Ghrelin alleviates early brain injury after subarachnoid hemorrhage via the PI3K/Akt signaling pathway

Brain Research

Volumn 1587, Issue 1, 2014, Pages 15-22

  Hao, Xiao Ke ^a   Wu, Wei ^a,b   Wang, Chun Xi ^b   Xie, Guang Bin ^b   Li, Tao ^b   Wu, He Ming ^a   Huang, Li Tian ^c   Zhou, Meng Liang ^b   Hang, Chun Hua ^a,b   Shi, Ji Xin ^a,b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Early brain injury; Ghrelin; PI3K Akt; Subarachnoid hemorrhage

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; GHRELIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; AKT1 PROTEIN, RAT; CHROMONE DERIVATIVE; MORPHOLINE DERIVATIVE; NERVE PROTEIN; NEUROPROTECTIVE AGENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN EDEMA; BRAIN INJURY; BRAIN NERVE CELL; BRAIN WATER; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EARLY BRAIN INJURY; ENZYME ACTIVATION; ENZYME ASSAY; MALE; MORTALITY; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE; UPREGULATION; WATER CONTENT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN DAMAGE, CHRONIC; DRUG EFFECTS; ENZYME INDUCTION; ENZYMOLOGY; GENETICS; METABOLISM; NERVE CELL; NEUROLOGIC EXAMINATION; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; SINGLE BLIND PROCEDURE; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; APOPTOSIS; BRAIN DAMAGE, CHRONIC; BRAIN EDEMA; CASPASE 3; CHROMONES; ENZYME INDUCTION; GHRELIN; MALE; MORPHOLINES; NERVE TISSUE PROTEINS; NEUROLOGIC EXAMINATION; NEURONS; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SINGLE-BLIND METHOD; SUBARACHNOID HEMORRHAGE; UP-REGULATION;

EID: 84922830506     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.08.069     Document Type: Article

References (41)

1. Ansar, S., Maddahi, A., Edvinsson, L., 2011. Inhibition of cerebrovascular raf activation attenuates cerebral blood flow and prevents upregulation of contractile receptors after subarachnoid hemorrhage. BMC Neurosci. 12, 107.
2. Dai, Y., Sun, Q., Zhang, X., Hu, Y., Zhou, M., Shi, J., 2014. Cyclosporin A ameliorates early brain injury after subarachnoid hemorrhage through inhibition of a Nur77 dependent apoptosis pathway. Brain Res. 1556, 67-76.
3. Date, Y., Kojima, M., Hosoda, H., Sawaguchi, A., Mondal, M.S., Suganuma, T., Matsukura, S., Kangawa, K., Nakazato, M., 2000. Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141, 4255-4261.
4. Endo, H., Nito, C., Kamada, H., Yu, F., Chan, P.H., 2006. Akt/GSK3beta survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 37, 2140-2146.
5. Ersahin, M., Toklu, H.Z., Erzik, C., Cetinel, S., Akakin, D., Velioglu-Ogunc, A., Tetik, S., Ozdemir, Z.N., Sener, G., Yegen, B.C., 2010. The anti-inflammatory and neuroprotective effects of ghrelin in subarachnoid hemorrhage-induced oxidative brain damage in rats. J. Neurotrauma 27, 1143-1155.
6. Friedrich, V., Flores, R., Sehba, F.A., 2012. Cell death starts early after subarachnoid hemorrhage. Neurosci. Lett. 512, 6-11.
7. Garcia, J.H., Wagner, S., Liu, K.F., Hu, X.J., 1995. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Stat. Validation Stroke 26, 627-634 (discussion 635).
8. Golan, E., Vasquez, D.N., Ferguson, N.D., Adhikari, N.K., Scales, D.C., 2013. Prophylactic magnesium for improving neurologic outcome after aneurysmal subarachnoid hemorrhage: systematic review and meta-analysis. J. Crit. Care 28, 173-181.
9. Hong, Y., Shao, A., Wang, J., Chen, S., Wu, H., McBride, D.W., Wu, Q., Sun, X., Zhang, J., 2014. Neuroprotective effect of hydrogen-rich saline against neurologic damage and apoptosis in early brain injury following subarachnoid hemorrhage: possible role of the Akt/GSK3 beta signaling pathway. PLoS One 9, e96212.
10. Kojima, M., Hosoda, H., Date, Y., Nakazato, M., Matsuo, H., Kangawa, K., 1999. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402, 656-660.
11. Krafft, P.R., Altay, O., Rolland, W.B., Duris, K., Lekic, T., Tang, J., Zhang, J.H., 2012. alpha7 nicotinic acetylcholine receptor agonism confers neuroprotection through GSK-3beta inhibition in a mouse model of intracerebral hemorrhage. Stroke 43, 844-850.
12. Kramer, A., Fletcher, J., 2009. Do endothelin-receptor antagonists prevent delayed neurological deficits and poor outcomes after aneurysmal subarachnoid hemorrhage? A meta-analysis. Stroke 40, 3403-3406.
13. Kusaka, G., Ishikawa, M., Nanda, A., Granger, D.N., Zhang, J.H., 2004. Signaling pathways for early brain injury after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 24, 916-925.
14. Lee, J.Y., Chung, H., Yoo, Y.S., Oh, Y.J., Oh, T.H., Park, S., Yune, T.Y., 2010. Inhibition of apoptotic cell death by ghrelin improves functional recovery after spinal cord injury. Endocrinology 151, 3815-3826.
15. Lee, J.Y., Oh, T.H., Yune, T.Y., 2011. Ghrelin inhibits hydrogen peroxide-induced apoptotic cell death of oligodendrocytes via ERK and p38MAPK signaling. Endocrinology 152, 2377-2386.
16. Lee, S., Kim, Y., Li, E., Park, S., 2012. Ghrelin protects spinal cord motoneurons against chronic glutamate excitotoxicity by inhibiting microglial activation. Korean J. Physiol. Pharmacol. 16, 43-48.
17. Li, H., Wu, W., Sun, Q., Liu, M., Li, W., Zhang, X.S., Zhou, M.L., Hang, C.H., 2014. Expression and cell distribution of receptor for advanced glycation end-products in the rat cortex following experimental subarachnoid hemorrhage. Brain Res. 1543, 315-323.
18. Lim, E., Lee, S., Li, E., Kim, Y., Park, S., 2011. Ghrelin protects spinal cord motoneurons against chronic glutamate-induced excitotoxicity via ERK1/2 and phosphatidylinositol-3-kinase/Akt/glycogen synthase kinase-3beta pathways. Exp. Neurol. 230, 114-122.
19. Mullonkal, C.J., Toledo-Pereyra, L.H., 2007. Akt in ischemia and reperfusion. J. Invest. Surg. 20, 195-203.
20. Nikolopoulos, D., Theocharis, S., Kouraklis, G., 2010. Ghrelin, another factor affecting bone metabolism. Med. Sci. Monit. 16, RA147-RA162.
21. Noshita, N., Lewen, A., Sugawara, T., Chan, P.H., 2001. Evidence of phosphorylation of Akt and neuronal survival after transient focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab. 21, 1442-1450.
22. Noshita, N., Lewen, A., Sugawara, T., Chan, P.H., 2002. Akt phosphorylation and neuronal survival after traumatic brain injury in mice. Neurobiol. Dis. 9, 294-304.
23. Noshita, N., Sugawara, T., Lewen, A., Hayashi, T., Chan, P.H., 2003. Copper-zinc superoxide dismutase affects Akt activation after transient focal cerebral ischemia in mice. Stroke 34, 1513-1518.
24. Ostrowski, R.P., Colohan, A.R., Zhang, J.H., 2006. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol. Res. 28, 399-414.
25. Qiu, W.C., Wang, Z.G., Lv, R., Wang, W.G., Han, X.D., Yan, J., Wang, Y., Zheng, Q., Ai, K.X., 2008. Ghrelin improves delayed gastrointestinal transit in alloxan-induced diabetic mice. World J. Gastroenterol. 14, 2572-2577.
26. Sabri, M., Lass, E., Macdonald, R.L., 2013. Early brain injury: a common mechanism in subarachnoid hemorrhage and global cerebral ischemia. Stroke Res. Treat 2013, 394036.
27. Sakata, I., Nakamura, K., Yamazaki, M., Matsubara, M., Hayashi, Y., Kangawa, K., Sakai, T., 2002. Ghrelin-producing cells exist as two types of cells, closed-and opened-type cells, in the rat gastrointestinal tract. Peptides 23, 531-536.
28. Sehba, F.A., Hou, J., Pluta, R.M., Zhang, J.H., 2012. The importance of early brain injury after subarachnoid hemorrhage. Prog. Neurobiol. 97, 14-37.
29. Sun, Q., Dai, Y., Zhang, X., Hu, Y.C., Zhang, D., Li, W., Zhang, X.S., Zhu, J.H., Zhou, M.L., Hang, C.H., 2013. Expression and cell distribution of myeloid differentiation primary response protein 88 in the cerebral cortex following experimental subarachnoid hemorrhage in rats: a pilot study. Brain Res. 1520, 134-144.
30. Topkoru, B.C., Altay, O., Duris, K., Krafft, P.R., Yan, J., Zhang, J.H., 2013. Nasal administration of recombinant osteopontin attenuates early brain injury after subarachnoid hemorrhage. Stroke 44, 3189-3194.
31. Tseng, M.Y., Czosnyka, M., Richards, H., Pickard, J.D., Kirkpatrick, P.J., 2005. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke 36, 1627-1632.
32. Wren, A.M., Small, C.J., Ward, H.L., Murphy, K.G., Dakin, C.L., Taheri, S., Kennedy, A.R., Roberts, G.H., Morgan, D.G., Ghatei, M.A., Bloom, S.R., 2000. The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 141, 4325-4328.
33. Xi, G., Hua, Y., Keep, R.F., Younger, J.G., Hoff, J.T., 2002. Brain edema after intracerebral hemorrhage: the effects of systemic complement depletion. Acta Neurochir. Suppl. 81, 253-256.
34. Xu, J., Wang, S., Lin, Y., Cao, L., Wang, R., Chi, Z., 2009. Ghrelin protects against cell death of hippocampal neurons in pilocarpine-induced seizures in rats. Neurosci. Lett. 453, 58-61.
35. Yu, F., Sugawara, T., Maier, C.M., Hsieh, L.B., Chan, P.H., 2005. Akt/Bad signaling and motor neuron survival after spinal cord injury. Neurobiol. Dis. 20, 491-499.
36. Zhang, R., Yang, G., Wang, Q., Guo, F., Wang, H., 2013. Acylated ghrelin protects hippocampal neurons in pilocarpine-induced seizures of immature rats by inhibiting cell apoptosis. Mol. Biol. Rep. 40, 51-58.
37. Zhao, S., Fu, J., Liu, X., Wang, T., Zhang, J., Zhao, Y., 2012. Activation of Akt/GSK-3beta/beta-catenin signaling pathway is involved in survival of neurons after traumatic brain injury in rats. Neurol. Res. 34, 400-407.
38. Zhou, X.M., Zhang, X., Zhang, X.S., Zhuang, Z., Li, W., Sun, Q., Li, T., Wang, C.X., Zhu, L., Shi, J.X., Zhou, M.L., 2014a. SIRT1 inhibition by sirtinol aggravates brain edema after experimental subarachnoid hemorrhage. J. Neurosci. Res. 92, 714-722.
39. Zhou, X.M., Zhou, M.L., Zhang, X.S., Zhuang, Z., Li, T., Shi, J.X., Zhang, X., 2014b. Resveratrol prevents neuronal apoptosis in an early brain injury model. J. Surg. Res. 189, 159-165.
40. Zhu, Y.M., Wang, C.C., Chen, L., Qian, L.B., Ma, L.L., Yu, J., Zhu, M.H., Wen, C.Y., Yu, L.N., Yan, M., 2013. Both PI3K/Akt and ERK1/2 pathways participate in the protection by dexmedetomidine against transient focal cerebral ischemia/reperfusion injury in rats. Brain Res. 1494, 1-8.
41. Zigman, J.M., Jones, J.E., Lee, C.E., Saper, C.B., Elmquist, J.K., 2006. Expression of ghrelin receptor mRNA in the rat and the mouse brain. J. Comp. Neurol. 494, 528-548.