Concentration-Dependent Effect of Nickel Ions on Amyloid Fibril Formation Kinetics of Hen Egg White Lysozyme: a Raman Spectroscopy Study
-
Abstract: Nickel, an important transition metal element, is one of the trace elements for human body and has a crucial impact on life and health. Some evidences show the excess exposure to metal ions might be associated with neurological diseases. Herein, we applied Raman spectroscopy to study the Ni(II) ion effect on kinetics of amyloid fibrillation of hen egg white lysozyme (HEWL) in thermal and acidic conditions. Using the well-known Raman indicators for protein tertiary and secondary structures, we monitored and analyzed the concentration effect of Ni(II) ions on the unfolding of tertiary structures and the transformation of secondary structures. The experimental evidence validates the accelerator role of the metal ion in the kinetics. Notably, the additional analysis of the amide I band profile, combined with thioflavin-T fluorescence assays, clearly indicates the inhibitory effect of Ni(II) ions on the formation of amyloid fibrils with organized β-sheets structures. Instead, a more significant promotion influence is affirmed on the assembly into other aggregates with disordered structures. The present results provide rich information about the specific metal-mediated protein fibrillation.
-
Key words:
- Amyloid fibrillation /
- Protein denaturation /
- Kinetics /
- Nickel ion /
- Lysozyme
-
Figure 1. Raman spectra of the native HEWL (in black) and the end-formed products in the presence of Ni(II) ions at the concentration of 1.36 mmol/L (in red) and 27.2 mmol/L (in blue) in the range of 730–790 cm−1 (a), 1300–1390 cm−1 (b), 910–1040 cm−1 (c), and 1610–1720 cm−1 (d), with thermal and acidic treatment.
Figure 2. The incubation time-dependence curves of the FWHM at 759 cm−1 (a) and the I1340/I1360 ratio (b) in the absence (in black) and presence of Ni(II) ions at the concentration of 1.36 mmol/L (in red) and 27.2 mmol/L (in blue) with thermal and acidic treatment.
Figure 3. Incubation time-dependent curves of the N-Cα-C stretching band intensity at 933 cm−1 and the peak position of amide I band, in the absence (a) and in the presence of Ni(II) ions at the concentration of 1.36 mmol/L (b) and 27.2 mmol/L (c) with thermal and acidic treatment.
Figure 4. Normalized amide I band profiles of HEWL in the denatured states in the absence (in black) and presence of Ni(II) ions at the concentrations of 1.36 mmol/L (in red) and 27.2 mmol/L (in blue) in thermal and acidic conditions.
Figure 5. (a) Fluorescence spectra of HEWL and ThT mixed solution in the native state and denaturation state after incubation for 196 h with thermal/acid (in black), thermal/acid/Ni(II) treatments ([Ni2+] of 1.36 mmol/L (in red), 27.2 mmol/L (in blue); (b) incubation time-dependence of the ThT fluorescence intensity at 477 nm.
Table I. The lag duration (T0), transition midpoint time (Tm), equilibrium duration (Te), and a half interval (ΔT) of the peak position of the amide I indicator in the HEWL amyloid fibrillation process with thermal and acidic treatment.
[Ni(II)]/(mmol/L) T0/h Tm/h Te/h ΔT/h 0 21 54±1 89 16 1.36 19 49±3 79 14 27.2 13 40±1 71 14 
下载: 导出CSV
-
[1] F. Chiti and C. M. Dobson, Annu. Rev. Biochem. 86, 27 (2017). doi: 10.1146/annurev-biochem-061516-045115 [2] R. N. Rambaran and L. C. Serpell, Prion 2, 112 (2008). doi: 10.4161/pri.2.3.7488 [3] K. A. Conway, J. D. Harper, and P. T. Lansbury, Biochemistry 39, 2552 (2000). doi: 10.1021/bi991447r [4] C. M. Dobson, Nature 426, 884 (2003). doi: 10.1038/nature02261 [5] C. Redfield and C. M. Dobson, Biochemistry 29, 7201 (1990). doi: 10.1021/bi00483a007 [6] R. Swaminathan, V. K. Ravi, S. Kumar, M. V. S. Kumar, and N. Chandra, Adv. Protein Chem. Struct. Biol. 84, 63 (2011). doi: 10.1016/B978-0-12-386483-3.00003-3 [7] H. Wang, J. Wu, R. Sternke-Hoffmann, W. Zheng, C. Morman, and J. Luo, Commun. Chem. 5, 171 (2022). doi: 10.1038/s42004-022-00786-1 [8] S. Y. Ow and D. E. Dunstan, Soft Matter 9, 9692 (2013). doi: 10.1039/c3sm51671g [9] N. A. Jamuna, A. Kamalakshan, B. R. Dandekar, A. M. Chittilappilly Devassy, J. Mondal, and S. Mandal, J. Phys. Chem. B 127, 2198 (2023). doi: 10.1021/acs.jpcb.3c00274 [10] P. Faller, C. Hureau, and O. Berthoumieu, Inorg. Chem. 52, 12193 (2013). doi: 10.1021/ic4003059 [11] J. Sheng, N. K. Olrichs, W. J. Geerts, D. V. Kaloyanova, and J. B. Helms, Sci. Rep. 9, 1 (2019). doi: 10.1038/s41598-018-37186-2 [12] M. Konar, A. Mathew, and S. Dasgupta, ACS Omega 4, 1015 (2019). doi: 10.1021/acsomega.8b03169 [13] J. A. Duce and A. I. Bush, Prog. Neurobiol. 92, 1 (2010). doi: 10.1016/j.pneurobio.2010.04.003 [14] L. M. Miller, Q. Wang, T. P. Telivala, R. J. Smith, A. Lanzirotti, and J. Miklossy, J. Struct. Biol. 155, 30 (2006). doi: 10.1016/j.jsb.2005.09.004 [15] M. A. Lovell, J. D. Robertson, W. J. Teesdale, J. L. Campbell, and W. R. Markesbery, J. Neurol. Sci. 158, 47 (1998). doi: 10.1016/S0022-510X(98)00092-6 [16] B. Ma, F. Zhang, X. Wang, and X. Zhu, Int. J. Biol. Macromol. 98, 717 (2017). doi: 10.1016/j.ijbiomac.2017.01.128 [17] R. Ceron, M. Peimbert, A. Rojo-Dominguez, and H. Najera, J. Biomol. Struct. Dyn. 41, 423 (2023). doi: 10.1080/07391102.2021.2006090 [18] S. E. Hill, T. Miti, T. Richmond, and M. Muschol, PLoS One 6, e18171 (2011). doi: 10.1371/journal.pone.0018171 [19] T. Miti, M. Mulaj, J. D. Schmit, and M. Muschol, Biomacromolecules 16, 326 (2015). doi: 10.1021/bm501521r [20] J. Wawer, M. Szocinski, M. Olszewski, R. Piatek, M. Naczk, and J. Krakowiak, Int. J. Biol. Macromol. 121, 63 (2019). doi: 10.1016/j.ijbiomac.2018.09.165 [21] B. Zambelli, V. N. Uversky, and S. Ciurli, Biochim. Biophys. Acta 1864, 1714 (2016). doi: 10.1016/j.bbapap.2016.09.008 [22] J. Zhao, X. Shi, V. Castranova, and M. Ding, J. Environ. Pathol. Toxicol. Oncol. 28, 177 (2009). doi: 10.1615/JEnvironPatholToxicolOncol.v28.i3.10 [23] G. Drochioiu, M. Manea, M. Dragusanu, M. Murariu, E. S. Dragan, B. A. Petre, G. Mezo, and M. Przybylski, Biophys. Chem 144, 9 (2009). doi: 10.3390/ijerph17030679 [24] S. J. Li, A. Nakagawa, and T. Tsukihara, Biochem. Biophys. Res. Commun. 324, 529 (2004). doi: 10.1016/j.bbrc.2004.09.078 [25] S. L. Benoit and R. J. Maier, Sci. Rep. 11, 1 (2021). doi: 10.1038/s41598-020-79139-8 [26] L. Jin, W. H. Wu, Q. Y. Li, Y. F. Zhao, and Y. M. Li, Nanoscale 3, 4746 (2011). doi: 10.1039/c1nr11029b [27] Y. Fan, H. Lan, Z. Qi, R. Liu, and C. Hu, Chemosphere 297, 134241 (2022). doi: 10.1016/j.chemosphere.2022.134241 [28] L. Xing, W. Fan, N. Chen, M. Li, X. Zhou, and S. Liu, J. Raman Spectrosc. 50, 629 (2019). doi: 10.1002/jrs.5567 [29] L. Xing, N. Chen, W. Fan, M. Li, X. Zhou, and S. Liu, Int. J. Biol. Macromol. 132, 929 (2019). doi: 10.1016/j.ijbiomac.2019.04.009 [30] A. Rygula, K. Majzner, K. M. Marzec, A. Kaczor, M. Pilarczyk, and M. Baranska, J. Raman Spectrosc. 44, 1061 (2013). doi: 10.1002/jrs.4335 [31] N. Kuhar, S. Sil, and S. Umapathy, Spectrochim. Acta Part A 258, 119712 (2021). doi: 10.1016/j.saa.2021.119712 [32] W. Fan, L. Xing, N. Chen, X. Zhou, Y. Yu, and S. Liu, J. Phys. Chem. B 123, 8057 (2019). doi: 10.1021/acs.jpcb.9b06958 [33] S. Dolui, A. Mondal, A. Roy, U. Pal, S. Das, A. Saha, and N. C. Maiti, J. Phys. Chem. B 124, 50 (2020). doi: 10.1021/acs.jpcb.9b09139 [34] M. R. R. de Planque, B. B. Bonev, J. A. A. Demmers, D. V. Greathouse, R. E. Koeppe, F. Separovic, A. Watts, and J. A. Killian, Biochemistry 42, 5341 (2003). doi: 10.1021/bi027000r [35] J. A. Sweeney and S. A. Asher, J. Phys. Chem. 94, 4784 (1990). doi: 10.1021/j100375a009 [36] I. Harada, T. Miura, and H. Takeuchi, Spectrochim. Acta Part A 42, 307 (1986). doi: 10.1016/0584-8539(86)80193-3 [37] V. Kocherbitov, J. Latynis, A. Misiunas, J. Barauskas, and G. Niaura, J. Phys. Chem. B 117, 4981 (2013). doi: 10.1021/jp4017954 [38] A. Barth, Biochim. Biophys. Acta 1767, 1073 (2007). doi: 10.1016/j.bbabio.2007.06.004 [39] S. Dolui, A. Roy, U. Pal, A. Saha, and N. C. Maiti, ACS Omega 3, 2452 (2018). doi: 10.1021/acsomega.7b01776 [40] A. Barth and C. Zscherp, Q. Rev. Biophys. 35, 369 (2002). doi: 10.1017/S0033583502003815 [41] K. Huang, N. C. Maiti, N. B. Phillips, P. R. Carey, and M. A. Weiss, Biochemistry 45, 10278 (2006). doi: 10.1021/bi060879g [42] S. Mangialardo, F. Piccirilli, A. Perucchi, P. Dore, and P. Postorino, J. Raman Spectros. 43, 692 (2012). doi: 10.1002/jrs.3097 [43] P. Ghosh and P. De, ACS Appl. Bio. Mater. 3, 9598 (2020). doi: 10.1021/acsabm.0c01021 [44] C. C. Lee, A. Nayak, A. Sethuraman, G. Belfort, and G. J. McRae, Biophys. J. 92, 3448 (2007). doi: 10.1529/biophysj.106.098608 [45] L. Nielsen, R. Khurana, A. Coats, S. Frokjaer, J. Brange, S. Vyas, V. N. Uversky, and A. L. Fink, Biochemistry 40, 6036 (2001). doi: 10.1021/bi002555c [46] A. Chaari, C. Fahy, A. Chevillot-Biraud, and M. Rholam, PLoS One 10, e0142095 (2015). doi: 10.1371/journal.pone.0142095 [47] X. Chen, X. Deng, X. Han, Y. Liang, Z. Meng, R. Liu, W. Su, H. Zhu, and T. Fu, ACS Omega 6, 3307 (2021). doi: 10.1021/acsomega.0c05788 [48] B. S. Moorthy, H. T. Ghomi, M. A. Lill, and E. M. Topp, Biophys. J. 108, 937 (2015). doi: 10.1016/j.bpj.2015.01.004 [49] S. Karmakar, N. Sarkar, and L. M. Pandey, Colloids Surf. B 174, 401 (2019). doi: 10.1016/j.colsurfb.2018.11.032 [50] H. Levine, Protein Sci. 2, 404 (1993). doi: 10.1002/pro.5560020312 [51] M. Biancalana and S. Koide, Biochim. Biophys. Acta 1804, 1405 (2010). doi: 10.1016/j.bbapap.2010.04.001 -
点击查看大图
计量
- 文章访问数: 137
- HTML全文浏览量: 69
- PDF下载量: 9
- 被引次数: 0
