Effects of Hofmeister series anions and cations on the amyloid fibrillation of lysozyme

doi:10.3969/j.issn.1000-1565.2023.02.006

Abstract

Abstract: In this work, the effects of nine Hofmeister series anions(SO₄^2- >F^- >COO^->Cl^->Br^->NO₃^->I^->ClO₄^->SCN^-)and nine Hofmeister cations(NH₄⁺>K⁺>Na⁺>Cs⁺>Li⁺>Rb⁺>Mg²⁺>Ca²⁺>Ba²⁺)on the amyloid fibrillation of lysozyme were studied using atomic force microscopy(AFM)and Fourier transform infrared(FTIR)spectroscopy. The AFM results indicated that anions at different locations in the Hofmeister series had different impacts on the morphologies of lysozyme amyloid fibril. Under the influences of the three kosmotropic anions of SO₄^2-, F^-, COO^-, the morphology of fibril displayed branching and thickening; while under the influences of the other chaotropic anions of Cl^-, Br^-, NO₃^-, I^-, ClO₄^-, SCN^- displayed the common long and thin morphologies. This phenomenon was attributed to the difference impacts of the two different types of anions on the secondary nucleation of lysozyme amyloid fibrillation. In contrast to the effects of anions, different cations showed similar effects- DOI:10.3969/j.issn.1000-1565.2023.02.006Hofmeister序列阴阳离子对溶菌酶淀粉样纤维的影响李妍, 曹思雨,马刚(河北大学化学与材料科学学院,河北保定 071002)摘要:应用原子力显微镜(AFM)技术和傅里叶变换红外光谱(FTIR)技术对Hofmeister阴阳离子序列中9种阴离子(SO₄^2->F^->COO^->Cl^->Br^->NO₃^->I^->ClO₄^->SCN^-)和9种阳离子(NH₄⁺>K⁺>Na⁺>Cs⁺>Li⁺>Rb⁺>Mg²⁺>Ca²⁺>Ba²⁺)对溶菌酶淀粉样纤维化的影响进行了研究.通过AFM技术研究,发现Hofmeister序列中不同位置的阴离子对溶菌酶淀粉样纤维的微观形貌存在不同的影响,其中受SO₄^2-、F^-、COO^-这3种亲水阴离子影响生成的纤维呈现纤维分枝和增厚的现象,而受Cl^-、Br^-、NO₃^-、I^-、ClO₄^-、SCN^-这6种疏水阴离子影响的纤维则为常见的细长纤维.本研究将出现这种现象的原因归因于这2类阴离子对溶菌酶淀粉样纤维化二次成核过程的影响差异.与阴离子效应相反,研究中发现9种Hofmeister序列阳离子对溶菌酶淀粉样纤维的形貌影响差异不大.利用红外光谱分峰拟合技术,探究了不同阴阳离子影响下生成的淀粉样纤维中各种二级结构含量由多到少的排序与Hofmeister序列的相关性.希望本工作中的这些新发现能为人们更加深入地理解淀粉样纤维化的影响因素提供有益参考.关键词:淀粉样纤维化;溶菌酶;Hofmeister序列;傅里叶变换红外光谱;原子力显微镜中图分类号:O643 文献标志码:A 文章编号:1000-1565(2023)02-0146-10Effects of Hofmeister series anions and cations on the amyloid fibrillation of lysozymeLI Yan, CAO Siyu, MA Gang(College of Chemistry and Materials Science, Hebei University, Baoding 071002, China)Abstract: In this work, the effects of nine Hofmeister series anions(SO₄^2- >F^- >COO^->Cl^->Br^->NO₃^->I^->ClO₄^->SCN^-)and nine Hofmeister cations(NH₄⁺>K⁺>Na⁺>Cs⁺>Li⁺>Rb⁺>Mg²⁺>Ca²⁺>Ba²⁺)on the amyloid fibrillation of lysozyme were studied using atomic force microscopy(AFM)and Fourier transform infrared(FTIR)spectroscopy. The AFM results indicated that anions at different locations in the Hofmeister series had different impacts on the morphologies of lysozyme amyloid fibril. Under the influences of the three kosmotropic anions of SO₄^2-, F^-, COO^-, the morphology of fibril displayed branching and thickening; while under the influences of the other chaotropic anions of Cl^-, Br^-, NO₃^-, I^-, ClO₄^-, SCN^- displayed the common long and thin morphologies. This phenomenon was attributed to the difference impacts of the two different types of anions on the secondary nucleation of lysozyme amyloid fibrillation. In contrast to the effects of anions, different cations showed similar effects- 收稿日期:2022-12-10 基金项目:国家自然科学基金资助项目(21973024) 第一作者:李妍(1978—),女,河北邯郸人,河北大学在读博士研究生,主要从事淀粉样纤维化方向的研究.E-mail:yanli0390@sina.com 通信作者:马刚(1971—),男,北京人,河北大学教授,主要从事淀粉样纤维化方向的研究.E-mail:gangma@hbu.edu.cn第2期李妍等:Hofmeister序列阴阳离子对溶菌酶淀粉样纤维的影响河北大学学报(自然科学版) 第43卷on the morphologies of the amyloid fibrillation of lysozyme. Using FTIR curve-fitting technique, the correlation between the orders of anions and cations in the Hofmeister series and the orders of the contents of various secondary structures in lysozyme amyloid fibrils was also explored. It is hoped that the new findings in this work are beneficial for deeper understanding of different factors that affect amyloid fibrillation.

Key words: amyloid fibrillation, lysozyme, Hofmeister series, FTIR spectroscopy, AFM

CLC Number:

O643

LI Yan, CAO Siyu, MA Gang. Effects of Hofmeister series anions and cations on the amyloid fibrillation of lysozyme[J]. Journal of Hebei University(Natural Science Edition), 2023, 43(2): 146-155.

References

[1] SAWAYA M R, SAMBASHIVAN S, NELSON R, et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers[J]. Nature, 2007, 447: 453-457.10.1038/nature05695.
[2] KE P C, ZHOU R, SERPELL L C, et al. Half a century of amyloids: past, present and future[J].Chem Soc Rev, 2020,49: 5473-5509.10.1039/c9cs00199a.
[3] CHITI F, DOBSON C M. Protein misfolding, functional amyloid, and human disease[J].Annu Rev Biochem, 2006,75: 333-366.10.1146/annurev.biochem.75.101304.123901.
[4] ABELEIN A, JARVET J, BARTH A, et al. Ionic strength modulation of the free energy landscape of Aβ(40)peptide fibril formation[J].J Am Chem Soc, 2016, 138: 6893-6902.10.1021/jacs.6b04511.
[5] ABELEIN A, GRASLUND A, DANIELSSON J. Zinc as chaperone-mimicking agent for retardation of amyloid beta peptide fibril formation[J].Proc Natl Acad Sci USA, 2015, 112: 5407-5412.10.1073/pnas.1421961112.
[6] ZHANG Y, CREMER P S. Interactions between macromolecules and ions: the Hofmeister series[J].Curr Opin Chem Biol, 2006, 10: 658-663.10.1016/j.cbpa.2006.09.020.
[7] LI X, HUANG K, LIN J, et al. Hofmeister ion series and its mechanism of action on affecting the behavior of macromolecular solutes in aqueous solution[J].Prog Chem, 2014, 26: 1285-1291.10.7536/pc140436.
[8] PARA G, JAREK E, WARSZYNSKI P. The Hofmeister series effect in adsorption of cationic surfactants-theoretical description and experimental results[J].Adv Colloid Interface Sci, 2006, 122: 39-55.10.1016/j.cis.2006.06.017.
[9] ZHANG Y, CREMER P S. Chemistry of Hofmeister anions and osmolytes[J].Annu Rev Phys Chem, 2010, 61: 63-83. 10.1146/annurev.physchem.59.032607.093635
[10] KLEMENT K, WIELIGMANN K, MEINHARDT J, et al. Effect of different salt ions on the propensity of aggregation and on the structure of Alzheimer's A beta(1-40)amyloid fibrils[J].J Mol Biol, 2007, 373: 1321-1333.10.1016/j.jmb.2007.08.068'.
[11] DOGRA P, ROY S S, JOSHI A, et al. Hofmeister ions modulate the autocatalytic amyloidogenesis of an intrinsically disordered functional amyloid domain via unusual biphasic kinetics[J].J Mol Biol, 2020, 432: 6173-6186.10.1016/j.jmb.2020.10.015.
[12] YEH V, BROERING J M, ROMANYUK A, et al. The Hofmeister effect on amyloid formation using yeast prion protein[J].Protein Sci, 2010, 19: 47-56.10.1002/pro.281.
[13] CHAABAN H, VALLOORAN J J, VAN DE WEERT M, et al. Ion-mediated morphological diversity in protein amyloid systems[J].J Phys Chem Lett, 2022, 13: 3586-3593.10.1021/acs.jpclett.2c00182.
[14] ZOU Y, HAO W, LI H, et al. New insight into amyloid fibril formation of hen egg white lysozyme using a two-step temperature-dependent FTIR approach[J].J Phys Chem B, 2014, 118: 9834-9843.10.1021/jp504201k.
[15] ZOU Y, LI Y, HAO W, et al. Parallel beta-sheet fibril and antiparallel beta-sheet oligomer: New insights into amyloid formation of hen egg white lysozyme under heat and acidic condition from FTIR spectroscopy[J].J Phys Chem B, 2013, 117: 4003-4013. 10.1021/jp4003559.
[16] MISHRA R, SORGJERD K, NYSTROM S, et al. Lysozyme amyloidogenesis is accelerated by specific nicking and fragmentation but decelerated by intact protein binding and conversion[J].J Mol Biol, 2007, 366(3): 1029-1044. 10.1016/j.jmb.2006.11.084.
[17] BOOTH D R, SUNDE M, BELLOTTI V, et al. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis[J].Nature, 1997, 385: 787-93.10.1038/385787a0.
[18] NILSSON M R. Techniques to study amyloid fibril formation in vitro[J].Methods, 2004, 34: 151-160.10.1016/j.ymeth.2004.03.012.
[19] SARROUKH R, GOORMAGHTIGH E, RUYSSCHAERT J-M, et al. ATR-FTIR: A "rejuvenated" tool to investigate amyloid proteins[J].Biochim Biophys Acta Biomembr, 2013, 1828: 2328-2338.10.1016/j.bbamem.2013.04.012.
[20] STROUD J C, LIU C, TENG P K, et al. Toxic fibrillar oligomers of amyloid-β have cross-β structure[J].Proc Natl Acad Sci USA, 2012, 109: 7717-7722.10.1073/pnas.1203193109.
[21] PERALVAREZ-MARIN A, MATEOS L, ZHANG C, et al. Influence of residue 22 on the folding, aggregation profile, and toxicity of the Alzheimer's amyloid beta peptide[J].Biophys J, 2009, 97: 277-285.10.1016/j.bpj.2009.04.017.
[22] GAO Y, ZOU Y, MA Y, et al. Infrared probe technique reveals a millipede-like structure for Aβ(8-28)amyloid fibril[J].Langmuir, 2016, 32: 937-946.10.1021/acs.langmuir.5b03616.
[23] SOLEDAD CELEJ M, SARROUKH R, GOORMAGHTIGH E, et al.Toxic prefibrillar alpha-synuclein amyloid oligomers adopt a distinctive antiparallel beta-sheet structure[J].Biochem J, 2012, 443: 719-726.10.1042/bj20111924.
[24] BARTH A, ZSCHERP C. What vibrations tell us about proteins[J].Q Rev Biophys, 2002, 35: 369-430.10.1017/s0033583502003815. (