Both JNK and P38 MAPK pathways participate in the protection by dexmedetomidine against isoflurane-induced neuroapoptosis in the hippocampus of neonatal rats

Brain Research Bulletin

Volumn 107, Issue , 2014, Pages 69-78

  Liao, Zhaoxia ^a   Cao, Dexiong ^a   Han, Xue ^a   Liu, Chuiliang ^b   Peng, Jun ^a   Zuo, Zhiyi ^a,c   Wang, Fei ^a   Li, Yujuan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b Department of Anesthesiology ChanCheng Center Hospital   (China)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Apoptosis; Caspase 3; Dexmedetomidine; Isoflurane; Mitogen activated protein kinase (MAPK)

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE 3; DEXMEDETOMIDINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOFLURANE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; PROTEIN BCL 2; STRESS ACTIVATED PROTEIN KINASE; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HIPPOCAMPUS; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; METABOLISM; NERVE CELL; NEWBORN; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; DEXMEDETOMIDINE; HIPPOCAMPUS; ISOFLURANE; MAP KINASE KINASE 4; NEURONS; NEUROPROTECTIVE AGENTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84904901200     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2014.07.001     Document Type: Article

References (46)

1. Bamji-Mirza M., Callaghan D., Najem D., Shen S., Hasim M.S., Yang Z., Zhang W. Stimulation of insulin signaling and inhibition of JNK-AP1 activation protect cells from amyloid-β-induced signaling dysregulation and inflammatory response. J. Alzheimer's Dis. 2014, 40:105-122.
2. Brambrink A.M., Evers A.S., Avidan M.S., Farber N.B., Smith D.J., Zhang X., Dissen G.A., Creeley C.E., Olney J.W. Isoflurane-induced neuroapoptosis in the neonatal rhesus macaque brain. Anesthesiology 2010, 112:834-841.
3. Brosnan H., Bickler P.E. Xenon neurotoxicity in rat hippocampal slice cultures is similar to isoflurane and sevoflurane. Anesthesiology 2013, 119:335-344.
4. Cao L., Li L., Lin D., Zuo Z. Isoflurane induces learning impairment that is mediated by interleukin 1β in rodents. PLoS ONE 2012, 7:e51431.
5. Cheng Y., Levy R.J. Subclinical carbon monoxide limits apoptosis in the developing brain after isoflurane exposure. Anesth. Analg. 2014, [Epub ahead of print].
6. DiMaggio C., Sun L.S., Li G. Early childhood exposure to anesthesia and risk of developmental and behavioral disorders in a sibling birth cohort. Anesth. Analg. 2011, 113:1143-1151.
7. Du T., Li B., Liu S., Zang P., Prevot V., Hertz L., Peng L. ERK phosphorylation in intact, adult brain by alpha(2)-adrenergic transactivation of EGF receptors. Neurochem. Int. 2009, 55:593-600.
8. Guan Q.H., Pei D.S., Zhang Q.G., Hao Z.B., Xu T.L., Zhang G.Y. The neuroprotective action of SP600125, a new inhibitor of JNK, on transient brain ischemia/reperfusion-induced neuronal death in rat hippocampal CA1 via nuclear and non-nuclear pathways. Brain Res. 2005, 1035:51-59.
9. Guan Q.H., Pei D.S., Zong Y.Y., Xu T.L., Zhang G.Y. Neuroprotection against ischemic brain injury by a small peptide inhibitor of c-Jun N-terminal kinase (JNK) via nuclear and non-nuclear pathways. Neuroscience 2008, 139:609-627.
10. Han J.Y., Jeong E.Y., Kim Y.S., Roh G.S., Kim H.J., Kang S.S., Cho G.J., Choi W.S. C-jun N-terminal kinase regulates the interaction between 14-3-3 and Bad in ethanol-induced cell death. J. Neurosci. Res. 2008, 86:3221-3229.
11. Harper S.J., Wilkie N. MAPKs: new targets for neurodegeneration. Expert Opin. Ther. Targets 2003, 7:187-200.
12. Ing C., DiMaggio C., Whitehouse A., Hegarty M.K., Brady J., von Ungern-Sternberg B.S., Davidson A., Wood A.J., Li G., Sun L.S. Long-term differences in language and cognitive function after childhood exposure to anesthesia. Pediatrics 2012, 130:e476-e485.
13. Jevtovic-Todorovic V., Hartman R.E., Izumi Y., Benshoff N.D., Dikranian K., Zorumski C.F., Olney J.W., Wozniak D.F. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J. Neurosci. 2003, 23:876-882.
14. Ji R.R., Gereau R.W., Malcangio M., Strichartz G.R. MAP kinase and pain. Brain Res. Rev. 2009, 60:135-148.
15. Kaminska B., Gozdz A., Zawadzka M., Ellert-Miklaszewska A., Lipko M. MAPK signal transduction underlying brain inflammation and gliosis as therapeutic target. Anat. Rec. (Hoboken) 2009, 292:1902-1913.
16. Kim Y.J., Hwang S.Y., Oh E.S., Oh S., Han I.O. IL-1beta, an immediate early protein secreted by activated microglia, induces iNOS/NO in C6 astrocytoma cells through p38 MAPK and NF-kappaB pathways. J. Neurosci. Res. 2006, 84:1037-1046.
17. Kong F., Xu L., He D., Zhang X., Lu H. Effects of gestational isoflurane exposure on postnatal memory and learning in rats. Eur. J. Pharmacol. 2011, 670:168-174.
18. Li B., Du T., Li H., Gu L., Zhang H., Huang J., Hertz L., Peng L. Signaling pathways for transactivation by dexmedetomidine of epidermal growth factor receptors in astrocytes and its paracrine effect on neurons. Br. J. Pharmacol. 2008, 154:191-203.
19. Li Y., Liu C., Zhao Y., Hu K., Zhang J., Zeng M., Luo T., Jiang W., Wang H. Sevoflurane induces short-term changes in proteins in the cerebral cortices of developing rats. Acta Anaesthesiol. Scand. 2013, 57:380-390.
20. Li Y., Wang F., Liu C., Zeng M., Han X., Luo T., Jiang W., Xu J., Wang H. JNK pathway may be involved in isoflurane-induced apoptosis in the hippocampi of neonatal rats. Neurosci. Lett. 2013, 545:17-22.
21. Li Y., Zeng M., Chen W., Liu C., Wang F., Han X., Zuo Z., Peng S. Dexmedetomidine reduces isoflurane-induced neuroapoptosis partly by preserving PI3K/Akt pathway in the hippocampus of neonatal rats. PLOS ONE 2014, 9:e93639.
22. Li Z.Q., Rong X.Y., Liu Y.J., Ni C., Tian X.S., Mo N., Chui D.H., Guo X.Y. Activation of the canonical nuclear factor-κB pathway is involved in isoflurane-induced hippocampal interleukin-1β elevation and the resultant cognitive deficits in aged rats. Biochem. Biophys. Res. Commun. 2013, 438:628-634.
23. Lin D., Zuo Z. Isoflurane induces hippocampal cell injury and cognitive impairments in adult rats. Neuropharmacology 2011, 61:1354-1359.
24. Liu L., Ji F., Liang J., He H., Fu Y., Cao M. Inhibition by dexmedetomidine of the activation of spinal dorsal horn glias and the intracellular ERK signaling pathway induced by nerve injury. Brain Res. 2012, 1427:1-9.
25. Ma D., Williamson P., Januszewski A., Nogaro M.C., Hossain M., Ong L.P., Shu Y., Franks N.P., Maze M. Xenon mitigates isoflurane-induced neuronal apoptosis in the developing rodent brain. Anesthesiology 2007, 106:746-753.
26. Mazoti M., Braz A., de Assis Golim M.G., Braz M., Dias L.G., Salvadori N.H., Braz D.M., Fecchio J.R.D. Comparison of inflammatory cytokine profiles in plasma of patients undergoing otorhinological surgery with propofol or isoflurane anesthesia. Inflamm. Res. 2013, 62:879-885.
27. Mousa A., Bakhiet M. Role of cytokine signaling during nervous system development. Int. J. Mol. Sci. 2013, 14:13931-13957.
28. Nijboer C.H., Bonestroo H.J., Zijlstra J., Kavelaars A., Heijnen C.J. Mitochondrial JNK phosphorylation as a novel therapeutic target to inhibit neuroinflammation and apoptosis after neonatal ischemic brain damage. Neurobiol. Dis. 2013, 54:432-444.
29. Orliaguet G., Vivien B., Langeron O., Bouhemad B., Coriat P., Riou B. Minimum alveolar concentration of volatile anesthetics in rats during postnatal maturation. Anesthesiology 2001, 95:34-39.
30. Paris A., Mantz J., Tonner P.H., Hein L., Brede M., Gressens P. The effects of dexmedetomidine on perinatal excitotoxic brain injury are mediated by the alpha2A-adrenoceptor subtype. Anesth. Analg. 2006, 102:456-461.
31. Paxinos G., Tork I., Teccot L.H., Valentino K. Atlas of the Developing Rat Brain 1990, Academic Press.
32. Sanders R.D., Sun P., Patel S., Li M., Maze M., Ma D. Dexmedetomidine provides cortical neuroprotection: impact on anaesthetic-induced neuroapoptosis in the rat developing brain. Acta Anaesthesiol. Scand. 2010, 54:710-716.
33. Sanders R.D., Xu J., Shu Y., Januszewski A., Halder S., Fidalgo A., Sun P., Hossain M., Ma D., Maze M. Dexmedetomidine attenuates isoflurane-induced neurocognitive impairment in neonatal rats. Anesthesiology 2009, 110:1077-1085.
34. Satomoto M., Satoh Y., Terui K., Miyao H., Takishima K., Ito M., Imaki J. Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 2009, 110:628-637.
35. Shen X., Dong Y., Xu Z., Wang H., Miao C., Soriano S.G., Sun D., Baxter M.G., Zhang Y., Xie Z. Selective anesthesia-induced neuroinflammation in developing mouse brain and cognitive impairment. Anesthesiology 2013, 118:502-515.
36. Shu Y., Patel S.M., Pac-Soo C., Fidalgo A.R., Wan Y., Maze M., Ma D. Xenon pretreatment attenuates anesthetic-induced apoptosis in the developing brain in comparison with nitrous oxide and hypoxia. Anesthesiology 2010, 113:360-368.
37. Shu Y., Zhou Z., Wan Y., Sanders R.D., Li M., Pac-Soo C.K., Maze M., Ma D. Nociceptive stimuli enhance anesthetic-induced neuroapoptosis in the rat developing brain. Neurobiol. Dis. 2012, 45:743-750.
38. Schoeler M., Loetscher P.D., Rossaint R., Fahlenkamp A.V., Eberhardt G., Rex S., Weis J., Coburn M. Dexmedetomidine is neuroprotective in an in vitro model for traumatic brain injury. BMC Neurol. 2012, 12:20.
39. Tachibana K.1., Hashimoto T., Kato R., Uchida Y., Ito R., Takita K., Morimoto Y. Neonatal administration with dexmedetomidine does not impair the rat hippocampal synaptic plasticity later in adulthood. Pediatr. Anaesth. 2012, 22:713-719.
40. Wang L.W., Tu Y.F., Huang C.C., Ho C.J. JNK signaling is the shared pathway linking neuroinflammation, blood-brain barrier disruption, and oligodendroglial apoptosis in the white matter injury of the immature brain. J. Neuroinflamm. 2012, 9:175.
41. Wang W.Y., Yang R., Hu S.F., Wang H., Ma Z.W., Lu Y. N-stearoyl-l-tyrosine ameliorates sevoflurane induced neuroapoptosis via MEK/ERK1/2 MAPK signaling pathway in the developing brain. Neurosci. Lett. 2013, 541:167-172.
42. Wei H., Liang G., Yang H. Isoflurane preconditioning inhibited isoflurane-induced neurotoxicity. Neurosci. Lett. 2007, 425:59-62.
43. Wu X., Lu Y., Dong Y., Zhang G., Zhang Y., Xu Z., Culley D.J., Crosby G., Marcantonio E.R., Tanzi R.E., Xie Z. The inhalation anesthetic isoflurane increases levels of proinflammatory TNF-α, IL-6, and IL-1β. Neurobiol. Aging 2012, 33:1364-1378.
44. Zhang L., Zhang J., Yang L., Dong Y., Zhang Y., Xie Z. Isoflurane and sevoflurane increase interleukin-6 levels through the nuclear factor-kappa B pathway in neuroglioma cells. Br. J. Anaesth. 2013, 110:i82-i91.
45. Zhang X., Wang J., Qian W., Zhao J., Sun L., Qian Y., Xiao H. Dexmedetomidine inhibits tumor necrosis factor-Alpha and interleukin 6 in lipopolysaccharide-stimulated astrocytes by suppression of c-Jun N-terminal kinases. Inflammation 2014, [Epub ahead of print].
46. Zheng S., Zuo Z. Isoflurane preconditioning induces neuroprotection against ischemia via activation of P38 mitogen-activated protein kinases. Mol. Pharmacol. 2004, 65:1172-1180.