Sunset Yellow Dye Induces Amorphous Aggregation in β-Lactoglobulin at Acidic pH: A Multi-Techniques Approach
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.1.1. Solution Preparation
2.1.2. Turbidity and Rayleigh Scattering Measurements
2.1.3. SY Dye-Induced Aggregation Kinetics
2.1.4. Circular Dichroism (CD)
2.1.5. Transmission Electron Microscopy (TEM)
3. Results
3.1. Turbidity
3.2. Rayleigh Light Scattering (R LS) Measurement
3.3. Kinetics of SY-Induced Aggregation
Effects of SY on BLG Aggregation
3.4. Circular Dichroism Detection
3.5. Morphology of SY-Induced Aggregate by TEM
3.6. Effect of pH on SY-Induced BLG Aggregation
3.7. Effect of NaCl Was Seen on Secondary Structure Modification of SY-Induced BLG Aggregates
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Yoshimura, Y.; Lin, Y.; Yagi, H.; Lee, Y.-H.; Kitayama, H.; Sakurai, K.; So, M.; Ogi, H.; Naiki, H.; Goto, Y. Distinguishing crystal-like amyloid fibrils and glass-like amorphous aggregates from their kinetics of formation. Proc. Natl. Acad. Sci. USA 2012, 109, 14446–14451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuo, L.; Motherwell, M.S. The impact of reactive oxygen species and genetic mitochondrial mutations in Parkinson’s disease. Gene 2013, 532, 18–23. [Google Scholar] [CrossRef] [PubMed]
- Qureshi, H.Y.; Li, T.; Macdonald, R.; Cho, C.M.; Leclerc, N.; Paudel, H.K. Interaction of 14-3-3ζ with Microtubule-Associated Protein Tau within Alzheimer’s Disease Neurofibrillary Tangles. Biochemistry 2013, 52, 6445–6455. [Google Scholar] [CrossRef] [PubMed]
- Breydo, L.; Wu, J.W.; Uversky, V.N. A-synuclein misfolding and Parkinson’s disease. Biochim. Biophys. Acta 2012, 1822, 261–285. [Google Scholar] [CrossRef] [Green Version]
- Boatz, J.C.; Whitley, M.J.; Li, M.; Gronenborn, A.M.; van der Wel, P.C.A. Cataract-associated P23T gD-crystallin retains a native-like fold in amorphous-looking aggregates formed at physiological pH. Nat. Commun. 2017, 8, 15137. [Google Scholar] [CrossRef] [Green Version]
- Demeule, B.; Gurny, R.; Arvinte, T. Where disease pathogenesis meets protein formulation: Renal deposition of immunoglobulin aggregates. Eur. J. Pharm. Biopharm. 2006, 62, 121–130. [Google Scholar] [CrossRef]
- Taboada, P.; Barbosa, S.; Castro, E.; Mosquera, V. Amyloid Fibril Formation and Other Aggregate Species Formed by Human Serum Albumin Association. J. Phys. Chem. B 2006, 110, 20733–20736. [Google Scholar] [CrossRef]
- March, D.; Bianco, V.; Franzese, G. Protein Unfolding and Aggregation near a Hydrophobic Interface. Polymers 2021, 13, 156. [Google Scholar] [CrossRef]
- Morimoto, D.; Nishizawa, R.; Walinda, E.; Takashima, S.; Sugase, K.; Shirakawa, M. Hydrogen-Deuterium Exchange Profiles of Polyubiquitin Fibrils. Polymers 2018, 10, 240. [Google Scholar] [CrossRef] [Green Version]
- Morel, B.; Varela, L.; Azuaga, A.I.; Conejero-Lara, F. Environmental Conditions Affect the Kinetics of Nucleation of Amyloid Fibrils and Determine Their Morphology. Biophys. J. 2010, 99, 3801–3810. [Google Scholar] [CrossRef] [Green Version]
- Friedman, R.; Caflisch, A. Surfactant Effects on Amyloid Aggregation Kinetics. J. Mol. Biol. 2011, 414, 303–312. [Google Scholar] [CrossRef] [Green Version]
- Al-Shabib, N.A.; Khan, J.M.; Malik, A.; Sen, P.; Ramireddy, S.; Chinnappan, S.; Alamery, S.F.; Husain, F.M.; Ahmad, A.; Choudhry, H.; et al. Allura red rapidly induces amyloid-like fibril formation in hen egg white lysozyme at physiological pH. Int. J. Biol. Macromol. 2019, 127, 297–305. [Google Scholar] [CrossRef]
- Al-Shabib, N.A.; Khan, J.M.; Malik, A.; Rehman, T.; Husain, F.M.; AlAjmi, M.F.; Alghamdi, O.H.A.; Khan, A. Quinoline yellow dye stimulates whey protein fibrillation via electrostatic and hydrophobic interaction: A biophysical study. J. Dairy Sci. 2021, 104, 5141–5151. [Google Scholar] [CrossRef]
- Al-Shabib, N.A.; Khan, J.M.; Malik, A.; Alsenaidy, A.M.; Alsenaidy, M.A.; Husain, F.M.; Shamsi, M.B.; Hidayathulla, S.; Khan, R.H. Negatively charged food additive dye “Allura Red” rapidly induces SDS-soluble amyloid fibril in beta-lactoglobulin protein. Int. J. Biol. Macromol. 2018, 107, 1706–1716. [Google Scholar] [CrossRef]
- Al-Shabib, N.A.; Khan, J.M.; Alsenaidy, M.A.; Alsenaidy, A.M.; Khan, M.S.; Husain, F.M.; Khan, M.R.; Naseem, M.; Sen, P.; Alam, P.; et al. Unveiling the stimulatory effects of tartrazine on human and bovine serum albumin fibrillogenesis: Spectroscopic and microscopic study. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2018, 191, 116–124. [Google Scholar] [CrossRef]
- Basu, A.; Kumar, G.S. Binding and Inhibitory Effect of the Dyes Amaranth and Tartrazine on Amyloid Fibrillation in Lysozyme. J. Phys. Chem. B 2017, 121, 1222–1239. [Google Scholar] [CrossRef]
- Basu, A.; Kumar, G.S. Interaction and inhibitory influence of the azo dye carmoisine on lysozyme amyloid fibrillogenesis. Mol. BioSyst. 2017, 13, 1552–1564. [Google Scholar] [CrossRef]
- Millan, S.; Satish, L.; Bera, K.; Sahoo, H. Binding and inhibitory effect of the food colorants Sunset Yellow and Ponceau 4R on amyloid fibrillation of lysozyme. New J. Chem. 2019, 43, 3956–3968. [Google Scholar] [CrossRef]
- Almeida, M.; Stephani, R.; Dos Santos, H.F.; de Oliveira, L.F.C. Spectroscopic and Theoretical Study of the “Azo”-Dye E124 in Condensate Phase: Evidence of a Dominant Hydrazo Form. J. Phys. Chem. A 2010, 114, 526–534. [Google Scholar] [CrossRef]
- Husain, A.; Sawaya, W.; Al-Omair, A.; Al-Zenki, S.; Al-Amiri, H.; Ahmed, N.; Al-Sinan, M. Estimates of dietary exposure of children to artificial food colours in Kuwait. Food Addit. Contam. 2006, 23, 245–251. [Google Scholar] [CrossRef]
- Gaunt, I.; Farmer, M.; Grasso, P.; Gangolli, S. Acute (rat and mouse) and short-term (rat) toxicity studies on sunset yellow FCF. Food Cosmet. Toxicol. 1967, 5, 747–754. [Google Scholar] [CrossRef]
- Yoshimoto, M.; Yamaguchi, M.; Hatano, S.; Watanabe, T. Configurational changes in rat liver nuclear chromatin caused by azo dyes. Food Chem. Toxicol. 1984, 22, 337–344. [Google Scholar] [CrossRef]
- Tanaka, T. Reproductive and Neurobehavioral Effects of Sunset Yellow FCF Administered To Mice in the Diet. Toxicol. Ind. Heal. 1996, 12, 69–79. [Google Scholar] [CrossRef]
- Masone, D.; Chanforan, C. Study on the interaction of artificial and natural food colorants with human serum albumin: A computational point of view. Comput. Biol. Chem. 2015, 56, 152–158. [Google Scholar] [CrossRef]
- Hinz, K.; O’Connor, P.M.; Huppertz, T.; Ross, R.; Kelly, A.L. Comparison of the principal proteins in bovine, caprine, buffalo, equine and camel milk. J. Dairy Res. 2012, 79, 185–191. [Google Scholar] [CrossRef] [Green Version]
- Liang, L.; Tajmirriahi, H.A.; Subirade, M. Interaction of β-Lactoglobulin with Resveratrol and its Biological Implications. Biomacromolecules 2008, 9, 50–56. [Google Scholar] [CrossRef]
- Flower, D.R. The lipocalin protein family: Structure and function. Biochem. J. 1996, 318, 1–14. [Google Scholar] [CrossRef]
- Sardar, S.; Pal, S.; Maity, S.; Chakraborty, J.; Halder, U.C. Amyloid fibril formation by β-lactoglobulin is inhibited by gold nanoparticles. Int. J. Biol. Macromol. 2014, 69, 137–145. [Google Scholar] [CrossRef] [PubMed]
- Kroes-Nijboer, A.; Venema, P.; van der Linden, E. Fibrillar structures in food. Food Funct. 2012, 3, 221–227. [Google Scholar] [CrossRef] [PubMed]
- Lambrecht, M.A.; Jansens, K.J.A.; Rombouts, I.; Brijs, K.; Rousseau, F.; Schymkowitz, J.; and Delcour, J.A. Conditions Governing Food Protein Amyloid FibrilFormation. Part II: Milk and Legume Proteins. Compr. Rev. Food Sci. Food Saf. 2019, 18, 1277–1291. [Google Scholar] [CrossRef] [PubMed]
- Jansens, K.J.A.; Lambrecht, M.A.; Rombouts, I.; Morera, M.M.; Brijs, K.; Rousseau, F.; Schymkowitz, J.; Delcour, J.A. Conditions Governing Food Protein Amyloid FibrilFormation—Part I: Egg and Cereal Proteins. Compr. Rev. Food Sci. Food Saf. 2019, 18, 1256–1276. [Google Scholar] [CrossRef] [Green Version]
- Collini, M.; D’alfonso, L.; Baldini, G. New insight on b-lactoglobulin bindingsites by 1-anilinonaphthalene-8-sulfonatefluorescence decay. Protein Sci. 2000, 9, 1968–1974. [Google Scholar] [CrossRef]
- Cheng, J.; Liu, J.-H.; Prasanna, G.; Jing, P. Spectrofluorimetric and molecular docking studies on the interaction of cyanidin-3- O -glucoside with whey protein, β-lactoglobulin. Int. J. Biol. Macromol. 2017, 105, 965–972. [Google Scholar] [CrossRef]
- Galvagnion, C.; Buell, A.K.; Meisl, G.; Michaels, T.; Vendruscolo, M.; Knowles, T.; Dobson, C.M. Lipid vesicles trigger α-synuclein aggregation by stimulating primary nucleation. Nat. Chem. Biol. 2015, 11, 229–234. [Google Scholar] [CrossRef] [Green Version]
- Saunders, H.M.; Hughes, V.A.; Cappai, R.; Bottomley, S.P. Conformational Behavior and Aggregation of Ataxin-3 in SDS. PLoS ONE 2013, 8, e69416. [Google Scholar] [CrossRef] [Green Version]
- Tew, D.J.; Bottomley, S.P.; Smith, D.P.; Ciccotosto, G.D.; Babon, J.; Hinds, M.G.; Masters, C.L.; Cappai, R.; Barnham, K.J. Stabilization of neurotoxic soluble beta-sheet-rich conformations of the Alzheimer’s disease amyloid-beta peptide. Biophys. J. 2008, 94, 2752–2766. [Google Scholar] [CrossRef] [Green Version]
- Al-Shabib, N.A.; Khan, J.M.; Malik, A.; Rehman, T.; AlAjmi, M.F.; Husain, F.M.; Ahmad, A.; Sen, P. Investigating the effect of food additive dye “tartrazine” on BLG fibrillation under in-vitro condition. A biophysical and molecular docking study. J. King Saud Univ. Sci. 2020, 32, 2034–2040. [Google Scholar] [CrossRef]
- Uversky, V.N.; Li, J.; Fink, A.L. Evidence for a Partially Folded Intermediate in α-Synuclein Fibril Formation. J. Biol. Chem. 2001, 276, 10737–10744. [Google Scholar] [CrossRef] [Green Version]
- Grey, M.; Linse, S.; Nilsson, H.; Brundin, P.; Sparr, E. Membrane Interaction of α-Synuclein in Different Aggregation States. J. Park. Dis. 2011, 1, 359–371. [Google Scholar] [CrossRef] [Green Version]
- Buell, A.K.; Galvagnion, C.; Gaspar, R.; Sparr, E.; Vendruscolo, M.; Knowles, T.P.J.; Linse, S.; Dobson, C.M. Solution conditions determine the relative importance of nucleation and growth processes in α-synuclein aggregation. Proc. Natl. Acad. Sci. USA 2014, 111, 7671–7676. [Google Scholar] [CrossRef] [Green Version]
- Jain, N.; Bhattacharya, M.; Mukhopadhyay, S. Kinetics of Surfactant-induced Aggregation of Lysozyme Studied by Fluorescence Spectroscopy. J. Fluoresc. 2010, 21, 615–625. [Google Scholar] [CrossRef]
- Klement, K.; Wieligmann, K.; Meinhardt, J.; Hortschansky, P.; Richter, W.; Fandrich, M. Effect of Different Salt Ions on the Propensity of Aggregation and on the Structure of Alzheimer’s Aβ(1-40) Amyloid Fibrils. J. Mol. Biol. 2007, 373, 1321–1333. [Google Scholar] [CrossRef]
- Ramis, R.; Ortega-Castro, J.; Vilanova, B.; Adrover, M.; Frau, J. Unraveling the NaCl Concentration Effect on the First Stages of α-Synuclein Aggregation. Biomacromolecules 2020, 21, 5200–5212. [Google Scholar] [CrossRef]
- Liang, Q.; Ren, X.; Qu, W.; Zhang, X.; Cheng, Y.; Ma, H. The impact of ultrasound duration on the structure of β-lactoglobulin. J. Food Eng. 2021, 292, 110365. [Google Scholar] [CrossRef]
- Mantovani, R.A.; Furtado, G.D.F.; Netto, F.M.; Cunha, R.L. Assessing the potential of whey protein fibril as emulsifier. J. Food Eng. 2018, 223, 99–108. [Google Scholar] [CrossRef]
- Topping, T.B.; Gloss, L.M. The impact of solubility and electrostatics on fibril formation by the H3 and H4 histones. Protein Sci. 2011, 20, 2060–2073. [Google Scholar] [CrossRef] [Green Version]
- Al-Shabib, N.A.; Khan, J.M.; Malik, A.; Sen, P.; Alsenaidy, M.A.; Husain, F.M.; Alsenaidy, A.M.; Khan, R.H.; Choudhry, H.; Zamzami, M.A.; et al. A quercetin-based flavanoid (rutin) reverses amyloid fibrillation in β-lactoglobulin at pH 2.0 and 358 K. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2019, 214, 40–48. [Google Scholar] [CrossRef]
- Ishtikhar, M.; Rahisuddin; Khan, M.V.; Khan, R.H. Anti-aggregation property of thymoquinone induced by copper-nanoparticles: A biophysical approach. Int. J. Biol. Macromol. 2016, 93, 1174–1182. [Google Scholar] [CrossRef]
- Mercadante, D.; Melton, L.D.; Norris, G.E.; Loo, T.S.; Williams, M.A.; Dobson, R.C.; Jameson, G.B. Bovine β-Lactoglobulin Is Dimeric Under Imitative Physiological Conditions: Dissociation Equilibrium and Rate Constants over the pH Range of 2.5–7.5. Biophys. J. 2012, 103, 303–312. [Google Scholar] [CrossRef] [Green Version]
S. No. | Conditions | Turbidity at 650 nm | Light Scattering at 650 nm |
---|---|---|---|
1 | BLG (0.2 mg/mL) + 0.0 SY | 0.0014 ± 0.0005 | 0.573 ± 0.094 |
2 | BLG (0.2 mg/mL) + 0.01 mM SY | 0.0023 ± 0.0002 | 0.589 ± 0.096 |
3 | BLG (0.2 mg/mL) + 0.02 mM SY | 0.0044 ± 0.0005 | 0.513 ± 0.016 |
4 | BLG (0.2 mg/mL) + 0.04 mM SY | 0.0219 ± 0.001 | 0.598 ± 1.456 |
5 | BLG (0.2 mg/mL) + 0.05 mM SY | 0.0323 ± 0.007 | 0.631 ± 4.945 |
6 | BLG (0.2 mg/mL) + 0.07 mM SY | 0.0779 ± 0.006 | 0.678 ± 3.478 |
7 | BLG (0.2 mg/mL) + 0.1 mM SY | 0.1454 ± 0.028 | 69.83 ± 5.820 |
8 | BLG (0.2 mg/mL) + 0.5 mM SY | 0.4065 ± 0.021 | 168.91 ± 4.323 |
9 | BLG (0.2 mg/mL) + 1.00 mM SY | 0.4179 ± 0.028 | 165.98 ± 5.455 |
10 | BLG (0.2 mg/mL) + 2.00 mM SY | 0.4219 ± 0.018 | 170.6 ± 7.104 |
11 | BLG (0.2 mg/mL) + 5.00 mM SY | 0.4138 ± 0.036 | 168.63 ± 8.027 |
12 | 1.0 mM SY | 0.0061 ± 0.0006 | 0.678 ± 0.034 |
13 | 5.0 mM SY | 0.0094 ± 0.0008 | 0.798 ± 0.086 |
S. No. | Conditions | % α-Helix | % β-Sheet |
---|---|---|---|
1 | BLG + 0.0 mM SY | 13.82 | 34.61 |
2 | BLG + 0.1 mM SY | 4.01 | 39.08 |
3 | BLG + 0.5 mM SY | 3.25 | 40.55 |
4 | BLG + 1.0 mM SY | 4.44 | 41.17 |
5 | BLG + 2.0 mM SY | 3.41 | 42.08 |
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Khan, J.M.; Malik, A.; Husain, F.M.; Hakeem, M.J.; Alhomida, A.S. Sunset Yellow Dye Induces Amorphous Aggregation in β-Lactoglobulin at Acidic pH: A Multi-Techniques Approach. Polymers 2022, 14, 395. https://0-doi-org.brum.beds.ac.uk/10.3390/polym14030395
Khan JM, Malik A, Husain FM, Hakeem MJ, Alhomida AS. Sunset Yellow Dye Induces Amorphous Aggregation in β-Lactoglobulin at Acidic pH: A Multi-Techniques Approach. Polymers. 2022; 14(3):395. https://0-doi-org.brum.beds.ac.uk/10.3390/polym14030395
Chicago/Turabian StyleKhan, Javed Masood, Ajamaluddin Malik, Fohad Mabood Husain, Mohammed J. Hakeem, and Abdullah S. Alhomida. 2022. "Sunset Yellow Dye Induces Amorphous Aggregation in β-Lactoglobulin at Acidic pH: A Multi-Techniques Approach" Polymers 14, no. 3: 395. https://0-doi-org.brum.beds.ac.uk/10.3390/polym14030395