Comparative study of chronic aluminum-induced neurofilamentous aggregates with intracytoplasmic inclusions of amyotrophic lateral sclerosis

Acta Neuropathologica

Volumn 92, Issue 6, 1996, Pages 545-554

  Wakayama, Ikuro ^a,b   Nerurkar, Vivek R ^b   Strong, Michael J ^c   Garruto, Ralph M ^b  

^a Kansai College of Oriental Medicine   (Japan)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Animal model; Bunina body; Immunocytochemistry; Neurofilament; Spheroid

Indexed keywords

ALUMINUM; HYALIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR HORN CELL; ARTICLE; CELL INCLUSION; CLINICAL FEATURE; COMPARATIVE STUDY; CONTROLLED STUDY; DIALYSIS ENCEPHALOPATHY; DISEASE COURSE; EOSINOPHIL; GAIT DISORDER; HINDLIMB; HYPERREFLEXIA; MOTOR NEURON DISEASE; MUSCLE ATROPHY; MUSCLE HYPERTONIA; NEURITE; NEUROFIBRILLARY TANGLE; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; RABBIT; SPINAL CORD; TONIC IMMOBILITY;

ALUMINUM; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BRAIN STEM; HUMANS; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; MICROSCOPY, ELECTRON; RABBITS; SPINAL CORD; TIME FACTORS;

EID: 0029801115     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004010050560     Document Type: Article

References (68)

1. Bergeron C, Beric-Maskarel K, Muntasser S, Weyer L, Somerville MJ, Percy ME (1994) Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J Neuropathol Exp Neurol 53: 221-230
2. Bugiani O, Ghetti B (1982) Progressing encephalomyelopathy with muscular atrophy, induced by aluminum powder. Neurobiol Aging 3: 209-222
3. Bunina TL (1962) On intracellular inclusions in familial amyotrophic lateral sclerosis. Korsakov J Neuropathol Psychiatry 62: 1293-1299
4. Chou SM (1979) Pathognomy of intraneuronal inclusions in ALS. In: Tsubaki T, Toyokura T (eds) Amyotrophic lateral sclerosis. University Park Press, Baltimore, pp 135-176
5. Cork L (1991) Hereditary canine spinal muscular atrophy: an animal model of motor neuron disease. Can J Neurol Sci 18: 432-434
6. Côté F, Collard J-F, Julien J-P (1993) Progressive neuropathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell 73: 35-46
7. Figlewicz DA, Krizus A, Martinoli MG, Meininger V, Dib M, Rouleau GA, Julien JP (1994) Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Hum Mol Genet 3: 1757-1761
8. Gajdusek DC, Salazar AM (1982) Amyotrophic lateral sclerosis and parkinsonian syndromes in high incidence among the Auyu and Jakai people in West New Guinea. Neurology 32: 107-126
9. Garruto RM (1991) Pacific paradigms of environmentally induced neurological disorders: clinical, epidemiological and molecular perspectives. Neurotoxicology 12: 347-377
10. Garruto RM (1996) Early environment, long latency and slow progression of late onset neuro-degenerative disorders. In: Henry CJK, Ulijaseek SJ (eds) Long term consequences of early environment. Cambridge University Press, Cambridge, pp 217-247
11. Garruto RM, Yase Y (1986) Neurodegenerative disorders of the western Pacific: the search for mechanisms of pathogenesis. Trends Neurosci 9: 368-374
12. Garruto RM, Yanagihara R, Gajdusek DC (1985) Disappearance of high-incidence amyotrophic lateral sclerosis and parkinsonism-dementia on Guam. Neurology 35: 193-198
13. Garruto RM, Shankar SK, Yanagihara R, Salazar AM, Amyx HL, Gajdusek DC (1989) Low-calcium, high-aluminum dietinduced motor neuron pathology in nonhuman primates. Acta Neuropathol 78: 210-219
14. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX (1994) Motor neuron degeneration in mice that express a human Cu, Zn Superoxide dismutase mutation. Science 264: 1772-1775
15. Hartmann HA, Sun DY (1992) Regional mRNA changes in brain stem motor neurons from patients with amyotrophic lateral sclerosis. Mol Chem Neuropathol 17: 249-257
16. Hiraga T, Leipold HW, Cash WC, Troyer DL (1993) Reduced numbers and intense anti-ubuquitin immunostaining of bovine motor neurons affected with spinal muscular atrophy. J Neurol Sci 118: 43-47
17. Hirano A, Donnenfeld H, Sasaki S, Nakano I (1984) Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 43: 461-470
18. Hirano A, Nakano I, Kurland LT, Mulder DW, Holley PW (1984) Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 43: 471-480
19. Kato T, Katagiri T, Hirano A, Sasaki H, Arai S (1988) Sporadic lower motor neuron disease with Lewy body-like inclusions: a new subgroup? Acta Neuropathol 76: 208-211
20. Kato T, Katagiri T, Hirano A, Kawanami T, Sasaki H (1989) Lewy body-like hyaline inclusions in sporadic motor neuron disease are ubiquitinated. Acta Neuropathol 77: 391-396
21. Kihira T, Mizusawa H, Tada J, Namikawa T, Yoshida S, Yase Y (1993) Lewy body-like inclusions in Onuf's nucleus from two cases of sporadic amyotrophic lateral sclerosis. J Neurol Sci 115: 51-57
22. Kihira T, Yoshida S, Uebayashi Y, Wakayama I, Yase Y (1994) Experimental model of motor neuron disease: oral aluminum neurotoxicity. Biomed Res 15: 27-36
23. Kihira T, Yoshida S, Komoto J, Wakayama I, Yase Y (1995) Aluminum-induced model of motor neuron degeneration: subperineural injection of aluminum in rabbits. Neurotoxicology 16:413-424
24. Klatzo I, Wisniewski H, Streicher E (1965) Experimental production of neurofibrillary degeneration. 1. Light microscopic observations. J Neuropathol Exp Neurol 24: 187-199
25. Lee MK, Marszalek JR, Cleveland DW (1994) A mutant neurofilament subunit causes massive, selective motor neuron death: implications for the pathogenesis of human motor neuron disease. Neuron 13: 975-988
26. Leigh PN, Anderton A, Dodson A (1988) Ubiquitin deposits in anterior horn cells in motor neurone diseases. Neurosci Lett 93: 197-203
27. Leigh PN, Dodson A, Swash M, Brion J-P, Anderton BH (1989) Cytoskeletal abnormalities in motor neuron disease: an immunocytochemical study. Brain 112: 521-535
28. Leigh PN, Whitwell H, Garofalo O, Buller J, Swash M, Martin JE, Gallo J-M, Weller RO, Anderton BH (1991) Ubiquitin-immunoreactive intraneuronal inclusions in amyotrophic lateral sclerosis: morphology, distribution and specificity. Brain 114: 775-788
29. Lowe J, Lennox G, Jefferson D, Morrel K, McQuire D, Gray T, Landon M, Doherty FJ, Mayer RJ (1988) A filamentous inclusion body within anterior horn neurones in motor neurone disease defined by immunocytochemical localization of ubiquitin. Neurosci Lett 94: 203-210
30. Ma W, Vacca-Galloway LL (1991) Reduced branching and length of dendrites detected in cervical spinal cord motoneurons of wobbler mouse, a model for inherited motoneuron disease. J Comp Neurol 311: 210-222
31. Manetto V, Sternberger NH, Perry G, Sternberger LA (1988) Phosphorylation of neurofilaments is altered in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 47: 642-653
32. Migheli A, Attanasio A, Schiffer D (1994) Ubiquitin and neurofilament expression in anterior horn cells in amyotrophic lateral sclerosis: possible clues to the pathogenesis. Neuropathol Appl Neurobiol 20: 282-289
33. Mizusawa H, Matsumoto S, Yen SH, Hirano A, Rojas-Corona RR, Donnenfeld H (1989) Focal accumulation of phosphorylated neurofilaments within anterior horn cell in familial amyotrophic lateral sclerosis. Acta Neuropathol 79: 37-43
34. Mizusawa H, Nakamura H, Wakayama I, Yen SHC, Hirano A (1991) Skein-like inclusions in the anterior horn cells in motor neuron disease. J Neurol Sci 105: 14-21
35. Mizusawa H, Hirano A, Yen S-H (1991) Anterior horn cell inclusions in familial amyotrophic lateral sclerosis contain ubiquitin and phosphorylated neurofilament epitopes. Neuropathology 11: 11-20
36. Mizusawa H, Koroda S, Ohama E, Tsuchiya K (1994) An immunocytochemical study of neuronal cytoplasmic inclusions in motor neuron disease. In: Yanagisawa N (ed) Annual Report of the Research Committee of the Degenerative CNS Diseases. Ministry of Health and Welfare of Japan, Tokyo, pp 192-195
37. Mohammed HO, Cummings JF, Divers TJ, Valentine B, Lahunta A de, Summers B, Farrow BRH, Trembicki-Graves K, Mauskopf A (1993) Risk factors associated with equine motor neuron disease: a possible model for human MND. Neurology 43: 966-971
38. Munoz DG, Greene C, Perl DP, Selkoe DJ (1988) Accumulation of phosphorylated neurofilaments in anterior horn motoneurons of amyotrophic lateral sclerosis patients. J Neuropathol Exp Neurol 47: 9-18
39. Murayama S, Mori H, Ihara Y, Bouldin TW, Suzuki K, Tomonaga M (1990) Immunocytochemical and ultrastructural studies of lower motor neurons in amyotrophic lateral sclerosis. Ann Neurol 27: 137-148
40. Okamoto K (1993) Bunina bodies in amyotrophic lateral sclerosis. Neurosci Lett 162: 125-128
41. Oppenheimer DR, Esiri MM (1992) Disease of the basal ganglia, cerebellum and motor neurons. In: Adams JH, Duchen LW (eds) Greenfield's neuropathology, 5th edn. Oxford University Press, New York, pp 988-1045
42. Orrell R, Belleroche J de, Marklund S, Bowe F, Hallewell R (1995) A novel SOD mutant and ALS. Nature 374: 504-505
43. Ripps ME, Huntley GW, Hof PR, Morrison JH, Gordon JW (1995) Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 92: 689-693
44. Rodgers-Johnson P, Garruto RM, Yanagihara R, Chen K-M, Gajdusek DC, Gibbs CJ Jr (1986) Amyotrophic lateral sclerosis and parkinsonism-dementia on Guam: a 30-year evaluation of clinical and neuropathological trends. Neurology 36: 7-13
45. Sasaki S, Maruyama S (1991) Immunocytochemical and ultrastructural studies of hyaline inclusions in sporadic motor neuron disease. Acta Neuropathol 82: 295-301
46. Sasaki S, Yamane K, Sakuma H, Murayama S (1989) Sporadic motor neuron disease with Lewy body-like hyaline inclusions. Acta Neuropathol 78: 555-560
47. Schmalbruch H, Jensen H-JS, Bjœrg M, Kamieniecka Z (1991) A new mouse mutant with progressive motor neuropathy. J Neuropathol Exp Neurol 50: 192-204
48. Schmidt ML, Carden MJ, Lee VM-Y, Trojanowski JQ (1987) Phosphate dependent and independent neurofilament epitopes in the axonal swellings of proteins with motor neuron disease and controls. Lab Invest 56: 282-294
49. Sobue G, Hashizume Y, Yasuda T, Mukai E, Kumagai T, Mitsuma T, Trojanowski Q (1990) Phosphorylated high molecular weight neurofilament protein in lower motor neurons in amyotrophic lateral sclerosis and other neurodegenerative diseases involving ventral horn cells. Acta Neuropathol 79: 402-408
50. Strong MJ, Garruto RM (1991) Neuron-specific thresholds of aluminum toxicity in vitro: a comparative analysis of dissociated fetal rabbit hippocampal and motor neuron-enriched cultures. Lab Invest 65: 243-249
51. Strong MJ, Garruto RM (1994) Experimental paradigms of motor neuron degeneration. In: Woodruff ML, Nonneman AJ (eds) Toxin induced models of neurological disorders. Plenum Press, New York, pp 39-88
52. Strong MJ, Yanagihara R, Wolff AV, Shankar SK, Garruto RM (1990) Experimental neurofilamentous aggregates: acute and chronic models of aluminum-induced encephalomyelopathy in rabbits. In: Rose FC, Norris FB (eds) Amyotrophic lateral sclerosis - New advances in toxicology and epidemiology. Smith-Gordon, London, pp 157-173
53. Strong MJ, Wolff AV, Wakayama I, Garruto RM (1991) Aluminum-induced chronic myelopathy in rabbits. Neurotoxicology 12: 9-22
54. Terry RD, Peña C (1965) Experimental production of neurofibrillary degeneration. 2. Electron microscopy, phosphatase histochemistry and electron probe analysis. J Neuropathol Exp Neurol 24: 200-210
55. Tomonaga M, Saito M, Yoshimura M, Shimada H, Tohgi H (1978) Ultrastructure of the Bunina bodies in anterior horn cells of amyotrophic lateral sclerosis. Acta Neuropathol (Berl) 42: 81-86
56. Uebayashi Y (1980) Epidemiological investigation of motor neuron disease in the Ku Peninsula, Japan and on Guam: the significance of long survival cases. Wakayama Med Rep 23: 13-27
57. Wakayama I (1992) Morphometry of spinal motor neurons in amyotrophic lateral sclerosis with special reference to chromatolysis and intracytoplasmic inclusion bodies. Brain Res 586: 12-18
58. Wakayama I, Nerurkar VR, Garruto RM (1992) Immunocytochemical and ultrastructural evidence of dendritic degeneration in motor neurons of aluminum-intoxicated rabbits. Acta Neuropathol 85: 122-128
59. Wisniewski H, Narkiewicz O, Wisniewski K (1967) Topography and dynamics of neurofibrillar degeneration in aluminum encephalopathy. Acta Neuropathol (Berl) 9: 127-133
60. Wisniewski HM, Sturman JA, Shek JW (1982) Chronic model of neurofibrillary changes induced in mature rabbits by metallic aluminum. Neurobiol Aging 3: 11-22
61. Wisniewski HM, Shek JW, Gruca S, Sturman JA (1984) Aluminum-induced neurofibrillary changes in axons and dendrites. Acta Neuropathol (Berl) 63: 190-197
62. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, Price DL (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14: 1105-1116
63. Xu Z, Cork LC, Griffin JW, Cleveland DW (1993) Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell 73: 23-33
64. Yamamoto T, Hirano A (1986) A comparative study of modified Bielschowsky, Bodian and thioflavin S stains on Alzheimer's neurofibrillary tangles. J Neuropathol Exp Neurol 12: 3-9
65. Yano I, Yoshida S, Uebayashi Y, Yoshimasu F, Yase Y (1989) Degenerative changes in the central nervous system of Japanese monkeys induced by oral administration aluminum salt. Biomed Res 10: 33-41
66. Yase Y (1972) The pathogenesis of amyotrophic lateral sclerosis. Lancet II: 292-296
67. Yase Y (1990) The role of metal/mineral metabolism in the amyotrophic lateral sclerosis process. The epidemiological and environmental background. In: Rose FC, Norris FH (eds) Amyotrophic lateral sclerosis - New advances in toxicology and epidemiology. Smith-Gordon, London, pp 197-203
68. Yoshida S, Kihira T, Mitani K, Wakayama I, Yase Y, Yoshida H, Iwata S (1990) Intraneuronal localization of aluminum: possible interaction with nucleic acids and pathogenic role in amyotrophic lateral sclerosis. In: Rose FC, Norris FH (eds) Amyotrophic lateral sclerosis - New advances in toxicology and epidemiology. Smith-Gordon, London, pp 211-223