Evaluation of protease resistance and toxicity of amyloid-like food fibrils from whey, soy, kidney bean, and egg white

Food Chemistry

Volumn 192, Issue , 2016, Pages 491-498

  Lassé, Moritz ^a,b   Ulluwishewa, Dulantha ^a,c   Healy, Jackie ^b   Thompson, Dion ^d   Miller, Antonia ^b,d   Roy, Nicole ^a,c   Chitcholtan, Kenny ^e   Gerrard, Juliet A ^a,b,d,f  

^a MASSEY UNIVERSITY   (New Zealand)

^b UNIVERSITY OF CANTERBURY   (New Zealand)

^c AGRESEARCH GRASSLANDS   (New Zealand)

^d CALLAGHAN INNOVATION   (New Zealand)

^e UNIVERSITY OF OTAGO   (New Zealand)

^f UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Aggregate; Amyloid; Caco 2; Cytotoxicity; Digestibility; Hec 1a; Protein

Indexed keywords

AGGREGATES; CELL CULTURE; CYTOTOXICITY; HEALTH RISKS; PROTEINS; SURFACE CHEMISTRY; TOXICITY;

AMYLOID; AMYLOID-LIKE FIBRIL; CACO-2; DIGESTIBILITY; FUNCTIONAL SURFACES; HEC-1A; HUMAN CANCER CELLS; PROTEOLYTIC DIGESTION;

GLYCOPROTEINS;

AMYLOID; EGG WHITE; PANCREATIN; PEPSIN A; PROTEINASE; PROTEINASE K; PEPTIDE HYDROLASE;

ARTICLE; CANCER CELL LINE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; IN VITRO STUDY; PHASEOLUS VULGARIS; PROTEIN DEGRADATION; SOYBEAN; ULTRASOUND; WHEY; CACO 2 CELL LINE; CHEMISTRY; EPITHELIUM CELL; METABOLISM; PHASEOLUS; PLANT SEED; TRANSFORMED CELL LINE;

PHASEOLUS VULGARIS;

AMYLOID; CACO-2 CELLS; CELL LINE, TRANSFORMED; EGG WHITE; EPITHELIAL CELLS; HUMANS; PEPTIDE HYDROLASES; PHASEOLUS; PROTEOLYSIS; SEEDS; SOYBEANS; WHEY;

EID: 84937232321     PISSN: 03088146     EISSN: 18737072     Source Type: Journal    
DOI: 10.1016/j.foodchem.2015.07.044     Document Type: Article

References (40)

1. C. Akkermans, A.J. Van der Goot, P. Venema, H. Gruppen, J.M. Vereijken, E. Van der Linden, and et al. Micrometer-sized fibrillar protein aggregates from soy glycinin and soy protein isolate Journal of Agricultural and Food Chemistry 55 24 2007 9877 9882 10.1021/jf0718897
2. Y. Ano, H. Nakayama, Y. Sakai, A. Sakudo, M. Endo, S. Ebisu, and et al. Incorporation of β-amyloid protein through the bovine ileal epithelium before and after weaning: Model for orally transmitted amyloidoses Microbiology and Immunology 52 8 2008 429 434 10.1111/j.1348-0421.2008.00054.x
3. L. Bateman, A. Ye, and H. Singh In vitro digestion of β-lactoglobulin fibrils formed by heat treatment at low pH Journal of Agricultural and Food Chemistry 58 17 2010 9800 9808 10.1021/jf101722t
4. L. Bateman, A. Ye, and H. Singh Re-formation of fibrils from hydrolysates of β-lactoglobulin fibrils during in vitro gastric digestion Journal of Agricultural and Food Chemistry 59 17 2011 9605 9611 10.1021/jf2020057
5. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, J. Zurdo, and et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 6880 2002 507 511 10.1038/416507a
6. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annual Review of Biochemistry 75 1 2006 333 366 10.1146/annurev.biochem.75.101304.123901
7. D. Cui, H. Kawano, Y. Hoshii, Y. Liu, and T. Ishihara Acceleration of murine AA amyloid deposition by bovine amyloid fibrils and tissue homogenates Amyloid 15 2 2008 77 83 10.1080/13506120802005833
8. J. De Groot, and H.H.J. de Jongh The presence of heat-stable conformers of ovalbumin affects properties of thermally formed aggregates Protein Engineering 16 12 2003 1035 1040 10.1093/protein/gzg123
9. F.C. Dehle, H. Ecroyd, I.F. Musgrave, and J.A. Carver ΑB-Crystallin inhibits the cell toxicity associated with amyloid fibril formation by κ-casein and the amyloid-β peptide Cell Stress & Chaperones 15 6 2010 1013 1026 10.1007/s12192-010-0212-z
10. E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M.R. Wilkins, R.D. Appel, and et al. Protein identification and analysis tools on the ExPASy server J.M. Walker, The proteomics protocols handbook 2005 Humana Press Portland 571 607
11. C.G. Glabe Common mechanisms of amyloid oligomer pathogenesis in degenerative disease Neurobiology of Aging 27 4 2006 570 575
12. C.G. Glabe, and R. Kayed Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis Neurology 66 1 2006 S74 S78
13. Graff, Brinch, and Madsen Simplified scintigraphic methods for measuring gastrointestinal transit times Clinical Physiology 20 4 2000 262 266
14. C.A. Hettiarachchi, L.D. Melton, J.A. Gerrard, and S.M. Loveday Formation of β-lactoglobulin nanofibrils by microwave heating gives a peptide composition different from conventional heating Biomacromolecules 13 9 2012 2868 2880
15. A.A. Kamat, W.M. Merritt, D. Coffey, Y.G. Lin, P.R. Patel, and R. Broaddus Clinical and biological significance of vascular endothelial growth factor in endometrial cancer Clinical Cancer Research 13 24 2007 7487 7495 10.1158/1078-0432.CCR-07-1017
16. M. Kaur, J. Healy, M. Vasudevamurthy, M. Lassé, L. Puskar, and M.J. Tobin Stability and cytotoxicity of crystallin amyloid nanofibrils Nanoscale 6 21 2014 13169 13178 10.1039/C4NR04624B
17. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 5618 2003 486 489 10.1126/science.1079469
18. A. Kroes-Nijboer, P. Venema, and E. van der Linden Fibrillar structures in food Food & Function 2012 3 2012 221 227 10.1039/c1fo10163c
19. C. Li, J. Adamcik, and R. Mezzenga Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties Nature Nanotechnology 7 7 2012 421 427 10.1038/nnano.2012.62
20. S.M. Loveday, M.A. Rao, L.K. Creamer, and H. Singh Factors affecting rheological characteristics of fibril gels: the case of β-lactoglobulin and α-lactalbumin Journal of Food Science 74 3 2009 47 55
21. S.M. Loveday, J. Su, M.A. Rao, S.G. Anema, and H. Singh Effect of calcium on the morphology and functionality of whey protein nanofibrils Biomacromolecules 12 10 2011 3780 3788 10.1021/bm201013b
22. 2 International Dairy Journal 20 9 2010 571 579 10.1016/j.idairyj.2010.02.014
23. M. Minekus, M. Alminger, P. Alvito, S. Ballance, T. Bohn, and C. Bourlieu A standardised static in vitro digestion method suitable for food - An international consensus Food & Function 5 6 2014 1113 10.1039/c3fo60702j
24. L. Nielsen, R. Khurana, A. Coats, and S. Frokjaer Effect of environmental factors on the kinetics of insulin fibril formation: Elucidation of the molecular mechanism Biochemistry 40 20 2001 6036 6046
25. A.T. Petkova, R.D. Leapman, Z. Guo, W.-M. Yau, M.P. Mattson, and R. Tycko Self-propagating, molecular-level polymorphism in Alzheimer's ß-amyloid fibrils Science 307 5707 2005 262 265 10.1126/science.1105850
26. J.K. Raynes, J.A. Carver, S.L. Gras, and J.A. Gerrard Protein nanostructures in food - Should we be worried? Trends in Food Science & Technology 37 1 2014 42 50 10.1016/j.tifs.2014.02.003
27. L.M.C. Sagis, C. Veerman, and E. van der Linden Mesoscopic properties of semiflexible amyloid fibrils Langmuir 20 3 2004 924 927 10.1021/la035390s
28. M. Stefani Biochemical and biophysical features of both oligomer/fibril and cell membrane in amyloid cytotoxicity FEBS Journal 277 22 2010 4602 4613 10.1111/j.1742-4658.2010.07889.x
29. M. Stefani, and C.M. Dobson Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution Journal of Molecular Medicine 81 11 2003 678 699 10.1007/s00109-003-0464-5
30. N. Tanaka, Y. Morimoto, Y. Noguchi, T. Tada, T. Waku, S. Kunugi, and et al. The mechanism of fibril formation of a non-inhibitory serpin ovalbumin revealed by the identification of amyloidogenic core regions Journal of Biological Chemistry 286 7 2011 5884 5894 10.1074/jbc.M110.176396
31. C.-H. Tang, and C.-S. Wang Formation and characterization of amyloid-like fibrils from soy β-conglycinin and glycinin Journal of Agricultural and Food Chemistry 58 20 2010 11058 11066 10.1021/jf1021658
32. C.-H. Tang, Y.-H. Zhang, Q.-B. Wen, and Q. Huang Formation of amyloid fibrils from kidney bean 7S globulin (phaseolin) at pH 2.0 Journal of Agricultural and Food Chemistry 58 13 2010 8061 8068 10.1021/jf101311f
33. E.K. Ulleberg, I. Comi, H. Holm, E.B. Herud, M. Jacobsen, and G.E. Vegarud Human gastrointestinal juices intended for use in in vitro digestion models Food Digestion 2 1-3 2011 52 61 10.1007/s13228-011-0015-4
34. D. Ulluwishewa, R.C. Anderson, W. Young, W.C. McNabb, P. van Baarlen, P.J. Moughan, and et al. Live Faecalibacterium prausnitzii in an apical anaerobic model of the intestinal epithelial barrier Cellular Microbiology 2014 10.1111/cmi.12360. http://doi.org/10.1111/cmi.12360
35. R. Vassar β-Secretase, APP and Aβ in Alzheimer's disease Alzheimer's Disease 2005 79 103
36. J.-M. Wang, X.-Q. Yang, S.-W. Yin, D.-B. Yuan, N. Xia, and J.-R. Qi Growth kinetics of amyloid-like fibrils derived from individual subunits of soy β-conglycinin Journal of Agricultural and Food Chemistry 59 20 2011 11270 11277 10.1021/jf202541m
37. J.C. Watts, J. Stöhr, S. Bhardwaj, H. Wille, A. Oehler, S.J. DeArmond, and et al. Protease-resistant prions selectively decrease shadoo protein PLoS Pathogens 7 11 2011 e1002382 10.1371/journal.ppat.1002382
38. Y. Xing, A. Nakamura, T. Chiba, K. Kogishi, T. Matsushita, and F. Li Transmission of mouse senile amyloidosis Laboratory Investigation 81 4 2001 493 499 10.1038/labinvest.3780257
39. W.-F. Xue, A.L. Hellewell, W.S. Gosal, S.W. Homans, E.W. Hewitt, and S.E. Radford Fibril fragmentation enhances amyloid cytotoxicity Journal of Biological Chemistry 284 49 2009 34272 34282 10.1074/jbc.M109.049809
40. T. Zako, M. Sakono, N. Hashimoto, M. Ihara, and M. Maeda Bovine insulin filaments induced by reducing disulfide bonds show a different morphology, secondary structure, and cell toxicity from intact insulin amyloid fibrils Biophysical Journal 96 8 2009 3331 3340 10.1016/j.bpj.2008.12.3957