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01-12-2013 | Review Paper

SUMO: a (Oxidative) Stressed Protein

Authors: Marco Feligioni, Robert Nisticò

Published in: NeuroMolecular Medicine | Issue 4/2013

Abstract

Redox species are produced during the physiological cellular metabolism of a normal tissue. In turn, their presence is also attributed to pathological conditions including neurodegenerative diseases. Many are the molecular changes that occur during the unbalance of the redox homeostasis. Interestingly, posttranslational protein modifications (PTMs) play a remarkable role. In fact, several target proteins are modified in their activation, localization, aggregation, and expression after the cellular stress. Among PTMs, protein SUMOylation represents a very important molecular modification pathway during “oxidative stress”. It has been reported that this ubiquitin-like modification is a fine sensor for redox species. Indeed, SUMOylation pathway efficiency is affected by the exposure to oxidative species in a different manner depending on the concentration and time of application. Thus, we here report updated evidence that states the role of SUMOylation in several pathological conditions, and we also outline the key involvement of c-Jun N-terminal kinase and small ubiquitin modifier pathway cross talk.

Anderson, D. B., Wilkinson, K. A., & Henley, J. M. (2009). Protein SUMOylation in neuropathological conditions. Drug news and perspectives, 22(5), 255–265.PubMed

Armogida, M., Nisticò, R., & Mercuri, N. B. (2012). Therapeutic potential of targeting hydrogen peroxide metabolism in the treatment of brain ischaemia. British Journal of Pharmacology, 166(4), 1211–1224.PubMed

Behrens, A., Sibilia, M., & Wagner, E. F. (1999). Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nature Genetics, 21(3), 326–329.PubMed

Boggio, R., Colombo, R., Hay, R. T., Draetta, G. F., & Chiocca, S. (2004). A mechanism for inhibiting the SUMO pathway. Molecular Cell, 16(4), 549–561.PubMed

Bohren, K. M., Nadkarni, V., Song, J. H., Gabbay, K. H., & Owerbach, D. (2004). A M55 V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. The Journal of biological chemistry, 279(26), 27233–27238.PubMed

Bononi, A., Agnoletto, C., De Marchi, E., Marchi, S., Patergnani, S., Bonora, M., et al. (2011). Protein kinases and phosphatases in the control of cell fate. Enzyme research, 2011, 329098.PubMed

Borsello, T., Clarke, P. G. H., Hirt, L., Vercelli, A., Repici, M., Schorderet, D. F., et al. (2003). A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nature Medicine, 9(9), 1180–1186.PubMed

Bossis, G., Malnou, C. E., Farras, R., Andermarcher, E., Hipskind, R., Rodriguez, M., et al. (2005). Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Molecular and Cellular Biology, 25(16), 6964–6979.PubMed

Bossis, G., & Melchior, F. (2006a). SUMO: Regulating the regulator. Cell division, 1, 13.PubMed

Bossis, G., & Melchior, F. (2006b). Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Molecular Cell, 21(3), 349–357.PubMed

Cadenas, E., & Davies, K. J. (2000). Mitochondrial free radical generation, oxidative stress, and aging. Free Radical Biology and Medicine, 29(3–4), 222–230.PubMed

Choi, S. J., Chung, S. S., Rho, E. J., Lee, H. W., Lee, M. H., Choi, H.-S., et al. (2006). Negative modulation of RXRalpha transcriptional activity by small ubiquitin-related modifier (SUMO) modification and its reversal by SUMO-specific protease SUSP1. The Journal of biological chemistry, 281(41), 30669–30677.PubMed

Choi, W.-S., Klintworth, H. M., & Xia, Z. (2011). JNK3-mediated apoptotic cell death in primary dopaminergic neurons. Methods in molecular biology (Clifton, NJ), 758, 279–292.

Ciechanover, A., Elias, S., Heller, H., Ferber, S., & Hershko, A. (1980). Characterization of the heat-stable polypeptide of the ATP-dependent proteolytic system from reticulocytes. The Journal of biological chemistry, 255(16), 7525–7528.PubMed

Dadke, S., Cotteret, S., Yip, S.-C., Jaffer, Z. M., Haj, F., Ivanov, A., et al. (2007). Regulation of protein tyrosine phosphatase 1B by sumoylation. Nature Cell Biology, 9(1), 80–85.PubMed

Dangoumau, A., Veyrat-Durebex, C., Blasco, H., Praline, J., Corcia, P., Andres, C. R., et al. (2013). Protein SUMOylation, an emerging pathway in amyotrophic lateral sclerosis. The International journal of neuroscience, 123(6), 366–374.PubMed

Davis, R. J. (2000). Signal transduction by the JNK group of MAP kinases. Cell, 103(2), 239–252.PubMed

De la Vega, L., Grishina, I., Moreno, R., Krüger, M., Braun, T., & Schmitz, M. L. (2012). A redox-regulated SUMO/acetylation switch of HIPK2 controls the survival threshold to oxidative stress. Molecular Cell, 46(4), 472–483.PubMed

Desterro, J. M., Rodriguez, M. S., & Hay, R. T. (1998). SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Molecular Cell, 2(2), 233–239.PubMed

Devasagayam, T. P. A., Tilak, J. C., Boloor, K. K., Sane, K. S., Ghaskadbi, S. S., & Lele, R. D. (2004). Free radicals and antioxidants in human health: current status and future prospects. The Journal of the Association of Physicians of India, 52, 794–804.PubMed

Dorval, V., & Fraser, P. E. (2006). Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein. The Journal of biological chemistry, 281(15), 9919–9924.PubMed

Dorval, V., Mazzella, M. J., Mathews, P. M., Hay, R. T., & Fraser, P. E. (2007). Modulation of Abeta generation by small ubiquitin-like modifiers does not require conjugation to target proteins. The Biochemical Journal, 404(2), 309–316.PubMed

Elsasser, S., Gali, R. R., Schwickart, M., Larsen, C. N., Leggett, D. S., Müller, B., et al. (2002). Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nature Cell Biology, 4(9), 725–730.PubMed

Fei, E., Jia, N., Yan, M., Ying, Z., Sun, Q., Wang, H., et al. (2006). SUMO-1 modification increases human SOD1 stability and aggregation. Biochemical and Biophysical Research Communications, 347(2), 406–412.PubMed

Feligioni, M., Brambilla, E., Camassa, A., Sclip, A., Arnaboldi, A., Morelli, F., et al. (2011). Crosstalk between JNK and SUMO Signaling Pathways: deSUMOylation Is Protective against H(2)O(2)-Induced Cell Injury. PLoS ONE, 6(12), e28185.PubMed

Foran, E., Bogush, A., Goffredo, M., Roncaglia, P., Gustincich, S., Pasinelli, P., et al. (2011). Motor neuron impairment mediated by a sumoylated fragment of the glial glutamate transporter EAAT2. Glia, 59(11), 1719–1731.PubMed

Gareau, J. R., & Lima, C. D. (2010). The SUMO pathway: Emerging mechanisms that shape specificity, conjugation and recognition. Nature Reviews Molecular Cell Biology, 11(12), 861–871.PubMed

Gibb, S. L., Boston-Howes, W., Lavina, Z. S., Gustincich, S., Brown, R. H., Pasinelli, P., et al. (2007). A caspase-3-cleaved fragment of the glial glutamate transporter EAAT2 is sumoylated and targeted to promyelocytic leukemia nuclear bodies in mutant SOD1-linked amyotrophic lateral sclerosis. The Journal of biological chemistry, 282(44), 32480–32490.PubMed

Giorgino, F., de Robertis, O., Laviola, L., Montrone, C., Perrini, S., McCowen, K. C., et al. (2000). The sentrin-conjugating enzyme mUbc9 interacts with GLUT4 and GLUT1 glucose transporters and regulates transporter levels in skeletal muscle cells. Proceedings of the National Academy of Sciences of the United States of America, 97(3), 1125–1130.PubMed

Gius, D., Botero, A., Shah, S., & Curry, H. A. (1999). Intracellular oxidation/reduction status in the regulation of transcription factors NF-kappaB and AP-1. Toxicology Letters, 106(2–3), 93–106.PubMed

Guo, D., Han, J., Adam, B.-L., Colburn, N. H., Wang, M.-H., Dong, Z., et al. (2005). Proteomic analysis of SUMO4 substrates in HEK293 cells under serum starvation-induced stress. Biochemical and Biophysical Research Communications, 337(4), 1308–1318.PubMed

Guo, D., Li, M., Zhang, Y., Yang, P., Eckenrode, S., Hopkins, D., et al. (2004). A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nature Genetics, 36(8), 837–841.PubMed

Henchcliffe, C., & Beal, M. F. (2008). Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nature clinical practice. Neurology, 4(11), 600–609.PubMed

Hernández, F., Gómez de Barreda, E., Fuster-Matanzo, A., Lucas, J. J., & Avila, J. (2010). GSK3: A possible link between beta amyloid peptide and tau protein. Experimental Neurology, 223(2), 322–325.PubMed

Hershko, A., & Ciechanover, A. (1998). The ubiquitin system. Annual Review of Biochemistry, 67, 425–479.PubMed

Hershko, A., Heller, H., Elias, S., & Ciechanover, A. (1983). Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. The Journal of biological chemistry, 258(13), 8206–8214.PubMed

Hochstrasser, M. (2000a). Biochemistry. All in the ubiquitin family. Science (New York, NY), 289(5479), 563–564.

Hochstrasser, M. (2000b). Evolution and function of ubiquitin-like protein-conjugation systems. Nature Cell Biology, 2(8), E153–E157.PubMed

Hochstrasser, Mark. (2009). Origin and function of ubiquitin-like proteins. Nature, 458(7237), 422–429.PubMed

Huang, J., & Berger, S. L. (2008). The emerging field of dynamic lysine methylation of non-histone proteins. Current Opinion in Genetics and Development, 18(2), 152–158.PubMed

Huang, H., Du, G., Chen, H., Liang, X., Li, C., Zhu, N., et al. (2011). Drosophila Smt3 negatively regulates JNK signaling through sequestering Hipk in the nucleus. Development(Cambridge, England), 138(12), 2477–2485.

Huang, E. J., & Reichardt, L. F. (2003). Trk receptors: Roles in neuronal signal transduction. Annual Review of Biochemistry, 72, 609–642.PubMed

Kerscher, O., Felberbaum, R., & Hochstrasser, M. (2006). Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell and Developmental Biology, 22, 159–180.PubMed

Kharb, S., Singh, V., Ghalaut, P. S., & Singh, G. P. (2000). Oxidative stress after acute myocardial infarction: Effect of thrombolytic treatment. The Journal of the Association of Physicians of India, 48(6), 578–580.PubMed

Krumova, P., Meulmeester, E., Garrido, M., Tirard, M., Hsiao, H–. H., Bossis, G., et al. (2011). Sumoylation inhibits alpha-synuclein aggregation and toxicity. The Journal of cell biology, 194(1), 49–60.PubMed

Krumova, P., & Weishaupt, J. H. (2013). Sumoylation in neurodegenerative diseases. Cellular and molecular life sciences : CMLS, 70(12), 2123–2138.PubMed

Kuan, C. Y., Yang, D. D., Samanta Roy, D. R., Davis, R. J., Rakic, P., & Flavell, R. A. (1999). The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron, 22(4), 667–676.PubMed

Kyriakis, J. M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E. A., Ahmad, M. F., et al. (1994). The stress-activated protein kinase subfamily of c-Jun kinases. Nature, 369(6476), 156–160.PubMed

La Rosa, L. R., Matrone, C., Ferraina, C., Panico, M. B., Piccirilli, S., Di Certo, M. G., et al. (2013). Age-related changes of hippocampal synaptic plasticity in AβPP-null mice are restored by NGF through p75NTR. Journal of Alzheimer’s disease : JAD, 33(1), 265–272.PubMed

Lalioti, V. S., Vergarajauregui, S., Pulido, D., & Sandoval, I. V. (2002). The insulin-sensitive glucose transporter, GLUT4, interacts physically with Daxx. Two proteins with capacity to bind Ubc9 and conjugated to SUMO1. The Journal of biological chemistry, 277(22), 19783–19791.PubMed

Lambeth, J. D. (2004). NOX enzymes and the biology of reactive oxygen. Nature Reviews Immunology, 4(3), 181–189.PubMed

Lee, Y.-S., Jang, M.-S., Lee, J.-S., Choi, E.-J., & Kim, E. (2005). SUMO-1 represses apoptosis signal-regulating kinase 1 activation through physical interaction and not through covalent modification. EMBO Reports, 6(10), 949–955.PubMed

Leitao, B. B., Jones, M. C., & Brosens, J. J. (2011). The SUMO E3-ligase PIAS1 couples reactive oxygen species-dependent JNK activation to oxidative cell death. The FASEB journal : Official Publication of the Federation of American Societies for Experimental Biology, 25(10), 3416–3425.

Li, M., Guo, D., Isales, C. M., Eizirik, D. L., Atkinson, M., She, J.-X., et al. (2005). SUMO wrestling with type 1 diabetes. Journal of molecular medicine (Berlin, Germany), 83(7), 504–513.

Li, T., Huang, S., Dong, M., Gui, Y., & Wu, D. (2012). Prognostic impact of SUMO-specific protease 1 (SENP1) in prostate cancer patients undergoing radical prostatectomy. Urologic Oncology. doi:10.1016/j.urolonc.2012.03.007.

Li, X., Luo, Y., Yu, L., Lin, Y., Luo, D., Zhang, H., et al. (2008). SENP1 mediates TNF-induced desumoylation and cytoplasmic translocation of HIPK1 to enhance ASK1-dependent apoptosis. Cell Death and Differentiation, 15(4), 739–750.PubMed

Liochev, S. I. (2013). Reactive oxygen species and the free radical theory of aging. Free Radical Biology and Medicine, 60, 1–4.PubMed

Ma, Q.-L., Yang, F., Rosario, E. R., Ubeda, O. J., Beech, W., Gant, D. J., et al. (2009). Beta-amyloid oligomers induce phosphorylation of tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. The Journal of neuroscience : The Official Journal of the Society for Neuroscience, 29(28), 9078–9089.

Mahajan, R., Delphin, C., Guan, T., Gerace, L., & Melchior, F. (1997). A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell, 88(1), 97–107.PubMed

Manza, L. L., Codreanu, S. G., Stamer, S. L., Smith, D. L., Wells, K. S., Roberts, R. L., et al. (2004). Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chemical Research in Toxicology, 17(12), 1706–1715.PubMed

Markesbery, W. R. (1997). Oxidative stress hypothesis in Alzheimer’s disease. Free Radical Biology and Medicine, 23(1), 134–147.PubMed

Matunis, M. J., Coutavas, E., & Blobel, G. (1996). A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. The Journal of cell biology, 135(6 Pt 1), 1457–1470.PubMed

May, J. M., & de Haën, C. (1979). Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. The Journal of biological chemistry, 254(7), 2214–2220.PubMed

McDoniels-Silvers, A. L., Nimri, C. F., Stoner, G. D., Lubet, R. A., & You, M. (2002). Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas. Clinical cancer research : An Official Journal of the American Association for Cancer Research, 8(4), 1127–1138.

McLennan, Y., Polussa, J., Tassone, F., & Hagerman, R. (2011). Fragile x syndrome. Current Genomics, 12(3), 216–224.PubMed

Melchior, F. (2000). SUMO–nonclassical ubiquitin. Annual Review of Cell and Developmental Biology, 16, 591–626.PubMed

Minty, A., Dumont, X., Kaghad, M., & Caput, D. (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. The Journal of Biological Chemistry, 275(46), 36316–36323.PubMed

Moore, D. J., Zhang, L., Dawson, T. M., & Dawson, V. L. (2003). A missense mutation (L166P) in DJ-1, linked to familial Parkinson’s disease, confers reduced protein stability and impairs homo-oligomerization. Journal of Neurochemistry, 87(6), 1558–1567.PubMed

Muller, S., Berger, M., Lehembre, F., Seeler, J. S., Haupt, Y., & Dejean, A. (2000). c-Jun and p53 activity is modulated by SUMO-1 modification. The Journal of Biological Chemistry, 275(18), 13321–13329.PubMed

Navascués, J., Bengoechea, R., Tapia, O., Vaqué, J. P., Lafarga, M., & Berciano, M. T. (2007). Characterization of a new SUMO-1 nuclear body (SNB) enriched in pCREB, CBP, c-Jun in neuron-like UR61 cells. Chromosoma, 116(5), 441–451.PubMed

Nisticò, R., Piccirilli, S., Cucchiaroni, M. L., Armogida, M., Guatteo, E., Giampà, C., et al. (2008). Neuroprotective effect of hydrogen peroxide on an in vitro model of brain ischaemia. British Journal of Pharmacology, 153(5), 1022–1029.PubMed

Ogata, M., Hino, S., Saito, A., Morikawa, K., Kondo, S., Kanemoto, S., et al. (2006). Autophagy is activated for cell survival after endoplasmic reticulum stress. Molecular and Cellular Biology, 26(24), 9220–9231.PubMed

Okura, T., Gong, L., Kamitani, T., Wada, T., Okura, I., Wei, C. F., et al. (1996). Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. The Journal of Immunology, 157(10), 4277–4281.PubMed

Olzmann, J. A., Brown, K., Wilkinson, K. D., Rees, H. D., Huai, Q., Ke, H., et al. (2004). Familial Parkinson’s disease-associated L166P mutation disrupts DJ-1 protein folding and function. The Journal of Biological Chemistry, 279(9), 8506–8515.PubMed

Patel, V. P., & Chu, C. T. (2011). Nuclear transport, oxidative stress, and neurodegeneration. International Journal of Clinical and Experimental Pathology, 4(3), 215–229.PubMed

Ploia, C., Antoniou, X., Sclip, A., Grande, V., Cardinetti, D., Colombo, A., et al. (2011). JNK plays a key role in tau hyperphosphorylation in Alzheimer’s disease models. Journal of Alzheimer’s Disease : JAD, 26(2), 315–329.PubMed

Pulverer, B. J., Kyriakis, J. M., Avruch, J., Nikolakaki, E., & Woodgett, J. R. (1991). Phosphorylation of c-jun mediated by MAP kinases. Nature, 353(6345), 670–674.PubMed

Rhee, S. G., Kang, S. W., Jeong, W., Chang, T.-S., Yang, K.-S., & Woo, H. A. (2005). Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Current Opinion in Cell Biology, 17(2), 183–189.PubMed

Rodriguez, M. S., Dargemont, C., & Hay, R. T. (2001). SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. The Journal of Biological Chemistry, 276(16), 12654–12659.PubMed

Rui, H.-L., Fan, E., Zhou, H.-M., Xu, Z., Zhang, Y., & Lin, S.-C. (2002). SUMO-1 modification of the C-terminal KVEKVD of Axin is required for JNK activation but has no effect on Wnt signaling. The Journal of Biological Chemistry, 277(45), 42981–42986.PubMed

Ruipérez, V., Darios, F., & Davletov, B. (2010). Alpha-synuclein, lipids and Parkinson’s disease. Progress in Lipid Research, 49(4), 420–428.PubMed

Ryu, J., Cho, S., Park, B. C., & Lee, D. H. (2010). Oxidative stress-enhanced SUMOylation and aggregation of ataxin-1: Implication of JNK pathway. Biochemical and Biophysical Research Communications, 393(2), 280–285.PubMed

Schneider Aguirre, R., & Karpen, S. J. (2013). Inflammatory Mediators Increase SUMOylation of RXRα in a JNK-Dependent Manner in Human Hepatocellular Carcinoma Cells. Molecular Pharmacology, 84(2), 218–226.PubMed

Sclip, A., Antoniou, X., Colombo, A., Camici, G. G., Pozzi, L., Cardinetti, D., et al. (2011). c-Jun N-terminal kinase regulates soluble Aβ oligomers and cognitive impairment in AD mouse model. The Journal of Biological Chemistry, 286(51), 43871–43880.PubMed

Shchemelinin, I., Sefc, L., & Necas, E. (2006). Protein kinases, their function and implication in cancer and other diseases. Folia Biologica, 52(3), 81–100.PubMed

Shin, J., Yu, S.-B., Yu, U. Y., Jo, S. A., & Ahn, J.-H. (2010). Swedish mutation within amyloid precursor protein modulates global gene expression towards the pathogenesis of Alzheimer’s disease. BMB Reports, 43(10), 704–709.PubMed

Shinbo, Y., Niki, T., Taira, T., Ooe, H., Takahashi-Niki, K., Maita, C., et al. (2006). Proper SUMO-1 conjugation is essential to DJ-1 to exert its full activities. Cell Death and Differentiation, 13(1), 96–108.PubMed

Singh, U., & Jialal, I. (2006). Oxidative stress and atherosclerosis. Pathophysiology: The Official Journal of the International Society for Pathophysiology/ISP, 13(3), 129–142.

Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G., & Chen, Y. (2004). Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proceedings of the National Academy of Sciences of the United States of America, 101(40), 14373–14378.PubMed

Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997). Alpha-synuclein in Lewy bodies. Nature, 388(6645), 839–840.PubMed

Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S., Vergoten, G., Guérardel, C., et al. (2007). An acetylation/deacetylation-SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Molecular and Cellular Biology, 27(7), 2661–2675.PubMed

Taira, T., Saito, Y., Niki, T., Iguchi-Ariga, S. M. M., Takahashi, K., & Ariga, H. (2004). DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Reports, 5(2), 213–218.PubMed

Takahashi, K., Ishida, M., Komano, H., & Takahashi, H. (2008). SUMO-1 immunoreactivity co-localizes with phospho-Tau in APP transgenic mice but not in mutant Tau transgenic mice. Neuroscience Letters, 441(1), 90–93.PubMed

Tare, M., Modi, R. M., Nainaparampil, J. J., Puli, O. R., Bedi, S., Fernandez-Funez, P., et al. (2011). Activation of JNK signaling mediates amyloid-ß-dependent cell death. PLoS ONE, 6(9), e24361.PubMed

Trigueros-Motos, L., Gonzalez, J. M., Rivera, J., & Andres, V. (2011). Hutchinson-Gilford progeria syndrome, cardiovascular disease and oxidative stress. Frontiers in Bioscience (Scholar edition), 3, 1285–1297.

Tsutsui, H., Kinugawa, S., & Matsushima, S. (2011). Oxidative stress and heart failure. American Journal of Physiology. Heart and Circulatory Physiology, 301(6), H2181–H2190.PubMed

Um, J. W., & Chung, K. C. (2006). Functional modulation of parkin through physical interaction with SUMO-1. Journal of Neuroscience Research, 84(7), 1543–1554.PubMed

Wang, L., & Banerjee, S. (2004). Differential PIAS3 expression in human malignancy. Oncology Reports, 11(6), 1319–1324.PubMed

Wang, C.-Y., Podolsky, R., & She, J.-X. (2006). Genetic and functional evidence supporting SUMO4 as a type 1 diabetes susceptibility gene. Annals of the New York Academy of Sciences, 1079, 257–267.PubMed

Wang, J., Wang, Y., & Lu, L. (2012). De-SUMOylation of CCCTC binding factor (CTCF) in hypoxic stress-induced human corneal epithelial cells. The Journal of Biological Chemistry, 287(15), 12469–12479.PubMed

Wilkinson, K. A., & Henley, J. M. (2010). Mechanisms, regulation and consequences of protein SUMOylation. The Biochemical Journal, 428(2), 133–145.PubMed

Wislet-Gendebien, S., D’Souza, C., Kawarai, T., St George-Hyslop, P., Westaway, D., Fraser, P., et al. (2006). Cytosolic proteins regulate alpha-synuclein dissociation from presynaptic membranes. The Journal of Biological Chemistry, 281(43), 32148–32155.PubMed

Xu, Z., Lam, L. S. M., Lam, L. H., Chau, S. F., Ng, T. B., & Au, S. W. N. (2008). Molecular basis of the redox regulation of SUMO proteases: A protective mechanism of intermolecular disulfide linkage against irreversible sulfhydryl oxidation. FASEB journal : Official Publication of the Federation of American Societies for Experimental Biology, 22(1), 127–137.

Xu, Y., Li, J., Zuo, Y., Deng, J., Wang, L.-S., & Chen, G.-Q. (2011). SUMO-specific protease 1 regulates the in vitro and in vivo growth of colon cancer cells with the upregulated expression of CDK inhibitors. Cancer Letters, 309(1), 78–84.PubMed

Yang, D. D., Kuan, C. Y., Whitmarsh, A. J., Rincón, M., Zheng, T. S., Davis, R. J., et al. (1997). Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature, 389(6653), 865–870.PubMed

Yang, X.-J., & Seto, E. (2008). Lysine acetylation: codified crosstalk with other posttranslational modifications. Molecular Cell, 31(4), 449–461.PubMed

Yoshikawa, T., Toyokuni, S., Yamamoto, Y., & Naito, Y. (2000). Free radicals in Chemistry, Biology and Medicine (pp. 580). UK: OICA International.

Yun, S.-M., Cho, S.-J., Song, J. C., Song, S. Y., Jo, S. A., Jo, C., et al. (2013). SUMO1 modulates Aβ generation via BACE1 accumulation. Neurobiology of Aging, 34(3), 650–662.PubMed

Zhang, F., & Chen, J. (2008). Leptin protects hippocampal CA1 neurons against ischemic injury. Journal of Neurochemistry, 107(2), 578–587.PubMed

Zhang, Y.-Q., & Sarge, K. D. (2008). Sumoylation of amyloid precursor protein negatively regulates Abeta aggregate levels. Biochemical and Biophysical Research Communications, 374(4), 673–678.PubMed

Zhang, F., Signore, A. P., Zhou, Z., Wang, S., Cao, G., & Chen, J. (2006). Erythropoietin protects CA1 neurons against global cerebral ischemia in rat: Potential signaling mechanisms. Journal of Neuroscience Research, 83(7), 1241–1251.PubMed

Zhao, J. (2007). Sumoylation regulates diverse biological processes. Cellular and Molecular Life Sciences : CMLS, 64(23), 3017–3033.PubMed

Title: SUMO: a (Oxidative) Stressed Protein
Authors: Marco Feligioni
Robert Nisticò
Publication date: 01-12-2013
Publisher: Springer US
Published in: NeuroMolecular Medicine / Issue 4/2013
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI: https://doi.org/10.1007/s12017-013-8266-6

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SUMO: a (Oxidative) Stressed Protein

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