Drebrin A regulates hippocampal LTP and hippocampus-dependent fear learning in adult mice

Neuroscience

Volumn 324, Issue , 2016, Pages 218-226

  Kojima, N ^a,b   Yasuda, H ^a   Hanamura, K ^a   Ishizuka, Y ^a   Sekino, Y ^a,c   Shirao, T ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOYO UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

Drebrin A; Drebrin E; Fear learning; Hippocampus; Isoform conversion; Synaptic plasticity

Indexed keywords

DREBRIN; DREBRIN A; DREBRIN E; ISOPROTEIN; UNCLASSIFIED DRUG; DREBRINS; NEUROPEPTIDE;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CONTROLLED STUDY; DENDRITE; FEAR; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; HISTOPATHOLOGY; LEARNING; LONG TERM POTENTIATION; MALE; MOUSE; MOUSE MUTANT; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; SYNAPSE; AGING; ANIMAL; C57BL MOUSE; CONDITIONING; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; TISSUE CULTURE TECHNIQUE;

AGING; ANIMALS; CONDITIONING (PSYCHOLOGY); DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; FEAR; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPEPTIDES; PROTEIN ISOFORMS; TISSUE CULTURE TECHNIQUES;

EID: 84961233625     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.03.015     Document Type: Article

References (52)

1. Aoki C., Sekino Y., Hanamura K., Fujisawa S., Mahadomrongkul V., Ren Y., Shirao T. Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J Comp Neurol 2005, 483:383-402.
2. Aoki C., Kojima N., Sabaliauskas N., Shah L., Ahmed T.H., Oakford J., Ahmed T., Yamazaki H., Hanamura K., Shirao T. Drebrin A knockout eliminates the rapid form of homeostatic synaptic plasticity at excitatory synapses of intact adult cerebral cortex. J Comp Neurol 2009, 517:105-121.
3. Bellot A., Guivernau B., Tajes M., Bosch-Morato M., Valls-Comamala V., Munoz F.J. The structure and function of actin cytoskeleton in mature glutamatergic dendritic spines. Brain Res 2014, 1573:1-16.
4. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
5. Bosch M., Hayashi Y. Structural plasticity of dendritic spines. Curr Opin Neurobiol 2012, 22:383-388.
6. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 2008, 31:47-67.
7. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., Rostaing P., Triller A., Salem N., Ashe K.H., Frautschy S.A., Cole G.M. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43:633-645.
8. Carlisle H.J., Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci 2005, 28:182-187.
9. Fiala J.C., Spacek J., Harris K.M. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res Brain Res Rev 2002, 39:29-54.
10. Fifkova E., Delay R.J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol 1982, 95:345-350.
11. Fujisawa S., Shirao T., Aoki C. In vivo, competitive blockade of N-methyl-d-aspartate receptors induces rapid changes in filamentous actin and drebrin A distributions within dendritic spines of adult rat cortex. Neuroscience 2006, 140:1177-1187.
12. Fukazawa Y., Saitoh Y., Ozawa F., Ohta Y., Mizuno K., Inokuchi K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 2003, 38:447-460.
13. Grintsevich E.E., Galkin V.E., Orlova A., Ytterberg A.J., Mikati M.M., Kudryashov D.S., Loo J.A., Egelman E.H., Reisler E. Mapping of drebrin binding site on F-actin. J Mol Biol 2010, 398:542-554.
14. Hatanpaa K., Isaacs K.R., Shirao T., Brady D.R., Rapoport S.I. Loss of proteins regulating synaptic plasticity in normal aging of the human brain and in Alzheimer disease. J Neuropathol Exp Neurol 1999, 58:637-643.
15. Hayashi K., Ishikawa R., Kawai-Hirai R., Takagi T., Taketomi A., Shirao T. Domain analysis of the actin-binding and actin-remodeling activities of drebrin. Exp Cell Res 1999, 253:673-680.
16. Hayashi K., Ishikawa R., Ye L.H., He X.L., Takata K., Kohama K., Shirao T. Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J Neurosci 1996, 16:7161-7170.
17. Ishikawa R., Hayashi K., Shirao T., Xue Y., Takagi T., Sasaki Y., Kohama K. Drebrin, a development-associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J Biol Chem 1994, 269:29928-29933.
18. Ishizuka Y., Shimizu H., Takagi E., Kato M., Yamagata H., Mikuni M., Shirao T. Histone deacetylase mediates the decrease in drebrin cluster density induced by amyloid beta oligomers. Neurochem Int 2014, 76:114-121.
19. Jensen V., Kaiser K.M., Borchardt T., Adelmann G., Rozov A., Burnashev N., Brix C., Frotscher M., Andersen P., Hvalby O., Sakmann B., Seeburg P.H., Sprengel R. A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J Physiol 2003, 553:843-856.
20. Jin M., Tanaka S., Sekino Y., Ren Y., Yamazaki H., Kawai-Hirai R., Kojima N., Shirao T. A novel, brain-specific mouse drebrin: cDNA cloning, chromosomal mapping, genomic structure, expression, and functional characterization. Genomics 2002, 79:686-692.
21. Kanda Y. Investigation of the freely available easy-to-use software 'EZR' for medical statistics. Bone Marrow Transplant 2013, 48:452-458.
22. Keon B.H., Jedrzejewski P.T., Paul D.L., Goodenough D.A. Isoform specific expression of the neuronal F-actin binding protein, drebrin, in specialized cells of stomach and kidney epithelia. J Cell Sci 2000, 113(Pt 2):325-336.
23. Kojima N., Shirao T., Obata K. Molecular cloning of a developmentally regulated brain protein, chicken drebrin A and its expression by alternative splicing of the drebrin gene. Brain Res Mol Brain Res 1993, 19:101-114.
24. Kojima N., Hanamura K., Yamazaki H., Ikeda T., Itohara S., Shirao T. Genetic disruption of the alternative splicing of drebrin gene impairs context-dependent fear learning in adulthood. Neuroscience 2010, 165:138-150.
25. Landis D.M., Reese T.S. Cytoplasmic organization in cerebellar dendritic spines. J Cell Biol 1983, 97:1169-1178.
26. Lynch G., Rex C.S., Gall C.M. Synaptic plasticity in early aging. Ageing Res Rev 2006, 5:255-280.
27. Malenka R.C., Nicoll R.A. Long-term potentiation-a decade of progress?. Science 1999, 285:1870-1874.
28. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
29. Matus A. Actin-based plasticity in dendritic spines. Science 2000, 290:754-758.
30. Mikati M.A., Grintsevich E.E., Reisler E. Drebrin-induced stabilization of actin filaments. J Biol Chem 2013, 288:19926-19938.
31. Misane I., Tovote P., Meyer M., Spiess J., Ogren S.O., Stiedl O. Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 2005, 15:418-426.
32. Mizui T., Sekino Y., Yamazaki H., Ishizuka Y., Takahashi H., Kojima N., Kojima M., Shirao T. Myosin II ATPase activity mediates the long-term potentiation-induced exodus of stable F-actin bound by drebrin A from dendritic spines. PLoS One 2014, 9:e85367.
33. Nepliouev I., Zhang Z.S., Stiber J.A. Effect of oxidative stress on homer scaffolding proteins. PLoS One 2011, 6:e26128.
34. Poukkula M., Kremneva E., Serlachius M., Lappalainen P. Actin-depolymerizing factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Cytoskeleton (Hoboken) 2011, 68:471-490.
35. Rex C.S., Gavin C.F., Rubio M.D., Kramar E.A., Chen L.Y., Jia Y., Huganir R.L., Muzyczka N., Gall C.M., Miller C.A., Lynch G., Rumbaugh G. Myosin IIb regulates actin dynamics during synaptic plasticity and memory formation. Neuron 2010, 67:603-617.
36. Rosenzweig E.S., Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 2003, 69:143-179.
37. Ryan M.M., Guevremont D., Luxmanan C., Abraham W.C., Williams J.M. Aging alters long-term potentiation-related gene networks and impairs synaptic protein synthesis in the rat hippocampus. Neurobiol Aging 2015, 36:1868-1880.
38. Ryu J., Liu L., Wong T.P., Wu D.C., Burette A., Weinberg R., Wang Y.T., Sheng M. A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 2006, 49:175-182.
39. Sekino Y., Kojima N., Shirao T. Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int 2007, 51:92-104.
40. Sekino Y., Tanaka S., Hanamura K., Yamazaki H., Sasagawa Y., Xue Y., Hayashi K., Shirao T. Activation of N-methyl-d-aspartate receptor induces a shift of drebrin distribution: disappearance from dendritic spines and appearance in dendritic shafts. Mol Cell Neurosci 2006, 31:493-504.
41. Shiraishi-Yamaguchi Y., Sato Y., Sakai R., Mizutani A., Knopfel T., Mori N., Mikoshiba K., Furuichi T. Interaction of Cupidin/Homer2 with two actin cytoskeletal regulators, Cdc42 small GTPase and Drebrin, in dendritic spines. BMC Neurosci 2009, 10:25.
42. Shirao T., Gonzalez-Billault C. Actin filaments and microtubules in dendritic spines. J Neurochem 2013, 126:155-164.
43. Shirao T., Obata K. Immunochemical homology of 3 developmentally regulated brain proteins and their developmental change in neuronal distribution. Brain Res 1986, 394:233-244.
44. Shirao T., Kojima N., Nabeta Y., Obata K. Two forms of drebrins, developmentally regulated brain proteins, in rat. Proc Japan Acad 1989, 65:169-172.
45. Song M., Kojima N., Hanamura K., Sekino Y., Inoue H.K., Mikuni M., Shirao T. Expression of drebrin E in migrating neuroblasts in adult rat brain: coincidence between drebrin E disappearance from cell body and cessation of migration. Neuroscience 2008, 152:670-682.
46. Tada T., Sheng M. Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 2006, 16:95-101.
47. Takahashi H., Mizui T., Shirao T. Down-regulation of drebrin A expression suppresses synaptic targeting of NMDA receptors in developing hippocampal neurones. J Neurochem 2006, 97(Suppl. 1):110-115.
48. Takahashi H., Yamazaki H., Hanamura K., Sekino Y., Shirao T. Activity of the AMPA receptor regulates drebrin stabilization in dendritic spine morphogenesis. J Cell Sci 2009, 122:1211-1219.
49. Watson J.B., Arnold M.M., Ho Y.S., O'Dell T.J. Age-dependent modulation of hippocampal long-term potentiation by antioxidant enzymes. J Neurosci Res 2006, 84:1564-1574.
50. Xu W., Stamnes M. The actin-depolymerizing factor homology and charged/helical domains of drebrin and mAbp1 direct membrane binding and localization via distinct interactions with actin. J Biol Chem 2006, 281:11826-11833.
51. Yasuda H., Mukai H. Turning off of GluN2B subunits and on of CICR in hippocampal LTD induction after developmental GluN2 subunit switch. Hippocampus 2015.
52. Yasuda H., Barth A.L., Stellwagen D., Malenka R.C. A developmental switch in the signaling cascades for LTP induction. Nat Neurosci 2003, 6:15-16.