Should digestion assays be used to estimate persistence of potential allergens in tests for safety of novel food proteins?

Clinical and Molecular Allergy

Volumn 7, Issue , 2009, Pages

  Schnell, Santiago ^a   Herman, Rod A ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b DOW AGROSCIENCES LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOOD ALLERGEN; PEPSIN A;

ALLERGENICITY; ALLERGIC REACTION; ASSAY; CROSS REACTION; DIGESTION; FOOD ALLERGY; FOOD INTAKE; FOOD SAFETY; GASTROINTESTINAL TRACT; IN VITRO STUDY; PROTEIN INTAKE; REVIEW; SIMULATED GASTRIC FLUID DIGESTION ASSAY; SIMULATION; STAINING;

EID: 61349161803     PISSN: None     EISSN: 14767961     Source Type: Journal    
DOI: 10.1186/1476-7961-7-1     Document Type: Review

References (87)

1. Deplancke B Gaskins HR Microbial modulation of innate defense: Goblet cells and the intestinal mucus layer American Journal of Clinical Nutrition 2001, 73:1131S-1141S 11393191
2. Brandtzaeg P Current understanding of gastrointestinal immunoregulation and its relation to food allergy Ann N Y Acad Sci 2002, 964:13-45 12023193
3. Faria AMC Weiner HL Oral tolerance Immunological Reviews 2005, 206:232-259 10.1111/j.0105-2896.2005.00280.x 16048553
4. Brunner M Walzer M Absorption of undigested proteins in human beings: the absorption of unaltered fish proteins in adults Arch Intern Med 1928, 42:173-179
5. Husby S Jensenius JC Svehag SE Passage of undegraded dietary antigen into the blood of healthy adults. Quantification, estimation of size distribution, and relation of uptake to levels of specific antibodies Scandinavian Journal of Immunology 1985, 22:83-92 10.1111/ j.1365-3083.1985.tb01862.x 4023632
6. Husby S Jensenius JC Svehag SE Passage of undegraded dietary antigen into the blood of healthy adults. Further characterization of the kinetics of uptake and the size distribution of the antigen Scandinavian Journal of Immunology 1986, 24:447-455 10.1111/ j.1365-3083.1986.tb02133.x 3764346
7. MacDonald TT Monteleone G Immunity, inflammation, and allergy in the gut Science 2005, 307:1920-1925 10.1126/science.1106442 15790845
8. Kanny G Moneret-Vautrin DA Flabbee J Beaudouin E Morisset M Thevenin F Population study of food allergy in France Journal of Allergy and Clinical Immunology 2001, 108:133-140 10.1067/mai.2001.116427
9. Sicherer SH Munoz-Furlong A Sampson HA Prevalence of seafood allergy in the United States determined by a random telephone survey Journal of Allergy and Clinical Immunology 2004, 114:159-165 10.1016/ j.jaci.2004.04.018
10. Brown AFT McKinnon D Emergency department anaphylaxis: A review of 142 patients in a single year Journal of Allergy and Clinical Immunology 2001, 108:861-866 10.1067/mai.2001.119028
11. Sampson HA Food anaphylaxis British Medical Bulletin 2000, 56:925-935 10.1258/0007142001903607 11359629
12. Sampson HA Food allergy. Part 1: Immunopathogenesis and clinical disorders Journal of Allergy and Clinical Immunology 1999, 103:717-728 10.1016/S0091-6749(99)70411-2
13. Breiteneder H Mills ENC Molecular properties of food allergens Journal of Allergy and Clinical Immunology 2005, 115:14-23 10.1016/ j.jaci.2004.10.022
14. Hauser M M E Wallner M Wopfner N Schmidt G Ferreira F Molecular Properties of Plant Food Allergens: A Current Classification into Protein Families The Open Immunology Journal 2008, 1:1-12
15. Lehrer SB Bannon GA Risks of allergic reactions to biotech proteins in foods: Perception and reality Allergy 2005, 60:559-564 10.1111/ j.1398-9995.2005.00704.x 15813800
16. Dirks CG Pedersen MH Platzer MH Bindsley-Jensen C Skov PS Poulsen LK Does absorption across the buccal mucosa explain early onset of food-induced allergic systemic reactions? Journal of Allergy and Clinical Immunology 2005, 115:1321-1323 10.1016/j.jaci.2005.03.027
17. Untersmayr E Vestergaard H Malling HJ Jensen LB Platzer MH Boltz-Nitulescu G Scheiner O Skov PS Jensen-Jarolim E Poulsen LK Incomplete digestion of codfish represents a risk factor for anaphylaxis in patients with allergy Journal of Allergy and Clinical Immunology 2007, 119:711-717 10.1016/j.jaci.2006.10.039
18. Husby S Foged N Host A Svehag SE Passage of dietary antigens into the blood of children with celiac disease. Quantification and size distribution of absorbed antigens Gut 1987, 28:1062-1072 1433239 3678964 10.1136/gut.28.9.1062
19. Erickson RH Kim YS Digestion and absorption of dietary protein Annual Review of Medicine 1990, 41:133-139 10.1146/annurev.me.41.020190.001025 2184718
20. York IA Goldberg AL Mo XY Rock KL Proteolysis and class I major histocompatibility complex antigen presentation Immunological Reviews 1999, 172:49-66 10.1111/j.1600-065X.1999.tb01355.x 10631936
21. Berrens L Digestion of atopic allergens with trypsin, α-chymotrypsin and pancreatic kallikrein, and influence of allergens upon the proteolytic and esterolytic activity of these enzymes Immunochemistry 1968, 5:585 10.1016/0019-2791(68)90094-3 5702352
22. Untersmayr E Jensen-Jarolim E The role of protein digestibility and antacids on food allergy outcomes Journal of Allergy and Clinical Immunology 2008, 121:1301-1308 10.1016/j.jaci.2008.04.025
23. Aalberse RC Food allergens Environmental Toxicology and Pharmacology 1997, 4:55-60 10.1016/S1382-6689(97)10042-4
24. Vieths S Allergenic cross-reactivity, food allergy and pollen Environmental Toxicology and Pharmacology 1997, 4:61-70 10.1016/ S1382-6689(97)10043-6
25. Bannon GA What makes a food protein an allergen? Current Allergy and Asthma Reports 2004, 4:43-46 10.1007/s11882-004-0042-0
26. Jensen-Jarolim E Wiedermann U Ganglberger E Zurcher A Stadler BM Boltz-Nitulescu G Scheiner O Breiteneder H Allergen mimotopes in food enhance type I allergic reactions in mice Faseb Journal 1999, 13:1586-1592 10463950
27. Vieths S Scheurer S Ballmer-Weber B Current understanding of cross-reactivity of food allergens and pollen Ann N Y Acad Sci 2002, 964:47-68 12023194
28. Bannon G Fu TJ Kimber I Hinton DM Protein digestibility and relevance to allergenicity Environmental Health Perspectives 2003, 111:1122-1124 1241561 12826484
29. Bannon GA Goodman RE Leach JN Rice E Fuchs RL Astwood JD Digestive Stability in the Context of Assessing the Potential Allergenicity of Food Proteins Comments on Toxicology 2002, 8:271-285 10.1080/ 08865140214384
30. Goodman RE Vieths S Sampson HA Hill D Ebisawa M Taylor SL van Ree R Allergenicity assessment of genetically modified crops - what makes sense? Nature Biotechnology 2008, 26:73-81 10.1038/nbt1343 18183024
31. Ofori-Anti AO Ariyarathna H Chen L Lee HL Pramod SN Goodman RE Establishing objective detection limits for the pepsin digestion assay used in the assessment of genetically modified foods Reg Toxicol Pharmacol 2008, 52:94-103 10.1016/j.yrtph.2008.06.006
32. EFSA Updated guidance document for the risk assessment of genetically modified plants and derived food and feed The EFSA Journal 2008, 727:1-135
33. Joint FAO/WHO Food Standard Programme, Twenty-Fifth Session Rome, Italy: CODEX Alimentarius Commission 2003
34. Astwood JD Leach JN Fuchs RL Stability of food allergens to digestion in vitro Nature Biotechnology 1996, 14:1269-1273 10.1038/nbt1096-1269 9631091
35. Lehrer SB Horner WE Reese G Why are some proteins allergenic? Implications for biotechnology Critical Reviews in Food Science and Nutrition 1996, 36:553-564 8841731
36. USP The United States Pharmacopeia 24. Simulated gastric fluid, TS The National Formulary Rockville, MD: United States Pharmacopeial Convention, Inc Trustees Bo 2000, 19:2235
37. Azarmi S Roa W Lobenberg R Current perspectives in dissolution testing of conventional and novel dosage forms International Journal of Pharmaceutics 2007, 328:12-21 10.1016/j.ijpharm.2006.10.001 17084051
38. Thomas K Aalbers M Bannon GA Bartels M Dearman RJ Esdaile DJ Fu TJ Glatt CM Hadfield N Hatzos C et al A multi-laboratory evaluation of a common in vitro pepsin digestion assay protocol used in assessing the safety of novel proteins Regulatory Toxicology and Pharmacology 2004, 39:87-98 10.1016/j.yrtph.2003.11.003
39. Oka T Morihara K Specificity of pepsin: Size and property of the active site FEBS Letters 1970, 10:222-224 10.1016/0014-5793(70)80633-0 11945397
40. Fontana A de Laureto PP Spolaore B Frare E Picotti P Zambonin M Probing protein structure by limited proteolysis Acta Biochimica Polonica 2004, 51:299-321 15218531
41. Park C Marqusee S Probing the high energy states in proteins by proteolysis Journal of Molecular Biology 2004, 343:1467-1476 10.1016/ j.jmb.2004.08.085 15491624
42. Herman R Gao Y Storer N Acid-induced unfolding kinetics in simulated gastric digestion of proteins Regulatory Toxicology and Pharmacology 2006, 46:93-99 10.1016/j.yrtph.2006.05.010
43. Kamatari YO Dobson CM Konno T Structural dissection of alkaline-denatured pepsin Protein Science 2003, 12:717-724 2323848 12649430 10.1110/ps.0219903
44. Brussock SM Currier TC Use of sodium dodecyl-sulfate polyacrylamide gel electrophoresis to quantify Bacillus thuringiensis delta-endotoxins ACS Symposium Series 1990, 432:78-87
45. Herman RA Schafer BW Korjagin VA Ernest AD Rapid digestion of Cry34Ab1 and Cry35Ab1 in simulated gastric fluid Journal of Agricultural and Food Chemistry 2003, 51:6823-6827 10.1021/jf034290p
46. Tal M Silberstein A Nusser E Why does Coomassie Brilliant Blue R interact differently with different proteins? A partial answer Journal of Biological Chemistry 1985, 260:9976-9980 4019521
47. Herman RA Woolhiser MM Ladics GS Korjagin VA Schafer BW Storer NP Green SB Kan L Stability of a set of allergens and non-allergens in simulated gastric fluid International Journal of Food Sciences and Nutrition 2007, 58:125-141 10.1080/09637480601149640
48. Huby RDJ Dearman RJ Kimber I Why are some proteins allergens? Toxicological Sciences 2000, 55:235-246 10.1093/toxsci/55.2.235 10828254
49. Scow KM Schmidt SK Alexander M Kinetics of biodegradation of mixtures of substrates in soil Soil Biology & Biochemistry 1989, 21:703-708 10.1016/0038-0717(89)90067-9
50. Herman RA Scherer PN Comparison of linear and nonlinear regression for modeling the first-order degradation of pest-control substances in soil Journal of Agricultural and Food Chemistry 2003, 51:4722-4726 10.1021/ jf034135a
51. Dvorchik BH Vesell ES Pharmacokinetic interpretation of data gathered during therapeutic drug monitoring Clinical Chemistry 1976, 22:868-878 776451
52. Vaintraub IA Kinetics of the co-operative proteolysis Nahrung-Food 1998, 42:59-60 10.1002/ (SICI)1521-3803(199804)42:02<59::AID-FOOD59>3.3.CO;2-N
53. Vaintraub IA Morari D Applying the increase in rate constants of cooperative proteolysis to the determination of transition curves of protein denaturation Journal of Biochemical and Biophysical Methods 2003, 57:191-201 10.1016/S0165-022X(03)00106-4
54. Herman RA Storer NA Gao Y Digestion assays in allergenicity assessment of transgenic proteins Environmental Health Perspectives 2006, 114:1154-1157 1552003 16882518
55. Srividhya J Schnell S Why substrate depletion has apparent first-order kinetics in enzymatic digestion Computational Biology and Chemistry 2006, 30:209-214 10.1016/j.compbiolchem.2006.03.003
56. Herman RA Korjagin VA Schafer BW Quantitative measurement of protein digestion in simulated gastric fluid Regulatory Toxicology and Pharmacology 2005, 41:175-184 10.1016/j.yrtph.2004.12.004
57. Imoto T Yamada H Ueda T Unfolding rates of globular proteins determined by kinetics of proteolysis Journal of Molecular Biology 1986, 190:647-649 10.1016/0022-2836(86)90250-0 3783715
58. Noda Y Fujiwara K Yamamoto K Fukuno T Segawa S Specificity of typsin digestion and conformational flexibility at different sites of unfolded lysozyme Biopolymers 1994, 34:217-226 10.1002/bip.360340208 8142590
59. Schnell S Mendoza C The condition for pseudo-first-order kinetics in enzymatic reactions is independent of the initial enzyme concentration Biophysical Chemistry 2004, 107:165-174 10.1016/j.bpc.2003.09.003 14962597
60. Terada S Kato T Izumiya N Synthesis and hydrolysis by pepsin and trypsin of a cyclic hexapeptide containing lysine and phenylalanine European Journal of Biochemistry 1975, 52:273-282 10.1111/ j.1432-1033.1975.tb03995.x 240680
61. Irvine GB Blumsom NL Elmore DT The kinetics of hydrolysis of some synthetic substrates containing neutral hydrophilic groups by pig pepsin and chicken liver cathepsin-D Biochemical Journal 1983, 211:237-242 1154347 6409091
62. Schnell S Maini PK Enzyme kinetics at high enzyme concentration Bulletin of Mathematical Biology 2000, 62:483-499 10.1006/bulm.1999.0163 10812718
63. Tzafriri AR Michaelis-Menten kinetics at high enzyme concentrations Bulletin of Mathematical Biology 2003, 65:1111-1129 10.1016/ S0092-8240(03)00059-4 14607291
64. Bandstra JZ Tratnyek PG Central limit theorem for chemical kinetics in complex systems Journal of Mathematical Chemistry 2005, 37:409-422 10.1007/s10910-004-1107-y
65. Fu TJ Digestion stability as a criterion for protein allergenicity assessment Ann N Y Acad Sci 2002, 964:99-110 12023197
66. Fu TT Abbott UR Hatzos C Digestibility of food allergens and nonallergenic proteins in simulated gastric fluid and simulated intestinal fluid - A comparative study Journal of Agricultural and Food Chemistry 2002, 50:7154-7160 10.1021/jf020599h
67. Chikwamba RK Scott MP Mejia LB Mason HS Wang K Localization of a bacterial protein in starch granules of transgenic maize kernels Proceedings of the National Academy of Sciences of the United States of America 2003, 100:11127-11132 196938 12960364 10.1073/pnas.1836901100
68. Takagi K Teshima R Okunuki H Sawada J Comparative study of in vitro digestibility of food proteins and effect of preheating on the digestion Biological & Pharmaceutical Bulletin 2003, 26:969-973 10.1248/ bpb.26.969 12843620
69. Moreno FJ Mackie AR Mills ENC Phospholipid interactions protect the milk allergen alpha-lactalbumin from proteolysis during in vitro digestion Journal of Agricultural and Food Chemistry 2005, 53:9810-9816 10.1021/ jf0515227
70. Tagliazucchi D Verzelloni E Conte A Effect of some phenolic compounds and beverages on pepsin activity during simulated gastric digestion Journal of Agricultural and Food Chemistry 2005, 53:8706-8713 10.1021/ jf058074n
71. Weangsripanaval T Moriyama T Kageura T Ogawa T Kawada T Dietary fat and an exogenous emulsifier increase the gastrointestinal absorption of a major soybean allergen, Gly m Bd 30K, in mice Journal of Nutrition 2005, 135:1738-1744 15987858
72. Peyron S Mouecoucou J Fremont S Sanchez C Gontard N Effects of heat treatment and pectin addition on beta-lactoglobulin allergenicity Journal of Agricultural and Food Chemistry 2006, 54:5643-5650 10.1021/ jf053178j
73. Polovic N Blanusa M Gavrovic-Jankulovic M Atanaskovic-Markovic M Burazer L Jankov R Velickovic TC A matrix effect in pectin-rich fruits hampers digestion of allergen by pepsin in vivo and in vitro Clinical and Experimental Allergy 2007, 37:764-771 10.1111/j.1365-2222.2007.02703.x
74. Yagami T Haishima Y Nakamura A Osuna H Ikezawa Z Digestibility of allergens extracted from natural rubber latex and vegetable foods Journal of Allergy and Clinical Immunology 2000, 106:752-762 10.1067/ mai.2000.109171
75. Vieths S Reindl J Muller U Hoffmann A Haustein D Digestibility of peanut and hazelnut allergens investigated by a simple in vitro procedure European Food Research and Technology 1999, 209:379-388 10.1007/ s002170050513
76. Moreno FJ Gastrointestinal digestion of food allergens: Effect on their allergenicity Biomedicine & Pharmacotherapy 2007, 61:50-60 10.1016/ j.biopha.2006.10.005
77. Untersmayr E Bakos N Scholl I Kundi M Roth-Walter F Szalai K Riemer AB Ankersmit HJ Scheiner O Boltz-Nitulescu G Jensen-Jarolim E Anti-ulcer drugs promote IgE formation toward dietary antigens in adult patients Faseb Journal 2005, 19:656-658 15671152
78. Untersmayr E Scholl I Swoboda I Beil WJ Forster-Waldl E Walter F Riemer A Kraml G Kinaciyan T Spitzauer S et al Antacid medication inhibits digestion of dietary proteins and causes food allergy: A fish allergy model in Balb/c mice Journal of Allergy and Clinical Immunology 2003, 112:616-623 10.1016/S0091-6749(03)01719-6
79. Untersmayr E Jensen-Jarolim E The effect of gastric digestion on food allergy Current Opinion in Allergy and Clinical Immunology 2006, 6:214-219 10.1097/01.all.0000225163.06016.93
80. Metcalfe DD Genetically modified crops and allergenicity Nature Immunology 2005, 6:857-860 10.1038/ni0905-857 16116460
81. Crevel RWR Briggs D Hefle SL Knulst AC Taylor SL Hazard characterisation in food allergen risk assessment: The application of statistical approaches and the use of clinical data Food Chem Toxicol 2007, 45:691-701 10.1016/j.fct.2006.09.005 17343968
82. Kimura T Higaki K Gastrointestinal transit and drug absorption Biological & Pharmaceutical Bulletin 2002, 25:149-164 10.1248/ bpb.25.149 11853157
83. Pasini G Simonato B Curioni A Vincenzi S Cristaudo A Santucci B Peruffo ADB Giannattasio M IgE-mediated allergy to corn: A 50 kDa protein, belonging to the Reduced Soluble Proteins, is a major allergen Allergy 2002, 57:98-106 10.1034/j.1398-9995.2002.1o3413.x 11929411
84. Mouecoucou J Villaume C Sanchez C Mejean L beta-lactoglobulin/ polysaccharide interactions during in vitro gastric and pancreatic hydrolysis assessed in dialysis bags of different molecular weight cut-offs Biochimica Et Biophysica Acta-General Subjects 2004, 1670:105-112 10.1016/j.bbagen.2003.10.017
85. Mouecoucou J Villaume C Sanchez C Mejean L Effects of gum arabic, low methoxy pectin and xylan on in vitro digestibility of peanut protein Food Research International 2004, 37:777-783 10.1016/ j.foodres.2004.04.002
86. Moreno FJ Mellon FA Wickham MSJ Bottrill AR Mills ENC Stability of the major allergen Brazil nut 2S albumin (Ber e 1) to physiologically relevant in vitro gastrointestinal digestion Febs Journal 2005, 272:341-352 10.1111/j.1742-4658.2004.04472.x 15654873
87. Dearman RJ Skinner RA Herouet C Labay K Debruyne E Kimber I Induction of IgE antibody responses by protein allergens: Inter-laboratory comparisons Food and Chemical Toxicology 2003, 41:1509-1516 10.1016/ S0278-6915(03)00167-4