Lysosomal dysfunction produces distinct alterations in synaptic α-amino-3-hydroxy-5-methylisoxazolepropionic acid and N-methyl-D-aspartate receptor currents in hippocampus

Journal of Neuropathology and Experimental Neurology

Volumn 66, Issue 9, 2007, Pages 779-788

  Kanju, Patrick M ^a   Parameshwaran, Kodeeswaran ^a   Vaithianathan, Thirumalini ^b   Sims, Catrina M ^a   Huggins, Kevin ^c   Bendiske, Jennifer ^d   Ryzhikov, Sophia ^e   Bahr, Ben A ^e   Suppiramaniam, Vishnu ^a  

^a AUBURN UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c AUBURN UNIVERSITY   (United States)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^e UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Glutamate receptors; Lysosomal dysfunction; Synaptic function

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONDUCTANCE; CONTROLLED STUDY; HIPPOCAMPUS; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROBABILITY; RAT; SYNAPSE; WESTERN BLOTTING;

AGING; ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CATHEPSIN D; CHLOROQUINE; ELECTRIC CONDUCTIVITY; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LYSOSOMES; NERVE TISSUE PROTEINS; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTOSOMES;

EID: 34548381681     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/nen.0b013e3181461ae7     Document Type: Article

References (43)

1. Cotman CW, Monaghan DT. Anatomical organization of excitatory amino acid receptors and their properties. Adv Exp Med Biol 1986;203:237-52
2. Monaghan DT, Bridges RJ, Cotman CW. The excitatory amino acid receptors: Their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol 1989;29:365-402
3. Shi SH, Hayashi Y, Petralia RS, et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 1999;284:1811-16
4. Conti F, Weinberg RJ. Shaping excitation at glutamatergic synapses. Trends Neurosci 1999;22:451-58
5. Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994;17:31-108
6. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science 1992;258:597-603
7. A, NMDA and AMPA receptors: A developmentally regulated 'menage a trois.' Trends Neurosci 1997;20:523-29
8. Muller D, Lynch G. Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc Natl Acad Sci U S A 1988;85:9346-50
9. Carlson MD, Penney JB Jr, Young AB. NMDA, AMPA, and benzodiazepine binding site changes in Alzheimer's disease visual cortex. Neurobiol Aging 1993;14:343-52
10. Dewar D, Chalmers DT, Graham DI, McCulloch J. Glutamate metabotropic and AMPA binding sites are reduced in Alzheimer's disease: An autoradiographic study of the hippocampus. Brain Res 1991;553:58-64
11. Almeida CG, Tampellini D, Takahashi RH, et al. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol Dis 2005;20:187-98
12. Bahr BA, Godshall AC, Hall RA, Lynch G. Mouse telencephalon exhibits an age-related decrease in glutamate (AMPA) receptors but no change in nerve terminal markers. Brain Res 1992;589:320-26
13. Hsieh H, Boehm J, Sato C, et al. AMPAR removal underlies Aβ-induced synaptic depression and dendritic spine loss. Neuron 2006;52:831-43
14. Ikonomovic MD, Mizukami K, Davies P, Hamilton R, Sheffield R, Armstrong DM. 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
15. Wakabayashi K, Narisawa-Saito M, Iwakura Y, et al. Phenotypic down-regulation of glutamate receptor subunit GluR1 in Alzheimer's disease. Neurobiol Aging 1999;20:287-95
16. Wenk GL, Barnes CA. Regional changes in the hippocampal density of AMPA and NMDA receptors across the lifespan of the rat. Brain Res 2000;885:1-5
17. Bahr BA, Abai B, Gall CM, Vanderklish PW, Hoffman KB, Lynch G. 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
18. 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
19. 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
20. Cha JH, Farrell LA, Ahmed SF, et al. Glutamate receptor dysregulation in the hippocampus of transgenic mice carrying mutated human amyloid precursor protein. Neurobiol Dis 2001;8:90-102
21. Magnusson KR, Cotman CW. Age-related changes in excitatory amino acid receptors in two mouse strains. Neurobiol Aging 1993;14:197-206
22. 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;88:10998-1002
23. Nakamura Y, Takeda M, Suzuki H, et al. Lysosome instability in aged rat brain. Neurosci Lett 1989;97:215-20
24. Nixon RA, Cataldo AM, Paskevich PA, Hamilton DJ, Wheelock TR, Kanaley-Andrews L. The lysosomal system in neurons. Involvement at multiple stages of Alzheimer's disease pathogenesis. Ann N Y Acad Sci 1992;674:65-88
25. 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
26. Cataldo AM, Hamilton DJ, Barnett JL, Paskevich PA, Nixon RA. Properties of the endosomal-lysosomal system in the human central nervous system: Disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J Neurosci 1996;16:186-99
27. Bi X, Zhou J, Lynch G. Lysosomal protease inhibitors induce meganeurites and tangle-like structures in entorhinohippocampal regions vulnerable to Alzheimer's disease. Exp Neurol 1999;158:312-27
28. Cataldo AM, Nixon RA. Enzymatically active lysosomal proteases are associated with amyloid deposits in Alzheimer brain. Proc Natl Acad Sci U S A 1990;87:3861-65
29. Cataldo AM, Thayer CY, Bird ED, Wheelock TR, Nixon RA. Lysosomal proteinase antigens are prominently localized within senile plaques of Alzheimer's disease: Evidence for a neuronal origin. Brain Res 1990;513:181-92
30. Nixon RA, Mathews PM, Cataldo AM. The neuronal endosomal-lysosomal system in Alzheimer's disease. J Alzheimers Dis 2001;3:97-107
31. Butler D, Brown QB, Chin DJ, et al. Cellular responses to protein accumulation involve autophagy and lysosomal enzyme activation. Rejuvenation Res 2005;8:227-37
32. Bendiske J, Bahr BA. Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis - an approach for slowing Alzheimer disease? J Neuropathol Exp Neurol 2003;62:451-63
33. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991;37:173-82
34. Caporaso GL, Gandy SE, Buxbaum JD, Greengard P. Chloroquine inhibits intracellular degradation but not secretion of Alzheimer beta/A4 amyloid precursor protein. Proc Natl Acad Sci U S A 1992;89:2252-56
35. 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
36. Vaithianathan T, Manivannan K, Kleene R, et al. Single channel recordings from synaptosomal AMPA receptors. Cell Biochem Biophys 2005;42:75-85
37. Bahr BA. Long-term hippocampal slices: A model system for investigating synaptic mechanisms and pathologic processes. J Neurosci Res 1995;42:294-305
38. 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
39. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis SF. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 2000;20:89-102
40. Rumbaugh G, Sia GM, Garner CC, Huganir RL. Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons. J Neurosci 2003;23:4567-76
41. Hsia AY, Malenka RC, Nicoll RA. Development of excitatory circuitry in the hippocampus. J Neurophysiol 1998;79:2013-24
42. Bahr BA, Bendiske J, Brown QB, et al. Survival signaling and selective neuroprotection through glutamatergic transmission. Exp Neurol 2002;174:37-47
43. Shimizu T, Hayashi Y, Yamasaki R, et al. Proteolytic degradation of glutamate decarboxylase mediates disinhibition of hippocampal CA3 pyramidal cells in cathepsin D-deficient mice. J Neurochem 2005;94:680-90