Quantitative and qualitative differences in celiac disease epitopes among durum wheat varieties identified through deep RNA-amplicon sequencing

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Salentijn, Elma M J ^a   Esselink, Danny G ^a   Goryunova, Svetlana V ^a,b   van der Meer, Ingrid M ^a   Gilissen, Luud J W J ^a   Smulders, Marinus J M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLIADIN;

AMPLICON; ARTICLE; CELIAC DISEASE; CONTROLLED STUDY; CULTIVAR; ENDOSPERM; GENETIC VARIABILITY; IMMUNOGENICITY; NONHUMAN; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RNA SEQUENCE; TRITICUM DURUM; TRITICUM TURGIDUM;

TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELIAC DISEASE; CLUSTER ANALYSIS; EPITOPES, T-LYMPHOCYTE; GENE EXPRESSION PROFILING; GEOGRAPHY; GLIADIN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEQUENCE ALIGNMENT; TRITICUM;

EID: 84890368402     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-905     Document Type: Article

References (53)

1. Shewry PR, Halford NG. Genetics of wheat gluten proteins. Adv Genet 2003, 49:111-184.
2. Tye-Din JA, Stewart JA, Dromey JA, Beissbarth T, van Heel DA, Tatham A, Henderson K, Mannering SI, Gianfrani C, Jewell DP, et al. Comprehensive, quantitative mapping of T cell epitopes in gluten in celiac disease. Sci Transl Med 2010, 2:41ra51.
3. 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(4):485-491. 10.1136/gut.2005.064550, 1856168, 16299041.
4. Henderson KN, Tye-Din JA, Reid HH, Chen Z, Borg NA, Beissbarth T, Tatham A, Mannering SI, Purcell AW, Dudek NL, et al. A structural and immunological basis for the role of human leukocyte antigen DQ8 in celiac disease. Immunity 2007, 27(1):23-34. 10.1016/j.immuni.2007.05.015, 17629515.
5. 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 2012, 64(6):455-460. 10.1007/s00251-012-0599-z, 3349865, 22322673.
6. Sollid LM. Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol 2002, 2(9):647-655. 10.1038/nri885, 12209133.
7. Rewers M. Epidemiology of celiac disease: what are the prevalence, incidence, and progression of celiac disease?. Gastroenterology 2005, 128(4):S47-S51. 10.1053/j.gastro.2005.02.030, 15825126.
8. Abadie V, Sollid LM, Barreiro LB, Jabri B. Integration of genetic and immunological insights into a model of celiac disease pathogenesis. Annu Rev Immunol 2011, 29:493-525. 10.1146/annurev-immunol-040210-092915, 21219178.
9. Shan L, Molberg O, Parrot I, Hausch F, Filiz F, Gray GM, Sollid LM, Khosla C. Structural basis for gluten intolerance in Celiac sprue. Science 2002, 297(5590):2275-2279. 10.1126/science.1074129, 12351792.
10. van de Wal Y, Kooy Y, van Veelen P, Pena S, Mearin L, Papadopoulos G, Koning F. Cutting edge: Selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T cell reactivity. J Immunol 1998, 161(4):1585-1588.
11. 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, et al. 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.
12. Spaenij-Dekking L, Kooy-Winkelaar Y, Van Veelen P, Drijfhout JW, Jonker H, Van Soest L, Smulders MJM, Bosch D, Gilissen LJWJ, Koning F. Natural variation in toxicity of wheat: potential for selection of nontoxic varieties for celiac disease patients. Gastroenterology 2005, 129(3):797-806. 10.1053/j.gastro.2005.06.017, 16143119.
13. Molberg O, Uhlen AK, Jensen T, Flaete NS, Fleckenstein B, Arentz-Hansen H, Raki M, Lundin KEA, Sollid LM. Mapping of gluten T-cell epitopes in the bread wheat ancestors: implications for celiac disease. Gastroenterology 2005, 128(2):393-401. 10.1053/j.gastro.2004.11.003, 15685550.
14. Vincentini O, Borrelli O, Silano M, Gazza L, Pogna N, Luchetti R, De Vincenzi M. T-cell response to different cultivars of farro wheat, Triticum turgidum ssp dicoccum, in celiac disease patients. Clin Nutr 2009, 28(3):272-277. 10.1016/j.clnu.2009.03.013, 19395130.
15. Arentz-Hansen H, Korner R, Molberg O, Quarsten H, Vader W, Kooy YMC, Lundin KEA, Koning F, Roepstorff P, Sollid LM, et al. 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 2000, 191(4):603-612. 10.1084/jem.191.4.603, 2195837, 10684852.
16. Anderson RP, Degano P, Godkin AJ, 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(3):337-342. 10.1038/73200, 10700238.
17. Harberd NPBD, Thompson RD. Analysis of the gliadin multigene loci in bread wheat using nullisomic-tetrasomic lines. Mol Gen Genet 1985, 1985:234-242.
18. Okita TW, Cheesbrough V, Reeves CD. Evolution and Heterogeneity of the Alpha-Type Beta-Type and Gamma-Type Gliadin DNA-Sequences. J Biol Chem 1985, 260(13):8203-8213.
19. Anderson OD, Litts JC, Greene FC. The α-gliadin gene family. I. Characterization of ten new wheat α-gliadin genomic clones, evidence for limited sequence conservation of flanking DNA, and southern analysis of the gene family. Theor Appl Genet 1997, 95:50-58.
20. Anderson OD, Greene FC. The alpha-gliadin gene family.2. DNA and protein sequence variation, subfamily structure, and origins of pseudogenes. Theor Appl Genet 1997, 95(1-2):59-65.
21. van Herpen TWJM, Goryunova SV, van der Schoot J, Mitreva M, Salentijn E, Vorst O, Schenk MF, van Veelen PA, Koning F, van Soest LJM, et al. Alpha-gliadin genes from the A, B, and D genomes of wheat contain different sets of celiac disease epitopes. BMC Genom 2006, 7:1.
22. Mitea C, Kooy-Winkelaar Y, van Veelen P, de Ru A, Drijfhout JW, Koning F, Dekking L. Fine specificity of monoclonal antibodies against celiac disease-inducing peptides in the gluteome. Am J Clin Nutr 2008, 88(4):1057-1066.
23. Londono DM, van 't Westende WPC, Goryunova S, Salentijn EMJ, van den Broeck HC, van der Meer IM, Visser RGF, Gilissen LJWM, Smulders MJM. Avenin diversity analysis of the genus Avena (oat). Relevance for people with celiac disease. J Cereal Sci 2013, 58:170-177.
24. Metzker ML. Applications of next-generation sequencing sequencing technologies - the next generation. Nat Rev Genet 2010, 11(1):31-46. 10.1038/nrg2626, 19997069.
25. Brautigam A, Gowik U. What can next generation sequencing do for you? Next generation sequencing as a valuable tool in plant research. Plant Biol 2010, 12(6):831-841. 10.1111/j.1438-8677.2010.00373.x, 21040298.
26. Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, et al. A physical map of the 1-gigabase bread wheat chromosome 3B. Science 2008, 322(5898):101-104. 10.1126/science.1161847, 18832645.
27. Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES. An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 2000, 407(6803):513-516. 10.1038/35035083, 11029002.
28. Van Tassell CP, Smith TPL, Matukumalli LK, Taylor JF, Schnabel RD, Lawley CT, Haudenschild CD, Moore SS, Warren WC, Sonstegard TS. SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nat Methods 2008, 5(3):247-252. 10.1038/nmeth.1185, 18297082.
29. Barbazuk WB, Emrich SJ, Chen HD, Li L, Schnable PS. SNP discovery via 454 transcriptome sequencing. Plant J 2007, 51(5):910-918. 10.1111/j.1365-313X.2007.03193.x, 2169515, 17662031.
30. Schreiber AW. Transcriptome-scale homoeolog-specific transcript assemblies of bread wheat. BMC Genom 2012, 13:492.
31. Lai KT, Duran C, Berkman PJ, Lorenc MT, Stiller J, Manoli S, Hayden MJ, Forrest KL, Fleury D, Baumann U, et al. Single nucleotide polymorphism discovery from wheat next-generation sequence data. Plant Biotechnol J 2012, 10(6):743-749. 10.1111/j.1467-7652.2012.00718.x, 22748104.
32. You FM, Huo NX, Deal KR, Gu YQ, Luo MC, McGuire PE, Dvorak J, Anderson OD. Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genom 2011, 12:59.
33. Trebbi D, Maccaferri M, de Heer P, Sorensen A, Giuliani S, Salvi S, Sanguineti MC, Massi A, van der Vossen EAG, Tuberosa R. High-throughput SNP discovery and genotyping in durum wheat (Triticum durum Desf.). Theor Appl Genet 2011, 123:555-569. 10.1007/s00122-011-1607-7, 21611761.
34. Pagliarani G, Paris R, Arens P, Tartarini S, Ricci G, Smulders MJM, van de Weg WE. A qRT-PCR assay for the expression of all Mal d 1 isoallergen genes. BMC Plant Biol 2013, 13:51. 10.1186/1471-2229-13-51, 3616815, 23522122.
35. van den Broeck HC, Hongbing C, Lacaze X, Dusautoir JC, Gilissen LJWJ, Smulders MJM, van der Meer IM. In search of tetraploid wheat accessions reduced in celiac disease-related gluten epitopes. Mol BioSyst 2010, 6(11):2206-2213. 10.1039/c0mb00046a, 20714643.
36. 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 Genom 2009, 10:48.
37. Rothberg JM, Leamon JH. The development and impact of 454 sequencing. Nat Biotechnol 2008, 26(10):1117-1124. 10.1038/nbt1485, 18846085.
38. Anderson OD. The B-hordein prolamin family of barley. Genome 2013, 56:179-185. 10.1139/gen-2013-0016, 23659702.
39. Ravel C, Praud S, Murigneux A, Canaguier A, Sapet F, Samson D, Balfourier F, Dufour P, Chalhoub B, Brunel D, et al. Single-nucleotide polymorphism frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 2006, 49(9):1131-1139. 10.1139/g06-067, 17110993.
40. Kawaura K, Mochida K, Ogihara Y. Expression profile of two storage-protein gene families in hexaploid wheat revealed by large-scale analysis of expressed sequence tags. Plant Physiol 2005, 139(4):1870-1880. 10.1104/pp.105.070722, 1310565, 16306141.
41. Goryunova SV, Salentijn EMJ, Chikida NN, Kochieva EZ, van der Meer IM, Gilissen LJWJ, Smulders MJM. Expansion of the gamma-gliadin gene family in Aegilops and Triticum. BMC Evol Biol 2012, 12:215. 10.1186/1471-2148-12-215, 3537741, 23137212.
42. Van Herpen TWJM, Riley M, Sparks C, Jones HD, Gritsch C, Dekking EH, Hamer RJ, Bosch D, Salentijn EMJ, Smulders MJM, et al. Detailed analysis of the expression of an alpha-gliadin promoter and the deposition of alpha-gliadin protein during wheat grain development. Ann Bot 2008, 102(3):331-342. 10.1093/aob/mcn114, 2701793, 18621967.
43. Kawaura K, Wu J, Matsumoto T, Kanamori H, Katagiri S, Ogihara Y. Genome change in wheat observed through the structure and expression of alpha/beta-gliadin genes. Funct Integr Genomic 2012, 12(2):341-355.
44. Altenbach SB, Vensel WH, DuPont FM. Integration of transcriptomic and proteomic data from a single wheat cultivar provides new tools for understanding the roles of individual alpha gliadin proteins in flour quality and celiac disease. J Cereal Sci 2010, 52(2):143-151.
45. Melnikova NV, Mitrofanova OP, Liapounova OA, Kudryavtsev AM. Global diversity of durum wheat Triticum durum Desf. for alleles of gliadin-coding loci. Russ J Genet+ 2010, 46(1):43-49.
46. Metakovsky EV, Knezevic D, Javornik B. Gliadin allele composition of Yugoslav winter-wheat cultivars. Euphytica 1991, 54(3):285-295.
47. Kudryavtsev AM, Metakovsky EV. The Gliadins of wheat - their genetics and a possibility of using blocks of Gliadin components as genetic-markers of wheat agronomically important characteristics and in phylogenetic investigations. Genetika 1993, 29(1):13-27.
48. Melnikova NV, Kudryavtseva AV, Kudryavtsev AM. Catalogue of alleles of gliadin-coding loci in durum wheat (Triticum durum Desf.). Biochimie 2012, 94(2):551-557. 10.1016/j.biochi.2011.09.004, 21946233.
49. Kumar A, Simons K, Iqbal MJ, Jimenez MM, Bassi FM, Ghavami F, Al-Azzam O, Drader T, Wang Y, Luo MC, et al. Physical mapping resources for large plant genomes: radiation hybrids for wheat D-genome progenitor Aegilops tauschii. BMC Genom 2012, 13:597.
50. van den Broeck HC, Gilissen LJWJ, Smulders MJM, van der Meer IM, Hamer RJ. Dough quality of bread wheat lacking alpha-gliadins with celiac disease epitopes and addition of celiac-safe avenins to improve dough quality. J Cereal Sci 2011, 53(2):206-216.
51. Thuillet AC, Bataillon T, Poirier S, Santoni S, David JL. Estimation of long-term effective population sizes through the history of durum wheat using microsatellite data. Genetics 2005, 169(3):1589-1599. 1449565, 15545658.
52. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. TM4: A free, open-source system for microarray data management and analysis. Biotechniques 2003, 34(2):374-378.
53. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.