Gephyrin alterations due to protein accumulation stress are reduced by the lysosomal modulator Z-Phe-Ala-diazomethylketone

Journal of Molecular Neuroscience

Volumn 34, Issue 2, 2008, Pages 131-139

  Ryzhikov, Sophia ^a   Bahr, Ben A ^a,b  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Synaptic Dynamics Inc   (United States)

Author keywords

Gephyrin breakdown products; Gephyrin isoforms; Lysosomal enhancement; Lysosomal modulation; PADK

Indexed keywords

CHLOROQUINE; GEPHYRIN; KETONE DERIVATIVE; NEUROTRANSMITTER RECEPTOR; PHENYLALANYLDIAZOMETHYLKETONE; AMPA RECEPTOR; CARRIER PROTEIN; DIAZOMETHANE; DIAZOMETHYL KETONES; DRUG DERIVATIVE; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; ISOPROTEIN; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DEGENERATIVE DISEASE; HIPPOCAMPUS; LYSOSOME; MICROTUBULE; NONHUMAN; RAT; ANIMAL; CHEMISTRY; CYTOLOGY; GUINEA PIG; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; CARRIER PROTEINS; CHLOROQUINE; DIAZOMETHANE; GUINEA PIGS; HIPPOCAMPUS; LYSOSOMES; MEMBRANE PROTEINS; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA;

EID: 42949101621     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-007-9009-7     Document Type: Article

References (66)

1. Bahr, B. A. (1995). Long-term hippocampal slices: A model system for investigating synaptic mechanisms and pathological processes. Journal of Neuroscience Research, 42, 294-305.
2. Bahr, B. A. (2003). Dysfunction and activation of the lysosomal system: Implications for and against Alzheimer's disease. In E. M. Welsh (Ed.), Focus on Alzheimer's disease research (pp. 115-150). Hauppauge, NY: Nova Science.
3. Bahr, B. A., Abai, B., Gall, C. M., Vanderklish, P. W., Hoffman, K. B., Lynch, G. (1994). Induction of β-amyloid-containing polypeptides in hippocampus: Evidence for a concomitant loss of synaptic proteins and interactions with an excitotoxin. Experimental Neurology, 129, 81-94.
4. Bahr, B. A., & Bendiske, J. (2002). The neuropathogenic contributions of lysosomal dysfunction. Journal of Neurochemistry, 83, 481-489.
5. R antigen (GR53) in brain tissue. Neuroscience, 74, 707-721.
6. Bahr, B. A., Kessler, M., Rivera, S., Vanderklish, P. W., Hall, R. A., Mutneja, M. S. et al. (1995). Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus, 5, 425-439.
7. Bendiske, J., & Bahr, B. A. (2003). Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis-an approach for slowing Alzheimer disease? Journal of Neuropathology and Experimental Neurology, 62, 481-489.
8. Bendiske, J., Caba, E., Brown, Q. B., & Bahr, B. A. (2002). Intracellular deposition, microtubule destabilization, and transport failure: an "early" pathogenic cascade leading to synaptic decline. Journal of Neuropathology and Experimental Neurology, 61, 640-650.
9. Bonde, C., Noraberg, J., Noer, H., & Zimmer, J. (2005). Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation of hippocampal slice cultures. Neuroscience, 136(3), 779-794.
10. Butler, D., Bendiske, J., Michaelis, M. L., Karanian, D. A., & Bahr, B. A. (2007). Microtubule-stabilizing agent prevents protein accumulation-induced loss of synaptic markers. European Journal of Pharmacology, 562, 20-27.
11. Butler, D., Brown, Q. B., Chin, D. J., Batey, L., Karim, S., Mutneja, M. S. et al. (2005). Cellular responses to protein accumulation involve autophagy and lysosomal enzyme activation. Rejuvenation Research, 8, 227-237.
12. Butler, D., Nixon, R. A., & Bahr, B. A. (2006). Potential compensatory responses through autophagic lysosomal pathways in neurodegenerative diseases. Autophagy, 2, 234-237.
13. Caba, E., & Bahr, B. A. (2004). Biphasic activation of NF-κB in the excitotoxic hippocampus. Acta Neuropathologica, 108, 173-182.
14. Caporaso, G. L., Gandy, S. E., Buxbaum, J. D., & Greengard, P. (1992). Chloroquine inhibits intracellular degradation but not secretion of Alzheimer/A4 amyloid precursor protein. Proceedings of the National Academy of Sciences of the United States of America, 89, 2252-2256.
15. Caspary, D. M., Schatleman, T. A., & Hughes, L. F. (2005). Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: Role of inhibitory inputs. Journal of Neuroscience, 25, 10952-10959.
16. Charrier, C., Ehrensperger, M. V., Dahan, M., Lèvi, S., & Triller, A. (2006). Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. Journal of Neuroscience, 26, 8502-8511.
17. Coleman, P., Federoff, H., & Kurlan, R. (2004). A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology, 63, 1155-1162.
18. Collins, P. R., Stack, C. M., O'Neill, S. M., Doyle, S., Ryan, T., Brennan, G. P. et al. (2004). Cathepsin L1, the major protease involved in liver fluke (Fasciola hepatica) virulence: Propeptide cleavage sites and autoactivation of the zymogen secreted from gastrodermal cells. Journal of Biological Chemistry, 279, 17038-17046.
19. Craig, A. M., Banker, G., Chang, W., McGrath, M. E., & Serpinskaya, A. S. (1996). Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. Journal of Neuroscience, 16, 3166-3177.
20. Craig, A. M., & Boudin, H. (2001). Molecular heterogeneity of central synapses: afferent and target regulation. Nature Neuroscience, 4, 569-578.
21. A receptors varies during development in cultured hippocampal neurons. Molecular and Cellular Neurosciences, 23, 264-278.
22. Essrich, C., Lorez, M., Benson, J. A., Fritschy, J. M., & Luscher, B. (1998). Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nature Neuroscience, 1, 563-571.
23. Fremeau, R. T. Jr., Troyer, M. D., Pahner, I., Nygaard, G. O., Tran, C. H., Reimer, R. J. et al. (2001). The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247-260.
24. Fuhrmann, J. C., Kins, S., Rostaing, P., El Far, O., Kirsch, J., Sheng, M. et al. (2002). Gephyrin interacts with Dynein light chains 1 and 2, components of motor protein complexes. Journal of Neuroscience, 22(13), 5393-5402, Jul 1.
25. Graf, R. A., & Kater, S. B. (1998). Inhibitory neuronal activity can compensate for adverse effects of beta-amyloid in hippocampal neurons. Brain Research, 786, 1558-1569.
26. Hanus, C., Vannier, C., & Triller, A. (2004). Intracellular association of glycine receptor with gephyrin increases its plasma membrane accumulation rate. Journal of Neuroscience, 24(5), 1119-1128 (Feb 4).
27. Heinonen, O., Soininen, H., Sorvari, H., Kosunen, O., Paljarvi, L., Koivisto, E. et al. (1995). Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neuroscience, 54, 375z-384.
28. Honer, W. G., Dickson, D. W., Gleeson, J., & Davies, P. (1992). Regional synaptic pathology in Alzheimer's disease. Neurobiology of Aging, 13, 375-382.
29. A receptors. Journal of Neuroscience, 25, 10469-10478.
30. Karanian, D. A., Brown, Q. B., Makriyannis, A., & Bahr, B. A. (2005). Blocking cannabinoid activation of FAK and ERK1/2 compromises synaptic integrity in hippocampus. European Journal of Pharmacology, 508, 47-56.
31. Karanian, D. A., Brown, Q. B., Makriyannis, A., Kosten, T. A., & Bahr, B. A. (2005). Dual modulation of endocannabinoid transport and fatty acid amide hydrolase protects against excitotoxicity. Journal of Neuroscience, 25, 7813-7820.
32. Kawasaki, B. T., Hoffman, K. B., Yamamoto, R. S., & Bahr, B. A. (1997). Variants of the receptor/channel clustering molecule gephyrin in brain: Distinct distribution patterns, developmental profiles, and proteolytic cleavage by calpain. Journal of Neuroscience Research, 49, 381-388.
33. Kim, E. Y., Schrader, N., Smolinsky, B., Bedet, C., Vannier, C., Schwarz, G., et al. (2006). Deciphering the structural framework of glycine receptor anchoring by gephyrin. EMBO Journal, 25, 1385-1395.
34. Kirsch, J., & Betz, H. (1993). Widespread expression of gephyrin, a putative glycine receptor-tubulin linker protein, in rat brain. Brain Research, 621, 301-310.
35. Kirsch, J., Wolters, I., Triller, A., Betz, H. (1993). Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature, 366, 745-748.
36. Kneussel, M., & Betz, H. (2000). Clustering of inhibitory neurotransmitter receptors at developing postsynaptic sites: the membrane activation model. Trends in Neurosciences, 23, 429-435.
37. Kneussel, M., Brandstatter, J. H., Laube, B., Stahl, S., Muller, U., & Betz, H. (1999). Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. Journal of Neuroscience, 19, 9289-9297.
38. Legendre, P. (2001). The glycinergic inhibitory synapse. Cellular and Molecular Life Sciences, 58, 760-793.
39. Lévi, S., Logan, S. M., Tovar, K. R., & Craig, A. M. (2004). Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. Journal of Neuroscience, 24, 207-217.
40. A receptors are present in the brain, one associated to lipid rafts and another one to the postsynaptic GABAergic complex. Journal of Neurochemistry, 102, 1329-1345.
41. Masliah, E. (1995). Mechanisms of synaptic dysfunction in Alzheimer's disease. Histology and Histopathology, 10, 509-519.
42. Meier, J., De Chaldee, M., Triller, A., Vannier, C. (2000). Functional heterogeneity of gephyrins. Molecular and Cellular Neurosciences, 16, 566-577.
43. Mielke, J. G., Murphy, M. P., Maritz, J., Bengualid, K. M., & Ivy, G. O. (1997). Chloroquine administration in mice increases β-amyloid immunoreactivity and attenuates kainate-induced blood-brain barrier dysfunction. Neuroscience Letters, 227, 169-172.
44. A receptor β2/3 subunits in the hippocampal formation of aged brains with Alzheimer-related neuropathologic changes. Experimental Neurology, 147, 333-345.
45. Niewiadomska, G., Baksalerska-Pazera, M., & Riedel, G. (2006). Cytoskeletal transport in the aging brain: focus on the cholinergic system. Reviews in the Neurosciences, 17(6), 581-618.
46. Nixon, R. A. (2000). A protease activation cascade" in the pathogenesis of Alzheimer's disease. Annals of the New York Academy of Sciences, 924, 117-131.
47. Oyama, F., Murakami, N., & Ihara, Y. (1998). Chloroquine myopathy suggests that tau is degraded in lysosomes: Implication for the formation of paired helical filaments in Alzheimer's disease. Neuroscience Research, 31, 1-8.
48. Poe, B. H., Linville, C., & Brunson-Bechtold, J. (2001). Age-related decline of presumptive inhibitory synapses in the sensimotor cortex as revealed by the physical dissector. Journal of Comparative Neurology, 439, 65-72.
49. Prior, P., Schmitt, B., Grenningloh, G., Pribilla, I., Multhaup, G., Beyreuther, K. et al. (1992). Primary structure and alternative splice variants of gephyrin, a putative glycine receptor-tubulin linker protein. Neuron, 8, 1161-1170.
50. Ramming, M., Kins, S., Werner, N., Hermann, A., Betz, H., & Kirsch, J. (2000). Diversity and phylogeny of gephyrin: tissue-specific splice variants, gene structure, and sequence similarities to molybdenum cofactor-synthesizing and cytoskeleton-associated proteins. Proceedings of the National Academy of Sciences of the United States of America, 97(18), 10266-10271.
51. A receptor subunits α1, α5, β1, β2 in the hippocampus of patients with Alzheimer's disease neuropathology. Neuroscience, 120, 695-704.
52. A receptors in Caenorhabditis elegans. Journal of Neuroscience, 26, 1711-1720.
53. Sabatini, D. M., Barrow, R. K., Blackshaw, S., Burnett, P. E., Lai, M. M., Field, M. E. et al. (1999). Interaction of RAFT1 with gephyrin required for rapamycin-sensitive signaling. Science, 284, 1161-1164.
54. Sassoé-Pognetto, M., Kirsch, J., Grunert, U., Greferath, U., Fritschy, J. M., Mohler, H. et al. (1995). Colocalization of gephyrin and GABAA-receptor subunits in the rat retina. Journal of Comparative Neurology, 357, 1-14.
55. Scornik, O. A. (1984). Effects of inhibitors of protein degradation on the rate of protein synthesis in Chinese hamster ovary cells. Journal of Cellular Physiology, 121, 257-262.
56. Scheff, S. W., Price, D. A., Schmitt, F. A., & Mufson, E. J. (2006). Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiology of Aging, 27, 1372-1384.
57. Stokin, G. B., Lillo, C., Falzone, T. L., Brusch, R. G., Rockenstein, E., Mount, S. L. et al. (2005). Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science, 307, 1282-1288.
58. Studler, B., Fritschy, J.-M., & Brunig, I. (2002). GABAergic and glutamatergic terminals differentially influence the organization of GABAergic synapses in rat cerebellar granule cells in vitro. Neuroscience, 114, 123-133.
59. Studler, B., Sidler, C., & Fritschy, J. M. (2005). Differential regulation of GABA(A) receptor and gephyrin postsynaptic clustering in immature hippocampal neuronal cultures. Journal of Comparative Neurology, 484, 344-355.
60. Takauchi, S., & Miyoshi, K. (1995). Cytoskeletal changes in rat cortical neurons induced by long-term intraventricular infusion of leupeptin. Acta Neuropathologica, 89, 8-16.
61. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R. et al. (1991). Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Annals of Neurology, 30, 572-580.
62. Tomita, S., Adesnik, H., Sekiguchi, M., Zhang, W., Wada, K., Howe, J. R. et al. (2005). Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature, 435, 1052-1058.
63. van Zundert, B., Albarran, F. A., & Aguayo, L. G. (2000). Effects of chronic ethanol treatment on gamma-aminobutyric acid(A) and glycine receptors in mouse glycinergic spinal neurons. Journal of Pharmacology and Experimental Therapeutics, 295, 423-429.
64. Vornov, J. J., Tasker, R. C., & Coyle, J. T. (1994). Delayed protection by MK-801 and tetrodotoxin in a rat organotypic hippocampal culture. Stroke, 25, 457-464.
65. Waldvogel, H. J., Baer, K., Snell, R. G., During, M. J., Faull, R. L. M., & Rees, M. I. (2003). Distribution of gephyrin in the human brain: an immunohistochemical analysis. Neuroscience, 116, 145-156.
66. Wheal, H. V., Chen, Y., Mitchell, S. M., Maerz, W., Wieland, H., van Rossum, D. et al. (1998). Molecular mechanisms that underlie structural and functional changes at the postsynaptic membrane during synaptic plasticity. Progress in Neurobiology, 55, 611-640.