Loss of F-box only protein 2 (Fbxo2) disrupts levels and localization of select NMDA receptor subunits, and promotes aberrant synaptic connectivity

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 6165-6178

  Atkin, Graham ^a,f   Moore, Shannon ^b   Lu, Yuan ^c,d   Nelson, Rick F ^e   Tipper, Nathan ^a   Rajpal, Gautam ^a   Hunt, Jack ^a   Tennant, William ^a   Hell, Johannes W ^c   Murphy, Geoffrey G ^a,b   Paulson, Henry ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF IOWA   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Van Andel Research Center   (United States)

Author keywords

Fbxo2; GluN1; GluN2A; NMDA; Synapse

Indexed keywords

F BOX ONLY PROTEIN 2; GLUN1 RECEPTOR; GLUN2A RECEPTOR; IONOTROPIC RECEPTOR; LIGASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMINO ACID RECEPTOR BLOCKING AGENT; F BOX PROTEIN; GPRIN1 PROTEIN, MOUSE; N-METHYL D-ASPARTATE RECEPTOR SUBTYPE 2A; NERVE PROTEIN; SLC17A7 PROTEIN, MOUSE; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOTINYLATION; BRAIN ELECTROPHYSIOLOGY; CELL LYSATE; CONNECTOME; CONTROLLED STUDY; DEGLYCOSYLATION; DNA DETERMINATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LOCALIZATION; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LEARNING; MEMORY CONSOLIDATION; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; QUANTITATIVE ANALYSIS; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN TRANSPORT; SYNAPSE; SYNAPTOSOME; ULTRASTRUCTURE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; BRAIN; CELLS, CULTURED; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; F-BOX PROTEINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; IN VITRO TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PROTEIN TRANSPORT; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTOSOMES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 84929231815     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3013-14.2015     Document Type: Article

References (78)

1. Al-Hallaq RA, Conrads TP, Veenstra TD, Wenthold RJ (2007) NMDA diheteromeric receptor populations and associated proteins in rat hippocampus. J Neurosci 27:8334-8343. CrossRef Medline
2. Ali DW, Salter MW (2001) NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr Opin Neurobiol 11:336-342. CrossRef Medline
3. Aoto J, Ting P, Maghsoodi B, Xu N, Henkemeyer M, Chen L (2007) Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation. J Neurosci 27:7508-7519. CrossRef Medline
4. Arellano JI, Benavides-Piccione R, Defelipe J, Yuste R (2007) Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1:131-143. CrossRef Medline
5. Atkin G, Hunt J, Minakawa E, Sharkey L, Tipper N, Tennant W, Paulson HL (2014) F-box only protein 2 (Fbxo2) regulates amyloid precursor protein levels and processing. J Biol Chem 289:7038-7048. CrossRef Medline
6. Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345-353. CrossRef Medline
7. Bassand P, Bernard A, Rafiki A, Gayet D, Khrestchatisky M (1999) Differential interaction of the tSXV motifs of the NR1 and NR2ANMDA receptor subunits with PSD-95 and SAP97. Eur J Neurosci 11:2031-2043. CrossRef Medline
8. Bloodgood BL, Giessel AJ, Sabatini BL (2009) Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol 7:el000190. CrossRef Medline
9. Bourne JN, Harris KM (2011) Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 21:354-373. CrossRef Medline
10. Chang FL, Greenough WT (1984) Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res 309:35-46. CrossRef Medline
11. Crump FT, Dillman KS, Craig AM (2001) cAMP-dependent protein kinase mediates activity-regulated synaptic targeting of NMDA receptors. J Neurosci 21:5079-5088. Medline
12. Cui-Wang T, Hanus C, Cui T, Helton T, Bourne J, Watson D, Harris KM, Ehlers MD (2012) Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell 148:309-321. CrossRef Medline
13. Dong C, Upadhya SC, Ding L, Smith TK, Hegde AN (2008) Proteasome inhibition enhances the induction and impairs the maintenance of latephase long-term potentiation. Learn Mem 15:335-347. CrossRef Medline
14. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231-242. CrossRef Medline
15. Elias GM, Elias LA, Apostolides PF, Kriegstein AR, Nicoll RA (2008) Differential trafficking of AMP A and NMDA receptors by SAP 102 and PSD-95 underlies synapse development. Proc Natl Acad Sci USA 105:20953-20958. CrossRef Medline
16. Ethell IM, Pasquale EB (2005) Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75:161-205. CrossRef Medline
17. Fallon L, Belanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, Moreau F, Voortman J, Haber M, Rouleau G, Thorarinsdottir T, Brice A, van Bergen En Henegouwen PM, Fon EA (2006) A regulated interaction with the UIM protein Epsl5 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 8:834-842. CrossRef Medline
18. 2+-permeable AMPA receptors recruited by CaM-kinase I. J Neurosci 30:11565-11575. CrossRef Medline
19. Foster KA, McLaughlin N, Edbauer D, Phillips M, Bolton A, Constantine-Paton M, Sheng M (2010) Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation. J Neurosci 30:2676-2685. CrossRef Medline
20. Gardoni F, Bellone C, Cattabeni F, Di Luca M (2001) Protein kinase C activation modulates alpha-calmodulin kinase II binding to NR2A subunit of N-methyl-D-aspartate receptor complex. J Biol Chem 276:7609-7613. CrossRef Medline
21. Gardoni F, Mauceri D, Fiorentini C, Bellone C, Missale C, Cattabeni F, Di Luca M (2003) CaMKII-dependent phosphorylation regulates SAP97/ NR2A interaction. J Biol Chem 278:44745-44752. CrossRef Medline
22. Gladding CM, Sepers MD, Xu J, Zhang LY, Milnerwood AJ, Lombroso PJ, Raymond LA (2012) Calpain and STriatal-Enriched protein tyrosine phosphatase (STEP) activation contribute to extrasynaptic NMDA receptor localization in a Huntington’s disease mouse model. Hum Mol Genet 21:3739-3752. CrossRef Medline
23. Glenn KA, Nelson RF, Wen HM, Mallinger AJ, Paulson HL (2008) Diversity in tissue expression, substrate binding, and SCF complex formation for a lectin family of ubiquitin ligases. J Biol Chem 283:12717-12729. CrossRef Medline
24. Gong B, Chen F, Pan Y, Arrieta-Cruz I, Yoshida Y, Haroutunian V, Pasinetti GM (2010) SCFFbx2-E3-ligase-mediated degradation of BACE1 attenuates Alzheimer’s disease amyloidosis and improves synaptic function. Aging Cell 9:1018-1031. CrossRef Medline
25. Gray JA, Shi Y, Usui H, During MJ, Sakimura K, Nicoll RA (2011) Distinct modes of AMPA receptor suppression at developing synapses by GluN2A and GluN2B: single-cell NMDA receptor subunit deletion in vivo. Neuron 71:1085-1101. CrossRef Medline
26. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, Van Endert P, Amigorena S (2003) ER-phagosome fusion defines an MHC class I crosspresentation compartment in dendritic cells. Nature 425:397-402. CrossRef Medline
27. Hall RA, Soderling TR (1997) Quantitation of AMPA receptor surface expression in cultured hippocampal neurons. Neuroscience 78:361-371. CrossRef Medline
28. Hanus C, Ehlers MD (2008) Secretory outposts for the local processing of membrane cargo in neuronal dendrites. Traffic 9:1437-1445. CrossRef Medline
29. Hardingham GE (2009) Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem Soc Trans 37:1147-1160. CrossRef Medline
30. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11:682-696. CrossRef Medline
31. Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019-1049. CrossRef Medline
32. Helmeke C, Ovtscharoff W Jr, Poeggel G, Braun K (2001) Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cereb Cortex 11:717-727. CrossRef Medline
33. Horak M, Chang K, Wenthold RJ (2008) Masking of the endoplasmic reticulum retention signals during assembly of the NMDA receptor. J Neurosci 28:3500-3509. CrossRef Medline
34. Houde M, Bertholet S, Gagnon E, Brunet S, Goyette G, Laplante A, Princiotta MF, Thibault P, Sacks D, Desjardins M (2003) Phagosomes are competent organelles for antigen cross-presentation. Nature 425:402-406. CrossRef Medline
35. Huang F, Zeng X, Kim W, Balasubramani M, Fortian A, Gygi SP, Yates NA, Sorkin A (2013) Lysine 63-linked polyubiquitination is required for EGF receptor degradation. Proc Natl Acad Sci U S A 110:15722-15727. CrossRef Medline
36. Huang YY, Kandel ER (2007) 5-Hydroxytryptamine induces a protein kinase A/mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J Neurosci 27:3111-3119. CrossRef Medline
37. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257. CrossRef Medline
38. Huh KH, Wenthold RJ (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274:151-157. CrossRef Medline
39. Iliff AJ, Renoux AJ, Krans A, Usdin K, Sutton MA, Todd PK (2013) Impaired activity-dependent FMRP translation and enhanced mGluR-dependent LTD in Fragile X premutation mice. Hum Mol Genet 22: 1180-1192. CrossRef Medline
40. Jeyifous O, Waites CL, Specht CG, Fujisawa S, Schubert M, Lin El, Marshall J, Aoki C, de Silva T, Montgomery JM, Garner CC, Green WN (2009) SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat Neurosci 12:1011-1019. CrossRef Medline
41. Jones TA, Klintsova AY, Kilman VL, Sirevaag AM, Greenough WT (1997) Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiol Learn Mem 68:13-20. CrossRef Medline
42. Jurd R, Thornton C, Wang J, Luong K, Phamluong K, Kharazia V, Gibb SL, Ron D (2008) Mind bomb-2 is an E3 ligase that ubiquitinates the N-methyl-D-aspartate receptor NR2B subunit in a phosphorylation-dependent manner. J Biol Chem 283:301-310. CrossRef Medline
43. Kato A, Rouach N, Nicoll RA, Bredt DS (2005) Activity-dependent NMDA receptor degradation mediated by retrotranslocation and ubiquitination. Proc Natl Acad Sci U S A 102:5600-5605. CrossRef Medline
44. Kim BG, Dai HN, McAtee M, Vicini S, Bregman BS (2007) Labeling of dendritic spines with the carbocyanine dye Dil for confocal microscopic imaging in lightly fixed cortical slices. J Neurosci Methods 162:237-243. CrossRef Medline
45. Kirov SA, Sorra KE, Harris KM (1999) Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876-2886. Medline
46. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9:1117-1124. CrossRef Medline
47. Kwon HB, Sabatini BL (2011) Glutamate induces de novo growth of functional spines in developing cortex. Nature 474:100-104. CrossRef Medline
48. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7:548-562. CrossRef Medline
49. Lee I, Kesner RP (2002) Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat Neurosci 5:162-168. CrossRef Medline
50. Lin Y, Jover-Mengual T, Wong J, Bennett MV, Zukin RS (2006) PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc Natl Acad Sci U S A 103:19902-19907. CrossRef Medline
51. Lussier MP, Nasu-Nishimura Y, Roche KW (2011) Activity-dependent ubiquitination of the AMPA receptor subunit GluA2. J Neurosci 31:3077-3081. CrossRef Medline
52. Megías M, Emri Z, Freund TF, Gulyás Al (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540. CrossRef Medline
53. Meier J, Vannier C, Sergé A, Triller A, Choquet D (2001) Fast and reversible trapping of surface glycine receptors by gephyrin. Nat Neurosci 4:253-260. CrossRef Medline
54. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, BurnashevN, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221. CrossRef Medline
55. Morris RG, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-Daspartate receptor antagonist, AP5. Nature 319:774-776. CrossRef Medline
56. Nelson RF, Glenn KA, Miller VM, Wen H, Paulson HL (2006) A novel route for F-box protein-mediated ubiquitination links CHIP to glycoprotein quality control. J Biol Chem 281:20242-20251. CrossRef Medline
57. Nelson RF, Glenn KA, Zhang Y, Wen H, Knutson T, Gouvion CM, Robinson BK, Zhou Z, Yang B, Smith RJ, Paulson HL (2007) Selective cochlear degeneration in mice lacking the F-box protein, Fbx2, a glycoprotein-specific ubiquitin ligase subunit. J Neurosci 27:5163-5171. CrossRef Medline
58. Newpher TM, Ehlers MD (2008) Glutamate receptor dynamics in dendritic microdomains. Neuron 58:472-497. CrossRef Medline
59. Nikolakopoulou AM, Davies HA, Stewart MG (2006) Passive avoidance training decreases synapse density in the hippocampus of the domestic chick. Eur J Neurosci 23:1054-1062. CrossRef Medline
60. Nikonenko I, Jourdain P, Alberi S, Toni N, Muller D (2002) Activity-induced changes of spine morphology. Hippocampus 12:585-591. CrossRef Medline
61. Parnas D, Linial M (1998) Highly sensitive ELISA-based assay for quantifying protein levels in neuronal cultures. Brain Res Brain Res Protoc 2:333-338. CrossRef Medline
62. Parsons CG, Stöffler A, Danysz W (2007) Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse. Neuropharmacology 53:699-723. CrossRef Medline
63. Petralia RS, Al-Hallaq RA, Wenthold RJ (2009) Trafficking and targeting of NMDA receptors. In: Biology of the NMDA receptor (Van Dongen AM, ed). Boca Raton, FL: CRC.
64. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D (2009) Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63:92-105. CrossRef Medline
65. Poliak TA, McCormack R, Peakman M, Nicholson TR, David AS (2014) Prevalence of anti-N-methyl-d-aspartate (NMDA) antibodies in patients with schizophrenia and related psychoses: a systematic review and metaanalysis. Psychol Med 44:2475-2487. CrossRef Medline
66. Rinaldi T, Kulangara K, Antoniello K, Markram H (2007) Elevated NMDA receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc Natl Acad Sci U S A 104:13501-13506. CrossRef Medline
67. Rowland LM, Astur RS, Jung RE, Bustillo JR, Lauriello J, Yeo RA (2005) Selective cognitive impairments associated with NMDA receptor blockade in humans. Neuropsychopharmacology 30:633-639. CrossRef Medline
68. Segev I, Rail W (1988) Computational study of an excitable dendritic spine. J Neurophysiol 60:499-523. Medline
69. Skeberdis VA, Chevaleyre V, Lau CG, Goldberg JH, Pettit DL, Suadicani SO, Lin Y, Bennett MV, Yuste R, Castillo PE, Zukin RS (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 9:501-510. CrossRef Medline
70. Sutton MA, Wall NR, Aakalu GN, Schuman EM (2004) Regulation of dendritic protein synthesis by miniature synaptic events. Science 304:1979-1983. CrossRef Medline
71. Swanger SA, Yao X, Gross C, Bassell GJ (2011) Automated 4D analysis of dendritic spine morphology: applications to stimulus-induced spine remodeling and pharmacological rescue in a disease model. Mol Brain 4:38. CrossRef Medline
72. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ (1999) Genetic enhancement of learning and memory in mice. Nature 401:63-69. CrossRef Medline
73. Thomas-Crusells J, Vieira A, Saarma M, Rivera C (2003) A novel method for monitoring surface membrane trafficking on hippocampal acute slice preparation. J Neurosci Methods 125:159-166. CrossRef Medline
74. Tovar KR, Westbrook GL (2002) Mobile NMDA receptors at hippocampal synapses. Neuron 34:255-264. CrossRef Medline
75. Tyan SH, Shih AY, Walsh JJ, Maruyama H, Sarsoza F, Ku L, Eggert S, Hof PR, Koo EH, Dickstein DL (2012) Amyloid precursor protein (APP) regulates synaptic structure and function. Mol Cell Neurosci 51:43-52. CrossRef Medline
76. Ultanir SK, Kim JE, Hall BJ, Deerinck T, Ellisman M, Ghosh A (2007) Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Proc Natl Acad Sci USA 104:19553-19558. CrossRef Medline
77. Yoshida Y, Chiba T, Tokunaga F, Kawasaki H, Iwai K, Suzuki T, Ito Y, Matsuoka K, Yoshida M, Tanaka K, Tai T (2002) E3 ubiquitin ligase that recognizes sugar chains. Nature 418:438-442. CrossRef Medline
78. Zha XM, Green SH, Dailey ME (2005) Regulation of hippocampal synapse remodeling by epileptiform activity. Mol Cell Neurosci 29:494-506. CrossRef Medline