Co-localization of Bunina bodies and TDP-43 inclusions in lower motor neurons in amyotrophic lateral sclerosis

Neuropathology

Volumn 34, Issue 1, 2014, Pages 71-76

  Mori, Fumiaki ^a   Kakita, Akiyoshi ^b   Takahashi, Hitoshi ^b   Wakabayashi, Koichi ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Bunina body; Cystatin C; Skein like inclusion; TDP 43

Indexed keywords

CYSTATIN C; TAR DNA BINDING PROTEIN;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BUNINA BODY; CELL INCLUSION; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; FACIAL NERVE NUCLEUS; FEMALE; HUMAN; HUMAN TISSUE; HYPOGLOSSAL NUCLEUS; MALE; MIDDLE AGED; MOTONEURON; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPINAL CORD; SPINAL CORD VENTRAL HORN; SYMPOSIUM; TDP 43 PROTEINOPATHY; VERY ELDERLY;

AMYOTROPHIC LATERAL SCLEROSIS; BUNINA BODY; CYSTATIN C; SKEIN-LIKE INCLUSION; TDP-43;

AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN STEM; DNA-BINDING PROTEINS; FEMALE; HUMANS; INCLUSION BODIES; MALE; MEDULLA OBLONGATA; MIDDLE AGED; MOTOR NEURONS; SPINAL CORD;

EID: 84892832451     PISSN: 09196544     EISSN: 14401789     Source Type: Journal    
DOI: 10.1111/neup.12044     Document Type: Article

References (33)

1. Piao YS, Wakabayashi K, Kakita A etal. Neuropathology with clinical correlations of sporadic amyotrophic lateral sclerosis: 102 autopsy cases examined between 1962 and 2000. Brain Pathol 2003; 13: 10-22.
2. Arai T, Hasegawa M, Akiyama H etal. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 2006; 351: 602-611.
3. Neumann M, Sampathu DM, Kwong LK etal. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314: 130-133.
4. Kato T, Katagiri T, Hirano A, Kawanami T, Sasaki H. Lewy body-like hyaline inclusions in sporadic motor neuron disease are ubiquitinated. Acta Neuropathol 1989; 77: 391-396.
5. Mizusawa H, Nakamura H, Wakayama I, Yen SH, Hirano A. Skein-like inclusions in the anterior horn cells in motor neuron disease. J Neurol Sci 1991; 105: 14-21.
6. Lowe J, Lennox G, Jefferson D etal. A filamentous inclusion body within anterior horn neurones in motor neurone disease defined by immunocytochemical localisation of ubiquitin. Neurosci Lett 1988; 94: 203-210.
7. Murayama S, Mori H, Ihara Y, Bouldin TW, Suzuki K, Tomonaga M. Immunocytochemical and ultrastructural studies of lower motor neurons in amyotrophic lateral sclerosis. Ann Neurol 1990; 27: 137-148.
8. Lowe J. New pathological findings in amyotrophic lateral sclerosis. J Neurol Sci 1994; 124 (Suppl): 38-51.
9. Sasaki S, Maruyama S. Ultrastructural study of skein-like inclusions in anterior horn neurons of patients with motor neuron disease. Neurosci Lett 1992; 147: 121-124.
10. Sasaki S, Maruyama S. Ultrastructural study of Bunina bodies in the anterior horn neurons of patients with amyotrophic lateral sclerosis. Neurosci Lett 1993; 154: 117-120.
11. van Welsem ME, Hogenhuis JA, Meininger V, Metsaars WP, Hauw JJ, Seilhean D. The relationship between Bunina bodies, skein-like inclusions and neuronal loss in amyotrophic lateral sclerosis. Acta Neuropathol 2002; 103: 583-589.
12. Mori F, Tanji K, Miki Y, Kakita A, Takahashi H, Wakabayashi K. Relationship between Bunina bodies and TDP-43 inclusions in spinal anterior horn in amyotrophic lateral sclerosis. Neuropathol Appl Neurobiol 2010; 36: 345-352.
13. Takahashi H, Ohama E, Ikuta F. Are Bunina bodies of endoplasmic reticulum origin? An ultrastructural study of subthalamic eosinophilic inclusions in a case of atypical motor neuron disease. Acta Pathol Jpn 1991; 41: 889-894.
14. Tomonaga M, Saito M, Yoshimura M, Shimada H, Tohgi H. Ultrastructure of the Bunina bodies in anterior horn cells of amyotrophic lateral sclerosis. Acta Neuropathol 1978; 42: 81-86.
15. Okamoto K, Hirai S, Amari M, Watanabe M, Sakurai A. Bunina bodies in amyotrophic lateral sclerosis immunostained with rabbit anti-cystatin C serum. Neurosci Lett 1993; 162: 125-128.
16. Mizuno Y, Amari M, Takatama M, Aizawa H, Mihara B, Okamoto K. Transferrin localizes in Bunina bodies in amyotrophic lateral sclerosis. Acta Neuropathol 2006; 112: 597-603.
17. Mizuno Y, Fujita Y, Takatama M, Okamoto K. Peripherin partially localizes in Bunina bodies in amyotrophic lateral sclerosis. J Neurol Sci 2011; 302: 14-18.
18. Hasegawa M, Arai T, Nonaka T etal. Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann Neurol 2008; 64: 60-70.
19. Cairns NJ, Neumann M, Bigio EH etal. TDP-43 in familial and sporadic frontotemporal lobar degeneration with ubiquitin inclusions. Am J Pathol 2007; 171: 227-240.
20. Davidson Y, Kelley T, Mackenzie IR etal. Ubiquitinated pathological lesions in frontotemporal lobar degeneration contain the TAR DNA-binding protein, TDP-43. Acta Neuropathol 2007; 113: 521-533.
21. Mackenzie IR, Bigio EH, Ince PG etal. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 2007; 61: 427-434.
22. Seelaar H, Schelhaas HJ, Azmani A etal. TDP-43 pathology in familial frontotemporal dementia and motor neuron disease without Progranulin mutations. Brain 2007; 130: 1375-1385.
23. Tan CF, Eguchi H, Tagawa A etal. TDP-43 immunoreactivity in neuronal inclusions in familial amyotrophic lateral sclerosis with or without SOD1 gene mutation. Acta Neuropathol 2007; 113: 535-542.
24. Mori F, Tanji K, Zhang HX etal. Maturation process of TDP-43-positive neuronal cytoplasmic inclusions in amyotrophic lateral sclerosis with and without dementia. Acta Neuropathol 2008; 116: 193-203.
25. Mori F, Tanji K, Kakita A, Takahashi H, Wakabayashi K. Enhancement of native and phosphorylated TDP-43 immunoreactivity by proteinase K treatment following autoclave heating. Neuropathology 2011; 31: 401-404.
26. Okamoto K, Mizuno Y, Fujita Y. Bunina bodies in amyotrophic lateral sclerosis. Neuropathology 2008; 28: 109-115.
27. Schiffer D, Autilio-Gambetti L, Chio A etal. Ubiquitin in motor neuron disease: study at the light and electron microscope. J Neuropathol Exp Neurol 1991; 50: 463-473.
28. Nycander M, Estrada S, Mort JS, Abrahamson M, Bjork I. Two-step mechanism of inhibition of cathepsin B by cystatin C due to displacement of the proteinase occluding loop. FEBS Lett 1998; 422: 61-64.
29. Mori F, Tanji K, Miki Y, Wakabayashi K. Decreased cystatin C immunoreactivity in spinal motor neurons and astrocytes in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 2009; 68: 1200-1206.
30. Zhang YJ, Xu YF, Dickey CA etal. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J Neurosci 2007; 27: 10530-10534.
31. Nonaka T, Arai T, Buratti E, Baralle FE, Akiyama H, Hasegawa M. Phosphorylated and ubiquitinated TDP-43 pathological inclusions in ALS and FTLD-U are recapitulated in SH-SY5Y cells. FEBS Lett 2009; 583: 394-400.
32. Winton MJ, Igaz LM, Wong MM, Kwong LK, Trojanowski JQ, Lee VM. Disturbance of nuclear and cytoplasmic TAR DNA-binding protein (TDP-43) induces disease-like redistribution, sequestration, and aggregate formation. J Biol Chem 2008; 283: 13302-13309.
33. Igaz LM, Kwong LK, Chen-Plotkin A etal. Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. J Biol Chem 2009; 284: 8516-8524.