Home LiteratureArticle Details
PMID: 1713021 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Epitope map of neurofilament protein domains in cortical and peripheral nervous system Lewy bodies.

The American journal of pathology ·Vol. 139 ·No. 1 ·1991-07-00 ·Pages 53-65

Schmidt ML, Murray J, Lee VM, Hill WD, Wertkin A, Trojanowski JQ

Abstract

A subset of demented elderly patients exhibit large numbers of cortical intraneuronal inclusions similar to the neurofilament (NF)-rich Lewy bodies (LB) found in pigmented subcortical neurons of patients with Parkinson's disease (PD). Because these cortical inclusions may contribute to the emergence of cognitive impairments in afflicted individuals, the authors mapped the distribution of NF epitopes in these so-called cortical LBs. This was done using ethanol-fixed tissues and a large library of monoclonal antibodies (MAbs) with well-characterized binding specificities to various regions of each NF triplet protein. Cortical LBs were examined by light, confocal, and electron microscopy, and they were compared with the subcortical LBs of PD and LBs in the peripheral nervous system (PNS). Monoclonal antibodies specific for the rod regions of each of the three NF subunits, or for phosphate-dependent and independent antigenic sites in the tail region of the high- (NF-H) and middle- (NF-M) molecular weight (Mr) NF subunits as well as other MAbs to the extreme COOH terminus of NF-L and NF-M or the head region of NF-M labeled a variable number of cortical LBs. Remarkably one of these anti-NF MAbs, RMO32, which recognized a phosphorylated epitope in the tail region of NF-M, immunolabeled nearly all cortical LBs, whereas each of the other anti-NF MAbs never labeled more than 10% of ubiquitin- or RMO32-positive cortical LBs. Further LBs in the PNS resembled those in the central nervous system (CNS) in their immunologic properties, and LBs in both sites were dominated by filamentous aggregates at the ultrastructural level. These findings suggest that NF proteins are profoundly altered during their incorporation into cortical and PNS LBs. Further the authors here identified immunologic and ultrastructural properties common to cortical LBs, PNS LBs, and classic substantia nigra LBs in PD. The accumulation of filamentous, perikaryal inclusions rich in NF proteins at diverse sites in the CNS and PNS of patients with a variety of neurodegenerative disorders suggests a widespread disruption of NF metabolism or transport.

MeSH Terms
Aged Cerebral Cortex/immunology,ultrastructure Epitopes Humans Inclusion Bodies/immunology,ultrastructure Intermediate Filament Proteins/immunology Microscopy, Electron Nerve Degeneration Nervous System Diseases/pathology Neurofilament Proteins Peripheral Nerves/immunology,ultrastructure Reference Values
Chemicals
Epitopes Intermediate Filament Proteins Neurofilament Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Schmidt M L
Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia.
Murray J
Lee V M
Hill W D
Wertkin A
Trojanowski J Q
References (48)
48 references, click to expand
  1. Cortical Lewy body dementia: clinical features and classification.
    J Neurol Neurosurg Psychiatry. 1989 Feb;52(2):185-92 PMID: 2467966
  2. A68: a major subunit of paired helical filaments and derivatized forms of normal Tau.
    Science. 1991 Feb 8;251(4994):675-8 PMID: 1899488
  3. Diffuse Lewy body disease: light and electron microscopic immunocytochemistry of senile plaques.
    Acta Neuropathol. 1989;78(6):572-84 PMID: 2683563
  4. Epitopes that span the tau molecule are shared with paired helical filaments.
    Neuron. 1988 Nov;1(9):817-25 PMID: 2483104
  5. Alzheimer disease tangles share immunological similarities with multiphosphorylation repeats in the two large neurofilament proteins.
    Proc Natl Acad Sci U S A. 1988 Oct;85(19):7384-8 PMID: 2459703
  6. Properties of antigenic determinants that distinguish neurofibrillary tangles in progressive supranuclear palsy and Alzheimer's disease.
    Lab Invest. 1988 Oct;59(4):460-6 PMID: 2459498
  7. Parkinson's disease and dementia with neuronal inclusions in the cerebral cortex: Lewy bodies or Pick bodies.
    J Neuropathol Exp Neurol. 1988 Sep;47(5):526-35 PMID: 2845001
  8. Intraneuronal and extracellular neurofibrillary tangles exhibit mutually exclusive cytoskeletal antigens.
    Ann Neurol. 1988 Feb;23(2):184-9 PMID: 3377439
  9. Ubiquitin and microtubule-associated protein tau immunoreactivity each define distinct structures with differing distributions and solubility properties in Alzheimer brain.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2854-8 PMID: 2833758
  10. Alz-50, ubiquitin and tau immunoreactivity of neurofibrillary tangles, Pick bodies and Lewy bodies.
    J Neuropathol Exp Neurol. 1988 Jul;47(4):393-405 PMID: 2838588
  11. Analysis of epitopes shared by Hirano bodies and neurofilament proteins in normal and Alzheimer's disease hippocampus.
    Lab Invest. 1989 Apr;60(4):513-22 PMID: 2468822
  12. Monoclonal antibodies to a synthetic peptide homologous with the first 28 amino acids of Alzheimer's disease beta-protein recognize amyloid and diverse glial and neuronal cell types in the central nervous system.
    Am J Pathol. 1989 May;134(5):973-8 PMID: 2524164
  13. Diagnosis of Alzheimer's disease.
    Arch Neurol. 1985 Nov;42(11):1097-105 PMID: 2864910
  14. Dementia with cerebral Lewy bodies. A mesocortical dopaminergic defect?
    Arch Neurol. 1986 May;43(5):524-7 PMID: 3964123
  15. Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses.
    Acta Neuropathol. 1988;76(3):217-221 PMID: 2850698
  16. Ubiquitin-mediated pathways for intracellular proteolysis.
    Annu Rev Cell Biol. 1987;3:1-30 PMID: 2825735
  17. Diffuse Lewy body disease and progressive dementia.
    Neurology. 1988 Oct;38(10):1520-8 PMID: 2843793
  18. Lewy body dementia without Alzheimer changes.
    Can J Neurol Sci. 1986 Nov;13(4 Suppl):490-7 PMID: 3024794
  19. The ubiquitin pathway for the degradation of intracellular proteins.
    Prog Nucleic Acid Res Mol Biol. 1986;33:19-56, 301 PMID: 3025922
  20. Progressive supranuclear palsy with Lewy bodies.
    Acta Neuropathol. 1986;71(3-4):344-6 PMID: 3026136
  21. Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats.
    J Neurosci. 1987 Nov;7(11):3474-88 PMID: 3119789
  22. Structural similarities and differences between neurofilament proteins from five different species as revealed using monoclonal antibodies.
    J Neurosci. 1986 Aug;6(8):2179-86 PMID: 3091782
  23. Phosphate-dependent and independent neurofilament protein epitopes are expressed throughout the cell cycle in human medulloblastoma (D283 MED) cells.
    Am J Pathol. 1989 Oct;135(4):747-58 PMID: 2478022
  24. Distribution of phosphate-independent MAP2 epitopes revealed with monoclonal antibodies in microwave-denatured human nervous system tissues.
    J Neurosci Methods. 1989 Aug;29(2):171-80 PMID: 2475725
  25. An antigenic profile of Lewy bodies: immunocytochemical indication for protein phosphorylation and ubiquitination.
    J Neuropathol Exp Neurol. 1989 Jan;48(1):81-93 PMID: 2462024
  26. Identification of the major multiphosphorylation site in mammalian neurofilaments.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1998-2002 PMID: 2450354
  27. Phosphate dependent and independent neurofilament epitopes in the axonal swellings of patients with motor neuron disease and controls.
    Lab Invest. 1987 Mar;56(3):282-94 PMID: 2434727
  28. alpha-MSH and neurofilament M-protein share a continuous epitope but not extended sequences. An explanation for neurofibrillary staining with alpha-MSH antibodies.
    FEBS Lett. 1985 Feb 25;181(2):343-6 PMID: 2578984
  29. Lewy bodies in tyrosine hydroxylase-synthesizing neurons of the human cerebral cortex.
    Neurosci Lett. 1989 Nov 20;106(1-2):49-54 PMID: 2573869
  30. Anti-ubiquitin immunocytochemistry is more sensitive than conventional techniques in the detection of diffuse Lewy body disease.
    J Neurol Neurosurg Psychiatry. 1989 Jan;52(1):67-71 PMID: 2540286
  31. Distribution of tau proteins in the normal human central and peripheral nervous system.
    J Histochem Cytochem. 1989 Feb;37(2):209-15 PMID: 2492045
  32. Lewy bodies are ubiquitinated. A light and electron microscopic immunocytochemical study.
    Acta Neuropathol. 1988;75(4):345-53 PMID: 3364159
  33. Diffuse type of Lewy body disease: progressive dementia with abundant cortical Lewy bodies and senile changes of varying degree--a new disease?
    Clin Neuropathol. 1984 Sep-Oct;3(5):185-92 PMID: 6094067
  34. Diffuse Lewy body disease. Neuropathological and biochemical studies of six patients.
    Acta Neuropathol. 1987;75(1):8-15 PMID: 3434218
  35. The structure, biochemical properties, and immunogenicity of neurofilament peripheral regions are determined by phosphorylation state.
    J Biol Chem. 1985 Aug 15;260(17):9805-17 PMID: 3926771
  36. Alzheimer disease proteins (A68) share epitopes with tau but show distinct biochemical properties.
    J Neurosci Res. 1990 Mar;25(3):420-30 PMID: 1691309
  37. Senile dementia of Lewy body type. A clinically and neuropathologically distinct form of Lewy body dementia in the elderly.
    J Neurol Sci. 1990 Feb;95(2):119-39 PMID: 2157823
  38. Defined neurofilament, tau, and beta-amyloid precursor protein epitopes distinguish Alzheimer from non-Alzheimer senile plaques.
    Proc Natl Acad Sci U S A. 1990 Mar;87(6):2249-53 PMID: 1690426
  39. Dementia lacking distinctive histologic features: a common non-Alzheimer degenerative dementia.
    Neurology. 1990 Feb;40(2):251-6 PMID: 2300243
  40. Relative abundance of tau and neurofilament epitopes in hippocampal neurofibrillary tangles.
    Am J Pathol. 1990 May;136(5):1069-75 PMID: 1693468
  41. Mapping of the Alz 50 epitope in microtubule-associated proteins tau.
    J Neurosci Res. 1990 Mar;25(3):412-9 PMID: 1691308
  42. Ubiquitin immunoreactive structures in normal human brains. Distribution and developmental aspects.
    Lab Invest. 1990 Jul;63(1):87-99 PMID: 2165197
  43. An electron microscopic study on atypical presenile dementia with numerous Lewy bodies in the cerebral cortex.
    Folia Psychiatr Neurol Jpn. 1982;36(1):99-106 PMID: 6284602
  44. Lewy bodies of Parkinson's disease contain neurofilament antigens.
    Science. 1983 Sep 9;221(4615):1082-4 PMID: 6308771
  45. Lewy bodies in cerebral cortex, report of three cases.
    Acta Neuropathol. 1978 May 24;42(2):127-34 PMID: 654884
  46. Idiopathic Parkinsonism with Lewy-type inclusions in cerebral cortex. A case report.
    Acta Neuropathol. 1978 Feb 20;41(2):165-8 PMID: 205083
  47. The distribution of Lewy bodies in the central and autonomic nervous systems in idiopathic paralysis agitans.
    J Neurol Neurosurg Psychiatry. 1960 Nov;23:283-90 PMID: 13711997
  48. The presence of tau distinguishes Lewy bodies of diffuse Lewy body disease from those of idiopathic Parkinson disease.
    Neurosci Lett. 1989 May 22;100(1-3):6-10 PMID: 2548130
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
1991-07-00
Pages
53-65
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1886123
Subset
IM
Grants
NIA NIH HHS · AG-09215 · United States
NIMH NIH HHS · MH-43880 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]