Modification of ubiquitin-C-terminal hydrolase-L1 by cyclopentenone prostaglandins exacerbates hypoxic injury

Neurobiology of Disease

Volumn 41, Issue 2, 2011, Pages 318-328

  Liu, Hao ^a,b   Li, Wenjin ^a,b   Ahmad, Muzamil ^a,b   Miller, Tricia M ^c   Rose, Marie E ^a,b   Poloyac, Samuel M ^c   Uechi, Guy ^c   Balasubramani, Manimalha ^c   Hickey, Robert W ^b   Graham, Steven H ^a,b  

^a GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Arachidonic acid; Cyclopentenone prostaglandins; Hypoxic neuronal injury; Protein post translational modification; Ubiquitin C terminal hydrolase L1; Ubiquitin proteasome pathway

Indexed keywords

ARACHIDONIC ACID; CYCLOPENTENONE; HYDROLASE; PROSTAGLANDIN; UBIQUITIN THIOLESTERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELL DEATH; CONTROLLED STUDY; ELECTROPHILICITY; ENZYME ACTIVITY; HYPOXIA; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; RAT; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; CELL HYPOXIA; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HYPOXIA-ISCHEMIA, BRAIN; NERVE DEGENERATION; PROSTAGLANDIN D2; RATS; RATS, SPRAGUE-DAWLEY; TRANSDUCTION, GENETIC; UBIQUITIN THIOLESTERASE;

EID: 78650598280     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.09.020     Document Type: Article

References (53)

1. Ahmad M., Zhang Y., Liu H., Rose M.E., Graham S.H. Prolonged opportunity for neuroprotection in experimental stroke with selective blockade of cyclooxygenase-2 activity. Brain Res. 2009, 1279:168-173.
2. Aldini G., Carini M., Vistoli G., Shibata T., Kusano Y., Gamberoni L., Dalle-Donne I., Milzani A., Uchida K. Identification of actin as a 15-deoxy-Delta12, 14-prostaglandin J2 target in neuroblastoma cells: mass spectrometric, computational, and functional approaches to investigate the effect on cytoskeletal derangement. Biochemistry 2007, 46:2707-2718.
3. Cao G., Pei W., Ge H., Liang Q., Luo Y., Sharp F.R., Lu A., Ran R., Graham S.H., Chen J. In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J. Neurosci. 2002, 22:5423-5431.
4. Choi J., Levey A.I., Weintraub S.T., Rees H.D., Gearing M., Chin L.S., Li L. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 2004, 279:13256-13264.
5. Colgan L., Liu H., Huang S.Y., Liu Y.J. Dileucine motif is sufficient for internalization and synaptic vesicle targeting of vesicular acetylcholine transporter. Traffic 2007, 8:512-522.
6. Garcia-Bueno B., Madrigal J.L., Lizasoain I., Moro M.A., Lorenzo P., Leza J.C. The anti-inflammatory prostaglandin 15d-PGJ2 decreases oxidative/nitrosative mediators in brain after acute stress in rats. Psychopharmacology (Berl.) 2005, 180:513-522.
7. Ge P., Luo Y., Liu C.L., Hu B. Protein aggregation and proteasome dysfunction after brain ischemia. Stroke 2007, 38:3230-3236.
8. Giasson B.I., Lee V.M. Are ubiquitination pathways central to Parkinson's disease?. Cell 2003, 114:1-8.
9. Gong B., Cao Z., Zheng P., Vitolo O.V., Liu S., Staniszewski A., Moolman D., Zhang H., Shelanski M., Arancio O. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 2006, 126:775-788.
10. Horiguchi T., Snipes J.A., Kis B., Shimizu K., Busija D.W. Cyclooxygenase-2 mediates the development of cortical spreading depression-induced tolerance to transient focal cerebral ischemia in rats. Neuroscience 2006, 140:723-730.
11. Kabuta T., Setsuie R., Mitsui T., Kinugawa A., Sakurai M., Aoki S., Uchida K., Wada K. Aberrant molecular properties shared by familial Parkinson's disease-associated mutant UCH-L1 and carbonyl-modified UCH-L1. Hum. Mol. Genet. 2008, 17:1482-1496.
12. Kim I.K., Lee J.H., Sohn H.W., Kim H.S., Kim S.H. Prostaglandin A2 and delta 12-prostaglandin J2 induce apoptosis in L1210 cells. FEBS Lett. 1993, 321:209-214.
13. Kliewer S.A., Lenhard J.M., Willson T.M., Patel I., Morris D.C., Lehmann J.M. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 1995, 83:813-819.
14. Koharudin L.M., Liu H., Di Maio R., Kodali R.B., Graham S.H., Gronenborn A.M. Cyclopentenone prostaglandin-induced unfolding and aggregation of the Parkinson disease-associated UCH-L1. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6835-6840.
15. Kondo M., Shibata T., Kumagai T., Osawa T., Shibata N., Kobayashi M., Sasaki S., Iwata M., Noguchi N., Uchida K. 15-Deoxy-Delta 12, 14-prostaglandin J2: the endogenous electrophile that induces neuronal apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2002, 21:21.
16. Kondo M., Shibata T., Kumagai T., Osawa T., Shibata N., Kobayashi M., Sasaki S., Iwata M., Noguchi N., Uchida K. 15-Deoxy-Delta(12, 14)-prostaglandin J(2): the endogenous electrophile that induces neuronal apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:7367-7372.
17. Li Z., Jansen M., Ogburn K., Salvatierra L., Hunter L., Mathew S., Figueiredo-Pereira M.E. Neurotoxic prostaglandin J2 enhances cyclooxygenase-2 expression in neuronal cells through the p38MAPK pathway: a death wish?. J. Neurosci. Res. 2004, 78:824-836.
18. Li Z., Melandri F., Berdo I., Jansen M., Hunter L., Wright S., Valbrun D., Figueiredo-Pereira M.E. Delta12-prostaglandin J2 inhibits the ubiquitin hydrolase UCH-L1 and elicits ubiquitin-protein aggregation without proteasome inhibition. Biochem. Biophys. Res. Commun. 2004, 319:1171-1180.
19. Li W., Wu S., Hickey R.W., Rose M.E., Chen J., Graham S.H. Neuronal cyclooxygenase-2 activity and prostaglandins PGE2, PGD2, and PGF2 alpha exacerbate hypoxic neuronal injury in neuron-enriched primary culture. Neurochem. Res. 2008, 33:490-499.
20. Li W., Wu S., Ahmad M., Jiang J., Liu H., Nagayama T., Rose M.E., Tyurin V.A., Tyurina Y.Y., Borisenko G.G., Belikova N., Chen J., Kagan V.E., Graham S.H. The cyclooxygenase site, but not the peroxidase site of cyclooxygenase-2 is required for neurotoxicity in hypoxic and ischemic injury. J. Neurochem. 2010, 113:965-977.
21. Lin T.N., Cheung W.M., Wu J.S., Chen J.J., Lin H., Chen J.J., Liou J.Y., Shyue S.K., Wu K.K. 15d-Prostaglandin J2 protects brain from ischemia-reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 2006, 26:481-487.
22. Liu Y., Fallon L., Lashuel H.A., Liu Z., Lansbury P.T. The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 2002, 111:209-218.
23. Liu Y., Lashuel H.A., Choi S., Xing X., Case A., Ni J., Yeh L.A., Cuny G.D., Stein R.L., Lansbury P.T. Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Chem. Biol. 2003, 10:837-846.
24. Liu C.L., Ge P., Zhang F., Hu B.R. Co-translational protein aggregation after transient cerebral ischemia. Neuroscience 2005, 134:1273-1284.
25. Liu Z., Meray R.K., Grammatopoulos T.N., Fredenburg R.A., Cookson M.R., Liu Y., Logan T., Lansbury P.T. Membrane-associated farnesylated UCH-L1 promotes alpha-synuclein neurotoxicity and is a therapeutic target for Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4635-4640.
26. Meller R. The role of the ubiquitin proteasome system in ischemia and ischemic tolerance. Neuroscientist 2009, 15:243-260.
27. Meray R.K., Lansbury P.T. Reversible monoubiquitination regulates the Parkinson disease-associated ubiquitin hydrolase UCH-L1. J. Biol. Chem. 2007, 282:10567-10575.
28. Miller T.M., Donnelly M.K., Crago E.A., Roman D.M., Sherwood P.R., Horowitz M.B., Poloyac S.M. Rapid, simultaneous quantitation of mono and dioxygenated metabolites of arachidonic acid in human CSF and rat brain. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2009, 877:3991-4000.
29. Milne G.L., Musiek E.S., Morrow J.D. The cyclopentenone (A2/J2) isoprostanes-unique, highly reactive products of arachidonate peroxidation. Antioxid. Redox Signal. 2005, 7:210-220.
30. Musiek E.S., Breeding R.S., Milne G.L., Zanoni G., Morrow J.D., McLaughlin B. Cyclopentenone isoprostanes are novel bioactive products of lipid oxidation which enhance neurodegeneration. J. Neurochem. 2006, 97:1301-1313.
31. Nakayama M., Uchimura K., Zhu R.L., Nagayama T., Rose M.E., Stetler R.A., Isakson P.C., Chen J., Graham S.H. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10954-10959.
32. Oddo, S., 2008. The ubiquitin-proteasome system in Alzheimer's disease. In: J Cell Mol Med), 2008/02/13 ed., vol. 12, 363-373.
33. Ogburn K.D., Figueiredo-Pereira M.E. Cytoskeleton/endoplasmic reticulum collapse induced by prostaglandin J2 parallels centrosomal deposition of ubiquitinated protein aggregates. J. Biol. Chem. 2006, 281:23274-23284.
34. Pereira M.P., Hurtado O., Cardenas A., Bosca L., Castillo J., Davalos A., Vivancos J., Serena J., Lorenzo P., Lizasoain I., Moro M.A. Rosiglitazone and 15-deoxy-Delta12, 14-prostaglandin J2 cause potent neuroprotection after experimental stroke through noncompletely overlapping mechanisms. J. Cereb. Blood Flow Metab. 2006, 26:218-229.
35. Pierre S.R., Lemmens M.A., Figueiredo-Pereira M.E. Subchronic infusion of the product of inflammation prostaglandin J2 models sporadic Parkinson's disease in mice. J. Neuroinflammation 2009, 6:18.
36. Renedo M., Gayarre J., Garcia-Dominguez C.A., Perez-Rodriguez A., Prieto A., Canada F.J., Rojas J.M., Perez-Sala D. Modification and activation of Ras proteins by electrophilic prostanoids with different structure are site-selective. Biochemistry 2007, 46:6607-6616.
37. Rohn T.T., Wong S.M., Cotman C.W., Cribbs D.H. 15-Deoxy-delta12, 14-prostaglandin J2, a specific ligand for peroxisome proliferator-activated receptor-gamma, induces neuronal apoptosis. Neuroreport 2001, 12:839-843.
38. Saito S., Takahashi S., Takagaki N., Hirose T., Sakai T. 15-Deoxy-Delta(12, 14)-prostaglandin J2 induces apoptosis through activation of the CHOP gene in HeLa cells. Biochem. Biophys. Res. Commun. 2003, 311:17-23.
39. Sakurai M., Sekiguchi M., Zushida K., Yamada K., Nagamine S., Kabuta T., Wada K. Reduction in memory in passive avoidance learning, exploratory behaviour and synaptic plasticity in mice with a spontaneous deletion in the ubiquitin C-terminal hydrolase L1 gene. Eur. J. Neurosci. 2008, 27:691-701.
40. Sanchez-Gomez F.J., Gayarre J., Avellano M.I., Perez-Sala D. Direct evidence for the covalent modification of glutathione-S-transferase P1-1 by electrophilic prostaglandins: implications for enzyme inactivation and cell survival. Arch. Biochem. Biophys. 2007, 457:150-159.
41. Satoh T., Lipton S.A. Redox regulation of neuronal survival mediated by electrophilic compounds. Trends Neurosci. 2007, 30:37-45.
42. Setsuie R., Wada K. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem. Int. 2007, 51:105-111.
43. Shan Z.Z., Masuko-Hongo K., Dai S.M., Nakamura H., Kato T., Nishioka K. A potential role of 15-deoxy-delta(12, 14)-prostaglandin J2 for induction of human articular chondrocyte apoptosis in arthritis. J. Biol. Chem. 2004, 279:37939-37950.
44. Shibata T., Kondo M., Osawa T., Shibata N., Kobayashi M., Uchida K. 15-Deoxy-delta 12, 14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes. J. Biol. Chem. 2002, 277:10459-10466.
45. Shibata T., Yamada T., Ishii T., Kumazawa S., Nakamura H., Masutani H., Yodoi J., Uchida K. Thioredoxin as a molecular target of cyclopentenone prostaglandins. J. Biol. Chem. 2003, 278:26046-26054.
46. Shibata T., Yamada T., Kondo M., Tanahashi N., Tanaka K., Nakamura H., Masutani H., Yodoi J., Uchida K. An endogenous electrophile that modulates the regulatory mechanism of protein turnover: inhibitory effects of 15-deoxy-Delta 12,14-prostaglandin J2 on proteasome. Biochemistry 2003, 42:13960-13968.
47. Shiraki T., Kamiya N., Shiki S., Kodama T.S., Kakizuka A., Jingami H. alpha, beta-Unsaturated ketone is a core moiety of natural ligands for covalent binding to peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 2005, 280:14145-14153.
48. Stamatakis K., Sanchez-Gomez F.J., Perez-Sala D. Identification of novel protein targets for modification by 15-deoxy-Delta12, 14-prostaglandin J2 in mesangial cells reveals multiple interactions with the cytoskeleton. J. Am. Soc. Nephrol. 2006, 17:89-98.
49. Uchida K., Shibata T. 15-Deoxy-Delta(12, 14)-prostaglandin J2: an electrophilic trigger of cellular responses. Chem. Res. Toxicol. 2008, 21:138-144.
50. Vernace V.A., Schmidt-Glenewinkel T., Figueiredo-Pereira M.E. Aging and regulated protein degradation: who has the UPPer hand?. Aging cell 2007, 6:599-606.
51. Wang Z., Figueiredo-Pereira M.E. Inhibition of sequestosome 1/p62 up-regulation prevents aggregation of ubiquitinated proteins induced by prostaglandin J2 without reducing its neurotoxicity. Mol. Cell. Neurosci. 2005, 29:222-231.
52. Wang Z., Aris V.M., Ogburn K.D., Soteropoulos P., Figueiredo-Pereira M.E. Prostaglandin J2 alters pro-survival and pro-death gene expression patterns and 26S proteasome assembly in human neuroblastoma cells. J. Biol. Chem. 2006, 281:21377-21386.
53. Zhao X., Zhang Y., Strong R., Grotta J.C., Aronowski J. 15d-Prostaglandin J2 activates peroxisome proliferator-activated receptor-gamma, promotes expression of catalase, and reduces inflammation, behavioral dysfunction, and neuronal loss after intracerebral hemorrhage in rats. J. Cereb. Blood Flow Metab. 2006, 26:811-820.