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Vascular Amyloid Deposition in Alzheimer's Disease: Neither Necessary Nor Sufficient for the Local Formation of Plaques or Tangles

Vascular Amyloid Deposition in Alzheimer's Disease: Neither Necessary Nor Sufficient for the... Abstract • Objective. —To determine the relationship between vascular β-amyloid (βA4) and senile plaques (SPs) and neurofibrillary tangles (NFTs). Design. —We counted vascular amyloid deposition with SP and NFT density in the medial temporal lobe (CA1 plus the subiculum) and the cerebellum. Patients. —The brains of seven patients with Alzheimer's disease and of three age-matched nondemented control subjects were studied. Results. —In Alzheimer's disease, the density of βA4-laden blood vessels was significantly higher in the cerebellum than in CA1 plus the subiculum. Conversely, the densities of SPs and NFTs were much greater in the CA1 plus the subiculum than in the cerebellum. Conclusions. —This study indicates that local vascular βA4 deposition is not directly correlated with SP and NFT densities. Deposition of βA4 in blood vessel walls may not be instrumental in the formation of SPs and/or NFTs in the brain. References 1. Joachim CL, Mori H, Selkoe DJ. Amyloid β-protein deposition in tissues other than brain in Alzheimer's disease . Nature . 1989;341:226-230.Crossref 2. Miyakawa T, Shimoji A, Kuramoto R, Higuchi Y. The relationship between senile plaques and cerebral blood vessels in Alzheimer's disease and senile dementia . Virchows Arch [B] . 1982;40:121-129.Crossref 3. van Duinen SG, Castano EM, Prelli F, Bots GT, Luyendijk W, Frangione B. Hereditary cerebral hemorrhage with amyloidoses in patients of Dutch origin is related to Alzheimer disease . Proc Natl Acad Sci U S A . 1987;84:5991-5994.Crossref 4. Hart MN, Merz P, Bennett-Grey J, et al. Beta-amyloid protein of Alzheimer's disease is found in cerebral and spinal cord vascular malformations . Am J Pathol . 1988;132:167-172. 5. Tamaoka A, Kalaria RN, Lieberburg I, Selkoe DJ. Identification of a stable fragment of the Alzheimer amyloid precursor containing the β-protein in brain microvessels . Proc Natl Acad Sci U S A . 1992;89:1345-1349.Crossref 6. Masters CL, Multhaup G, Simms G, Pottigiesser J, Martins RN, Beyreuther K. Neuronal origin of a cerebral amyloid: neurofibrillary tangles of Alzheimer's disease contain the same protein as the amyloid of plaque cores and blood vessels . EMBO J . 1985;4:2757-2763. 7. Siman R, Card JP, Nelson RB, Davis LG. Expression of beta amyloid precursor protein in reactive astrocytes following neuronal damage . Neuron . 1989;3:275-285.Crossref 8. Wisniewski HM, Weigel J, Wang KC, Kujawa M, Lach B. Ultrastructural study of the cells forming amyloid fibers in classical plaques . Can J Neurol Sci . 1989;16:535-542. 9. Yankner BA, Dawes LR, Fisher S, Villa-Komaroff L, Oster-Granite M, Neve RL. Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease . Science . 1989;245:417-420.Crossref 10. Yankner BA, Duffy LK, Kirschner DA. Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides . Science . 1990;250:279-282.Crossref 11. Mckhann G, Drachman DA, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Health and Human services task force on Alzheimer's disease . Neurology . 1984;34:939-944.Crossref 12. Khachaturian ZS. Diagnosis of Alzheimer's disease . Arch Neurol . 1985;42:1097-1105.Crossref 13. Goudsmit J, White BJ, Weitkamp LR, Keats BJ, Morrow CH, Gajdusek DC. Familial Alzheimer's disease in two kindreds of the same geographic and ethnic origin . J Neurol Sci . 1981;49:79-89.Crossref 14. Foncin JF, Salmon D, Supino-Viterbo V, et al. Demence presenile d'Alzheimer transmise dans une famille etendue . Rev Neurol (Paris) . 1985; 141:194-202. 15. McLean IW, Nakane PK. Periodate-lysine-paraformaldehyde fixative: a new fixative for immunoelectron microscopy . J Histochem Cytochem . 1974;22:1077-1083.Crossref 16. Campbell SK, Switzer RC, Martin TL. Alzheimer's plaques and tangles: a controlled and enhanced silver staining method . Soc Neurosci Abstr . 1987;13:678. Abstract 17. Selkoe DJ, Abraham CR, Podlisny MB, Duffy LK. Isolation of low-molecular-weight proteins from amyloid plaque fibers in Alzheimer's disease . J Neurochem . 1986;46:1820-1834.Crossref 18. Joachim CL, Duffy LK, Morris LK, Selkoe DJ. Protein, chemical and immunocytochemical studies of meningovascular β-amyloid protein in Alzheimer's disease and normal aging . Brain Res . 1988;474:100-111.Crossref 19. Selkoe DJ. Amyloid protein and Alzheimer's disease . Sci Am . 1991; 265:68-71, 74-76, 78.Crossref 20. Castano EM, Frangione B. Alzheimer's disease from the perspective of the systemic and localized forms of amyloidosis . Brain Pathol . 1991;1:263-271.Crossref 21. Ikeda S, Allsop D, Glenner GG. Morphology and distribution of plaque and related deposits in the brains of Alzheimer's disease and control cases . Lab Invest . 1989;60:113-122. 22. Bergeron C, Ranalli PJ, Miceli PN. Amyloid angiopathy in Alzheimer's disease . Can J Neurol Sci . 1988;14:564-569. 23. Mountjoy CQ, Tomlinson BE, Gibson PH. Amyloid and senile plaques and cerebral blood vessels . J Neurol Sci . 1982;57:89-103.Crossref 24. Rosenblum WI, Haider A. Negative correlations between parenchymal amyloid and vascular amyloid in the hippocampus . Am J Pathol . 1988; 130:532-536. 25. Coria F, Castano EM, Frangione B. Brain amyloid in normal aging and cerebral amyloid angiopathy is antigenically related to Alzheimer's disease β-protein . Am J Pathol . 1987;129:422-428. 26. Bush A, Martins R, Rumble B, et al. The amyloid precursor protein of Alzheimer's disease is released by human platelets . J Biol Chem . 1990;265: 15977-15983. 27. Cole GM, Galasko D, Shapiro IP, Saitoh T. Stimulated platelets release amyloid β protein precursor . Biochem Biophys Res Commun . 1990;170: 288-295.Crossref 28. Gardella JE, Ghiso J, Gorgone GA, et al. Intact amyloid precursor protein (APP) is present in platelet membrane and is encoded by platelet mRNA . Biochem Biophys Res Commun . 1990;173:1292-1298.Crossref 29. Rumble B, Retallack R, Hilbich C, et al. Amyloid A4 protein and its precursor in Down's syndrome and Alzheimer's disease . N Engl J Med . 1989;320:1446-1452.Crossref 30. Mooradian AD. Effect of aging on the blood-brain barrier . Neurobiol Aging . 1988;9:31-39.Crossref 31. Mancardi GL, Perdelli F, Rivano C, Leonardi A, Bugiani O. Thickening of the basement membrane of cortical capillaries in Alzheimer's disease . Acta Neuropathol (Berl) . 1980;49:79-93.Crossref 32. Mancardi GL, Liwnicz BH, Manbybur TI. Fibrous astrocytes in Alzheimer's disease and senile dementia of Alzheimer type . Acta Neuropathol (Berl) . 1983;61:76-80.Crossref 33. Ishii T, Haga S, Shimuzu F. Identification of components of immunoglobulins in senile plaques by means of fluorescent antibody techniques . Acta Neuropathol (Berl) . 1975;32:157-162.Crossref 34. Ishii T, Haga S. Immunoelectron microscopic localization of immunoglobulins in amyloid fibrils of senile plaques . Acta Neuropathol (Berl) . 1976;36:243-249.Crossref 35. Probst A, Heitz PU, Ulrich J. Histochemical analysis of senile plaque amyloid and amyloid angiopathy . Virchows Arch [A] . 1980;388:327-334.Crossref 36. Powers JM, Schlaepfer WW, Willingham MC, Hall BJ. An immunoperoxidase study of senile cerebral amyloidosis with pathogenic considerations . J Neuropathol Exp Neurol . 1981;40:592-612.Crossref 37. Torack RN, Lynch RG. Cytochemistry of brain amyloid in adult dementia . Acta Neuropathol (Berl) . 1981;53:189-196.Crossref 38. Wisniewski HM, Kozlowski PB. Evidence for blood-brain barrier changes in senile dementia of the Alzheimer type (SDAT) . Ann N Y Acad Sci . 1982;396:119-129.Crossref 39. Eikelenboom P, Stam FC. An immunohistochemical study on cerebral vascular and senile plaque amyloid in Alzheimer's dementia . Virchows Arch [B] . 1984;47:17-25.Crossref 40. Selkoe DJ, Podlisny MB, Joachim CL, Vickers EA, Lee G, Oitersorf T. Beta-amyloid precursor protein of Alzheimer's disease occurs as 110- to 135-kilodalton membrane-associated proteins in neural and nonneural tissues . Proc Natl Acad Sci USA . 1988;85:7341-7345.Crossref 41. Tagliavini F, Ghiso J, Timmers WF, Giaccone G, Bugiani O, Frangione B. Coexistence of Alzheimer's amyloid precursor protein and amyloid protein in cerebral vessel walls . Lab Invest . 1990;62:761-767. 42. Kawai M, Kalaria RN, Harik S, Perry G. The relationship of amyloid plaques to cerebral capillaries in Alzheimer's disease . Am J Pathol . 1990; 137:1435-1446. 43. Luthert PJ, Williams JA. A quantitative study of the coincidence of blood vessels and A4 protein deposits in Alzheimer's disease . Neurosci Lett . 1991;126:110-112.Crossref 44. Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular protein . Biochem Biophys Res Commun . 1984;120:885-890.Crossref 45. Prelli F, Castano E, Glenner GG, Frangione B. Differences between vascular and plaque core amyloid in Alzheimer's disease . J Neurochem . 1988;51:648-651.Crossref 46. Miller DL, Potempska A, Papayannopoulos IA, et al. Characterization of the cerebral amyloid peptides and their precursors . J Neuropathol Exp Neurol . 1990;49:267. Abstract.Crossref 47. Joachim CL, Selkoe DJ. The seminal role of β-amyloid in the pathogenesis of Alzheimer's disease . Alzheimer Dis Related Disord . 1992;6:7-34.Crossref 48. Kang J, Lemaire HG, Unterbeck A, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor . Nature . 1987; 325:733-736.Crossref 49. Probst A, Langui D, Ipsen S, Robakis N. Deposition of beta/A44 protein along neuronal plasma membranes in diffuse senile plaques . Acta Neuropathol (Berl) . 1991;83:21-29.Crossref 50. Cras P, Kawai M, Lowery D, Gonzalez-DeWhitt P, Greenberg B, Perry G. Senile plaque neurites in Alzheimer disease accumulate amyloid precursor protein . Proc Natl Acad Sci U S A . 1991;88:7552-7556.Crossref 51. Lewis DA, Higgins GA, Young WG, et al. Distribution of precursor amyloid β protein messenger RNA in human cerebral cortex: relationship to neurofibrillary tangles and blood vessels . Proc Natl Acad Sci U S A . 1988; 85:1691-1695.Crossref 52. Kosik KS. Alzheimer's disease: a cell biological perspective . Science . 1992;256:780-783.Crossref 53. Schmechel DE, Goldgaber D, Burkhart DS, Gilbert JR, Gadjusek DC, Roses AD. Cellular localization of messenger RNA encoding amyloid-beta-protein in normal tissue and in Alzheimer disease . Alzheimer Dis Related Disord . 1988;2:96-111.Crossref 54. Mita S, Schon EA, Herbert J. Widespread expression of amyloid beta-protein precursor gene in rat brain . Am J Pathol . 1989;134:1253-1261. 55. Cras P, Kawai M, Siedlak S, et al. Neuronal and microglial involvement in β-amyloid protein deposition in Alzheimer's disease . Am J Pathol . 1990; 137:241-246. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Neurology American Medical Association

Vascular Amyloid Deposition in Alzheimer's Disease: Neither Necessary Nor Sufficient for the Local Formation of Plaques or Tangles

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Publisher
American Medical Association
Copyright
Copyright © 1993 American Medical Association. All Rights Reserved.
ISSN
0003-9942
eISSN
1538-3687
DOI
10.1001/archneur.1993.00540100073019
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Abstract

Abstract • Objective. —To determine the relationship between vascular β-amyloid (βA4) and senile plaques (SPs) and neurofibrillary tangles (NFTs). Design. —We counted vascular amyloid deposition with SP and NFT density in the medial temporal lobe (CA1 plus the subiculum) and the cerebellum. Patients. —The brains of seven patients with Alzheimer's disease and of three age-matched nondemented control subjects were studied. Results. —In Alzheimer's disease, the density of βA4-laden blood vessels was significantly higher in the cerebellum than in CA1 plus the subiculum. Conversely, the densities of SPs and NFTs were much greater in the CA1 plus the subiculum than in the cerebellum. Conclusions. —This study indicates that local vascular βA4 deposition is not directly correlated with SP and NFT densities. Deposition of βA4 in blood vessel walls may not be instrumental in the formation of SPs and/or NFTs in the brain. References 1. Joachim CL, Mori H, Selkoe DJ. Amyloid β-protein deposition in tissues other than brain in Alzheimer's disease . Nature . 1989;341:226-230.Crossref 2. Miyakawa T, Shimoji A, Kuramoto R, Higuchi Y. The relationship between senile plaques and cerebral blood vessels in Alzheimer's disease and senile dementia . Virchows Arch [B] . 1982;40:121-129.Crossref 3. van Duinen SG, Castano EM, Prelli F, Bots GT, Luyendijk W, Frangione B. Hereditary cerebral hemorrhage with amyloidoses in patients of Dutch origin is related to Alzheimer disease . Proc Natl Acad Sci U S A . 1987;84:5991-5994.Crossref 4. Hart MN, Merz P, Bennett-Grey J, et al. Beta-amyloid protein of Alzheimer's disease is found in cerebral and spinal cord vascular malformations . Am J Pathol . 1988;132:167-172. 5. Tamaoka A, Kalaria RN, Lieberburg I, Selkoe DJ. Identification of a stable fragment of the Alzheimer amyloid precursor containing the β-protein in brain microvessels . Proc Natl Acad Sci U S A . 1992;89:1345-1349.Crossref 6. Masters CL, Multhaup G, Simms G, Pottigiesser J, Martins RN, Beyreuther K. Neuronal origin of a cerebral amyloid: neurofibrillary tangles of Alzheimer's disease contain the same protein as the amyloid of plaque cores and blood vessels . EMBO J . 1985;4:2757-2763. 7. Siman R, Card JP, Nelson RB, Davis LG. Expression of beta amyloid precursor protein in reactive astrocytes following neuronal damage . Neuron . 1989;3:275-285.Crossref 8. Wisniewski HM, Weigel J, Wang KC, Kujawa M, Lach B. Ultrastructural study of the cells forming amyloid fibers in classical plaques . Can J Neurol Sci . 1989;16:535-542. 9. Yankner BA, Dawes LR, Fisher S, Villa-Komaroff L, Oster-Granite M, Neve RL. Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease . Science . 1989;245:417-420.Crossref 10. Yankner BA, Duffy LK, Kirschner DA. Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides . Science . 1990;250:279-282.Crossref 11. Mckhann G, Drachman DA, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Health and Human services task force on Alzheimer's disease . Neurology . 1984;34:939-944.Crossref 12. Khachaturian ZS. Diagnosis of Alzheimer's disease . Arch Neurol . 1985;42:1097-1105.Crossref 13. Goudsmit J, White BJ, Weitkamp LR, Keats BJ, Morrow CH, Gajdusek DC. Familial Alzheimer's disease in two kindreds of the same geographic and ethnic origin . J Neurol Sci . 1981;49:79-89.Crossref 14. Foncin JF, Salmon D, Supino-Viterbo V, et al. Demence presenile d'Alzheimer transmise dans une famille etendue . Rev Neurol (Paris) . 1985; 141:194-202. 15. McLean IW, Nakane PK. Periodate-lysine-paraformaldehyde fixative: a new fixative for immunoelectron microscopy . J Histochem Cytochem . 1974;22:1077-1083.Crossref 16. Campbell SK, Switzer RC, Martin TL. Alzheimer's plaques and tangles: a controlled and enhanced silver staining method . Soc Neurosci Abstr . 1987;13:678. Abstract 17. Selkoe DJ, Abraham CR, Podlisny MB, Duffy LK. Isolation of low-molecular-weight proteins from amyloid plaque fibers in Alzheimer's disease . J Neurochem . 1986;46:1820-1834.Crossref 18. Joachim CL, Duffy LK, Morris LK, Selkoe DJ. Protein, chemical and immunocytochemical studies of meningovascular β-amyloid protein in Alzheimer's disease and normal aging . Brain Res . 1988;474:100-111.Crossref 19. Selkoe DJ. Amyloid protein and Alzheimer's disease . Sci Am . 1991; 265:68-71, 74-76, 78.Crossref 20. Castano EM, Frangione B. Alzheimer's disease from the perspective of the systemic and localized forms of amyloidosis . Brain Pathol . 1991;1:263-271.Crossref 21. Ikeda S, Allsop D, Glenner GG. Morphology and distribution of plaque and related deposits in the brains of Alzheimer's disease and control cases . Lab Invest . 1989;60:113-122. 22. Bergeron C, Ranalli PJ, Miceli PN. Amyloid angiopathy in Alzheimer's disease . Can J Neurol Sci . 1988;14:564-569. 23. Mountjoy CQ, Tomlinson BE, Gibson PH. Amyloid and senile plaques and cerebral blood vessels . J Neurol Sci . 1982;57:89-103.Crossref 24. Rosenblum WI, Haider A. Negative correlations between parenchymal amyloid and vascular amyloid in the hippocampus . Am J Pathol . 1988; 130:532-536. 25. Coria F, Castano EM, Frangione B. Brain amyloid in normal aging and cerebral amyloid angiopathy is antigenically related to Alzheimer's disease β-protein . Am J Pathol . 1987;129:422-428. 26. Bush A, Martins R, Rumble B, et al. The amyloid precursor protein of Alzheimer's disease is released by human platelets . J Biol Chem . 1990;265: 15977-15983. 27. Cole GM, Galasko D, Shapiro IP, Saitoh T. Stimulated platelets release amyloid β protein precursor . Biochem Biophys Res Commun . 1990;170: 288-295.Crossref 28. Gardella JE, Ghiso J, Gorgone GA, et al. Intact amyloid precursor protein (APP) is present in platelet membrane and is encoded by platelet mRNA . Biochem Biophys Res Commun . 1990;173:1292-1298.Crossref 29. Rumble B, Retallack R, Hilbich C, et al. Amyloid A4 protein and its precursor in Down's syndrome and Alzheimer's disease . N Engl J Med . 1989;320:1446-1452.Crossref 30. Mooradian AD. Effect of aging on the blood-brain barrier . Neurobiol Aging . 1988;9:31-39.Crossref 31. Mancardi GL, Perdelli F, Rivano C, Leonardi A, Bugiani O. Thickening of the basement membrane of cortical capillaries in Alzheimer's disease . Acta Neuropathol (Berl) . 1980;49:79-93.Crossref 32. Mancardi GL, Liwnicz BH, Manbybur TI. Fibrous astrocytes in Alzheimer's disease and senile dementia of Alzheimer type . Acta Neuropathol (Berl) . 1983;61:76-80.Crossref 33. Ishii T, Haga S, Shimuzu F. Identification of components of immunoglobulins in senile plaques by means of fluorescent antibody techniques . Acta Neuropathol (Berl) . 1975;32:157-162.Crossref 34. Ishii T, Haga S. Immunoelectron microscopic localization of immunoglobulins in amyloid fibrils of senile plaques . Acta Neuropathol (Berl) . 1976;36:243-249.Crossref 35. Probst A, Heitz PU, Ulrich J. Histochemical analysis of senile plaque amyloid and amyloid angiopathy . Virchows Arch [A] . 1980;388:327-334.Crossref 36. Powers JM, Schlaepfer WW, Willingham MC, Hall BJ. An immunoperoxidase study of senile cerebral amyloidosis with pathogenic considerations . J Neuropathol Exp Neurol . 1981;40:592-612.Crossref 37. Torack RN, Lynch RG. Cytochemistry of brain amyloid in adult dementia . Acta Neuropathol (Berl) . 1981;53:189-196.Crossref 38. Wisniewski HM, Kozlowski PB. Evidence for blood-brain barrier changes in senile dementia of the Alzheimer type (SDAT) . Ann N Y Acad Sci . 1982;396:119-129.Crossref 39. Eikelenboom P, Stam FC. An immunohistochemical study on cerebral vascular and senile plaque amyloid in Alzheimer's dementia . Virchows Arch [B] . 1984;47:17-25.Crossref 40. Selkoe DJ, Podlisny MB, Joachim CL, Vickers EA, Lee G, Oitersorf T. Beta-amyloid precursor protein of Alzheimer's disease occurs as 110- to 135-kilodalton membrane-associated proteins in neural and nonneural tissues . Proc Natl Acad Sci USA . 1988;85:7341-7345.Crossref 41. Tagliavini F, Ghiso J, Timmers WF, Giaccone G, Bugiani O, Frangione B. Coexistence of Alzheimer's amyloid precursor protein and amyloid protein in cerebral vessel walls . Lab Invest . 1990;62:761-767. 42. Kawai M, Kalaria RN, Harik S, Perry G. The relationship of amyloid plaques to cerebral capillaries in Alzheimer's disease . Am J Pathol . 1990; 137:1435-1446. 43. Luthert PJ, Williams JA. A quantitative study of the coincidence of blood vessels and A4 protein deposits in Alzheimer's disease . Neurosci Lett . 1991;126:110-112.Crossref 44. Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular protein . Biochem Biophys Res Commun . 1984;120:885-890.Crossref 45. Prelli F, Castano E, Glenner GG, Frangione B. Differences between vascular and plaque core amyloid in Alzheimer's disease . J Neurochem . 1988;51:648-651.Crossref 46. Miller DL, Potempska A, Papayannopoulos IA, et al. Characterization of the cerebral amyloid peptides and their precursors . J Neuropathol Exp Neurol . 1990;49:267. Abstract.Crossref 47. Joachim CL, Selkoe DJ. The seminal role of β-amyloid in the pathogenesis of Alzheimer's disease . Alzheimer Dis Related Disord . 1992;6:7-34.Crossref 48. Kang J, Lemaire HG, Unterbeck A, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor . Nature . 1987; 325:733-736.Crossref 49. Probst A, Langui D, Ipsen S, Robakis N. Deposition of beta/A44 protein along neuronal plasma membranes in diffuse senile plaques . Acta Neuropathol (Berl) . 1991;83:21-29.Crossref 50. Cras P, Kawai M, Lowery D, Gonzalez-DeWhitt P, Greenberg B, Perry G. Senile plaque neurites in Alzheimer disease accumulate amyloid precursor protein . Proc Natl Acad Sci U S A . 1991;88:7552-7556.Crossref 51. Lewis DA, Higgins GA, Young WG, et al. Distribution of precursor amyloid β protein messenger RNA in human cerebral cortex: relationship to neurofibrillary tangles and blood vessels . Proc Natl Acad Sci U S A . 1988; 85:1691-1695.Crossref 52. Kosik KS. Alzheimer's disease: a cell biological perspective . Science . 1992;256:780-783.Crossref 53. Schmechel DE, Goldgaber D, Burkhart DS, Gilbert JR, Gadjusek DC, Roses AD. Cellular localization of messenger RNA encoding amyloid-beta-protein in normal tissue and in Alzheimer disease . Alzheimer Dis Related Disord . 1988;2:96-111.Crossref 54. Mita S, Schon EA, Herbert J. Widespread expression of amyloid beta-protein precursor gene in rat brain . Am J Pathol . 1989;134:1253-1261. 55. Cras P, Kawai M, Siedlak S, et al. Neuronal and microglial involvement in β-amyloid protein deposition in Alzheimer's disease . Am J Pathol . 1990; 137:241-246.

Journal

Archives of NeurologyAmerican Medical Association

Published: Oct 1, 1993

References