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The domain swapping of human cystatin C induced by synchrotron radiation

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Taube, Michal, Pietralik, Zuzanna, Szymanska, Aneta, Szutkowski, Kosma, Clemens, Daniel, Grubb, Anders, Kozak, Maciej·2019·Scientific Reports
DOI 10.1038/s41598-019-44811-1PMC PMC6561922
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Abstract

Domain swapping is observed for many proteins with flexible conformations. This phenomenon is often associated with the development of conformational diseases. Importantly, domain swapping has been observed for human cystatin C (HCC), a protein capable of forming amyloid deposits in brain arteries. In this study, the ability of short exposure to high-intensity X-ray radiation to induce domain swapping in solutions of several HCC variants (wild-type HCC and V57G, V57D, V57N, V57P, and L68V mutants) was determined. The study was conducted using time-resolved small-angle X-ray scattering (TR-SAXS) synchrotron radiation. The protein samples were also analysed using small-angle neutron scattering and NMR diffusometry. Exposing HCC to synchrotron radiation (over 50 ms) led to a gradual increase in the dimeric fraction, and for exposures longer than 150 ms, the oligomer fraction was dominant. In contrast, the non-irradiated protein solutions, apart from the V57P variant, were predominantly monomeric (e.g., V57G) or in monomer/dimer equilibrium. This work might represent the first observation of domain swapping induced by high-intensity X-rays.

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  1. [1]Žerovnik E Mechanisms of amyloid fibril formation–focus on domain-swapping FEBS J. 2011 278 2263 2282 10.1111/j.1742-4658.2011.08149.x 21535473 · DOI
  2. [2]Knaus KJ Crystal structure of the human prion protein reveals a mechanism for oligomerization Nat. Struct. Mol. Biol. 2001 8 770 774 10.1038/nsb0901-770 11524679 · DOI
  3. [3]Zhang M Zheng J Nussinov R Ma B Oncogenic Mutations Differentially Affect Bax Monomer, Dimer, and Oligomeric Pore Formation in the Membrane Sci. Rep. 2016 6 33340 10.1038/srep33340 27630059 PMC5024136 · DOI
  4. [4]Janowski R Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping Nat. Struct. Mol. Biol. 2001 8 316 320 10.1038/86188 11276250 · DOI
  5. [5]Janowski R Abrahamson M Grubb A Jaskolski M Domain swapping in N-truncated human cystatin C J. Mol. Biol. 2004 341 151 160 10.1016/j.jmb.2004.06.013 15312769 · DOI
  6. [6]Janowski R Kozak M Abrahamson M Grubb A Jaskolski M 3D domain‐swapped human cystatin C with amyloidlike intermolecular beta‐sheets Proteins: Struct. Funct., Bioinf. 2005 61 570 578 10.1002/prot.20633 16170782 · DOI
  7. [7]Bennett MJ Sawaya MR Eisenberg D Deposition diseases and 3D domain swapping Structure 2006 14 811 824 10.1016/j.str.2006.03.011 16698543 · DOI
  8. [8]Wahlbom M Fibrillogenic oligomers of human cystatin C are formed by propagated domain swapping J. Biol. Chem. 2007 282 18318 18326 10.1074/jbc.M611368200 17470433 · DOI
  9. [9]Östner G Stabilization, Characterization, and Selective Removal of Cystatin C Amyloid Oligomers J. Biol. Chem. 2013 288 16438 16450 10.1074/jbc.M113.469593 23629649 PMC3675580 · DOI
  10. [10]Perlenfein TJ Mehlhoff JD Murphy RM Insights into the mechanism of cystatin C oligomer and amyloid formation and its interaction with β-amyloid J. Biol. Chem. 2017 292 11485 11498 10.1074/jbc.M117.786558 28487367 PMC5500812 · DOI
  11. [11]Bennett M Schlunegger M Eisenberg D 3D domain swapping: A mechanism for oligomer assembly Protein Sci. 1995 4 2455 2468 10.1002/pro.5560041202 8580836 PMC2143041 · DOI
  12. [12]Szymańska A Governing the monomer-dimer ratio of human cystatin C by single amino acid substitution in the hinge region Acta Biochim. Pol. 2009 56 455 463 10.18388/abp.2009_2480 19636441 · DOI
  13. [13]Garman EF Weik M Macromolecular crystallography radiation damage research: what’s new? J. Synchrotron Radiat. 2011 18 313 317 10.1107/S0909049511013859 21525638 PMC3083910 · DOI
  14. [14]Garman EF Radiation damage in macromolecular crystallography: what is it and why should we care? Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010 66 339 351 10.1107/S0907444910008656 20382986 PMC2852297 · DOI
  15. [15]Duke E Johnson L Macromolecular crystallography at synchrotron radiation sources: current status and future developments Proc. R. Soc. A 2010 466 3421 3452 10.1098/rspa.2010.0448 · DOI
  16. [16]Hasegawa K Development of a dose-limiting data collection strategy for serial synchrotron rotation crystallography J. Synchrotron Radiat. 2017 24 29 41 10.1107/S1600577516016362 28009544 PMC5182019 · DOI
  17. [17]Weik M Specific chemical and structural damage to proteins produced by synchrotron radiation Proc. Natl. Acad. Sci. USA 2000 97 623 628 10.1073/pnas.97.2.623 10639129 PMC15380 · DOI
  18. [18]Meents A Gutmann S Wagner A Schulze-Briese C Origin and temperature dependence of radiation damage in biological samples at cryogenic temperatures Proc. Natl. Acad. Sci. USA 2010 107 1094 1099 10.1073/pnas.0905481107 20080548 PMC2798883 · DOI
  19. [19]Murray J Garman E Investigation of possible free-radical scavengers and metrics for radiation damage in protein cryocrystallography J. Synchrotron Radiat. 2002 9 347 354 10.1107/S0909049502014632 12409621 · DOI
  20. [20]Ravelli RB Garman EF Radiation damage in macromolecular cryocrystallography Curr. Opin. Struct. Biol. 2006 16 624 629 10.1016/j.sbi.2006.08.001 16938450 · DOI
  21. [21]Brooks-Bartlett JC Development of tools to automate quantitative analysis of radiation damage in SAXS experiments J. Synchrotron Radiat. 2017 24 63 72 10.1107/S1600577516015083 28009547 PMC5182020 · DOI
  22. [22]Putnam CD Hammel M Hura GL Tainer JA X-ray solution scattering (SAXS) combined with crystallography and computation: Defining accurate macromolecular structures, conformations and assemblies in solution Q. Rev. Biophys. 2007 40 191 285 10.1017/S0033583507004635 18078545 · DOI · Paper page
  23. [23]Jeffries CM Graewert MA Svergun DI Blanchet CE Limiting radiation damage for high-brilliance biological solution scattering: practical experience at the EMBL P12 beamline PETRAIII J. Synchrotron Radiat. 2015 22 273 279 10.1107/S1600577515000375 25723929 · DOI
  24. [24]Meisburger SP Breaking the Radiation Damage Limit with Cryo-SAXS Biophys. J. 2013 104 227 236 10.1016/j.bpj.2012.11.3817 23332075 PMC3540250 · DOI
  25. [25]Abrahamson M Dalbøge H Olafsson I Carlsen S Grubb A Efficient production of native, biologically active human cystatin C by Escherichia coli FEBS Lett. 1988 236 14 18 10.1016/0014-5793(88)80276-X 3042461 · DOI
  26. [26]Neu HC Heppel LA The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts J. Biol. Chem. 1965 240 3685 3692 4284300
  27. [27]Petoukhov MV New developments in the ATSAS program package for small-angle scattering data analysis J. Appl. Crystallogr. 2012 45 342 350 10.1107/S0021889812007662 25484842 PMC4233345 · DOI
  28. [28]Konarev PV Volkov VV Sokolova AV Koch MH Svergun DI PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 2003 36 1277 1282 10.1107/S0021889803012779 · DOI
  29. [29]Guinier A La diffraction des rayons X aux tres petits angles; application a l’etude de phenomenes ultramicroscopiques Ann. Phys. (Paris, Fr.) 1939 12 161 237 10.1051/anphys/193911120161 · DOI
  30. [30]Kołodziejczyk R Crystal structure of human cystatin C stabilized against amyloid formation FEBS J. 2010 277 1726 1737 10.1111/j.1742-4658.2010.07596.x 20175878 · DOI
  31. [31]Blobel J Bernad P Svergun D Tauler R Pons M Low-Resolution Structures of Transient Protein−Protein Complexes Using Small-Angle X-ray Scattering J. Am. Chem. Soc. 2009 131 4378 4386 10.1021/ja808490b 19275229 · DOI
  32. [32]Jaumot J Gargallo R de Juan A Tauler R A graphical user-friendly interface for MCR-ALS: a new tool for multivariate curve resolution in MATLAB Chemom. Intell. Lab. Syst. 2005 76 101 110 10.1016/j.chemolab.2004.12.007 · DOI
  33. [33]David G Pérez J Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline J. Appl. Crystallogr. 2009 42 892 900 10.1107/S0021889809029288 · DOI
  34. [35]Chrabąszczewska M Cyclic trimer of human cystatin C, an amyloidogenic protein-molecular dynamics and experimental studies J. Appl. Phys. 2018 123 174701 10.1063/1.5023807 · DOI
  35. [36]Vogtt K A new time-of-flight small-angle scattering instrument at the Helmholtz-Zentrum Berlin: V16/VSANS J. Appl. Crystallogr. 2014 47 237 244 10.1107/S1600576713030227 · DOI
  36. [37]Arnold O Mantid—data analysis and visualization package for neutron scattering and μ SR experiments Nucl. Instrum. Methods Phys. Res., Sect. A 2014 764 156 166 10.1016/j.nima.2014.07.029 · DOI
  37. [38]Stejskal EO Tanner JE Spin Diffusion Measurements: Spin Echoes in the Presence of a Time‐Dependent Field Gradient J. Chem. Phys. 1965 42 288 292 10.1063/1.1695690 · DOI
  38. [39]Szymańska A Influence of point mutations on the stability, dimerization, and oligomerization of human cystatin C and its L68Q variant Front. Mol. Neurosci. 2012 5 82 10.3389/fnmol.2012.00082 22866027 PMC3406405 · DOI
  39. [40]Herranz-Trillo F Structural Analysis of Multi-component Amyloid Systems by Chemometric SAXS Data Decomposition Structure 2017 25 5 15 10.1016/j.str.2016.10.013 27889205 · DOI
  40. [41]Weljie AM Yamniuk AP Yoshino H Izumi Y Vogel H Protein conformational changes studied by diffusion NMR spectroscopy: application to helix-loop-helix calcium binding proteins J. Protein Sci. 2003 12 228 236 10.1110/ps.0226203 PMC2312419 12538886 · DOI
  41. [42]Grubb A Löfberg H Barrett AJ The disulphide bridges of human cystatin C (γ-trace) and chicken cystatin FEBS Lett. 1984 170 370 374 10.1016/0014-5793(84)81346-0 · DOI
  42. [43]Mascarenhas NM Gosavi S Understanding Protein Domain-Swapping in the Cystatin-Monellin Family of Proteins Biophys. J. 2017 112 168a 10.1016/j.bpj.2016.11.925 PMC7127520 27867057 · DOI
  43. [44]Orlikowska M Structural characterization of V57D and V57P mutants of human cystatin C, an amyloidogenic protein Acta Crystallogr., Sect. D: Biol. Crystallogr. 2013 69 577 586 10.1107/S0907444912051657 23519666 PMC3976269 · DOI
  44. [45]Kozak M Expression of a selenomethionyl derivative and preliminary crystallographic studies of human cystatin C Acta Crystallogr., Sect. D: Struct. Biol. 1999 55 1939 1942 10.1107/S090744499901121X PMC7161602 10531502 · DOI
  45. [46]Xie J-B Photoinduced fibrils formation of chicken egg white lysozyme under native conditions Proteins: Struct., Funct., Bioinf. 2012 80 2501 2513 10.1002/prot.24132 22730151 · DOI
  46. [47]Zarei H Bahreinipour M Eskandari K Mousavi Zarandi S-A Ardestani SK Spectroscopic study of gamma irradiation effect on the molecular structure of bovine serum albumin Vacuum 2017 136 91 96 10.1016/j.vacuum.2016.11.029 · DOI
  47. [48]Hopkins JB Thorne RE Quantifying radiation damage in biomolecular small-angle X-ray scattering J. Appl. Crystallogr. 2016 49 880 890 10.1107/S1600576716005136 27275138 PMC4886981 · DOI
  48. [49]Burchard W Schmidt M Stockmayer W Information on Polydispersity and Branching from Combined Quasi-Elastic and Intergrated Scattering Macromolecules 1980 13 1265 1272 10.1021/ma60077a045 · DOI

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Sorted by citations

Authors
Taube, M., Pietralik, Z., Szymanska, A., Szutkowski, K., Clemens, D., Grubb, A., & Kozak, M.
Affiliations
  • Adam Mickiewicz University in Poznań (PL)
  • Helmholtz-Zentrum Berlin für Materialien und Energie (DE)
  • Lund University (SE)
Corresponding author
Kozak, Maciej
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2019-06-12
Volume
9
Issue
1
Pages
8548-8548
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-019-44811-1
PMC
PMC6561922
OpenAlex
W2953286694
Cited by
20
References
0
Citations by year
2026: 2 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 2 · 2020: 5 · 2019: 4 · 2018: 1
FWCI
0.99
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HZB Repository (Helmholtz-Zentrum Berlin für Materialien und Energie GmbH (HZB)) (submittedVersion, other-oa)
  • Desy Publications Database (Deutsches Elektronen-Synchrotron DESY) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Lund University Publications (Lund University) (submittedVersion)
  • DESY Publication Database (PUBDB) (Deutsches Elektronen-Synchrotron)
Funders
Narodowe Centrum Nauki (DEC-2012/06/M/ST4/00036)
Topics
  • Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords
domain swapping, synchrotron radiation, protein oligomerization, amyloid deposition, protein dimerization, radiation-induced protein damage
MeSH terms
Protein Domains, Humans, X-Rays, Synchrotrons, Neutron Diffraction, Scattering, Small Angle, Cystatin C

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