Nuclear factor-κB/Bcl-XL pathway is involved in the protective effect of hydrogen-rich saline on the brain following experimental subarachnoid hemorrhage in rabbits

Journal of Neuroscience Research

Volumn 91, Issue 12, 2013, Pages 1599-1608

  Zhuang, Zong ^a   Sun, Xue Jun ^b   Zhang, Xing ^a   Liu, Huan Dong ^c   You, Wan Chun ^a   Ma, Chi Yuan ^a   Zhu, Lin ^a   Zhou, Meng liang ^a   Shi, Ji Xin ^a  

^a NANJING UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Early brain injury; Hydrogen; NF B Bcl xL; Subarachnoid hemorrhage

Indexed keywords

CASPASE 3; HYDROGEN; HYDROGEN RICH SALINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL XL; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN INJURY; CONTROLLED STUDY; DISEASE SEVERITY; EARLY BRAIN INJURY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNOFLUORESCENCE; MALE; NERVE CELL LESION; NEUROPROTECTION; NICK END LABELING; NISSL STAINING; NONHUMAN; OCCIPITAL CORTEX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SUBARACHNOID HEMORRHAGE; WESTERN BLOTTING;

APOPTOSIS; EARLY BRAIN INJURY; HYDROGEN; NF-ΚB/BCL-XL; SUBARACHNOID HEMORRHAGE;

ANIMALS; APOPTOSIS; BCL-X PROTEIN; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HYDROGEN; IN SITU NICK-END LABELING; MALE; NEUROPROTECTIVE AGENTS; NF-KAPPA B; RABBITS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; SUBARACHNOID HEMORRHAGE;

EID: 84886640538     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23281     Document Type: Article

References (57)

1. Barkett M, Gilmore TD. 1999. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18:6910-6924.
2. Bederson JB, Germano IM, Guarino L. 1995. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 26:1086-1091; discussion 1091-1082.
3. Bederson JB, Connolly ES Jr, Batjer HH, Dacey RG, Dion JE, Diringer MN, Duldner JE Jr, Harbaugh RE, Patel AB, Rosenwasser RH. 2009. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 40:994-1025.
4. Beg AA, Baltimore D. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274:782-784.
5. Buchholz BM, Kaczorowski DJ, Sugimoto R, Yang R, Wang Y, Billiar TR, McCurry KR, Bauer AJ, Nakao A. 2008. Hydrogen inhalation ameliorates oxidative stress in transplantation induced intestinal graft injury. Am J Transplant 8:2015-2024.
6. Burstein E, Duckett CS. 2003. Dying for NF-kappaB? Control of cell death by transcriptional regulation of the apoptotic machinery. Curr Opin Cell Biol 15:732-737.
7. Cahill J, Zhang JH. 2009. Subarachnoid hemorrhage: is it time for a new direction? Stroke 40(Suppl):S86-S87.
8. Cahill J, Calvert JW, Zhang JH. 2006. Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 26:1341-1353.
9. Cahill J, Calvert JW, Marcantonio S, Zhang JH. 2007. p53 May play an orchestrating role in apoptotic cell death after experimental subarachnoid hemorrhage. Neurosurgery 60:531-545; discussion 545.
10. Cai J, Kang Z, Liu K, Liu W, Li R, Zhang JH, Luo X, Sun X. 2009. Neuroprotective effects of hydrogen saline in neonatal hypoxia-ischemia rat model. Brain Res 1256:129-137.
11. Chen C, Edelstein LC, Gelinas C. 2000. The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol Cell Biol 20:2687-2695.
12. Chen C, Chen Q, Mao Y, Xu S, Xia C, Shi X, Zhang JH, Yuan H, Sun X. 2010. Hydrogen-rich saline protects against spinal cord injury in rats. Neurochem Res 35:1111-1118.
13. Crowley RW, Medel R, Dumont AS, Ilodigwe D, Kassell NF, Mayer SA, Ruefenacht D, Schmiedek P, Weidauer S, Pasqualin A, Macdonald RL. 2011. Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke 42:919-923.
14. Du Y, Dodel RC, Bales KR, Jemmerson R, Hamilton-Byrd E, Paul SM. 1997. Involvement of a caspase-3-like cysteine protease in 1-methyl-4-phenylpyridinium-mediated apoptosis of cultured cerebellar granule neurons. J Neurochem 69:1382-1388.
15. Duckett CS, Li F, Wang Y, Tomaselli KJ, Thompson CB, Armstrong RC. 1998. Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Mol Cell Biol 18:608-615.
16. Glasgow JN, Wood T, Perez-Polo JR. 2000. Identification and characterization of nuclear factor kappaB binding sites in the murine bcl-x promoter. J Neurochem 75:1377-1389.
17. Greenlund LJ, Deckwerth TL, Johnson EM Jr. 1995. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14:303-315.
18. Gutierrez H, Hale VA, Dolcet X, Davies A. 2005. NF-kappaB signalling regulates the growth of neural processes in the developing PNS and CNS. Development 132:1713-1726.
19. Hamanoue M, Middleton G, Wyatt S, Jaffray E, Hay RT, Davies AM. 1999. p75-Mediated NF-kappaB activation enhances the survival response of developing sensory neurons to nerve growth factor. Mol Cell Neurosci 14:28-40.
20. Hasegawa Y, Suzuki H, Sozen T, Altay O, Zhang JH. 2011. Apoptotic mechanisms for neuronal cells in early brain injury after subarachnoid hemorrhage. Acta Neurochir Suppl 110:43-48.
21. Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, van Crevel H. 1988. Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke 19:1250-1256.
22. Huang CS, Kawamura T, Lee S, Tochigi N, Shigemura N, Buchholz BM, Kloke JD, Billiar TR, Toyoda Y, Nakao A. 2010. Hydrogen inhalation ameliorates ventilator-induced lung injury. Crit Care 14:R234.
23. Huang CS, Kawamura T, Peng X, Tochigi N, Shigemura N, Billiar TR, Nakao A, Toyoda Y. 2011. Hydrogen inhalation reduced epithelial apoptosis in ventilator-induced lung injury via a mechanism involving nuclear factor-kappa B activation. Biochem Biophys Res Commun 408:253-258.
24. Jeon H, Ai J, Sabri M, Tariq A, Shang X, Chen G, Macdonald RL. 2009. Neurological and neurobehavioral assessment of experimental subarachnoid hemorrhage. BMC Neurosci 10:103.
25. Ji Q, Hui K, Zhang L, Sun X, Li W, Duan M. 2011. The effect of hydrogen-rich saline on the brain of rats with transient ischemia. J Surg Res 168:e95-e101.
26. Kaltschmidt B, Heinrich M, Kaltschmidt C. 2002. Stimulus-dependent activation of NF-kappaB specifies apoptosis or neuroprotection in cerebellar granule cells. Neuromol Med 2:299-309.
27. Kawamura T, Huang CS, Tochigi N, Lee S, Shigemura N, Billiar TR, Okumura M, Nakao A, Toyoda Y. 2010. Inhaled hydrogen gas therapy for prevention of lung transplant-induced ischemia/reperfusion injury in rats. Transplantation 90:1344-1351.
28. Koulich E, Nguyen T, Johnson K, Giardina C, D'Mello S. 2001. NF-kappaB is involved in the survival of cerebellar granule neurons: association of IkappaBbeta [correction of Ikappabeta] phosphorylation with cell survival. J Neurochem 76:1188-1198.
29. Labiche LA, Grotta JC. 2004. Clinical trials for cytoprotection in stroke. NeuroRx 1:46-70.
30. Li W, Liu HD, You WC, Zhou ML, Ling HP, Shen W, Zhu L, Hang CH. 2012. Enhanced cortical expression of myeloid differentiation primary response protein 88 (Myd88) in patients with traumatic brain injury. J Surg Res (in press).
31. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-157.
32. Mao YF, Zheng XF, Cai JM, You XM, Deng XM, Zhang JH, Jiang L, Sun XJ. 2009. Hydrogen-rich saline reduces lung injury induced by intestinal ischemia/reperfusion in rats. Biochem Biophys Res Commun 381:602-605.
33. Mattson MP, Meffert MK. 2006. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 13:852-860.
34. Meyers PM, Connolly ES Jr. 2011. Stroke: disappointing results for clazosentan in CONSCIOUS-2. Nat Rev Neurol 7:660-661.
35. Nau R, Haase S, Bunkowski S, Bruck W. 2002. Neuronal apoptosis in the dentate gyrus in humans with subarachnoid hemorrhage and cerebral hypoxia. Brain Pathol 12:329-336.
36. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S. 2007. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13:688-694.
37. Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH. 2004. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke 35:2412-2417.
38. Piccioli P, Porcile C, Stanzione S, Bisaglia M, Bajetto A, Bonavia R, Florio T, Schettini G. 2001. Inhibition of nuclear factor-kappaB activation induces apoptosis in cerebellar granule cells. J Neurosci Res 66:1064-1073.
39. Pizzi M, Spano P. 2006. Distinct roles of diverse nuclear factor-kappaB complexes in neuropathological mechanisms. Eur J Pharmacol 545:22-28.
40. Pizzi M, Goffi F, Boroni F, Benarese M, Perkins SE, Liou HC, Spano P. 2002. Opposing roles for NF-kappa B/Rel factors p65 and c-Rel in the modulation of neuron survival elicited by glutamate and interleukin-1beta. J Biol Chem 277:20717-20723.
41. Prunell GF, Mathiesen T, Diemer NH, Svendgaard NA. 2003. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery 52:165-175; discussion 175-166.
42. Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. 2005. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg 102:1046-1054.
43. Sehba FA, Bederson JB. 2006. Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res 28:381-398.
44. Shingu C, Koga H, Hagiwara S, Matsumoto S, Goto K, Yokoi I, Noguchi T. 2010. Hydrogen-rich saline solution attenuates renal ischemia-reperfusion injury. J Anesthesiol 24:569-574.
45. Simard JM, Geng Z, Woo SK, Ivanova S, Tosun C, Melnichenko L, Gerzanich V. 2009. Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J Cereb Blood Flow Metab 29:317-330.
46. Taglialatela G, Robinson R, Perez-Polo JR. 1997. Inhibition of nuclear factor kappa B (NFkappaB) activity induces nerve growth factor-resistant apoptosis in PC12 cells. J Neurosci Res 47:155-162.
47. Tamatani M, Che YH, Matsuzaki H, Ogawa S, Okado H, Miyake S, Mizuno T, Tohyama M. 1999. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem 274:8531-8538.
48. Tamatani M, Mitsuda N, Matsuzaki H, Okado H, Miyake S, Vitek MP, Yamaguchi A, Tohyama M. 2000. A pathway of neuronal apoptosis induced by hypoxia/reoxygenation: roles of nuclear factor-kappaB and Bcl-2. J Neurochem 75:683-693.
49. Tsukahara T, Kannagi M, Ohashi T, Kato H, Arai M, Nunez G, Iwanaga Y, Yamamoto N, Ohtani K, Nakamura M, Fujii M. 1999. Induction of Bcl-x(L) expression by human T-cell leukemia virus type 1 Tax through NF-kappaB in apoptosis-resistant T-cell transfectants with Tax. J Virol 73:7981-7987.
50. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM. 1996. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274:787-789.
51. van Gijn J, Rinkel GJ. 2001. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 124:249-278.
52. Wang C, Li J, Liu Q, Yang R, Zhang JH, Cao YP, Sun XJ. 2011a. Hydrogen-rich saline reduces oxidative stress and inflammation by inhibit of JNK and NF-kappaB activation in a rat model of amyloid-beta-induced Alzheimer's disease. Neurosci Lett 491:127-132.
53. Wang Z, Zuo G, Shi XY, Zhang J, Fang Q, Chen G. 2011b. Progesterone administration modulates cortical TLR4/NF-kappaB signaling pathway after subarachnoid hemorrhage in male rats. Mediators Inflamm 2011:848309.
54. You WC, Li W, Zhuang Z, Tang Y, Lu HC, Ji XJ, Shen W, Shi JX, Zhou ML. 2012. Biphasic activation of nuclear factor-kappa B in experimental models of subarachnoid hemorrhage in vivo and in vitro. Mediators Inflamm 2012:786242.
55. Zhou ML, Shi JX, Zhu JQ, Hang CH, Mao L, Chen KF, Yin HX. 2007. Comparison between one- and two-hemorrhage models of cerebral vasospasm in rabbits. J Neurosci Methods 159:318-324.
56. Zhuang Z, Zhao X, Wu Y, Huang R, Zhu L, Zhang Y, Shi J. 2011. The anti-apoptotic effect of PI3K-Akt signaling pathway after subarachnoid hemorrhage in rats. Ann Clin Lab Sci 41:364-372.
57. Zhuang Z, Zhou ML, You WC, Zhu L, Ma CY, Sun XJ, Shi JX. 2012. Hydrogen-rich saline alleviates early brain injury via reducing oxidative stress and brain edema following experimental subarachnoid hemorrhage in rabbits. BMC Neurosci 13:47.