Ultrastructural differences in pretangles between Alzheimer disease and corticobasal degeneration revealed by comparative light and electron microscopy

详细信息    查看全文

• 作者：Shinsui Tatsumi (1) (2) (3)
  Toshiki Uchihara (2)
  Ikuko Aiba (4)
  Yasushi Iwasaki (1)
  Maya Mimuro (1)
  Ryosuke Takahashi (3)
  Mari Yoshida (1)
  
  1. Department of Neuropathology ; Institute for Medical Science of Aging ; Aichi Medical University ; Nagakute ; Aichi ; Japan
  2. Laboratory of Structural Neuropathology ; Tokyo Metropolitan Institute of Medical Science ; 2-1-6 Kamikitazawa ; Setagaya ; Tokyo ; 156-8506 ; Japan
  3. Department of Neurology ; Kyoto University ; Kyoto ; Japan
  4. Department of Neurology ; Higashi Nagoya National Hospital ; Nagoya ; Aichi ; Japan
  
• 刊名：Acta Neuropathologica Communications
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：2
• 期：1
• 全文大小：1,582 KB
• 参考文献：1. Ross, CA, Poirier, MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10: pp. S10-S17 CrossRef
  2. Bancher, C, Grundke-Iqbal, I, Iqbal, K, Fried, VA, Smith, HT, Wisniewski, HM (1991) Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer disease. Brain Res 539: pp. 11-18 CrossRef
  3. Braak, E, Braak, H, Mandelkow, EM (1994) A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 87: pp. 554-567 CrossRef
  4. Uchihara T (2014) Pretangles and neurofibrillary changes -Similarities and differences between AD and CBD based on molecular and morphological evolution. Neuropathology 34(6):571鈥?, doi:10.1111/neup.12108
  5. Kidd, M (1963) Paired helical filaments in electron microscopy of Alzheimer鈥檚 disease. Nature 197: pp. 192-193 CrossRef
  6. Dickson, DW, Bergeron, C, Chin, SS, Duyckaerts, C, Horoupian, D, Ikeda, K, Jellinger, K, Lantos, PL, Lippa, CF, Mirra, SS, Tabaton, M, Vonsattel, JP, Wakabayashi, K, Litvan, I (2002) Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 61: pp. 935-946
  7. Uchihara, T, Mitani, K, Mori, H, Kondo, H, Yamada, M, Ikeda, K (1994) Abnormal cytoskeletal pathology peculiar to corticobasal degeneration is different from that of Alzheimer鈥檚 disease or progressive supranuclear palsy. Acta Neuropathol 88: pp. 379-383 CrossRef
  8. Tatsumi, S, Mimuro, M, Iwasaki, Y, Takahashi, R, Kakita, A, Takahashi, H, Yoshida, M (2014) Argyrophilic grains are reliable disease-specific features of corticobasal degeneration. J Neuropathol Exp Neurol 73: pp. 30-38 CrossRef
  9. Watanabe, S, Punge, A, Hollopeter, G, Willig, KI, Hobson, RJ, Davis, MW, Hell, SW, Jorgensen, EM (2011) Protein localization in electron micrographs using fluorescence nanoscopy. Nat Methods 8: pp. 80-84 CrossRef
  10. Modla, S, Czymmek, KJ (2011) Correlative microscopy: a powerful tool for exploring neurological cells and tissues. Micron 42: pp. 773-792 CrossRef
  11. Jahn, KA, Barton, DA, Kobayashi, K, Ratinac, KR, Overall, RL, Braet, F (2012) Correlative microscopy: providing new understanding in the biomedical and plant sciences. Micron 43: pp. 565-582 CrossRef
  12. Caplan, J, Niethammer, M, Taylor, RM, Czymmek, KJ (2011) The power of correlative microscopy: multi-modal, multi-scale, multi-dimensional. Curr Opin Struct Biol 21: pp. 686-693 CrossRef
  13. Giepmans, BN, Deerinck, TJ, Smarr, BL, Jones, YZ, Ellisman, MH (2005) Correlated light and electron microscopic imaging of multiple endogenous proteins using Quantum dots. Nat Methods 2: pp. 743-749 CrossRef
  14. Karreman, MA, Agronskaia, AV, Donselaar, EG, Vocking, K, Fereidouni, F, Humbel, BM, Verrips, CT, Verkleij, AJ, Gerritsen, HC (2012) Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen. J Struct Biol 180: pp. 382-386 CrossRef
  15. Deerinck, TJ (2008) The application of fluorescent quantum dots to confocal, multiphoton, and electron microscopic imaging. Toxicol Pathol 36: pp. 112-116 CrossRef
  16. Cortese, K, Diaspro, A, Tacchetti, C (2009) Advanced correlative light/electron microscopy: current methods and new developments using Tokuyasu cryosections. J Histochem Cytochem 57: pp. 1103-1112 CrossRef
  17. Faas, FG, Barcena, M, Agronskaia, AV, Gerritsen, HC, Moscicka, KB, Diebolder, CA, Driel, LF, Limpens, RW, Bos, E, Ravelli, RB, Koning, RI, Koster, AJ (2013) Localization of fluorescently labeled structures in frozen-hydrated samples using integrated light electron microscopy. J Struct Biol 181: pp. 283-290 CrossRef
  18. Heines, MA, Guyot-Sionnest, P (1996) Synthesis and characterization of strongly luminsecing ZnS-capped CdSe nanocrystals. J Phys Chem 100: pp. 468-471 CrossRef
  19. Uematsu, M, Adachi, E, Nakamura, A, Tsuchiya, K, Uchihara, T (2012) Atomic identification of fluorescent Q-dots on tau-positive fibrils in 3D-reconstructed pick bodies. Am J Pathol 180: pp. 1394-1397 CrossRef
  20. Kanazawa, T, Adachi, E, Orimo, S, Nakamura, A, Mizusawa, H, Uchihara, T (2012) Pale neurites, premature alpha-synuclein aggregates with centripetal extension from axon collaterals. Brain Pathol 22: pp. 67-78 CrossRef
  21. Montine, TJ, Phelps, CH, Beach, TG, Bigio, EH, Cairns, NJ, Dickson, DW, Duyckaerts, C, Frosch, MP, Masliah, E, Mirra, SS, Nelson, PT, Schneider, JA, Thal, DR, Trojanowski, JQ, Vinters, HV, Hyman, BT (2012) National Institute on Aging-Alzheimer鈥檚 Association guidelines for the neuropathologic assessment of Alzheimer鈥檚 disease: a practical approach. Acta Neuropathol 123: pp. 1-11 CrossRef
  22. Takahashi, T, Amano, N, Hanihara, T, Nagatomo, H, Yagishita, S, Itoh, Y, Yamaoka, K, Toda, H, Tanabe, T (1996) Corticobasal degeneration: widespread argentophilic threads and glia in addition to neurofibrillary tangles. Similarities of cytoskeletal abnormalities in corticobasal degeneration and progressive supranuclear palsy. J Neurol Sci 138: pp. 66-77 CrossRef
  23. Arima, K, Uesugi, H, Fujita, I, Sakurai, Y, Oyanagi, S, Andoh, S, Izumiyama, Y, Inose, T (1994) Corticonigral degeneration with neuronal achromasia presenting with primary progressive aphasia: ultrastructural and immunocytochemical studies. J Neurol Sci 127: pp. 186-197 CrossRef
  24. Feany, MB, Dickson, DW (1995) Widespread cytoskeletal pathology characterizes corticobasal degeneration. Am J Pathol 146: pp. 1388-1396
  25. Ksiezak-Reding, H, Morgan, K, Mattiace, LA, Davies, P, Liu, WK, Yen, SH, Weidenheim, K, Dickson, DW (1994) Ultrastructure and biochemical composition of paired helical filaments in corticobasal degeneration. Am J Pathol 145: pp. 1496-1508
  26. Mori, H, Nishimura, M, Namba, Y, Oda, M (1994) Corticobasal degeneration: a disease with widespread appearance of abnormal tau and neurofibrillary tangles, and its relation to progressive supranuclear palsy. Acta Neuropathol 88: pp. 113-121 CrossRef
  27. Lippa, CF, Smith, TW, Fontneau, N (1990) Corticonigral degeneration with neuronal achromasia. A clinicopathologic study of two cases. J Neurol Sci 98: pp. 301-310 CrossRef
  28. Wakabayashi, K, Oyanagi, K, Makifuchi, T, Ikuta, F, Homma, A, Homma, Y, Horikawa, Y, Tokiguchi, S (1994) Corticobasal degeneration: etiopathological significance of the cytoskeletal alterations. Acta Neuropathol 87: pp. 545-553 CrossRef
  29. Kato, S, Nakamura, H, Otomo, E (1989) Reappraisal of neurofibrillary tangles. Immunohistochemical, ultrastructural, and immunoelectron microscopical studies. Acta Neuropathol 77: pp. 258-266 CrossRef
  30. Lowe, J, Mirra, SS, Hyman, B, Dickson, DW Histopathology of Alzheimer鈥檚 disease. In: Love, S, Louis, DN, Ellison, DW eds. (2008) Greenfield鈥檚 neuropathology. Edward Arnold, London, pp. 1031-1152
  31. Metuzals, J, Robitaille, Y, Houghton, S, Gauthier, S, Leblanc, R (1988) Paired helical filaments and the cytoplasmic-nuclear interface in Alzheimer鈥檚 disease. J Neurocytol 17: pp. 827-833 CrossRef
  32. Hara, M, Hirokawa, K, Kamei, S, Uchihara, T (2013) Isoform transition from four-repeat to three-repeat tau underlies dendrosomatic and regional progression of neurofibrillary pathology. Acta Neuropathol 125: pp. 565-579 CrossRef
  33. Andorfer, C, Acker, CM, Kress, Y, Hof, PR, Duff, K, Davies, P (2005) Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 25: pp. 5446-5454 CrossRef
  34. Yang, Y, Geldmacher, DS, Herrup, K (2001) DNA replication precedes neuronal cell death in Alzheimer鈥檚 disease. J Neurosci 21: pp. 2661-2668
  35. Nisman, R, Dellaire, G, Ren, Y, Li, R, Bazett-Jones, DP (2004) Application of quantum dots as probes for correlative fluorescence, conventional, and energy-filtered transmission electron microscopy. J Histochem Cytochem 52: pp. 13-18 CrossRef
  36. Leapman, RD, Ornberg, RL (1988) Quantitative electron energy loss spectroscopy in biology. Ultramicroscopy 24: pp. 251-268 CrossRef
  
• 刊物主题：Neurosciences;
• 出版者：BioMed Central
• ISSN：2051-5960

文摘

Pretangles are defined under the light microscope as diffuse and granular tau immunoreactivity in neurons in tissue from patients with Alzheimer disease (AD) or corticobasal degeneration (CBD) and are considered to be a premature stage before neurofibrillary tangle formation. However, the ultrastructure of pretangles remains to be described. To clarify the similarities and differences between pretangles from patients with AD and CBD (AD-pretangles and CBD-pretangles, respectively), we examined cortical pretangles in tissue from patients with each of diseases. For direct light and electron microscopic (LM/EM) correlation of the pretangles, we used quantum dot nanocrystals (QDs) with dual fluorescent and electron-dense properties. We first identified tau-labeled pretangles on fluorescence LM and subsequently examined the same neurons on EM. Energy dispersive X-ray spectrometry (EDX) color mapping identified selenium (Se) and cadmium (Cd) as elementary components of QDs and highlighted each QD particle clearly against gray-scale EM images. With these methods, we were successful for the first time in demonstrating accurately that LM-defined pretangles are tau-positive straight filaments sparsely distributed throughout neuronal cytoplasm and neurites in both AD and CBD at the EM level. Notably, AD-pretangles showed a strong tendency to form fibrillary tangles even at an early stage, whereas pretangles or Pick-like inclusions in tissue from patients with CBD did not even at an advanced stage. In conclusion, AD-pretangles and CBD-pretangles showed essential differences at the EM level.