Abstract
Structure of amyloid β (Aβ) fibrils is rigidly stacked by β-sheet conformation, and the fibril state of Aβ is profoundly related to pathogenesis of Alzheimer’s disease (AD). Although mid-infrared light has been used for various biological researches, it has not yet been known whether the infrared light changes the fibril structure of Aβ. In this study, we tested the effect of irradiation of intense mid-infrared light from a free-electron laser (FEL) targeting the amide bond on the reduction of β-sheet content in Aβ fibrils. The FEL reduced entire contents of proteins exhibiting β-sheet structure in brain sections from AD model mice, as shown by synchrotron-radiation infrared microscopy analysis. Since Aβ1-42 fibril absorbed a considerable FEL energy at amide I band (6.17 μm), we irradiated the FEL at 6.17 μm and found that β-sheet content of naked Aβ1-42 fibril was decreased using infrared microscopic analysis. Consistent with the decrease in the β-sheet content, Congo-red signal is decreased after the irradiation to Aβ1-42 fibril. Furthermore, electron microscopy analysis revealed that morphologies of the fibril and proto-fibril were largely changed after the irradiation. Thus, mid-infrared light dissociates β-sheet structure of Aβ fibrils, which justifies exploration of possible laser-based therapy for AD.
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Abbreviations
- Aβ:
-
Amyloid beta
- AD:
-
Alzheimer’s disease
- AICD:
-
APP intracellular domain
- APP:
-
Amyloid precursor protein
- FEL:
-
Free-electron laser
- PS1:
-
Presenilin 1
- sAPPβ:
-
Secreted amyloid precursor protein-β
- YAG:
-
Yttrium aluminum garnet
References
Ahmed M et al (2010) Structural conversion of neurotoxic amyloid-beta(1-42) oligomers to fibrils. Nat Struct Mol Biol 17(5):561–567
Austin RH et al (2005) Picosecond thermometer in the amide I band of myoglobin. Phys Rev Lett 94(12):128101
Chung H et al (2012) The nuts and bolts of low-level laser (light) therapy. Ann Biomed Eng 40(2):516–533
Edwards G et al (1994) Tissue ablation by a free-electron laser tuned to the amide II band. Nature 371(6496):416–419
Fandrich M (2012) Oligomeric intermediates in amyloid formation: structure determination and mechanisms of toxicity. J Mol Biol 421(4–5):427–440
Farfara D et al (2015) Low-level laser therapy ameliorates disease progression in a mouse model of Alzheimer’s disease. J Mol Neurosci 55(2):430–436
Gouras GK, Olsson TT, Hansson O (2015) beta-Amyloid peptides and amyloid plaques in Alzheimer’s disease. Neurotherapeutics 12(1):3–11
Hutson MS et al (2009) Interplay of wavelength, fluence and spot-size in free-electron laser ablation of cornea. Opt Express 17(12):9840–9850
Kawasaki T et al (2012) Effect of mid-infrared free-electron laser irradiation on refolding of amyloid-like fibrils of lysozyme into native form. Protein J 31(8):710–716
Kawasaki T et al (2014) Mid-infrared free-electron laser tuned to the amide I band for converting insoluble amyloid-like protein fibrils into the soluble monomeric form. Lasers Med Sci 29(5):1701–1707
Kawasaki T et al (2016a) Application of mid-infrared free-electron laser tuned to amide bands for dissociation of aggregate structure of protein. J Synchrotron Rad 23(1):152–157
Kawasaki T et al (2016b) Picosecond pulsed infrared laser tuned to amide I band dissociates polyglutamine fibrils in cells. Lasers Med Sci 31(7):1425–1431
Kozub J et al (2011) Raman-shifted alexandrite laser for soft tissue ablation in the 6- to 7-microm wavelength range. Biomed Opt Express 2(5):1275–1281
Lambracht-Washington D, Rosenberg RN (2013) Anti-amyloid beta to tau—based immunization: Developments in immunotherapy for Alzheimer disease. Immunotargets Ther 2013(2):105–114
Lanzillotta A et al (2011) The gamma-secretase modulator CHF5074 reduces the accumulation of native hyperphosphorylated tau in a transgenic mouse model of Alzheimer’s disease. J Mol Neurosci 45(1):22–31
Mackanos MA et al (2012) Comparing an optical parametric oscillator (OPO) as a viable alternative for mid-infrared tissue ablation with a free electron laser (FEL). Lasers Med Sci 27(6):1213–1223
Madey JMJ (1971) Stimulated emission of bremsstrahlung in a periodic magnetic field. J Appl Phys 42(5):1906–1913
Meng C, He Z, Xing D (2013) Low-level laser therapy rescues dendrite atrophy via upregulating BDNF expression: implications for Alzheimer’s disease. J Neurosci 33(33):13505–13517
Miller LM, Bourassa MW, Smith RJ (2013) FTIR spectroscopic imaging of protein aggregation in living cells. Biochim Biophys Acta 1828(10):2339–2346
Morel B, Varela L, Conejero-Lara F (2010) The thermodynamic stability of amyloid fibrils studied by differential scanning calorimetry. J Phys Chem B 114(11):4010–4019
Mori T et al (2013) Ferulic acid is a nutraceutical beta-secretase modulator that improves behavioral impairment and alzheimer-like pathology in transgenic mice. PLoS ONE 8(2):e55774
Morris GP, Clark IA, Vissel B (2014) Inconsistencies and controversies surrounding the amyloid hypothesis of Alzheimer’s disease. Acta Neuropathol Commun 2:135
Oddo S et al (2003) Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39(3):409–421
Oomens J et al (2005) Charge-state resolved mid-infrared spectroscopy of a gas-phase protein. Phys Chem Chem Phys 7(7):1345–1348
Ovelmen-Levitt J et al (2003) Brain ablation in the rat cerebral cortex using a tunable-free electron laser. Lasers Surg Med 33(2):81–92
Petruzziello F et al (2010) Amyloid in bone marrow smears of patients affected by multiple myeloma. Ann Hematol 89(5):469–474
Purushothuman S et al (2014) Photobiomodulation with near infrared light mitigates Alzheimer’s disease-related pathology in cerebral cortex—evidence from two transgenic mouse models. Alzheimers Res Ther 6(1):2
Purushothuman S et al (2015) Near infrared light mitigates cerebellar pathology in transgenic mouse models of dementia. Neurosci Lett 591:155–159
Reches M, Porat Y, Gazit E (2002) Amyloid fibril formation by pentapeptide and tetrapeptide fragments of human calcitonin. J Biol Chem 277(38):35475–35480
Saltmarche AE et al (2017) Significant improvement in cognition in mild to moderately severe dementia cases treated with transcranial plus intranasal photobiomodulation: case series report. Photomed Laser Surg 35(8):432–441
Sarver RW Jr, Krueger WC (1991) Protein secondary structure from Fourier transform infrared spectroscopy: a data base analysis. Anal Biochem 194(1):89–100
Soto C et al (1998) Beta-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer’s therapy. Nat Med 4(7):822–826
Stancu IC et al (2014) Models of beta-amyloid induced Tau-pathology: the long and “folded” road to understand the mechanism. Mol Neurodegener 9:51
Thirumalai D, Reddy G, Straub JE (2012) Role of water in protein aggregation and amyloid polymorphism. Acc Chem Res 45(1):83–92
Tjernberg L et al (2002) Charge attraction and beta propensity are necessary for amyloid fibril formation from tetrapeptides. J Biol Chem 277(45):43243–43246
Vogel A, Venugopalan V (2003) Mechanisms of pulsed laser ablation of biological tissues. Chem Rev 103(2):577–644
Wagner W, Sokolow A, Pearlstein R, Edwards G (2009) Thermal vapor bubble and pressure dynamics during infrared laser ablation of tissue. Appl Phys Lett 94:013901
Yamada T et al (2002) Observation of molecular changes of a necrotic tissue from a murine carcinoma by Fourier-transform infrared microspectroscopy. Clin Cancer Res 8(6):2010–2014
Acknowledgements
We thank Dr. Kanjiro Torigoe (Graduate School of Science and Technology, Tokyo University of Science) for technical support of TEM analyses. We also thank Dr. Takayuki Imai (FEL-TUS), Mr. Tetsuo Morotomi, and Mr. Keiichi Hisazumi (MITSUBISHI ELECTRIC SYSTEM & SERVICE CO., LTD.) for operating the FEL instrument. This work was supported by the Open Advanced Research Facilities Initiative and the Photon Beam Platform Project of the Ministry of Education, Culture, Sport, Science and Technology, Japan (to T. K., T. O., and K. T.), JSPS KAKENHI Grant Number JP16K15553 (to K. N.), and grants from SENSHIN Medical Research Foundation (to K. N.) and Takeda Science Foundation (to K. N.).
Funding
T.K. and K.N. set up the hypothesis. T.K., T.O., K.T., and K.N. designed the experiments. T.K., T.Y., and K.N. performed experiments and analyzed the data. T.K., K.T., and K.N. wrote the manuscript.
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Kawasaki, T., Yaji, T., Ohta, T. et al. Dissociation of β-Sheet Stacking of Amyloid β Fibrils by Irradiation of Intense, Short-Pulsed Mid-infrared Laser. Cell Mol Neurobiol 38, 1039–1049 (2018). https://doi.org/10.1007/s10571-018-0575-8
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DOI: https://doi.org/10.1007/s10571-018-0575-8