Synaptic autoregulation by metalloproteases and γ-secretase

Journal of Neuroscience

Volumn 31, Issue 34, 2011, Pages 12083-12093

  Restituito, Sophie ^a   Khatri, Latika ^a   Ninan, Ipe ^b   Mathews, Paul M ^b,c   Liu, Xin ^d   Weinberg, Richard J ^e   Ziff, Edward B ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GAMMA SECRETASE; METALLOPROTEINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; PLAKOGLOBIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME SUBSTRATE; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CATENINS; CELLS, CULTURED; FEMALE; HIPPOCAMPUS; HOMEOSTASIS; MALE; METALLOPROTEASES; MICE; MICE, KNOCKOUT; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION;

EID: 80052176398     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2513-11.2011     Document Type: Article

References (51)

1. Auffret A, Gautheron V, Repici M, Kraftsik R, Mount HT, Mariani J, Rovira C, (2009) Age-dependent impairment of spine morphology and synaptic plasticity in hippocampal CA1 neurons of a presenilin 1 transgenic mouse model of Alzheimer's disease. J Neurosci 29:10144-10152.
2. Bao J, Lin H, Ouyang Y, Lei D, Osman A, Kim TW, Mei L, Dai P, Ohlemiller KK, Ambron RT (2004) Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nat Neurosci 7:1250-1258.
3. Brückner K, Pablo Labrador J, Scheiffele P, Herb A, Seeburg PH, Klein R, (1999) EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 22:511-524.
4. Cartier AE, Djakovic SN, Salehi A, Wilson SM, Masliah E, Patrick GN, (2009) Regulation of synaptic structure by ubiquitin C-terminal hydrolase L1. J Neurosci 29:7857-7868.
5. Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci 8:206-220.
6. Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8:458-467.
7. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
8. Farmery MR, Tjernberg LO, Pursglove SE, Bergman A, Winblad B, Näslund J, (2003) Partial purification and characterization of gamma-secretase from post-mortem human brain. J Biol Chem 278:24277-24284.
9. Georgakopoulos A, Marambaud P, Friedrich VL Jr, Shioi J, Efthimiopoulos S, Robakis NK, (2000) Presenilin-1: a component of synaptic and endothelial adherens junctions. Ann NY Acad Sci 920:209-214.
10. Georgakopoulos A, Litterst C, Ghersi E, Baki L, Xu C, Serban G, Robakis NK (2006) Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. EMBO J 25:1242-1252.
11. Haapasalo A, Kim DY, Carey BW, Turunen MK, Pettingell WH, Kovacs DM (2007) Presenilin/gamma-secretase-mediated cleavage regulates association of leukocyte-common antigen-related (LAR) receptor tyrosine phosphatase with beta-catenin. J Biol Chem 282:9063-9072.
12. Hass MR, Sato C, Kopan R, Zhao G (2009) Presenilin: RIP and beyond. Semin Cell Dev Biol 20:201-210.
13. Israely I, Costa RM, Xie CW, Silva AJ, Kosik KS, Liu X, (2004) Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction. Curr Biol 14:1657-1663.
14. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, Neubert TA (2004) Identification and verification of novel rodent postsynaptic density proteins. Mol Cell Proteomics 3:857-871.
15. Kaether C, Haass C, Steiner H (2006) Assembly, trafficking and function of gamma-secretase. Neurodegener Dis 3:275-283.
16. Knobloch M, Mansuy IM (2008) Dendritic spine loss and synaptic alterations in Alzheimer's disease. Mol Neurobiol 37:73-82.
17. Kosik KS, Donahue CP, Israely I, Liu X, Ochiishi T (2005) Delta-catenin at the synaptic-adherens junction. Trends Cell Biol 15:172-178.
18. Kouchi Z, Barthet G, Serban G, Georgakopoulos A, Shioi J, Robakis NK (2009) p120 catenin recruits cadherins to γ-secretase and inhibits production of Aβ peptide. J Biol Chem 284:1954-1961.
19. Lah JJ, Heilman CJ, Nash NR, Rees HD, Yi H, Counts SE, Levey AI (1997) Light and electron microscopic localization of presenilin-1 in primate brain. J Neurosci 17:1971-1980.
20. Lee HK, Kameyama K, Huganir RL, Bear MF (1998) NMDA induces longterm synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21:1151-1162.
21. Leonoudakis D, Conti LR, Radeke CM, McGuire LM, Vandenberg CA (2004) A multiprotein trafficking complex composed of SAP97, CASK, Veli, and Mint1 is associated with inward rectifier Kir2 potassium channels. J Biol Chem 279:19051-19063.
22. Levesque G, Yu G, Nishimura M, Zhang DM, Levesque L, Yu H, Xu D, Liang Y, Rogaeva E, Ikeda M, Duthie M, Murgolo N, Wang L, VanderVere P, Bayne ML, Strader CD, Rommens JM, Fraser PE, St George-Hyslop P (1999) Presenilins interact with armadillo proteins including neuralspecific plakophilin-related protein and beta-catenin. J Neurochem 72:999-1008.
23. Li YM, Lai MT, Xu M, Huang Q, DiMuzio-Mower J, Sardana MK, Shi XP, Yin KC, Shafer JA, Gardell SJ (2000) Presenilin 1 is linked with gammasecretase activity in the detergent solubilized state. Proc Natl Acad Sci U S A 97:6138-6143.
24. Mabb AM, Ehlers MD (2010) Ubiquitination in postsynaptic function and plasticity. Annu Rev Cell Dev Biol 26:179-210.
25. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61:541-555.
26. Malinverno M, Carta M, Epis R, Marcello E, Verpelli C, Cattabeni F, Sala C, Mulle C, Di Luca M, Gardoni F (2010) Synaptic localization and activity of ADAM10 regulate excitatory synapses through N-cadherin cleavage. J Neurosci 30:16343-16355.
27. Marambaud P, Wen PH, Dutt A, Shioi J, Takashima A, Siman R, Robakis NK (2003) A CBP binding transcriptional repressor produced by the PS1/ epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114:635-645.
28. Marcello E, Gardoni F, Mauceri D, Romorini S, Jeromin A, Epis R, Borroni B, Cattabeni F, Sala C, Padovani A, Di Luca M (2007) Synapse-associated protein-97 mediates alpha-secretase ADAM10 trafficking and promotes its activity. J Neurosci 27:1682-1691.
29. Matteoli M, Takei K, Perin MS, Südhof TC, De Camilli P (1992) Exoendocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 117:849-861.
30. McCarthy JV, Twomey C, Wujek P (2009) Presenilin-dependent regulated intramembrane proteolysis and gamma-secretase activity. Cell Mol Life Sci 66:1534-1555.
31. Miller CC, McLoughlin DM, Lau KF, Tennant ME, Rogelj B (2006) The X11 proteins, Abeta production and Alzheimer's disease. Trends Neurosci 29:280-285.
32. Monea S, Jordan BA, Srivastava S, DeSouza S, Ziff EB (2006) Membrane localization of membrane type 5 matrix metalloproteinase by AMPA receptor binding protein and cleavage of cadherins. J Neurosci 26:2300-2312.
33. Osten P, Srivastava S, Inman GJ, Vilim FS, Khatri L, Lee LM, States BA, Einheber S, Milner TA, Hanson PI, Ziff EB (1998) The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha-and beta-SNAPs. Neuron 21:99-110.
34. Parent AT, Barnes NY, Taniguchi Y, Thinakaran G, Sisodia SS (2005) Presenilin attenuates receptor-mediated signaling and synaptic function. J Neurosci 25:1540-1549.
35. Peiretti F, Deprez-Beauclair P, Bonardo B, Aubert H, Juhan-Vague I, Nalbone G (2003) Identification of SAP97 as an intracellular binding partner of TACE. J Cell Sci 116:1949-1957.
36. Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W, Shan WS, Arndt K, Frank M, Gordon RE, Gawinowicz MA, Zhao Y, Colman DR (2001) The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 32:63-77.
37. Postina R (2008) A closer look at alpha-secretase. Current Alzheimer research 5:179-186.
38. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337-351.
39. Pratt KG, Zhu P, Watari H, Cook DG, Sullivan JM (2011) A novel role for {gamma}-secretase: selective regulation of spontaneous neurotransmitter release from hippocampal neurons. J Neurosci 31:899-906.
40. Reiss K, Maretzky T, Ludwig A, Tousseyn T, de Strooper B, Hartmann D, Saftig P (2005) ADAM10 cleavage of N-cadherin and regulation of cell- celladhesion and beta-catenin nuclear signalling. EMBO J 24:742-752.
41. Saura CA, Choi SY, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao BS, Chattarji S, Kelleher RJ 3rd, Kandel ER, Duff K, Kirkwood A, Shen J (2004) Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42:23-36.
42. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284.
43. Silverman JB, Restituito S, Lu W, Lee-Edwards L, Khatri L, Ziff EB (2007) Synaptic anchorage of AMPA receptors by cadherins through neural plakophilin-related arm protein AMPA receptor-binding protein complexes. J Neurosci 27:8505-8516.
44. Tai CY, Mysore SP, Chiu C, Schuman EM (2007) Activity-regulated N-cadherin endocytosis. Neuron 54:771-785.
45. Tanahashi H, Tabira T (1999) Isolation of human delta-catenin and its binding specificity with presenilin 1. Neuroreport 10:563-568.
46. Tanaka H, Shan W, Phillips GR, Arndt K, Bozdagi O, Shapiro L, Huntley GW, Benson DL, Colman DR (2000) Molecular modification of N-cadherin in response to synaptic activity. Neuron 25:93-107.
47. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283:29615-29619.
48. Uemura K, Kihara T, Kuzuya A, Okawa K, Nishimoto T, Ninomiya H, Sugimoto H, Kinoshita A, Shimohama S (2006) Characterization of sequential N-cadherin cleavage by ADAM10 and PS1. Neurosci Lett 402:278-283.
49. Wierenga CJ, Walsh MF, Turrigiano GG (2006) Temporal regulation of the expression locus of homeostatic plasticity. J Neurophysiol 96:2127-2133.
50. Zhang Q, Thomas SM, Lui VW, Xi S, Siegfried JM, Fan H, Smithgall TE, Mills GB, Grandis JR (2006) Phosphorylation of TNF-alpha converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation. Proc Natl Acad Sci U S A 103:6901-6906.
51. Zhou J, Liyanage U, Medina M, Ho C, Simmons AD, Lovett M, Kosik KS (1997) Presenilin 1 interaction in the brain with a novel member of the Armadillo family. Neuroreport 8:2085-2090.