Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis - An approach for slowing Alzheimer disease?

Journal of Neuropathology and Experimental Neurology

Volumn 62, Issue 5, 2003, Pages 451-463

  Bendiske, Jennifer ^b   Bahr, Ben A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b NONE

Author keywords

Hippocampal slice culture; Lysosomal activation; Lysosomal modulation; N Cbz L phenylalanyl L alanyl diazomethylketone (PADK); Neuroprotection; Protein deposition disease; Synaptic recovery

Indexed keywords

BENZYLOXYCARBONYLPHENYLALANYLALANYL DIAZOMETHYL KETONE; BETA GLUCURONIDASE; CATHEPSIN B; CATHEPSIN D; CATHEPSIN L; CHLOROQUINE; ELASTASE; GLUTAMATE RECEPTOR; LYSOSOME ENZYME; PHENYLALANINE DERIVATIVE; PROTEIN; SYNAPTOPHYSIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; HYPOTHESIS; LYSOSOME; MICROTUBULE; NERVE FIBER; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; UPREGULATION;

EID: 0037989761     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/62.5.451     Document Type: Article

References (76)

1. Bahr BA, Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J Neurochem 2002;83:481-89
2. Benowitz LI, Rodriguez W, Paskevich P, et al. The amyloid precursor protein is concentrated in neuronal lysosomes in normal and Alzheimer disease subjects. Exp Neurol 1989;106:237-50
3. Cataldo AM, Paskevich PA, Kominami E, Nixon RA. Lysosomal hydrolases of different classes are abnormally distributed in brains of patients with Alzheimer disease. Proc Natl Acad Sci U S A 1991; 88:10998-11002
4. Golde TE, Estus S, Younkin LH, Selkoe DJ, Younkin SG. Processing of the amyloid protein precursor to potentially amyloidogenic derivatives. Science 1992;255:728-30
5. Bahr BA, Abai B, Gall CM, et al. Induction of β-amyloid -containing polypeptides in hippocampus: Evidence for a concomitant loss of synaptic proteins and interactions with an excitotoxin. Exp Neurol 1994;129:81-94
6. Hajimohammadreza I, Anderson VER, Cavanagh JB, et al. β-Amyloid precursor protein fragments and lysosomal dense bodies are found in rat brain neurons after ventricular infusion of leupeptin. Brain Res 1994;640:25-32
7. Nixon RA, Mathews PM, Cataldo AM. The neuronal endosomallysosomal system in Alzheimer's disease. J Alzheimer's Disease 2001;3:97-107
8. Ivy GO. Protease inhibition causes some manifestations of aging and Alzheimer's disease in rodent and primate brain. Ann NY Acad Sci 1992;674:89-102
9. Bahr BA. Long-term hippocampal slices: A model system for investigating synaptic mechanisms and pathologic processes. J Neurosci Res 1995;42:294-305
10. Takauchi S, Miyoshi K. Cytoskeletal changes in rat cortical neurons induced by long-term intraventricular infusion of leupeptin. Acta Neuropathol 1995;89:8-16
11. Bi X, Yong AP, Zhou J, Ribak CE, Lynch G. Rapid induction of intraneuronal neurofibrillary tangles in apolipoprotein E-deficient mice. Proc Natl Acad Sci U S A 2001;98:8832-37
12. Bendiske J, Caba E, Brown QB, Bahr BA. Intracellular deposition, microtubule destabilization, and transport failure: An 'early' pathogenic cascade leading to synaptic decline. J Neuropathol Exp Neurol 2002;61:640-50
13. Sapp E, Schwarz C, Chase K, et al. Huntingtin localization in brains of normal and Huntington's disease patients. Ann Neurol 1997;42: 604-12
14. DiFiglia M, Sapp E, Chase KO, et al. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997;277:1990-93
15. Cataldo AM, Barnett JL, Berman SA, et al. Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: Evidence for early up-regulation of the endosomal-lysosomal system. Neuron 1995;14:671-80
16. Cataldo AM, Hamilton DJ, Barnett JL, Paskevich PA, Nixon RA. Properties of the endosomal-lysosomal system in the human central nervous system: Disturbance mark most neurons in populations at risk to degenerate in Alzheimer's disease. J Neurosci 1996;16: 186-99
17. Cross AJ, Crow TJ, Dawson JM, et al. Subcellular pathology of human neurodegenerative disorders: Alzheimer-type dementia and Huntington's disease. J Neurochem 1986;47:882-89
18. Haas U, Sparks DL. Cortical cathepsin D activity and immunolocalization in Alzheimer disease, critical coronary artery disease, and aging. Mol Chem Neuropath 1996;29:1-14
19. Ii K, Ito H, Kominami E, Hirano A. Abnormal distribution of cathepsin proteinases and endogenous inhibitors (cystatins) in the hippocampus of patients with Alzheimer's disease, Parkinsonism-dementia complex on Guam, and senile dementia and in the aged. Virchows Arch A, Path Anat Histopath 1993;423:185-94
20. Callahan LM, Vaules WA, Coleman PD. Quantitative decrease in synaptophysin message expression and increase in cathepsin D message expression in Alzheimer disease neurons containing neurofibrillary tangles. J Neuropathol Exp Neurol 1999;58:275-87
21. Lemere CA, Munger JS, Shi GP, et al. The lysosomal cysteine protease, cathepsin S, is increased in Alzheimer's disease and Down syndrome brain. An immunocytochemical study. Am J Path 1995; 146:848-60
22. Kegel KB, Kim M, Sapp E, et al. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J Neurosci 2000;20:7268-78
23. Hoffman KB, Bi X, Pham JT, Lynch G. β-Amyloid increases cathepsin D levels in hippocampus. Neurosci Lett 1998;250:75-78
24. Burdick D, Kosmoski J, Knauer MF, Glabe CG. Preferential adsorption, internalization and resistance to degradation of the major isoform of the Alzheimer's amyloid peptide, Aβ 1-42, in differentiated PC12 cells. Brain Res 1997;746:275-84
25. Bahr BA, Hoffman KB, Yang AJ, et al. Amyloid β protein is internalized selectively by hippocampal field CA1 and causes neurons to accumulate amyloidogenic carboxyterminal fragments of the amyloid precursor protein. J Comp Neurol 1998;397:139-47
26. Yang AJ, Chandswangbhuvana D, Margol L, Glabe CG. Loss of endosomal/lysosomal membrane impermeability is an early event in amyloid Aβ1-42 pathogenesis. J Neurosci Res 1998;52:691-98
27. Ditaranto K, Tekirian TL, Yang AJ. Lysosomal membrane damage in soluble Aβ-mediated cell death in Alzheimer's disease. Neurobiol Dis 2001;8:19-31
28. Davies CA, Mann DM, Sumpter PQ, Yates PO. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 1987;78:151-64
29. Terry RD, Masliah E, Salmon DP, et al. Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991;30:572-80
30. Honer WG, Dickson DW, Gleeson J, Davies P. Regional synaptic pathology in Alzheimer's disease. Neurobiol Aging 1992;13: 375-82
31. Small DH, Mok SS, Bornstein JC. Alzheimer's disease and Aβ toxicity: From top to bottom. Nat Rev Neurosci 2001;2:595-98
32. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 2002; 298:789-91
33. Samuel W, Masliah E, Hill LR, Butters N, Terry R. Hippocampal connectivity and Alzheimer's dementia: Effects of synapse loss and tangle frequency in a two-component model. Neurology 1994;44: 2081-88
34. Heinonen O, Soininen H, Sorvari H, et al. Loss of synaptophysin like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neurosci 1995;54:375-84
35. Callahan LM, Vaules WA, Coleman PD. Progressive reduction of synaptophysin message in single neurons in Alzheimer disease. J Neuropathol Exp Neurol 2002;61:384-95
36. Bahr BA, Bendiske J, Brown QB, et al. Survival signaling and selective neuroprotection through glutamatergic transmission. Exp Neurol 2002;174:37-47
37. Garcia-Ladona FJ, Palacios JM, Probst A, Wieser HG, Mengod GA. Excitatory amino acid AMPA receptor mRNA localization in several regions of normal and neurological disease affected human brain. An in situ hybridization histochemistry study. Brain Res Mol Brain Res 1994;21:75-84
38. Thorns V, Mallory M, Hansen L, Masliah E. Alterations in glutamate receptor 2/3 subunits and amyloid precursor protein expression during the course of Alzheimer's disease and Lewy body variant. Acta Neuropathol (Berl) 1997;94:539-48
39. Ikonomovic MD, Mizukami K, Davies P, et al. The loss of GluR2(3) immunoreactivity precedes neurofibrillary tangle formation in the entorhinal cortex and hippocampus of Alzheimer brains. J Neuropathol Exp Neurol 1997;56:1018-27
40. Yasuda RP, Ikonomovic MD, Sheffield R, et al. Reduction of AMPA-selective glutamate receptor subunits in the entorhinal cortex of patients with Alzheimer's disease pathology: A biochemical study. Brain Res 1995;678:161-67
41. Sze CI, Troncoso JC, Kawas C, et al. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol 1997;56: 933-44
42. Masliah E, Mallory M, Alford M, et al. Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 2001;56:127-29
43. Hsia AY, Masliah E, McConlogue L, et al. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 1999;96:3228-33
44. Mucke L, Masliah E, Yu GO, et al. High-level neuronal expression of Aβ1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 2000; 20:4050-58
45. R antigen (GR53) in brain tissue. Neurosci 1996;74:707-21
46. Burdick D, Soreghan B, Kwon M, et al. Assembly and aggregation properties of synthetic Alzheimer's Aβ amyloid peptide analogs. J Biol Chem 1992;267:546-54
47. Bahr BA, Kessler M, Rivera S, et al. Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus 1995;5:425-39
48. Caporaso GL, Gandy SE, Buxbaum JD, Greengard P. Chloroquine inhibits intracellular degradation but not secretion of Alzheimer β/A4 amyloid precursor protein. Proc Natl Acad Sci U S A 1992;89: 2252-56
49. Scornik OA. Effects of inhibitors of protein degradation on the rate of protein synthesis in Chinese hamster ovary cells. J Cell Physiol 1984;121:257-62
50. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 2002;156:1051-63
51. Brunk U, Brun A. The effect of aging on lysosomal permeability in nerve cells of the central nervous system. An enzyme histochemical study in rat. Histochemie 1972;30:315-24
52. Nakamura Y, Takeda M, Suzuki K, et al. Lysosome instability in aged rat brain. Neurosci Lett 1998;97:215-20
53. Dobrenis K, Joseph A, Rattazzi MC. Neuronal lysosomal enzyme replacement using fragment C of tetanus toxin. Proc Natl Acad Sci U S A 1992;6:2297-2301
54. Li Y, Xu C, Schubert D. The up-regulation of endosomal-lysosomal components in amyloid β-resistant cells. J Neurochem 1999;73: 1477-82
55. Munger JS, Haass C, Lemere CA, et al. Lysosomal processing of the amyloid precursor protein to Aβ peptides: A distinct role for cathepsin S. Biochem J 1995;311:299-305
56. Petanceska S, Burke S, Watson SJ, Devi L. Differential distribution of messenger RNAs for cathepsins B, L and S in adult rat brain: An in situ hybridization study. Neurosci 1994;59:729-38
57. Kenessey A, Nacharaju P, Ko LW, Yen SH. Degradation of tau by lysosomal enzyme cathepsin D: Implication for Alzheimer neurofibrillary degeneration. J Neurochem 1997;69:2026-38
58. Ikeda K, Akiyama H, Arai T, et al. Alz-50/Gallyas-positive lysosome-like intraneuronal granules in Alzheimer's disease and control brains. Neurosci Lett 1998;258:113-16
59. Bi X, Haque TS, Zhou J, et al. Novel cathepsin D inhibitors block the formation of hyperphosphorylated tau fragments in hippocampus. J Neurochem 2000;74:1469-77
60. Adamec E, Mohan PS, Cataldo AM, Vonsattel JP, Nixon RA. Upregulation of the lysosomal system in experimental models of neuronal injury: Implications for Alzheimer's disease. Neurosci 2000; 100:663-75
61. Robker RL, Russell DL, Espey LL, et al. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci U S A 2000;97:4689-94
62. Wang F, Samudio I, Safe S. Transcriptional activation of cathepsin D gene expression by 17β-estradiol: Mechanism of aryl hydrocarbon receptor-mediated inhibition. Mol Cell Endocrinol 2001;172: 91-103
63. Greenfield JP, Leung LW, Cai D, et al. Estrogen lowers Alzheimer β-amyloid generation by stimulating trans-Golgi network vesicle biogenesis. J Biol Chem 2002;277:12128-36
64. Petanceska SS, Nagy V, Frail D, Gandy S. Ovariectomy and 17βestradiol modulate the levels of Alzheimer's amyloid β peptides in brain. Neurology 2000;54:2212-17
65. Zheng H, Xu H, Wang H, et al. Modulation of Aβ peptides by estrogen in mouse models. J Neurochem 2002;80:191-96
66. Turner RS. Alzheimer's disease in man and transgenic mice: Females at higher risk. Am J Pathol 2001;158:797-801
67. Bahr BA, Vicente JS. Age-related phosphorylation and fragmentation events influence the distribution profiles of distinct tau isoforms in mouse brain. J Neuropathol Exp Neurol 1998;57:111-21
68. Delacourte A, Flament S, Dibe EM, et al. Pathological proteins Tau 64 and 69 are specifically expressed in the somatodendritic domain of the degenerating cortical neurons during Alzheimer's disease: Demonstration with a panel of antibodies against tau proteins. Acta Neuropathol (Berl) 1990;80:111-17
69. Goedert M, Spillantini MG, Cairns NJ, Crowther RA. Tau proteins of Alzheimer paired helical filaments: Abnormal phosphorylation of all six brain isoforms. Neuron 1992;8:159-68
70. Ikeda K, Akiyama H, Arai T, et al. Neurons containing Alz-50-immunoreactive granules around the cerebral infarction: Evidence for the lysosomal degradation of altered tau in human brain? Neurosci Lett 2000;284:187-89
71. Oyama F, Murakami N, Ihara Y. Chloroquine myopathy suggests that tau is degraded in lysosomes: Implication for the formation of paired helical filaments in Alzheimer's disease. Neurosci Res 1998; 31:1-8
72. Black MM, Baas PW, Humphries S. Dynamics of α-tubulin deacetylation in intact neurons. J Neurosci 1989;9:358-68
73. Hempen B, Brion JP. Reduction of acetylated α-tubulin immunoreactivity in neurofibrillary tangle-bearing neurons in Alzheimer's disease. J Neuropathol Exp Neurol 1996;55:964-72
74. Kotilinek LA, Bacskai B, Westerman M, et al. Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 2002;22:6331-35
75. Bambrick LL, Yarowsky PJ, Krueger BK. Glutamate as a hippocampal neuron survival factor: An inherited defect in the trisomy 16 mouse. Proc Natl Acad Sci U S A 1995;92:9692-96
76. McKinney RA, Capogna M, Durr R, Gahwiler BH, Thompson SM. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 1999;2:44-49