Prostaglandin D2 toxicity in primary neurons is mediated through its bioactive cyclopentenone metabolites

NeuroToxicology

Volumn 39, Issue , 2013, Pages 35-44

  Liu, Hao ^a,b   Li, Wenjin ^a,b   Rose, Marie E ^a,b   Pascoe, Jordan L ^a,b   Miller, Tricia M ^c   Ahmad, Muzamil ^a,b,d   Poloyac, Samuel M ^c   Hickey, Robert W ^b   Graham, Steven H ^a,b  

^a VA Pittsburgh Healthcare System   (United States)

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

^c UNIVERSITY OF PITTSBURGH   (United States)

^d CSIR INDIAN INSTITUTE OF INTEGRATIVE MEDICINE   (India)

Author keywords

Cell death; Cyclopentenone prostaglandins; DP receptors; Primary neuron; Prostaglandin D2; Ubiquitinated protein

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; ACETYLCYSTEINE; ASCORBIC ACID; DELTA12 PROSTAGLANDIN J2; GLUTATHIONE; LIPOCALIN; PROSTAGLANDIN D SYNTHASE; PROSTAGLANDIN D2; PROSTAGLANDIN J2; THIOL GROUP; TOCOPHEROL; UBIQUITINATED PROTEIN; 15 DEOXYPROSTAGLANDIN J2; 15-DEOXYPROSTAGLANDIN J2; 9-DEOXY-DELTA-9-PROSTAGLANDIN D2; CARBAZOLE DERIVATIVE; CYCLOPENTANE DERIVATIVE; CYCLOPENTENONE; DRUG DERIVATIVE; ISOMERASE; PROSTAGLANDIN R2 D ISOMERASE; PROSTAGLANDIN R2 D-ISOMERASE; PROSTAGLANDIN RECEPTOR; RAMATROBAN; SULFONAMIDE;

ANIMAL CELL; ARTICLE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; HYPOXIA; METABOLITE; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; ANIMAL EMBRYO; ANOXIA; APOPTOSIS; BRAIN CORTEX; CELL CULTURE; CYCLOPENTENONE PROSTAGLANDINS; CYTOLOGY; DOSE RESPONSE; DP RECEPTORS; DRUG EFFECT; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PRIMARY NEURON; PROSTAGLANDIN D(2); SPRAGUE DAWLEY RAT;

CELL DEATH; CYCLOPENTENONE PROSTAGLANDINS; DP RECEPTORS; PRIMARY NEURON; PROSTAGLANDIN D(2); UBIQUITINATED PROTEIN;

ANIMALS; ANOXIA; APOPTOSIS; CARBAZOLES; CELLS, CULTURED; CEREBRAL CORTEX; CYCLOPENTANES; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; INTRAMOLECULAR OXIDOREDUCTASES; LIPOCALINS; MICE; MICE, KNOCKOUT; NEURONS; PROSTAGLANDIN D2; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PROSTAGLANDIN; SULFONAMIDES;

EID: 84883660064     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2013.08.001     Document Type: Article

References (45)

1. Abdel-Halim M.S., Lunden I., Cseh G., Anggard E. Prostaglandin profiles in nervous tissue and blood vessels of the brain of various animals. Prostaglandins 1980, 19:249-258.
2. 2 DP1 receptor is beneficial in ischemic stroke and in acute exicitotoxicity in young and old mice. Age (Dordr) 2010, 32:271-282.
3. Auer R.N., Siesjo B.K. Biological differences between ischemia, hypoglycemia, and epilepsy. Ann Neurol 1988, 24:699-707.
4. 2, is metabolized by HepG2 cells via conjugation with glutathione. Chem Res Toxicol 2007, 20:1528-1535.
5. 2-stimulated beta-cell apoptosis is associated with prolonged UPR activation. J Physiol Endocrinol Metab 2007, 292:E1052-E1061.
6. Chen J., Marsh T., Zhang J.S., Graham S.H. Expression of cyclo-oxygenase 2 in rat brain following kainate treatment. Neuroreport 1995, 6:245-248.
7. Chen Y.C., Shen S.C., Tsai S.H. Prostaglandin D(2) and J(2) induce apoptosis in human leukemia cells via activation of the caspase 3 cascade and production of reactive oxygen species. Biochim Biophys Acta 2005, 1743:291-304.
8. Chiu E.K., Richardson J.S. Behavioral and neurochemical aspects of prostaglandins in brain function. Gen Pharmacol 1985, 16:163-175.
9. Crider J.Y., Griffin B.W., Sharif N.A. Prostaglandin DP receptors positively coupled to adenylyl cyclase in embryonic bovine tracheal (EBTr) cells: pharmacological characterization using agonists and antagonists. Br J Pharmacol 1999, 127:204-210.
10. Dringen R., Gutterer J.M., Hirrlinger J. Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur J Biochem 2000, 267:4912-4916.
11. Hatanaka M., Shibata N., Shintani N., Haba R., Hayata A., Hashimoto H., et al. 15d-Prostaglandin J2 enhancement of nerve growth factor-induced neurite outgrowth is blocked by the chemoattractant receptor-homologous molecule expressed on T-helper type 2 cells (CRTH2) antagonist CAY10471 in PC12 cells. J Pharmacol Sci 2010, 113:89-93.
12. Higdon A., Diers A.R., Oh J.Y., Landar A., Darley-Usmar V.M. Cell signalling by reactive lipid species: new concepts and molecular mechanisms. Biochem J 2012, 442:453-464.
13. 2 in microglia contributes to neuropathic pain via DP2 receptor in spinal neurons. Glia 2013, 61:943-956.
14. Katsura K., Rodriguez de Turco E.B., Folbergrova J., Bazan N.G., Siesjo B.K. Coupling among energy failure, loss of ion homeostasis, and phospholipase A2 and C activation during ischemia. J Neurochem 1993, 61:1677-1684.
15. Kondo M., Shibata T., Kumagai T., Osawa T., Shibata N., Kobayashi M., et al. 15-Deoxy-Delta(12,14)-prostaglandin J(2): the endogenous electrophile that induces neuronal apoptosis. Proc Natl Acad Sci USA 2002, 99:7367-7372.
16. 2-independent effects. J Biol Chem 2012, 287:9414-9428.
17. 2 alpha exacerbate hypoxic neuronal injury in neuron-enriched primary culture. Neurochem Res 2008, 33:490-499.
18. Li Z., Jansen M., Pierre S.R., Figueiredo-Pereira M.E. Neurodegeneration: linking ubiquitin/proteasome pathway impairment with inflammation. Int J Biochem Cell Biol 2003, 35:547-552.
19. Li Z., Melandri F., Berdo I., Jansen M., Hunter L., Wright S., et al. 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.
20. 2 mediates neuronal protection via the DP1 receptor. J Neurochem 2005, 92:477-486.
21. Liu H., Li W., Ahmad M., Miller T.M., Rose M.E., Poloyac S.M., et al. Modification of ubiquitin-C-terminal hydrolase-L1 by cyclopentenone prostaglandins exacerbates hypoxic injury. Neurobiol Dis 2011, 41:318-328.
22. Liu H., Li W., Ahmad M., Rose M.E., Miller T.M., Yu M., et al. Increased generation of cyclopentenone prostaglandins after brain ischemia and their role in aggregation of ubiquitinated proteins in neurons. Neurotox Res 2013, 24:191-204.
23. Matsuoka T., Narumiya S. Prostaglandin receptor signaling in disease. ScientificWorldJournal 2007, 7:1329-1347.
24. Miller T.M., Donnelly M.K., Crago E.A., Roman D.M., Sherwood P.R., Horowitz M.B., et al. Rapid, simultaneous quantitation of mono and dioxygenated metabolites of arachidonic acid in human CSF and rat brain. J Chromatogr B: Analyt Technol Biomed Life Sci 2009, 877:3991-4000.
25. 2-mediated microglia/astrocyte interaction enhances astrogliosis and demyelination in twitcher. J Neurosci 2006, 26:4383-4393.
26. Nakayama M., Uchimura K., Zhu R.L., Nagayama T., Rose M.E., Stetler R.A., et al. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc Natl Acad Sci USA 1998, 95:10954-10959.
27. Nogawa S., Zhang F., Ross M.E., Iadecola C. Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J Neurosci 1997, 17:2746-2755.
28. 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.
29. Saleem S., Zhuang H., de Brum-Fernandes A.J., Maruyama T., Narumiya S., Dore S. PGD(2) DP1 receptor protects brain from ischemia-reperfusion injury. Eur J Neurosci 2007, 26:73-78.
30. 2 metabolite generated during inflammatory processes. J Biol Chem 2002, 277:10459-10466.
31. 2 in macrophages. Exp Cell Res 2010, 316:3140-3149.
32. Takei S., Hasegawa-Ishii S., Uekawa A., Chiba Y., Umegaki H., Hosokawa M., et al. Immunohistochemical demonstration of increased prostaglandin F(2)alpha levels in the rat hippocampus following kainic acid-induced seizures. Neuroscience 2012, 218:295-304.
33. 2 protects neonatal mouse brain from hypoxic ischemic injury. J Neurosci 2007, 27:4303-4312.
34. Traber M.G., Stevens J.F. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med 2011, 51:1000-1013.
35. Urade Y., Hayaishi O. Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase. Biochim Biophys Acta 2000, 1482:259-271.
36. Urade Y., Kitahama K., Ohishi H., Kaneko T., Mizuno N., Hayaishi O. Dominant expression of mRNA for prostaglandin D synthase in leptomeninges, choroid plexus, and oligodendrocytes of the adult rat brain. Proc Natl Acad Sci USA 1993, 90:9070-9074.
37. 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 26 S proteasome assembly in human neuroblastoma cells. J Biol Chem 2006, 281:21377-21386.
38. 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.
39. 2 is suggested by distribution studies of the rat DP prostanoid receptor. Eur J Pharmacol 1999, 377:101-115.
40. Wu L., Wang Q., Liang X., Andreasson K. Divergent effects of prostaglandin receptor signaling on neuronal survival. Neurosci Lett 2007, 421:253-258.
41. 2 induces apoptosis of mouse oligodendrocyte precursor cells. J Neuroinflammation 2007, 4:18.
42. Yagami T., Ueda K., Asakura K., Sakaeda T., Kuroda T., Hata S., et al. Effects of S-2474, a novel nonsteroidal anti-inflammatory drug, on amyloid beta protein-induced neuronal cell death. Br J Pharmacol 2001, 134:673-681.
43. Yagami T., Ueda K., Asakura K., Takasu N., Sakaeda T., Itoh N., et al. Novel binding sites of 15-deoxy-Delta12,14-prostaglandin J2 in plasma membranes from primary rat cortical neurons. Exp Cell Res 2003, 291:212-227.
44. Yamamoto Y., Takase K., Kishino J., Fujita M., Okamura N., Sakaeda T., et al. Proteomic identification of protein targets for 15-deoxy-Delta(12,14)-prostaglandin J2 in neuronal plasma membrane. PLoS ONE 2011, 6:e17552.
45. Zhu F., Wang P., Kontrogianni-Konstantopoulos A., Konstantopoulos K. Prostaglandin (PG)D(2) and 15-deoxy-Delta(12,14)-PGJ(2), but not PGE(2), mediate shear-induced chondrocyte apoptosis via protein kinase A-dependent regulation of polo-like kinases. Cell Death Differ 2010, 17:1325-1334.