Use of a Mid-Infrared Free-Electron Laser (MIR-FEL) for Dissociation of the Amyloid Fibril Aggregates of a Peptide
ABSTRACT
Amyloid fibrils are deposited in various tissues in the body, and are linked to the putative causes of serious diseases such as amyloidosis. Although the conditions of the disease would be expected to improve if the fibril structure could be destroyed, the aggregated structure is stable under physiological conditions. Recently, we found that the amyloid fibrils of lysozyme could be refolded into their active form by using a mid-infrared free-electron laser (MIR-FEL) tuned to the amide I band (corresponding to the C=O stretch vibration), with the MIR-FEL having specific oscillation characteristics of a picosecond pulse structure, a tunable wavelength within mid-infrared frequencies, and high photon density. In the study, we tested the usability of the FEL for dissociation of aggregates of pathological amyloid fibrils by using a short peptide of human thyroid hormone. The fibrils (after being placed on a glass slide) were irradiated using the FEL tuned to the amide I band (1644 cm?1), and those in situ were analyzed by Congo-Red assay, scanning-electron microscopy, and transmission-electron microscopy. All of the results obtained using these microscopic analyses indicated that the amyloid fibril formation was considerably decreased by FEL irradiation. Moreover, upon irradiation, a strong fibril peak at the amide I band in the infrared spectrum was transformed into a broad peak. These results imply that the β-sheet-rich structure of the amyloid fibrils changed into non-ordered or unspecified structures after the FEL irradiation. This FEL irradiation system, combined with various analytical methods, shows promise for the dissociation of amyloid aggregates.
Cite this paper
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. doi: 10.4236/jasmi.2014.41002.
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. doi: 10.4236/jasmi.2014.41002.
References
[1] Stroud, J.C., Liu, C., Teng, P.K. and Eisenberg, D. (2012) Toxic Fibrillar Oligomers of Amyloid-β Have Cross-β Structure. Proceedings of the National Academy of Sciences of the United States of America, 109, 7717-7722.
http://dx.doi.org/10.1073/pnas.1203193109 [2] Zhu, H.-L., Meng, S.-R., Fan, J.-B., Chen, J. and Liang, Y. (2011) Fibrillization of Human Tau Is Accelerated by Exposure to Lead via Interaction with His-330 and His-362. ProS One, 6, Article ID: e25020.
http://dx.doi.org/10.1371/journal.pone.0025020 [3] Smith, M.H., Miles, T.F., Sheehan, M., Alfieri, K.N., Kokona, B. and Fairman, R. (2010) Polyglutamine Fibrils Are Formed Using a Simple Designed β-Hairpin Model. Proteins, 78, 1971-1979. http://dx.doi.org/10.1002/prot.22713 [4] Panza, G., Stohr, J., Dumpitak, C., Papathanassiou, D., Weib, J., Riesner, D., Willbold, D. and Birkmann, E. (2008) Spontaneous and BSE-Prion-Seeded Amyloid Formation of Full Length Recombinant Bovine Prion Protein. Biochemical and Biophysical Research Communications, 373, 493-497. http://dx.doi.org/10.1016/j.bbrc.2008.06.059 [5] 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 [6] Spillantini, M.G., Schmidt, M.L., Lee, V. M.-Y., Trojanowski, J.Q., Jakes, R. and Goedert, M. (1997) α-Synuclein in Lewy Bodies. Nature, 388, 839-840. [7] Lu, M., Hiramatsu, H., Goto, Y. and Kitagawa, T. (2006) Structure of Interacting Segments in the Growing Amyloid Fibril of β2-Microglobulin Probed with IR Spectroscopy. Journal of Molecular Biology, 362, 355-364.
http://dx.doi.org/10.1016/j.jmb.2006.07.023 [8] 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 [9] 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 [10] 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. [11] 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. [12] 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. [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] Ovelmen-Levitt, J., Straub, K.D., Hauger, S., Szarmes, E., Madey, J., Pearlstein, R.D. and Nashold Jr., B.S. (2003) Brain Ablation in the Rat Cerebral Cortex Using a Tunable-Free Electron Laser. Lasers in Surgery and Medicine, 33, 81-92. http://dx.doi.org/10.1002/lsm.10197 [15] Annenkov, V.V., Kozlov, A.S., Danilovtseva, E.N., Basharina, T. N. and Petrov, A.K. (2013) Dissection of the Frustules of the Diatom Synedraacus under the Action of Picosecond Impulses of Submillimeter Laser Irradiation. European Biophysics Journal, 42, 587-590. http://dx.doi.org/10.1007/s00249-013-0913-1 [16] Austin, R.H., Xie, A., van der Meer, L., Redlich, B., Lindgard, P.-A., Frauenfelder, H. and Fu, D. (2005) Picosecond Thermometer in the Amide I Band of Myoglobin. Physical Review Letters, 94, 128101-1-4.
http://dx.doi.org/10.1103/PhysRevLett.94.128101 [17] Hutson, M.S., Ivanov, B., Jayasinghe, A., Adunas, G., Xiao, Y., Guo, M. and Kozub, J. (2009) Interplay of Wavelength, Fluence and Spot-Size in Free-Electron Laser Ablation of Cornea. Optics Express, 17, 9840-9850. [18] 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 [19] Zandomeneghi, G., Krebs, M.R.H., McCammon, M.G. and Fandrich, 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 [20] 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 [21] 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 [22] Bandekar, J. (1992) Amide Modes and Protein Conformation. Biochimica et Biophysica Acta—Protein Structure and Molecular Enzymology, 1120, 123-143. [23] Thirumalai, D., Reddy, G. and Straub, J.E. (2012) Role of Water in Protein Aggregation and Amyloid Polymorphism. Accounts of Chemical Research, 45, 83-92. http://dx.doi.org/10.1021/ar2000869 [24] Zavalin, A., Hachey, D.L., Sundaramoorthy, M., Banerjee, S., Morgan, S., Feldman, L., Tolk, N. and Piston, D.W. (2008) Kinetics of a Collagen-Like Polypeptide Fragmentation after Mid-IR Free-Electron Laser Ablation. Biophysical Journal, 95, 1371-1381. http://dx.doi.org/10.1529/biophysj.107.122002 [25] Anfinsen, C.B. (1973) Principles That Govern the Folding of Protein Chains. Science, 181, 223-230. [26] Wagner, W., Sokolow, A., Pearlstein, R. and Edwards, G. (2009) Thermal Vapor Bubble and Pressure Dynamics during Infrared Laser Ablation of Tissue. Applied Physics Letters, 94, 013901-1-3. http://dx.doi.org/10.1063/1.3063127 [27] Itoh-Watanabe, H., Kamihira-Ishijima, M., Javkhlantugs, N., Inoue, R., Itoh, Y., Endo, H., Tuzi, S., Sait, 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 [28] Botelho, H.M., Leal, S.S., Cardoso, I., Yanamandra, K., Morozova-Roche, L.A., Fritz, G. and Gomes, C.M. (2012) S100A6 Amyloid Fibril Formation Is Calcium-Modulated and Enhances Superoxide Dismutase-1 (SOD1) Aggregation. The Journal of Biological Chemistry, 287, 42233-42242. http://dx.doi.org/10.1074/jbc.M112.396416
[1] Stroud, J.C., Liu, C., Teng, P.K. and Eisenberg, D. (2012) Toxic Fibrillar Oligomers of Amyloid-β Have Cross-β Structure. Proceedings of the National Academy of Sciences of the United States of America, 109, 7717-7722.
http://dx.doi.org/10.1073/pnas.1203193109 [2] Zhu, H.-L., Meng, S.-R., Fan, J.-B., Chen, J. and Liang, Y. (2011) Fibrillization of Human Tau Is Accelerated by Exposure to Lead via Interaction with His-330 and His-362. ProS One, 6, Article ID: e25020.
http://dx.doi.org/10.1371/journal.pone.0025020 [3] Smith, M.H., Miles, T.F., Sheehan, M., Alfieri, K.N., Kokona, B. and Fairman, R. (2010) Polyglutamine Fibrils Are Formed Using a Simple Designed β-Hairpin Model. Proteins, 78, 1971-1979. http://dx.doi.org/10.1002/prot.22713 [4] Panza, G., Stohr, J., Dumpitak, C., Papathanassiou, D., Weib, J., Riesner, D., Willbold, D. and Birkmann, E. (2008) Spontaneous and BSE-Prion-Seeded Amyloid Formation of Full Length Recombinant Bovine Prion Protein. Biochemical and Biophysical Research Communications, 373, 493-497. http://dx.doi.org/10.1016/j.bbrc.2008.06.059 [5] 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 [6] Spillantini, M.G., Schmidt, M.L., Lee, V. M.-Y., Trojanowski, J.Q., Jakes, R. and Goedert, M. (1997) α-Synuclein in Lewy Bodies. Nature, 388, 839-840. [7] Lu, M., Hiramatsu, H., Goto, Y. and Kitagawa, T. (2006) Structure of Interacting Segments in the Growing Amyloid Fibril of β2-Microglobulin Probed with IR Spectroscopy. Journal of Molecular Biology, 362, 355-364.
http://dx.doi.org/10.1016/j.jmb.2006.07.023 [8] 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 [9] 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 [10] 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. [11] 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. [12] 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. [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] Ovelmen-Levitt, J., Straub, K.D., Hauger, S., Szarmes, E., Madey, J., Pearlstein, R.D. and Nashold Jr., B.S. (2003) Brain Ablation in the Rat Cerebral Cortex Using a Tunable-Free Electron Laser. Lasers in Surgery and Medicine, 33, 81-92. http://dx.doi.org/10.1002/lsm.10197 [15] Annenkov, V.V., Kozlov, A.S., Danilovtseva, E.N., Basharina, T. N. and Petrov, A.K. (2013) Dissection of the Frustules of the Diatom Synedraacus under the Action of Picosecond Impulses of Submillimeter Laser Irradiation. European Biophysics Journal, 42, 587-590. http://dx.doi.org/10.1007/s00249-013-0913-1 [16] Austin, R.H., Xie, A., van der Meer, L., Redlich, B., Lindgard, P.-A., Frauenfelder, H. and Fu, D. (2005) Picosecond Thermometer in the Amide I Band of Myoglobin. Physical Review Letters, 94, 128101-1-4.
http://dx.doi.org/10.1103/PhysRevLett.94.128101 [17] Hutson, M.S., Ivanov, B., Jayasinghe, A., Adunas, G., Xiao, Y., Guo, M. and Kozub, J. (2009) Interplay of Wavelength, Fluence and Spot-Size in Free-Electron Laser Ablation of Cornea. Optics Express, 17, 9840-9850. [18] 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 [19] Zandomeneghi, G., Krebs, M.R.H., McCammon, M.G. and Fandrich, 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 [20] 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 [21] 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 [22] Bandekar, J. (1992) Amide Modes and Protein Conformation. Biochimica et Biophysica Acta—Protein Structure and Molecular Enzymology, 1120, 123-143. [23] Thirumalai, D., Reddy, G. and Straub, J.E. (2012) Role of Water in Protein Aggregation and Amyloid Polymorphism. Accounts of Chemical Research, 45, 83-92. http://dx.doi.org/10.1021/ar2000869 [24] Zavalin, A., Hachey, D.L., Sundaramoorthy, M., Banerjee, S., Morgan, S., Feldman, L., Tolk, N. and Piston, D.W. (2008) Kinetics of a Collagen-Like Polypeptide Fragmentation after Mid-IR Free-Electron Laser Ablation. Biophysical Journal, 95, 1371-1381. http://dx.doi.org/10.1529/biophysj.107.122002 [25] Anfinsen, C.B. (1973) Principles That Govern the Folding of Protein Chains. Science, 181, 223-230. [26] Wagner, W., Sokolow, A., Pearlstein, R. and Edwards, G. (2009) Thermal Vapor Bubble and Pressure Dynamics during Infrared Laser Ablation of Tissue. Applied Physics Letters, 94, 013901-1-3. http://dx.doi.org/10.1063/1.3063127 [27] Itoh-Watanabe, H., Kamihira-Ishijima, M., Javkhlantugs, N., Inoue, R., Itoh, Y., Endo, H., Tuzi, S., Sait, 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 [28] Botelho, H.M., Leal, S.S., Cardoso, I., Yanamandra, K., Morozova-Roche, L.A., Fritz, G. and Gomes, C.M. (2012) S100A6 Amyloid Fibril Formation Is Calcium-Modulated and Enhances Superoxide Dismutase-1 (SOD1) Aggregation. The Journal of Biological Chemistry, 287, 42233-42242. http://dx.doi.org/10.1074/jbc.M112.396416