Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease

Neuroscience

Volumn 92, Issue 3, 1999, Pages 791-805

  Bruckner G ^a   Hausen, D ^a   Hartig W ^a   Drlicek, M ^b   Arendt, T ^a   Brauer, K ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

Author keywords

Cerebral cortex; Extracellular matrix; Human; Neurodegeneration

Indexed keywords

PROTEOGLYCAN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX; CLINICAL ARTICLE; CYTOSKELETON; FEMALE; HUMAN; HUMAN TISSUE; MALE; NERVE DEGENERATION; NEUROPATHOLOGY; PATHOGENESIS; PATHOLOGICAL ANATOMY; PRIORITY JOURNAL; TISSUE DISTRIBUTION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; CEREBRAL CORTEX; CYTOSKELETON; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MALE; MIDDLE AGED; NEUROFIBRILS; PROTEOCHONDROITIN SULFATES; REFERENCE VALUES;

EID: 0343939111     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00071-8     Document Type: Article

References (127)

1. Abel P.L., O'Brien B.J., Lia B., Olavarria J.F. Distribution of neurons projecting to the superior colliculus correlates with thick cytochrome oxidase stripes in macaque visual area V2. J. comp. Neurol. 377:1997;313-323.
2. Amitai Y. and Connors B. W. (1995) Intrinsic physiology and morphology of single neurons in neocortex. In Cerebral Cortex, Vol. 11 (eds Jones G. and Diamond I. T.), pp. 299-331. Plenum, New York.
3. Arendt T., Brückner M.K., Gertz H.J., Marcova L. Cortical distribution of neurofibrillary tangles in Alzheimer's disease matches the pattern of neurons that retain their capacity of plastic remodelling in the adult brain. Neuroscience. 83:1998;991-1002.
4. Arnold S.E., Hyman B.T., Flory J., Damasio A.R., Van Hoesen G.W. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cerebr. Cortex. 1:1991;103-116.
5. Arnold S.E., Hyman B.T., Van Hoesen G.W. Neuropathological changes of the temporal pole in Alzheimer's disease and Pick's disease. Archs Neurol. 51:1994;145-150.
6. Bancher C., Grundke-Iqbal I., Iqbal K., Fried V.A., Smith H.T., Wisniewski H.M. Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer disease. Brain Res. 539:1991;11-18.
7. Bertolotto A., Palmucci L., Gagliano A., Mongini T., Tarone G. Immunohistochemical localization of chondroitin sulfate in normal and pathological human muscle. J. neurol. Sci. 73:1986;233-244.
8. Bertolotto A., Rocca G., Cavanese G., Migheli A., Schiffer D. Chondroitin sulfate proteoglycan surrounds a subset of human and rat CNS neurons. J. Neurosci. Res. 29:1991;225-234.
9. Bignami A., Asher R., Perides G. Co-localization of hyaluronic acid and chondroitin sulphate proteoglycan in rat cerebral cortex. Brain Res. 579:1992;173-177.
10. Bignami A., Asher R., Perides G., Rahemtulla F. The extracellular matrix of cerebral gray matter: Golgi's pericellular nets and Nissl's 'nervöses Grau' revisited. Int. J. dev. Neurosci. 10:1992;291-299.
11. Braak H. (1980) Architectonics of the human telencephalic cortex. In Studies of Brain Function. (eds Braitenberg V., Barlow H. B., Bizzi E., Florey E., Grüsser O. J. and van der Loos H.), Vol. 4, pp. 1-147. Springer, Berlin.
12. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta neuropath. 82:1991;239-259.
13. Braak H., Braak E. The human entorhinal cortex: normal pathology and lamina-specific pathology in various diseases. J. Neurosci. Res. 15:1992;6-31.
14. Braak H., Braak E. Entorhinal-hippocampal interactions in mnestic disorders. Hippocampus. 3:1993;239-246.
15. Braak H., Braak E. Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta neuropath. 92:1996;197-201.
16. Braak H., Braak E., Bohl J. Stages of Alzheimer-related cortical destruction. Eur. Neurol. 33:1993;403-408.
17. Braak H., Braak E., Kalus P. Alzheimer's disease: areal and laminar pathology in the occipital cortex. Acta neuropath. 77:1989;494-506.
18. Braak H., Braak E., Yilmazer D., DeVos R.A.I., Jansen E.N.H., Bohl J. Patterns of brain destruction in Parkinson's and Alzheimer's diseases. J. neural Transm. 103:1996;455-490.
19. Brady D.R., Mufson E.J. Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseases brain. Neuroscience. 80:1997;1113-1125.
20. Brauer K., Brückner G., Leibnitz L., Werner L. Structural and cytochemical features of perineuronal glial nets in the rat brain. Acta histochem. 74:1984;53-60.
21. Brauer K., Werner L., Leibnitz L. Perineuronal nets of glia. J. Hirnforsch. 23:1982;701-708.
22. Brodmann K. (1909) Vergleichende Lokalisationslehre der Grosshirnrinde. Barth, Leipzig.
23. Brückner G., Brauer K., Härtig W., Wolff J.R., Rickmann M.J., Derouiche A., Delpech B., Girard A., Oertel W.H., Reichenbach A. Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia. 8:1993;183-200.
24. Brückner G., Bringmann A., Härtig W., Köppe G., Delpech B., Brauer K. Acute and long-lasting changes in extracellular-matrix chondroitin-sulphate proteoglycans induced by injection of chondroitinase ABC in the adult rat brain. Expl Brain Res. 121:1998;300-310.
25. Brückner G., Härtig W., Kacza J., Seeger J., Welt K., Brauer K. Extracellular matrix organization in various regions of rat brain grey matter. J. Neurocytol. 25:1996;333-346.
26. Brückner G., Härtig W., Seeger J., Rübsamen R., Reimer K., Brauer K. Cortical perineuronal nets in the gray short-tailed opossum (Monodelphis domestica): a distribution pattern contrasting with that shown in placental mammals. Anat. Embryol. 197:1998;249-262.
27. Brückner G., Seeger G., Brauer K., Härtig W., Kacza J., Bigl V. Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res. 658:1994;67-86.
28. Celio M.R., Blümcke I. Perineuronal nets - a specialized form of extracellular matrix in the adult nervous system. Brain Res. Rev. 19:1994;128-145.
29. Celio M.R., Spreafico R., De Biasi S., Vitellaro-Zuccarello L. Perineuronal nets: past and present. Trends Neurosci. 21:1998;510-515.
30. Crutcher K.A., Anderton B.H., Barger S.W., Ohm T.G., Snow A.D. Cellular and molecular pathology in Alzheimer's disease. Hippocampus. 3:1993;271-288.
31. De Lacoste M.C., White III C.L. The role of cortical connectivity in Alzheimer's disease pathogenesis: a review and model system. Neurobiol. Aging. 14:1993;1-16.
32. Delpech B., Delpech A., Brückner G., Girard N. and Maingonnat C (1989) Hyaluronan and hyaluronectin in the nervous system. In The Biology of Hyaluronan (eds Evered D. and Whelan J.), Ciba Foundation Symposium 143, pp. 208-232. Wiley, Chichester.
33. Derouiche A., Härtig W., Brauer K., Brückner G. Spatial relationship of lectin-labelled extracellular matrix and glutamine synthetase-immunoreactive astrocytes in rat cortical forebrain regions. J. Anat. 189:1996;363-372.
34. DeWitt D.A., Silver J., Canning D.R., Perry G. Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer's disease. Expl Neurol. 121:1993;149-152.
35. DeYoe E.A., Hockfield S., Garren H., Van Essen D.C. Antibody labelling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey. Vis. Neurosci. 5:1990;67-81.
36. Duong T., Gallagher K.A. Immunoreactivity patterns in neurofibrillary tangles of the inferior temporal cortex in Alzheimer's disease. Molec. chem. Neuropath. 22:1994;105-122.
37. Esiri M.M., Pearson R.C.A., Powell T.P.S. The cortex of the primary auditory area in Alzheimer's disease. Brain Res. 366:1986;385-387.
38. Ferrer I., Soriano E., Tunón T., Fonseca M., Guionnet N. Parvalbumin immunoreactive neurons in normal human temporal neocortex and in patients with Alzheimer's disease. J. neurol. Sci. 106:1991;135-141.
39. Fillit H., Leveugle B. Disorders of the extracellular matrix and the pathogenesis of senile dementia of the Alzheimer's type. Lab. Invest. 72:1995;249-253.
40. Flechsig P. (1920) Anatomie des Menschlichen Gehirns auf Myelogenetischer Grundlage. Thieme, Leipzig.
41. Gertz H.-J., Xuereb J., Huppert F., Brayne C., McGee M.A., Paykel E., Harrington C., Mukaetova-Ladinska E., Arendt T., Wischik C.M. Examination of the validity of the hierarchical model of neuropathological staging in normal aging and Alzheimer's disease. Acta neuropath. 95:1998;154-158.
42. Goedert M., Jakes R., Spillantini M.G., Hasegawa M., Smith M.J., Crowther R.A. Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature. 383:1996;550-553.
43. Goedert M., Jakes R., Vanmechelen E. Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci. Lett. 189:1995;167-170.
44. Goldman-Rakic P.S. Topography of cognition: parallel distributed networks in primate association cortex. A. Rev. Neurosci. 11:1988;137-156.
45. Gómez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 41:1997;17-24.
46. Härtig W., Brauer K., Bigl V., Brückner G. Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labeled perineuronal nets around parvalbumin-containing neurons. Brain Res. 635:1994;307-311.
47. Härtig W., Brauer K., Brückner G. Wisteria floribunda agglutinin-labeled nets surround parvalbumin-containing neurons. NeuroReport. 3:1992;869-872.
48. Hausen D., Brückner G., Drlicek M., Härtig W., Brauer K., Bigl V. Pyramidal cells ensheathed by perineuronal nets in human motor and somatosensory cortex. NeuroReport. 7:1996;1725-1729.
49. Hendry S.H.C., Jones E.G., Hockfield S., McKay R.D.G. Neuronal populations stained with the monoclonal antibody Cat-301 in the mammalian cerebral cortex and thalamus. J. Neurosci. 8:1988;518-542.
50. Hirano A., Zimmerman H.M. Alzheimer's neurofibrillary changes - a topographic study. Archs Neurol. 7:1962;227-242.
51. Hockfield S., Tootell R.B., Zaremba S. Molecular differences among neurons reveal an organization of human visual cortex. Proc. natn. Acad. Sci. U.S.A. 87:1990;3027-3031.
52. Hof P.R. Morphology and neurochemical characteristics of the vulnerable neurons in brain aging and Alzheimer's disease. Eur. Neurol. 37:1997;71-81.
53. Hof P.R., Cox K., Morrison J.H. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: I. Superior frontal and inferior temporal cortex. J. comp. Neurol. 301:1990;44-54.
54. Hof P.R., Cox K., Young W.G., Celio M.R., Rogers J., Morrison J.H. Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer's disease. J. Neuropath. exp. Neurol. 50:1991;452-462.
55. Hof P.R., Giannakopoulos P., Vickers J.C., Bouras C., Morrison J.H. The morphological and neurochemical basis of dementia: aging, hierarchical patterns of lesion distribution and vulnerable neuronal phenotype. Revs Neurosci. 6:1995;97-124.
56. Hof P.R., Morrison J.H. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: II. Primary and secondary visual cortex. J. comp. Neurol. 301:1990;55-64.
57. Hof P. R. and Morrison J. H. (1994) The cellular basis of cortical disconnection in Alzheimer disease and related dementing conditions. In Alzheimer Disease (eds Terry R. D., Katzman R. and Bick K. L.), pp. 197-229. Raven, New York.
58. Holzer M., Holzapfel H.P., Zedlick D., Brückner M.K., Arendt T. Abnormally phosphorylated tau protein in Alzheimer's disease: heterogeneity of individual regional distribution and relationship to clinical severity. Neuroscience. 63:1994;499-516.
59. Hopf A. Registration of the myeloarchitecture of the human frontal lobe with an extinction method. J. Hirnforsch. 10:1968;259-269.
60. Hopf A. Photometric studies on the myeloarchitecture of the human temporal lobe. J. Hirnforsch. 10:1968;285-297.
61. Hyman B.T., Damasio H., Damasio A.R., Van Hoesen G. Alzheimer's disease. A. Rev. Public Health. 10:1989;115-140.
62. Ikonomovic M.D., Mizukami K., Davies P., Hamilton R., Sheffield R., Armstrong D.M. The loss of GluR2(3) immunoreactivity precedes neurofibrillary tangle formation in the entorhinal cortex and hippocampus of Alzheimer brains. J. Neuropath. exp. Neurol. 56:1997;1018-1027.
63. Insausti R., Tuñon T., Sobreviela T., Insausti A.M., Gonzalo L.M. The human entorhinal cortex: a cytoarchitectonic analysis. J. comp. Neurol. 355:1995;171-198.
64. Jain N., Preuss T.M., Kaas J.H. Subdivisions of the visual system labeled with the Cat-301 antibody in tree shrews. Vis. Neurosci. 11:1994;731-741.
65. Jones E. G. (1984) Laminar distribtion of cortical efferent cells. In Cerebral Cortex (eds Peters A. and Jones E. G.), Vol. 1, pp. 521-553. Plenum, New York.
66. Kalaria R.N., Kroon S.N., Grahovac I., Perry G. Acetylcholinesterase and its association with heparan sulphate proteoglycans in cortical amyloid deposits of Alzheimer's disease. Neuroscience. 51:1992;177-184.
67. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebr. Cortex. 7:1997;476-486.
68. Khachaturian Z.S. Diagnosis of Alzheimer's disease. Archs Neurol. 42:1985;1097-1105.
69. Kitamoto T., Ogomori K., Tateishi J., Prusiner S.B. Formic acid pretreatment enhances immunostaining of cerebral and systemic amyloidosis. Lab. Invest. 57:1987;230-236.
70. Kobayashi K., Emson P.C., Mountjoy C.Q. Vicia villosa lectin-positive neurones in human cerebral cortex. Loss in Alzheimer-type dementia. Brain Res. 498:1989;170-174.
71. Kosaka T., Heizmann C.W., Fujita S.C. Monoclonal antibody 473 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Expl Brain Res. 89:1992;109-114.
72. Lander A.D. Proteoglycans in the nervous system. Curr. Opin. Neurobiol. 3:1993;716-723.
73. Lander C., Kind M., Maleski M., Hockfield S. A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J. Neurosci. 17:1997;1928-1939.
74. Lewis D.A., Campbell M.J., Terry R.D., Morrison J.H. Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices. J. Neurosci. 7:1987;1799-1808.
75. Lüth H.-J., Fischer J., Celio M.R. Soybean lectin binding neurons in the visual cortex of rat contain parvalbumin and are covered by glial nets. J. Neurocytol. 21:1992;211-221.
76. Magnus J.H., Stenstad T. Proteoglycans and the extracellular matrix in amyloidosis. Amyloid: Int. J. exp. clin. Invest. 4:1997;121-134.
77. Margolis R.U., Margolis R.K. Aggrecan-neurocan-versican family of proteoglycans. Meth. Enzym. 245:1994;105-126.
78. Margolis R.K., Rauch U., Maurel P., Margolis R.U. Neurocan and phosphacan: two major nervous tissue-specific chondroitin sulfate proteoglycans. Perspect. dev. Neurobiol. 3:1996;273-290.
79. Mattson M.P. Degenerative and protective signaling mechanisms in the neurofibrillary pathology of AD. Neurobiol. Aging. 16:1995;447-463.
80. McGuire P.K., Hockfield S., Goldman-Rakic P.S. Distribution of Cat-301 immunoreactivity in the frontal and parietal lobes of the macaque monkey. J. comp. Neurol. 288:1989;280-296.
81. Mercken M., Vandermeeren M., Lübke U., Six J., Boons J., Vanmechelen E., Van De Voorde A., Gheuens J. Affinity purification of human τ proteins and the construction of a sensitive sandwich enzyme-linked immunosorbent assay for human τ detection. J. Neurochem. 58:1992;548-553.
82. Milev P., Chiba A., Häring M., Rauvala H., Schachner M., Ranscht B., Margolis R.K., Margolis R.U. High affinity binding and overlapping localization of neurocan and phosphacan/protein-tyrosine phosphatase-ξ/β with tenascin-R, amphoterin, and the heparin-binding growth-associated molecule. J. biol. Chem. 273:1998;6998-7005.
83. Morino-Wannier P., Fujita S.C., Jones E.G. GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium binding proteins and surface antigens. Expl Brain Res. 88:1992;422-432.
84. Morrison J.H., Hof P. Life and death of neurons in the aging brain. Science. 278:1997;412-419.
85. Morrison J. H., Lewis D. A. and Campbell M. J. (1987) Distribution of neurofibrillary tangles and nonphosphorylated neurofilament protein-immunoreactive neurons in cerebral cortex: implications for loss of corticocortical circuits in Alzheimer's disease. In Molecular Neuropathology of Aging (eds Davies P. and Finch C. E.), Banbury Report, Vol. 27, pp. 109-124. Cold Spring Harbour Laboratory, New York.
86. Mulligan K.A., Van Brederode J.F.M., Hendrickson A.E. The lectin Vicia villosa labels a distinct subset of GABAergic cells in macaque visual cortex. Vis. Neurosci. 2:1989;63-72.
87. Multhaup G. Identification and regulation of the high affinity binding site of the Alzheimer's disease amyloid precursor (APP) to glycosaminoglycans. Biochimie. 76:1994;304-311.
88. Murakami T., Ohtsuka A., Taguchi T. Neurons with intensely negatively charged extracellular matrix in the human visual cortex. Archs Histol. Cytol. 57:1994;509-522.
89. Naegele J.R., Arimatsu Y., Schwartz P., Barnstable C.J. Selective staining of a subset of GABAergic neurons in cat visual cortex by monoclonal antibody VC1.1. J. Neurosci. 8:1988;79-89.
90. Naegele J.R., Barnstable C.J. Molecular determinants of GABAergic local-circuit neurons in the visual cortex. Trends Neurosci. 12:1989;28-34.
91. Nieuwenhuys R., Voogd J. and van Huijzen C. (1988) The Human Nervous System - A Synopsis and Atlas. Springer, Berlin.
92. Ojima H., Kuroda M., Ohyama J., Kishi K. Two classes of cortical neurones labelled with Vicia villosa lectin in the guinea-pig. NeuroReport. 6:1995;617-620.
93. Ojima H., Sakai M., Ohyama J. Molecular heterogeneity of Vicia villosa-recognized perineuronal nets surrounding pyramidal and nonpyramidal neurons in the guinea pig cerebral cortex. Brain Res. 786:1998;274-280.
94. Okamoto M., Mori S., Ichimura M., Endo H. Chondroitin sulfate proteoglycans protect cultured rat's cortical and hippocampal neurons from delayed cell death induced by excitatory amino acids. Neurosci. Lett. 172:1994;51-54.
95. Pangalos M.N., Shioi J., Efthimiopoulos S., Wu A.F., Robakis N.K. Characterization of appican, the chondroitin sulfate proteoglycan form of the Alzheimer amyloid precursor protein. Neurodegeneration. 5:1996;445-451.
96. Pearson R.C.A., Esiri M.M., Hiorns R.W., Wilcock G.K., Powell T.P.S. Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. Proc. natn. Acad. Sci. U.S.A. 82:1985;4531-4534.
97. Perides G., Rahemtulla F., Lane W.S., Asher R.A., Bignami A. Isolation of a large aggregating proteoglycan from human brain. J. biol. Chem. 267:1992;23,883-23,887.
98. Perlmutter L.S., Chui H.C., Saperia D., Athanikar J. Microangiography and the colocalization of heparan sulfate proteoglycan with amyloid in senile plaques of Alzheimer's disease. Brain Res. 508:1990;13-19.
99. Perry G., Siedlack S.L., Richey P. Association of heparansulfate proteoglycan with the neurofibrillary tangles of Alzheimer disease. J. Neurosci. 11:1991;3679-3683.
100. Rapoport S. I. (1987) Alzheimer's disease: phylogenetic vulnerability of associative neocortex and its connections. In Molecular Neuropathology of Aging (eds Davies P. and Finch C. E.), Banbury Report, Vol. 27, pp. 37-54. Cold Spring Harbor Laboratory, New York.
101. Rogers J., Morrison J.H. Quantitative morphology and regional and laminar distributions of senile plaques in Alzheimer's disease. J. Neurosci. 5:1985;2801-2808.
102. Rouslahti E. Brain extracellular matrix. Glycobiology. 6:1996;489-492.
103. Sampson V., Morrison J.H., Vickers J.C. The cellular basis for the relative resistance of parvalbumin and calretinin immunoreactive neocortical neurons to the pathology of Alzheimer's disease. Expl Neurol. 145:1997;295-302.
104. Saper C.B., Wainer B.H., German D.C. Axonal and transneuronal transport in the transmission of neurological disease: potential role in system degenerations, including Alzheimer's disease. Neuroscience. 23:1987;389-398.
105. Scheff S.W., Price D.A. Synapse loss in the temporal lobe in Alzheimer's disease. Ann. Neurol. 33:1993;190-199.
106. Schmidt S., Braak E., Braak H. Parvalbumin immunoreactive structures of the adult human entorhinal and transentorhinal region. Hippocampus. 3:1993;459-470.
107. Seeger G., Brauer K., Härtig W., Brückner G. Mapping of perineuronal nets in the rat brain stained by colloidal iron hydroxide histochemistry and lectin cytochemistry. Neuroscience. 58:1994;371-388.
108. Seeger G., Lüth H.-J., Winkelmann E., Brauer K. Distribution patterns of Wisteria floribunda agglutinin binding sites and parvalbumin-immunoreactive neurons in the human visual cortex: a double-labelling study. Brain Res. 3:1996;351-366.
109. Shioi J., Anderson J.P., Ripellino J.A., Robakis N.K. Chondroitin sulfate proteoglycan form of the Alzheimer's ß-amyloid precursor. J. biol. Chem. 267:1992;13,819-13,822.
110. Shioi J., Palangos M.N., Ripellino J.A., Vassilacopoulou D., Mytilineou C., Margolis R.U., Robakis N.K. The Alzheimer amyloid precursor proteoglycan (appican) is present in brain and is produced by astrocytes but not by neurons in primary neural cultures. J. biol. Chem. 270:1995;11,839-11,844.
111. Shioi J., Refolo L.M., Efthimiopoulos S., Robakis N.K. Chondroitin sulfate proteoglycan form of cellular and cell-surface Alzheimer amyloid precursor. Neurosci. Lett. 154:1993;121-124.
112. Snow A.D., Castillo G.M. Specific proteoglycans as potential causative agents and relevant targets for therapeutic intervention in Alzheimer's disease and other amyloidoses. Amyloid: Int. J. exp. clin. Invest. 4:1997;135-141.
113. Snow A.D., Mar H., Nochlin D., Kresse H., Wight T.N. Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease. J. Histochem. Cytochem. 40:1992;105-113.
114. Snow A.D., Nochlin D., Sekiguchi R., Carlson S. Identification and immunolocalization of a new class of proteoglycan (keratan sulfate) to the neuritic plaques of Alzheimer's disease. Expl Neurol. 138:1996;305-317.
115. Snow A.D., Sekiguchi R., Nochlin D., Fraser P., Kimata K., Mizutani A., Arai M., Schreier W.A., Morgan D.G. An important role of heparan sulfate proteoglycan (perlecan) in a model system for the deposition and persistence of fibrillar Aβ-amyloid in rat brain. Neuron. 12:1994;219-234.
116. Snow A.D., Wight T.N. Proteoglycans in the pathogenesis of Alzheimer's disease and other amyloidoses. Neurobiol. Aging. 10:1989;481-497.
117. Solodkin A., Van Hoesen G.W. Entorhinal cortex modules of the human brain. J. comp. Neurol. 365:1996;610-627.
118. Terry R. D., Masliah E. and Hansen L. A. (1994) Structural basis of the cognitive alterations in Alzheimer's disease. In Alzheimer disease (eds Terry R. D., Katzman R. and Bick K. L.), pp. 179-196. Raven, New York.
119. Tootell R.B., Taylor T.B. Anatomical evidence for MT and additional cortical visual areas in humans. Cerebr. Cortex. 5:1995;39-55.
120. Van Hoesen G. W. and Damasio A. R. (1987) Neural correlates of cognitive impairment in Alzheimer's disease. In: Handbook of Physiology. Section I. The Nervous System, part 5. Higher Functions of the Brain, part 2 (eds Mountcastle V. B., Plum F. and Geiger S. R.), pp. 871-898. American Physiological Society, Washington DC.
121. Van Hoesen G.W., Hyman B.T., Damasio A.R. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus. 1:1991;1-8.
122. Vermersch P., Frigard B., Delacourte A. Mapping of neurofibrillary degeneration of Alzheimer's disease: evaluation of heterogeneity using the quantification of abnormal tau proteins. Acta neuropath. 85:1992;48-54.
123. Vickers J.C. A cellular mechanism for the neuronal changes underlying Alzheimer's disease. Neuroscience. 78:1997;629-639.
124. Wintergerst E.S., Faissner A., Celio M.R. The proteoglycan DSD-1-PG occurs in perineuronal nets around parvalbumin-immunoreactive interneurons of the rat cerebral cortex. Int. J. dev. Neurosci. 14:1996;249-255.
125. Yasuhara O., Akiyama H., McGeer E., McGeer P.L. Immunohistochemical localization of hyaluronic acid in rat and human brain. Brain Res. 635:1994;269-282.
126. Zaremba S., Guimaraes A., Kalb R.G., Hockfield S. Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron. 2:1989;1207-1219.
127. Zilles K. (1990) Cortex. In The Human Nervous System (ed. Paxinos G.), pp. 757-802. Academic, San Diego.