Prostaglandin e 2 type 1 receptors contribute to neuronal apoptosis after transient forebrain ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 8, 2013, Pages 1207-1214

  Shimamura, Munehisa ^a   Zhou, Ping ^a   Casolla, Barbara ^a   Qian, Liping ^a   Capone, Carmen ^a   Kurinami, Hitomi ^a   Iadecola, Costantino ^a   Anrather, Josef ^a  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

Author keywords

AKT; apoptosis; calcineurin; cerebral ischemia; cyclooxygenase; prostaglandin E2

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; NEUROPROTECTIVE AGENT; PROSTAGLANDIN E RECEPTOR 1; SC 51089; UNCLASSIFIED DRUG; CALCINEURIN; HYDRAZINE DERIVATIVE; ONCOPROTEIN; OXAZEPINE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; PTGER1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CAROTID ARTERY OBSTRUCTION; CELL SURVIVAL; COMMON CAROTID ARTERY OCCLUSION; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPAL CA1 REGION; MALE; MOUSE; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; ANIMAL; APOPTOSIS; C57BL MOUSE; DRUG ANTAGONISM; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVE CELL; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSIENT ISCHEMIC ATTACK; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BLOTTING, WESTERN; CA1 REGION, HIPPOCAMPAL; CALCINEURIN; CASPASE 3; DINOPROSTONE; HYDRAZINES; IMMUNOHISTOCHEMISTRY; ISCHEMIC ATTACK, TRANSIENT; MICE; MICE, INBRED C57BL; NEURONS; ONCOGENE PROTEIN V-AKT; OXAZEPINES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE;

EID: 84881134135     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.69     Document Type: Article

References (44)

1. Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA et al. Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 2006; 12: 225-229.
2. Cimino PJ, Keene CD, Breyer RM, Montine KS, Montine TJ. Therapeutic targets in prostaglandin E2 signaling for neurologic disease. Curr Med Chem 2008; 15: 1863-1869.
3. Abe T, Kunz A, Shimamura M, Zhou P, Anrather J, Iadecola C. The neuroprotective effect of prostaglandin E2 EP1 receptor inhibition has a wide therapeutic window, is sustained in time and is not sexually dimorphic. J Cereb Blood Flow Metab 2009; 29: 66-72.
4. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010; 67: 181-198.
5. Watabe A, Sugimoto Y, Honda A, Irie A, Namba T, Negishi M et al. Cloning and expression of cDNA for a mouse EP1 subtype of prostaglandin E receptor. J Biol Chem 1993; 268: 20175-20178.
6. Asboth G, Phaneuf S, Europe-Finner GN, Toth M, Bernal AL. Prostaglandin E2 activates phospholipase C and elevates intracellular calcium in cultured myometrial cells: involvement of EP1 and EP3 receptor subtypes. Endocrinology 1996; 137: 2572-2579.
7. Katoh H, Watabe A, Sugimoto Y, Ichikawa A, Negishi M. Characterization of the signal transduction of prostaglandin E receptor EP1 subtype in cDNA-transfected Chinese hamster ovary cells. Biochim Biophys Acta 1995; 1244: 41-48.
8. Zhou P, Qian L, Chou T, Iadecola C. Neuroprotection by PGE2 receptor EP1 inhibition involves the PTEN/AKT pathway. Neurobiol Dis 2008; 29: 543-551.
9. Park CH, Kim YS, Kim YH, Choi MY, Yoo JM, Kang SS et al. Calcineurin mediates AKT dephosphorylation in the ischemic rat retina. Brain Res 2008; 1234: 148-157.
10. Berry K, Wisniewski HM, Svarzbein L, Baez S. On the relationship of brain vasculature to production of neurological deficit and morphological changes following acute unilateral common carotid artery ligation in gerbils. J Neurol Sci 1975; 25: 75-92.
11. Kitagawa K, Matsumoto M, Yang G, Mabuchi T, Yagita Y, Hori M et al. Cerebral ischemia after bilateral carotid artery occlusion and intraluminal suture occlusion in mice: evaluation of the patency of the posterior communicating artery. J Cereb Blood Flow Metab 1998; 18: 570-579.
12. Murakami K, Kondo T, Kawase M, Chan PH. The development of a new mouse model of global ischemia: focus on the relationships between ischemia duration, anesthesia, cerebral vasculature, and neuronal injury following global ischemia in mice. Brain Res 1998; 780: 304-310.
13. Nagayama M, Niwa K, Nagayama T, Ross ME, Iadecola C. The cyclooxygenase-2 inhibitor NS-398 ameliorates ischemic brain injury in wild-type mice but not in mice with deletion of the inducible nitric oxide synthase gene. J Cereb Blood Flow Metab 1999; 19: 1213-1219.
14. Anrather J, Gallo EF, Kawano T, Orio M, Abe T, Gooden C et al. Purinergic signaling induces cyclooxygenase-1-dependent prostanoid synthesis in microglia: roles in the outcome of excitotoxic brain injury. PLoS One 2011; 6: e25916.
15. Koike K, Hashimoto K, Fukami G, Okamura N, Zhang L, Ohgake S et al. The immunophilin ligand FK506 protects against methamphetamine-induced dopaminergic neurotoxicity in mouse striatum. Neuropharmacology 2005; 48: 391-397.
16. Marmarou CR, Povlishock JT. Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp Neurol 2006; 197: 353-362.
17. Olive MF, McGeehan AJ, Kinder JR, McMahon T, Hodge CW, Janak PH et al. The mGluR5 antagonist 6-methyl-2-(phenylethynyl)pyridine decreases ethanol consumption via a protein kinase C epsilon-dependent mechanism. Mol Pharmacol 2005; 67: 349-355.
18. Zhou P, Qian L, Iadecola C. Nitric oxide inhibits caspase activation and apoptotic morphology but does not rescue neuronal death. J Cereb Blood Flow Metab 2005; 25: 348-357.
19. Lee SR, Lok J, Rosell A, Kim HY, Murata Y, Atochin D et al. Reduction of hippocampal cell death and proteolytic responses in tissue plasminogen activator knockout mice after transient global cerebral ischemia. Neuroscience 2007; 150: 50-57.
20. Candelario-Jalil E, Gonzalez-Falcon A, Garcia-Cabrera M, Alvarez D, Al-Dalain S, Martinez G et al. Assessment of the relative contribution of COX-1 and COX-2 isoforms to ischemia-induced oxidative damage and neurodegeneration following transient global cerebral ischemia. J Neurochem 2003; 86: 545-555.
21. Zhen G, Dore S. Optimized protocol to reduce variable outcomes for the bilateral common carotid artery occlusion model in mice. J Neurosci Methods 2007; 166: 73-80.
22. Kirino T. Delayed neuronal death. Neuropathology 2000; 20(Suppl): S95-S97.
23. Graham SH, Chen J. Programmed cell death in cerebral ischemia. J Cereb Blood Flow Metab 2001; 21: 99-109.
24. Eldadah BA, Faden AI. Caspase pathways, neuronal apoptosis, and CNS injury. J Neurotrauma 2000; 17: 811-829.
25. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
26. Krantic S, Mechawar N, Reix S, Quirion R. Apoptosis-inducing factor: a matter of neuron life and death. Prog Neurobiol 2007; 81: 179-196.
27. Cao G, Xing J, Xiao X, Liou AK, Gao Y, Yin XM et al. Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J Neurosci 2007; 27: 9278-9293.
28. Mullonkal CJ, Toledo-Pereyra LH. Akt in ischemia and reperfusion. J Invest Surg 2007; 20: 195-203.
29. Kim NH, Kim K, Park WS, Son HS, Bae Y. PKB/Akt inhibits ceramide-induced apoptosis in neuroblastoma cells by blocking apoptosis-inducing factor (AIF) translocation. J Cell Biochem 2007; 102: 1160-1170.
30. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994; 269: 5241-5248.
31. Meier R, Alessi DR, Cron P, Andjelkovic M, Hemmings BA. Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bbeta. J Biol Chem 1997; 272: 30491-30497.
32. Macleod MR, O'Collins T, Horky LL, Howells DW, Donnan GA. Systematic review and metaanalysis of the efficacy of FK506 in experimental stroke. J Cereb Blood Flow Metab 2005; 25: 713-721.
33. Nakayama M, Uchimura K, Zhu RL, Nagayama T, Rose ME, Stetler RA et al. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc Natl Acad Sci USA 1998; 95: 10954-10959.
34. Sasaki T, Kitagawa K, Yamagata K, Takemiya T, Tanaka S, Omura-Matsuoka E et al. Amelioration of hippocampal neuronal damage after transient forebrain ischemia in cyclooxygenase-2-deficient mice. J Cereb Blood Flow Metab 2004; 24: 107-113.
35. Stevens MK, Yaksh TL. Time course of release in vivo of PGE2, PGF2 alpha, 6-keto-PGF1 alpha, and TxB2 into the brain extracellular space after 15minutes of complete global ischemia in the presence and absence of cyclooxygenase inhibition. J Cereb Blood Flow Metab 1988; 8: 790-798.
36. Smith CJ, Zhang Y, Koboldt CM, Muhammad J, Zweifel BS, Shaffer A et al. Pharmacological analysis of cyclooxygenase-1 in inflammation. Proc Natl Acad Sci USA 1998; 95: 13313-13318.
37. Johnson JL, Wimsatt J, Buckel SD, Dyer RD, Maddipati KR. Purification and characterization of prostaglandin H synthase-2 from sheep placental cotyledons. Arch Biochem Biophys 1995; 324: 26-34.
38. Iadecola C, Sugimoto K, Niwa K, Kazama K, Ross ME. Increased susceptibility to ischemic brain injury in cyclooxygenase-1-deficient mice. J Cereb Blood Flow Metab 2001; 21: 1436-1441.
39. Ahmad AS, Saleem S, Ahmad M, Dore S. Prostaglandin EP1 receptor contributes to excitotoxicity and focal ischemic brain damage. Toxicol Sci 2006; 89: 265-270.
40. Zhen G, Kim YT, Li RC, Yocum J, Kapoor N, Langer J et al. PGE2 EP1 receptor exacerbated neurotoxicity in a mouse model of cerebral ischemia and Alzheimer's disease. Neurobiol Aging 2012; 33: 2215-2219.
41. Zhang HM, Rao JN, Guo X, Liu L, Zou T, Turner DJ et al. Akt kinase activation blocks apoptosis in intestinal epithelial cells by inhibiting caspase-3 after polyamine depletion. J Biol Chem 2004; 279: 22539-22547.
42. Graef IA, Mermelstein PG, Stankunas K, Neilson JR, Deisseroth K, Tsien RW et al. L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 1999; 401: 703-708.
43. Hara MR, Snyder SH. Cell signaling and neuronal death. Annu Rev Pharmacol Toxicol 2007; 47: 117-141.
44. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F et al. Ca2\+induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999; 284: 339-343.