Celiac disease T-cell epitopes from gamma-gliadins: immunoreactivity depends on the genome of origin, transcript frequency, and flanking protein variation

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Salentijn, Elma M J ^a   Mitea, D C ^b   Goryunova, Svetlana V ^c   van der Meer, Ingrid M ^a   Padioleau, Ismael ^a   Gilissen, Luud J W J ^a   Koning, Frits ^b   Smulders, Marinus J M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

gliadins; Celiac disease; Gluten; T cell epitopes; Wheat

Indexed keywords

COMPLEMENTARY DNA; EPITOPE; GLIADIN;

ARTICLE; CELIAC DISEASE; CELL PROLIFERATION; CULTIVAR; DIPLOIDY; GENE ACTIVITY; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GLI A1 GENE; GLI B1 GENE; GLI D1 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENE; PLANT GENOME; T LYMPHOCYTE; TRITICUM AESTIVUM;

CELIAC DISEASE; CELLS, CULTURED; EPITOPES, T-LYMPHOCYTE; GENOME, PLANT; GLIADIN; HUMANS; TRITICUM;

TRITICUM AESTIVUM;

EID: 84862579962     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-277     Document Type: Article

References (59)

1. Dicke WK, Weijers NA, van der Kramer JH. Coeliac disease 2: The presence in wheat of a deleterious effect in cases of coeliac disease. Acta Paediatr 1953, 42:34.
2. Shan L, Molberg T, Parrot I, Hausch F, Filiz F, Gray GM, Sollid LM, Khosla C. structural basis for gluten intolerance in celiac sprue. Science 2002, 297:2275-2279. 10.1126/science.1074129, 12351792.
3. Van de Wal Y, Kooy YMC, Drijfhout JW, Amons R, Koning F. Peptide binding characteristics of the coeliac disease-associated DQ (α1*0501, β1*0201) molecule. Immunogenetics 1996, 44:246-253. 10.1007/BF02602553, 8753854.
4. Vartdal F, Johansen BH, Friede T, Thorpe CJ, Stevanovic S, Eriksen JE, Sletten K, Thorsby E, Rammensee HG, Sollid LM. The peptide binding motif of the disease associated HLA-DQ (α1*0501, β1*0201) molecule. Eur J Immunol 1996, 26:2764-2772. 10.1002/eji.1830261132, 8921967.
5. Godkin A, Friede T, Davenport M, Stevanovic S, Willis A, Jewell D, Hill A, Rammensee HG. Use of eluted peptide sequence data to identify the binding characteristics of peptides to the insulin-dependent diabetes susceptibility allele HLA-DQ8 (DQ 3.2). Int Immunol 1997, 9:905-911. 10.1093/intimm/9.6.905, 9199974.
6. Kim C-Y, Quarsten H, Bergseng E, Khosla C, Sollid LM. Structural basis for HLA-DQ2-mediated presentation of gluten epitopes in celiac disease. Proc Natl Acad Sci U S A 2004, 101:4175-4179. 10.1073/pnas.0306885101, 384714, 15020763.
7. Qiao S-W, Bergseng E, Molberg T, Jung G, Fleckenstein B, Sollid LM. 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 2005, 175:254-261.
8. Tollefsen S, Arentz-Hansen H, Fleckenstein B, Molberg T, Ráki, Kwok WW, Jung G, Lundin KEA, Sollid LM. HLA-DQ2 and -DQ8 signatures of gluten T-cell epitopes in celiac disease. J Clin Invest 2006, 116:2226-2236. 10.1172/JCI27620, 1518792, 16878175.
9. Henderson KN, Tye-Din JA, Reid HH, Chen Z, Borg NA, Beissbarth T, Tatham A, Mannering SI, Purcell AW, Dudek NL, Van Heel DA, McCluskey J, Rossjohn J, Anderson RP. A structural and immunological basis for the role of human leukocyte antigen DQ8 in celiac disease. Immunity 2007, 27:23-34. 10.1016/j.immuni.2007.05.015, 17629515.
10. Stepniak D, Wiesner M, de Ru AH, Moustakas AK, Drijfhout JW, Papadopoulos GK, van Veelen PA, Koning F. Large-scale characterization of natural ligands explains the unique gluten-binding properties of HLA-DQ2. J Immunol 2008, 180:3268-3278.
11. Molberg T, Mcadam SN, Körner R, Quarsten H, Kristiansen C, Madsen L, Fugger L, Scott H, Norén O, Roepstorff P, Lundin KEA, Sjöström H, Sollid LM. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T-cells in celiac disease. Nat Med 1998, 4:713-717. 10.1038/nm0698-713, 9623982.
12. Van de Wal Y, Kooy YMC, van Veelen P, Pena AS, Mearin ML, Papadopoulos GK, Koning F. Selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T-cell reactivity. J Immunol 1998, 161:1585-1588.
13. Vader LW, De Ru A, Van der Wal Y, Kooy YMC, Benckhuijsen W, Mearin ML, Drijfhout JW, Van Veelen PA, Koning F. Specificity of tissue transglutaminase explains cereal toxicity in celiac disease. J Exp Med 2002, 195:643-649. 10.1084/jem.20012028, 2193762, 11877487.
14. Fleckenstein B, Molberg T, Qiao SW, Schmid DG, von der MF M, Elgstøen K, Jung G, Sollid LM. Gliadin T-cell epitope selection by tissue transglutaminase in celiac disease. J Biol Chem 2002, 277:34109-34116. 10.1074/jbc.M204521200, 12093810.
15. Van de Wal Y, Kooy YMC, Van Veelen P, Pẽna AS, Mearin ML, Molberg T, Lundin KE, Sollid LM, Mutis T, Benckhuijsen WB, Drijfhout JW, Koning F. Small intestinal T-cells of celiac disease patients recognize a natural pepsin fragment of gliadin. Proc Natl Acad Sci USA 1998, 95:10050-10054. 10.1073/pnas.95.17.10050, 21459, 9707598.
16. de Wal V, Kooy YMC, Van Veelen P, Vader W, August SA, Drijfhout JW, Pẽna SA, Koning F. Glutenin is involved in the gluten-driven mucosal T-cell response. Eur J Immunol 1999, 29:3133-3139. 10.1002/(SICI)1521-4141(199910)29:10<3133::AID-IMMU3133>3.0.CO;2-G, 10540324.
17. Sjöström H, Lundin KE, Molberg O, Körner R, McAdam SN, Anthonsen D, Quarsten H, Norén O, Roepstorff P, Thorsby E, Sollid LM. 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. 10.1046/j.1365-3083.1998.00397.x, 9716100.
18. Arentz-Hansen H, Körner R, Molberg T, Quarsten H, Vader W, Kooy YMC, Lundin KEA, Koning F, Roepstorff P, Sollid LM, McAdam SN. The intestinal T-cell response to α-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J Exp Med 2000, 191:603-612. 10.1084/jem.191.4.603, 2195837, 10684852.
19. Arentz-Hansen H, McAdam SN, Molberg T, Fleckenstein B, Lundin KEA, Jørgensen TJD, Jung G, Roepstorff P, Sollid LM. Celiac lesion T-cells recognize epitopes that cluster in regions of gliadins rich in proline residues. Gastroenterology 2002, 123:803-809. 10.1053/gast.2002.35381, 12198706.
20. Arentz-Hansen H, Fleckenstein B, Molberg T, Scott H, Koning F, Jung G, Roepstorff P, Lundin KEA, Sollid LM. The molecular basis for oat intolerance in patients with celiac disease. PLoS Med 2004, 1:84-92.
21. Stepniak D, Vader WL, Kooy Y, van Veelen PA, Moustakas A, Papandreou NA, Eliopoulos E, Drijfhout JW, Papadopoulos GK, Koning F. T-cell recognition of HLA-DQ2-bound gluten peptides can be influenced by an N-terminal proline at p-1. Immunogenetics 2005, 57:8-15. 10.1007/s00251-005-0780-8, 15714306.
22. Vader LW, Kooy Y, Van Veelen PA, De Ru A, Harris D, Benckhuijsen W, Pen S, Mearin ML, Drijfhout JW, Koning F. The gluten response in children with celiac disease is directed toward multiple gliadin and glutenin peptides. Gasteroenterology 2002, 122:1729-1737.
23. Vader LW, Stepniak, Bunnik EM, Kooy YMC, De Haan W, Drijfhout JW, Van Veelen PA, Koning F. Characterization of cereal toxicity for celiac disease patients based on protein homology in grains. Gasteroenterology 2003, 125:1105-1113.
24. Camarca A, Anderson RP, Mamone G, Fierro O, Facchiano A, Costantini S, Zanzi D, Sidney J, Auricchio S, Sette A, Troncone R, Gianfrani C. Intestinal T-cell responses to gluten peptides are largely heterogeneous: implications for a peptide-based therapy in celiac disease. J Immunol 2009, 182:4158-4166. 10.4049/jimmunol.0803181, 3306175, 19299713.
25. Anderson RP, van Heel DA, Tye-Din JA, Jewell DP, Hill AVS. In vivo antigen challenge in celiac disease identifies a single transglutaminase-modified peptide as the dominant A-gliadin T-cell epitope. Nat Med 2000, 6:337-342. 10.1038/73200, 10700238.
26. Anderson RP, van Heel DA, Tye-Din JA, Jewell DP, Hill AVS. Antagonists and non-toxic variants of the dominant wheat gliadin T-cell epitope in coeliac disease. Gut 2006, 55:485-491. 10.1136/gut.2005.064550, 1856168, 16299041.
27. Qiao S-W, Bergseng E, Molberg T, Xia J, Fleckenstein B, Khosla C, Sollid LM. Antigen presentation to celiac lesion-derived T-cells of a 33-mer gliadin peptide naturally formed by gastrointestinal digestion. J Immunol 2004, 173:1757-1762.
28. Dørum S, Qiao SW, Sollid LM, Fleckenstein B. A quantitative analysis of transglutaminase 2-mediated deamidation of gluten peptides: Implications for the T-cell response in celiac disease. J Proteome Res 2009, 8:1748-1755. 10.1021/pr800960n, 19239248.
29. Dørum S, Arntzen M, Qiao S-W, Holm A, Koehler CJ, Thiede B, Sollid LM, Fleckenstein B. The preferred substrates for transglutaminase 2 in a complex wheat gluten digest are peptide fragments harboring celiac disease T-cell epitopes. PLoS One 2010, 5:e14056. 10.1371/journal.pone.0014056, 2988817, 21124911.
30. Spaenij-Dekking L, Kooy-Winkelaar Y, Van Veelen P, Drijfhout JW, Jonker H, van Soest L, Smulders MJM, Bosch D, gilissen LJWJ, Koning F, Bosch D. Natural variation in toxicity of wheat: potential for selection of nontoxic varieties for celiac disease patients. Gasteroenterology 2005, 129:797-806.
31. Molberg O, Uhlen AK, Jensen T, Solheim Flaete N, Fleckenstein B, Arentz-Hanzen H, Raki M, Lundin KEA, Sollid LM. Mapping of gluten T-cell epitopes in the bread wheat ancestors: implications for celiac disease. Gasteroenterology 2005, 128:393-401.
32. Dupont FM, Vensel WH, Tanaka CK, Hurkman WJ, Altenbach SB. Deciphering the complexities of the wheat flour proteome using quantitative two-dimensional electrophoresis, three proteases and tandem mass spectrometry. Proteome Sci 2011, 9:10. 10.1186/1477-5956-9-10, 3238214, 21314956.
33. Payne PI. Genetics of wheat storage proteins and the effect of allelic variation on bread making quality. Annu Rev Plant Physiol 1987, 38:141-153.
34. Gao S, Gu Y-Q, Wu J, Coleman-Derr D, Huo N, Crossman C, Jia J, Zuo Q, Ren Z, Anderson OD, Kong X. Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 2007, 65:189-203. 10.1007/s11103-007-9208-1, 17629796.
35. Sabelli P, Shewry PR. Characterization and organisation of gene families at the Gli-1 loci of bread and durum wheats by restriction fragment analysis. Theor Appl Genet 1991, 83:209-216.
36. Anderson OD, Hsia CC, Torres V. The wheat γ-gliadin genes: characterization of ten new sequences and further understanding of γ-gliadin gene family structure. Theor Appl Genet 2001, 103:323-330.
37. Pistón F, Dorado G, Martín A, Barro F. Cloning of nine γ-gliadin mRNAs (cDNAs) from wheat and the molecular characterization of comparative transcript levels of γ-gliadin subclasses. J Cereal Sci 2006, 43:120-128.
38. Zhang W, Gianibelli MC, Ma W, Rampling L, Gale KR. Identification of SNPs and development of allele-specific PCR markers for gamma-gliadin alleles in Triticum aestivum. Theor Appl Genet 2003, 107(1):130-138.
39. Qi P-F, Wei Y-M, Ouellet T, Chen Q, Tan X, Zheng Y-L. The gamma-gliadin multigene family in common wheat (Triticum aestivum) and its closely related species. BMC Genomics 2009, 10:168. 10.1186/1471-2164-10-168, 2685405, 19383144.
40. Huang Z, Long H, Wei YM, Qi PF, Tan ZH, Zheng YL. Characterization and classification of γ-gliadin multigene sequences from Aegilops section Sitopsis. Cereal Res Commun 2010, 38(1):1-14.
41. Altenbach SB, Vensel WH, DuPont FM. Analysis of expressed sequence tags from a single wheat cultivar facilitates interpretation of tandem mass spectrometry data and discrimination of gamma gliadin proteins that may play different functional roles in flour. BMC Plant Biology 2010, 10:7. 10.1186/1471-2229-10-7, 2827424, 20064259.
42. Metakovsky EV. Gliadin allele identification in common wheat II. Catalogue of gliadin alleles in common wheat. J Genet Breed 1991, 45:325-344.
43. Van Herpen TWJM, Goryunova SV, Schoot J, Mitreva M, Salentijn EMJ, Vorst O, Schenk MF, Van Veelen PA, Koning F, Van Soest LJM, Vosman B, Bosch D, Hamer RJ, Gilissen LJWJ, Smulders MJM. Alpha-gliadin genes from the A, B, and D genomes of wheat contain different sets of celiac disease epitopes. BMC Genomics 2006, 7:1. 10.1186/1471-2164-7-1, 1368968, 16403227.
44. Van den Broeck HC, de Jong HC, Salentijn EMJ, Dekking L, Bosch D, Hamer RJ, Gilissen LJWJ, van der Meer IM, Smulders MJM. Presence of celiac disease epitopes in modern and old hexaploid wheat varieties: wheat breeding may have contributed to increased prevalence of celiac disease. Theor Appl Genet 2010, 121:1527-1539. 10.1007/s00122-010-1408-4, 2963738, 20664999.
45. Van den Broeck H, Chen H, Lacaze X, Dusautoir J-C, Gilissen L, Smulders M, Van der Meer I. In search of tetraploid wheat accessions reduced in celiac disease-related gluten epitopes. Mol Biosyst 2010, 6:2206-2213. 10.1039/c0mb00046a, 20714643.
46. Mitea C, Salentijn EMJ, van Veelen P, Goryunova SV, van der Meer IM, van den Broeck HC, Mujico JR, Monserrat V, Gilissen LJWJ, Drijfhout JW, Dekking L, Koning F, Smulders MJM. A universal approach to eliminate antigenic properties of alpha-gliadin peptides in celiac disease. PLoS One 2010, 5(12):e15637. 10.1371/journal.pone.0015637, 3002971, 21179575.
47. Van Slageren MW. Wild wheats: a monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae). Wageningen Agriculture University Papers, ICARDA, Wageningen 1994, 94(7):1-513.
48. Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P. Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci U S A 2002, 99(12):8133-8138. 10.1073/pnas.072223799, 123033, 12060759.
49. Feldman M, Lupton FGH, Miller TE. Wheats. Evolution of Crop Plants 1995, 184-192. Longman Group, London, Smart J, Simmonds NW.
50. Salse J, Chagué V, Bolot S, Magdelenat G, Huneau C, Pont C, Belcram H, Couloux A, Gardais S, Evrard A, Segurens B, Charles M, Ravel C, Samain S, Charmet G, Boudet N, Chalhoub B. New insights into the origin of the B genome of hexaploid wheat: evolutionary relationships at the SPA genomic region with the S genome of the diploid relative Aegilops speltoides. BMC Genomics 2008, 9:555-567. 10.1186/1471-2164-9-555, 2612700, 19032732.
51. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
52. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
53. Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 2004, 101:11030-11035. 10.1073/pnas.0404206101, 491989, 15258291.
54. Cassidy BG, Dvorak J, Anderson OD. The wheat low-molecular-weight glutenin genes: characterization of six new genes and progress in understanding gene family structure. Theor Appl Genet 1998, 96:743-750.
55. Sollid LM, Qiao SW, Anderson RP, Gianfrani C, Koning F. Nomenclature and listing of celiac disease relevant gluten T-cell epitopes restricted by HLA-DQ molecules. Immunogenetics 64(6):455-460.
56. Shan L, Qiao S-W, Arentz-Hansen H, Molberg T, Gray GM, Sollid LM, Khosla C. Identification and analysis of multivalent proteolytically resistant peptides from gluten: implications for celiac sprue. J Proteome Res 2005, 4(5):1732-1741. 10.1021/pr050173t, 1343496, 16212427.
57. Tye-Din JA, Steward JA, Dromey JA, Beissbarth T, Van Heel DA, Tatham A, Henderson K, Mannering SI, Gianfrani C, Jewell DP, Hill AVS, McCluskey J, Rossjohn J, Anderson RP. Comprehensive, quantitative mapping of T-cell epitopes in gluten in celiac disease. Sci Transl Med 2010, 2:1-14.
58. Salentijn EMJ, Goryunova SV, Bas N, Van der Meer IM, Van den Broeck HC, Bastien T, Gilissen LJWJ, Smulders MJM. Tetraploid and hexaploid wheat varieties reveal large differences in expression of alpha-gliadins from homoeologous Gli-2 loci. BMC Genomics 2009, 10:48. 10.1186/1471-2164-10-48, 2636828, 19171027.
59. Pizzuti D, Buda A, D'Odorico A, D'Incà R, Chiarelli S, Curioni A, Martines D. Lack of intestinalmucosal toxicity of Triticum monococcum in celiac disease patients. Scand J Gastroenterol 2006, 41:1305-1311. 10.1080/00365520600699983, 17060124.