Skip to main content
Log in

Lysozyme stability and amyloid fibrillization dependence on Hofmeister anions in acidic pH

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

We have explored an effect of Hofmeister anions, Na2SO4, NaCl, NaBr, NaNO3, NaSCN and NaClO4, on stability and amyloid fibrillization of hen egg white lysozyme at pH 2.7. The stability of the protein was analyzed by differential scanning calorimetry. The Hofmeister effect of the anions was assessed by the parameter dT trs/d[anion] (T trs, transition temperature). We show that dT trs/d[anion] correlates with anion surface tension effects and anion partition coefficients indicating direct interactions between anions and lysozyme. The kinetic of amyloid fibrillization of lysozyme was followed by Thioflavin T (ThT) fluorescence. Negative correlation between dT trs/d[anion] and the nucleation rate of fibrillization in the presence of monovalent anions indicates specific effect of anions on fibrillization rate of lysozyme. The efficiency of monovalent anions to accelerate fibrillization correlates with inverse Hofmeister series. The far-UV circular dichroism spectroscopy and atomic force microscopy findings show that conformational properties of fibrils depend on fibrillization rate. In the presence of sodium chloride, lysozyme forms typical fibrils with elongated structure and with the secondary structure of the β-sheet. On the other hand, in the presence of both chaotropic perchlorate and kosmotropic sulfate anions, the fibrils form clusters with secondary structure of β-turn. Moreover, the acceleration of fibril formation is accompanied by decreased amount of the formed fibrils as indicated by ThT fluorescence. Taken together, our study shows Hofmeister effect of monovalent anions on: (1) lysozyme stability; (2) ability to accelerate nucleation phase of lysozyme fibrillization; (3) amount, and (4) conformational properties of the formed fibrils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Booth DR, Sunde M, Bellotti V, Robinson CV, Hutchinson WL, Fraser PE, Hawkins PN, Dobson CM, Radford SE, Blake CC, Pepys MB (1997) Nature 385:787–793

    Article  CAS  PubMed  Google Scholar 

  2. Tan SY, Pepys MP (1994) Histopathology 25:403–414

    Article  CAS  PubMed  Google Scholar 

  3. Pepys MB, Hawkins PN, Booth DR, Vigushin DM, Tennent GA, Soutar AK, Totty N, Nguyen O, Blake CC, Terry CJ, Feest TG, Zalin AM, Hsuan JJ (1963) Nature 362:553–557

    Article  Google Scholar 

  4. Morozova-Roche LA, Zurdo J, Spencer A, Noppe W, Receveur V, Archer DB, Joniau M, Dobson CM (2000) J Struct Biol 130:339–351

    Article  CAS  PubMed  Google Scholar 

  5. Krebs MR, Wilkins DK, Chung EW, Pitkeathly MC, Chamberlain AK, Zurdo J, Robinson CV, Dobson CM (2000) J Mol Biol 300:541–549

    Article  CAS  PubMed  Google Scholar 

  6. Arnaudov LN, de Vries R (2005) Biophys J 8:515–526

    Article  Google Scholar 

  7. Redfield C, Dobson CM (1988) Biochemistry 27:122–136

    Article  CAS  PubMed  Google Scholar 

  8. Radford SE, Dobson CM, Evans PA (1992) Nature 358:302–307

    Article  CAS  PubMed  Google Scholar 

  9. Itzhaki LS, Evans PA, Dobson CM, Radford SE (1994) Biochemistry 33:5212–5520

    Article  CAS  PubMed  Google Scholar 

  10. Goda S, Takano K, Yamagata Y, Nagata R, Akutsu H, Maki S, Namba K, Yutani K (2000) Protein Sci 9:369–375

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Tanaka S, Oda Y, Ataka M, Onuma K, Fujiwara S, Yonezawa Y (2001) Biopolymers 59:370–379

    Article  CAS  PubMed  Google Scholar 

  12. Yonezawa Y, Tanaka S, Kubota T, Wakabayashi K, Yutani K, Fujiwara S (2002) J Mol Biol 323:237–251

    Article  CAS  PubMed  Google Scholar 

  13. Cao A, Hu D, Lai L (2004) Protein Sci 13:319–324

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Blake CCF, Koenig DF, Mair GA, Sarma R (1965) Nature 206:757–761

    Article  CAS  PubMed  Google Scholar 

  15. Kuehner DE, Engmann J, Fergg F, Wernick M, Blanch HW, Prausnitz JM (1999) J Phys Chem B 103:1368–1374

    Article  CAS  Google Scholar 

  16. Zhang Y, Cremer PS (2009) Proc Natl Acad Sci USA 106:15249–15253

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Privalov PL, Khechinashvili NN (1974) J Mol Biol 86:665–684

    Article  CAS  PubMed  Google Scholar 

  18. Bye JW, Falconer RJ (2013) Protein Sci 22:1563–1570

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Hofmeister F (1888) Arch Exp Pathol Pharmacol 24:247–260

    Article  Google Scholar 

  20. Kunz W, Henle J, Ninham BW (2004) Curr Opin Colloid Interface Sci 9:19–37

    Article  CAS  Google Scholar 

  21. Zhang Y, Cremer PS (2010) Annu Rev Phys Chem 61:63–83

    Article  CAS  PubMed  Google Scholar 

  22. Parsons DF, Boström M (2011) Lo Nostro P, Ninham BW. Phys Chem Chem Phys 13:12352–12367

    Article  CAS  PubMed  Google Scholar 

  23. Lo Nostro P, Ninham BW (2012) Chem Rev 112:2286–2322

  24. Collins KD (2012) Biophys Chem 167:43–59

    Article  PubMed  Google Scholar 

  25. Record MT Jr, Guinn E, Pegram L, Capp M (2013) Faraday Discuss 160:9–44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Salis A, Ninham BW (2014) Chem Soc Rev 43:7358–7377

    Article  CAS  PubMed  Google Scholar 

  27. Jungwirth P, Tobias DJ (2002) J Phys Chem B 106:6361–6373

    Article  CAS  Google Scholar 

  28. Jungwirth P, Tobias DJ (2006) Chem Rev 109:1259–1281

    Article  Google Scholar 

  29. Pegram LM, Record MT (2006) Proc Natl Acad Sci USA 103:14278–14281

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Pegram LM, Record MT (2007) J Phys Chem B 111:5411–5417

    Article  CAS  PubMed  Google Scholar 

  31. Pegram LM, Record MT (2008) J Phys Chem B 112:9428–9436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Collins KD (2006) Biophys Chem 119:271–281

    Article  CAS  PubMed  Google Scholar 

  33. Flores SC, Kherb J, Cremer PS (2012) J Phys Chem C 116:11408–14413

    Article  Google Scholar 

  34. Bogár F, Bartha F, Násztor Z, Fábián L, Leitgeb B, Dér A (2014) J Phys Chem B 118:8496–8504

    Article  PubMed  Google Scholar 

  35. Buell AK, Hung P, Salvatella X, Welland ME, Dobson CM, Knowles TP (2013) Biophys J 104:1116–1126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Jain S, Udgaonkar JB (2010) Biochemistry 49:7615–7624

    Article  CAS  PubMed  Google Scholar 

  37. Pedersen JS, Flink JM, Dikov D, Otzen DE (2006) Biophys J 90:4181–4194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Zurdo J, Guijarro JI, Jiménez JL, Saibil HR, Dobson CM (2001) J Mol Biol 311:325–340

    Article  CAS  PubMed  Google Scholar 

  39. Marek PJ, Patsalo V, Green DF, Raleigh DP (2012) Biochemistry 51:8478–8490

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Klement K, Wieligmann K, Meinhardt J, Hortschansky P, Richter W, Fändrich M (2007) J Mol Biol 373:1321–1333

    Article  CAS  PubMed  Google Scholar 

  41. Campioni S, Mannini B, López-Alonso JP, Shalova IN, Penco A, Mulvihill E, Laurents DV, Relini A, Chiti F (2012) J Mol Biol 424:132–149

    Article  CAS  PubMed  Google Scholar 

  42. Ruzafa D, Conejero-Lara F, Morel B (2013) Phys Chem Chem Phys 15:15508–15517

    Article  CAS  PubMed  Google Scholar 

  43. Owczarz M, Arosio P (2014) Biophys J 107:197–207

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Raman B, Chatani E, Kihara M, Ban T, Sakai M, Hasegawa K, Naiki H, Rao CM, Goto Y (2005) Biochemistry 44:1288–1299

    Article  CAS  PubMed  Google Scholar 

  45. Campos LA, Sancho J (2006) Proteins 63:581–594

    Article  CAS  PubMed  Google Scholar 

  46. Nielsen L, Khurana R, Coats A, Frokjaer S, Brange J, Vyas S, Uversky VN, Fink AL (2001) Biochemistry 40:6036–6046

    Article  CAS  PubMed  Google Scholar 

  47. Baldwin RL (1996) Biophys J 71:2056–2063

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Sedlák E, Stagg L, Wittung-Stafshede P (2008) Arch Biochem Biophys 479:69–73

    Article  PubMed  Google Scholar 

  49. LeVine H (1995) Int J Exp Clin Invest 2:1–6

    CAS  Google Scholar 

  50. Biancalana M, Koide S (2010) Biochim Biophys Acta 1804:1405–1412

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Urry DW, Long MM, Ohnishi T, Jacobs M (1974) Biochem Biophys Res Commun 61:1427–1433

    Article  CAS  PubMed  Google Scholar 

  52. Bush CA, Sarkar SK, Kopple KD (1978) Biochemistry 17:4951–4954

    Article  CAS  PubMed  Google Scholar 

  53. Privalov PL, Griko YV, Venyaminov SY, Kutyshenko VP (1986) J Mol Biol 190:487–498

    Article  CAS  PubMed  Google Scholar 

  54. Pedersen JS, Dikov D, Flink JL, Hjuler HA, Christiansen G, Otzen DE (2006) J Mol Biol 355:501–523

    Article  CAS  PubMed  Google Scholar 

  55. Omta AW, Kropman MF, Woutersen S, Bakker HJ (2003) Science 301:347–349

    Article  CAS  PubMed  Google Scholar 

  56. Batchelor JD, Olteanu A, Tripathy A, Pielak GJ (2004) J Am Chem Soc 126:1958–1961

    Article  CAS  PubMed  Google Scholar 

  57. Näslund LA, Edwards DC, Wernet P, Bergmann U, Ogasawara H, Pettersson LG, Myneni S, Nilsson A (2005) J Phys Chem A 109:5995–6002

    Article  PubMed  Google Scholar 

  58. Chen X, Yang T, Kataoka S, Cremer PS (2007) J Am Chem Soc 129:12272–12279

    Article  CAS  PubMed  Google Scholar 

  59. Guest WL, Lewis WCM (1939) Proc R Soc Lond A 170:501–513

    Article  CAS  Google Scholar 

  60. Aveyard R, Saleem SM (1976) J Chem Soc Farad Trans 72:1609–1617

    Article  CAS  Google Scholar 

  61. Holz M, Grunder R, Sacco A, Meleleo A (1993) J Chem Soc, Faraday Trans 89:1215–1222

    Article  CAS  Google Scholar 

  62. Sacco A, De Cillis FM, Holz M (1998) J Chem Soc Faraday Trans 94:2089–2092

    Article  CAS  Google Scholar 

  63. Chang TM, Dang LX (2006) Chem Rev 106:1305–1322

    Article  CAS  PubMed  Google Scholar 

  64. Funahashi J, Takano K, Ogasahara K, Yamagata Y, Yutani K (1996) J Biochem 120:1216–1223

    Article  CAS  PubMed  Google Scholar 

  65. Canet D, Last AM, Tito P, Sunde M, Spencer A, Archer DB, Redfield C, Robinson CV, Dobson CM (2002) Nat Struct Biol 9:308–315

    Article  CAS  PubMed  Google Scholar 

  66. Buell AK, Dhulesia A, Mossuto MF, Cremades N, Kumita JR, Dumoulin M, Welland ME, Knowles TP, Salvatella X, Dobson CM (2011) J Am Chem Soc 133:7737–7743

    Article  CAS  PubMed  Google Scholar 

  67. Frare E, De Laureto PP, Zurdo J, Dobson CM, Fontana A (2004) J Mol Biol 340:1153–1165

    Article  CAS  PubMed  Google Scholar 

  68. Uversky VN, Fink AL (2004) Biochim Biophys Acta 1698:131–153

    Article  CAS  PubMed  Google Scholar 

  69. Gokarn YR, Fesinmeyer RM, Saluja A, Razinkov V, Chase SF, Laue TM, Brems DN (2011) Protein Sci 20:580–587

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  70. Möller J, Grobelny S, Schulze J, Steffen A, Bieder S, Paulus M, Tolan M, Winter R (2014) Phys Chem Chem Phys 16:7423–7429

    Article  PubMed  Google Scholar 

  71. Goto Y, Calciano LJ, Fink AL (1990) Proc Natl Acad Sci USA 87:573–577

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Gjerde DT, Schmuckler G, Fritz JS (1980) J Chromatogr 187:35–45

    Article  CAS  Google Scholar 

  73. Gregor HP, Belle J, Marcus RA (1955) J Am Chem Soc 77:2713–2719

    Article  CAS  Google Scholar 

  74. Boström M, Parsons DF, Salis A, Ninham BW, Monduzzi M (2011) Langmuir 27:9504–9511

    Article  PubMed  Google Scholar 

  75. Parmar AS, Muschol M (2009) Biophys J 97:590–598

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Marcus Y (1997) Ion Properties. Marcel Dekker, New York

    Google Scholar 

Download references

Acknowledgments

This work was supported by research grants from the Slovak Grant Agency VEGA (Projects No. 1/0521/12, 2/0181/13, 2/0175/14), from Slovak Research and Development Agency (Project APVV 0526-11), ESF 26220220005, and from CELIM (316310) funded by 7FP EU (REGPOT). We also thank Ivana Petrenčáková for her editorial help in preparing the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zuzana Gažová or Erik Sedlák.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 219 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Poniková, S., Antošová, A., Demjén, E. et al. Lysozyme stability and amyloid fibrillization dependence on Hofmeister anions in acidic pH. J Biol Inorg Chem 20, 921–933 (2015). https://doi.org/10.1007/s00775-015-1276-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-015-1276-0

Keywords

Navigation