Sumoylated MEF2A coordinately eliminates orphan presynaptic sites and promotes maturation of presynaptic boutons

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 4726-4740

  Yamada, Tomoko ^a   Yang, Yue ^a   Huang, Ju ^a   Coppola, Giovanni ^b   Geschwind, Daniel H ^b   Bonni, Azad ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; MYOCYTE ENHANCER FACTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPSIN; SYNAPTOBREVIN 2; SYNAPTOTAGMIN I;

ANIMAL CELL; ARTICLE; CEREBELLUM CORTEX; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPORATION; GEL MOBILITY SHIFT ASSAY; IMMUNOBLOTTING; MICROARRAY ANALYSIS; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CEREBELLUM; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ELECTROPORATION; FEMALE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MADS DOMAIN PROTEINS; MALE; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MYOGENIC REGULATORY FACTORS; NERVE TISSUE PROTEINS; NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, LONG-EVANS; SUMOYLATION; TIME FACTORS; TRANSFECTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84874923254     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4191-12.2013     Document Type: Article

References (55)

1. Abrahams BS, Geschwind DH (2008) Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 9:341-355. Medline
2. Akhtar MW, Kim MS, Adachi M, Morris MJ, Qi X, Richardson JA, Bassel-Duby R, Olson EN, Kavalali ET, Monteggia LM (2012) In vivo analysis of MEF2 transcription factors in synapse regulation and neuronal survival. PLo S One 7:e34863. CrossRef Medline
3. Altman J, Bayer SA (1997) Development of the cerebellar system: in relation to its evolution, structure, and functions. Boca Raton, FL: CRC.
4. Andrews-Zwilling YS, Kawabe H, Reim K, Varoqueaux F, Brose N (2006) Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J Biol Chem 281:19720-19731. CrossRef Medline
5. Black BL, Olson EN (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14:167-196. Medline
6. Chi P, Greengard P, Ryan TA (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187-1193. Medline
7. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421-433. CrossRef Medline
8. Colón-Ramos DA, Margeta MA, Shen K (2007) Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318:103-106. CrossRef Medline
9. de la Torre-Ubieta L, Gaudillière B, Yang Y, Ikeuchi Y, Yamada T, DiBacco S, Stegmüller J, Schüller, Salih DA, Rowitch D, Brunet A, Bonni A (2010) A FOXO-Pak1 transcriptional pathway controls neuronal polarity. Genes Dev 24:799-813. CrossRef Medline
10. Flavell SW, Cowan CW, Kim TK, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C, Greenberg ME (2006) Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311:1008-1012. CrossRef Medline
11. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM, Greenberg ME (2008) Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60:1022-1038. CrossRef Medline
12. Fukaya M, Watanabe M (2000) Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment: a study in the adult mouse brain. J Comp Neurol 426:572-586. CrossRef Medline
13. Gaudilliere B, Shi Y, Bonni A (2002) RNA interference reveals a requirement for myocyte enhancer factor 2A in activity-dependent neuronal survival. J Biol Chem 277:46442-46446. Medline
14. Gossett LA, Kelvin DJ, Sternberg EA, Olson EN (1989) A new myocytespecific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol Cell Biol 9:5022-5033. Medline
15. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026. CrossRef Medline
16. Grégoire S, Yang XJ (2005) Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol Cell Biol 25:2273-2287. CrossRef Medline
17. Hietakangas V, Anckar J, Blomster HA, Fujimoto M, Palvimo JJ, Nakai A, Sistonen L (2006) PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci U S A 103:45-50. CrossRef Medline
18. Kelleher RJ 3rd, Bear MF (2008) The autistic neuron: troubled translation? Cell 135:401-406. CrossRef Medline
19. Kim AH, Puram SV, Bilimoria PM, Ikeuchi Y, Keough S, Wong M, Rowitch D, Bonni A (2009) A centrosomal Cdc20-APC pathway controls dendritic morphogenesis in postmitoic neurons. Cell 136:322-336. CrossRef Medline
20. Konishi Y, Lehtinen M, Donovan N, Bonni A (2002) Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol Cell 9:1005-1016. Medline
21. Konishi Y, Stegmüller J, Matsuda T, Bonni S, Bonni A (2004) Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 303:1026-1030. CrossRef Medline
22. Konopka G, Bomar JM, Winden K, Coppola G, Jonsson ZO, Gao F, Peng S, Preuss TM, Wohlschlegel JA, Geschwind DH (2009) Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 462:213-217. CrossRef Medline
23. Krueger SR, Kolar A, Fitzsimonds RM (2003) The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40:945-957. CrossRef Medline
24. Litterman N, Ikeuchi Y, Gallardo G, O'Connell BC, Sowa ME, Gygi SP, Harper JW, Bonni A (2011) An OBSL1-Cul7Fbxw8 ubiquitin ligase signaling mechanism regulates Golgi morphology and dendrite patterning. PLo S Biol 9:e1001060. CrossRef Medline
25. Lyons GE, Micales BK, Schwarz J, Martin JF, Olson EN (1995) Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J Neurosci 15:5727-5738. Medline
26. Matsuda T, Cepko CL (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci U S A 101:16-22. CrossRef Medline
27. McAllister AK (2007) Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30:425-450. Medline
28. Morrow EM, Yoo SY, Flavell SW, Kim TK, Lin Y, Hill RS, Mukaddes NM, Balkhy S, Gascon G, Hashmi A, Al-Saad S, Ware J, Joseph RM, Greenblatt R, Gleason D, Ertelt JA, Apse KA, Bodell A, Partlow JN, Barry B, et al. (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science 321:218-223. CrossRef Medline
29. Nakamura Y, Tamura H, Horinouchi K, Shiosaka S (2006) Role of neuropsin in formation and maturation of Schaffer-collateral L1camimmunoreactive synaptic boutons. J Cell Sci 119:1341-1349. CrossRef Medline
30. Palay SL, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. New York: Springer.
31. Pfeiffer BE, Zang T, Wilkerson JR, Taniguchi M, Maksimova MA, Smith LN, Cowan CW, Huber KM (2010) Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron 66:191-197. CrossRef Medline
32. Pichitpornchai C, Rawson JA, Rees S (1994) Morphology of parallel fibres in the cerebellar cortex of the rat: an experimental light and electron microscopic study with biocytin. J Comp Neurol 342:206-220. Medline
33. Polo-Parada L, Bose CM, Landmesser LT (2001) Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAMdeficient neuromuscular junctions. Neuron 32:815-828. CrossRef Medline
34. Poskanzer KE, Marek KW, Sweeney ST, Davis GW (2003) Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426:559-563. CrossRef Medline
35. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, Davis MM, Greengard P, Nairn AC, Nestler EJ, Cowan CW (2008) Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59:621-633. CrossRef Medline
36. Puram SV, Kim AH, Ikeuchi Y, Wilson-Grady JT, Merdes A, Gygi SP, Bonni A (2011) A CaMKIIbeta signaling pathway at the centrosome regulates dendrite patterning in the brain. Nat Neurosci 14:973-983. Medline
37. Ross S, Best JL, Zon LI, Gill G (2002) SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol Cell 10:831-842. Medline
38. Sabo SL, Gomes RA, McAllister AK (2006) Formation of presynaptic terminals at predefined sites along axons. J Neurosci 26:10813-10825. CrossRef Medline
39. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669. CrossRef Medline
40. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791. CrossRef Medline
41. Shalizi AK, Bonni A (2005) Brawn for brains: the role of MEF2 proteins in the developing nervous system. Curr Top Dev Biol 69:239-266. CrossRef Medline
42. Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A (2006) A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311: 1012-1017. CrossRef Medline
43. Shepherd GM, Harris KM (1998) Three-dimensional structure and composition of CA3->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 18:8300-8310. Medline
44. Simpson JH, Bland KS, Fetter RD, Goodman CS (2000) Short-range and long-range guidance by Slit and its Robo receptors: a combinatorial code of Robo receptors controls lateral position. Cell 103:1019-1032. CrossRef Medline
45. Smyth GK (2005) Limma: linear models for microarray data. In: Bioinformatics and computational biology solutions using R and bioconductor (Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, eds), pp 397-420. New York: Springer.
46. Stegmuller J, Bonni A (2007) Using RNAi in studies of cerebellar development. In: Inhibitory RNAs in neuroscience (Davidson B, ed). San Diego: Society for Neuroscience.
47. Südhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455:903-911. CrossRef Medline
48. Tang J, Maximov A, Shin OH, Dai H, Rizo J, Südhof TC (2006) A complexin/ synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126:1175-1187. CrossRef Medline
49. (2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54:567-581. CrossRef Medline
50. Yamasaki M, Miyazaki T, Azechi H, Abe M, Natsume R, Hagiwara T, Aiba A, Mishina M, Sakimura K, Watanabe M (2011) Glutamate receptor δ2 is essential for input pathway-dependent regulation of synaptic AMPAR contents in cerebellar Purkinje cells. J Neurosci 31:3362-3374. CrossRef Medline
51. Yang Y, Kim AH, Yamada T, Wu B, Bilimoria PM, Ikeuchi Y, de la Iglesia N, Shen J, Bonni A (2009) A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 326:575-578. CrossRef Medline
52. Yuan Z, Becker EB, Merlo P, Yamada T, DiBacco S, Konishi Y, Schaefer EM, Bonni A (2008) Activation of FOXO1 by Cdk1 in cycling cells and postmitotic neurons. Science 319:1665-1668. CrossRef Medline
53. Zhao C, Takita J, Tanaka Y, Setou M, Nakagawa T, Takeda S, Yang HW, Terada S, Nakata T, Takei Y, Saito M, Tsuji S, Hayashi Y, Hirokawa N (2001) Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 105:587-597. CrossRef Medline
54. Ziv NE, Garner CC (2004) Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci 5:385-399. CrossRef Medline
55. Zoghbi HY (2003) Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302:826-830. CrossRef Medline