Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement

Journal of Neuropathology and Experimental Neurology

Volumn 55, Issue 4, 1996, Pages 481-490

  Shibata, Noriyuki ^a   Hirano, Asao ^b   Kobayashi, Makio ^a   Siddique, Teepu ^c   Deng, Han Xiang ^c   Hung, Wu Yen ^c   Kato, Takeo ^d   Asayama, Kohtaro ^e  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^b MONTEFIORE MEDICAL CENTER   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d YAMAGATA UNIVERSITY   (Japan)

^e UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Anterior horn cells; Gene analysis; Immunoelectron microscopy; Immunohistochemistry; Intracytoplasmic hyaline inclusions; Superoxide dismutase

Indexed keywords

HYALIN; SUPEROXIDE DISMUTASE;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN BIOPSY; CASE REPORT; DNA DETERMINATION; HUMAN; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; NEUROFILAMENT; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0029927679     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199604000-00011     Document Type: Article

References (67)

1. Fridovich I. Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol 1986;58:61-97
2. McCord JM, Fridovich I. Superoxide dismutase: An enzymic function for erythrocuprein (hemocuprein) J Biol Chem 1969;244: 6049-55
3. Weisiger RA, Fridovich I. Superoxide dismutase: Organelle specificity. J Biol Chem 1973;248:3582-92
4. Marklund SL, Holme E, Hellner L. Superoxide dismutase in extracellular fluids Clin Chim Acta 1982;126:41-51
5. Levanon D, Lieman-Hurwitz J, Dafni N, et al. Architecture and anatomy of the chromosomal locus in human chromosome 21 encoding the Cu/Zn superoxide dismutase. EMBO J 1985;4:77-84
6. Rosen DR, Siddique T, Patterson D, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993;362:59-62
7. Deng H-X, Hentati A, Tainer JA, et al. Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 1993;261:1047-51
8. Ogasawara M, Matsubara Y, Narisawa K, et al. Mild ALS in Japan associated with novel SOD mutation. Nature Genet 1993;5:323-24
9. Aoki M, Ogasawara M, Matsubara Y, et al. Familial amyotrophic lateral sclerosis (ALS) in Japan associated with H46R mutation in Cu/Zn superoxide dismutase gene: A possible new subtype of familial ALS. J Neurol Sci 1994;126:77-83
10. Elshafey A, Lanyon WG, Connor JM. Identification of a new missense point mutation in exon 4 of the Cu/Zn superoxide dismutase (SOD-1) gene in a family with amyotrophic lateral sclerosis. Hum Mol Genet 1994;3:363-64
11. Esteban J, Rosen DR, Bowling AC, et al. Identification of two novel mutations and a new polymorphism in the gene for Cu/Zn superoxide dismutase in patients with amyotrophic lateral sclerosis. Hum Mol Genet 1994;3:997-98
12. 7 → Glu) deduced from lymphocyte mRNA sequences from Japanese patients with familial amyotrophic lateral sclerosis. Biochem Biophys Res Commun 1994;204:572-77
13. 106 → Val (CTC → GTC) mutation of superoxide dismutase-1 gene in patient with familial amyotrophic lateral sclerosis in Japan. Lancet 1994;343:1501
14. Kostrzewa M, Burck-Lehmann U, Müller U. Autosomal dominant amyotrophic lateral sclerosis: A novel mutation in the Cu/Zn superoxide dismutase-1 gene. Hum Mol Genet 1994;3:2261-62
15. Nakano R, Sato S, Inuzuka T, et al. A novel mutation in Cu/Zn superoxide dismutase gene in Japanese familial amyotrophic lateral sclerosis. Biochem Biophys Res Commun 1994;200:695-703
16. Pramatarova A, Goto J, Nanba E, et al. A two basepair delection in the SOD1 gene causes familial amyotrophic lateral sclerosis. Hum Mol Genet 1994;3:2061-62
17. Rainero I, Pinessi L, Tsuda T, et al. SOD1 missense mutation in an Italian family with ALS. Neurology 1994;44:347-49
18. Bachus R, Claus A, Megow D, et al. Cu, Zn SOD in German families with ALS. J Neurol Sci 1995;129S:93-95
19. Orrell R, De Belleroche J, Marklund S, Bowe F, Hallewell R. A novel SOD mutant and ALS. Nature 1995;374:504-5
20. Pramatarova A, Figlewicz DA, Krizus A, et al. Identification of new mutations in the Cu/Zn superoxide dismutase gene of patients with familial amyotrophic lateral sclerosis. Am J Hum Genet 1995;56:592-96
21. Deng H-X, Tainer JA, Mitsumoto H, et al. Two novel SOD1 mutations in patients with familial amyotrophic lateral sclerosis. Hum Mol Genet 1995;4:1113-16
22. Nakano I, Hirano A, Kurland LT, Mulder DW, Holley PW, Saccomanno G. Familial amyotrophic lateral sclerosis: Neuropathology of two brothers in American "C" family. Neurol Med (Tokyo) 1984;20:458-71
23. Kato T, Hirano A, Kurland LT. Asymmetric involvement of the spinal cord involving both large and small anterior horn cells in a case of familial amyotrophic lateral sclerosis. Clin Neuropathol 1987;6:67-70
24. Kurland LT, Mulder DW. Epidemiologic investigations of amyotrophic lateral sclerosis. 2. Familial aggregations indicative of dominant inheritance. Part II. Neurology 1955;5:249-68
25. Shibata N, Hirano A, Kobayashi M, et al. Immunohistochemical demonstration of Cu/Zn superoxide dismutase in the spinal cord of patients with familial amyotrophic lateral sclerosis. Acta Histochem Cytochem 1993;26:619-22
26. Hirano A, Kurland LT, Sayre GP. Familial amyotrophic lateral sclerosis: A subgroup characterized by posterior and spinocerebellar tract involvement and hyaline inclusions in the anterior horn cells. Arch Neurol 1967;16:232-A3
27. Engel WK, Kurland LT, Klatzo I. An inherited disease similar to amyotrophic lateral sclerosis with a pattern of posterior column involvement. An intermediate form? Brain 1959;82:203 20
28. Murayama S, Ookawa Y, Mori H, et al. Immunocytochemical and ultrastructural study of Lewy body-like hyaline inclusions in familial amyotrophic lateral sclerosis. Acta Neuropathol 1989;78: 143-52
29. Mizusawa H, Hirano A, Yen S-H. Anterior horn cell inclusions in familial amyotrophic lateral sclerosis contain ubiquitin and phosphorylated neurofilament epitopes. Neuropathology 1991;11:11-20
30. Takahashi H, Makifuchi T, Nakano R, et al. Familial amyotrophic lateral sclerosis with a mutation in the Cu/Zn superoxide dismutase gene. Acta Neuropathol 1994;88:185-88
31. Rechsteiner M. Ubiquitin-mediated pathways for intracellular proteolysis. Annu Rev Cell Biol 1987;3:1-30
32. Schlesinger MJ. The ubiquitin system and the heat shock response. In: Schlesinger MJ, Santoro MG, Garaci E, eds. Stress proteins. Berlin: Springer-Verlag, 1990:81-88
33. Goldstein ME, Sternberger LA, Sternberger NH. Microheterogeneity (neurotypy) of neurofilament proteins. Proc Natl Acad Sci USA 1983;80:3101-5
34. Sternberger LA, Sternberger NH. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 1983;80:6126-30
35. Asayama K, Burr IM. Joint purification of mangano and cuprozinc superoxide dismutase from a single source: A simplified method. Anal Biochem 1984;136:336-39
36. Asayama K, Janco RL, Burr IM. Selective induction of maganous superoxide dismutase in human monocytes. Am J Physiol 1985;249:C393-97
37. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 1979;76:4350-54
38. Siddique T, Pericak-Vance MA, Brooks BR, et al. Linkage analysis in familial amyotrophic lateral sclerosis. Neurology 1989;39:919-25
39. Hirano A, Nakano I, Kurland LT, Mulder DW, Holley PW, Sacco manno G. Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1984;43:471-80
40. Gurney ME, Pu H, Chiu AY, et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994;264:1772-75
41. Dal Canto MC, Gurney ME. Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am J Pathol 1994;145:1271-80
42. Matsumoto S, Mizusawa H, Yen S-H, Hirano A. Immunocytochemical study of phosphorylated neurofilaments in the anterior horn cells of amyotrophic lateral sclerosis. Neurol Med 1989;30:370-77
43. Beckman JS, Carson M, Smith CD, Koppenol WH. ALS, SOD and peroxynitrite. Nature 1993;364:584
44. Ischiropoulos H, Zhu L, Chen J, et al Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 1992;298:431-37
45. Beckman JS, Ischiropoulos H, Zhu L, et al. Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch Biochem Biophys 1992;298:438-45
46. Brady ST. Motor neurons and neurofilaments in sickness and in health. Cell 1993;73:1-3
47. Côté F, Collard J-F, Julien J-P. Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene: A mouse model of amyotrophic lateral sclerosis. Cell 1993;73:35-46
48. Xu Z, Cork LC, Griffin JW, Cleveland DW. Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell 1993;73:23-33
49. Eyer J, Peterson A. Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-β-galactosidase fusion protein. Neuron 1994;12:389-405
50. Lee MK, Marszalek JR, Cleveland DW. A mutant neurofilament subunit causes massive, selective motor neuron death: Implications for the pathogenesis of human motor neuron disease. Neuron 1994;13:975-88
51. Figlewicz DA, Krizus A, Martinoli MG. et al. Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Hum Mol Genet 1994;3:1757-61
52. Robberecht W, Sapp P, Viaene MK, et al. Cu/Zn superoxide dismutase activity in familial and sporadic amyotrophic lateral sclerosis. J Neurochem 1994;62:384-87
53. Rosen DR, Bowling AC, Patterson D, et al. A frequent ala 4 to val superoxide dismutase-1 mutation is associated with a rapidly progressive familial amyotrophic lateral sclerosis. Hum Mol Genet 1994;3:981-87
54. Garofalo O, Figlewicz DA, Thomas SM, et al. Superoxide dismutase activity in lymphoblastoid cells from motor neuron disease/ amyotrophic lateral sclerosis (MND/ALS) patients. J Neurol Sci 1995;129S:90-92
55. Borchelt DR, Lee MK, Slunt HS, et al. Superoxide dismutase-1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 1994;91:8292-96
56. Brown RH. Clinical implications of basic research: A transgenic-mousc model of amyotrophic lateral sclerosis. N Engl J Med 1994;331:1091-92
57. Rowland LP. Amyotrophic lateral sclerosis: Human challenge for neuroscience. Proc Natl Acad Sci USA 1995;92:1251-53
58. Ripps ME, Huntley GW, Hof PR, Morrison JH, Gordon JW. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 1995;92:689-93
59. Reiss U, Gershon D. Rat-liver superoxide dismutase: Purification and age-related modifications. Eur J Biochem 1976;63:617-23
60. Dovrat A, Gershon D. Rat lens superoxide dismutase and glucose 6-phosphate dehydrogenase. Studies on the catalytic activity and the fate of the enzyme antigen as a function of age. Expl Eye Res 1981;33:651-61
61. Smith CD, Carney JM, Starke-Reed PE, et al. Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci USA 1991;88:10540-43
62. Oliver CN, Ahn B, Wittenberger ME, Stadtman ER. Oxidative inactivation of enzymes: Implication in protein turnover and aging. In: Ebashi S, ed. Cellular regulation and malignant growth. Berlin. Springer-Verlag, 1985:320-31
63. Arai K, Maguchi S, Fujii S, Ishibashi H, Oikawa K, Taniguchi N Glycation and inactivation of human Cu-Zn-superoxide dismutase: Identification of the in vitro glycated sites. J Biol Chem 1987;262: 16969-72
64. Ookawara T, Kawamura N, Kitagawa Y, Tanigukchi N. Site-specific and random fragmentation of Cu,Zn-superoxide dismutase by glycation reaction: Implication of reactive oxygen species. J Biol Chem 1992;267:18505-10
65. Schalf J, Dovrat A. Superoxide dismutase molecules in human cataractous lenses. Ophthalmic Res 1986;18:332-37
66. Ogawa K, Kanematsu S, Takabe K, Asada K. Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: Detection by immuno-gold labeling after rapid freezing and substitution method. Plant Cell Physiol 1995;36:565-75
67. Shibata N, Hirano A, Kobayashi M, et al. Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis. Neurosci Lett 1994;179: 149-52