Skip to main content
SpringerLink
Log in

Ultrastructural localization of butyrylcholinesterase in senile plaques in the brains of aged and Alzheimer disease patients

  • Original Articles
  • Published:
Molecular and Chemical Neuropathology

Abstract

Histochemical localization of butyrylcholinesterase has been carried out in primitive, perivascular, and classic plaques in the brains of both nondemented and Alzheimer disease (AD) patients. Butyrylcholinesterase histochemistry has been compared to amyloid β-protein (AβP) immunocytochemistry in adjacent sections. In small primitive plaques, most of the butyrylcholinesterase reaction product appears ultrastructurally located over plasma membranes of healthy-looking cell processes. In more extensive primitive plaques, butyrylcholinesterase reaction product also decorates amyloid filaments, which become identifiable as delicate wisps. In classic plaques, large aggregates of butyrylcholinesterase reaction product colocalize with bundles of amyloid filaments, as well as with the compact amyloid core. Thus, deposition of butyrylcholinesterase in senile plaques follows a close parellelism with the progressive aggregation of amyloid β-protein, supporting the possibility that cholinesterases may play some role in the maturation of these structures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allsop D., Haga S. I., Haga C., Ikeda S. I., Mann D. M. A., and Ishii T. (1989) Early senile plaques in Down's syndrome brains show a close relationship with cell bodies of neurons.Neuropathol. Appl. Neurobiol. 15, 531–542.

    PubMed  CAS  Google Scholar 

  • Appleyard M. E. (1992) Secreted acetylcholinesterase: non-classical aspects of a classical enzyme.Trends Neurosci. 15, 485–490.

    Article  PubMed  CAS  Google Scholar 

  • Barrow C. J. and Zagorski M. G. (1991) Solution structures of β peptides and its constituent fragments: relation to amyloid deposition.Science 253, 179–182.

    Article  PubMed  CAS  Google Scholar 

  • Brunden K. R., Richter-Cook N. J., Chaturvedi N., and Frederickson R. C. A. (1993) pH-dependent binding of synthetic β-amyloid peptides to glycosaminoglycans.J. Neurochem. 61, 2147–2154.

    Article  PubMed  CAS  Google Scholar 

  • El Hachimi K. H., Verga L., Giaccone G., Tagliavini F., Frangione B., Bugiani O., and Foncin J-F. (1991) Relationship between non-fibrillary amyloid precursors and cell processes in the cortical neuropil of Alzheimer patients.Neurosci. Lett. 129, 119–122.

    Article  PubMed  Google Scholar 

  • Fraser P. E., Lévesque L., and McLachlan D. R. (1993) Biochemistry of Alzheimer's disease amyloid plaques.Clin. Biochem. 26, 339–349.

    Article  PubMed  CAS  Google Scholar 

  • Friede R. L. (1965) Enzyme histochemical studies of senile plaques.J. Neuropathol. Exp. Neurol. 24, 477–491.

    CAS  Google Scholar 

  • Friede R. L. (1967) A comparative histochemical mapping of the distribution of butyryl cholinesterase in the brains of four species of mammals, including man.Acta Anat. 66, 161–177.

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Ramos P. and Morán M. A. (1994) Ultrastructural localization of butyrylcholinesterase on senile plaques in aged and Alzheimer's brains.Soc. Neurosci. Abstract 20, 605.

    Google Scholar 

  • Gómez-Ramos P., Mufson E. J., and Morán M. A. (1992) Ultrastructural localization of acetylcholinesterase in neurofibrillary tangles, neuropil threads and senile plaques in aged and Alzheimer's brain.Brain Res. 569, 229–237.

    Article  PubMed  Google Scholar 

  • Greenfield S. (1984) Acetylcholinesterase may have novel functions in the brain.Trends Neurosci. 7, 364–368.

    Article  CAS  Google Scholar 

  • Haass C., Hung A. Y., and Selkoe D. N. (1991) Processing of β-amyloid precursor protein in microglia and astrocytes favors an internal localization over constitutive secretion.J. Neurosci. 11, 3783–3793.

    PubMed  CAS  Google Scholar 

  • Ikeda K., Haga C., Kosaka K., and Oyanagi S. (1989) Senile plaque-like structures: observation of a probably unknown type of senile plaque by periodicacid methenamine silver (PAM) electron microscopy.Acta Neuropathol. 78, 137–142.

    Article  PubMed  CAS  Google Scholar 

  • Ikeda S. I., Yanagisawa N., Allsop D., and Glenner G. G. (1990) Early senile plaques in Alzheimer disease demonstrated by histochemistry, immunocytochemistry and electron microscopy.Human Pathol. 21, 1221–1226.

    Article  CAS  Google Scholar 

  • Kalaria R. N., Kroon S. N., Grahovac I., and Perry G. (1992) Acetylcholinesterase and its association with heparan sulphate proteoglycans in cortical amyloid deposits of Alzheimer's Disease.Neuroscience 51, 177–184.

    Article  PubMed  CAS  Google Scholar 

  • Khachaturian Z. S. (1985) Diagnosis of Alzheimer's Disease.Arch. Neurol. 42, 1097–1105.

    PubMed  CAS  Google Scholar 

  • Kim K. S., Miller D. L, Sapienza V. J., Chen C. J., Bai C., Grundke-Iqbal I., Currie J. R., and Wisniewski H. M. (1988) Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide.Neurosci. Res. Commun. 2, 121–130.

    CAS  Google Scholar 

  • Kitamoto T., Ogomori K., Tateishi J., and Prusiner S. B. (1987) Formic acid pretreatment enhances immunostaining of cerebral and systemic amyloids.Labs. Invest. 57, 230–236.

    CAS  Google Scholar 

  • Massoulié J. and Bon S. (1982) The molecular forms of cholinesterase and acetylcholinesterase in vertebrates.Ann. Rev. Neurosci. 5, 57–106.

    Article  PubMed  Google Scholar 

  • Mesulam M-M. and Morán M. A. (1987) Cholinesterases within neurofibrillary tangles of aging and Alzheimer's disease.Ann. Neurol. 22, 223–228.

    Article  PubMed  CAS  Google Scholar 

  • Mesulam M.-M., Geula C., and Morán M. A. (1987) Anatomy of cholinesterase inhibition in Alzheimer's Disease: Effect of physostigmine and tetrahydroaminoacridine on plaques and tangles.Ann. Neurol. 22, 683–691.

    Article  PubMed  CAS  Google Scholar 

  • Miyakawa T., Katsugari S., Yamashita K., and Ohuchi K. (1992) Morphological study of amyloid fibrils and preamyloid deposits in the brain with Alzheimer's disease.Acta Neuropathol. 83, 340–346.

    Article  PubMed  CAS  Google Scholar 

  • Morán M. A., Mufson E. J., and Gómez-Ramos P. (1993) Colocalization of cholinesterases with β amyloid protein in aged and Alzheimer's brains.Acta Neuropathol. 85, 362–369.

    Article  PubMed  Google Scholar 

  • Nakamura S., Takemura M., Suenaga T., Akiguchi I., Kimura J., Yasuhara O., Kimura T., and Kitaguchi N. (1992) Occurrence of acetylcholinesterase activity closely associated with amyloid β/A4 protein is not correlated with acetylcholinesterase-positive fiber density in amygdala of Alzheimer's disease.Acta Neuropathol. 84, 425–432.

    PubMed  CAS  Google Scholar 

  • Papolla M. A., Omar R. A., Sambamurti K., Anderson J. P., and Robakis N. K. (1992) The genesis of the senile plaque. Further evidence in support of its neuronal origin.Am. J. Pathol. 141, 1151–1159.

    Google Scholar 

  • Pavlin R. (1983) Activity of total cholinesterase, butyrylcholinesterase, tyrosine hydroxylase, dopa- and glutamic acid decarboxylase within single nerve cells isolated from substantia nigra and reticular formation of man and rat.Jugoslav. Physiol. Pharmacol. Acta 19, 315–325.

    CAS  Google Scholar 

  • Powers J. M. and Skeen J. T. (1988) Ultrastructural heterogeneity in cerebral amyloid of Alzheimer's disease.Acta Neuropathol. 76, 613–623.

    Article  PubMed  CAS  Google Scholar 

  • Probst A., Langui D., Ipsen S., Robakis N., and Ulrich J. (1991) Deposition of β/A4 protein along neuronal plasma membranes in diffuse senile plaques.Acta Neuropathol. 83, 21–29.

    Article  PubMed  CAS  Google Scholar 

  • Rotundo R. L. and Carbonetto S. T. (1987) Neurons segregate clusters of membrane-bound acetylcholinesterase along their neurites.Proc. Natl. Acad. Sci. USA 84, 2063–2067.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M. L., DiDario A. G., Otvos L., Hoshi N., Kant J. A., Lee V. M-H., and Trojanowsky J. Q. (1994) Plaque-associated neuronal proteins: A recurrent motif in neuritic amyloid deposits throughout diverse cortical areas of the Alzheimer disease brain.Exp. Neurol. 130, 311–322.

    Article  PubMed  CAS  Google Scholar 

  • Selkoe D. J. (1989) Molecular pathology of amyloidogenic proteins and the role of vascular amyloidosis in Alzheimer's disease.Neurobiol. Aging 10, 387–395.

    Article  PubMed  CAS  Google Scholar 

  • Snow A. D., Mar H., Nochlin D., Kimata K., Kato M., Suzuki S., Hassell J., and Wight T. N. (1988) The presence of, heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease.Am. J. Pathol. 133, 456–463.

    PubMed  CAS  Google Scholar 

  • Snow A. D., Mar H., Nochlin D., Kresse H., and Wight T. N. (1992) Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease.J. Histochem. Cytochem. 40, 105–113.

    PubMed  CAS  Google Scholar 

  • Tagliavini F., Giaccone G., Frangione B., and Bugiani O. (1988) Preamyloid deposits in the cerebral cortex of patients with Alzheimer's disease and nondemented individuals.Neurosci. Lett. 93, 191–196.

    Article  PubMed  CAS  Google Scholar 

  • Tennent G. A., Lovat L. G., and Pepys M. B. (1995) Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis.Proc. Natl. Acad. Sci. USA 92, 4299–4303.

    Article  PubMed  CAS  Google Scholar 

  • Terry R. D. and Katzman R. (1983) Senile dementia of Alzheimer type.Ann. Neurol. 14, 497–506.

    Article  PubMed  CAS  Google Scholar 

  • Terzi E., Hölzemann G., and Seelig J. (1994) Alzheimer β-amyloid peptide 25–35: electrostatic interactions with phospholipid membranes.Biochemistry 33, 7434–7441.

    Article  PubMed  CAS  Google Scholar 

  • Ueda K., Fukui Y., and Kageyama H. (1994) Amyloid β protein-induced neuronal cell death: neurotoxic properties of aggregated amyloid β protein.Brain Res. 639, 240–244.

    Article  PubMed  CAS  Google Scholar 

  • Ulrich J., Meier-Ruge W., Probst A., Meier E., and Ipsen S. (1990) Senile plaques: staining for acetylcholinesterase and A4 protein: a comparative study in the hippocampus and entorhinal cortex.Acta Neuropathol. 80, 624–628.

    Article  PubMed  CAS  Google Scholar 

  • Wright C. I., Geula C., and Mesulam M-M. (1993) Protease inhibitors and indoleamines selectively inhibit cholinesterases in the histopathologic structures of Alzheimer disease.Proc. Natl. Acad. Sci. USA 90, 683–686.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi H., Hirai S., Morimatsu M., Shoji M., and Ihara Y. (1988a) A variety of cerebral amyloid deposits in the brains of Alzheimer-type dementia demonstrated by β-protein immunostaining.Acta Neuropathol. 76, 541–549.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi H., Hirai S., Morimatsu M., Shoji M., and Harigaya Y. (1988b) Diffuse type of senile plaques in the brains of Alzheimer-type dementia.Acta Neuropathol. 77, 113–119.

    PubMed  CAS  Google Scholar 

  • Yamaguchi H., Nakazato Y., Hirai S., Shoji M., and Harigaya Y. (1989) Electron micrograph of diffuse plaques. Initial stage of senile plaque formation in the Alzheimer brain.Am. J. Pathol. 135, 593–597.

    PubMed  CAS  Google Scholar 

  • Yamaguchi H., Nakazato Y., Hirai S., and Shoji M. (1990) Immunoelectron microscopic localization of amyloid β protein in the diffuse plaques of Alzheimertype dementia.Brain Res. 508, 320–324.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi H., Yamazaki T., Ishiguro K., Shoji M., Nakazato Y., and Hirai S. (1992) Ultrastructural localization of Alzheimer amyloid β/A4 protein precursor in the cytoplasm of neurons and senile plaque-associated astrocytes.Acta Neuropathol. 85, 15–22.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki T., Yamaguchi H., Okamoto K., and Hirai S. (1991) Ultrastructural localization of argyrophilic substances in diffuse plaques of Alzheimer-type dementia demonstrated by methenamine silver staining.Acta Neuropathol. 81, 540–545.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki T., Yamaguchi H., Nakazato Y., Ishiguro K., Kawarabayashi T., and Hirai S. (1992) Ultrastructural characterization of cerebellar diffuse plaques in Alzheimer's disease.J. Neuropathol. Exp. Neurol. 51, 281–286.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Morphology, School of Medicine, C/Arzobispo Morcillo s/n, 28029, Madrid, Spain

    Pilar Gómez-Ramos & M. A. Morán

Authors
  1. Pilar Gómez-Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Morán
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

For papers with multiple authorship, the asterisk identifies the author to whom correspondence and reprint requests should be addressed.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gómez-Ramos, P., Morán, M.A. Ultrastructural localization of butyrylcholinesterase in senile plaques in the brains of aged and Alzheimer disease patients. Molecular and Chemical Neuropathology 30, 161–173 (1997). https://doi.org/10.1007/BF02815095

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02815095

Index Entries

Search

Navigation