β-Lactoglobulin nanofibrils: The long and the short of it

International Dairy Journal

Volumn 67, Issue , 2017, Pages 35-45

  Loveday, Simon M ^a   Anema, Skelte G ^b   Singh, Harjinder ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b FONTERRA RESEARCH CENTRE   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

NANOFIBERS;

BETA-LACTOGLOBULIN; FIBRIL FORMATION; FOOD INGREDIENTS; LOW IONIC STRENGTH; MICRO-STRUCTURAL; RESEARCH EFFORTS; RHEOLOGICAL PROPERTY; SELF ASSEMBLED STRUCTURES;

IONIC STRENGTH;

EID: 85006701477     PISSN: 09586946     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.idairyj.2016.09.011     Document Type: Review

References (91)

1. Adamcik, J., Jung, J.M., Flakowski, J., De los Rios, P., Dietler, G., Mezzenga, R., Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nature Nanotechnology 5 (2010), 423–428.
2. Adamcik, J., Mezzenga, R., Adjustable twisting periodic pitch of amyloid fibrils. Soft Matter 7 (2011), 5437–5443.
3. Adamcik, J., Mezzenga, R., Proteins fibrils from a polymer physics perspective. Macromolecules 45 (2012), 1137–1150.
4. Akkermans, C., van der Goot, A.J., Venema, P., van der Linden, E., Boom, R.M., Formation of fibrillar whey protein aggregates: Influence of heat and shear treatment, and resulting rheology. Food Hydrocolloids 22 (2008), 1315–1325.
5. Akkermans, C., van der Goot, A.J., Venema, P., van der Linden, E., Boom, R.M., Properties of protein fibrils in whey protein isolate solutions: Microstructure, flow behaviour and gelation. International Dairy Journal 18 (2008), 1034–1042.
6. Akkermans, C., Venema, P., Rogers, S., van der Goot, A., Boom, R., van der Linden, E., Shear pulses nucleate fibril aggregation. Food Biophysics 1 (2006), 144–150.
7. Akkermans, C., Venema, P., van der Goot, A.J., Boom, R.M., van der Linden, E., Enzyme-induced formation of β-lactoglobulin fibrils by AspN endoproteinase. Food Biophysics 3 (2008), 390–394.
8. Akkermans, C., Venema, P., van der Goot, A.J., Gruppen, H., Bakx, E.J., Boom, R.M., et al. Peptides are building blocks of heat-induced fibrillar protein aggregates of β-lactoglobulin formed at pH 2. Biomacromolecules 9 (2008), 1474–1479.
9. Alting, A.C., de Jongh, H.H.J., Visschers, R.W., Simons, J.W.F.A., Physical and chemical interactions in cold gelation of food proteins. Journal of Agricultural and Food Chemistry 50 (2002), 4682–4689.
10. Arnaudov, L.N., de Vries, R., Strong impact of ionic strength on the kinetics of fibrilar aggregation of bovine β-lactoglobulin. Biomacromolecules 7 (2006), 3490–3498.
11. Arnaudov, L.N., de Vries, R., Ippel, H., van Mierlo, C.P.M., Multiple steps during the formation of β-lactoglobulin fibrils. Biomacromolecules 4 (2003), 1614–1622.
12. Arosio, P., Beeg, M., Nicoud, L., Morbidelli, M., Time evolution of amyloid fibril length distribution described by a population balance model. Chemical Engineering Science 78 (2012), 21–32.
13. Aymard, P., Nicolai, T., Durand, D., Clark, A., Static and dynamic scattering of β-lactoglobulin aggregates formed after heat-induced denaturation at pH 2. Macromolecules 32 (1999), 2542–2552.
14. Bateman, L., Ye, A., Singh, H., In vitro digestion of β-lactoglobulin fibrils formed by heat treatment at low pH. Journal of Agricultural and Food Chemistry 58 (2010), 9800–9808.
15. Bateman, L., Ye, A., Singh, H., Re-formation of fibrils from hydrolysates of β-lactoglobulin fibrils during in vitro gastric digestion. Journal of Agricultural and Food Chemistry 59 (2011), 9605–9611.
16. Bekard, I.B., Asimakis, P., Bertolini, J., Dunstan, D.E., The effects of shear flow on protein structure and function. Biopolymers 95 (2011), 733–745.
17. Berson, J.F., Theos, A.C., Harper, D.C., Tenza, D., Raposo, G., Marks, M.S., Proprotein convertase cleavage liberates a fibrillogenic fragment of a resident glycoprotein to initiate melanosome biogenesis. Journal of Cell Biology 161 (2003), 521–533.
18. Blijdenstein, T.B.J., Veerman, C., van der Linden, E., Depletion-flocculation in oil-in-water emulsions using fibrillar protein assemblies. Langmuir 20 (2004), 4881–4884.
19. Bolder, S.G., Hendrickx, H., Sagis, L.M.C., van der Linden, E., Fibril assemblies in aqueous whey protein mixtures. Journal of Agricultural and Food Chemistry 54 (2006), 4229–4234.
20. Bolder, S.G., Sagis, L.M.C., Venema, P., van der Linden, E., Effect of stirring and seeding on whey protein fibril formation. Journal of Agricultural and Food Chemistry 55 (2007), 5661–5669.
21. Bolisetty, S., Boddupalli, C.S., Handschin, S., Chaitanya, K., Adamcik, J., Saito, Y., et al. Amyloid fibrils enhance transport of metal nanoparticles in living cells and induced cytotoxicity. Biomacromolecules 15 (2014), 2793–2799.
22. Bolisetty, S., Harnau, L., Jung, J.M., Mezzenga, R., Gelation, phase behavior, and dynamics of β-lactoglobulin amyloid fibrils at varying concentrations and ionic strengths. Biomacromolecules 13 (2012), 3241–3252.
23. Bolisetty, S., Mezzenga, R., Amyloid-carbon hybrid membranes for universal water purification. Nature Nanotechnology 11 (2016), 365–371.
24. Dave, A.C., Loveday, S.M., Anema, S.G., Jameson, G.B., Singh, H., Glycation as a tool to probe the mechanism of β-lactoglobulin nanofibril self-assembly. Journal of Agricultural and Food Chemistry 62 (2014), 3269–3278.
25. Dave, A.C., Loveday, S.M., Anema, S.G., Jameson, G.B., Singh, H., Modulating β-lactoglobulin nanofibril self-assembly at pH 2 using glycerol and sorbitol. Biomacromolecules 15 (2014), 95–103.
26. Dave, A.C., Loveday, S.M., Anema, S.G., Loo, T.S., Norris, G.E., Jameson, G.B., et al. β-Lactoglobulin self-assembly: Structural changes in early stages and disulfide bonding in fibrils. Journal of Agricultural and Food Chemistry 61 (2013), 7817–7828.
27. Dueholm, M.S., Albertsen, M., Otzen, D., Nielsen, P.H., Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS One, 7, 2012, e51274.
28. Dunstan, D.E., Hamilton-Brown, P., Asimakis, P., Ducker, W., Bertolini, J., Shear-induced structure and mechanics of β-lactoglobulin amyloid fibrils. Soft Matter 5 (2009), 5020–5028.
29. Edwards, P.J.B., Jameson, G.B., Structure and stability of whey proteins. Thompson, A., Boland, M., Singh, H., (eds.) Milk proteins: From expression to food, 2nd ed., 2014, Academic Press, San Diego, CA, USA, 202–242.
30. nd ed., 2011, Academic Press, San Diego, CA, USA, 873–878.
31. Goers, J., Permyakov, S.E., Permyakov, E.A., Uversky, V.N., Fink, A.L., Conformational prerequisites for α-lactalbumin fibrillation. Biochemistry 41 (2002), 12546–12551.
32. Goldschmidt, L., Teng, P.K., Riek, R., Eisenberg, D., Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proceedings of the National Academy of Sciences of the United States of America 107 (2010), 3487–3492.
33. Gosal, W.S., Clark, A.H., Ross-Murphy, S.B., Fibrillar β-lactoglobulin gels: Part 1. Fibril formation and structure. Biomacromolecules 5 (2004), 2408–2419.
34. Gosal, W.S., Clark, A.H., Ross-Murphy, S.B., Fibrillar β-lactoglobulin gels: Part 2. Dynamic mechanical characterization of heat-set systems. Biomacromolecules 5 (2004), 2420–2429.
35. Hamada, D., Dobson, C.M., A kinetic study of β-lactoglobulin amyloid fibril formation promoted by urea. Protein Science 11 (2002), 2417–2426.
36. Hamada, D., Tanaka, T., Tartaglia, G.G., Pawar, A., Vendruscolo, M., Kawamura, M., et al. Competition between folding, native-state dimerisation and amyloid aggregation in β-lactoglobulin. Journal of Molecular Biology 386 (2009), 878–890.
37. Hettiarachchi, C.A., β-Lactoglobulin nanofibrils and their interactions with pectins. PhD thesis, 2013, University of Auckland, Auckland, New Zealand Retrieved 25 July 2016 from http://hdl.handle.net/2292/21095.
38. Hettiarachchi, C.A., Melton, L.D., Gerrard, J.A., Loveday, S.M., Formation of β-lactoglobulin nanofibrils by microwave heating gives a structural assembly different to conventional heating. Biomacromolecules 13 (2012), 2868–2880.
39. Hettiarachchi, C.A., Melton, L.D., McGillivray, D.J., Loveday, S.M., Gerrard, J.A., Williams, M.A.K., β-Lactoglobulin nanofibrils can be assembled into nanotapes via site-specific interactions with pectin. Soft Matter 12 (2016), 756–768.
40. Hettiarachchi, C.A., Melton, L.D., Williams, M.A.K., McGillivray, D.J., Gerrard, J.A., Loveday, S.M., Morphology of complexes formed between β-lactoglobulin nanofibrils and pectins is influenced by the pH and structural characteristics of the pectins. Biopolymers 105 (2016), 819–831.
41. Hill, E.K., Krebs, B., Goodall, D.G., Howlett, G.J., Dunstan, D.E., Shear flow induces amyloid fibril formation. Biomacromolecules 7 (2006), 10–13.
42. Hoare, D.G., Koshland, D.E. Jr., A procedure for the selective modification of carboxyl groups in proteins. Journal of the American Chemical Society 88 (1966), 2057–2058.
43. Iconomidou, V.A., Hamodrakas, S.J., Natural protective amyloids. Current Protein and Peptide Science 9 (2008), 291–309.
44. Ipsen, R., Otte, J., Self-assembly of partially hydrolysed α-lactalbumin. Biotechnology Advances 25 (2007), 602–605.
45. Jones, O.G., Handschin, S., Adamcik, J., Harnau, L., Bolisetty, S., Mezzenga, R., Complexation of β-lactoglobulin fibrils and sulfated polysaccharides. Biomacromolecules 12 (2011), 3056–3065.
46. Jordens, S., Ruhs, P.A., Sieber, C., Isa, L., Fischer, P., Mezzenga, R., Bridging the gap between the nanostructural organization and macroscopic interfacial rheology of amyloid fibrils at liquid interfaces. Langmuir 30 (2014), 10090–10097.
47. Jung, J.M., Gunes, D.Z., Mezzenga, R., Interfacial activity and interfacial shear rheology of native β-lactoglobulin monomers and their heat-induced fibers. Langmuir 26 (2010), 15366–15375.
48. Kavanagh, G.M., Clark, A.H., Ross-Murphy, S.B., Heat-induced gelation of globular proteins: Part 3. Molecular studies on low pH β-lactoglobulin gels. International Journal of Biological Macromolecules 28 (2000), 41–50.
49. 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 16 (2000), 9584–9594.
50. Krebs, M.R.H., Morozova-Roche, L.A., Daniel, K., Robinson, C.V., Dobson, C.M., Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein Science 13 (2004), 1933–1938.
51. Kroes-Nijboer, A., Venema, P., Bouman, J., van der Linden, E., Influence of protein hydrolysis on the growth kinetics of β-lg fibrils. Langmuir 27 (2011), 5753–5761.
52. Lara, C., Adamcik, J., Jordens, S., Mezzenga, R., General self-assembly mechanism converting hydrolyzed globular proteins into giant multistranded amyloid ribbons. Biomacromolecules 12 (2011), 1868–1875.
53. Lassé, M., Ulluwishewa, D., Healy, J., Thompson, D., Miller, A., Roy, N., et al. Evaluation of protease resistance and toxicity of amyloid-like food fibrils from whey, soy, kidney bean, and egg white. Food Chemistry 192 (2015), 491–498.
54. Lawrence, L., Moore, W.J., Kinetics of the hydrolysis of simple glycine peptides. Journal of the American Chemical Society 73 (1951), 3973–3977.
55. Loveday, S.M., β-lactoglobulin heat denaturation: A critical assessment of kinetic modelling. International Dairy Journal 52 (2016), 92–100.
56. Loveday, S.M., Rao, M.A., Creamer, L.K., Singh, H., Factors affecting rheological characteristics of fibril gels: The case of β-lactoglobulin and α-lactalbumin. Journal of Food Science 74 (2009), R47–R55.
57. 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 12 (2011), 3780–3788.
58. Loveday, S.M., Su, J., Rao, M.A., Anema, S.G., Singh, H., Whey protein nanofibrils: Kinetic, rheological and morphological effects of group IA and IIA cations. International Dairy Journal 26 (2012), 133–140.
59. Loveday, S.M., Su, J., Rao, M.A., Anema, S.G., Singh, H., Whey protein nanofibrils: The environment-morphology-functionality relationship in lyophilization, rehydration, and seeding. Journal of Agricultural and Food Chemistry 60 (2012), 5229–5236.
60. 2. International Dairy Journal 20 (2010), 571–579.
61. 2 and temperature on self-assembly of β-lactoglobulin into nanofibrils: A central composite design study. Journal of Agricultural and Food Chemistry 59 (2011), 8467–8474.
62. Loveday, S.M., Wang, X.L., Rao, M.A., Anema, S.G., Singh, H., β-Lactoglobulin nanofibrils: Effect of temperature on fibril formation kinetics, fibril morphology and the rheological properties of fibril dispersions. Food Hydrocolloids 27 (2012), 242–249.
63. Mercadante, D., Melton, L.D., Norris, G.E., Loo, T.S., Williams, M.A.K., Dobson, R.C.J., et al. Bovine β-lactoglobulin is dimeric under imitative physiological conditions: Dissociation equilibrium and rate constants over the pH range of 2.5–7.5. Biophysical Journal 103 (2012), 303–312.
64. Mezzenga, R., Fischer, P., The self-assembly, aggregation and phase transitions of food protein systems in one, two and three dimensions. Reports on Progress in Physics, 76, 2013, 046601.
65. Mishra, R., Sörgjerd, K., Nyström, S., Nordigården, A., Yu, Y.-C., Hammarström, P., Lysozyme amyloidogenesis is accelerated by specific nicking and fragmentation but decelerated by intact protein binding and conversion. Journal of Molecular Biology 366 (2007), 1029–1044.
66. Mudgal, P., Daubert, C.R., Foegeding, E.A., Cold-set thickening mechanism of β-lactoglobulin at low pH: Concentration effects. Food Hydrocolloids 23 (2009), 1762–1770.
67. 2 on cold-set thickening mechanism of β-lactoglobulin at low pH. International Dairy Journal 21 (2011), 319–326.
68. Munialo, C.D., de Jongh, H.H.J., Broersen, K., van der Linden, E., Martin, A.H., Modulation of the gelation efficiency of fibrillar and spherical aggregates by means of thiolation. Journal of Agricultural and Food Chemistry 61 (2013), 11628–11635.
69. Murray, B., Rosenthal, J., Zheng, Z., Isaacson, D., Zhu, Y., Belfort, G., Cosolute effects on amyloid aggregation in a nondiffusion limited regime: Intrinsic osmolyte properties and the volume exclusion principle. Langmuir 31 (2015), 4246–4254.
70. Nilsson, M.R., Techniques to study amyloid fibril formation in vitro. Methods 34 (2004), 151–160.
71. Oboroceanu, D., Wang, L., Brodkorb, A., Magner, E., Auty, M.A.E., Characterization of β-lactoglobulin fibrillar assembly using atomic force microscopy, polyacrylamide gel electrophoresis, and in situ Fourier transform infrared spectroscopy. Journal of Agricultural and Food Chemistry 58 (2010), 3667–3673.
72. Oboroceanu, D., Wang, L., Magner, E., Auty, M.A.E., Fibrillization of whey proteins improves foaming capacity and foam stability at low protein concentrations. Journal of Food Engineering 121 (2014), 102–111.
73. Otzen, D., Functional amyloid: Turning swords into plowshares. Prion 4 (2010), 256–264.
74. Peng, J., Kroes-Nijboer, A., Venema, P., van der Linden, E., Stability of colloidal dispersions in the presence of protein fibrils. Soft Matter 12 (2016), 3514–3526.
75. Peram, M.R., Loveday, S.M., Ye, A., Singh, H., In vitro gastric digestion of heat-induced aggregates of β-lactoglobulin. Journal of Dairy Science 96 (2013), 63–74.
76. Rasmussen, P., Barbiroli, A., Bonomi, F., Faoro, F., Ferranti, P., Iriti, M., et al. Formation of structured polymers upon controlled denaturation of β-lactoglobulin with different chaotropes. Biopolymers 86 (2007), 57–72.
77. Sasso, L., Suei, S., Domigan, L., Healy, J., Nock, V., Williams, M.A.K., et al. Versatile multi-functionalization of protein nanofibrils for biosensor applications. Nanoscale 6 (2014), 1629–1634.
78. Schleeger, M., Van den Akker, C.C., Deckert-Gaudig, T., Deckert, V., Velikov, K.P., Koenderink, G., et al. Amyloids: From molecular structure to mechanical properties. Polymer 54 (2013), 2473–2488.
79. Schultz, J., Cleavage at aspartic acid. Methods in Enzymology 11 (1967), 255–263.
80. Serfert, Y., Lamprecht, C., Tan, C.P., Keppler, J.K., Appel, E., Rossier-Miranda, F.J., et al. Characterisation and use of β-lactoglobulin fibrils for microencapsulation of lipophilic ingredients and oxidative stability thereof. Journal of Food Engineering 143 (2014), 53–61.
81. Sipe, J.D., Cohen, A.S., Review: History of the amyloid fibril. Journal of Structural Biology 130 (2000), 88–98.
82. Sukenik, S., Harries, D., Insights into the disparate action of osmolytes and macromolecular crowders on amyloid formation. Prion 6 (2012), 26–31.
83. Sukenik, S., Politi, R., Ziserman, L., Danino, D., Friedler, A., Harries, D., Crowding alone cannot account for cosolute effect on amyloid aggregation. PLoS One, 6, 2011, e15608.
84. Swaisgood, H.E., Chemistry of milk protein. Developments in dairy chemistry, Vol. 1, 1982, Applied Science Publishers, London, UK, 1–59.
85. Thorn, D.C., Ecroyd, H., Carver, J.A., Holt, C., Casein structures in the context of unfolded proteins. International Dairy Journal 46 (2015), 2–11.
86. Usov, I., Adamcik, J., Mezzenga, R., Polymorphism in bovine serum albumin fibrils: Morphology and statistical analysis. Faraday Discussions 166 (2013), 151–162.
87. Usov, I., Mezzenga, R., Correlation between nanomechanics and polymorphic conformations in amyloid fibrils. ACS Nano 8 (2014), 11035–11041.
88. Veerman, C., Method for improving the functional properties of a globular protein, protein thus prepared, use thereof and products containing the protein. Patent PCT/EP03/13678 (US2006/0204454A1), 2006.
89. 2+-induced cold gelation process for β-lactoglobulin. Journal of Agricultural and Food Chemistry 51 (2003), 3880–3885.
90. Veerman, C., Sagis, L.M.C., Heck, J., van der Linden, E., Mesostructure of fibrillar bovine serum albumin gels. International Journal of Biological Macromolecules 31 (2003), 139–146.
91. Wu, X., Nishinari, K., Gao, Z., Zhao, M., Zhang, K., Fang, Y., et al. Gelation of β-lactoglobulin and its fibrils in the presence of transglutaminase. Food Hydrocolloids 52 (2016), 942–951.