Role of PGE2 EP1 receptor in intracerebral hemorrhage-induced brain injury

Neurotoxicity Research

Volumn 24, Issue 4, 2013, Pages 549-559

  Singh, Nilendra ^a   Ma, Bo ^b   Leonardo, Christopher Charles ^a   Ahmad, Abdullah Shafique ^a   Narumiya, Shuh ^c   Doré, Sylvain ^a,d  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

Collagenase; Hematoma; Microglia; Neurodegeneration; Prostaglandin

Indexed keywords

COLLAGENASE; PROSTAGLANDIN E RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HEMORRHAGE; BRAIN INJURY; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE EXACERBATION; FUNCTIONAL ASSESSMENT; IMMUNOREACTIVITY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MICROGLIA; MOLECULAR MECHANICS; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; STAINING; WILD TYPE;

MUS;

ANIMALS; BRAIN INJURIES; CELL DEATH; CEREBRAL HEMORRHAGE; CORPUS STRIATUM; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; PHAGOCYTOSIS; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE;

EID: 84885419622     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-013-9410-7     Document Type: Article

References (62)

1. Abe T, Kunz A, Shimamura M, Zhou P, Anrather J, Iadecola C (2009) 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 29(1):66-72. doi: 10.1038/jcbfm.2008.88
2. Abe S, Watabe H, Takaseki S, Aihara M, Yoshitomi T (2013) The effects of prostaglandin analogues on intracellular Ca2 + in ciliary arteries of wild-type and prostanoid receptor-deficient mice. J Ocul Pharmacol Ther 29(1):55-60. doi: 10.1089/jop.2011.0197
3. Ahmad AS, Saleem S, Ahmad M, Doré S (2006) Prostaglandin EP1 receptor contributes to excitotoxicity and focal ischemic brain damage. Toxicol Sci 89(1):265-270. doi: 10.1093/toxsci/kfj022
4. Ahmad AS, Yun YT, Ahmad M, Maruyama T, Doré S (2008) Selective blockade of PGE2 EP1 receptor protects brain against experimental ischemia and excitotoxicity, and hippocampal slice cultures against oxygen-glucose deprivation. Neurotox Res 14(4):343-351
5. Ahmad AS, Maruyama T, Narumiya S, Doré S (2013) PGE2 EP1 receptor deletion attenuates 6-OHDA-induced parkinsonism in mice: old switch. New Target Neurotox Res 23(3):260-266. doi: 10.1007/s12640-013-9381-8
6. Aronowski J, Hall CE (2005) New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol Res 27(3):268-279. doi: 10.1179/016164105X25225
7. Aronowski J, Zhao X (2011) Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke 42(6):1781-1786. doi: 10.1161/STROKEAHA.110.596718
8. Broderick JP, Adams HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski JM, Zuccarello M (1999) Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for healthcare professionals from a special writing group of the stroke council. Am Heart Assoc Stroke 30(4):905-915
9. Carlson NG, Rojas MA, Black JD, Redd JW, Hille J, Hill KE, Rose JW (2009) Microglial inhibition of neuroprotection by antagonists of the EP1 prostaglandin E2 receptor. J Neuroinflammation 6:5. doi: 10.1186/1742-2094-6-5
10. Chen L, Zhang X, Chen-Roetling J, Regan RF (2011) Increased striatal injury and behavioral deficits after intracerebral hemorrhage in hemopexin knockout mice. J Neurosurg 114(4):1159-1167. doi: 10.3171/2010.10.JNS10861
11. Choi JS, Kim HY, Chun MH, Chung JW, Lee MY (2006) Expression of prostaglandin E2 receptor subtypes, EP2 and EP4, in the rat hippocampus after cerebral ischemia and ischemic tolerance. Cell Tissue Res 324(2):203-211. doi: 10.1007/s00441-005-0121-0
12. Chu K, Jeong SW, Jung KH, Han SY, Lee ST, Kim M, Roh JK (2004) Celecoxib induces functional recovery after intracerebral hemorrhage with reduction of brain edema and perihematomal cell death. J Cereb Blood Flow Metab 24(8):926-933. doi: 10.1097/01.WCB.0000130866.25040.7D
13. Cimino PJ, Keene CD, Breyer RM, Montine KS, Montine TJ (2008) Therapeutic targets in prostaglandin E2 signaling for neurologic disease. Curr Med Chem 15(19):1863-1869
14. Clark W, Gunion-Rinker L, Lessov N, Hazel K (1998) Citicoline treatment for experimental intracerebral hemorrhage in mice. Stroke 29(10):2136-2140
15. Davis SM, Donnan GA (2006) The stroke-prone state: rapid assessment of transient ischemic attacks. Stroke 37(4):1140. doi: 01.STR.0000209245.05915.df
16. Doré S, Otsuka T, Mito T, Sugo N, Hand T, Wu L, Hurn PD, Traystman RJ, Andreasson K (2003) Neuronal overexpression of cyclooxygenase-2 increases cerebral infarction. Ann Neurol 54(2):155-162. doi: 10.1002/ana.10612
17. Dunham NW, Miya TS (1957) A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharm Assoc Am Pharm Assoc (Baltim) 46(3):208-209
18. Funk CD, Furci L, FitzGerald GA, Grygorczyk R, Rochette C, Bayne MA, Abramovitz M, Adam M, Metters KM (1993) Cloning and expression of a cDNA for the human prostaglandin E receptor EP1 subtype. J Biol Chem 268(35):26767-26772
19. Giulian D, Chen J, Ingeman JE, George JK, Noponen M (1989) The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J Neurosci 9(12):4416-4429
20. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB (2013) Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127(1):e6-e245. doi: 10.1161/CIR.0b013e31828124ad
21. Gu Y, Hua Y, Keep RF, Morgenstern LB, Xi G (2009) Deferoxamine reduces intracerebral hematoma-induced iron accumulation and neuronal death in piglets. Stroke 40(6):2241-2243. doi: 10.1161/STROKEAHA.108.539536
22. Hebert RL, Jacobson HR, Breyer MD (1990) PGE2 inhibits AVP-induced water flow in cortical collecting ducts by protein kinase C activation. Am J Physiol 259(2 Pt 2):F318-F325
23. Hoffmann PR, Kench JA, Vondracek A, Kruk E, Daleke DL, Jordan M, Marrack P, Henson PM, Fadok VA (2005) Interaction between phosphatidylserine and the phosphatidylserine receptor inhibits immune responses in vivo. J Immunol 174(3):1393-1404. doi: 174/3/1393
24. Huynh ML, Fadok VA, Henson PM (2002) Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest 109(1):41-50. doi: 10.1172/JCI11638
25. Ito D, Tanaka K, Suzuki S, Dembo T, Fukuuchi Y (2001) Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32(5):1208-1215
26. James ML, Wang H, Venkatraman T, Song P, Lascola CD, Laskowitz DT (2010) Brain natriuretic peptide improves long-term functional recovery after acute CNS injury in mice. J Neurotrauma 27(1):217-228. doi: 10.1089/neu.2009.1022
27. Jones BJ, Roberts DJ (1968) The quantitative measurement of motor inco-ordination in naive mice using an accelerating rotarod. J Pharm Pharmacol 20(4):302-304
28. Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA, Kunz A, Cho S, Orio M, Iadecola C (2006) Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 12(2):225-229. doi: nm1362
29. Keep RF, Xi G, Hua Y, Hoff JT (2005) The deleterious or beneficial effects of different agents in intracerebral hemorrhage: think big, think small, or is hematoma size important? Stroke 36(7):1594-1596. doi: 01.STR.0000170701.41507.e1
30. Keep RF, Hua Y, Xi G (2012) Intracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol 11(8):720-731. doi: 10.1016/S1474-4422(12)70104-7
31. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, Joshi BV, Jacobson KA, Kohsaka S, Inoue K (2007) UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446(7139):1091-1095. doi: nature05704
32. Komotar RJ, Kim GH, Sughrue ME, Otten ML, Rynkowski MA, Kellner CP, Hahn DK, Merkow MB, Garrett MC, Starke RM, Connolly ES (2007) Neurologic assessment of somatosensory dysfunction following an experimental rodent model of cerebral ischemia. Nat Protoc 2(10):2345-2347. doi: nprot.2007.359
33. MacLellan CL, Silasi G, Poon CC, Edmundson CL, Buist R, Peeling J, Colbourne F (2008) Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J Cereb Blood Flow Metab 28(3):516-525. doi: 9600548
34. Matsushita K, Meng W, Wang X, Asahi M, Asahi K, Moskowitz MA, Lo EH (2000) Evidence for apoptosis after intercerebral hemorrhage in rat striatum. J Cereb Blood Flow Metab 20(2):396-404. doi: 10.1097/00004647-200002000-00022
35. Nguyen VT, Benveniste EN (2002) Critical role of tumor necrosis factor-alpha and NF-kappa B in interferon-gamma -induced CD40 expression in microglia/macrophages. J Biol Chem 277(16):13796-13803. doi: 10.1074/jbc.M111906200
36. Phillis JW, Horrocks LA, Farooqui AA (2006) Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders. Brain Res Rev 52(2):201-243. doi: S0165-0173(06)00011-7
37. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF (2001) Spontaneous intracerebral hemorrhage. N Engl J Med 344(19):1450-1460. doi: 10.1056/NEJM200105103441907
38. Regan RF, Panter SS (1993) Neurotoxicity of hemoglobin in cortical cell culture. Neurosci Lett 153(2):219-222
39. Ribo M, Grotta JC (2006) Latest advances in intracerebral hemorrhage. Curr Neurol Neurosci Rep 6(1):17-22
40. Saleem S, Li RC, Wei G, Doré S (2007) Effects of EP1 receptor on cerebral blood flow in the middle cerebral artery occlusion model of stroke in mice. J Neurosci Res 85(11):2433-2440. doi: 10.1002/jnr.21399
41. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39(5):777-787. doi: S0028390800000058
42. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874(2):123-130. doi: S0006-8993(00)02513-0
43. Shah ZA, Nada SE, Dore S (2011) Heme oxygenase 1, beneficial role in permanent ischemic stroke and in Gingko biloba (EGb 761) neuroprotection. Neuroscience 180:248-255. doi: 10.1016/j.neuroscience.2011.02.031
44. Simmer JP, Hu Y, Lertlam R, Yamakoshi Y, Hu JC (2009) Hypomaturation enamel defects in Klk4 knockout/LacZ knockin mice. J Biol Chem 284(28):19110-19121. doi: 10.1074/jbc.M109.013623
45. Smirkin A, Matsumoto H, Takahashi H, Inoue A, Tagawa M, Ohue S, Watanabe H, Yano H, Kumon Y, Ohnishi T, Tanaka J (2010) Iba1(+)/NG2(+) macrophage-like cells expressing a variety of neuroprotective factors ameliorate ischemic damage of the brain. J Cereb Blood Flow Metab 30(3):603-615. doi: 10.1038/jcbfm.2009. 233
46. Takahashi K, Rochford CD, Neumann H (2005) Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201(4):647-657. doi: jem.20041611
47. Takahashi K, Prinz M, Stagi M, Chechneva O, Neumann H (2007) TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. PLoS Med 4(4):e124. doi: 06-PLME-RA-0690R2
48. Tang ZP, Xie XW, Shi YH, Liu N, Zhu SQ, Li ZW, Chen Y (2010) Combined transplantation of neural stem cells and olfactory ensheathing cells improves the motor function of rats with intracerebral hemorrhage. Biomed Environ Sci 23(1):62-67
49. Tikka TM, Koistinaho JE (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 166(12):7527-7533
50. Wang J, Doré S (2007a) Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 130(Pt 6):1643-1652. doi: 130/6/1643
51. Wang J, Doré S (2007b) Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab 27(5):894-908. doi: 9600403
52. Wang J, Zhuang H, Doré S (2006) Heme oxygenase 2 is neuroprotective against intracerebral hemorrhage. Neurobiol Dis 22(3):473-476. doi: S0969-9961(05)00343-8
53. Wang J, Fields J, Zhao C, Langer J, Thimmulappa RK, Kensler TW, Yamamoto M, Biswal S, Doré S (2007) Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic Biol Med 43(3):408-414. doi: S0891-5849(07)00287-0
54. Wasserman JK, Schlichter LC (2007) Neuron death and inflammation in a rat model of intracerebral hemorrhage: effects of delayed minocycline treatment. Brain Res 1136(1):208-218. doi: S0006-8993(06)03576-1
55. Watabe A, Sugimoto Y, Honda A, Irie A, Namba T, Negishi M, Ito S, Narumiya S, Ichikawa A (1993) Cloning and expression of cDNA for a mouse EP1 subtype of prostaglandin E receptor. J Biol Chem 268(27):20175-20178
56. Wu G, Xi G, Huang F (2006) Spontaneous intracerebral hemorrhage in humans: hematoma enlargement, clot lysis, and brain edema. Acta Neurochir Suppl 96:78-80
57. Xue M, Del Bigio MR (2000) Intracerebral injection of autologous whole blood in rats: time course of inflammation and cell death. Neurosci Lett 283(3):230-232. doi: S030439400000971X
58. Yang SX, Wang YR, Qian C, He C (2008) Neuron regeneration in aged rats after intracerebral hemorrhage. Zhejiang Da Xue Xue Bao Yi Xue Ban 37(4):386-392
59. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A 96(23):13496-13500
60. Zhao X, Sun G, Zhang J, Strong R, Song W, Gonzales N, Grotta JC, Aronowski J (2007) Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann Neurol 61(4):352-362. doi: 10.1002/ana.21097
61. Zhao X, Grotta J, Gonzales N, Aronowski J (2009) Hematoma resolution as a therapeutic target: the role of microglia/macrophages. Stroke 40(3 Suppl):S92-S94. doi: 10.1161/STROKEAHA.108.533158
62. Zhou P, Qian L, Chou T, Iadecola C (2008) Neuroprotection by PGE2 receptor EP1 inhibition involves the PTEN/AKT pathway. Neurobiol Dis 29(3):543-551. doi: 10.1016/j.nbd.2007.11.010