Silver ions as em marker of congo red ligation sites in amyloids and amyloid-like aggregates

• Authors: Janina Rybarska , Leszek Konieczny , Anna Jagusiak , Katarzyna Chłopaś , Grzegorz Zemanek , Barbara Piekarska , Barbara Stopa , Piotr Piwowar , Olga Woźnicka , Irena Roterman
• Languages of publication: EN

Abstracts

EN

Congo red (CR) is a known selective amyloid ligand. The focus of our work is identification (by EM imaging) of dye binding sites and their distribution in amyloids and amyloid-like aggregates formed in vitro. In order to produce the required contrast, CR has been indirectly combined with metal via including Titan yellow (TY) by intercalation which exhibits a relatively strong affinity for silver ions. The resulting combined ligand retains its ability to bind to proteins (which it owes to CR) and can easily be detected in EM studies thanks to TY. We have found, however, that in protein aggregates where unfolding is stabilized by aggregation and therefore is irreversible, TY alone may serve as both, the ligand and the metal carrier. The formation of ordered structures in amyloids was studied using IgG light chains with amyloidogenic properties, converted into amyloids by shaking. The resulting EM images were subjected to interpretation on the basis of the authors' earlier research on the CR/light chain complexation process. Our results indicate that dimeric light chains, which are the subject of our study, produce amyloids or amyloid-like complexes with chain-like properties and strong helicalization tendencies. Cursory analysis suggests that the edge polypeptide loops belonging to unstable light chains form intermolecular bridges which promote creation of loose gel deposits, or are otherwise engaged in the swapping processes leading to higher structural ordering.

Keywords

EN

Congo red; Titan yellow; amyloids; supramolecular dyes; metal markers; light chain; amyloid-like aggregates; edge loop

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2017
• Volume: 64
• Issue: 1
• Pages: 161-169

Dates

published

2017

received

2016-07-17

revised

2016-08-16

accepted

2016-09-05

(unknown)

2016-12-19

Contributors

author

Janina Rybarska

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Leszek Konieczny

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Anna Jagusiak

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Katarzyna Chłopaś

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Grzegorz Zemanek

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Barbara Piekarska

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Barbara Stopa

• Chair of Medical Biochemistry, Medical College - Jagiellonian University, Kraków, Poland

author

Piotr Piwowar

• Department of Measurements and Electronics, AGH University of Science and Technology, Kraków, Poland

author

Olga Woźnicka

• Department of Cell Biology Imaging, Faculty of Biology, Earth Sciences, Jagiellonian University, Kraków, Poland

author

Irena Roterman

• Department of Bioinformatics and Telemedicine, Medical College - Jagiellonian University, Kraków, Poland

References

• Banach M, Konieczny L, Roterman I (2014) The fuzzy oil drop model, based on hydrophobicity density distribution, generalizes the influence of water environment on protein structure and function. J Theor Biol 359: 6-17. doi: 10.1016/j.jtbi.2014.05.007.
• Barrow CJ, Yasuda A, Kenny PT, Zagorski MG (1992) Solution conformations and aggregational properties of synthetic amyloid beta-peptides of Alzheimer's disease. Analysis of circular dichroism spectra. J Mol Biol 225: 1075-1093.
• Bennett MJ, Schlunegger MP, Eisenberg D (1995) 3D domain swapping: a mechanism for oligomer assembly. Protein Sci 4: 2455-24568. doi: 10.1002/pro.5560041202.
• Bross P, Corydon TJ, Andresen BS, Jørgensen MM, Bolund L, Gregersen N (1999) Protein misfolding and degradation in genetic diseases Hum Mutat 14: 186-198. doi: 10.1002/(SICI)1098-1004(1999)14:3<186::AID-HUMU2>3.0.CO;2-J.
• Chłopaś K, Jagusiak A, Konieczny L, Piekarska B, Roterman I, Rybarska J, Stopa B, Zemanem G, Bielańska E, Piwowar P, Sadlik K (2015) The use of Titan yellow dye as a metal ion binding marker for studies on the formation of specific complexes by supramolecular Congo red. Bio-Algorithms and Med-Systems 11: 9-18. doi: 10.1515/bams-2015-0001
• Churukian CJ (2000) Improved Puchtler's Congo red method for demonstrating amyloid. J Histotechnology 23: 139-141.
• Cohen FE. (1999) Protein misfolding and prion diseases. J Mol Biol 293: 313-320.
• Colon W, Kelly JW (1992) Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro. Biochemistry 31: 8654-8660.
• Dealwis C, Wall J (2004) Towards understanding the structure-function relationship of human amyloid disease. Curr Drug Targets 5: 159-171.
• Demeule B, Gurny R, Arvinte T (2007) Detection and characterization of protein aggregates by fluorescence microscopy. Int J Pharm 329: 37-45.
• Elhaddaoui A, Pigorsch E, Delacourte A, Turrell S (1995) Competition of Congo red and Thioflavin S binding to amyloid sites in Alzheimer's diseased tissue. Biospectroscopy 1: 351-356.
• Ewert AS, Honegger A, Plückthun A (2004) Stability improvement of antibodies for extracellular and intracellular applications: CDR grafting to stable frameworks and structure-based framework engineering. Methods 34: 184-199. doi: 10.1016/j.ymeth.2004.04.007.
• Fan ZC, Shan L, Guddat LW, He XM, Gray WR, Raison RL, Edmundson AB (1992) Three-dimensional structure of an Fv from a human IgM immunoglobulin. J Mol Biol 228: 188-207.
• Fink AL (1998) Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold Des 3: R9-R23.
• Frid P, Anisimov SV, Popovic N (2007) Congo red and protein aggregation in neurodegenerative diseases. Brain Res Rev 53: 135-160. doi: 10.1016/j.brainresrev.2006.08.001.
• Heegaard NH, Sen JW, Nissen MH (2000) Congophilicity (Congo red affinity) of different beta2-microglobulin conformations characterized by dye affinity capillary electrophoresis. J Chromatogr A 894: 319-327.
• Helms LR, Wetzel R (1996) Specificity of abnormal assembly in immunoglobulin light chain deposition disease and amyloidosis J Mol Biol 257: 77-86.
• Howie AJ, Brewer DB (2009) Optical properties of amyloid stained by Congo red: history and mechanisms. Micron 40: 285-301. doi: 10.1016/j.micron.2008.10.002.
• Hurle MR, Helms LR, Li L, Chan W, Wetzel R (1994) A role for destabilizing amino acid replacements in light-chain amyloidosis. Proc Natl Acad Sci U S A 91: 5446-5450.
• Iconomidou VA, Chryssikos GD, Gionis V, Hoenger A, Hamodrakas SJ (2003) FT-Raman spectroscopy as diagnostic tool of Congo red binding to amyloids. Biopolymers 72: 185-192. doi: 10.1002/bip.10344.
• Inouye H, Kirschner DA (2000) A beta fibrillogenesis: kinetic parameters for fibril formation from congo red binding. J Struct Biol 130: 123-129.
• Jagusiak A, Konieczny L, Krol M, Marszalek P, Piekarska B, Piwowar P, Roterman I, Rybarska J, Stopa B, Zemanek G (2014) Intramolecular immunological signal hypothesis revived - structural background of signalling revealed by using Congo Red as a specific tool. Mini Rev Med Chem 14: 1104–1113.
• Jiang X, Smith CS, Petrassi HM, Hammarström P, White JT, Sacchettini JC, Kelly JW (2001) An engineered transthyretin monomer that is nonamyloidogenic, unless it is partially denatured Biochemistry 40: 11442-11452.
• Jin LW, Claborn KA, Kurimoto M, Geday MA, Maezawa I, Sohraby F, Estrada M, Kaminksy W, Kahr B (2003) Imaging linear birefringence and dichroism in cerebral amyloid pathologies. Proc Natl Acad Sci U S A 100: 15294-15298. doi: 10.1073/pnas.2534647100.
• Kelly JW (1997) Amyloid fibril formation and protein misassembly: a structural quest for insights into amyloid and prion diseases. Structure 5: 595-600.
• Khurana R, Uversky VN, Nielsen L, Fink AL (2001) Is Congo red an amyloid-specific dye? J Biol Chem 276: 22715-22721.
• Khurana R, Gillespie JR, Talapatra A, Minert LJ, Ionescu-Zanetti C, Millett I, Fink AL (2001) Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates. Biochemistry 40: 3525-3535.
• Kim YS, Randolph TW, Manning MC, Stevens FJ, Carpenter JF (2003) Congo red populates partially unfolded states of an amyloidogenic protein to enhance aggregation and amyloid fibril formation J Biol Chem 278: 10842-10850.
• King HGC, Pruden G (1967) The component of commercial titan yellow most reactive towards magnesium: Its isolation and use in determining magnesium in silicate minerals. Analyst 92: 83-90. doi: 10.1074/jbc.M212540200
• Klunk WE, Jacob RF, Mason RP (1999) Quantifying amyloid beta-peptide (Abeta) aggregation using the Congo red-Abeta (CR-abeta) spectrophotometric assay. Anal Biochem 266: 66-76.
• Król M, Roterman I, Piekarska B, Konieczny L, Rybarska J, Stopa B, Spólnik P, Szneler E (2005) An approach to understand the complexation of supramolecular dye Congo red with immunoglobulin L chain lambda. Biopolymers 77: 155-162. doi: 10.1002/bip.20197.
• Lakdawala AS, Morgan DM, Liotta DC, Lynn DG, Snyder JP (2002) Dynamics and fluidity of amyloid fibrils: a model of fibrous protein aggregates. J Am Chem Soc 124: 15150-15151.
• Lendel C, Bolognesi B, Wahlström A, Dobson CM, Gräslund A (2010) Detergent-like interaction of Congo red with the amyloid beta peptide. Biochemistry 49: 1358-1360. doi: 10.1021/bi902005t.
• Liu Y, Hart PJ, Schlunegger MP, Eisenberg D (1998) The crystal structure of a 3D domain-swapped dimer of RNase A at a 2.1-A resolution. Proc Natl Acad Sci U S A 95: 3437-3442.
• Lu JX, Qiang W, Yau WM, Schwieters CD, Meredith SC, Tycko R (2013) Molecular structure of β-amyloid fibrils in Alzheimer's disease brain tissue. Cell 154: 1257-1268. doi: 10.1016/j.cell.2013.08.035.
• Lührs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Döbeli H, Schubert D, Riek R (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci U S A 102: 17342-17347. doi: 10.1073/pnas.0506723102.
• Maji SK, Wang L, Greenwald J, Riek R (2009) Structure-activity relationship of amyloid fibrils. FEBS Lett 583: 2610-2617. doi: 10.1016/j.febslet.2009.07.003.
• Mizobata T, Kawata Y (1994) The guanidine-induced conformational changes of the chaperonin GroEL from Escherichia coli. Evidence for the existence of an unfolding intermediate state. Biochim Biophys Acta 1209: 83-88.
• Nagradova NK (2002) Three-dimensional domain swapping in homooligomeric proteins and its functional significance. Biochemistry (Moscow) 67: 839-849.
• Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16: 260-265.
• Pedersen MØ, Mikkelsen K, Behrens MA, Pedersen JS, Enghild JJ, Skrydstrup T, Malmendal A, Nielsen NC (2010) NMR reveals two-step association of Congo Red to amyloid β in low-molecular-weight aggregates. J Phys Chem B 114: 16003-16010.
• Pellarin R, Schuetz P, Guarnera E, Caflisch AJ (2010) Amyloid fibril polymorphism is under kinetic control. J Am Chem Soc 132: 14960-14970. doi: 10.1021/ja106044u.
• Petkova AT, Yau WM, Tycko R (2006) Experimental constraints on quaternary structure in Alzheimer's beta-amyloid fibrils. Biochemistry 45: 498-512. doi: 10.1021/bi051952q.
• Picken MM (2001) The changing concepts of amyloid. Arch Pathol Lab Med 125: 38-43. doi: 10.1043/0003-9985(2001)125<0038:TCCOA>2.0.CO;2.
• Piekarska B, Konieczny L, Rybarska J, Stopa B, Zemanek G, Szneler E, Król M, Nowak M, Roterman I (2001) Heat-induced formation of a specific binding site for self-assembled Congo Red in the V domain of immunoglobulin L chain lambda. Biopolymers 59: 446-456. doi: 10.1002/1097-0282(200111)59:6<446::AID-BIP1049>3.0.CO;2-X.
• Pollack SJ, Sadler II, Hawtin SR, Tailor VJ, Shearman MS (1995) Sulfonated dyes attenuate the toxic effects of beta-amyloid in a structure-specific fashion. Neurosci Lett 197: 211-214.
• del Pozo YL, Ortiz E, Sánchez R, Sánchez-López R, Güereca L, Murphy CL, Allen A, Wall JS, Fernández-Velasco DA, Solomon A, Becerril B (2008) Influence of the germline sequence on the thermodynamic stability and fibrillogenicity of human lambda 6 light chains. Proteins 72: 684-692. doi: 10.1002/prot.21934.
• Pratim Bose P, Chatterjee U, Xie L, Johansson J, Göthelid E, Arvidsson PI (2010) Effects of Congo red on aβ(1-40) fibril formation process and morphology. ACS Chem Neurosci 1: 315-324. doi: 10.1021/cn900041x.
• Qin Z, Hu D, Zhu M, Fink AL (2007) Structural characterization of the partially folded intermediates of an immunoglobulin light chain leading to amyloid fibrillation and amorphous aggregation. Biochemistry 46: 3521-3531. doi: 10.1021/bi061716v.
• Quintas A, Vaz DC, Cardoso I, Saraiva MJ, Brito RM (2001) Tetramer dissociation and monomer partial unfolding precedes protofibril formation in amyloidogenic transthyretin variants. J Biol Chem 276: 27207-27213. doi: 10.1074/jbc.M101024200.
• Roterman I, Rybarska J, Konieczny L, Skowronek M, Stopa B, Piekarska B, Bakalarski G (1998) Congo red bound to α-1-proteinase inhibitor as a model of supramolecular ligand and protein complex. Computers Chem 22: 61-70.
• Schormann N, Murrell JR, Liepnieks JJ, Benson MD (1995) Tertiary structure of an amyloid immunoglobulin light chain protein: a proposed model for amyloid fibril formation. Proc Natl Acad Sci U S A 92: 9490-9494.
• Serpell LC (2000) Alzheimer's amyloid fibrils: structure and assembly. Biochim Biophys Acta 1502: 16-30.
• Sinha N, Tsai CJ, Nussinov R (2001) A proposed structural model for amyloid fibril elongation: domain swapping forms an interdigitating beta-structure polymer. Protein Eng 14: 93-103.
• Skowronek M, Stopa B, Konieczny L, Rybarska J, Szneler E, Bakalarski G, Roterman I (1998) Self- assembly of Congo red - A theoretical and experimental approach to identify its supramolecular organization in water and salt solution. Biolpolymers 46: 267–281.
• Spólnik P, Konieczny L, Piekarska B, Rybarska J, Stopa B, Zemanek G, Król M, Roterman I (2004) Instability of monoclonal myeloma protein may be identified as susceptibility to penetration and binding by newly synthesized Congo red derivatives. Biochimie 86: 397-401.
• Stopa B, Górny M, Konieczny L, Piekarska B, Rybarska J, Skowronek M, Roterman I (1998) Supramolecular ligands: monomer structure and protein ligation capability. Biochimie 80: 963-968.
• Stopa B, Piekarska B, Konieczny L, Rybarska J, Spólnik P, Zemanek G, Roterman I, Król M (2003) The structure and protein binding of amyloid-specific dye reagents. Acta Biochim Pol 50: 1213-1227.
• Teng PK, Anderson NJ, Goldschmidt L, Sawaya MR, Sambashivan S, Eisenberg D (2012) Ribonuclease A suggests how proteins self-chaperone against amyloid fiber formation. Protein Sci 21: 26-37. doi: 10.1002/pro.754.
• Turnell WG, Finch JT (1992) Binding of the dye congo red to the amyloid protein pig insulin reveals a novel homology amongst amyloid-forming peptide sequences. J Mol Biol 227: 1205-1223.
• Tycko R (2004) Progress towards a molecular-level structural understanding of amyloid fibrils. Curr Opin Struct Biol 14: 96-103. doi: 10.1016/j.sbi.2003.12.002.
• Wall J, Schell M, Murphy C, Hrncic RR, Stevens FJ, Solomon A (1999) Thermodynamic instability of human lambda 6 light chains: correlation with fibrillogenicity. Biochemistry 38: 14101-14108.
• Wood SJ, Maleeff B, Hart T, Wetzel R (1996) Physical, morphological and functional differences between ph 5.8 and 7.4 aggregates of the Alzheimer's amyloid peptide Abeta. J Mol Biol 256: 870-877. doi: 10.1006/jmbi.1996.0133.
• Woodcock S, Henrissat B, Sugiyama J (1995) Docking of congo red to the surface of crystalline cellulose using molecular mechanics. Biopolymers 36: 201-210. doi: 10.1002/bip.360360208.
• Wu C, Wang Z, Lei H, Zhang W, Duan Y (2007) Dual binding modes of Congo red to amyloid protofibril surface observed in molecular dynamics simulations. J Am Chem Soc 129: 1225-1232. doi: 10.1021/ja0662772.
• Wu C, Scott J, Shea JE (2012) Binding of Congo red to amyloid protofibrils of the Alzheimer Aβ(9-40) peptide probed by molecular dynamics simulations. Biophys J 103: 550-557. doi: 10.1016/j.bpj.2012.07.008.
• Yang M, Lei M, Huo S (2003) Why is Leu55-->Pro55 transthyretin variant the most amyloidogenic: insights from molecular dynamics simulations of transthyretin monomers. Protein Sci 12: 1222-1231. doi: 10.1110/ps.0239703.

Identifiers

DOI

10.18388/abp.2016_1393