Amyloids and Amyloid-like Protein Aggregates in Foods: Challenges and
New Perspectives

Shweta      Malik; Jay   Kant   Yadav
doi:10.2174/1389203724666230104163924
Abstract

Protein misfolding and amyloid formations are associated with many neurodegenerative and systemic diseases. The discovery of Alzheimer’s disease and its association with the accumulation of Amyloid-β (Aβ) peptides in the plaques uncovered the pleiotropic nature of peptides/ proteins. As of today, more than 50 proteins/ peptides are reported to form amyloids or amyloid-like protein aggregates under different conditions, establishing that amyloid formation could be a generic property of many proteins. In principle, under certain conditions, all the proteins have this property to form amyloid-like aggregates, which can be toxic or non-toxic. The extensive research in this direction led to an understanding of the ubiquitous nature of amyloids. Mounting evidences suggest that processed foods, particularly protein-rich foods, could be a plethora of amyloids or amyloid-like protein aggregates. Many are reported to be toxic, and their consumption raises health concerns. The assimilation of dietary proteins in the human body largely depends upon their conformational states and the digestive integrity of the gastrointestinal system. Amyloids or amyloid-like protein aggregates are usually protease resistant, and their presence in foods is likely to reduce nutritional value. Several biochemical and biophysical factors, commonly evident in various food processing industries, such as high temperature, the addition of acid, etc., are likely to induce the formation of protease-resistant protein aggregates. Aging significantly alters gastrointestinal health, predisposing aged individuals to be more susceptible to protein aggregation-related diseases. Consumption of foods containing such protein aggregates will lead to a poor supply of essential amino acids and might exaggerate the amyloid-related disease etiology.
On the other hand, the gut microbiome plays a crucial role during pathological events leading to the development of Alzheimer’s and Parkinson’s diseases. The activity of gastrointestinal proteases, pH change, gut microbiome, and intestinal epithelium integrity would largely determine the outcome of consuming foods loaded with such protein aggregates. The current review outlines the recent development in this area and a new perspective for designing safe protein-rich diets for healthy nutrition.
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Graphical Abstract

[1]
Harvard Health Publishing Staff. How much protein do you need every day?, 2022. Available from: https://www.health.harvard.edu/blog/how-much-protein-do-you-need-every-day-201506188096

[2]
Wu, G. Dietary protein intake and human health. Food Funct.,  2016, 7(3), 1251-1265.
 [http://dx.doi.org/10.1039/C5FO01530H] [PMID:  26797090]

[3]
Kundu, D; Prerna, K; Chaurasia, R; Bharty, MK; Dubey, VK Advances in protein misfolding, amyloidosis and its correlation
with human diseases. 3 Biotech,  2020, 10
 [http://dx.doi.org/10.1007/s13205-020-2166-x]

[4]
Ke, P.C.; Zhou, R.; Serpell, L.C.; Riek, R.; Knowles, T.P.J.; Lashuel, H.A.; Gazit, E.; Hamley, I.W.; Davis, T.P.; Fändrich, M.; Otzen, D.E.; Chapman, M.R.; Dobson, C.M.; Eisenberg, D.S.; Mezzenga, R. Half a century of amyloids: Past, present and future. Chem. Soc. Rev.,  2020, 49(15), 5473-5509.
 [http://dx.doi.org/10.1039/C9CS00199A] [PMID:  32632432]

[5]
Kavanagh, G.M.; Clark, A.H.; Ross-Murphy, S.B. Heat-induced gelation of globular proteins: 4. Gelation kinetics of low pH β-lactoglobulin gels. Langmuir,  2000, 16(24), 9584-9594.
 [http://dx.doi.org/10.1021/la0004698]

[6]
Veerman, C.; de Schiffart, G.; Sagis, L.M.C.; van der Linden, E. Irreversible self-assembly of ovalbumin into fibrils and the resulting network rheology. Int. J. Biol. Macromol.,  2003, 33(1-3), 121-127.
 [http://dx.doi.org/10.1016/S0141-8130(03)00076-X] [PMID:  14599594]

[7]
Wei, G.; Su, Z.; Reynolds, N.P.; Arosio, P.; Hamley, I.W.; Gazit, E.; Mezzenga, R. Self-assembling peptide and protein amyloids: from structure to tailored function in nanotechnology. Chem. Soc. Rev.,  2017, 46(15), 4661-4708.
 [http://dx.doi.org/10.1039/C6CS00542J] [PMID:  28530745]

[8]
Knowles, T.P.J.; Mezzenga, R. Amyloid fibrils as building blocks for natural and artificial functional materials. Adv. Mater.,  2016, 28(31), 6546-6561.
 [http://dx.doi.org/10.1002/adma.201505961] [PMID:  27165397]

[9]
Bolisetty, S.; Mezzenga, R. Amyloid–carbon hybrid membranes for universal water purification. Nat. Nanotechnol.,  2016, 11(4), 365-371.
 [http://dx.doi.org/10.1038/nnano.2015.310] [PMID:  26809058]

[10]
Velasco, P.T.; Heffern, M.C.; Sebollela, A.; Popova, I.A.; Lacor, P.N.; Lee, K.B.; Sun, X.; Tiano, B.N.; Viola, K.L.; Eckermann, A.L.; Meade, T.J.; Klein, W.L. Synapse-binding subpopulations of Aβ oligomers sensitive to peptide assembly blockers and scFv antibodies. ACS Chem. Neurosci.,  2012, 3(11), 972-981.
 [http://dx.doi.org/10.1021/cn300122k] [PMID:  23173076]

[11]
Soeda, Y.; Yoshikawa, M.; Almeida, O.F.X.; Sumioka, A.; Maeda, S.; Osada, H.; Kondoh, Y.; Saito, A.; Miyasaka, T.; Kimura, T.; Suzuki, M.; Koyama, H.; Yoshiike, Y.; Sugimoto, H.; Ihara, Y.; Takashima, A. Toxic tau oligomer formation blocked by capping of cysteine residues with 1,2-dihydroxybenzene groups. Nat. Commun.,  2015, 6(1), 10216.
 [http://dx.doi.org/10.1038/ncomms10216] [PMID:  26671725]

[12]
Loveday, S.M. Food Proteins: Technological, nutritional, and sustainability attributes of traditional and emerging proteins. Annu. Rev. Food Sci. Technol.,  2019, 10(1), 311-339.
 [http://dx.doi.org/10.1146/annurev-food-032818-121128] [PMID:  30649962]

[13]
Phillips, G.O.; Williams, P.A. Handbook of Food Proteins, 1st ed; Elsevier: Amsterdam, 2011, pp. 1-432.
 [http://dx.doi.org/10.1533/9780857093639]

[14]
Boland, M.J.; Rae, A.N.; Vereijken, J.M.; Meuwissen, M.P.M.; Fischer, A.R.H.; van Boekel, M.A.J.S.; Rutherfurd, S.M.; Gruppen, H.; Moughan, P.J.; Hendriks, W.H. The future supply of animal-derived protein for human consumption. Trends Food Sci. Technol.,  2013, 29(1), 62-73.
 [http://dx.doi.org/10.1016/j.tifs.2012.07.002]

[15]
Wen, C.; Zhang, J.; Yao, H.; Zhou, J.; Duan, Y.; Zhang, H.; Ma, H. Advances in renewable plant-derived protein source: The structure, physicochemical properties affected by ultrasonication. Ultrason. Sonochem.,  2019, 53, 83-98.
 [http://dx.doi.org/10.1016/j.ultsonch.2018.12.036] [PMID:  30600214]

[16]
Cao, Y.; Mezzenga, R. Food protein amyloid fibrils: Origin, structure, formation, characterization, applications and health implications. Adv. Colloid Interface Sci.,  2019, 269, 334-356.
 [http://dx.doi.org/10.1016/j.cis.2019.05.002] [PMID:  31128463]

[17]
Goldschmidt, L.; Teng, P.K.; Riek, R.; Eisenberg, D. Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc. Natl. Acad. Sci. USA,  2010, 107(8), 3487-3492.
 [http://dx.doi.org/10.1073/pnas.0915166107] [PMID:  20133726]

[18]
Lambrecht, M.A.; Monge-Morera, M.; Godefroidt, T.; Vluymans, N.; Deleu, L.J.; Goos, P.; Schymkowitz, J.; Rousseau, F.; Delcour, J.A. Hydrothermal treatments cause wheat gluten-derived peptides to form amyloid-like fibrils. J. Agric. Food Chem.,  2021, 69(6), 1963-1974.
 [http://dx.doi.org/10.1021/acs.jafc.0c05868] [PMID:  33544593]

[19]
Monge-Morera, M.; Lambrecht, M.A.; Deleu, L.J.; Louros, N.N.; Rousseau, F.; Schymkowitz, J.; Delcour, J.A. Heating wheat gluten promotes the formation of amyloid-like fibrils. ACS Omega,  2021, 6(3), 1823-1833.
 [http://dx.doi.org/10.1021/acsomega.0c03670] [PMID:  33521423]

[20]
Malik, S.; De, I.; Singh, M.; Galanakis, C.M.; Alamri, A.S.; Yadav, J.K. Isolation and characterisation of milk-derived amyloid-like
protein aggregates (MAPA) from cottage cheese. Food Chem.,  2022, 373(Pt B), 131486.
 [http://dx.doi.org/10.1016/j.foodchem.2021.131486] [PMID: 34800818]

[21]
Feng, Z.; Li, Y.; Bai, Y. Elevated temperatures accelerate the formation of toxic amyloid fibrils of hen egg-white lysozyme. Vet. Med. Sci.,  2021, 7(5), 1938-1947.
 [http://dx.doi.org/10.1002/vms3.522] [PMID:  33978313]

[22]
Chatterjee, G.; Roy, D.; Kumar Khemka, V.; Chattopadhyay, M.; Chakrabarti, S. Genistein, the isoflavone in soybean, causes amyloid beta peptide accumulation in human neuroblastoma cell line: Implications in Alzheimer’s disease. Aging Dis.,  2015, 6(6), 456-465.
 [http://dx.doi.org/10.14336/AD.2015.0327] [PMID:  26618047]

[23]
Aryee, A.N.A.; Boye, J.I. Improving the Digestibility of Lentil Flours and Protein Isolate and Characterization of Their Enzymatically Prepared Hydrolysates. Int. J. Food Prop.,  2016, 19(12), 2649-2665.
 [http://dx.doi.org/10.1080/10942912.2015.1123269]

[24]
Kroghsbo, S.; Rigby, N.M.; Johnson, P.E.; Adel-Patient, K.; Bøgh, K.L.; Salt, L.J.; Mills, E.N.C.; Madsen, C.B. Assessment of the sensitizing potential of processed peanut proteins in Brown Norway rats: Roasting does not enhance allergenicity. PLoS One,  2014, 9(5), e96475.
 [http://dx.doi.org/10.1371/journal.pone.0096475] [PMID:  24805813]

[25]
Boye, J.I.; Aksay, S.; Roufik, S.; Ribéreau, S.; Mondor, M.; Farnworth, E.; Rajamohamed, S.H. Comparison of the functional properties of pea, chickpea and lentil protein concentrates processed using ultrafiltration and isoelectric precipitation techniques. Food Res. Int.,  2010, 43(2), 537-546.
 [http://dx.doi.org/10.1016/j.foodres.2009.07.021]

[26]
Aryee, A.N.A.; Agyei, D.; Udenigwe, C.C. Impact of processing on the chemistry and functionality of food proteins. In: Proteins in Food Processing. Second Edition;; Woodhead Publishing: Cambridge, 2018; pp. 27-45.
 [http://dx.doi.org/10.1016/B978-0-08-100722-8.00003-6]

[27]
Chiti, F.; Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem.,  2006, 75(1), 333-366.
 [http://dx.doi.org/10.1146/annurev.biochem.75.101304.123901] [PMID:  16756495]

[28]
Noorani, A.A.; Yamashita, H.; Gao, Y.; Islam, S.; Sun, Y.; Nakamura, T.; Enomoto, H.; Zou, K.; Michikawa, M. High temperature promotes amyloid β-protein production and γ-secretase complex formation via Hsp90. J. Biol. Chem.,  2020, 295(52), 18010-18022.
 [http://dx.doi.org/10.1074/jbc.RA120.013845] [PMID:  33067321]

[29]
Chernova, T.A.; Chernoff, Y.O.; Wilkinson, K.D. Prion-based memory of heat stress in yeast. Prion,  2017, 11(3), 151-161.
 [http://dx.doi.org/10.1080/19336896.2017.1328342] [PMID:  28521568]

[30]
Loveday, S.M.; Wang, X.L.; Rao, M.A.; Anema, S.G.; Singh, H. Effect of pH, NaCl, CaCl2 and temperature on self-assembly of β-lactoglobulin into nanofibrils: A central composite design study. J. Agric. Food Chem.,  2011, 59(15), 8467-8474.
 [http://dx.doi.org/10.1021/jf201870z] [PMID:  21726070]

[31]
Monge-Morera, M.; Lambrecht, M.A.; Deleu, L.J.; Gallardo, R.; Louros, N.N.; De Vleeschouwer, M.; Rousseau, F.; Schymkowitz, J.; Delcour, J.A. Processing induced changes in food proteins: Amyloid formation during boiling of hen egg white. Biomacromolecules,  2020, 21(6), 2218-2228.
 [http://dx.doi.org/10.1021/acs.biomac.0c00186] [PMID:  32202759]

[32]
Minteer, C.J.; Siegart, N.M.; Colelli, K.M.; Liu, X.; Linhardt, R.J.; Wang, C.; Gomez, A.V.; Reitter, J.N.; Mills, K.V. Intein-promoted cyclization of aspartic acid flanking the intein leads to atypical N-terminal cleavage. Biochemistry,  2017, 56(8), 1042-1050.
 [http://dx.doi.org/10.1021/acs.biochem.6b00894] [PMID:  28165720]

[33]
Amininasab, M.; Ebrahim-Habibi, M.B.; Ebrahim-Habibi, A.; Nemat-Gorgani, M. Amyloid fibrillation of bovine alpha lactalbumin. Biophys. J.,  2009, 96(3), 447a.
 [http://dx.doi.org/10.1016/j.bpj.2008.12.2296]

[34]
Loveday, S.M.; Su, J.; Rao, M.A.; Anema, S.G.; Singh, H. Effect of calcium on the morphology and functionality of whey protein nanofibrils. Biomacromolecules,  2011, 12(10), 3780-3788.
 [http://dx.doi.org/10.1021/bm201013b] [PMID:  21894942]

[35]
Adamcik, J.; Mezzenga, R. Amyloid-polymorphie in der energielandschaft der faltung und aggregation von proteinen. Angew. Chem.,  2018, 130(28), 8502-8515.
 [http://dx.doi.org/10.1002/ange.201713416]

[36]
Stathopulos, P.B.; Scholz, G.A.; Hwang, Y.M.; Rumfeldt, J.A.O.; Lepock, J.R.; Meiering, E.M. Sonication of proteins causes formation of aggregates that resemble amyloid. Protein Sci.,  2004, 13(11), 3017-3027.
 [http://dx.doi.org/10.1110/ps.04831804] [PMID:  15459333]

[37]
Ohhashi, Y.; Kihara, M.; Naiki, H.; Goto, Y. Ultrasonication-induced amyloid fibril formation of β2-microglobulin. J. Biol. Chem.,  2005, 280(38), 32843-32848.
 [http://dx.doi.org/10.1074/jbc.M506501200] [PMID:  16046408]

[38]
Maity, S.; Kumar, P.; Haldar, D. Sonication-induced instant amyloid-like fibril formation and organogelation by a tripeptide. Soft Matter,  2011, 7(11), 5239-5245.
 [http://dx.doi.org/10.1039/c1sm05277b]

[39]
Solomon, A.; Richey, T.; Murphy, C.L.; Weiss, D.T.; Wall, J.S.; Westermark, G.T.; Westermark, P. Amyloidogenic potential of foie gras. Proc. Natl. Acad. Sci. USA,  2007, 104(26), 10998-11001.
 [http://dx.doi.org/10.1073/pnas.0700848104] [PMID:  17578924]

[40]
Yoshida, T.; Zhang, P.; Fu, X.; Higuchi, K.; Ikeda, S.I. Slaughtered aged cattle might be one dietary source exhibiting amyloid enhancing factor activity. Amyloid,  2009, 16(1), 25-31.
 [http://dx.doi.org/10.1080/13506120802676831] [PMID:  19291511]

[41]
Lara, C.; Gourdin-Bertin, S.; Adamcik, J.; Bolisetty, S.; Mezzenga, R. Self-assembly of ovalbumin into amyloid and non-amyloid fibrils. Biomacromolecules,  2012, 13(12), 4213-4221.
 [http://dx.doi.org/10.1021/bm301481v] [PMID:  23098330]

[42]
Humblet-Hua, N.P.; Sagis, L.M.C.; van der Linden, E. Effects of flow on hen egg white lysozyme (HEWL) fibril formation: length distribution, flexibility, and kinetics. J. Agric. Food Chem.,  2008, 56(24), 11875-11882.
 [http://dx.doi.org/10.1021/jf803377n] [PMID:  19035658]

[43]
Xing, L.; Fan, W.; Chen, N.; Li, M.; Zhou, X.; Liu, S. Amyloid formation kinetics of hen egg white lysozyme under heat and acidic conditions revealed by Raman spectroscopy. J. Raman Spectrosc.,  2019, 50(5), 629-640.
 [http://dx.doi.org/10.1002/jrs.5567]

[44]
Rauscher, S.; Baud, S.; Miao, M.; Keeley, F.W.; Pomès, R. Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. Structure,  2006, 14(11), 1667-1676.
 [http://dx.doi.org/10.1016/j.str.2006.09.008] [PMID:  17098192]

[45]
Mackintosh, S.H.; Meade, S.J.; Healy, J.P.; Sutton, K.H.; Larsen, N.G.; Squires, A.M.; Gerrard, J.A. Wheat glutenin proteins assemble into a nanostructure with unusual structural features. J. Cereal Sci.,  2009, 49(1), 157-162.
 [http://dx.doi.org/10.1016/j.jcs.2008.08.003]

[46]
Mejia, C.D.; Mauer, L.J.; Hamaker, B.R. Similarities and differences in secondary structure of viscoelastic polymers of maize α-zein and wheat gluten proteins. J. Cereal Sci.,  2007, 45(3), 353-359.
 [http://dx.doi.org/10.1016/j.jcs.2006.09.009]

[47]
Mejia, C.D.; Gonzalez, D.C.; Mauer, L.J.; Campanella, O.H.; Hamaker, B.R. Increasing and stabilizing β-sheet structure of maize zein causes improvement in its rheological properties. J. Agric. Food Chem.,  2012, 60(9), 2316-2321.
 [http://dx.doi.org/10.1021/jf203073a] [PMID:  22239645]

[48]
Zhang, Y.H.; Huang, L.H.; Wei, Z.C. Effects of additional fibrils on structural and rheological properties of rice bran albumin solution and gel. Eur. Food Res. Technol.,  2014, 239(6), 971-978.
 [http://dx.doi.org/10.1007/s00217-014-2294-9]

[49]
Bolder, S.G.; Hendrickx, H.; Sagis, L.M.C.; van der Linden, E. Fibril assemblies in aqueous whey protein mixtures. J. Agric. Food Chem.,  2006, 54(12), 4229-4234.
 [http://dx.doi.org/10.1021/jf060606s] [PMID:  16756351]

[50]
Liu, J.; Dehle, F.C.; Liu, Y.; Bahraminejad, E.; Ecroyd, H.; Thorn, D.C.; Carver, J.A. The effect of milk constituents and crowding agents on amyloid fibril formation by κ-. Casein. J. Agric. Food Chem.,  2016, 64(6), 1335-1343.
 [http://dx.doi.org/10.1021/acs.jafc.5b04977] [PMID:  26807595]

[51]
Thorn, D.C.; Bahraminejad, E.; Grosas, A.B.; Koudelka, T.; Hoffmann, P.; Mata, J.P.; Devlin, G.L.; Sunde, M.; Ecroyd, H.; Holt, C.; Carver, J.A. Native disulphide-linked dimers facilitate amyloid fibril formation by bovine milk αS2-casein. Biophys. Chem.,  2021, 270, 106530.
 [http://dx.doi.org/10.1016/j.bpc.2020.106530] [PMID:  33545456]

[52]
Rizzo, G.; Baroni, L. Soy. Nutrients,  2018, 10(1), 43.
 [http://dx.doi.org/10.3390/nu10010043] [PMID:  29304010]

[53]
Lambrecht, M.A.; Jansens, K.J.A.; Rombouts, I.; Brijs, K.; Rousseau, F.; Schymkowitz, J.; Delcour, J.A. Conditions governing food protein amyloid fibril formation. Part II: Milk and legume proteins. Compr. Rev. Food Sci. Food Saf.,  2019, 18(4), 1277-1291.
 [http://dx.doi.org/10.1111/1541-4337.12465] [PMID:  33337003]

[54]
Jangir, N.; Bangrawa, S.; Yadav, T.; Malik, S.; Alamri, A.S.; Galanakis, C.M.; Singh, M.; Yadav, J.K. Isolation and characterization of amyloid-like protein aggregates from soya beans and the effect of low PH and heat treatment on their stability. J. Food Biochem.,  2022, 46(10), e14369.
 [http://dx.doi.org/10.1111/jfbc.14369] [PMID:  35945661]

[55]
Sneideris, T.; Darguzis, D.; Botyriute, A.; Grigaliunas, M.; Winter, R.; Smirnovas, V. PH-driven polymorphism of insulin amyloid-like fibrils. PLoS One,  2015, 10(8), e0136602.
 [http://dx.doi.org/10.1371/journal.pone.0136602] [PMID:  26313643]

[56]
Ohno, Y.; Seki, T.; Kojima, Y.; Miki, R.; Egawa, Y.; Hosoya, O.; Kasono, K.; Seki, T. Investigation of factors that cause insulin precipitation and/or amyloid formation in insulin formulations. J. Pharm. Health Care Sci.,  2019, 5(1), 22.
 [http://dx.doi.org/10.1186/s40780-019-0151-5] [PMID:  31687164]

[57]
Schützmann, M.P.; Hasecke, F.; Bachmann, S.; Zielinski, M.; Hänsch, S.; Schröder, G.F.; Zempel, H.; Hoyer, W. Endo-lysosomal Aβ concentration and pH trigger formation of Aβ oligomers that potently induce Tau missorting. Nat. Commun.,  2021, 12(1), 4634.
 [http://dx.doi.org/10.1038/s41467-021-24900-4] [PMID:  34330900]

[58]
Lassé, M.; Ulluwishewa, D.; Healy, J.; Thompson, D.; Miller, A.; Roy, N.; Chitcholtan, K.; Gerrard, J.A. Evaluation of protease resistance and toxicity of amyloid-like food fibrils from whey, soy, kidney bean, and egg white. Food Chem.,  2016, 192, 491-498.
 [http://dx.doi.org/10.1016/j.foodchem.2015.07.044] [PMID:  26304377]

[59]
Bateman, L.; Ye, A.; Singh, H. Re-formation of fibrils from hydrolysates of β-lactoglobulin fibrils during in vitro gastric digestion. J. Agric. Food Chem.,  2011, 59(17), 9605-9611.
 [http://dx.doi.org/10.1021/jf2020057] [PMID:  21790203]

[60]
Martinez-Guryn, K.; Leone, V.; Chang, E.B. Regional diversity of the gastrointestinal microbiome. Cell Host Microbe,  2019, 26(3), 314-324.
 [http://dx.doi.org/10.1016/j.chom.2019.08.011] [PMID:  31513770]

[61]
Martínez, J.; Sánchez, R.; Castellanos, M.; Fernández-Escamilla, A.M.; Vazquez-Cortés, S.; Fernández-Rivas, M.; Gasset, M. Fish β-parvalbumin acquires allergenic properties by amyloid assembly. Swiss Med. Wkly.,  2015, 145, w14128.
 [http://dx.doi.org/10.4414/smw.2015.14128] [PMID:  26023765]

[62]
Parker, D.M.; Bernard, R.T.F. A comparison of two diet analysis techniques for a browsing megaherbivore. J. Wildl. Manage.,  2006, 70(5), 1477-1480.
 [http://dx.doi.org/10.2193/0022-541X(2006)70[1477:ACOTDA]2.0.CO;2]

[63]
de Azevedo, M.F.; Gilson, P.R.; Gabriel, H.B.; Simões, R.F.; Angrisano, F.; Baum, J.; Crabb, B.S.; Wunderlich, G. Systematic analysis of FKBP inducible degradation domain tagging strategies for the human malaria parasite Plasmodium falciparum. PLoS One,  2012, 7(7), e40981.
 [http://dx.doi.org/10.1371/journal.pone.0040981] [PMID:  22815885]

[64]
Matsumoto, A.; Itoh, K.; Matsumoto, R. A novel carboxypeptidase B that processes native β-amyloid precursor protein is present in human hippocampus. Eur. J. Neurosci.,  2000, 12(1), 227-238.
 [http://dx.doi.org/10.1046/j.1460-9568.2000.00908.x] [PMID:  10651877]

[65]
Chaudhuri, P.; Prajapati, K.P.; Anand, B.G.; Dubey, K.; Kar, K. Amyloid cross-seeding raises new dimensions to understanding of amyloidogenesis mechanism. Ageing Res. Rev.,  2019, 56, 100937.
 [http://dx.doi.org/10.1016/j.arr.2019.100937] [PMID:  31430565]

[66]
Vaneyck, J.; Segers-Nolten, I.; Broersen, K.; Claessens, M.M.A.E. Cross-seeding of alpha-synuclein aggregation by amyloid fibrils of food proteins. J. Biol. Chem.,  2021, 296, 100358.
 [http://dx.doi.org/10.1016/j.jbc.2021.100358] [PMID:  33539920]

[67]
Ono, K.; Takahashi, R.; Ikeda, T.; Mizuguchi, M.; Hamaguchi, T.; Yamada, M. Exogenous amyloidogenic proteins function as seeds in amyloid β-protein aggregation. Biochim. Biophys. Acta Mol. Basis Dis.,  2014, 1842(4), 646-653.
 [http://dx.doi.org/10.1016/j.bbadis.2014.01.002] [PMID:  24440525]

[68]
Quigley, E.M.M. Probiotics and prebiotics and the gut microbiota. In: Probiotics and Prebiotics in Food; Nutrition and Health, 1st Edition; CRC Press: Boca Raton, Florida, 2013; pp. 258-268.
 [http://dx.doi.org/10.1201/b15561-13]

[69]
Guarner, F. Probiotics and Chronic Gastrointestinal Disease. In: Prebiotics and Probiotics Science and Technology; , 2009; pp. 949-75.
 [http://dx.doi.org/10.1007/978-0-387-79058-9_24]

[70]
Chapman, M.R.; Robinson, L.S.; Pinkner, J.S.; Roth, R.; Heuser, J.; Hammar, M.; Normark, S.; Hultgren, S.J. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science,  2002, 295(5556), 851-855.
 [http://dx.doi.org/10.1126/science.1067484] [PMID:  11823641]

[71]
O’Toole, G.; Kaplan, H.B.; Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol.,  2000, 54(1), 49-79.
 [http://dx.doi.org/10.1146/annurev.micro.54.1.49] [PMID:  11018124]

[72]
Hasegawa, S.; Goto, S.; Tsuji, H.; Okuno, T.; Asahara, T.; Nomoto, K.; Shibata, A.; Fujisawa, Y.; Minato, T.; Okamoto, A.; Ohno, K.; Hirayama, M. Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in parkinson’s disease. PLoS One,  2015, 10(11), e0142164.
 [http://dx.doi.org/10.1371/journal.pone.0142164] [PMID:  26539989]

[73]
Unger, M.M.; Spiegel, J.; Dillmann, K.U.; Grundmann, D.; Philippeit, H.; Bürmann, J.; Faßbender, K.; Schwiertz, A.; Schäfer, K.H. Short chain fatty acids and gut microbiota differ between patients with Parkinson’s disease and age-matched controls. Parkinsonism Relat. Disord.,  2016, 32, 66-72.
 [http://dx.doi.org/10.1016/j.parkreldis.2016.08.019] [PMID:  27591074]

[74]
Sharon, G.; Sampson, T.R.; Geschwind, D.H.; Mazmanian, S.K. The central nervous system and gut microbiome. Cell,  2016, 167(4), 915-932.
 [http://dx.doi.org/10.1016/j.cell.2016.10.027] [PMID:  27814521]

[75]
Chen, S.G.; Stribinskis, V.; Rane, M.J.; Demuth, D.R.; Gozal, E.; Roberts, A.M.; Jagadapillai, R.; Liu, R.; Choe, K.; Shivakumar, B.; Son, F.; Jin, S.; Kerber, R.; Adame, A.; Masliah, E.; Friedland, R.P. Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged fischer 344 rats and C, elegans. Sci. Rep.,  2016, 6(1), 34477.
 [http://dx.doi.org/10.1038/srep34477] [PMID:  27708338]

[76]
Quinti, L; Forte, AM; Kim, DY; Griciuc, A; Tanzi, RE [P4–404]: A novel drug‐screening platform in microglial cells identifies
potential ad drugs. Alzheimer’s Dement.,  2017, 13(7S_Part_31)

[77]
Skaper, SD; Facci, L; Zusso, M; Giusti, P Corrigendum: An inflammation-centric view of neurological disease: Beyond the neuron. Front. Cell. Neurosci.,  2020, 13, 578.
 [http://dx.doi.org/10.3389/fncel.2018.00072]

[78]
Nicolai, T.; Durand, D. Controlled food protein aggregation for new functionality. Curr. Opin. Colloid Interface Sci.,  2013, 18(4), 249-256.
 [http://dx.doi.org/10.1016/j.cocis.2013.03.001]

[79]
Nicolai, T. Gelation of food protein-protein mixtures. Adv. Colloid Interface Sci.,  2019, 270, 147-164.
 [http://dx.doi.org/10.1016/j.cis.2019.06.006] [PMID:  31229885]

[80]
Hu, C.; Lu, W.; Mata, A.; Nishinari, K.; Fang, Y. Ions-induced gelation of alginate: Mechanisms and applications. Int. J. Biol. Macromol.,  2021, 177, 578-588.
 [http://dx.doi.org/10.1016/j.ijbiomac.2021.02.086] [PMID:  33617905]

[81]
Sacco, P.; Pedroso-Santana, S.; Kumar, Y.; Joly, N.; Martin, P.; Bocchetta, P. Ionotropic gelation of chitosan flat structures and potential applications. Molecules,  2021, 26(3), 660.
 [http://dx.doi.org/10.3390/molecules26030660] [PMID:  33513925]

[82]
Bos, M.A.; van Vliet, T. Interfacial rheological properties of adsorbed protein layers and surfactants: A review. Adv. Colloid Interface Sci.,  2001, 91(3), 437-471.
 [http://dx.doi.org/10.1016/S0001-8686(00)00077-4] [PMID:  11511044]

[83]
Martin, A.H.; Bos, M.A.; van Vliet, T. Interfacial rheological properties and conformational aspects of soy glycinin at the air/water interface. Food Hydrocoll.,  2002, 16(1), 63-71.
 [http://dx.doi.org/10.1016/S0268-005X(01)00059-5]

[84]
Ho, T.M.; Razzaghi, A.; Ramachandran, A.; Mikkonen, K.S. Emulsion characterization via microfluidic devices: A review on interfacial tension and stability to coalescence. Adv. Colloid Interface Sci.,  2022, 299, 102541.
 [http://dx.doi.org/10.1016/j.cis.2021.102541] [PMID:  34920366]

[85]
Pinthus, E.J.; Saguy, I. Initial interfacial tension and oil uptake by deep-fat fried foods. J. Food Sci.,  1994, 59(4), 804-807.
 [http://dx.doi.org/10.1111/j.1365-2621.1994.tb08132.x]

[86]
Jung, T.; Choi, H.; Kim, J. Effects of the air layer of an idealized superhydrophobic surface on the slip length and skin-friction drag. J. Fluid Mech.,  2016, 790, R1.
 [http://dx.doi.org/10.1017/jfm.2016.36]

[87]
Fameau, A.L.; Salonen, A. Effect of particles and aggregated structures on the foam stability and aging. C. R. Phys.,  2014, 15(8-9), 748-760.
 [http://dx.doi.org/10.1016/j.crhy.2014.09.009]

[88]
Lomakina, K.; Míková, K. A study of the factors affecting the foaming properties of egg white-a review. Czech J. Food Sci.,  2006, 24(3), 110-118.
 [http://dx.doi.org/10.17221/3305-CJFS]

[89]
Blijdenstein, T.B.J.; Veerman, C.; van der Linden, E. Depletion-flocculation in oil-in-water emulsions using fibrillar protein assemblies. Langmuir,  2004, 20(12), 4881-4884.
 [http://dx.doi.org/10.1021/la0497447] [PMID:  15984245]

[90]
Mohammadian, M.; Salami, M.; Momen, S.; Alavi, F.; Emam-Djomeh, Z.; Moosavi-Movahedi, A.A. Enhancing the aqueous solubility of curcumin at acidic condition through the complexation with whey protein nanofibrils. Food Hydrocoll.,  2019, 87, 902-914.
 [http://dx.doi.org/10.1016/j.foodhyd.2018.09.001]

[91]
Vieira, M.N.N.; Forny-Germano, L.; Saraiva, L.M.; Sebollela, A.; Martinez, A.M.B.; Houzel, J.C.; De Felice, F.G.; Ferreira, S.T. Soluble oligomers from a non-disease related protein mimic Aβ-induced tau hyperphosphorylation and neurodegeneration. J. Neurochem.,  2007, 103(2), 736-748.
 [http://dx.doi.org/10.1111/j.1471-4159.2007.04809.x] [PMID:  17727639]

[92]
Yang, M.; Liu, Y.; Dai, J.; Li, L.; Ding, X.; Xu, Z.; Mori, M.; Miyahara, H.; Sawashita, J.; Higuchi, K. Apolipoprotein A-II induces acute-phase response associated AA amyloidosis in mice through conformational changes of plasma lipoprotein structure. Sci. Rep.,  2018, 8(1), 5620.
 [http://dx.doi.org/10.1038/s41598-018-23755-y] [PMID:  29618729]

[93]
Huang, J.; Yang, Y.; He, P. Serum apolipoprotein A-II and alpha-2-antiplasmin levels in midtrimester can be used as predictors of preterm delivery. J. Int. Med. Res.,  2020, 48(9)
 [http://dx.doi.org/10.1177/0300060520952280] [PMID:  32962505]

[94]
Zvintzou, E.; Xepapadaki, E.; Kalogeropoulou, C.; Filou, S.; Kypreos, K.E. Pleiotropic effects of apolipoprotein A-II on high-density lipoprotein functionality, adipose tissue metabolic activity and plasma glucose homeostasis. J. Biomed. Res.,  2020, 34(1), 14-26.

[95]
Cui, D.; Kawano, H.; Takahashi, M.; Hoshii, Y.; Setoguchi, M.; Gondo, T.; Ishihara, T. Acceleration of murine AA amyloidosis by oral administration of amyloid fibrils extracted from different species. Pathol. Int.,  2002, 52(1), 40-45.
 [http://dx.doi.org/10.1046/j.1440-1827.2002.01309.x] [PMID:  11940205]

[96]
Grodin, J.L.; Anderson, L.D., Jr; Kansagra, A. Cardiac amyloidosis. Circulation,  2022, 145(1), 18-20.
 [http://dx.doi.org/10.1161/CIRCULATIONAHA.121.057538] [PMID:  34965166]

[97]
Picken, M.M. The pathology of amyloidosis in classification: A review. Acta Haematol.,  2020, 143(4), 322-334.
 [http://dx.doi.org/10.1159/000506696] [PMID:  32392555]

[98]
Muchtar, E.; Dispenzieri, A.; Magen, H.; Grogan, M.; Mauermann, M.; McPhail, E.D.; Kurtin, P.J.; Leung, N.; Buadi, F.K.; Dingli, D.; Kumar, S.K.; Gertz, M.A. Systemic amyloidosis from A (AA) to T (ATTR): A review. J. Intern. Med.,  2021, 289(3), 268-292.
 [http://dx.doi.org/10.1111/joim.13169] [PMID:  32929754]

[99]
Brunger, A.F.; Nienhuis, H.L.A.; Bijzet, J.; Hazenberg, B.P.C. Causes of AA amyloidosis: A systematic review. Amyloid,  2020, 27(1), 1-12.
 [http://dx.doi.org/10.1080/13506129.2019.1693359] [PMID:  31766892]

[100]
Galkin, A.P. Hypothesis: AA amyloidosis is a factor causing systemic complications after coronavirus disease. Prion,  2021, 15(1), 53-55.
 [http://dx.doi.org/10.1080/19336896.2021.1910468] [PMID:  33876719]

[101]
Sjekloća, L.; Ferré-D’Amaré, A.R. Binding between G quadruplexes at the homodimer interface of the corn RNA aptamer strongly activates Thioflavin T fluorescence. Cell Chem. Biol.,  2019, 26(8), 1159-1168.e4.
 [http://dx.doi.org/10.1016/j.chembiol.2019.04.012] [PMID:  31178406]

[102]
Huo, W.; Zhu, W.; Mao, S. Effects of feeding increasing proportions of corn grain on concentration of lipopolysaccharide in the rumen fluid and the subsequent alterations in immune responses in goats. Asian-Australas. J. Anim. Sci.,  1970, 26(10), 1437-1445.
 [http://dx.doi.org/10.5713/ajas.2013.13143] [PMID:  25049727]

[103]
Shen, Y.Z.; Ding, L.Y.; Chen, L.M.; Xu, J.H.; Zhao, R.; Yang, W.Z.; Wang, H.R.; Wang, M.Z. Feeding corn grain steeped in citric acid modulates rumen fermentation and inflammatory responses in dairy goats. Animal,  2019, 13(2), 301-308.
 [http://dx.doi.org/10.1017/S1751731118001064] [PMID:  29860962]

[104]
Mohtashami, B.; Khalilvandi-Behroozyar, H.; Pirmohammadi, R.; Dehghan-Banadaky, M.; Kazemi-Bonchenari, M.; Dirandeh, E.; Ghaffari, M.H. The effect of supplemental bioactive fatty acids on growth performance and immune function of milk-fed Holstein dairy calves during heat stress. Br. J. Nutr.,  2022, 127(2), 188-201.
 [http://dx.doi.org/10.1017/S0007114521000908] [PMID:  33722330]

[105]
Ma, W.; Xiang, L.; Yu, H.L.; Yuan, L.H.; Guo, A.M.; Xiao, Y.X.; Li, L.; Xiao, R. Neuroprotection of soyabean isoflavone co-administration with folic acid against β-amyloid 1-40-induced neurotoxicity in rats. Br. J. Nutr.,  2009, 102(4), 502-505.
 [http://dx.doi.org/10.1017/S0007114509274757] [PMID:  19534845]

[106]
Xia, W.; Zhang, H.; Chen, J.; Hu, H.; Rasulov, F.; Bi, D.; Huang, X.; Pan, S. Formation of amyloid fibrils from soy protein hydrolysate: Effects of selective proteolysis on β-conglycinin. Food Res. Int.,  2017, 100(Pt 2), 268-276.
 [http://dx.doi.org/10.1016/j.foodres.2017.08.059] [PMID:  28888450]

[107]
Antonets, K.S.; Belousov, M.V.; Sulatskaya, A.I.; Belousova, M.E.; Kosolapova, A.O.; Sulatsky, M.I.; Andreeva, E.A.; Zykin, P.A.; Malovichko, Y.V.; Shtark, O.Y.; Lykholay, A.N.; Volkov, K.V.; Kuznetsova, I.M.; Turoverov, K.K.; Kochetkova, E.Y.; Bobylev, A.G.; Usachev, K.S.; Demidov, O.N.; Tikhonovich, I.A.; Nizhnikov, A.A. Accumulation of storage proteins in plant seeds is mediated by amyloid formation. PLoS Biol.,  2020, 18(7), e3000564.
 [http://dx.doi.org/10.1371/journal.pbio.3000564] [PMID:  32701952]

[108]
D’Agostino, G.; Russo, R.; Avagliano, C.; Cristiano, C.; Meli, R.; Calignano, A. Palmitoylethanolamide protects against the amyloid-β25-35-induced learning and memory impairment in mice, an experimental model of Alzheimer disease. Neuropsychopharmacology,  2012, 37(7), 1784-1792.
 [http://dx.doi.org/10.1038/npp.2012.25] [PMID:  22414817]

[109]
Santos, J.; Ventura, S. Functional amyloids germinate in plants. Trends Plant Sci.,  2021, 26(1), 7-10.
 [http://dx.doi.org/10.1016/j.tplants.2020.10.001] [PMID:  33097401]

[110]
Tang, C.H.; Zhang, Y.H.; Wen, Q.B.; Huang, Q. Formation of amyloid fibrils from kidney bean 7S globulin (Phaseolin) at pH 2.0. J. Agric. Food Chem.,  2010, 58(13), 8061-8068.
 [http://dx.doi.org/10.1021/jf101311f] [PMID:  20533826]

[111]
Liu, J.; Tang, C.H. Heat-induced fibril assembly of vicilin at pH2.0: Reaction kinetics, influence of ionic strength and protein concentration, and molecular mechanism. Food Res. Int.,  2013, 51(2), 621-632.
 [http://dx.doi.org/10.1016/j.foodres.2012.12.049]

[112]
Esmaillzadeh, A.; Azadbakht, L. Legume consumption is inversely associated with serum concentrations of adhesion molecules and inflammatory biomarkers among Iranian women. J. Nutr.,  2012, 142(2), 334-339.
 [http://dx.doi.org/10.3945/jn.111.146167] [PMID:  22190025]

[113]
Li, T.; Wang, L.; Zhang, X.; Geng, H.; Xue, W.; Chen, Z. Assembly behavior, structural characterization and rheological properties of legume proteins based amyloid fibrils. Food Hydrocoll.,  2021, 111, 106396.
 [http://dx.doi.org/10.1016/j.foodhyd.2020.106396]

[114]
Josefsson, L.; Ye, X.; Brett, C.J.; Meijer, J.; Olsson, C.; Sjögren, A.; Sundlöf, J.; Davydok, A.; Langton, M.; Emmer, Å.; Lendel, C. Potato protein nanofibrils produced from a starch industry sidestream. ACS Sustain. Chem.& Eng.,  2020, 8(2), 1058-1067.
 [http://dx.doi.org/10.1021/acssuschemeng.9b05865]

[115]
Youm, J.W.; Kim, H.; Han, J.H.L.; Jang, C.H.; Ha, H.J.; Mook-Jung, I.; Jeon, J.H.; Choi, C.Y.; Kim, Y.H.; Kim, H.S.; Joung, H. Transgenic potato expressing Aβ reduce Aβ burden in Alzheimer’s disease mouse model. FEBS Lett.,  2005, 579(30), 6737-6744.
 [http://dx.doi.org/10.1016/j.febslet.2005.11.003] [PMID:  16310782]

[116]
Kim, H.S.; Euym, J.W.; Kim, M.S.; Lee, B.C.; Mook-Jung, I.; Jeon, J.H.; Joung, H. Expression of human β-amyloid peptide in transgenic potato. Plant Sci.,  2003, 165(6), 1445-1451.
 [http://dx.doi.org/10.1016/j.plantsci.2003.07.007]

[117]
Friedland, R.P.; Tedesco, J.M.; Wilson, A.C.; Atwood, C.S.; Smith, M.A.; Perry, G.; Zagorski, M.G. Antibodies to potato virus Y bind the amyloid β peptide: Immunohistochemical and NMR studies. J. Biol. Chem.,  2008, 283(33), 22550-22556.
 [http://dx.doi.org/10.1074/jbc.M802088200] [PMID:  18505725]

[118]
O’Mahony, M.C.; Healy, A.M.; Harte, D.; Walshe, K.G.; Torgerson, P.R.; Doherty, M.L. Milk amyloid A: Correlation with cellular indices of mammary inflammation in cows with normal and raised serum amyloid A. Res. Vet. Sci.,  2006, 80(2), 155-161.
 [http://dx.doi.org/10.1016/j.rvsc.2005.05.005] [PMID:  16083930]

[119]
Kalmus, P.; Simojoki, H.; Pyörälä, S.; Taponen, S.; Holopainen, J.; Orro, T. Milk haptoglobin, milk amyloid A, and N-acetyl-β-d-glucosaminidase activity in bovines with naturally occurring clinical mastitis diagnosed with a quantitative PCR test. J. Dairy Sci.,  2013, 96(6), 3662-3670.
 [http://dx.doi.org/10.3168/jds.2012-6177] [PMID:  23548292]

[120]
Li, H.; Zhao, T.; Li, H.; Yu, J. Effect of heat treatment on the property, structure, and aggregation of skim milk proteins. Front. Nutr.,  2021, 8, 714869.
 [http://dx.doi.org/10.3389/fnut.2021.714869] [PMID:  34604276]

[121]
Goda, S.; Takano, K.; Yutani, K.; Yamagata, Y.; Nagata, R.; Akutsu, H.; Maki, S.; Namba, K. Amyloid protofilament formation of hen egg lysozyme in highly concentrated ethanol solution. Protein Sci.,  2000, 9(2), 369-375.
 [http://dx.doi.org/10.1110/ps.9.2.369] [PMID:  10716189]

[122]
Tokunaga, Y.; Sakakibara, Y.; Kamada, Y.; Watanabe, K.; Sugimoto, Y. Analysis of core region from egg white lysozyme forming amyloid fibrils. Int. J. Biol. Sci.,  2013, 9(2), 219-227.
 [http://dx.doi.org/10.7150/ijbs.5380] [PMID:  23459392]

[123]
Wang, M.; Wang, S.; Li, B.; Tian, Y.; Zhang, H.; Bai, L.; Ba, X. Synthesis of linear polyglucoside and inhibition on the amyloid fibril formation of hen egg white lysozyme. Int. J. Biol. Macromol.,  2021, 166, 771-777.
 [http://dx.doi.org/10.1016/j.ijbiomac.2020.10.234] [PMID:  33157132]

[124]
Toombs, J.; Zetterberg, H. In the blood: Biomarkers for amyloid pathology and neurodegeneration in Alzheimer’s disease. Brain Commun.,  2020, 2(1), fcaa054.
 [http://dx.doi.org/10.1093/braincomms/fcaa054] [PMID:  32954304]

[125]
Ridler, C. Blood amyloid-β successfully signals AD. Nat. Rev. Neurol.,  2018, 14(4), 195.
 [http://dx.doi.org/10.1038/nrneurol.2018.19] [PMID:  29449699]

[126]
Sotolongo-Grau, O.; Pesini, P.; Valero, S.; Lafuente, A.; Buendía, M.; Pérez-Grijalba, V.; Josè, I.S.; Ibarria, M.; Tejero, M.A.; Giménez, J.; Hernández, I.; Tárraga, L.; Ruiz, A.; Boada, M.; Sarasa, M. Association between cell-bound blood amyloid-β(1 - 40) levels and hippocampus volume. Alzheimers Res. Ther.,  2014, 6(5-8), 56.
 [http://dx.doi.org/10.1186/s13195-014-0056-3] [PMID:  25484928]

[127]
Jayawardena, N.; Kaur, M.; Nair, S.; Malmstrom, J.; Goldstone, D.; Negron, L.; Gerrard, J.; Domigan, L. Amyloid fibrils from hemoglobin. Biomolecules,  2017, 7(4), 37.
 [http://dx.doi.org/10.3390/biom7020037] [PMID:  28398221]

[128]
Ishiguro, N.; Murakami, T.; Elhelaly, A.E.; Inoshima, Y. Surveillance of amyloid deposition and bacterial contamination in chicken liver from meat market. J. Poult. Sci.,  2014, 51, 104-107.
 [http://dx.doi.org/10.2141/jpsa.0130028]

[129]
Rising, A.; Gherardi, P.; Chen, G.; Johansson, J.; Oskarsson, M.E.; Westermark, G.T.; Westermark, P. AA amyloid in human food chain is a possible biohazard. Sci. Rep.,  2021, 11(1), 21069.
 [http://dx.doi.org/10.1038/s41598-021-00588-w] [PMID:  34702933]
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DOI https://dx.doi.org/10.2174/1389203724666230104163924	Print ISSN 1389-2037
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Current Protein & Peptide Science

Amyloids and Amyloid-like Protein Aggregates in Foods: Challenges and New Perspectives

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