Prostaglandin E2 EP2 receptor deletion attenuates intracerebral hemorrhage-induced brain injury and improves functional recovery

ASN Neuro

Volumn 7, Issue 2, 2015, Pages

  Leclerc, Jenna L ^a   Lampert, Andrew S ^a   Diller, Matthew A ^a   Immergluck, Joshua B ^a   Doré, Sylvain ^a,b  

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

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Collagenase; Gliosis; Iron; Neuroinflammation; Neuroprotection; Stroke

Indexed keywords

HEMOGLOBIN; PROSTAGLANDIN E RECEPTOR 2; IRON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BLOOD BRAIN BARRIER; BRAIN HEMORRHAGE; BRAIN INJURY; COGNITION; CONTROLLED STUDY; GENE SILENCING; GLIOSIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IRON METABOLISM; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; COMPLICATION; CONVALESCENCE; DEFICIENCY; DISEASE MODEL; GENETICS; IMMUNOMODULATION; KNOCKOUT MOUSE; METABOLISM; MICROGLIA; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; GLIOSIS; IRON; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NEUROIMMUNOMODULATION; NEUTROPHIL INFILTRATION; RECEPTORS, PROSTAGLANDIN E, EP2 SUBTYPE; RECOVERY OF FUNCTION;

EID: 84976242338     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1177/1759091415578713     Document Type: Article

References (50)

1. Ahmad, A. S., Saleem, S., Ahmad, M., & Doré, S. (2006a). Prostaglandin EP1 receptor contributes to excitotoxicity and focal ischemic brain damage. Toxicological Sciences, 89, 265-270.
2. Ahmad, A. S., Zhuang, H., Echeverria, V., & Doré, S. (2006b). Stimulation of prostaglandin EP2 receptors prevents NMDAinduced excitotoxicity. Journal of Neurotrauma, 23, 1895-1903.
3. Ahmad, M., Saleem, S., Shah, Z., Maruyama, T., Narumiya, S., Doré, S. (2010). The PGE2 EP2 receptor and its selective activation are beneficial against ischemic stroke. Experimental & Translational Stroke Medicine, 2, 12.
4. Aronowski, J., & Zhao, X. (2011). Molecular pathophysiology of cerebral hemorrhage: Secondary brain injury. Stroke, 42, 1781-1786.
5. Bhattathiri, P. S., Gregson, B., Prasad, K. S., Mendelow, A. D., & STICH Investigators. (2006). Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: Results from the STICH trial. Acta Neurochirurgica Supplement, 96, 65-68.
6. Blamire, A. M., Anthony, D. C., Rajagopalan, B., Sibson, N. R., Perry, V. H., Styles, P. (2000). Interleukin-1 beta-induced changes in blood-brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: A magnetic resonance study. The Journal of Neuroscience, 20, 8153-8159.
7. Bos, J. L. (2006). Epac proteins: Multi-purpose cAMP targets. Trends in Biochemical Sciences, 31, 680-686.
8. Candelario-Jalil, E., Slawik, H., Ridelis, I., Waschbisch, A., Akundi, R. S., Hull, M., … Fiebich, B. L. (2005). Regional distribution of the prostaglandin E2 receptor EP1 in the rat brain: Accumulation in Purkinje cells of the cerebellum. Journal of Molecular Neuroscience, 27, 303-310.
9. Chen, L., Zhang, X., Chen-Roetling, J., & Regan, R. F. (2011). Increased striatal injury and behavioral deficits after intracerebral hemorrhage in hemopexin knockout mice. Journal of Neurosurgery, 114, 1159-1167.
10. Chen, M., & Regan, R. F. (2007). Time course of increased heme oxygenase activity and expression after experimental intracerebral hemorrhage: Correlation with oxidative injury. Journal of Neurochemistry, 103, 2015-2021.
11. Crandall, K. M., Rost, N. S., & Sheth, K. N. (2011). Prognosis in intracerebral hemorrhage. Reviews in Neurological Diseases, 8, 23-29.
12. Echeverria, V., Clerman, A., & Doré, S. (2005). Stimulation of PGE2 receptors EP2 and EP4 protects cultured neurons against oxidative stress and cell death following b-amyloid exposure. The European Journal of Neuroscience, 22, 2199-2206.
13. Furuyashiki, T., & Narumiya, S. (2011). Stress responses: The contribution of prostaglandin E(2) and its receptors. Nature Reviews Endocrinology, 7, 163-175.
14. Glushakov, A. V., Robbins, S. W., Bracy, C. L., Narumiya, S., & Doré, S. (2013). Prostaglandin F2alpha FP receptor antagonist improves outcomes after experimental traumatic brain injury. Journal of Neuroinflammation, 10, 132.
15. Gonzalez-Perez, A., Gaist, D., Wallander, M. A., McFeat, G., & Garcia-Rodriguez, L. A. (2013). Mortality after hemorrhagic stroke: Data from general practice (The Health Improvement Network). Neurology, 81, 559-565.
16. Hara, S., Kobayashi, M., Kuriiwa, F., Mukai, T., & Mizukami, H. (2012). Dual contradictory roles of cAMP signaling pathways in hydroxyl radical production in the rat striatum. Free Radical Biology Medicine, 52, 1086-1092.
17. Hizaki, H., Segi, E., Sugimoto, Y., Hirose, M., Saji, T., Ushikubi, F., … Ichikawa, A. (1999). Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proceedings of the National Academy of Sciences of the United States of America, 96, 10501-10506.
18. Jiang, J., & Dingledine, R. (2013). Prostaglandin receptor EP2 in the crosshairs of anti-inflammation, anti-cancer, and neuroprotection. Trends in Pharmacological Sciences, 34, 413-423.
19. Jiang, J., Ganesh, T., Du, Y., Quan, Y., Serrano, G., Qui, M., … Dingledine, R. (2012). Small molecule antagonist reveals seizure-induced mediation of neuronal injury by prostaglandin E2 receptor subtype EP2. Proceedings of the National Academy of Sciences of the United States of America, 109, 3149-3154.
20. Jiang, J., Quan, Y., Ganesh, T., Pouliot, W. A., Dudek, F. E., Dingledine, R. (2013). Inhibition of the prostaglandin receptor EP2 following status epilepticus reduces delayed mortality and brain inflammation. Proceedings of the National Academy of Sciences of the United States of America, 110, 3591-3596.
21. Jin, J., Shie, F. S., Liu, J., Wang, Y., Davis, J., Schantz, A. M., … Zhang, J. (2007). Prostaglandin E2 receptor subtype 2 (EP2) regulates microglial activation and associated neurotoxicity induced by aggregated alpha-synuclein. Journal of Neuroinflammation, 4, 2.
22. Johansson, J. U., Pradhan, S., Lokteva, L. A., Woodling, N. S., Ko, N., Brown, H. D., …Andreasson, K. I. (2013). Suppression of inflammation with conditional deletion of the prostaglandin E2 EP2 receptor in macrophages and brain microglia. The Journal of Neuroscience, 33, 16016-16032.
23. Liang, X., Wang, Q., Hand, T., Wu, L., Breyer, R. M., Montine, T. J., … Andreasson, K. (2005). Deletion of the prostaglandin E2 EP2 receptor reduces oxidative damage and amyloid burden in a model of Alzheimer’s disease. The Journal of Neuroscience, 25, 10180-10187.
24. Liang, X., Wang, Q., Shi, J., Lokteva, L., Breyer, R. M., Montine, T. J., … Andreasson, K. (2008). The prostaglandin E2 EP2 receptor accelerates disease progression and inflammation in a model of amyotrophic lateral sclerosis. Annals of Neurology, 64, 304-314.
25. Liu, D., Wu, L., Breyer, R., Mattson, M. P., & Andreasson, K. (2005). Neuroprotection by the PGE2 EP2 receptor in permanent focal cerebral ischemia. Annals of Neurology, 57, 758-761.
26. Manabe, Y., Anrather, J., Kawano, T., Niwa, K., Zhou, P., Ross, M. E., … Iadecola, C. (2004). Prostanoids, not reactive oxygen species, mediate COX-2-dependent neurotoxicity. Annals of Neurology, 55, 668-675.
27. Mayer, S. A., Brun, N. C., Begtrup, K., Broderick, J., Davis, S., Diringer, M. N., … Trial Investigators, FAST. (2008). Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. The New England Journal of Medicine, 358, 2127-2137.
28. McCullough, L., Wu, L., Haughey, N., Liang, X., Hand, T., Wang, Q., …Andreasson, K. (2004). Neuroprotective function of the PGE2 EP2 receptor in cerebral ischemia. The Journal of Neuroscience, 24, 257-268.
29. Medeiros, A. I., Serezani, C. H., Lee, S. P., & Peters-Golden, M. (2009). Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling. The Journal of Experimental Medicine, 206, 61-68.
30. Mendez, N. V., Wharton, J. A., Leclerc, J. L., Blackburn, S. L., Douglas-Escobar, M. V., Weiss, M. D., … Doré, S. (2013). Clinical implications of bilirubin-associated neuroprotection and neurotoxicity. International Journal of Clinical Anesthesiology, 1, 1013.
31. Mohan, S., Narumiya, S., & Doré, S. (2015). Neuroprotective role of prostaglandin PGE2 EP2 receptor in hemin-mediated toxicity. Neurotoxicology, 46, 53-59.
32. Moradiya, Y., Murthy, S. B., Newman-Toker, D. E., Hanley, D. F., & Ziai, W. C. (2014). Intraventricular thrombolysis in intracerebral hemorrhage requiring ventriculostomy: A decade-long real-world experience. Stroke, 45, 2629-2635.
33. Munakata, M., Shirakawa, H., Nagayasu, K., Miyanohara, J., Miyake, T., Nakagawa, T., … Kaneko, S. (2013). Transient receptor potential canonical 3 inhibitor Pyr3 improves outcomes and attenuates astrogliosis after intracerebral hemorrhage in mice. Stroke, 44, 1981-1987.
34. Nagano, T., Kimura, S. H., & Takemura, M. (2010). Prostaglandin E2 reduces amyloid beta-induced phagocytosis in cultured rat microglia. Brain Research, 1323, 11-17.
35. Pooler, A. M., Arjona, A. A., Lee, R. K., & Wurtman, R. J. (2004). Prostaglandin E2 regulates amyloid precursor protein expression via the EP2 receptor in cultured rat microglia. Neuroscience Letters, 362, 127-130.
36. Poon, M. T., Fonville, A. F., & Al-Shahi Salman, R. (2014). Longterm prognosis after intracerebral haemorrhage: Systematic review and meta-analysis. Journal of Neurology, Neurosurgery, and Psychiatry, 85, 660-667.
37. Quan, Y., Jiang, J., & Dingledine, R. (2013). EP2 receptor signaling pathways regulate classical activation of microglia. The Journal of Biological Chemistry, 288, 9293-9302.
38. Rincon, F., & Mayer, S. A. (2008). Clinical review: Critical care management of spontaneous intracerebral hemorrhage. Critical Care, 12, 237.
39. Sahni, R., & Weinberger, J. (2007). Management of intracerebral hemorrhage. Vascular Health and Risk Management, 3, 701-709.
40. Savonenko, A., Munoz, P., Melnikova, T., Wang, Q., Liang, X., Breyer, R. M., … Andreasson, K. (2009). Impaired cognition, sensorimotor gating, and hippocampal long-term depression in mice lacking the prostaglandin E2 EP2 receptor. Experimental Neurology, 217, 63-73.
41. Shie, F. S., Breyer, R. M., & Montine, T. J. (2005a). Microglia lacking E Prostanoid Receptor subtype 2 have enhanced Abeta phagocytosis yet lack Abeta-activated neurotoxicity. The American Journal of Pathology, 166, 1163-1172.
42. Shie, F. S., Montine, K. S., Breyer, R. M., & Montine, T. J. (2005b). Microglial EP2 is critical to neurotoxicity from activated cerebral innate immunity. Glia, 52, 70-77.
43. Singh, N., Ma, B., Leonardo, C. C., Ahmad, A. S., Narumiya, S., Doré, S. (2013). Role of PGE(2) EP1 receptor in intracerebral hemorrhage-induced brain injury. Neurotoxicity Research, 24, 549-559.
44. Suzuki, S., Yokoyama, U., Abe, T., Kiyonari, H., Yamashita, N., Kato, Y., … Ishikawa, Y. (2010). Differential roles of Epac in regulating cell death in neuronal and myocardial cells. The Journal of Biological Chemistry, 285, 24248-24259.
45. van Asch, C. J., Luitse, M. J., Rinkel, G. J., van der Tweel, I., Algra, A., Klijn, C. J. (2010). Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: A systematic review and meta-analysis. The Lancet Neurology, 9, 167-176.
46. Wang, J., & Doré, S. (2007a). Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain, 130, 1643-1652.
47. Wang, J., & Doré, S. (2007b). Inflammation after intracerebral hemorrhage. Journal of Cerebral Blood Flow and Metabolism, 27, 894-908.
48. Yang, H., Zhang, J., Breyer, R. M., & Chen, C. (2009). Altered hippocampal long-term synaptic plasticity in mice deficient in the PGE2 EP2 receptor. Journal of Neurochemistry, 108, 295-304.
49. Zaslona, Z., Serezani, C. H., Okunishi, K., Aronoff, D. M., & Peters-Golden, M. (2012). Prostaglandin E2 restrains macrophage maturation via E prostanoid receptor 2/protein kinase A signaling. Blood, 119, 2358-2367.
50. Zhang, J., & Rivest, S. (1999). Distribution, regulation and colocalization of the genes encoding the EP2- and EP4-PGE2 receptors in the rat brain and neuronal responses to systemic inflammation. The European Journal of Neuroscience, 11, 2651-2668.