Ghrelin attenuates brain injury in septic mice via PI3K/Akt signaling activation

Brain Research Bulletin

Volumn 124, Issue , 2016, Pages 278-285

  Sun, Ning ^a   Wang, Hui ^a   Ma, Li ^a   Lei, Ping ^a   Zhang, Qiang ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Cecal ligation and puncture; Ghrelin; PI3K Akt signaling; Sepsis

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; GHRELIN; INTERLEUKIN 1BETA; MALONALDEHYDE; NEUROPROTECTIVE AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; CYTOKINE; ENZYME INHIBITOR; MORPHOLINE DERIVATIVE; ONCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN EDEMA; BRAIN INJURY; BRAIN WATER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; MALE; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANIMAL; BRAIN INJURIES; C57BL MOUSE; CAPILLARY PERMEABILITY; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BLOOD-BRAIN BARRIER; BRAIN EDEMA; BRAIN INJURIES; CAPILLARY PERMEABILITY; CHROMONES; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GHRELIN; MALE; MICE; MICE, INBRED C57BL; MORPHOLINES; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; SEPSIS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84976313505     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2016.06.002     Document Type: Article

References (43)

1. Alexander, J.J., Jacob, A., Cunningham, P., Hensley, L., Quigg, R.J., TNF is a key mediator of septic encephalopathy acting through its receptor, TNF receptor-1. Neurochem. Int. 52 (2008), 447–456.
2. Chandra, J., Samali, A., Orrenius, S., Triggering and modulation of apoptosis by oxidative stress. ‎Free Radic. Biol. Med. 29 (2000), 323–333.
3. Chen, L., Wei, X., Hou, Y., Liu, X., Li, S., Sun, B., Liu, X., Liu, H., Tetramethylpyrazine analogue CXC195 protects against cerebral ischemia/reperfusion-induced apoptosis through PI3K/Akt/GSK3beta pathway in rats. Neurochem. Int. 66 (2014), 27–32.
4. Chuang, T.Y., Chang, H.T., Chung, K.P., Cheng, H.S., Liu, C.Y., Liu, Y.C., Huang, H.H., Chou, T.C., Chang, B.L., Lee, M.R., Lin, C.J., Lee, S.W., Yu, C.J., Hsueh, P.R., High levels of serum macrophage migration inhibitory factor and interleukin 10 are associated with a rapidly fatal outcome in patients with severe sepsis. Int. J. Infect. Dis. 20 (2014), 13–17.
5. Date, Y., Kojima, M., Hosoda, H., Sawaguchi, A., Mondal, M.S., Suganuma, T., Matsukura, S., Kangawa, K., Nakazato, M., 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 (2000), 4255–4261.
6. Davies, D.C., Blood-brain barrier breakdown in septic encephalopathy and brain tumours. J. Anat. 200 (2002), 639–646.
7. Deng, Y.Y., Fang, M., Zhu, G.F., Zhou, Y., Zeng, H.K., Role of microglia in the pathogenesis of sepsis-associated encephalopathy. CNS Neurolo. Disord. Drug Targets 12 (2013), 720–725.
8. Duronio, V., The life of a cell: apoptosis regulation by the PI3K/PKB pathway. Biochem. J. 415 (2008), 333–344.
9. Endo, H., Nito, C., Kamada, H., Yu, F., Chan, P.H., Akt/GSK3beta survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 37 (2006), 2140–2146.
10. Ersahin, M., Toklu, H.Z., Erzik, C., Cetinel, S., Akakin, D., Velioglu-Ogunc, A., Tetik, S., Ozdemir, Z.N., Sener, G., Yegen, B.C., The anti-inflammatory and neuroprotective effects of ghrelin in subarachnoid hemorrhage-induced oxidative brain damage in rats. J. Neurotrauma 27 (2010), 1143–1155.
11. Fang, F., Pan, J., Li, Y., Xu, L., Su, G., Li, G., Wang, J., Association between interleukin 1 receptor antagonist gene 86-bp VNTR polymorphism and sepsis: a meta-analysis. Hum. Immunol. 76 (2015), 1–5.
12. Feng, B., Mao, Z.R., Pang, K., Zhang, S.L., Li, L., Association of tumor necrosis factor alpha −308G/A and interleukin-6-174G/C gene polymorphism with pneumonia-induced sepsis. J. Crit. Care, 2015.
13. Gofton, T.E., Young, G.B., Sepsis-associated encephalopathy. Nat. Rev. Neurol. 8 (2012), 557–566.
14. Gyurkovska, V., Ivanovska, N., Tyrosine kinase inhibitor tyrphostin AG490 reduces liver injury in LPS-induced shock. Eur. J. Pharmacol. 751 (2015), 118–126.
15. Hao, X.K., Wu, W., Wang, C.X., Xie, G.B., Li, T., Wu, H.M., Huang, L.T., Zhou, M.L., Hang, C.H., Shi, J.X., Ghrelin alleviates early brain injury after subarachnoid hemorrhage via the PI3K/Akt signaling pathway. Brain Res. 1587 (2014), 15–22.
16. Hong, Y., Shao, A., Wang, J., Chen, S., Wu, H., McBride, D.W., Wu, Q., Sun, X., Zhang, J., Neuroprotective effect of hydrogen-rich saline against neurologic damage and apoptosis in early brain injury following subarachnoid hemorrhage: possible role of the Akt/GSK3beta signaling pathway. PLoS One, 9, 2014, e96212.
17. Hopkins, R.O., Sepsis, oxidative stress, and brain injury. Crit. Care Med. 35 (2007), 2233–2234.
18. Jiang, S., Zhu, W., Li, C., Zhang, X., Lu, T., Ding, Z., Cao, K., Liu, L., alpha-Lipoic acid attenuates LPS-induced cardiac dysfunction through a PI3K/Akt-dependent mechanism. Int. Immunopharmacol. 16 (2013), 100–107.
19. Jie, P., Hong, Z., Tian, Y., Li, Y., Lin, L., Zhou, L., Du, Y., Chen, L., Chen, L., Activation of transient receptor potential vanilloid 4 induces apoptosis in hippocampus through downregulating PI3K/Akt and upregulating p38 MAPK signaling pathways. Cell. Death Dis., 6, 2015, e1775.
20. Kim, T.H., Kim, S.J., Lee, S.M., Stimulation of the alpha7 nicotinic acetylcholine receptor protects against sepsis by inhibiting Toll-like receptor via phosphoinositide 3-kinase activation. J. Infect. Dis. 209 (2014), 1668–1677.
21. Kojima, M., Hosoda, H., Date, Y., Nakazato, M., Matsuo, H., Kangawa, K., Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402 (1999), 656–660.
22. Lahiri, R., Derwa, Y., Bashir, Z., Giles, E., Torrance, H.D., Owen, H.C., O'Dwyer, M.J., O'Brien, A., Stagg, A.J., Bhattacharya, S., Foster, G.R., Alazawi, W., Systemic inflammatory response syndrome after major abdominal surgery predicted by early upregulation of TLR4 and TLR5. Ann. Surg., 2015.
23. Lin, K.H., Kuo, W.W., Jiang, A.Z., Pai, P., Lin, J.Y., Chen, W.K., Day, C.H., Shen, C.Y., Padma, V.V., Huang, C.Y., Tetramethylpyrazine ameliorated hypoxia-induced myocardial cell apoptosis via HIF-1alpha/JNK/p38 and IGFBP3/BNIP3 inhibition to upregulate PI3K/Akt survival signaling, cellular physiology and biochemistry. Int. J. Exp. Cell. Physiol. Biochem. Pharmacol. 36 (2015), 334–344.
24. Liu, L., Xie, K., Chen, H., Dong, X., Li, Y., Yu, Y., Wang, G., Yu, Y., Inhalation of hydrogen gas attenuates brain injury in mice with cecal ligation and puncture via inhibiting neuroinflammation, oxidative stress and neuronal apoptosis. Brain Res. 1589 (2014), 78–92.
25. Liu, X.Y., Zhou, X.Y., Hou, J.C., Zhu, H., Wang, Z., Liu, J.X., Zheng, Y.Q., Ginsenoside Rd promotes neurogenesis in rat brain after transient focal cerebral ischemia via activation of PI3K/Akt pathway. Acta Pharmacol. Sin. 36 (2015), 421–428.
26. Nikolopoulos, D., Theocharis, S., Kouraklis, G., Ghrelin, another factor affecting bone metabolism. Med. Sci. Monit. 16 (2010), RA147–RA162.
27. Pytel, P., Alexander, J.J., Pathogenesis of septic encephalopathy. Curr. Opin. Neurol. 22 (2009), 283–287.
28. Rajaram, M.V., Ganesan, L.P., Parsa, K.V., Butchar, J.P., Gunn, J.S., Tridandapani, S., Akt/Protein kinase B modulates macrophage inflammatory response to Francisella infection and confers a survival advantage in mice. J. Immunol. 177 (2006), 6317–6324.
29. Reho, J.J., Zheng, X., Asico, L.D., Fisher, S.A., Redox signaling and splicing dependent change in myosin phosphatase underlie early versus late changes in NO vasodilator reserve in a mouse LPS model of sepsis. Am. J. Physiol. Heart Circ. Physiol. 308 (2015), H1039–H1050.
30. Riedemann, N.C., Guo, R.F., Ward, P.A., Novel strategies for the treatment of sepsis. Nat. Med. 9 (2003), 517–524.
31. Savva, A., Roger, T., Targeting toll-like receptors: promising therapeutic strategies for the management of sepsis-associated pathology and infectious diseases. Front. Immunol., 4, 2013, 387.
32. Sharief, M.K., Thompson, E.J., In vivo relationship of tumor necrosis factor-alpha to blood-brain barrier damage in patients with active multiple sclerosis. J. Neuroimmunol. 38 (1992), 27–33.
33. Spencer, S.J., Miller, A.A., Andrews, Z.B., The role of ghrelin in neuroprotection after ischemic brain injury. Brain Sci. 3 (2013), 344–359.
34. Srinivasan, V., Pandi-Perumal, S.R., Spence, D.W., Kato, H., Cardinali, D.P., Melatonin in septic shock: some recent concepts. J. Crit. Care 25 (2010), e651–e656 656.
35. Wang, H.E., Shapiro, N.I., Angus, D.C., Yealy, D.M., National estimates of severe sepsis in United States emergency departments. Crit. Care Med. 35 (2007), 1928–1936.
36. Wang, H., Hong, L.J., Huang, J.Y., Jiang, Q., Tao, R.R., Tan, C., Lu, N.N., Wang, C.K., Ahmed, M.M., Lu, Y.M., Liu, Z.R., Shi, W.X., Lai, E.Y., Wilcox, C.S., Han, F., P2RX7 sensitizes Mac-1/ICAM-1-dependent leukocyte-endothelial adhesion and promotes neurovascular injury during septic encephalopathy. Cell Res. 25 (2015), 674–690.
37. Wang, S.Y., Li, Z.J., Wang, X., Li, W.F., Lin, Z.F., Effect of ulinastatin on HMGB1 expression in rats with acute lung injury induced by sepsis. Genet. Mol. Res. 14 (2015), 4344–4353.
38. Wei, H., Cao, X., Zeng, Q., Zhang, F., Xue, Q., Luo, Y., Lee, J.W., Yu, B., Feng, X., Ghrelin inhibits proinflammatory responses and prevents cognitive impairment in septic rats. Crit. Care Med. 43 (2015), e143–150.
39. Xu, J., Wang, S., Lin, Y., Cao, L., Wang, R., Chi, Z., Ghrelin protects against cell death of hippocampal neurons in pilocarpine-induced seizures in rats. Neurosci. Lett. 453 (2009), 58–61.
40. Xu, L., Cao, F., Xu, F., He, B., Dong, Z., Bexarotene reduces blood-brain barrier permeability in cerebral ischemia-reperfusion injured rats. PLoS One, 10, 2015, e0122744.
41. Zhang, W.J., Wei, H., Hagen, T., Frei, B., Alpha-lipoic acid attenuates LPS-induced inflammatory responses by activating the phosphoinositide 3-kinase/Akt signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 104 (2007), 4077–4082.
42. Zhang, Q.H., Sheng, Z.Y., Yao, Y.M., Septic encephalopathy: when cytokines interact with acetylcholine in the brain. Mil. Med. Res., 1, 2014, 20.
43. de Souza Costa, M.F., Bastos Trigo de Negreiros, C., Ugarte Bornstein, V., Hemmi Valente, R., Mengel, J., Henriques, M., Farias Benjamim, C., Penido, C., Murine IL-17(+) Vgamma4 T lymphocytes accumulate in the lungs and play a protective role during severe sepsis. BMC Immunol., 16, 2015, 36.