Cerebral ischemia/stroke and small ubiquitin-like modifier (SUMO) conjugation - A new target for therapeutic intervention?

Journal of Neurochemistry

Volumn 106, Issue 3, 2008, Pages 989-999

  Yang, Wei ^a   Sheng, Huaxin ^a   Homi, H Mayumi ^a   Warner, David S ^a   Paschen, Wulf ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Brain; Focal cerebral ischemia; Forebrain ischemia; Post translational protein modification; Small ubiquitin like modifier conjugation; Stress response

Indexed keywords

SUMO PROTEIN;

BRAIN ISCHEMIA; HUMAN; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MODIFICATION; REVIEW; STROKE; SUMOYLATION;

ANIMALS; BRAIN ISCHEMIA; DRUG DELIVERY SYSTEMS; HUMANS; PHARMACEUTICAL PREPARATIONS; SIGNAL TRANSDUCTION; STROKE; SUMO-1 PROTEIN;

EID: 48349123998     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05404.x     Document Type: Review

References (137)

1. Abe K., Aoki M., Kawagoe J., Yoshida T., Hattori A., Kogure K. Itoyama Y. (1995) Ischemic delayed neuronal death. A mitochondrial hypothesis. Stroke 26, 1478 1489.
2. Althausen S., Mengesdorf T., Mies G., Olah L., Nairn A. C., Proud C. G. Paschen W. (2001) Changes in the phosphorylation of initiation factor eIF-2α, elongation factor eEF-2 and P70 S6 kinase after transient focal cerebral ischemia in mice. J. Neurochem. 78, 779 787.
3. Anckar J., Hietakangas V., Denessiouk K., Thiele D. J., Johnson M. S. Sistonen L. (2006) Inhibition of DNA binding by differential sumoylation of heat shock factors. Mol. Cell. Biol. 26, 955 964.
4. Ayaydin F. Dasso M. (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 15, 5208 5218.
5. Bae S. H., Jeong J. W., Park J. A., Kim S. H., Bae M. K., Choi S. J. Kim K. W. (2004) Sumoylation increases HIF-1alpha stability and its transcriptional activity. Biochem. Biophys. Res. Commun. 324, 394 400.
6. Bailey D. O'Hare P. (2004) Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J. Biol. Chem. 279, 692 703.
7. Barone F. C., Irving E. A., Ray A. M. et al. (2001) Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med. Res. Rev. 21, 129 145.
8. Bernstam L. Nriagu J. (2000) Molecular aspects of arsenic stress. J. Toxicol. Env. Health B Crit. Rev. 3, 293 322.
9. Besnault-Mascard L., Leprince C., Auffredou M. T., Meunier B., Bourgeade M. F., Camonis J., Lorenzo H. K. Vazquez A. (2005) Caspase-8 sumoylation is associated with nuclear localization. Oncogene 24, 3268 3273.
10. Bonny C., Borsello T. Zine A. (2005) Targeting the JNK pathway as a therapeutic protective strategy for nervous system diseases. Rev. Neurosci. 16, 57 67.
11. Bossis G. Melchior F. (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 21, 349 357.
12. Bright R. Mochly-Rosen D. (2005) The role of protein kinase C in cerebral ischemic and reperfusion injury. Stroke 36, 2781 2790.
13. Bronstein J. M., Farber D. B. Wasterlain C. G. (1993) Regulation of type-II calmodulin kinase: functional implications. Brain Res. Rev. 18, 135 147.
14. Burda J., Martin M. E., Garcia A., Alcazar A., Fando J. L. Salinas M. (1994) Phosphorylation of the α subunit of initiation factor 2 correlates with the inhibition of translation following transient cerebral ischemia in the rat. Biochem. J. 302, 335 338.
15. Carbia-Nagashima A., Gerez J., Perez-Castro C., Paez-Pereda M., Silberstein S., Stalla G. K., Holsboes F. Arzt E. (2007) RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1 alpha during hypoxia. Cell 131, 309 323.
16. Carey H. V., Andrews M. T. Martin S. L. (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 83, 1153 1181.
17. Chan P. H. (2001) Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metabol. 21, 2 14.
18. Chan H. Y., Warrick J. M., Andriola I., Merry D. Bonini N. M. (2002) Genetic modulation of polyglutamine toxicity by protein conjugation pathways in Drosophila. Hum. Mol. Gen. 11, 2895 2904.
19. Chavez J. C. LaManna J. C. (2002) Activation of hypoxia-inducible factor-1 in the rat cerebral cortex after transient global ischemia: potential role of insulin-like growth factor-1. J. Neurosci. 22, 8922 8931.
20. Chen J., Graham S. H., Zhu R. L. Simon R. P. (1996) Stress proteins and tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metabol. 16, 566 577.
21. Cheng J., Kang X., Zhang S. Yeh E. T. (2007) SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 131, 584 595.
22. Chu C. T., Levinthal D. J., Kulich S. M., Chalovich E. M. DeFranco D. B. (2004) Oxidative neuronal injury. The dark side of ERK1/2. Eur. J. Biochem. 271, 2060 2066.
23. Chung K. K., Dawson T. M. Dawson V. L. (2005) Nitric oxide, S-nitrosylation and neurodegeneration. Cell. Mol. Biol. 51, 247 254.
24. Cimarosti H., Lindberg C., Bomholt S. F., Ronn L. C. Henley J. M. (2008) Increased protein SUMOylation following focal cerebral ischemia. Neuropharmacology 54, 280 289.
25. DeGracia D. J. Hu B. R. (2007) Irreversible translation arrest in the reperfused brain. J. Cereb. Blood Flow Metabol. 27, 875 893.
26. DeGracia D. J. Montie H. L. (2004) Cerebral ischemia and the unfolded protein response. J. Neurochem. 91, 1 8.
27. DeGracia D. J., Neumar R. W., White B. C. Krause G. S. (1996) Global brain ischemia and reperfusion: modifications in eukaryotic initiation factors associated with inhibition of translation initiation. J. Neurochem. 67, 2005 2012.
28. Desterro J. M. P., Thomson J. Hay R. T. (1997) Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett. 417, 297 300.
29. Desterro J. M. P., Rodriguez M. S., Kemp G. D. Hay R. T. (1999) Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274, 10618 10624.
30. Dirnagl U., Simon R. P. Hallenbeck J. M. (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 26, 248 254.
31. Domanska-Janik K. (1996) Protein serine/threonine kinases (PKA, PKC, CaMKII) involved in ischemic brain pathology. Acta Neurobiol. Exp. 56, 579 585.
32. Dorval V. Fraser P. E. (2006) Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein. J. Biol. Chem. 281, 9919 9924.
33. Dorval V. Fraser P. E. (2007) SUMO on the road to neurodegeneration. Biochim. Biophys. Acta 1773, 694 706.
34. Dorval V., Mazzella M. J., Mathews P. M., Hay R. T. Fraser P. E. (2007) Modulation of Aβ generation by small ubiquitin-like modifiers does not require conjugation to target proteins. Biochem. J. 404, 309 316.
35. Fei E., Jia N., Yan M. et al. (2006) SUMO-1 modification increases human SOD1 stability and aggregation. Biochem. Biophys. Res. Commun. 347, 406 412.
36. Ferrer I., Friguls B., Dalfo E. Planas A. M. (2003) Early modifications in the expression of mitogen-activated protein kinase (MAPK/ERK), stress-activated kinases SAPK/JNK and p38, and their phosphorylated substrates following focal cerebral ischemia. Acta Neuropathol. 105, 425 437.
37. Fiskum G. (2000) Mitochondrial participation in ischemic and traumatic neuronal cell death. J. Neurotrauma 17, 843 855.
38. Frerichs K. U. Hallenbeck J. M. (1998) Hibernation in ground squirrels induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. J. Cereb. Blood Flow Metabol. 18, 168 175.
39. Frerichs K. U., Kennedy C., Sokoloff L. Hallenbeck J. M. (1994) Local cerebral blood flow during hibernation, a model of natural tolerance to 'cerebral ischemia'. J. Cereb. Blood Flow Metabol. 14, 193 205.
40. Frerichs K. U., Smith C. B., Brenner M., DeGracia D. J., Krause G. S., Marrone L., Dever T. E. Hallenbeck J. M. (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc. Natl Acad. Sci. USA 95, 14511 14516.
41. Ge P., Luo Y., Liu C. L. Hu B. (2007) Protein aggregation and proteasome dysfunction after brain ischemia. Stroke 38, 3230 3236.
42. 2+ as a key regulator of cell life and death. Cell Death Diff. 14, 1267 1274.
43. Gibb S. L., Boston-Howes W., Lavina Z. S., Gustincich S., Brown R. H. Jr, Pasinelli P. Trotti D. (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. J. Biol. Chem. 282, 32480 32490.
44. Giffard R. G., Xu L., Zhao H., Carrico W., Ouyang Y., Qiao Y., Sapolsky R., Steinberg G., Hu B. Yenari M. A. (2004) Chaperones, protein aggregation, and brain protection from hypoxic/ischemic injury. J. Exp. Biol. 207, 3213 3220.
45. Gill G. (2003) Post-translational modifications by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr. Opin. Genet. Dev. 13, 108 113.
46. Giorgino F., de Robertis O., Laviola L., Montrone C., Perrini S., McCowen K. C. Smith R. J. (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 1130.
47. Gong L. Yeh E. T. (2006) Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 and SUMO-3. J. Biol. Chem. 281, 15869 15877.
48. Gong L., Li B., Millas S. Yeh E. T. H. (1999) Molecular cloning and characterization of human AOS1 and UBA2, components of the sentrin-activating enzyme complex. FEBS Lett. 448, 185 189.
49. Guo B., Yang S.-H., Witty J. Sharrocks A. D. (2007) Signalling pathways and the regulation of SUMO conjugation. Biochem. Soc. Trans. 35, 1414 1418.
50. Gustavsson M., Anderson M. F., Mallard C. Hagberg H. (2005) Hypoxic preconditioning confers long-term reduction of brain injury and improvement of neurological ability in immature rats. Pediatr. Res. 57, 305 309.
51. Gustavsson M., Mallard C., Vannucci S. J., Wilson M. A., Johnston M. V. Hagberg H. (2007) Vascular response to hypoxic preconditioning in the immature brain. J. Cereb. Blood Flow Metabol. 27, 928 938.
52. Halliwell B. (2006) Proteasomal dysfunction: a common feature of neuro degenerative diseases? Implications for the environmental origins of neurodegeneration. Antioxid. Redox Signal. 8, 2007 2019.
53. Harding H. P., Zhang Y. Ron D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271 274.
54. Hay R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1 12.
55. Hay R. T. (2007) SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 17, 370 376.
56. Hayashi N., Shirakura H., Uehara T. Nomura Y. (2006) Relationship between SUMO-1 modification of caspase-7 and its nuclear localization in human neuronal cells. Neurosci. Lett. 397, 5 9.
57. Hegde A. N. Upadhya S. C. (2007) The ubiquitin-proteasome pathway in health and disease of the nervous system. Trends Neurosci. 30, 587 595.
58. Heun P. (2007) SUMOrganization of the nucleus. Curr. Opin. Cell Biol. 19, 350 355.
59. Hietakangas V., Ahlskog J. K., Jakobsson A. M., Hellesuo M., Sahlberg N. M., Holmberg C. I., Mikhailov A., Palvimo J. J., Pirkkala L. Sistonen L. (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953 2968.
60. Higashi T., Nakai A., Uemura Y., Kikuchi H. Nagata K. (1995) Activation of heat shock factor 1 in rat brain during cerebral ischemia or after heat shock. Mol. Brain Res. 34, 262 270.
61. Hilgarth R. S., Hong Y. L., Park-Sarge O. K. Sarge K. D. (2003) Insights into the regulation of heat shock transcription factor 1 SUMO-1 modification. Biochem. Biophys. Res. Commun. 303, 196 200.
62. Hong Y., Rogers R., Matunis M. J., Mayhew C. N., Goodson M. L., Park-Sarge O. K. Sarge K. D. (2001) Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J. Biol. Chem. 276, 40263 40267.
63. Hu B. R., Martone M. E., Jones Y. Z. Liu C. L. (2000) Protein aggregation after transient cerebral ischemia. J. Neurosci. 20, 3191 3199.
64. Hu B. R., Janelidze S., Ginsberg M. D., Busto R., Perez-Pinzon M., Sick T. J., Siesjo B. K. Liu C. L. (2001) Protein aggregation after focal brain ischemia and reperfusion. J. Cereb. Blood Flow Metabol. 21, 865 875.
65. Huang T. T., Wuerzberger-Davis S. M., Wu Z. H. Miyamoto S. (2003) Sequential modification of NEMO/IKKγ by SUMO-1 and ubiquitin mediates NF-κB activation by genotoxic stress. Cell 115, 565 576.
66. Irving E. A. Bamford M. (2002) Role of mitogen- and stress-activated kinases in ischemic in jury. J. Cereb. Blood Flow Metabol. 22, 631 647.
67. Johnson E. S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355 382.
68. Johnson E. S. Blobel G. (1997) Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272, 26799 26802.
69. Johnson E. S., Schwienhorst I., Dohmen R. J. Blobel G. (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16, 5509 5519.
70. Kadare G., Toutant M., Formstecher E., Corvol J. C., Carnaud M., Boutterin M. C. Girault J. A. (2003) PIAS1-mediated sumoylation of focal adhesion kinase activates its autophosphorylation. J. Biol. Chem. 278, 47434 47440.
71. Kaminska B. (2005) MAPK signaling pathways as molecular targets for anti-inflammatory therapy - from molecular mechanisms to therapeutic benefits. Biochim. Biophys. Acta 1754, 253 262.
72. Kassed C. A., Butler T. L., Patton G. W., Demesquita D. D., Navidomskis M. T., Memet S., Israel A. Pennypacker K. R. (2004) Injury-induced NF-kappa B activation in the hippocampus: implications for neuronal survival. FASEB J. 18, 723 724.
73. Koh D. W., Dawson T. M. Dawson V. L. (2005) Poly(ADP-ribosyl)ation regulation of life and death in the nervous system. Cell. Mol. Life Sci. 62, 760 768.
74. Kristian T. Siesjo B. K. (1998) Calcium in ischemic cell death. Stroke 29, 705 718.
75. Kumar R., Azam S., Sullivan J. M. et al. (2001) Brain ischemia and reperfusion activates the eukaryotic initiation factor 2α kinase PERK. J. Neurochem. 77, 1418 1421.
76. Kumar R., Krause G. S., Yoshida H., Hori K. DeGracia D. J. (2003) Dysfunction of the unfolded protein response during global brain ischemia and reperfusion. J. Cereb. Blood Flow Metabol. 23, 462 471.
77. La Spada A. R., Wilson E. M., Lubahn D. B., Harding A. E. Fischbeck K. H. (1991) Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 352, 77 79.
78. Lee Y.j., Miyake S., Wakita H., McMullen D. C., Azuma Y., Auh S. Hallenbeck J. M. (2007) Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J. Cereb. Blood Flow Metabol. 27, 950 962.
79. Lewen A., Matz P. Chan P. H. (2000) Free radical pathways in CNS injury. J. Neurotrauma 17, 871 890.
80. Li Y., Wang H., Wang S., Quon D., Liu Y. W. Cordell B. (2003) Positive and negative regulation of APP amyloidogenesis by symoylation. Proc. Natl Acad. Sci. USA 100, 259 264.
81. Lipton S. A. (1996) Similarity of neuronal cell injury and death in AIDS dementia and focal cerebral ischemia - potential treatment with NMDA open-channel blockers and nitric oxide-related species. Brain Pathol. 6, 507 517.
82. Long X. Griffith L. C. (2000) Identification and characterization of a SUMO-1 conjugation system that modifies neuronal calcium/calmodulin-dependent protein kinase II in Drosophila melanogaster. J. Biol. Chem. 275, 40765 40776.
83. Mackay K. B., Stiefel T. H. Foster A. C. (2002) Ischemic preconditioning reduces infarct volume after subdural hematoma in the rat. Brain Res. 930, 200 205.
84. 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, 97 107.
85. Malhotra S., Savitz S. I., Ocava L. Rosenbaum D. M. (2006) Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack. J. Neurosci. Res. 83, 19 27.
86. Manza L. L., Codreanu S. G., Stamer S. L., Smith D. L., Wells K. S., Roberts R. L. Liebler D. C. (2004) Global shift in protein sumoylation in response to electrophile and oxidative stress. Chem. Res. Toxicol. 17, 1706 1715.
87. Martin S., Wilkinson K. A., Nishimune A. Henley J. M. (2007a) Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction. Nat. Rev. Neurosci. 8, 948 959.
88. Martin S., Nishimune A., Mellor J. R. Henley J. M. (2007b) SUMOylation regulates kainite-receptor-mediated synaptic transmission. Nature 447, 321 325.
89. Mattson M. P. (2006) Neuronal life-and-death signaling, apoptosis, and neurodegenerative disorders. Antioxid. Redox Signal. 8, 1997 2006.
90. 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. J. Cell Biol. 135, 1457 1470.
91. McFadden K., Hamilton R. L., Insalaco S. J., Lavine L., Al-Mateen M., Wang G. Wiley C. A. (2005) Neuronal intranuclear inclusion disease without polyglutamine inclusions in a child. J. Neuropathol. Exp. Neurol. 64, 545 552.
92. Melchior F., Schergaut M. Pichler A. (2003) SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem. Sci. 28, 612 618.
93. Mitra S. K., Hanson D. A. Schlaepfer D. D. (2005) Focal adhesion kinase: in commend and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56 58.
94. Mo Y. Y., Yu Y., Theodosiou E., Rachel Ee P. L. Beck W. T. (2005) A role for Ubc9 in tumorigenesis. Oncogene 24, 2677 2683.
95. Moschos S. J. Mo Y. Y. (2006) Role of SUMO/Ubc9 in DNA damage repair and tumorigenesis. J. Mol. Histol. 37, 309 319.
96. Mukhopadhyay D. Dasso M. (2007) Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286 295.
97. Muller S., Ledl A. Schmidt D. (2004) SUMO: a regulator of gene expression and genome integrity. Oncogene 23, 1998 2008.
98. Nguyen H. V., Chen J. L., Zhong J., Kim K. J., Crandall E. D., Borok Z., Chen Y. Ann D. K. (2006) SUMOylation attenuates sensitivity toward hypoxia- or desferroxamine-induced injury by modulating adaptive responses in salivary epithelial cells. Am. J. Pathol. 168, 1452 1463.
99. Nowak M. Hammerschmidt M. (2006) Ubc9 regulates mitosis and cell survival during zebrafish development. Mol. Biol. Cell 17, 5324 5336.
100. Nozaki K., Nishimura M. Hashimoto N. (2001) Mitogen-activated protein kinases and cerebral ischemia. Mol. Neurobiol. 23, 1 19.
101. Ogawa S., Kitao Y. Hori O. (2007) Ischemia-induced neuronal cell death and stress response. Antioxid. Redox Signal. 9, 573 587.
102. Ohshima T. Shimotohno K. (2003) Transforming growth factor-β- mediated signaling via the p38 MAP kinase pathway activates Smad-dependent transcription through SUMO-1 modification of Smad4. J. Biol. Chem. 278, 50833 50842.
103. Orth M. Schapira A. H. (2001) Mitochondria and degenerative disorders. Am. J.Med. Genet. 106, 27 36.
104. Paschen W. (2003a) Shutdown of translation: lethal or protective? Unfolded protein response versus apoptosis. J. Cereb. Blood Flow Metabol. 23, 773 779.
105. Paschen W. (2003b) Mechanisms of neuronal cell death: diverse roles of calcium in the various subcellular compartments. Cell Calcium 34, 305 310.
106. Paschen W. Doutheil J. (1999) Disturbances of the functioning of endoplasmic reticulum: a key mechanism underlying neuronal cell injury? J. Cereb. Blood Flow Metabol. 19, 1 18.
107. Paschen W. Frandsen A. (2001) Endoplasmic reticulum dysfunction - a common denominator for cell injury in acute and degenerative diseases of the brain? J. Neurochem. 79, 719 725.
108. Paschen W., Proud C. G. Mies G. (2007) Shut-down of translation, a global stress response: mechanisms and pathological relevance. Curr. Pharm. Design 13, 1887 1902.
109. Perez-Pinzon M. A., Dave K. R. Raval A. P. (2005) Role of reactive oxygen species and protein kinase C in ischemic tolerance in the brain. Antioxid. Redox Signal. 7, 1150 1157.
110. Pichler A. Melchior F. (2002) Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport. Traffic 3, 381 387.
111. Planas A. M., Gorina R. Chamorro A. (2006) Signalling pathways mediating inflammatory responses in brain ischaemia. Biochem. Soc. Trans. 34, 1267 1270.
112. Pountney D. L., Huang Y., Burns R. J., Haan E., Thompson P. D., Blumbergs P. C. Gai W. P. (2003) SUMO-1 marks the nuclear inclusions in familial neuronal intranuclear inclusion disease. Exp. Neurol. 184, 436 446.
113. Pountney D. L., Chegini F., Shen X., Blumbergs P. C. Gai W. P. (2005) SUMO-1 marks subdomains within glial cytoplasmic inclusions of multiple system atrophy. Neurosci. Lett. 381, 74 79.
114. Riley B. E., Zoghbi H. Y. Orr H. T. (2005) SUMOylation of the polyglutamine repeat protein, ataxin-1, is dependent on a functional nuclear localization signal. J. Biol. Chem. 280, 21942 21948.
115. Rodriguez-Munoz M., Bermudez D., Sanchez-Blazquez P. Garzon J. (2007) Sumoylated RGS-Rz proteins act as scaffolds for Mu-opioid receptors and G-protein complexes in mouse brain. Neuropsychopharmacology 32, 842 850.
116. Roybal C. N., Hunsaker L. A., Barbash O., Jagt D. L. V. Abcouwer S. F. (2005) The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism. J. Biol. Chem. 280, 20331 20339.
117. Schneider R. J. (2000) Translational control during heat shock, in Translational Control of Gene Expression (Sonenberg N., Hershes J. W. B. Mathews M. B., eds pp. 581 594. Cold Spring Habor Laboratory Press, Cold Spring Habor.
118. Seeler J. S. Dejean A. (2003) Nuclear and unuclear functions of SUMO. Nat. Rev. Cell Biol. 4, 690 699.
119. Shao R., Zhang F. P., Tian F., Friberg P. A., Wang X., Sjoeland H. Billig H. (2004) Increase in SUMO-1 expression in response to hypoxia: direct interaction with HIF-1α in adult mouse brain and heart in vivo. FEBS Lett. 569, 293 300.
120. Steffan J. S., Agrawal N., Pallos J. et al. (2004) SUMO modification of Huntington's disease pathology. Science 304, 100 104.
121. Storey K. B. (2003) Mammalian hibernation. Transcriptional and translational controls. Adv. Exp. Med. Biol. 543, 21 38.
122. Sun X. C., Li W. B., Zhang M., Xian X. H., Qi J., Jin R. L. Li S. Q. (2006) Limb ischemic preconditioning induces brain ischemic tolerance via p38 MAPK. Brain Res. 1084, 165 174.
123. Takahashi-Fujigasaki J., Arai K., Funata N. Fujigasaki H. (2006) SUMOylation substrates in neuronal intranuclear inclusion disease. Neuropathol. Appl. Neurobiol. 32, 92 100.
124. Terashima T., Kawai H., Fujitani M., Maeda K. Yasuda H. (2002) SUMO-1 co-localized with mutant atrophin-1 with expanded polyglutamines accelerates intranuclear aggregation and cell death. Neuroreport 13, 2359 2364.
125. Toyoda T., Kassell N. F. Lee K. S. (1997) Induction of ischemic tolerance and antioxidant activity by brief focal ischemia. Neuroreport 8, 847 851.
126. Trushina E. McMurray C. T. (2007) Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 145, 1233 1248.
127. Tymianski M. Tator C. H. (1996) Normal and abnormal calcium homeostasis in neurons - a basis for the pathophysiology of traumatic and ischemic central nervous system injury. Neurosurgery 38, 1176 1195.
128. Ueda H., Goto J., Hashida H., Lin X., Oyanagi K., Kawano H., Zoghbi H. Y., Kanazawa I. Okazawa H. (2002) Enhanced SUMOylation in polyglutamine diseases. Biochem. Biophys. Res. Commun. 293, 307 313.
129. Um J. W. Chung K. C. (2006) Functional modulation of Parkin through physical interaction with SUMO-1. J. Neurosci. Res. 84, 1543 1554.
130. Van Niekerk E. A., Willis D. E., Chang J. H., Reumann K., Heise T. Twiss J. L. (2007) Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc. Natl Acad. Sci. USA 104, 12913 12918.
131. Vertegaal A. C. O. (2007) Small ubiquitin-related modifiers in chains. Biochem. Soc. Trans. 35, 1422 1423.
132. 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 J. 22, 127 137.
133. Yang W., Sheng H., Warner D. S. Paschen W. (2008a) Transient global cerebral ischemia induces a massive increase in protein sumoylation. J. Cereb. Blood Flow Metabol. 28, 269 279.
134. Yang W., Sheng H., Warner D. S. Paschen W. (2008b) Transient focal cerebral ischemia induces a dramatic activation of small ubiquitin-like modifier conjugation. J. Cereb. Blood Flow Metabol. DOI:.
135. Zhao J. (2007) Sumoylation regulates diverse biological processes. Cell. Mol. Life Sci. 64, 3017 3033.
136. Zhao H., Sapolsky R. M. Steinberg G. K. (2006) Phosphoinositide-3-kinase/ akt survival signal pathways are implicated in neuronal survival after stroke. Mol. Neurobiol. 34, 249 270.
137. Zhong N., Kim C. Y., Rizzu P., Geula C., Porter D. R., Pothos E. N., Squitieri F., Heutink P. Xu J. (2006) DJ-1 transcriptionally up-regulates the human tyrosine hydroxylase by inhibiting the sumoylation of pyrimidine tract-binding protein-associated splicing factor. J. Biol. Chem. 281, 20940 20948.