K. Transepithelial transport and enzymatic detoxification of gluten in gluten-sensitive rhesus macaques. PLoS ONE 26 (2008) e1857
9. Bethune M.T., Siegel M., Howles-Banerji S., and Khosla C. Interferon-gamma released by gluten-stimulated celiac disease-specific intestinal T cells enhances the transepithelial flux of gluten peptides. J. Pharmacol. Exp. Ther. 329 (2009) 657-668
10. Bruewer M., Utech M., Ivanov A.I., Hopkins A.M., Parkos C.A., and Nusrat A. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J. 19 (2005) 923-933
11. Catassi C., Fabiani E., Corrao G., Barbato M., De Renzo A., Carella A.M., Gabrielli A., Leoni P., Carroccio A., Baldassarre M., et al. Risk of non-Hodgkin lymphoma in celiac disease. JAMA 287 (2002) 1413-1419
12. Ciacci C., Cirillo M., Cavallaro R., and Mazzacca G. Long-term follow-up of celiac adults on gluten-free diet: prevalence and correlates of intestinal damage. Digestion 66 (2002) 178-185
13. Clayburgh D.R., Shen L., and Turner J.R. A porous defense: the leaky epithelial barrier in intestinal disease. Lab. Invest. 84 (2004) 282-291
14. Cornell H.J., Macrae F.A., Melny J., Pizzey C.J., Cook F., Mason S., Bhathal P.S., and Stelmasiak T. Enzyme therapy for management of coeliac disease. Scand. J. Gastroenterol. 40 (2005) 1304-1312
15. Corrao G., Corazza G.R., Bagnardi V., Brusco G., Ciacci C., Cottone M., Sategna Guidetti C., Usai P., Cesari P., Pelli M.A., et al. Mortality in patients with coeliac disease and their relatives: a cohort study. Lancet 358 (2001) 356-361
16. Cummins A.G., Thompson F.M., Butler R.N., Cassidy J.C., Gillis D., Lorenzetti M., Southcott E.K., and Wilson P.C. Improvement in intestinal permeability precedes morphometric recovery of the small intestine in coeliac disease. Clin. Sci. (Lond.) 100 (2001) 379-386
17. Demaude J., Salvador-Cartier C., Fioramonti J., Ferrier L., and Bueno L. Phenotypic changes in colonocytes following acute stress or activation of mast cells in mice: implications for delayed epithelial barrier dysfunction. Gut 55 (2006) 655-661
18. Dicke W.K., Weijers H.A., and Van De Kamer J.H. Coeliac disease. II. The presence in wheat of a factor having a deleterious effect in cases of coeliac disease. Acta Paediatr. 42 (1953) 34-42
19. Dieterich W., Ehnis T., Bauer M., Donner P., Volta U., Riecken E.O., and Schuppan D. Identification of tissue transglutaminase as the autoantigen of celiac disease. Nat. Med. 3 (1997) 797-801
20. Duerksen D.R., Wilhelm-Boyles C., and Parry D.M. Intestinal permeability in long-term follow-up of patients with celiac disease on a gluten-free diet. Dig. Dis. Sci. 50 (2005) 785-790
21. Friis S., Dabelsteen E., Sjostrom H., Noren O., and Jarnum S. Gliadin uptake in human enterocytes. Differences between coeliac patients in remission and control individuals. Gut 33 (1992) 1487-1492
22. Gass J., Vora H., Bethune M.T., Gray G.M., and Khosla C. Effect of barley endoprotease EP-B2 on gluten digestion in the intact rat. J. Pharmacol. Exp. Ther. 318 (2006) 1178-1186
23. Gass J., Bethune M.T., Siegel M., Spencer A., and Khosla C. Combination enzyme therapy for gastric digestion of dietary gluten in patients with celiac sprue. Gastroenterology 133 (2007) 472-480
24. Green P.H., and Jabri B. Celiac disease. Annu. Rev. Med. 57 (2006) 207-221
25. Hue S., Mention J.J., Monteiro R.C., Zhang S., Cellier C., Schmitz J., Verkarre V., Fodil N., Bahram S., Cerf-Bensussan N., and Caillat-Zucman S. A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity 21 (2004) 367-377
26. Jabri B., Kasarda D.D., and Green P.H. Innate and adaptive immunity: the yin and yang of celiac disease. Immunol. Rev. 206 (2005) 219-231
27. Kessler M., Acuto O., Storelli C., Murer H., Muller M., and Semenza G. A modified procedure for the rapid preparation of efficiently transporting vesicles from small intestinal brush border membranes. Their use in investigating some properties of D-glucose and choline transport systems. Biochim. Biophys. Acta 506 (1978) 136-154
28. Kim C.Y., Quarsten H., Bergseng E., Khosla C., and Sollid L.M. Structural basis for HLA-DQ2-mediated presentation of gluten epitopes in celiac disease. Proc. Natl. Acad. Sci. USA 101 (2004) 4175-4179
29. Koskinen O., Collin P., Korponay-Szabo I., Salmi T., Iltanen S., Haimila K., Partanen J., Maki M., and Kaukinen K. Gluten-dependent small bowel mucosal transglutaminase 2-specific IgA deposits in overt and mild enteropathy coeliac disease. J. Pediatr. Gastroenterol. Nutr. 47 (2008) 436-442
30. Luyer M.D., Buurman W.A., Hadfoune M., Wolfs T., van't Veer C., Jacobs J.A., Dejong C.H., and Greve J.W. Exposure to bacterial DNA before hemorrhagic shock strongly aggravates systemic inflammation and gut barrier loss via an IFN-gamma-dependent route. Ann. Surg. 245 (2007) 795-802
31. Madara J.L., and Stafford J. Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 83 (1989) 724-727
32. Maiuri L., Ciacci C., Ricciardelli I., Vacca L., Raia V., Auricchio S., Picard J., Osman M., Quaratino S., and Londei M. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet 362 (2003) 30-37
33. March J.B. High antigliadin IgG titers in laboratory rabbits fed a wheat-containing diet: a model for celiac disease?. Dig. Dis. Sci. 48 (2003) 608-610
34. Matysiak-Budnik T., Candalh C., Dugave C., Namane A., Cellier C., Cerf-Bensussan N., and Heyman M. Alterations of the intestinal transport and processing of gliadin peptides in celiac disease. Gastroenterology 125 (2003) 696-707
35. 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., et al. Secretory IgA mediates retrotranscytosis of intact gliadin peptides via the transferrin receptor in celiac disease. J. Exp. Med. 205 (2008) 143-154
36. Molberg O., McAdam S.N., Korner R., Quarsten H., Kristiansen C., Madsen L., Fugger L., Scott H., Noren O., Roepstorff P., et al. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat. Med. 4 (1998) 713-717
37. Molberg Ø., McAdam S., Lundin K., and Sollid L. Studies of gliadin-specific T cells in celiac disease. In Celiac disease: Methods and protocols. In: Marsh M.N. (Ed) (2000), Humana, Totowa, NJ 105-124
38. Moron B., Cebolla A., Manyani H., Alvarez-Maqueda M., Megias M., Thomas Mdel C., Lopez M.C., and Sousa C. Sensitive detection of cereal fractions that are toxic to celiac disease patients by using monoclonal antibodies to a main immunogenic wheat peptide. Am. J. Clin. Nutr. 87 (2008) 405-414
39. Musch M.W., Clarke L.L., Mamah D., Gawenis L.R., Zhang Z., Ellsworth W., Shalowitz D., Mittal N., Efthimiou P., Alnadjim Z., et al. T cell activation causes diarrhea by increasing intestinal permeability and inhibiting epithelial Na+/K+-ATPase. J. Clin. Invest. 110 (2002) 1739-1747
40. Nilsen E.M., Lundin K.E., Krajci P., Scott H., Sollid L.M., and Brandtzaeg P. Gluten specific, HLA-DQ restricted T cells from coeliac mucosa produce cytokines with Th1 or Th0 profile dominated by interferon gamma. Gut 37 (1995) 766-776
41. Nilsen E.M., Jahnsen F.L., Lundin K.E., Johansen F.E., Fausa O., Sollid L.M., Jahnsen J., Scott H., and Brandtzaeg P. Gluten induces an intestinal cytokine response strongly dominated by interferon gamma in patients with celiac disease. Gastroenterology 115 (1998) 551-563
42. Paterson B.M., Lammers K.M., Arrieta M.C., Fasano A., and Meddings J.B. The safety, tolerance, pharmacokinetic and pharmacodynamic effects of single doses of AT-1001 in coeliac disease subjects: a proof of concept study. Aliment. Pharmacol. Ther. 26 (2007) 757-766
43. Peyrin-Biroulet L., Desreumaux P., Sandborn W.J., and Colombel J.F. Crohn's disease: beyond antagonists of tumour necrosis factor. Lancet 372 (2008) 67-81
44. Pietzak M.M. Follow-up of patients with celiac disease: achieving compliance with treatment. Gastroenterology 128 (2005) S135-S141
45. Piper J.L., Gray G.M., and Khosla C. High selectivity of human tissue transglutaminase for immunoactive gliadin peptides: implications for celiac sprue. Biochemistry 41 (2002) 386-393
46. Piper J.L., Gray G.M., and Khosla C. Effect of prolyl endopeptidase on digestive-resistant gliadin peptides in vivo. J. Pharmacol. Exp. Ther. 311 (2004) 213-219
47. Qiao S.W., Bergseng E., Molberg O., Jung G., Fleckenstein B., and Sollid L.M. Refining the rules of gliadin T cell epitope binding to the disease-associated DQ2 molecule in celiac disease: importance of proline spacing and glutamine deamidation. J. Immunol. 175 (2005) 254-261
48. Quarsten H., Molberg O., Fugger L., McAdam S.N., and Sollid L.M. HLA binding and T cell recognition of a tissue transglutaminase-modified gliadin epitope. Eur. J. Immunol. 29 (1999) 2506-2514
49. Raki M., Tollefsen S., Molberg O., Lundin K.E., Sollid L.M., and Jahnsen F.L. A unique dendritic cell subset accumulates in the celiac lesion and efficiently activates gluten-reactive T cells. Gastroenterology 131 (2006) 428-438
50. Raki M., Fallang L.E., Brottveit M., Bergseng E., Quarsten H., Lundin K.E., and Sollid L.M. Tetramer visualization of gut-homing gluten-specific T cells in the peripheral blood of celiac disease patients. Proc. Natl. Acad. Sci. USA 104 (2007) 2831-2836
51. Schumann M., Richter J.F., Wedell I., Moos V., Zimmermann-Kordmann M., Schneider T., Daum S., Zeitz M., Fromm M., and Schulzke J.D. Mechanisms of epithelial translocation of the alpha(2)-gliadin-33mer in coeliac sprue. Gut 57 (2008) 747-754
52. Scopes R.K. Measurement of protein by spectrophotometry at 205 nm. Anal. Biochem. 59 (1974) 277-282
53. See J., and Murray J.A. Gluten-free diet: the medical and nutrition management of celiac disease. Nutr. Clin. Pract. 21 (2006) 1-15
54. Shan L., Molberg O., Parrot I., Hausch F., Filiz F., Gray G.M., Sollid L.M., and Khosla C. Structural basis for gluten intolerance in celiac sprue. Science 297 (2002) 2275-2279
55. Shan L., Marti T., Sollid L.M., Gray G.M., and Khosla C. Comparative biochemical analysis of three bacterial prolyl endopeptidases: implications for coeliac sprue. Biochem. J. 383 (2004) 311-318
56. Shan L., Qiao S.W., Arentz-Hansen H., Molberg O., Gray G.M., Sollid L.M., and Khosla C. Identification and analysis of multivalent proteolytically resistant peptides from gluten: implications for celiac sprue. J. Proteome Res. 4 (2005) 1732-1741
57. Siegel M., Bethune M.T., Gass J., Ehren J., Xia J., Johannsen A., Stuge T.B., Gray G.M., Lee P.P., and Khosla C. Rational design of combination enzyme therapy for celiac sprue. Chem. Biol. 13 (2006) 649-658
58. Silvester J.A., and Rashid M. Long-term follow-up of individuals with celiac disease: an evaluation of current practice guidelines. Can. J. Gastroenterol. 21 (2007) 557-564
59. Sollid L.M. Coeliac disease: dissecting a complex inflammatory disorder. Nat. Rev. Immunol. 2 (2002) 647-655
60. Sollid L.M., Markussen G., Ek J., Gjerde H., Vartdal F., and Thorsby E. Evidence for a primary association of celiac disease to a particular HLA-DQ alpha/beta heterodimer. J. Exp. Med. 169 (1989) 345-350
61. Stepniak D., Spaenij-Dekking L., Mitea C., Moester M., de Ru A., Baak-Pablo R., van Veelen P., Edens L., and Koning F. Highly efficient gluten degradation with a newly identified prolyl endoprotease: implications for celiac disease. Am. J. Physiol. Gastrointest. Liver Physiol. 291 (2006) G621-G629
62. Sturgess R., Day P., Ellis H.J., Lundin K.E., Gjertsen H.A., Kontakou M., and Ciclitira P.J. Wheat peptide challenge in coeliac disease. Lancet 343 (1994) 758-761
63. Troncone R., Gianfrani C., Mazzarella G., Greco L., Guardiola J., Auricchio S., and De Berardinis P. Majority of gliadin-specific T-cell clones from celiac small intestinal mucosa produce interferon-gamma and interleukin-4. Dig. Dis. Sci. 43 (1998) 156-161
64. Vora H., McIntire J., Kumar P., Deshpande M., and Khosla C. A scaleable manufacturing process for pro-EP-B2, a cysteine protease from barley indicated for celiac sprue. Biotechnol. Bioeng. 98 (2007) 177-185
65. Wapenaar M.C., van Belzen M.J., Fransen J.H., Sarasqueta A.F., Houwen R.H., Meijer J.W., Mulder C.J., and Wijmenga C. The interferon gamma gene in celiac disease: augmented expression correlates with tissue damage but no evidence for genetic susceptibility. J. Autoimmun. 23 (2004) 183-190
66. Watts T., Berti I., Sapone A., Gerarduzzi T., Not T., Zielke R., and Fasano A. Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc. Natl. Acad. Sci. USA 102 (2005) 2916-2921
67. Xia J., Sollid L.M., and Khosla C. Equilibrium and kinetic analysis of the unusual binding behavior of a highly immunogenic gluten peptide to HLA-DQ2. Biochemistry 44 (2005) 4442-4449
68. Xia J., Siegel M., Bergseng E., Sollid L.M., and Khosla C. Inhibition of HLA-DQ2-mediated antigen presentation by analogues of a high affinity 33-residue peptide from alpha2-gliadin. J. Am. Chem. Soc. 128 (2006) 1859-1867