Bax inhibitor-1 suppresses early brain injury following experimental subarachnoid hemorrhage in rats Corrigendum in /10.3892/ijmm.2024.5362

Liu,Jiaxin; Zhou,Shuai; Zhang,Yueting; Li,Xiuying; Qian,Xiying; Tao,Weihua; Jin,Lide; Zhao,Jianhua

doi:10.3892/ijmm.2018.3858

Bax inhibitor-1 suppresses early brain injury following experimental subarachnoid hemorrhage in rats

Corrigendum in: /10.3892/ijmm.2024.5362

Authors:
- Jiaxin Liu
- Shuai Zhou
- Yueting Zhang
- Xiuying Li
- Xiying Qian
- Weihua Tao
- Lide Jin
- Jianhua Zhao
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Affiliations: Department of Environmental Science, Faculty of Environmental Science and Engineering, Kunming University of Science and Technology, Kunming, Yunnan 650504, P.R. China, Department of Neurosurgery, The First Affiliated Hospital of Kunming University of Science and Technology, Kunming, Yunnan 650032, P.R. China, Very Important Person Ward, The Second Affiliated Hospital of Kunming Medical College, Kunming, Yunnan 650032, P.R. China, Department of Pharmacology, Medical School, Kunming University of Science and Technology, Kunming, Yunnan 650504, P.R. China
Published online on: September 5, 2018 https://doi.org/10.3892/ijmm.2018.3858
Pages: 2891-2902

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Abstract

Early brain injury (EBI) following subarachnoid hemorrhage (SAH) is an important cause of high mortality and poor prognosis in SAH. B‑cell lymphoma 2‑associated X protein inhibitor‑1 (BI‑1) is an evolutionarily conserved antiapoptotic protein that is primarily located in the membranes of endoplasmic reticulum (ER). BI‑1 has been studied in certain nervous system‑associated diseases, but the role of this protein in SAH remains unclear. In the present study, the role of BI‑1 in EBI following SAH was investigated in rat models and its associated mechanisms were examined. The SAH rat model was generated by inserting nylon cords into the internal carotid artery from the external carotid artery. Samples were assessed using neurological scores, brain water content measurements, hematoxylin and eosin (H&E) staining, blood‑brain barrier (BBB) permeability, terminal deoxynucleotidyl transferase‑mediated dUTP nick‑end labeling and quantitative polymerase chain reaction assays, and western blot analyses. It was identified that the mRNA and protein levels of BI‑1 decreased markedly and were lowest at 24 h after SAH. BI‑1 overexpression and small hairpin RNA (shRNA)‑mediated silencing markedly suppressed or severely exacerbated EBI following SAH, respectively. BI‑1 overexpression in the SAH model improved neurological scores and decreased the brain water content, BBB permeability and levels of apoptosis compared with the control and sham groups following SAH. BI‑1 shRNA in the SAH model demonstrated contrary results. In addition, the mRNA or protein expression levels of ER stress‑associated genes (glucose regulated protein, 78 kDa, C/EBP homologous protein, Serine/threonine‑protein kinase/endoribonuclease IRE1, c‑Jun N terminal kinases and apoptotic signaling kinase‑1) were markedly suppressed or increased following BI‑1 overexpression and shRNA‑mediated silencing, respectively. The present study suggested that BI‑1 serves a neuroprotective role in EBI following SAH by attenuating BBB disruption, brain edema and apoptosis mediated by ER stress.

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1	Al-Khindi T, Macdonald RL and Schweizer TA: Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 41:e519–e536. 2010. View Article : Google Scholar : PubMed/NCBI
2	Cahill J, Calvert JW and Zhang JH: Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 26:1341–1353. 2006. View Article : Google Scholar : PubMed/NCBI
3	Ayer R, Chen W, Sugawara T, Suzuki H and Zhang JH: Role of gap junctions in early brain injury following subarachnoid hemorrhage. Brain Res. 1315:150–158. 2010. View Article : Google Scholar :
4	Fujii M, Yan J, Rolland WB, Soejima Y, Caner B and Zhang JH: Early brain injury, an evolving frontier in subarachnoid hemorrhage research. Transl Stroke Res. 4:432–446. 2013. View Article : Google Scholar : PubMed/NCBI
5	Ayer R and Zhang J: Connecting the early brain injury of aneurysmal subarachnoid hemorrhage to clinical practice. Turk Neurosurg. 20:159–166. 2010.PubMed/NCBI
6	Yuksel S, Tosun YB, Cahill J and Solaroglu I: Early brain injury following aneurysmal subarachnoid hemorrhage: Emphasis on cellular apoptosis. Turk Neurosurg. 22:529–533. 2012.PubMed/NCBI
7	Hasegawa Y, Suzuki H, Sozen T, Altay O and Zhang JH: Apoptotic mechanisms for neuronal cells in early brain injury after subarachnoid hemorrhage. Acta Neurochir Suppl. 110:43–48. 2011.
8	Cheng G, Chunlei W, Pei W, Zhen L and Xiangzhen L: Simvastatin activates Akt/glycogen synthase kinase-3beta signal and inhibits caspase-3 activation after experimental subarachnoid hemorrhage. Vascul Pharmacol. 52:77–83. 2010. View Article : Google Scholar
9	Kusaka G, Ishikawa M, Nanda A, Granger DN and Zhang JH: Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 24:916–925. 2004. View Article : Google Scholar : PubMed/NCBI
10	Endo H, Nito C, Kamada H, Yu F and Chan PH: Akt/GSK3beta survival signaling is involved in acute brain injury after subarach-noid hemorrhage in rats. Stroke. 37:2140–2146. 2006. View Article : Google Scholar : PubMed/NCBI
11	Xu Q and Reed JC: Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell. 1:337–346. 1998. View Article : Google Scholar : PubMed/NCBI
12	Chae HJ, Kim HR, Xu C, Bailly-Maitre B, Krajewska M, Krajewski S, Banares S, Cui J, Digicaylioglu M, Ke N, et al: BI-1 regulates an apoptosis pathway linked to endoplasmic reticulum stress. Mol Cell. 15:355–366. 2004. View Article : Google Scholar : PubMed/NCBI
13	Bredesen DE, Rao RV and Mehlen P: Cell death in the nervous system. Nature. 443:796–802. 2006. View Article : Google Scholar : PubMed/NCBI
14	Kim I, Xu W and Reed JC: Cell death and endoplasmic reticulum stress: Disease relevance and therapeutic opportunities. Nat Rev Drug Discov. 7:1013–1030. 2008. View Article : Google Scholar : PubMed/NCBI
15	Patil C and Walter P: Intracellular signaling from the endoplasmic reticulum to the nucleus: The unfolded protein response in yeast and mammals. Curr Opin Cell Biol. 13:349–355. 2001. View Article : Google Scholar : PubMed/NCBI
16	Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH and Korsmeyer SJ: Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science. 312:572–576. 2006. View Article : Google Scholar : PubMed/NCBI
17	Szegezdi E, Logue SE, Gorman AM and Samali A: Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 7:880–885. 2006. View Article : Google Scholar : PubMed/NCBI
18	Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A and Ichijo H: ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16:1345–1355. 2002. View Article : Google Scholar : PubMed/NCBI
19	Lei K and Davis RJ: JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA. 100:2432–2437. 2003. View Article : Google Scholar : PubMed/NCBI
20	Krajewska M, Xu L, Xu W, Krajewski S, Kress CL, Cui J, Yang L, Irie F, Yamaguchi Y, Lipton SA and Reed JC: Endoplasmic reticulum protein BI-1 modulates unfolded protein response signaling and protects against stroke and traumatic brain injury. Brain Res. 1370:227–237. 2011. View Article : Google Scholar :
21	Bailly-Maitre B, Fondevila C, Kaldas F, Droin N, Luciano F, Ricci JE, Croxton R, Krajewska M, Zapata JM, Kupiec-Weglinski JW, et al: Cytoprotective gene bi-1 is required for intrinsic protection from endoplasmic reticulum stress and ischemia-reperfusion injury. Proc Natl Acad Sci USA. 103:2809–2814. 2006. View Article : Google Scholar : PubMed/NCBI
22	Lu B, Li Y, Li H, Zhang Y, Xu J, Ren L, Fu S and Zhou Y: Bax inhibitor-1 is overexpressed in non-small cell lung cancer and promotes its progression and metastasis. Int J Clin Exp Pathol. 8:1411–1418. 2015.PubMed/NCBI
23	Grzmil M, Thelen P, Hemmerlein B, Schweyer S, Voigt S, Mury D and Burfeind P: Bax inhibitor-1 is overexpressed in prostate cancer and its specific down-regulation by RNA interference leads to cell death in human prostate carcinoma cells. Am J Pathol. 163:543–552. 2003. View Article : Google Scholar : PubMed/NCBI
24	Bailly-Maitre B, Bard-Chapeau E, Luciano F, Droin N, Bruey JM, Faustin B, Kress C, Zapata JM and Reed JC: Mice lacking bi-1 gene show accelerated liver regeneration. Cancer Res. 67:1442–1450. 2007. View Article : Google Scholar : PubMed/NCBI
25	Bailly-Maitre B, Belgardt BF, Jordan SD, Coornaert B, von Freyend MJ, Kleinridders A, Mauer J, Cuddy M, Kress CL, Willmes D, et al: Hepatic Bax inhibitor-1 inhibits IRE1alpha and protects from obesity-associated insulin resistance and glucose intolerance. J Biol Chem. 285:6198–6207. 2010. View Article : Google Scholar
26	Jeon K, Lim H, Kim JH, Han D, Lee ER, Yang GM, Song MK, Kim JH and Cho SG: Bax inhibitor-1 enhances survival and neuronal differentiation of embryonic stem cells via differential regulation of mitogen-activated protein kinases activities. Biochim Biophys Acta. 1823:2190–2200. 2012. View Article : Google Scholar : PubMed/NCBI
27	Dohm CP, Siedenberg S, Liman J, Esposito A, Wouters FS, Reed JC, Bähr M and Kermer P: Bax inhibitor-1 protects neurons from oxygen-glucose deprivation. J Mol Neurosci. 29:1–8. 2006. View Article : Google Scholar : PubMed/NCBI
28	Prunell GF, Mathiesen T and Svendgaard NA: A new experimental model in rats for study of the pathophysiology of subarachnoid hemorrhage. Neuroreport. 13:2553–2556. 2002. View Article : Google Scholar : PubMed/NCBI
29	Sugawara T, Ayer R, Jadhav V and Zhang JH: A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods. 167:327–334. 2008. View Article : Google Scholar
30	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar
31	Alafuzoff I, Adolfsson R, Bucht G and Winblad B: Albumin and immunoglobulin in plasma and cerebrospinal fluid, and blood-cerebrospinal fluid barrier function in patients with dementia of Alzheimer type and multi-infarct dementia. J Neurol Sci. 60:465–472. 1983. View Article : Google Scholar : PubMed/NCBI
32	Sorjonen DC: Total protein, albumin quota, and electrophoretic patterns in cerebrospinal fluid of dogs with central nervous system disorders. Am J Vet Res. 48:301–305. 1987.PubMed/NCBI
33	Kumar A, Mittal R, Khanna HD and Basu S: Free radical injury and blood-brain barrier permeability in hypoxic-ischemic encephalopathy. Pediatrics. 122:e722–e727. 2008. View Article : Google Scholar : PubMed/NCBI
34	Schmidt-Kastner R, Szymas J and Hossmann KA: Immunohistochemical study of glial reaction and serum-protein extravasation in relation to neuronal damage in rat hippocampus after ischemia. Neuroscience. 38:527–540. 1990. View Article : Google Scholar : PubMed/NCBI
35	Suzuki H: What is early brain injury? Transl Stroke Res. 6:1–3. 2015. View Article : Google Scholar
36	Sehba FA, Hou J, Pluta RM and Zhang JH: The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol. 97:14–37. 2012. View Article : Google Scholar : PubMed/NCBI
37	Hosaka K and Hoh BL: Inflammation and cerebral aneurysms. Transl Stroke Res. 5:190–198. 2014. View Article : Google Scholar
38	Chen S, Yang Q, Chen G and Zhang JH: An update on inflammation in the acute phase of intracerebral hemorrhage. Transl Stroke Res. 6:4–8. 2015. View Article : Google Scholar
39	Sabri M, Kawashima A, Ai J and Macdonald RL: Neuronal and astrocytic apoptosis after subarachnoid hemorrhage: A possible cause for poor prognosis. Brain Res. 1238:163–171. 2008. View Article : Google Scholar : PubMed/NCBI
40	Matz PG, Fujimura M and Chan PH: Subarachnoid hemolysate produces DNA fragmentation in a pattern similar to apoptosis in mouse brain. Brain Res. 858:312–319. 2000. View Article : Google Scholar : PubMed/NCBI
41	Lindholm D, Wootz H and Korhonen L: ER stress and neurodegenerative diseases. Cell Death Differ. 13:385–392. 2006. View Article : Google Scholar : PubMed/NCBI
42	He Z, Ostrowski RP, Sun X, Ma Q, Huang B, Zhan Y and Zhang JH: CHOP silencing reduces acute brain injury in the rat model of subarachnoid hemorrhage. Stroke. 43:484–490. 2012. View Article : Google Scholar :
43	Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA and Marciniak SJ: Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol. 12:105–118. 2013. View Article : Google Scholar
44	Placido AI, Pereira CM, Duarte AI, Candeias E, Correia SC, Carvalho C, Cardoso S, Oliveira CR and Moreira PI: Modulation of endoplasmic reticulum stress: An opportunity to prevent neurodegeneration? CNS Neurol Disord Drug Targets. 14:518–533. 2015. View Article : Google Scholar : PubMed/NCBI
45	Stefani IC, Wright D, Polizzi KM and Kontoravdi C: The role of ER stress-induced apoptosis in neurodegeneration. Curr Alzheimer Res. 9:373–387. 2012. View Article : Google Scholar : PubMed/NCBI
46	McManus MJ, Murphy MP and Franklin JL: Mitochondria-derived reactive oxygen species mediate caspase-dependent and-independent neuronal deaths. Mol Cell Neurosci. 63:13–23. 2014. View Article : Google Scholar : PubMed/NCBI
47	Winklhofer KF and Haass C: Mitochondrial dysfunction in Parkinson's disease. Biochim Biophys Acta. 1802:29–44. 2010. View Article : Google Scholar
48	Itoh K, Nakamura K, Iijima M and Sesaki H: Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 23:64–71. 2013. View Article : Google Scholar :
49	Chen J, Wang L, Wu C, Hu Q, Gu C, Yan F, Li J, Yan W and Chen G: Melatonin-enhanced autophagy protects against neural apoptosis via a mitochondrial pathway in early brain injury following a subarachnoid hemorrhage. J Pineal Res. 56:12–19. 2014. View Article : Google Scholar
50	Liang Y, Che X, Zhao Q, Darwazeh R, Zhang H, Jiang D, Zhao J, Xiang X, Qin W, Liu L and He Z: Thioredoxin-interacting protein mediates mitochondrion-dependent apoptosis in early brain injury after subarachnoid hemorrhage. Mol Cell Biochem. 2018. View Article : Google Scholar