Synaptic activity prompts γ-secretase-mediated cleavage of EphA4 and dendritic spine formation

Journal of Cell Biology

Volumn 185, Issue 3, 2009, Pages 551-564

  Inoue, Eiji ^a   Deguchi Tawarada, Maki ^a   Togawa, Aki ^a   Matsui, Chiyuki ^a   Arita, Kohei ^a   Katahira Tayama, Sayaka ^a   Sato, Toshitaka ^b   Yamauchi, Emiko ^b   Oda, Yoshiya ^b   Takai, Yoshimi ^c  

^a KAN Research Institute ^*  (Japan)

^b EISAI CO LTD   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR A4; GAMMA SECRETASE; MATRIX METALLOPROTEINASE; PRESENILIN 1; RAC PROTEIN; DIMETHYL SULFOXIDE; SECRETASE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRANCHING MORPHOGENESIS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME SUBSTRATE; HIPPOCAMPUS; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; CYTOLOGY; DENDRITE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; METABOLISM; NERVE CELL; NEUROFIBRILLARY TANGLE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINE; SYNAPSE;

ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; DENDRITES; DIMETHYL SULFOXIDE; HIPPOCAMPUS; HUMANS; MICE; NEUROFIBRILLARY TANGLES; NEURONS; RATS; RECEPTOR, EPHA4; SPINE; SYNAPSES;

EID: 65649092174     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200809151     Document Type: Article

References (50)

1. Annaert, W.G., L. Levesque, K. Craessaerts, I. Dierinck, G. Snellings, D. Westaway, P. St. George-Hyslop, B. Cordell, P. Fraser, and B. De Strooper. 1999. Presenilin 1 controls γ-secretase processing of the amyloid precursor protein in pre-Golgi compartments of hippocampal neurons. J. Cell Biol. 147:277-294.
2. Aoto, J., and L. Chen. 2007. Bidirectional ephrin/Eph signaling in synaptic functions. Brain Res. 1184:72-80.
3. Arriagada, P.V., K. Marzloff, and B.T. Hyman. 1992. Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology. 42:1681-1688.
4. Beher, D., C. Elle, J. Underwood, J.B. Davis, R. Ward, E. Karran, C.L. Masters, K. Beyreuther, and G. Multhaup. 1999. Proteolytic fragments of Alzheimer's disease-associated presenilin 1 are present in synaptic organelles and growth cone membranes of rat brain. J. Neurochem. 72:1564-1573.
5. Bentahir, M., O. Nyabi, J. Verhamme, A. Tolia, K. Horré, J. Wiltfang, H. Esselmann, and B. De Strooper. 2006. Presenilin clinical mutations can affect ?-secretase activity by different mechanisms. J. Neurochem. 96:732-742.
6. Bickel, P.E., P.E. Scherer, J.E. Schnitzer, P. Oh, M.P. Lisanti, and H.F. Lodish. 1997. Flotillin and epidermal surface antigen defne a new family of caveolaeassociated integral membrane proteins. J. Biol. Chem. 272:13793-13802.
7. Bourgin, C., K.K. Murai, M. Richter, and E.B. Pasquale. 2007. The EphA4 receptor regulates dendritic spine remodeling by affecting β1-integrin signaling pathways. J. Cell Biol. 178:1295-1307.
8. Derkach, V.A., M.C. Oh, E.S. Guire, and T.R. Soderling. 2007. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8:101-113.
9. De Strooper, B. 2003. Aph-1, Pen-2, and Nicastrin with Presenilin generate an active γ-secretase complex. Neuron. 38:9-12.
10. Elia, L.P., M. Yamamoto, K. Zang, and L.F. Reichardt. 2006. p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron. 51:43-56.
11. Fu, W.Y., Y. Chen, M. Sahin, X.S. Zhao, L. Shi, J.B. Bikoff, K.O. Lai, W.H. Yung, A.K. Fu, M.E. Greenberg, and N.Y. Ip. 2007. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 10:67-76.
12. Garcia, R.A., K. Vasudevan, and A. Buonanno. 2000. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc. Natl. Acad. Sci. USA. 97:3596-3601.
13. Georgakopoulos, A., C. Litterst, E. Ghersi, L. Baki, C. Xu, G. Serban, and N.K. Robakis. 2006. Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. EMBO J. 25:1242-1252.
14. Haapasalo, A., D.Y. Kim, B.W. Carey, M.K. Turunen, W.H. Pettingell, and D.M. Kovacs. 2007. Presenilin/γ-secretase-mediated cleavage regulates associa-tion of leukocyte-common antigen-related (LAR) receptor tyrosine phospha-tase with β-catenin. J. Biol. Chem. 282:9063-9072.
15. Hering, H., C.C. Lin, and M. Sheng. 2003. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23:3262-3271.
16. Herreman, A., D. Hartmann, W. Annaert, P. Saftig, K. Craessaerts, L. Serneels, L. Umans, V. Schrijvers, F. Checler, H. Vanderstichele, et al. 1999. Presenilin 2 defciency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 defciency. Proc. Natl. Acad. Sci. USA. 96:11872-11877.
17. Herreman, A., G. Van Gassen, M. Bentahir, O. Nyabi, K. Craessaerts, U. Mueller, W. Annaert, and B. De Strooper. 2003. γ-secretase activity requires the presenilin-dependent traffcking of nicastrin through the Golgi apparatus but not its complex glycosylation. J. Cell Sci. 116:1127-1136.
18. Hoogenraad, C.C., M.I. Feliu-Mojer, S.A. Spangler, A.D. Milstein, A.W. Dunah, A.Y. Hung, and M. Sheng. 2007. Liprin α1 degradation by calcium/calmodulin-dependent protein kinase II regulates LAR receptor tyrosine phosphatase distribution and dendrite development. Dev. Cell. 12:587-602.
19. Inoue, E., S. Mochida, H. Takagi, S. Higa, M. Deguchi-Tawarada, E. TakaoRikitsu, M. Inoue, I. Yao, K. Takeuchi, I. Kitajima, et al. 2006. SAD: a presynaptic kinase associated with synaptic vesicles and the active zone cytomatrix that regulates neurotransmitter release. Neuron. 50:261-275.
20. Isaac, J.T., R.A. Nicoll, and R.C. Malenka. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron. 15:427-434.
21. Iwasato, T., H. Katoh, H. Nishimaru, Y. Ishikawa, H. Inoue, Y.M. Saito, R. Ando, M. Iwama, R. Takahashi, M. Negishi, and S. Itohara. 2007. RacGAP α-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell. 130:742-753.
22. Kamal, A., A. Almenar-Queralt, J.F. LeBlanc, E.A. Roberts, and L.S. Goldstein. 2001. Kinesin-mediated axonal transport of a membrane compartment containing β-secretase and presenilin-1 requires APP. Nature. 414:643-648.
23. Kazee, A.M., and E.M. Johnson. 1998. Alzheimer's disease pathology in non-demented elderly. J. Alzheimers Dis. 1:81-89.
24. Kim, E., and M. Sheng. 2004. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5:771-781.
25. Kopec, C.D., B. Li, W. Wei, J. Boehm, and R. Malinow. 2006. Glutamate receptor exocytosis and spine enlargement during chemically induced longterm potentiation. J. Neurosci. 26:2000-2009.
26. Landman, N., and T.W. Kim. 2004. Got RIP? Presenilin-dependent intramembrane proteolysis in growth factor receptor signaling. Cytokine Growth Factor Rev. 15:337-351.
27. Le Borgne, R., A. Bardin, and F. Schweisguth. 2005. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development. 132:1751-1762.
28. Litterst, C., A. Georgakopoulos, J. Shioi, E. Ghersi, T. Wisniewski, R. Wang, A. Ludwig, and N.K. Robakis. 2007. Ligand binding and calcium infux induce distinct ectodomain/γ-secretase-processing pathways of EphB2 receptor. J. Biol. Chem. 282:16155-16163.
29. Machesky, L.M., and A. Hall. 1997. Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J. Cell Biol. 138:913-926.
30. Marambaud, P., P.H. Wen, A. Dutt, J. Shioi, A. Takashima, R. Siman, and N.K. Robakis. 2003. A CBP binding transcriptional repressor produced by the PS1/ε-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell. 114:635-645.
31. Maretzky, T., M. Schulte, A. Ludwig, S. Rose-John, C. Blobel, D. Hartmann, P. Altevogt, P. Saftig, and K. Reiss. 2005. L1 is sequentially processed by two differently activated metalloproteases and presenilin/γ- secretase and regulates neural cell adhesion, cell migration, and neurite outgrowth. Mol. Cell. Biol. 25:9040-9053.
32. Matsuzaki, M., G.C. Ellis-Davies, T. Nemoto, Y. Miyashita, M. Iino, and H. Kasai. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4:1086-1092.
33. Moehlmann, T., E. Winkler, X. Xia, D. Edbauer, J. Murrell, A. Capell, C. Kaether, H. Zheng, B. Ghetti, C. Haass, and H. Steiner. 2002. Presenilin-1 mutations of leucine 166 equally affect the generation of the Notch and APP intracellular domains independent of their effect on Aβ 42 production. Proc. Natl. Acad. Sci. USA. 99:8025-8030.
34. Murai, K.K., L.N. Nguyen, F. Irie, Y. Yamaguchi, and E.B. Pasquale. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6:153-160.
35. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Effcient selection for high-expression transfectants with a novel eukaryotic vector. Gene. 108:193-199.
36. Oh, M.C., V.A. Derkach, E.S. Guire, and T.R. Soderling. 2006. Extrasynaptic membrane traffcking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J. Biol. Chem. 281:752-758.
37. Otmakhov, N., L. Khibnik, N. Otmakhova, S. Carpenter, S. Riahi, B. Asrican, and J. Lisman. 2004. Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J. Neurophysiol. 91:1955-1962.
38. Penzes, P., M.E. Cahill, K.A. Jones, and D.P. Srivastava. 2008. Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol. 18:405-413.
39. Ramakers, G.J. 2002. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 25:191-199.
40. Rechards, M., W. Xia, V.M. Oorschot, D.J. Selkoe, and J. Klumperman. 2003. Presenilin-1 exists in both pre- and post-Golgi compartments and recycles via COPI-coated membranes. Traffc. 4:553-565.
41. Rumbaugh, G., J.P. Adams, J.H. Kim, and R.L. Huganir. 2006. SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons. Proc. Natl. Acad. Sci. USA. 103:4344-4351.
42. Saura, C.A., S.Y. Choi, V. Beglopoulos, S. Malkani, D. Zhang, B.S. Shankaranarayana Rao, S. Chattarji, R.J. Kelleher III, E.R. Kandel, K. Duff, et al. 2004. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron. 42:23-36.
43. Scheff, S.W., D.A. Price, F.A. Schmitt, and E.J. Mufson. 2006. Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging. 27:1372-1384.
44. Tabata, T., T. Sato, J. Kuromitsu, and Y. Oda. 2007. Pseudo internal standard approach for label-free quantitative proteomics. Anal. Chem. 79:8440-8445.
45. Tashiro, A., and R. Yuste. 2004. Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Mol. Cell. Neurosci. 26:429-440.
46. Van de Ven, T.J., H.M. VanDongen, and A.M. VanDongen. 2005. The nonkinase phorbol ester receptor α1-chimerin binds the NMDA receptor NR2A sub-unit and regulates dendritic spine density. J. Neurosci. 25:9488-9496.
47. Vetrivel, K.S., H. Cheng, W. Lin, T. Sakurai, T. Li, N. Nukina, P.C. Wong, H. Xu, and G. Thinakaran. 2004. Association of γ-secretase with lipid rafts in post-Golgi and endosome membranes. J. Biol. Chem. 279:44945-44954.
48. Walsh, D.M., and D.J. Selkoe. 2004. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron. 44:181-193.
49. Xie, Z., D.P. Srivastava, H. Photowala, L. Kai, M.E. Cahill, K.M. Woolfrey, C.Y. Shum, D.J. Surmeier, and P. Penzes. 2007. Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron. 56:640-656.
50. Zhao, L., Q.L. Ma, F. Calon, M.E. Harris-White, F. Yang, G.P. Lim, T. Morihara, O.J. Ubeda, S. Ambegaokar, J.E. Hansen, et al. 2006. Role of p21-activated kinase pathway defects in the cognitive defcits of Alzheimer disease. Nat. Neurosci. 9:234-242.