Synthetic peptides reproducing tissue transglutaminase-gliadin complex neo-epitopes as probes for antibody detection in celiac disease patients' sera

Journal of Medicinal Chemistry

Volumn 58, Issue 3, 2015, Pages 1390-1399

  Di Pisa, Margherita ^a,d   Pascarella, Simona ^a   Scrima, Mario ^b   Sabatino, Giuseppina ^a   Real Fernández, Feliciana ^a   Chelli, Mario ^a   Renzi, Daniela ^c   Calabrò, Antonio ^c   D'Ursi, Anna Maria ^b   Papini, Anna Maria ^a   Rovero, Paolo ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; ENDOMYSIUM ANTIBODY; EPITOPE; GLIADIN; IMMUNOGLOBULIN A ANTIBODY; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; SYNTHETIC PEPTIDE; ANTIBODY; GUANINE NUCLEOTIDE BINDING PROTEIN; PEPTIDE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ANTIBODY DETECTION; ARTICLE; BLOOD DONOR; CELIAC DISEASE; CONFORMATIONAL TRANSITION; CROSS LINKING; DEAMINATION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMUNOGENICITY; MOLECULAR DYNAMICS; MOLECULAR MODEL; PEPTIDE SYNTHESIS; RECEIVER OPERATING CHARACTERISTIC; SEROLOGY; SERUM; STRUCTURE ANALYSIS; ADOLESCENT; ADULT; ANTIGEN ANTIBODY REACTION; BLOOD; CHEMICAL STRUCTURE; CHEMISTRY; CHILD; FEMALE; IMMUNOLOGY; MALE; PRESCHOOL CHILD; SYNTHESIS; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIBODIES; ANTIGEN-ANTIBODY REACTIONS; CELIAC DISEASE; CHILD; CHILD, PRESCHOOL; EPITOPES; FEMALE; GLIADIN; GTP-BINDING PROTEINS; HUMANS; MALE; MODELS, MOLECULAR; PEPTIDES; TRANSGLUTAMINASES; YOUNG ADULT;

EID: 84922826656     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm5017126     Document Type: Article

References (48)

1. Murray, J. A. The widening spectrum of celiac disease Am. J. Clin. Nutr. 1999, 69, 354-365
2. Shaoul, R.; Lerner, A. Associated autoantibodies in celiac disease Autoimmun. Rev. 2007, 6, 559-565
3. Wieser, H. Chemistry of gluten proteins Food Microbiol. 2007, 24, 115-159
4. Schuppan, D.; Dennis, M. D.; Kelly, C. P. Celiac disease: Epidemiology, pathogenesis, diagnosis, and nutritional management Nutr. Clin. Care 2005, 8, 54-69
5. Rubio-Tapia, A.; Hill, I. D.; Kelly, C. P.; Calderwood, A. H.; Murray, J. A. ACG clinical guidelines: Diagnosis and management of celiac disease Am. J. Gastroenterol. 2013, 108, 656-676 (quiz 677).
6. Dieterich, W.; Laag, E.; Schöpper, H.; Volta, U.; Ferguson, A.; Gillett, H.; Riecken, E. O.; Schuppan, D. Autoantibodies to tissue transglutaminase as predictors of celiac disease Gastroenterology 1998, 115, 1317-1321
7. Troncone, R.; Maurano, F.; Rossi, M.; Micillo, M.; Greco, L.; Auricchio, R.; Salerno, G.; Salvatore, F.; Sacchetti, L. IgA antibodies to tissue transglutaminase: An effective diagnostic test for celiac disease J. Pediatr. 1999, 134 (2) 166-171
8. Reif, S.; Lerner, A. Tissue transglutaminase-the key player in celiac disease: a review Autoimmun. Rev. 2004, 3, 40-45
9. Husby, S.; Koletzko, S.; Korponay-Szabó, I. R.; Mearin, M. L.; Phillips, A.; Shamir, R.; Troncone, R.; Giersiepen, K.; Branski, D.; Catassi, C.; Lelgeman, M.; Mäki, M.; Ribes-Koninckx, C.; Ventura, A.; Zimmer, K. P. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease J. Pediatr. Gastroenterol. Nutr. 2012, 54 (1) 136-160
10. Bruins, M. J. The clinical response to gluten challenge: A review of the literature Nutrients 2013, 5, 4614-4641
11. Bizzaro, N.; Tampoia, M.; Villalta, D.; Platzgummer, S.; Liguori, M.; Tozzoli, R.; Tonutti, E. Low specificity of anti-tissue transglutaminase antibodies in patients with primary biliary cirrhosis J. Clin. Lab. Anal. 2006, 20, 184-189
12. Bakker, S. F.; Tushuizen, M. E.; Stokvis-Brantsma, W. H.; Aanstoot, H. J.; Winterdijk, P.; van Setten, P. A.; von Blomberg, B. M.; Mulder, C. J.; Simsek, S. Frequent delay of coeliac disease diagnosis in symptomatic patients with type 1 diabetes mellitus: Clinical and genetic characteristics Eur. J. Intern. Med. 2013, 24, 456-460
13. Scaramuzza, A. E.; Mantegazza, C.; Bosetti, A.; Zuccotti, G. V. Type 1 diabetes and celiac disease: The effects of gluten free diet on metabolic control World J. Diabetes 2013, 4, 130-134
14. Rolan, P.; Atkinson, A. J.; Lesko, L. J.; Committee, S. O.; Committee, C. R. Use of biomarkers from drug discovery through clinical practice: Report of the Ninth European Federation of Pharmaceutical Sciences Conference on Optimizing Drug Development Clin. Pharmacol. Ther. 2003, 73, 284-291
15. Baker, M. In biomarkers we trust? Nat. Biotechnol. 2005, 23, 297-304
16. Meloen, R. H.; Puijk, W. C.; Langeveld, J. P.; Langedijk, J. P.; Timmerman, P. Design of synthetic peptides for diagnostics Curr. Protein Pept. Sci. 2003, 4, 253-260
17. Papini, A. M. The use of post-translationally modified peptides for detection of biomarkers of immune-mediated diseases J. Pept. Sci. 2009, 15, 621-628
18. Ballew, J. T.; Murray, J. A.; Collin, P.; Mäki, M.; Kagnoff, M. F.; Kaukinen, K.; Daugherty, P. S. Antibody biomarker discovery through in vitro directed evolution of consensus recognition epitopes Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 19330-19335
19. Nenna, R.; Tiberti, C.; Petrarca, L.; Lucantoni, F.; Mennini, M.; Luparia, R. P.; Panimolle, F.; Mastrogiorgio, G.; Pietropaoli, N.; Magliocca, F. M.; Bonamico, M. The celiac iceberg: Characterization of the disease in primary schoolchildren J. Pediatr. Gastroenterol. Nutr. 2013, 56, 416-421
20. Aleanzi, M.; Demonte, A. M.; Esper, C.; Garcilazo, S.; Waggener, M. Celiac disease: Antibody recognition against native and selectively deamidated gliadin peptides Clin. Chem. 2001, 47, 2023-2028
21. Mothes, T. Deamidated gliadin peptides as targets for celiac disease-specific antibodies Adv. Clin. Chem. 2007, 44, 35-63
22. Schwertz, E.; Kahlenberg, F.; Sack, U.; Richter, T.; Stern, M.; Conrad, K.; Zimmer, K. P.; Mothes, T. Serologic assay based on gliadin-related nonapeptides as a highly sensitive and specific diagnostic aid in celiac disease Clin. Chem. 2004, 50, 2370-2375
23. Qiao, S. W.; Sollid, L. M.; Blumberg, R. S. Antigen presentation in celiac disease Curr. Opin. Immunol. 2009, 21, 111-117
24. Tollefsen, S.; Arentz-Hansen, H.; Fleckenstein, B.; Molberg, O.; Ráki, M.; Kwok, W. W.; Jung, G.; Lundin, K. E.; Sollid, L. M. HLA-DQ2 and -DQ8 signatures of gluten T cell epitopes in celiac disease J. Clin. Invest. 2006, 116, 2226-2236
25. Matthias, T.; Neidhöfer, S.; Pfeiffer, S.; Prager, K.; Reuter, S.; Gershwin, M. E. Novel trends in celiac disease Cell. Mol. Immunol. 2011, 8, 121-125
26. Matthias, T.; Pfeiffer, S.; Selmi, C.; Gershwin, M. E. Diagnostic challenges in celiac disease and the role of the tissue transglutaminase-neo-epitope Clin. Rev. Allergy Immunol. 2010, 38, 298-301
27. Fleckenstein, B.; Qiao, S. W.; Larsen, M. R.; Jung, G.; Roepstorff, P.; Sollid, L. M. Molecular characterization of covalent complexes between tissue transglutaminase and gliadin peptides J. Biol. Chem. 2004, 279, 17607-17616
28. Liu, S.; Cerione, R. A.; Clardy, J. Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 2743-2747
29. Pinkas, D. M.; Strop, P.; Brunger, A. T.; Khosla, C. Transglutaminase 2 undergoes a large conformational change upon activation PLoS Biol. 2007, 5 e327
30. Miller, M. L.; Johnson, G. V. Rapid, single-step procedure for the identification of transglutaminase-mediated isopeptide crosslinks in amino acid digests J. Chromatogr. B: Biomed. Sci. Appl. 1999, 732, 65-72
31. Dørum, S.; Arntzen, M.; Qiao, S. W.; Holm, A.; Koehler, C. J.; Thiede, B.; Sollid, L. M.; 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
32. Shan, L.; Molberg, Ø.; Parrot, I.; Hausch, F.; Filiz, F.; Gray, G. M.; Sollid, L. M.; Khosla, C. Structural basis for gluten intolerance in celiac sprue Science 2002, 297, 2275-2279
33. Van Regenmortel, M. H. Antigenicity and immunogenicity of synthetic peptides Biologicals 2001, 29, 209-13
34. Habbema, J. D.; Eijkemans, R.; Krijnen, J.; Knottnerus, J. E. Analysis of data on the accuracy of diagnostic tests. In: The Evidence Base of Clinical Diagnosis; Knottnerus, J. E., Ed.; BMJ Books: London, 2002; pp 117-143.
35. Kim, D. E.; Chivian, D.; Baker, D. Protein structure prediction and analysis using the Robetta server Nucleic Acids Res. 2004, 32, W526-531
36. Hutchinson, E. G.; Thornton, J. M. PROMOTIF - a program to identify and analyze structural motifs in proteins Protein Sci. 1996, 5, 212-220
37. Laskowski, R. A.; MacArthur, M. W.; Moss, D. S.; Thornton, J. M. PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 1993, 26, 283-291
38. De Vries, S. J.; van Dijk, M.; Bonvin, A. M. The HADDOCK web server for data-driven biomolecular docking Nat. Protoc 2010, 5, 883-897
39. Benkert, P.; Biasini, M.; Schwede, T. Toward the estimation of the absolute quality of individual protein structure models Bioinformatics 2011, 27, 343-350
40. Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M. R.; Smith, J. C.; Kasson, P. M.; van der Spoel, D. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 2013, 29, 845-854
41. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins: Struct., Funct., Bioinf. 2010, 78, 1950-1958
42. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98, 10089-10092
43. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A smooth particle mesh Ewald method J. Chem. Phys. 1995, 103, 8577-8593
44. Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method J. Appl. Phys. 1981, 52, 7182-7190
45. Nosé, S. A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 1984, 52, 255-268
46. Hoover, W. G. Canonical dynamics: eEquilibrium phase-space distributions Phys. Rev. A 1985, 31, 1695
47. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Biopolymers 1983, 22, 2577-2637
48. Daura, X.; Gademann, K.; Jaun, B.; Seebach, D.; van Gunsteren, W. F.; Mark, A. E. Peptide folding: When simulation meets experiment Angew. Chem., Int. Ed. 1999, 38, 236-240