Fibrillar β-amyloid induces microglial phagocytosis, expression of inducible nitric oxide synthase, and loss of a select population of neurons in the rat CNS in vivo

Journal of Neuroscience

Volumn 18, Issue 6, 1998, Pages 2161-2173

  Weldon, Derik T ^a   Rogers, Scott D ^b   Ghilardi, Joseph R ^b   Finke, Matthew P ^b   Cleary, James P ^b,c   O'Hare, Eugene ^b,c   Esler, William P ^d   Maggio, John E ^d   Mantyh, Patrick W ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Alzheimer's disease; Astrocyte; Glia; Inducible nitric oxide synthase; Microgila; Neurotoxicity; Nitric oxide synthase

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; NITRIC OXIDE SYNTHASE;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL POPULATION; COGNITIVE DEFECT; CONTROLLED STUDY; DEMENTIA; ENZYME INDUCTION; MALE; MICROGLIA; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN STABILITY; RAT;

EID: 0032521111     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-06-02161.1998     Document Type: Article

References (87)

1. Adamson DC, Wildemann B, Sasaki M, Glass JD, McArthur JC, Christov VI, Dawson TM, Dawson VL (1996) Immunologic NO synthase-elevation in severe AIDS dementia and induction by HIV-1 Gp41. Science 274:1917-1921.
2. Akiyama H, Schwab C, Kondo H, Mori H. Kametani F, Ikeda K, McGeer PL (1996) Granules in glial cells of patients with Alzheimer's disease arc immunopositive for C-terminal sequences of beta-amyloid protein. Neurosci Lett 206:169-172.
3. Ard MD, Cole GM, Wei J, Mehrle AP, Fratkin JD (1996) Scavenging of Alzheimer's amyloid beta-protein by microglia in culture. J Neurosci Res 43:190-202.
4. Barron KD (1995) The microglial cell. A historical review. J Neurol Sci 134:57-68.
5. Bennett BD, Bolam JP (1993) Two populations of calbindin D28k-immunoreactive neurones in the striatum of the rat. Brain Res 610:305-310.
6. Benson JR, Louie PC, Bradshaw RA (1981) Amino acid analysis of peptides. In: The peptides, Vol 4 (Gross E, Mienhofer J, eds), pp 217-260. New York: Academic.
7. Bo L, Dawson TM, Wesselingh S, Mork S, Choi S, Kong PA, Hanley D, Trapp BD (1994) Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann Neurol 36:778-786.
8. Boje KM, Arora PK (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res 587:250-256.
9. Brelje TC, Wessendorf M, Sorenson RL (1993) Multicolor laser scanning confocal immunofluorescence microscopy: practical application and limitations. In: Methods in cell biology, Vol 38 (Matsumoto B, ed), pp 97-181. San Diego: Academic.
10. Brosnan CF, Battistini L, Raine CS, Dickson DW, Casadevall A, Lee SC (1994) Reactive nitrogen intermediates in human neuropathology: an overview. Dev Neurosci 16:152-161.
11. Busciglio J, Gabuzda DH, Matsudaira P, Yankner BA (1993) Generation of beta-amyloid in the secretory pathway in neuronal and nonneuronal cells. Proc Natl Acad Sci USA 90:2092-2096.
12. Bush AI, Pettingell WH, Multhaup G, Paradis M, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, Tanzi RE (1994) Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 265:1464-1467.
13. Canning DR, McKeon RJ, DeWitt DA, Perry G, Wujek JR, Frederickson RC, Silver J (1993) Beta-amyloid of Alzheimer s disease induces reactive gliosis that inhibits axonal outgrowth. Exp Neurol 124:289-298.
14. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, Seubert P, Vigo-Pelfrey C, Lieberburg I, Selkoe DJ (1992) Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360:672-674.
15. Cummings BJ, Cotman CW (1995) Image analysis of beta-amyloid load in Alzheimer's disease and relation to dementia severity. Lancet 346:1524-1528.
16. DeWitt DA, Silver J (1996) Regenerative failure: a potential mechanism for neuritic dystrophy in Alzheimer's disease. Exp Neurol 142:103-110.
17. Dickson DW, Ksiezak-Reding H, Liu WK, Davies P, Crowe A, Yen SH (1992) Immunocytochemistry of neurofibrillary tangles with antibodies to subregions of tau protein: identification of hidden and cleaved tau epitopes and a new phosphorylation site. Acta Neuropathol (Berl) 84:596-605.
18. Eddleston M, Mucke L (1993) Molecular profile of reactive astrocytes-implications for their role in neurologic disease. Neuroscience 54:15-36.
19. El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD (1996) Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 382:716-719.
20. Esler WP, Stimson ER, Jennings JM, Ghilardi JR, Mantyh PW, Maggio JE (1996) Zinc-induced aggregation of human and rat beta-amyloid peptides in vitro. J Neurochem 66:723-732.
21. Esler WP, Stimson ER, Ghilardi JR, Felix AM, Lu Y, Vinters HV, Mantyh PW, Maggio JE (1997) A-beta deposition inhibitor screen using synthetic amyloid. Nature Biotech 15:258-263.
22. Evans KC, Berger EP, Cho CG, Weisgraber KH, Lansbury Jr PT (1995) Apolipoprotein E is a kinetic but not a thermodynamic inhibitor of amyloid formation: implications for the pathogenesis and treatment of Alzheimer disease. Proc Natl Acad Sci USA 92:763-767.
23. Ferrer I, Tunon T, Soriano E, del Rio A, Iraizoz I, Fonseca M, Guionnet N (1993) Calbindin D-28k immunoreactivity in the temporal neocortex in patients with Alzheimer's disease. Clin Neuropathol 12:53-58.
24. Frackowiak J, Wisniewski HM, Wegiel J, Merz GS, Iqbal K, Wang KC (1992) Ultrastructure of the microglia that phagocytose amyloid and the microglia that produce beta-amyloid fibrils. Acta Neuropathol (Berl) 84:225-233.
25. Fraser PE, Nguyen JT, Chin DT, Kirschner DA (1992) Effects of sulfate ions on Alzheimer beta/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions. J Neurochem 59:1531-1540.
26. Frautschy SA, Cole GM, Baird A (1992) Phagocytosis and deposition of vascular beta-amyloid in rat brains injected with Alzheimer beta-amyloid. Am J Pathol 140:1389-1399.
27. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyder B, Soriano F, Tan H, Vitale J, Wadsworth S, Wolozin B, Zhao J (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527.
28. Giovannelli L, Casamenti F, Scali C, Bartolini L, Pepeu G (1995) Differential effects of amyloid peptides β-(1-40) and β-(25-35) injections into the rat nucleus basalis. Neuroscience 66:781-792.
29. Giulian D, Haverkamp LJ, Li J, Karshin WL, Yu J, Tom D, Li X, Kirkpatrick JB (1995) Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer brain. Neurochem Int 27:119-137.
30. Giulian D, Haverkamp LJ, Yu JH, Karshin W, Tom D, Li J, Kirkpatrick J, Kuo YM, Roher AE (1996) Specific domains of beta-amyloid from Alzheimer plaques elicit neuron killing in human microglia. J Neurosci 16:6021-6037.
31. Glenner GG, Wong CW (1984) Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122:1131-1135.
32. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L, Mant R, Newton P, Rooke K, Roques P, Talbot C, Pericak-Vance M, Roses A, Williamson R, Rossor M, Owen M, Hardy J (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-706.
33. Goodwin JL, Uemura E, Cunnick JE (1995) Microglial release of nitric oxide by the synergistic action of beta-amyloid and IFN-gamma. Brain Res 692:207-214.
34. Gramsbergen JB, van den Berg KJ (1994) Regional and temporal profiles of calcium accumulation and glial fibrillary acidic protein levels in rat brain after systemic injection of kainic acid. Brain Res 667:216-228.
35. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, Ostaszewski BL, Lieberburg I, Koo EH, Schenk D, Teplow DB, Selkoe DJ (1992) Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 359:322-325.
36. Haga S, Ikeda K, Sato M, Ishii T (1993) Synthetic Alzheimer amyloid beta/A4 peptides enhance production of complement C3 component by cultured microglial cells. Brain Res 601:88-94.
37. Harrigan MR, Kunkel DD, Nguyen LB, Malouf AT (1995) Beta amyloid is neurotoxic in hippocampal slice cultures. Neurobiol Aging 16:779-789.
38. Ishii T, Haga S (1992) Complements, microglial cells and amyloid fibril formation. Res Immunol 143:614-616.
39. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 24:173-182.
40. Jarrett JT, Lansbury Jr PT (1992) Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 31:12345-12352.
41. Jarrett JT, Lansbury Jr PT (1993) Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73:1055-1058.
42. Jarrett JT, Berger EP, Lansbury Jr PT (1993) The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32:4693-4697.
43. Jarrett JT, Costa PR, Griffin RG, Lansbury Jr PT (1994) Models of the beta protein C-terminus: differences in amyloid structure may lead to segregation of "long" and "short" fibrils. J Am Chem Soc 116:9741-9742.
44. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, Multhaup G, Beyreuther K, Muller-Hill B (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325:733-736.
45. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
46. Kelly JF, Furukawa K, Barger SW, Rengen MR, Mark RJ, Blanc EM, Roth GS, Mattson MP (1996) Amyloid beta-peptide disrupts carbachol-induced muscarinic cholinergic signal transduction in cortical neurons. Proc Natl Acad Sci USA 93:6753-6758.
47. Kennedy WR, Wendelschafer-Crabb G, Brelje TC (1994) Innervation and vasculature of human sweat glands: an immunohistochemistry-laser scanning confocal fluorescence microscopy study. J Neurosci 14:6825-6833.
48. Kirschner DA, Abraham C, Selkoe DJ (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation. Proc Natl Acad Sci USA 83:503-507.
49. Kirschner DA, Inouye H, Duffy LK, Sinclair A, Lind M, Selkoe DJ (1987) Synthetic peptide homologous to beta protein from Alzheimer disease forms amyloid-like fibrils in vitro. Proc Natl Acad Sci USA 84:6953-6957.
50. Klegeris A, Walker DG, McGeer PL (1994) Activation of macrophages by Alzheimer beta amyloid peptide. Biochem Biophys Res Commun 199:984-991.
51. Koh JY, Yang LL, Cotman CW (1990) Beta-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res 533:315-320.
52. Ma J, Yee A, Brewer Jr HB, Das S, Potter H (1994) Amyloid-associated proteins alpha 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer beta-protein into filaments. Nature 372:92-94.
53. Mantyh PW, Ghilardi JR, Rogers S, DeMaster E, Allen CJ, Stimson ER, Maggio JE (1993) Aluminum, iron, and zinc ions promote aggregation of physiological concentrations of beta-amyloid peptide. J Neurochem 61:1171-1174.
54. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992) Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389.
55. McGeer PL, McGeer EG (1996) Anti-inflammatory drugs in the fight against Alzheimer's disease. Ann NY Acad Sci 777:213-220.
56. Meda L, Cassatella MA, Szendrei GI, Otvos Jr L, Baron P, Villalba M, Ferrari D, Rossi F (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650.
57. Mrak RE, Sheng JG, Griffin WS (1995) Glial cytokines in Alzheimer's disease: review and pathogenic implications. Hum Pathol 26:816-823.
58. Murphy S, Simmons ML, Agullo L, Garcia A, Feinstein DL, Galea E, Reis DJ, Minc-Golomb D, Schwartz JP (1993) Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 16:323-328.
59. Nishiyama E, Ohwada J, Iwamoto N, Arai H (1993) Selective loss of calbindin D28K-immunoreactive neurons in the cortical layer II in brains of Alzheimer's disease: a morphometric study. Neurosci Lett 163:223-226.
60. O'Callaghan JP, Jensen KF, Miller DB (1995) Quantitative aspects of drug and toxicant-induced astrogliosis. Neurochem Int 26:115-124.
61. Paresce DM, Ghosh RN, Maxfield FR (1996) Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 17:553-565.
62. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. North Ryde, New South Wales, Australia: Academic.
63. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991a) Aggregation-related toxicity of synthetic beta-amyloid protein in hippocampal cultures. Eur J Pharmacol 207:367-368.
64. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991b) In vitro aging of beta-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res 563:311-314.
65. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW (1993) Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 13:1676-1687.
66. Pike CJ, Cummings BJ, Monzavi R, Cotman CW (1994) Beta-amyloid-induced changes in cultured astrocytes parallel reactive astrocytosis associated with senile plaques in Alzheimer's disease. Neuroscience 63:517-531.
67. Pike CJ, Walencewicz-Wasserman AJ, Kosmoski J, Cribbs DH, Glabe CG, Cotman CW (1995) Structure-activity analyses of beta-amyloid peptides: contributions of the beta 25-35 region to aggregation and neurotoxicity. J Neurochem 64:253-265.
68. Price DL, Borchelt DR, Walker LC, Sisodia SS (1992) Toxicity of synthetic Aβ peptides and modeling of Alzheimer's disease. Neurobiology of Aging 13:623-625.
69. Sanan DA, Weisgraber KH, Russell SJ, Mahley RW, Huang D, Saunders A, Schmechel D, Wisniewski T, Frangione B, Roses AD, Strittmatter WJ (1994) Apolipoprotein E associates with beta amyloid peptide of Alzheimer's disease to form novel monofibrils. Isoform apoE4 associates more efficiently than apoE3. J Clin Invest 94:860-869.
70. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, Bird TD, Hardy J, Mutton M, Kukull W, Larson E, Levy-Lahad E, Viitanen M, Peskind E, Poorkaj P, Schellenberg G, Tanzi R, Wasco W, Lannfelt L, Selkoe D, Younkin S (1996) Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 2:864-870.
71. Scott SA, Johnson SA, Zarow C, Perlmutter LS (1993) Inability to detect beta-amyloid protein precursor mRNA in Alzheimer plaque-associated microglia. Exp Neurol 121:113-118.
72. Selden N, Geula C, Hersh L, Mesulam MM (1994) Human striatum: chemoarchitecture of the caudate nucleus, putamen and ventral striatum in health and Alzheimer's disease. Neuroscience 60:621-636.
73. Selkoe DJ (1991) The molecular pathology of Alzheimer's disease Neuron 6:487-498.
74. Selkoe DJ (1994) Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53:438-447.
75. Selkoe DJ (1997) Alzheimer's disease -genotypes, phenotype, and treatments. Science 275:630-631.
76. Selkoe DJ, Abraham CR (1986) Isolation of paired helical filaments and amyloid fibers from human brain. Methods Enzymol 134:388-404.
77. Seubert P, Vigo-Pelfrey C, Esch F, Lee M, Dovey H, Davis D, Sinha S, Schlossmacher M, McCormack R, Wolfert R, Selkoe D, Lieberburg I, Schenk D (1992) Isolation and quantification of soluble Alzheimer's beta-peptide from biological fluids. Nature 359:325-327.
78. Shaffer LM, Dority MD, Gupta-Bansal R, Frederickson RC, Younkin SG, Brunden KR (1995) Amyloid beta protein (A beta) removal by neuroglial cells in culture. Neurobiol Aging 16:737-745.
79. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, Shaffer LM, Cai XD, McKay DM, Tintner R, Frangione B, Younkin SG (1992) Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 258:126-129.
80. Soreghan B, Kosmoski J, Glabe C (1994) Surfactant properties of Alzheimer s A beta peptides and the mechanism of amyloid aggregation. J Biol Chem 269:28551-28554.
81. Uchihara T, Kondo H, Akiyama H, Ikeda K (1995) Single-laser three-color immunolabeling of a histological section by laser scanning microscopy: application to senile plaque-related structures in post-mortem human brain tissue. J Histochem Cytochem 43:103-106.
82. van Gool WA, Kuiper MA, Walstra GJ, Wolters EC, Bolhuis PA (1995) Concentrations of amyloid beta protein in cerebrospinal fluid of patients with Alzheimer's disease. Ann Neurol 37:277-279.
83. Waldvogel HJ, Faull RL, Williams MN, Dragunow M (1991) Differential sensitivity of calbindin and parvalbumin immunorcactive cells in the striatum to excitotoxins. Brain Res 546:329-335.
84. Wisniewski T, Castano EM, Golabek A, Vogel T, Frangione B (1994) Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro. Am J Pathol 145:1030-1035.
85. Wong M-L, Rettori V, Al-Shekhlee A, Bongiorno PB, Canteros G, McCann SM, Gold PW, Licinio J (1996) Inducible nitric oxide synthase gene expression in the brain during systemic inflammation. Nat Med 2:581-584.
86. Van SD, Chen X, Fu J, Chen M, Zhu HJ, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382:685-691.
87. Yankner BA, Duffy LK, Kirschner DA (1990) Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 250:279-282.