Synchrotron-Infrared Microscopy Analysis of Amyloid Fibrils Irradiated by Mid-Infrared Free-Electron Laser

Abstract

Amyloid fibrils are widely recognized as a cause of serious amyloidosis such as Alzheimer’s disease. Although dissociation of amyloid fibril aggregates is expected to lead to a decrease in the toxicity of the fibrils in cells, the fibril structure is robust under physiological conditions. We have irradiated amyloid fibrils with a free-electron laser (FEL) tuned to mid-infrared frequencies to induce dissociation of the aggregates into monomer forms. We have previously succeeded in dissociating fibril structures of a short peptide of the thyroid hormone by tuning the oscillation frequency to the amide I band, but the detailed structural changes of the peptide have not yet been determined at a high spatial resolution. Synchrotron-radiation infrared microscopy (SR-IRM) is a powerful tool for in situ analysis of minute structural changes of various materials, and in this study, the feasibility of SR-IRM for analyzing the microscopic conformational changes of amyloid fibrils after FEL irradiation was investigated. Reflection spectra of the amyloid fibril surface showed that the amide I peaks shifted to higher wave numbers after the FEL irradiation, indicating that the initial β-sheet-rich structure transformed into a mixture of non-ordered and turn-like peptide conformations. This result demonstrates that conformational changes of the fibril structure after the FEL irradiation can be observed at a high spatial resolution using SR-IRM analysis and the FEL irradiation system can be useful for dissociation of amyloid aggregates.

Share and Cite:

Kawasaki, T. , Yaji, T. , Imai, T. , Ohta, T. and Tsukiyama, K. (2014) Synchrotron-Infrared Microscopy Analysis of Amyloid Fibrils Irradiated by Mid-Infrared Free-Electron Laser. American Journal of Analytical Chemistry, 5, 384-394. doi: 10.4236/ajac.2014.56047.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Woldemeskel, M. (2012) A Concise Review of Amyloidosis in Animals. Veterinary Medicine International, 2012, Article ID: 427296.
http://dx.doi.org/10.1155/2012/427296
[2] Gertz, M.A. (2013) Immunoglobulin Light Chain Amyloidosis: 2013 Update on Diagnosis, Prognosis, and Treatment. American Journal of Hematology, 88, 417-425.
http://dx.doi.org/10.1002/ajh.23400
[3] Dobson, C.M. (2001) The Structural Basis of Protein Folding and Its Links with Human Disease. Philosophical Transactions of the Royal Society B, 356, 133-145.
http://dx.doi.org/10.1098/rstb.2000.0758
[4] Prince, M., Prina, M. and Guerchet, M. (2013) The World Alzheimer Report 2013 in the Global Voice on Dementia. Alzheimer Disease International.
http://www.alz.co.uk/adi-research
[5] Petruzziello, F., Zeppa, P., Catalano, L., Cozzolino, I., Gargiulo, G., Musto, P., D’Auria, F., Liso, V., Rizzi, R., Caruso, N., Califano, C., Piro, E., Musso, M., Bonanno, V., Falcone, A.P., Tafuto, S., Raimondo, F.D., Laurentiis, M.D., Pane, F., Palombini, L. and Rotoli, B. (2010) Amyloid in Bone Marrow Smears of Patients Affected by Multiple Myeloma. Annals of Hematology, 89, 469-474.
http://dx.doi.org/10.1007/s00277-009-0857-9
[6] Booth, D.R., Sunde, M., Bellotti, V., Robinson, C.V., Hutchinson, W.L., Fraser, P.E., Hawkins, P.N., Dobson, C.M., Radford, S.E., Blake, C.C.F. and Pepys, M.B. (1997) Instability, Unfolding and Aggregation of Human Lysozyme Variants Underlying Amyloid Fibrillogenesis. Nature, 385, 787-793.
[7] Cheng, B., Gong, H., Xiao, H., Petersen, R.B., Zheng, L. and Huang, K. (2013) Inhibiting Toxic Aggregation of Amyloidogenic Proteins: A Therapeutic Strategy for Protein Misfolding Diseases. Biochimica et Biophysica Acta, 1830, 4860-4871.
http://dx.doi.org/10.1016/j.bbagen.2013.06.029
[8] Kawasaki, T., Fujioka, J., Imai, T. and Tsukiyama, K. (2012) Effect of Mid-Infrared Free-Electron Laser Irradiation on Refolding of Amyloid-Like Fibrils of Lysozyme into Native Form. The Protein Journal, 31, 710-716.
http://dx.doi.org/10.1007/s10930-012-9452-3
[9] Kawasaki, T., Imai, T. and Tsukiyama, K. (2014) Use of a Mid-Infrared Free-Electron Laser (MIR-FEL) for Dissociation of the Amyloid Fibril Aggregates of a Peptide. Journal of Analytical Sciences, Methods and Instrumentation, 4, 9-18.
http://dx.doi.org./10.4236/jasmi.2014.41002
[10] Edwards, G., Logan, R., Copeland, M., Reinisch, L., Davidson, J., Johnson, B., Maciunas, R., Mendenhall, M., Ossoff, R., Tribble, J., Werkhaven, J. and O’Day, D. (1994) Tissue Ablation by a Free-Electron Laser Tuned to the Amide II Band. Nature, 371, 416-419.
[11] Austin, R.H., Xie, A., van der Meer, L., Redlich, B., Lindgård, P.-A., Frauenfelder, H. and Fu, D. (2005) Picosecond Thermometer in the Amide I Band of Myoglobin. Physical Review Letters, 94, 128101.
http://dx.doi.org/10.1103/PhysRevLett.94.128101
[12] Xiao, Y., Guo, M., Zhang, P., Shanmugam, G., Polavarapu, P.L. and Hutson, M.S. (2008) Wavelength-Dependent Conformational Changes in Collagen after Mid-Infrared Laser Ablation of Cornea. Biophysical Journal, 94, 1359-1366.
http://dx.doi.org/10.1529/biophysj.107.114389
[13] Oomens, J., Polfer, N., Moore, D.T., van der Meer, L., Marshall, A.G., Eyler, J.R., Meijer, G. and von Helden, G. (2005) Charge-State Resolved Mid-Infrared Spectroscopy of a Gas-Phase Protein. Physical Chemistry Chemical Physics, 7, 1345-1348.
http://dx.doi.org/10.1039/B502322J
[14] Nomaru, K., Kawai, M., Yokoyama, M., Oda, F., Nakayama, A., Koike, H. and Kuroda, H. (2000) Optical Beam Transport System at FEL-SUT. Nuclear Instruments and Methods in Physics Research Section A, 445, 379-383.
[15] Apostol, M.I., Perry, K. and Surewicz, W.K. (2013) Crystal Structure of a Human Prion Protein Fragment Reveals a Motif for Oligomer Formation. Journal of the American Chemical Society, 135, 10202-10205.
http://dx.doi.org/10.1021/ja403001q
[16] Paravastu, A.K., Leapman, R.D., Yau, W.-M. and Tycko, R. (2008) Molecular Structural Basis for Polymorphism in Alzheimer’s β-Amyloid Fibrils. Proceedings of the National Academy of Sciences of the United States of America, 105, 18349-18354.
http://dx.doi.org/10.1073/pnas.0806270105
[17] Itoh-Watanabe, H., Kamihira-Ishijima, M., Javkhlantugs, N., Inoue, R., Itoh, Y., Endo, H., Tuzi, S., Saitô, H., Ueda, K. and Naito, A. (2013) Role of Aromatic Residues in Amyloid Fibril Formation of Human Calcitonin by Solid-State 13C NMR and Molecular Dynamics Simulation. Physical Chemistry Chemical Physics, 15, 8890-8901.
http://dx.doi.org/10.1039/c3cp44544e
[18] Bandekar, J. (1992) Amide Modes and Protein Conformation. Biochimica et Biophysica Acta—Protein Structure and Molecular Enzymology, 1120, 123-143.
[19] Ahmad, A., Uversky, V.N., Hong, D. and Fink, A.L. (2005) Early Events in the Fibrillation of Monomeric Insulin. The Journal of Biological Chemistry, 280, 42669-42675.
http://dx.doi.org/10.1074/jbc.M504298200
[20] Zandomeneghi, G., Krebs, M.R.H., McCammon, M.G. and Fändrich, M. (2004) FTIR Reveals Structural Differences between Native β-Sheet Proteins and Amyloid Fibrils. Protein Science, 13, 3314-3321.
http://dx.doi.org/10.1110/ps.041024904
[21] Miller, L.M., Bourassa, M.W. and Smith, R.J. (2013) FTIR Spectroscopic Imaging of Protein Aggregation in Living Cells. Biochimica et Biophysica Acta, 1828, 2339-2346.
http://dx.doi.org/10.1016/j.bbamem.2013.01.014
[22] Acerbo, A.S., Lawrence Carr, G., Judex, S. and Miller, L.M. (2012) Imaging the Material Properties of Bone Specimens Using Reflection-Based Infrared Microspectroscopy. Analytical Chemistry, 84, 3607-3613.
http://dx.doi.org/10.1021/ac203375d
[23] Gautam, R., Chandrasekar, B., Deobagkar-Lele, M., Rakshit, S., Vinay Kumar, B.N., Umapathy, S. and Nandi, D. (2012) Identification of Early Biomarkers during Acetaminophen-Induced Hepatotoxicity by Fourier Transform Infrared Microspectroscopy. PLoS ONE, 7, Article ID: e45521.
http://dx.doi.org/10.1371/journal.pone.0045521
[24] Kakoulli, I., Prikhodko, S.V., Fischer, C., Cilluffo, M., Uribe, M., Bechtel, H.A., Fakra, S.C. and Marcus, M.A. (2013) Distribution and Chemical Speciation of Arsenic in Ancient Human Hair Using Synchrotron Radiation. Analytical Chemistry, 86, 521-526.
http://dx.doi.org/10.1021/ac4024439
[25] Ling, S., Qi, Z., Knight, D.P., Huang, Y., Huang, L., Zhou, H., Shao, Z. and Chen, X. (2013) Insight into the Structure of Single Antheraea pernyi Silkworm Fibers Using Synchrotron FTIR Microspectroscopy. Biomacromolecules, 14, 1885-1892.
http://dx.doi.org/10.1021/bm400267m
[26] Chen, L., Holman, H.-Y.N., Hao, Z., Bechtel, H.A., Martin, M.C., Wu, C. and Chu, S. (2012) Synchrotron Infrared Measurements of Protein Phosphorylation in Living Single PC12 Cells during Neuronal Differentiation. Analytical Chemistry, 84, 4118-4125.
http://dx.doi.org/10.1021/ac300308x
[27] Yaji, T., Yamamoto, Y., Ohta, T. and Kimura, S. (2008) A New Beamline for Infrared Microscopy in the SR Center of Ritsumeikan University. Infrared Physics & Technology, 51, 397-399.
http://dx.doi.org/10.1016/j.infrared.2007.12.014
[28] Reches, M., Porat, Y. and Gazit, E. (2002) Amyloid Fibril Formation by Pentapeptide and Tetrapeptide Fragments of Human Calcitonin. The Journal of Biological Chemistry, 277, 35475-35480.
http://dx.doi.org/10.1074/jbc.M206039200
[29] Tenidis, K., Waldner, M., Bernhagen, J., Fischle, W., Bergmann, M., Weber, M., Merkle, M.-L., Voelter, W., Brunner, H. and Kapurniotu, A. (2000) Identification of a Penta- and Hexapeptide of Islet Amyloid Polypeptide (IAPP) with Amyloidogenic and Cytotoxic Properties. Journal of Molecular Biology, 295, 1055-1071.
[30] Santi, S., Musi, V., Descrovi, E., Paeder, V., Di Francesco, J., Hvozdara, L., van der Wal, P., Lashuel, H.A., Pastore, A., Neier, R. and Herzig, H.P. (2013) Real-Time Amyloid Aggregation Monitoring with a Photonic Crystal-Based Approach. ChemPhysChem, 14, 3476-3482.
http://dx.doi.org/10.1002/cphc.201300633

Copyright © 2021 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.