Plaque-associated lipids in Alzheimer's diseased brain tissue visualized by nonlinear microscopy

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kiskis, Juris ^a   Fink, Helen ^a   Nyberg, Lena ^a   Thyr, Jacob ^b   Li, Jia Yi ^c   Enejder, Annika ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b K Analys ^*  (Sweden)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID;

ALZHEIMER DISEASE; AMYLOID PLAQUE; BRAIN; CHEMISTRY; FLUORESCENCE; HUMAN; MICROSCOPY; NONLINEAR SYSTEM; PATHOLOGY; PROCEDURES; RAMAN SPECTROMETRY;

ALZHEIMER DISEASE; BRAIN; FLUORESCENCE; HUMANS; LIPIDS; MICROSCOPY; NONLINEAR DYNAMICS; PLAQUE, AMYLOID; SPECTRUM ANALYSIS, RAMAN;

EID: 84940510248     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13489     Document Type: Article

References (58)

1. World health organization, The top 10 causes of death. Available at: http://www.who.int/mediacentre/factsheets/fs310/en/index1.html (Date of access: 18/02/2015)
2. World Health Organization, Executive summary in Dementia: a public health priority, 1-2 (WHO, 2012). Available at: http://apps. who.int/iris/bitstream/10665/75263/1/9789241564458-eng.pdf?ua= 1 (Date of access: 18/02/ 2015)
3. Lue, L. F. et al. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862 (1999).
4. Mucke, L. et al. High-level neuronal expression of A beta(1-42) in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J. Neurosci. 20, 4050-4058 (2000).
5. Gong, Y. S. et al. Alzheimer's disease-affected brain: Presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. U.S.A. 100, 10417-10422 (2003).
6. Cleary, J. P. et al. Natural oligomers of the amyloid-protein specifically disrupt cognitive function. Nature Neurosci. 8, 79-84 (2005).
7. Shankar, G. M. et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842 (2008).
8. Lesne, S. E. et al. Brain amyloid-beta oligomers in ageing and Alzheimer's disease. Brain 136, 1383-1398 (2013).
9. Deshpande, A., Mina, E., Glabe, C. & Busciglio, J. Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J. Neurosci. 26, 6011-6018 (2006).
10. Stefani, M. Structural features and cytotoxicity of amyloid oligomers: Implications in Alzheimer's disease and other diseases with amyloid deposits. Prog. Neurobiol. 99, 226-245 (2012).
11. Larson, M. E. & Lesne, S. E. Soluble Aβ oligomer production and toxicity. J. Neurochem. 120, 125-139 (2012).
12. Overk, C. R. & Masliah, E. Pathogenesis of synaptic degeneration in Alzheimer's disease and Lewy body disease. Biochem. Pharmacol. 88, 508-516 (2014).
13. Koffie, R. M., et al. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl. Acad. Sci. U.S.A. 106, 4012-4017 (2009).
14. Canevari, L., Abramov, A. Y. & Duchen, M. R. Toxicity of amyloid beta peptide: Tales of calcium, mitochondria, and oxidative stress. Neurochem. Res. 29, 637-650 (2004).
15. Cha, M. Y. et al. Mitochondria-Specific Accumulation of Amyloid beta Induces Mitochondrial Dysfunction Leading to Apoptotic Cell Death. Plos One 7, e34929 (2012). doi: 10.1371/journal.pone.0034929
16. doi: 10.1371/journal.pone.0034929 16. Sanchez, L. et al. A beta 40 and A beta 42 Amyloid Fibrils Exhibit Distinct Molecular Recycling Properties. J. Am. Chem. Soc. 133, 6505-6508 (2011).
17. Widenbrant, M. J. O., Rajadas, J., Sutardja, C. & Fuller, G. G. Lipid-induced beta-amyloid peptide assemblage fragmentation. Biophys. J. 91, 4071-4080 (2006).
18. Martins, I. C. et al. Lipids revert inert A beta amyloid fibrils to neurotoxic protofibrils that affect learning in mice. Embo J. 27, 224-233 (2008).
19. Rak, M., Del Bigio, M. R., Mai, S., Westaway, D. & Gough, K. Dense-core and diffuse Abeta plaques in TgCRND8 mice studied with synchrotron FTIR microspectroscopy. Biopolymers 87, 207-217 (2007).
20. Kuzyk, A. et al. Association among Amyloid Plaque, Lipid, and Creatine in Hippocampus of TgCRND8 Mouse Model for Alzheimer Disease. J. Biol. Chem. 285, 31202-31207 (2010).
21. Panchal, M. et al. Enrichment of cholesterol in microdissected Alzheimer's disease senile plaques as assessed by mass spectrometry. J. Lipid. Res. 51, 598-605 (2010).
22. Kastyak-Ibrahim, M. Z. et al. Biochemical label-free tissue imaging with subcellular-resolution synchrotron FTIR with focal plane array detector. Neuroimage 60, 376-383 (2012).
23. Liao, C. R. et al. Synchrotron FTIR reveals lipid around and within amyloid plaques in transgenic mice and Alzheimer's disease brain. Analyst 138, 3991-3997 (2013).
24. Sole-Domenech, S. et al. Localization of cholesterol, amyloid and glia in Alzheimer's disease transgenic mouse brain tissue using time-of-flight secondary ion mass spectrometry (ToF-SIMS) and immunofluorescence imaging. Acta Neuropathol. 125, 145-157 (2013).
25. Friedman, R., Pellarin, R. & Caflisch, A. Soluble Protofibrils as Metastable Intermediates in Simulations of Amyloid Fibril Degradation Induced by Lipid Vesicles. J. Phys. Chem. Lett. 1, 471-474 (2010).
26. Kaplan, B., Martin, B. M., Livneh, A., Pras, M. & Gallo, G. Biochemical micro-techniques in the diagnosis and classification of amyloidosis. Curr. Pharm. Anal. 2, 45-52 (2006).
27. Nesterov, E. E. et al. In vivo optical Imaging of amyloid aggregates in brain: Design of fluorescent markers. Angew. Chem. Int. Ed. (English) 44, 5452-5456 (2005).
28. Pedersen, J. T. & Heegaard, N. H. H. Analysis of Protein Aggregation in Neurodegenerative Disease. Anal. Chem. 85, 4215-4227 (2013).
29. Touboul, D. & Gaudin, M. Lipidomics of Alzheimer's disease. Bioanalysis 6, 541-561 (2014).
30. Mori T. et al. Cholesterol accumulates in senile plaques of Alzheimer disease patients and in transgenic APP(SW) mice. J. Neuropathol. Exp. 60, 778-785 (2001).
31. Burns, M. P. et al. Co-localization of cholesterol, apolipoprotein E and fibrillar A beta in amyloid plaques. Mol. Brain Res. 110, 119-125 (2003).
32. Lebouvier, T., Perruchini, C., Panchal, M., Potier, M. C. & Duyckaerts, C. Cholesterol in the senile plaque: often mentioned, never seen. Acta Neuropathol. 117, 31-34 (2009).
33. Lazar, A. N. et al. Time-of-flight secondary ion mass spectrometry (TOF-SIMS) imaging reveals cholesterol overload in the cerebral cortex of Alzheimer disease patients. Acta Neuropathol. 125, 133-144 (2013).
34. Carlred, L. et al. Simultaneous Imaging of Amyloid-beta and Lipids in Brain Tissue Using Antibody-Coupled Liposomes and Time-of-Flight Secondary Ion Mass Spectrometry. J. Am. Chem. Soc. 136, 9973-9981 (2014).
35. Le, T. T., Yue, S. & Cheng, J. X. Shedding new light on lipid biology with coherent anti-Stokes Raman scattering microscopy. J. Lipid Res. 51, 3091-3102 (2010).
36. Evans, C. L., Potma, E. O., Puoris'haag, M., Cote, D., Lin, C. P. & Xie, X. S. Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy. Proc. Natl. Acad. Sci. U.S.A. 102, 16807-16812 (2005).
37. Evans, C. L., Xu, X., Kesari, S., Xie, X. S., Wong, S. T. C. & Young, G. S. Chemically-selective imaging of brain structures with CARS microscopy. Opt Express 15, 12076-12087 (2007).
38. Hellerer, T., Axang, C., Brackmann, C., Hillertz, P., Pilon, M. & Enejder, A. Monitoring of lipid storage in Caenorhabditis elegans using coherent anti-Stokes Raman scattering (CARS) microscopy. Proc. Natl. Acad. Sci. U.S.A. 104, 14658-14663 (2007).
39. Wang, H. F., Fu, Y., Zickmund, P., Shi, R. Y. & Cheng, J. X. Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues. Biophys. J. 89, 581-591 (2005).
40. Kelenyi, G. Thioflavin S fluorescent and Congo Red anisotropic stainings in histologic demonstration of amyloid. Acta Neuropathol. 7, 336-348 (1967).
41. Johansson, A. S. et al. Docosahexaenoic acid stabilizes soluble amyloid-beta protofibrils and sustains amyloid-beta-induced neurotoxicity in vitro. Febs J. 274, 990-1000 (2007).
42. Nan, X., Cheng, J. X. & Xie, X. S. Vibrational imaging of lipid droplets in live fibroblast cells with coherent anti-Stokes Raman scattering microscopy. J. Lipid. Res. 44, 2202-2208 (2003).
43. Lim, R. S. et al. Identification of cholesterol crystals in plaques of atherosclerotic mice using hyperspectral CARS imaging. J. Lipid. Res. 52, 2177-2186 (2011).
44. Larsson, K. & Rand, R. P. Detection of changes in the environment of hydrocarbon chains by Raman spectroscopy and its application to lipid-protein systems. Biochim. Biophys. Acta 326, 245-255 (1973).
45. Bonn, M., Muller, M., Rinia, H. A. & Burger, K. N. J. Imaging of chemical and physical state of individual cellular lipid droplets using multiplex CARS microscopy. J. Raman Spectrosc. 40, 763-769 (2009).
46. Krafft, C., Sobottka, S. B., Schackert, G. & Salzer, R. Near infrared Raman spectroscopic mapping of native brain tissue and intracranial tumors. Analyst 130, 1070-1077 (2005).
47. Sane, S. U., Cramer, S. M. & Przybycien, T. M. A Holistic Approach to Protein Secondary Structure Characterization Using Amide I Band Raman Spectroscopy. Anal. Biochem. 269, 255-272 (1999).
48. Chen, P. et al. Raman signature from brain hippocampus could aid Alzheimer's disease diagnosis. Appl. Optics 48, 4743-4748 (2009).
49. Krafft, C., Neudert, L., Simat, T. & Salzer, R. Near infrared Raman spectra of human brain lipids. Spectrochim. Acta Mol. Biomol. Spectros. 61, 1529-1535 (2005).
50. Milanesi, L. et al. Direct three-dimensional visualization of membrane disruption by amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 109, 20455-20460 (2012).
51. Coutinho, A., Loura, L. M. S. & Prieto, M. FRET studies of lipid-protein aggregates related to amyloid-like fibers. J. Neurochem. 116, 696-701 (2011).
52. Hellstrand, E., Nowacka, A., Topgaard, D., Linse, S. & Sparr, E. Membrane Lipid Co-Aggregation with alpha-Synuclein Fibrils. Plos One 8, e77235 (2013). doi: 10.1371/journal.pone.0077235
53. doi: 10.1371/journal.pone.0077235 53. Joshi, P. et al. Microglia convert aggregated amyloid-beta into neurotoxic forms through the shedding of microvesicles. Cell Death Differ. 21, 582-593 (2014).
54. Verghese, P. B. et al. ApoE influences amyloid-beta (A beta) clearance despite minimal apoE/A beta association in physiological conditions. Proc. Natl. Acad. Sci. U.S.A. 110, E1807-E1816 (2013).
55. Liu, C. C., Kanekiyo, T., Xu, H. X. & Bu, G. J. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 9, 106-118 (2013).
56. Galli, R. et al. Effects of tissue fixation on coherent anti-Stokes Raman scattering images of brain. J. Biomed. Opt. 19, 071402-071402 (2014).
57. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
58. Zhang, Z. M., Chen, S. & Liang, Y. Z. Baseline correction using adaptive iteratively reweighted penalized least squares. Analyst 135, 1138-1146 (2010).