Targets and consequences of protein SUMOylation in neurons

Brain Research Reviews - Tập 64 - Trang 195-212 - 2010
Kevin A. Wilkinson1, Yasuko Nakamura1, Jeremy M. Henley1
1Medical Research Council Centre for Synaptic Plasticity, Department of Anatomy, School of Medical Sciences, University of Bristol, University Walk, Bristol, BS8 1TD, UK

Tài liệu tham khảo

Agbor, 2008, SUMO, hypoxia and the regulation of metabolism, Biochem. Soc. Trans., 36, 445, 10.1042/BST0360445 Ahima, 2000, Leptin, Annu. Rev. Physiol., 62, 413, 10.1146/annurev.physiol.62.1.413 Ahn, 2009, Ubc9 gene polymorphisms and late-onset Alzheimer's disease in the Korean population: a genetic association study, Neurosci. Lett., 465, 272, 10.1016/j.neulet.2009.09.017 Anderson, 2009, Protein SUMOylation in neuropathological conditions, Drug News Perspect., 22, 255, 10.1358/dnp.2009.22.5.1378636 Appella, 2001, Post-translational modifications and activation of p53 by genotoxic stresses, Eur. J. Biochem., 268, 2764, 10.1046/j.1432-1327.2001.02225.x Bauer, 1992, Phosducin is a protein kinase A-regulated G-protein regulator, Nature, 358, 73, 10.1038/358073a0 Bence, 2006, Neuronal PTP1B regulates body weight, adiposity and leptin action, Nat. Med., 12, 917, 10.1038/nm1435 Benson, 2007, SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5, Proc. Natl. Acad. Sci. USA, 104, 1805, 10.1073/pnas.0606702104 Berciano, 2007, Cajal body number and nucleolar size correlate with the cell body mass in human sensory ganglia neurons, J. Struct. Biol., 158, 410, 10.1016/j.jsb.2006.12.008 Berman, 1998, Mammalian RGS proteins: barbarians at the gate, J. Biol. Chem., 273, 1269, 10.1074/jbc.273.3.1269 Besnault-Mascard, 2005, Caspase-8 sumoylation is associated with nuclear localization, Oncogene, 24, 3268, 10.1038/sj.onc.1208448 Bhat, 2004, Glycogen synthase kinase 3: a drug target for CNS therapies, J. Neurochem., 89, 1313, 10.1111/j.1471-4159.2004.02422.x Blackshaw, 2004, Genomic analysis of mouse retinal development, PLoS Biol., 2, E247, 10.1371/journal.pbio.0020247 Bohren, 2004, A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus, J. Biol. Chem., 279, 27233, 10.1074/jbc.M402273200 Bossis, 2006, Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes, Mol. Cell, 21, 349, 10.1016/j.molcel.2005.12.019 Braschi, 2009, MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission, EMBO Rep., 10, 748, 10.1038/embor.2009.86 Bryant, 2002, Regulated transport of the glucose transporter GLUT4, Nat. Rev. Mol. Cell Biol., 3, 267, 10.1038/nrm782 Cardone, 2005, Circadian clock control by SUMOylation of BMAL1, Science, 309, 1390, 10.1126/science.1110689 Carter, 2007, C-terminal modifications regulate MDM2 dissociation and nuclear export of p53, Nat. Cell Biol., 9, 428, 10.1038/ncb1562 Carvalho, 1999, The spinal muscular atrophy disease gene product, SMN: A link between snRNP biogenesis and the Cajal (coiled) body, J. Cell Biol., 147, 715, 10.1083/jcb.147.4.715 Chan, 2006, Mitochondrial fusion and fission in mammals, Annu. Rev. Cell Dev. Biol., 22, 79, 10.1146/annurev.cellbio.22.010305.104638 Chan, 2002, Genetic modulation of polyglutamine toxicity by protein conjugation pathways in Drosophila, Hum. Mol. Genet., 11, 2895, 10.1093/hmg/11.23.2895 Chao, 2008, SUMOylation of the MAGUK protein CASK regulates dendritic spinogenesis, J. Cell Biol., 182, 141, 10.1083/jcb.200712094 Chen, 1998, Transforming growth factor beta type I receptor kinase mutant associated with metastatic breast cancer, Cancer Res., 58, 4805 Chen, 2001, Novel inactivating mutations of transforming growth factor-beta type I receptor gene in head-and-neck cancer metastases, Int. J. Cancer, 93, 653, 10.1002/ijc.1381 Cimarosti, 2008, Investigating the mechanisms underlying neuronal death in ischemia using in vitro oxygen-glucose deprivation: potential involvement of protein SUMOylation, Neuroscientist, 14, 626, 10.1177/1073858408322677 Cimarosti, 2008, Increased protein SUMOylation following focal cerebral ischemia, Neuropharmacology, 54, 280, 10.1016/j.neuropharm.2007.09.010 Dadke, 2007, Regulation of protein tyrosine phosphatase 1B by sumoylation, Nat. Cell Biol., 9, 80, 10.1038/ncb1522 Dorval, 2006, Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein, J. Biol. Chem., 281, 9919, 10.1074/jbc.M510127200 Dorval, 2007, SUMO on the road to neurodegeneration, Biochim. Biophys. Acta, 1773, 694, 10.1016/j.bbamcr.2007.03.017 Dorval, 2007, Modulation of Abeta generation by small ubiquitin-like modifiers does not require conjugation to target proteins, Biochem. J., 404, 309, 10.1042/BJ20061451 Dube, 2005, Involvement of the small protein tyrosine phosphatases TC-PTP and PTP1B in signal transduction and diseases: from diabetes, obesity to cell cycle, and cancer, Biochim. Biophys. Acta, 1754, 108, 10.1016/j.bbapap.2005.07.030 Eizenberg, 1996, p53 plays a regulatory role in differentiation and apoptosis of central nervous system-associated cells, Mol. Cell. Biol., 16, 5178, 10.1128/MCB.16.9.5178 Eldar-Finkelman, 2002, Glycogen synthase kinase 3: an emerging therapeutic target, Trends Mol. Med., 8, 126, 10.1016/S1471-4914(01)02266-3 Eun Jeoung, 2008, Regulation of glycogen synthase kinase 3beta functions by modification of the small ubiquitin-like modifier, Open Biochem. J., 2, 67, 10.2174/1874091X00802010067 Feliciangeli, 2007, Does sumoylation control K2P1/TWIK1 background K+ channels?, Cell, 130, 563, 10.1016/j.cell.2007.06.012 Feliciangeli, 2010, Potassium channel silencing by constitutive endocytosis and intracellular sequestration, J. Biol. Chem., 285, 4798, 10.1074/jbc.M109.078535 Feligioni, 2009, Protein SUMOylation modulates calcium influx and glutamate release from presynaptic terminals, Eur. J. Neurosci., 29, 1348, 10.1111/j.1460-9568.2009.06692.x Figueroa-Romero, 2009, SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle, FASEB J., 23, 3917, 10.1096/fj.09-136630 Flanders, 1998, Transforming growth factor-betas in neurodegenerative disease, Prog. Neurobiol., 54, 71, 10.1016/S0301-0082(97)00066-X Flavell, 2006, Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number, Science, 311, 1008, 10.1126/science.1122511 Gatchel, 2005, Diseases of unstable repeat expansion: mechanisms and common principles, Nat. Rev. Genet., 6, 743, 10.1038/nrg1691 Geiss-Friedlander, 2007, Concepts in sumoylation: a decade on, Nat. Rev. Mol. Cell Biol., 8, 947, 10.1038/nrm2293 Geoffroy, 2009, An additional role for SUMO in ubiquitin-mediated proteolysis, Nat. Rev. Mol. Cell Biol., 10, 564, 10.1038/nrm2707 Gil, 2008, Mechanisms of neurodegeneration in Huntington's disease, Eur. J. Neurosci., 27, 2803, 10.1111/j.1460-9568.2008.06310.x Giorgino, 2000, The sentrin-conjugating enzyme mUbc9 interacts with GLUT4 and GLUT1 glucose transporters and regulates transporter levels in skeletal muscle cells, Proc. Natl. Acad. Sci. USA, 97, 1125, 10.1073/pnas.97.3.1125 Giuditta, 2002, Axonal and presynaptic protein synthesis: new insights into the biology of the neuron, Trends Neurosci., 25, 400, 10.1016/S0166-2236(02)02188-4 Gocke, 2005, Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates, J. Biol. Chem., 280, 5004, 10.1074/jbc.M411718200 Gong, 1999, Molecular cloning and characterization of human AOS1 and UBA2, components of the sentrin-activating enzyme complex, FEBS Lett., 448, 185, 10.1016/S0014-5793(99)00367-1 Gostissa, 1999, Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1, EMBO J., 18, 6462, 10.1093/emboj/18.22.6462 Gowran, 2009, Delta(9)-tetrahydrocannabinol regulates the p53 post-translational modifiers Murine double minute 2 and the small ubiquitin modifier protein in the rat brain, FEBS Lett., 583, 3412, 10.1016/j.febslet.2009.09.056 Hankins, 2008, Melanopsin: an exciting photopigment, Trends Neurosci., 31, 27, 10.1016/j.tins.2007.11.002 Hardeland, 2002, Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover, EMBO J., 21, 1456, 10.1093/emboj/21.6.1456 Harder, 2004, Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission, Curr. Biol., 14, 340, 10.1016/j.cub.2004.02.004 Hay, 2005, SUMO: a history of modification, Mol. Cell, 18, 1, 10.1016/j.molcel.2005.03.012 Hayashi, 2002, Ubc9 is essential for viability of higher eukaryotic cells, Exp. Cell Res., 280, 212, 10.1006/excr.2002.5634 Hayashi, 2006, Relationship between SUMO-1 modification of caspase-7 and its nuclear localization in human neuronal cells, Neurosci. Lett., 397, 5, 10.1016/j.neulet.2005.11.057 Heun, 2007, SUMOrganization of the nucleus, Curr. Opin. Cell Biol., 19, 350, 10.1016/j.ceb.2007.04.014 Hietakangas, 2006, PDSM, a motif for phosphorylation-dependent SUMO modification, Proc. Natl. Acad. Sci. USA, 103, 45, 10.1073/pnas.0503698102 Hilgarth, 2004, Regulation and function of SUMO modification, J. Biol. Chem., 279, 53899, 10.1074/jbc.R400021200 Hirokawa, 2005, Molecular motors and mechanisms of directional transport in neurons, Nat. Rev. Neurosci., 6, 201, 10.1038/nrn1624 Hofmann, 2000, Covalent modification of the transactivator protein IE2-p86 of human cytomegalovirus by conjugation to the ubiquitin-homologous proteins SUMO-1 and hSMT3b, J. Virol., 74, 2510, 10.1128/JVI.74.6.2510-2524.2000 Ishihara, 2009, Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice, Nat. Cell Biol., 11, 958, 10.1038/ncb1907 Ja Lee, 2009, SUMOylation participates in induction of ischemic tolerance, J. Neurochem., 109, 257, 10.1111/j.1471-4159.2009.05957.x Janer, 2010, SUMOylation attenuates the aggregation propensity and cellular toxicity of the polyglutamine expanded ataxin-7, Hum. Mol. Genet., 19, 181, 10.1093/hmg/ddp478 Jaskolski, 2005, Subcellular localization and trafficking of kainate receptors, Trends Pharmacol. Sci., 26, 20, 10.1016/j.tips.2004.11.008 Johnson, 2004, Protein modification by SUMO, Annu. Rev. Biochem., 73, 355, 10.1146/annurev.biochem.73.011303.074118 Kadare, 2003, PIAS1-mediated sumoylation of focal adhesion kinase activates its autophosphorylation, J. Biol. Chem., 278, 47434, 10.1074/jbc.M308562200 Kang, 2008, The type I TGF-beta receptor is covalently modified and regulated by sumoylation, Nat. Cell Biol., 10, 654, 10.1038/ncb1728 Katsuno, 2006, Pathogenesis, animal models and therapeutics in spinal and bulbar muscular atrophy (SBMA), Exp. Neurol., 200, 8, 10.1016/j.expneurol.2006.01.021 Kim, 2009, Emerging roles of desumoylating enzymes, Biochim. Biophys. Acta, 1792, 155, 10.1016/j.bbadis.2008.12.008 Klenk, 2006, SUMO-1 controls the protein stability and the biological function of phosducin, J. Biol. Chem., 281, 8357, 10.1074/jbc.M513703200 Kozlovsky, 2002, GSK-3 and the neurodevelopmental hypothesis of schizophrenia, Eur. Neuropsychopharmacol., 12, 13, 10.1016/S0924-977X(01)00131-6 Lapenta, 1997, SMT3A, a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family, Genomics, 40, 362, 10.1006/geno.1996.4556 Lavin, 2006, The complexity of p53 stabilization and activation, Cell Death Differ., 13, 941, 10.1038/sj.cdd.4401925 Lee, 2009, SUMO modification of DNA topoisomerase II: trying to get a CENse of it all, DNA Repair (Amst.), 8, 557, 10.1016/j.dnarep.2009.01.004 Lee, 2008, Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex, Mol. Cell. Biol., 28, 6056, 10.1128/MCB.00583-08 Levine, 1997, p53, the cellular gatekeeper for growth and division, Cell, 88, 323, 10.1016/S0092-8674(00)81871-1 Li, 1998, Mammalian DNA topoisomerase IIIalpha is essential in early embryogenesis, Proc. Natl. Acad. Sci. USA, 95, 1010, 10.1073/pnas.95.3.1010 Li, 2003, Positive and negative regulation of APP amyloidogenesis by sumoylation, Proc. Natl. Acad. Sci. USA, 100, 259, 10.1073/pnas.0235361100 Li, 2004, The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses, Cell, 119, 873, 10.1016/j.cell.2004.11.003 Liu, 2007, The SUMO conjugating enzyme Ubc9 is a regulator of GLUT4 turnover and targeting to the insulin-responsive storage compartment in 3T3-L1 adipocytes, Diabetes, 56, 1977, 10.2337/db06-1100 Lu, 2009, The activity-dependent stimuli increase SUMO modification in SHSY5Y cells, Biochem. Biophys. Res. Commun., 390, 872, 10.1016/j.bbrc.2009.10.065 Mahajan, 1997, A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2, Cell, 88, 97, 10.1016/S0092-8674(00)81862-0 Mao, 2000, SUMO-1 conjugation to human DNA topoisomerase II isozymes, J. Biol. Chem., 275, 26066, 10.1074/jbc.M001831200 Mao, 2000, SUMO-1 conjugation to topoisomerase I: A possible repair response to topoisomerase-mediated DNA damage, Proc. Natl. Acad. Sci. USA, 97, 4046, 10.1073/pnas.080536597 Mao, 2004, RGS17/RGSZ2, a novel regulator of Gi/o, Gz, and Gq signaling, J. Biol. Chem., 279, 26314, 10.1074/jbc.M401800200 Martin, 2004, Local protein synthesis during axon guidance and synaptic plasticity, Curr. Opin. Neurobiol., 14, 305, 10.1016/j.conb.2004.05.009 Martin, 2007, SUMOylation regulates kainate-receptor-mediated synaptic transmission, Nature, 447, 321, 10.1038/nature05736 Martin, 2007, Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction, Nat. Rev. Neurosci., 8, 948, 10.1038/nrn2276 Matunis, 1996, A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex, J. Cell Biol., 135, 1457, 10.1083/jcb.135.6.1457 McBride, 2006, Mitochondria: more than just a powerhouse, Curr. Biol., 16, R551, 10.1016/j.cub.2006.06.054 McFadden, 2005, Neuronal intranuclear inclusion disease without polyglutamine inclusions in a child, J. Neuropathol. Exp. Neurol., 64, 545, 10.1093/jnen/64.6.545 Melchior, 2002, SUMO-1 and p53, Cell Cycle, 1, 245, 10.4161/cc.1.4.131 Meulmeester, 2008, Cell biology: SUMO, Nature, 452, 709, 10.1038/452709a Minty, 2000, Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif, J. Biol. Chem., 275, 36316, 10.1074/jbc.M004293200 Mishra, 2004, Dynamin interacts with members of the sumoylation machinery, J. Biol. Chem., 279, 31445, 10.1074/jbc.M402911200 Mitra, 2005, Focal adhesion kinase: in command and control of cell motility, Nat. Rev. Mol. Cell Biol., 6, 56, 10.1038/nrm1549 Mukherjee, 2009, Small ubiquitin-like modifier (SUMO) modification of the androgen receptor attenuates polyglutamine-mediated aggregation, J. Biol. Chem., 284, 21296, 10.1074/jbc.M109.011494 Mukhopadhyay, 2007, Modification in reverse: the SUMO proteases, Trends Biochem. Sci., 32, 286, 10.1016/j.tibs.2007.05.002 Muller, 2001, SUMO, ubiquitin's mysterious cousin, Nat. Rev. Mol. Cell Biol., 2, 202, 10.1038/35056591 Nacerddine, 2005, The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice, Dev. Cell, 9, 769, 10.1016/j.devcel.2005.10.007 Navascues, 2008, SUMO-1 transiently localizes to Cajal bodies in mammalian neurons, J. Struct. Biol., 163, 137, 10.1016/j.jsb.2008.04.013 Neef, 2006, Dementia with Lewy bodies: an emerging disease, Am. Fam. Physician, 73, 1223 Neuspiel, 2008, Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers, Curr. Biol., 18, 102, 10.1016/j.cub.2007.12.038 Nimchinsky, 2002, Structure and function of dendritic spines, Annu. Rev. Physiol., 64, 313, 10.1146/annurev.physiol.64.081501.160008 Nishida, 2002, PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription, J. Biol. Chem., 277, 41311, 10.1074/jbc.M206741200 Onishi, 2009, Pias3-dependent SUMOylation directs rod photoreceptor development, Neuron, 61, 234, 10.1016/j.neuron.2008.12.006 Orias, 1997, Cloning and localization of a double-pore K channel, KCNK1: exclusive expression in distal nephron segments, Am. J. Physiol., 273, F663 Owerbach, 2005, A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation, Biochem. Biophys. Res. Commun., 337, 517, 10.1016/j.bbrc.2005.09.090 Palancade, 2008, Sumoylating and desumoylating enzymes at nuclear pores: underpinning their unexpected duties?, Trends Cell Biol., 18, 174, 10.1016/j.tcb.2008.02.001 Peineau, 2007, LTP inhibits LTD in the hippocampus via regulation of GSK3beta, Neuron, 53, 703, 10.1016/j.neuron.2007.01.029 Pierce, 2002, Seven-transmembrane receptors, Nat. Rev. Mol. Cell Biol., 3, 639, 10.1038/nrm908 Pinheiro, 2006, Kainate receptors, Cell Tissue Res., 326, 457, 10.1007/s00441-006-0265-6 Plant, 2005, K2P channels and their protein partners, Curr. Opin. Neurobiol., 15, 326, 10.1016/j.conb.2005.05.008 Poukka, 2000, Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1), Proc. Natl. Acad. Sci. USA, 97, 14145, 10.1073/pnas.97.26.14145 Pountney, 2003, SUMO-1 marks the nuclear inclusions in familial neuronal intranuclear inclusion disease, Exp. Neurol., 184, 436, 10.1016/j.expneurol.2003.07.004 Pountney, 2005, SUMO-1 marks subdomains within glial cytoplasmic inclusions of multiple system atrophy, Neurosci. Lett., 381, 74, 10.1016/j.neulet.2005.02.013 Pountney, 2008, NSF, Unc-18-1, dynamin-1 and HSP90 are inclusion body components in neuronal intranuclear inclusion disease identified by anti-SUMO-1-immunocapture, Acta Neuropathol., 116, 603, 10.1007/s00401-008-0437-4 Pratt, 1997, TGF-beta in the central nervous system: potential roles in ischemic injury and neurodegenerative diseases, Cytokine Growth Factor Rev., 8, 267, 10.1016/S1359-6101(97)00018-X Rajan, 2005, Sumoylation silences the plasma membrane leak K+channel K2P1, Cell, 121, 37, 10.1016/j.cell.2005.01.019 Reppert, 2002, Coordination of circadian timing in mammals, Nature, 418, 935, 10.1038/nature00965 Riley, 2005, SUMOylation of the polyglutamine repeat protein, ataxin-1, is dependent on a functional nuclear localization signal, J. Biol. Chem., 280, 21942, 10.1074/jbc.M501677200 Rodriguez, 1999, SUMO-1 modification activates the transcriptional response of p53, EMBO J., 18, 6455, 10.1093/emboj/18.22.6455 Rodriguez, 2001, SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting, J. Biol. Chem., 276, 12654, 10.1074/jbc.M009476200 Rodriguez-Munoz, 2007, Sumoylated RGS-Rz proteins act as scaffolds for Mu-opioid receptors and G-protein complexes in mouse brain, Neuropsychopharmacology, 32, 842, 10.1038/sj.npp.1301184 Rui, 2002, SUMO-1 modification of the C-terminal KVEKVD of Axin is required for JNK activation but has no effect on Wnt signaling, J. Biol. Chem., 277, 42981, 10.1074/jbc.M208099200 Ryu, 2010, Oxidative stress-enhanced SUMOylation and aggregation of ataxin-1: Implication of JNK pathway, Biochem. Biophys. Res. Commun., 393, 280, 10.1016/j.bbrc.2010.01.122 Sahar, 2010, Regulation of BMAL1 protein stability and circadian function by GSK3beta-mediated phosphorylation, PLoS ONE, 5, e8561, 10.1371/journal.pone.0008561 Saitoh, 2000, Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3, J. Biol. Chem., 275, 6252, 10.1074/jbc.275.9.6252 Sampson, 2001, The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification, J. Biol. Chem., 276, 21664, 10.1074/jbc.M100006200 Schilling, 1999, Nuclear accumulation of truncated atrophin-1 fragments in a transgenic mouse model of DRPLA, Neuron, 24, 275, 10.1016/S0896-6273(00)80839-9 Seeler, 2003, Nuclear and unclear functions of SUMO, Nat. Rev. Mol. Cell Biol., 4, 690, 10.1038/nrm1200 Shalizi, 2006, A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation, Science, 311, 1012, 10.1126/science.1122513 Shalizi, 2007, PIASx is a MEF2 SUMO E3 ligase that promotes postsynaptic dendritic morphogenesis, J. Neurosci., 27, 10037, 10.1523/JNEUROSCI.0361-07.2007 Shi, 2003, Mechanisms of TGF-beta signaling from cell membrane to the nucleus, Cell, 113, 685, 10.1016/S0092-8674(03)00432-X Shinbo, 2006, Proper SUMO-1 conjugation is essential to DJ-1 to exert its full activities, Cell Death Differ., 13, 96, 10.1038/sj.cdd.4401704 Smirnova, 2001, Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells, Mol. Biol. Cell, 12, 2245, 10.1091/mbc.12.8.2245 Song, 2004, Identification of a SUMO-binding motif that recognizes SUMO-modified proteins, Proc. Natl. Acad. Sci. USA, 101, 14373, 10.1073/pnas.0403498101 Steffan, 2004, SUMO modification of Huntingtin and Huntington's disease pathology, Science, 304, 100, 10.1126/science.1092194 Stehmeier, 2009, Regulation of p53 family members by the ubiquitin-like SUMO system, DNA Repair (Amst.), 8, 491, 10.1016/j.dnarep.2009.01.002 Subramaniam, 2009, Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity, Science, 324, 1327, 10.1126/science.1172871 Sung, 1980, An unusual degenerative disorder of neurons associated with a novel intranuclear hyaline inclusion (neuronal intranuclear hyaline inclusion disease). A clinicopathological study of a case, J. Neuropathol. Exp. Neurol., 39, 107, 10.1097/00005072-198003000-00001 Taira, 2004, DJ-1 has a role in antioxidative stress to prevent cell death, EMBO Rep., 5, 213, 10.1038/sj.embor.7400074 Takahashi, 2001, DJ-1 positively regulates the androgen receptor by impairing the binding of PIASx alpha to the receptor, J. Biol. Chem., 276, 37556, 10.1074/jbc.M101730200 Takahashi-Fujigasaki, 2006, SUMOylation substrates in neuronal intranuclear inclusion disease, Neuropathol. Appl. Neurobiol., 32, 92, 10.1111/j.1365-2990.2005.00705.x Tan, 2007, Pathogenic mutations in Parkinson disease, Hum. Mutat., 28, 641, 10.1002/humu.20507 Tang, 2005, Pias1 interaction and sumoylation of metabotropic glutamate receptor 8, J. Biol. Chem., 280, 38153, 10.1074/jbc.M508168200 Tatham, 2001, Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9, J. Biol. Chem., 276, 35368, 10.1074/jbc.M104214200 Tedeschi, 2009, The tumor suppressor p53 transcriptionally regulates cGKI expression during neuronal maturation and is required for cGMP-dependent growth cone collapse, J. Neurosci., 29, 15155, 10.1523/JNEUROSCI.4416-09.2009 Tempe, 2008, SUMO under stress, Biochem. Soc. Trans., 36, 874, 10.1042/BST0360874 Terashima, 2002, SUMO-1 co-localized with mutant atrophin-1 with expanded polyglutamines accelerates intranuclear aggregation and cell death, NeuroReport, 13, 2359, 10.1097/00001756-200212030-00038 Ueda, 2002, Enhanced SUMOylation in polyglutamine diseases, Biochem. Biophys. Res. Commun., 293, 307, 10.1016/S0006-291X(02)00211-5 Um, 2006, Functional modulation of parkin through physical interaction with SUMO-1, J. Neurosci. Res., 84, 1543, 10.1002/jnr.21041 Um, 2006, Parkin ubiquitinates and promotes the degradation of RanBP2, J. Biol. Chem., 281, 3595, 10.1074/jbc.M504994200 van Niekerk, 2007, Sumoylation in axons triggers retrograde transport of the RNA-binding protein La, Proc. Natl. Acad. Sci. USA., 104, 12913, 10.1073/pnas.0611562104 Vassilatis, 2003, The G protein-coupled receptor repertoires of human and mouse, Proc. Natl. Acad. Sci. USA, 100, 4903, 10.1073/pnas.0230374100 Wasiak, 2007, Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death, J. Cell Biol., 177, 439, 10.1083/jcb.200610042 Watanabe, 2008, Developmental regulation of Ubc9 in the rat nervous system, Acta Biochim. Pol., 55, 681, 10.18388/abp.2008_3027 Watts, 2004, SUMO modification of proteins other than transcription factors, Semin. Cell Dev. Biol., 15, 211, 10.1016/j.semcdb.2003.12.002 Wilkinson, 2008, Analysis of SUMO-1 modification of neuronal proteins containing consensus SUMOylation motifs, Neurosci. Lett., 436, 239, 10.1016/j.neulet.2008.03.029 Wolin, 2002, The La protein, Annu. Rev. Biochem., 71, 375, 10.1146/annurev.biochem.71.090501.150003 Yang, 2006, An extended consensus motif enhances the specificity of substrate modification by SUMO, EMBO J., 25, 5083, 10.1038/sj.emboj.7601383 Yang, 2008, Cerebral ischemia/stroke and small ubiquitin-like modifier (SUMO) conjugation–a new target for therapeutic intervention?, J. Neurochem., 106, 989, 10.1111/j.1471-4159.2008.05404.x Yang, 2008, Transient focal cerebral ischemia induces a dramatic activation of small ubiquitin-like modifier conjugation, J. Cereb. Blood Flow Metab., 28, 892, 10.1038/sj.jcbfm.9600601 Yazawa, 1995, Abnormal gene product identified in hereditary dentatorubral-pallidoluysian atrophy (DRPLA) brain, Nat. Genet., 10, 99, 10.1038/ng0595-99 Yeh, 2009, SUMOylation and De-SUMOylation: wrestling with life's processes, J. Biol. Chem., 284, 8223, 10.1074/jbc.R800050200 Zhang, 2008, Sumoylation of amyloid precursor protein negatively regulates Abeta aggregate levels, Biochem. Biophys. Res. Commun., 374, 673, 10.1016/j.bbrc.2008.07.109 Zoghbi, 2000, Glutamine repeats and neurodegeneration, Annu. Rev. Neurosci., 23, 217, 10.1146/annurev.neuro.23.1.217 Zunino, 2009, Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis, J. Biol. Chem., 284, 17783, 10.1074/jbc.M901902200