PGE2 receptor agonist misoprostol protects brain against intracerebral hemorrhage in mice

Neurobiology of Aging

Volumn 36, Issue 3, 2015, Pages 1439-1450

  Wu, He ^a,b   Wu, Tao ^b,c   Hua, Wei ^a   Dong, Xianghui ^a   Gao, Yufeng ^b   Zhao, Xiaochun ^b   Chen, Wenwu ^b   Cao, Wangsen ^d   Yang, Qingwu ^e   Qi, Jiping ^a   Zhou, Jin ^a   Wang, Jian ^b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

^d MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^e THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Glycyrrhizin; High mobility group box 1; Inflammation; Matrix metalloproteinase; PGE2; Src

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; COLLAGENASE; CYCLOOXYGENASE 2; GELATINASE A; GELATINASE B; GLYCYRRHIZIC ACID; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1BETA; MISOPROSTOL; PROSTAGLANDIN E RECEPTOR; PROSTAGLANDIN RECEPTOR STIMULATING AGENT; PROTEIN TYROSINE KINASE; FIBROBLAST GROWTH FACTOR 1; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; BRAIN ATROPHY; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INFARCTION SIZE; BRAIN PROTECTION; CONTROLLED STUDY; DRUG EFFICACY; FUNCTIONAL STATUS; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; AGONISTS; ANIMAL; C57BL MOUSE; CEREBRAL HEMORRHAGE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY;

ANIMALS; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; FIBROBLAST GROWTH FACTOR 1; GENE EXPRESSION; GLYCYRRHIZIC ACID; INFLAMMATION; INTERLEUKIN-1BETA; MALE; MATRIX METALLOPROTEINASE 2; MICE, INBRED C57BL; MISOPROSTOL; NEUROPROTECTIVE AGENTS; RECEPTORS, PROSTAGLANDIN E; SRC-FAMILY KINASES;

EID: 84923595111     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.12.029     Document Type: Article

References (48)

1. Ardizzone T.D., Zhan X., Ander B.P., Sharp F.R. SRC kinase inhibition improves acute outcomes after experimental intracerebral hemorrhage. Stroke 2007, 38:1621-1625.
2. Chu K., Jeong S.W., Jung K.H., Han S.Y., Lee S.T., Kim M., Roh J.K. Celecoxib induces functional recovery after intracerebral hemorrhage with reduction of brain edema and perihematomal cell death. J.Cereb. Blood Flow Metab. 2004, 24:926-933.
3. Cipollone F., Prontera C., Pini B., Marini M., Fazia M., De Cesare D., Iezzi A., Ucchino S., Boccoli G., Saba V., Chiarelli F., Cuccurullo F., Mezzetti A. Overexpression of functionally coupled cyclooxygenase-2 and prostaglandin E synthase in symptomatic atherosclerotic plaques as a basis of prostaglandin E(2)-dependent plaque instability. Circulation 2001, 104:921-927.
4. Fisher M., Feuerstein G., Howells D.W., Hurn P.D., Kent T.A., Savitz S.I., Lo E.H. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40:2244-2250.
5. Gao H.M., Liu B., Zhang W., Hong J.S. Synergistic dopaminergic neurotoxicity of MPTP and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease. FASEB J. 2003, 17:1957-1959.
6. Girard J.P. Adirect inhibitor of HMGB1 cytokine. Chem. Biol. 2007, 14:345-347.
7. Gong C., Ennis S.R., Hoff J.T., Keep R.F. Inducible cyclooxygenase-2 expression after experimental intracerebral hemorrhage. Brain Res. 2001, 901:38-46.
8. Grossetete M., Rosenberg G.A. Matrix metalloproteinase inhibition facilitates cell death in intracerebral hemorrhage in mouse. J.Cereb. Blood Flow Metab. 2008, 28:752-763.
9. Hurn P.D., Vannucci S.J., Hagberg H. Adult or perinatal brain injury: does sex matter?. Stroke 2005, 36:193-195.
10. Jones R.L., Giembycz M.A., Woodward D.F. Prostanoid receptor antagonists: development strategies and therapeutic applications. Br. J. Pharmacol. 2009, 158:104-145.
11. Kim J.B., Sig Choi J., Yu Y.M., Nam K., Piao C.S., Kim S.W., Lee M.H., Han P.L., Park J.S., Lee J.K. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J.Neurosci. 2006, 26:6413-6421.
12. Li J., Liang X., Wang Q., Breyer R.M., McCullough L., Andreasson K. Misoprostol, an anti-ulcer agent and PGE2 receptor agonist, protects against cerebral ischemia. Neurosci. Lett. 2008, 438:210-215.
13. Liang X., Lin L., Woodling N.S., Wang Q., Anacker C., Pan T., Merchant M., Andreasson K. Signaling via the prostaglandin E receptor EP4 exerts neuronal and vascular protection in a mouse model of cerebral ischemia. J.Clin. Invest. 2011, 121:4362-4371.
14. Liu D.Z., Cheng X.Y., Ander B.P., Xu H., Davis R.R., Gregg J.P., Sharp F.R. Src kinase inhibition decreases thrombin-induced injury and cell cycle re-entry in striatal neurons. Neurobiol. Dis. 2008, 30:201-211.
15. Liu D.Z., Sharp F.R. The dual role of SRC kinases in intracerebral hemorrhage. Acta Neurochir Suppl. 2011, 111:77-81.
16. 2 EP2 receptor in permanent focal cerebral ischemia. Ann. Neurol. 2005, 57:758-761.
17. McCullough L., Wu L., Haughey N., Liang X., Hand T., Wang Q., Breyer R.M., Andreasson K. Neuroprotective function of the PGE2 EP2 receptor in cerebral ischemia. J.Neurosci. 2004, 24:257-268.
18. Mollica L., De Marchis F., Spitaleri A., Dallacosta C., Pennacchini D., Zamai M., Agresti A., Trisciuoglio L., Musco G., Bianchi M.E. Glycyrrhizin binds to high-mobility group box 1 protein and inhibits its cytokine activities. Chem. Biol. 2007, 14:431-441.
19. Moxon-Emre I., Schlichter L.C. Neutrophil depletion reduces blood-brain barrier breakdown, axon injury, and inflammation after intracerebral hemorrhage. J.Neuropathol. Exp. Neurol. 2011, 70:218-235.
20. Numo R. Prevention of NSAID-induced ulcers by the coadministration of misoprostol: implications in clinical practice. Scand. J. Rheumatol. Suppl. 1992, 92:25-29.
21. Ohnishi M., Katsuki H., Fukutomi C., Takahashi M., Motomura M., Fukunaga M., Matsuoka Y., Isohama Y., Izumi Y., Kume T., Inoue A., Akaike A. HMGB1 inhibitor glycyrrhizin attenuates intracerebral hemorrhage-induced injury in rats. Neuropharmacology 2011, 61:975-980.
22. Park L., Anrather J., Girouard H., Zhou P., Iadecola C. Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J.Cereb. Blood Flow Metab. 2007, 27:1908-1918.
23. Qiu J., Nishimura M., Wang Y., Sims J.R., Qiu S., Savitz S.I., Salomone S., Moskowitz M.A. Early release of HMGB-1 from neurons after the onset of brain ischemia. J.Cereb. Blood Flow Metab. 2008, 28:927-938.
24. Qiu J., Xu J., Zheng Y., Wei Y., Zhu X., Lo E.H., Moskowitz M.A., Sims J.R. High-mobility group box 1 promotes metalloproteinase-9 upregulation through Toll-like receptor 4 after cerebral ischemia. Stroke 2010, 41:2077-2082.
25. Reimer R., Heim H.K., Muallem R., Odes H.S., Sewing K.F. Effects of EP-receptor subtype specific agonists and other prostanoids on adenylate cyclase activity of duodenal epithelial cells. Prostaglandins 1992, 44:485-493.
26. Rosell A., Ortega-Aznar A., Alvarez-Sabin J., Fernandez-Cadenas I., Ribo M., Molina C.A., Lo E.H., Montaner J. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 2006, 37:1399-1406.
27. Roskoski R. Src protein-tyrosine kinase structure and regulation. Biochem. Biophys. Res. Commun. 2004, 324:1155-1164.
28. Shalhoub J., Falck-Hansen M.A., Davies A.H., Monaco C. Innate immunity and monocyte-macrophage activation in atherosclerosis. J.Inflamm. (Lond) 2011, 8:9.
29. Taniguchi H., Anacker C., Suarez-Mier G.B., Wang Q., Andreasson K. Function of prostaglandin E2 EP receptors in the acute outcome of rodent hypoxic ischemic encephalopathy. Neurosci. Lett. 2011, 504:185-190.
30. Wang J. Preclinical and clinical research on inflammation after intracerebral hemorrhage. Prog. Neurobiol. 2010, 92:463-477.
31. Wang J., Dore S. Inflammation after intracerebral hemorrhage. J.Cereb. Blood Flow Metab. 2007, 27:894-908.
32. Wang J., Fields J., Dore S. The development of an improved preclinical mouse model of intracerebral hemorrhage using double infusion of autologous whole blood. Brain Res. 2008, 1222:214-221.
33. Wang J., Fields J., Zhao C., Langer J., Thimmulappa R.K., Kensler T.W., Yamamoto M., Biswal S., Dore S. Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic. Biol. Med. 2007, 43:408-414.
34. Wang J., Rogove A.D., Tsirka A.E., Tsirka S.E. Protective role of tuftsin fragment 1-3 in an animal model of intracerebral hemorrhage. Ann. Neurol. 2003, 54:655-664.
35. Wang J., Tsirka S.E. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 2005, 128:1622-1633.
36. Wang J., Tsirka S.E. Tuftsin fragment 1-3 is beneficial when delivered after the induction of intracerebral hemorrhage. Stroke 2005, 36:613-618.
37. Wasserman J.K., Yang H., Schlichter L.C. Glial responses, neuron death and lesion resolution after intracerebral hemorrhage in young vs. aged rats. Eur. J. Neurosci. 2008, 28:1316-1328.
38. Wu H., Wu T., Li M., Wang J. Efficacy of the lipid-soluble iron chelator 2,2'-dipyridyl against hemorrhagic brain injury. Neurobiol. Dis. 2012, 45:388-394.
39. Wu T., Wu H., Wang J., Wang J. Expression and cellular localization of cyclooxygenases and prostaglandin E synthases in the hemorrhagic brain. J.Neuroinflammation 2011, 8:22.
40. Wu H., Wu T., Xu X., Wang J., Wang J. Iron toxicity in mice with collagenase-induced intracerebral hemorrhage. J.Cereb. Blood Flow Metab. 2011, 31:1243-1250.
41. Wu H., Zhang Z., Hu X., Zhao R., Song Y., Ban X., Qi J., Wang J. Dynamic changes of inflammatory markers in brain after hemorrhagic stroke in humans: a postmortem study. Brain Res. 2010, 1342:111-117.
42. Xue M., Fan Y., Liu S., Zygun D.A., Demchuk A., Yong V.W. Contributions of multiple proteases to neurotoxicity in a mouse model of intracerebral haemorrhage. Brain 2009, 132:26-36.
43. Xue M., Hollenberg M.D., Demchuk A., Yong V.W. Relative importance of proteinase-activated receptor-1 versus matrix metalloproteinases in intracerebral hemorrhage-mediated neurotoxicity in mice. Stroke 2009, 40:2199-2204.
44. Xue M., Hollenberg M.D., Yong V.W. Combination of thrombin and matrix metalloproteinase-9 exacerbates neurotoxicity in cell culture and intracerebral hemorrhage in mice. J.Neurosci. 2006, 26:10281-10291.
45. Zan L., Wu H., Jiang J., Zhao S., Song Y., Teng G., Li H., Jia Y., Zhou M., Zhang X., Qi J., Wang J. Temporal profile of Src, SSeCKS, and angiogenic factors after focal cerebral ischemia: correlations with angiogenesis and cerebral edema. Neurochem. Int. 2011, 58:872-879.
46. Zan L., Zhang X., Xi Y., Wu H., Song Y., Teng G., Li H., Qi J., Wang J. Src regulates angiogenic factors and vascular permeability after focal cerebral ischemia-reperfusion. Neuroscience 2014, 262:118-128.
47. Zhang J., Takahashi H.K., Liu K., Wake H., Liu R., Maruo T., Date I., Yoshino T., Ohtsuka A., Mori S., Nishibori M. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke 2011, 42:1420-1428.
48. Zhou Y., Xiong K.L., Lin S., Zhong Q., Lu F.L., Liang H., Li J.C., Wang J.Z., Yang Q.W. Elevation of high-mobility group protein box-1 in serum correlates withseverity of acute intracerebral hemorrhage. Mediators Inflamm. 2010, pii:142458.