ESE1 is Associated with Neuronal Apoptosis in Lipopolysaccharide Induced Neuroinflammation

Overview

Journal Neurochem Res

Specialties Chemistry
Neurology

Date 2016 Jun 29

PMID 27350582

Citations 6

Authors

Yi Feng

Huaqing Xue

Jie Zhu

Likun Yang

Feng Zhang

Rong Qian

Wei Lin

Yuhai Wang

Affiliations

Soon will be listed here.

Abstract

Neuronal apoptosis induced by the over-activation of microglia during neuroinflammation contributes to the pathology of central nervous system (CNS) degenerative diseases. ESE1 regulates apoptosis of intestinal epithelial cells in ulcerative colitis via accelerating NF-κB activation. NF-κB activation participates in neuronal apoptosis. However, the expression and functions of ESE1 in neuronal apoptosis during CNS inflammatory response remain unclear. In present study, ESE1 expression significantly increased in cerebral cortex after lipopolysaccharide (LPS) intracerebroventricular injection. Immunofluorescence staining indicated that ESE1 was located in neurons. Furthermore, there was a concomitant up-regulation of apoptotic markers including active caspase-3, BAX and decreased expression of anti-apoptosis protein Bcl-2. In vitro, ESE1 depletion in cortical primary neurons inhibited active caspase-3 and BAX expression as well as lactate dehydrogenase (LDH) release with up-regulation of Bcl-2, while ESE1 overexpression can exert opposite effects, indicating that ESE1 promoted neuronal apoptosis induced by LPS or LPS exposed microglia conditioned media (CM). ESE1 accelerated NF-κB activation in neurons with CM treatment. Collectively, all these data suggested that ESE1 might boost neuronal apoptosis during neuroinflammation via up-regulating NF-κB activation. These findings have implications on the potential target of ESE1 in CNS inflammation treatment.

Citing Articles

Transcription factor ETS proto-oncogene 1 contributes to neuropathic pain by regulating histone deacetylase 1 in primary afferent neurons.

Zheng H, Sun S, Jin T, Zhang M, Zeng Y, Liu Q Mol Pain. 2023; 19:17448069231152125.

PMID: 36604795 PMC: 9909074. DOI: 10.1177/17448069231152125.

Postconditioning with Sevoflurane or Propofol Alleviates Lipopolysaccharide-Induced Neuroinflammation but Exerts Dissimilar Effects on the NR2B Subunit and Cognition.

Liu H, Chen B, Guo B, Deng X, Wang B, Dou X Mol Neurobiol. 2021; 58(9):4251-4267.

PMID: 33970453 DOI: 10.1007/s12035-021-02402-0.

ESE1 expression correlates with neuronal apoptosis in the hippocampus after cerebral ischemia/reperfusion injury.

Yu H, Wang L, Zhang L, Chen B, Zhang H, Li Y Neural Regen Res. 2019; 14(5):841-849.

PMID: 30688270 PMC: 6375036. DOI: 10.4103/1673-5374.249232.

Gestational Exposure to Particulate Matter 2.5 (PM) Leads to Spatial Memory Dysfunction and Neurodevelopmental Impairment in Hippocampus of Mice Offspring.

Zheng X, Wang X, Wang T, Zhang H, Wu H, Zhang C Front Neurosci. 2019; 12:1000.

PMID: 30666183 PMC: 6330280. DOI: 10.3389/fnins.2018.01000.

Tart Cherry Extracts Reduce Inflammatory and Oxidative Stress Signaling in Microglial Cells.

Shukitt-Hale B, Kelly M, Bielinski D, Fisher D Antioxidants (Basel). 2016; 5(4).

PMID: 27669317 PMC: 5187531. DOI: 10.3390/antiox5040033.

References

Hu Q, Li B, Xu R, Chen D, Mu C, Fei E . The protease Omi cleaves the mitogen-activated protein kinase kinase MEK1 to inhibit microglial activation. Sci Signal. 2012; 5(238):ra61. DOI: 10.1126/scisignal.2002946. View

Rudders S, Gaspar J, Madore R, Voland C, Grall F, Patel A . ESE-1 is a novel transcriptional mediator of inflammation that interacts with NF-kappa B to regulate the inducible nitric-oxide synthase gene. J Biol Chem. 2000; 276(5):3302-9. DOI: 10.1074/jbc.M006507200. View

Longoni N, Sarti M, Albino D, Civenni G, Malek A, Ortelli E . ETS transcription factor ESE1/ELF3 orchestrates a positive feedback loop that constitutively activates NF-κB and drives prostate cancer progression. Cancer Res. 2013; 73(14):4533-47. DOI: 10.1158/0008-5472.CAN-12-4537. View

Yamashima T . Hsp70.1 and related lysosomal factors for necrotic neuronal death. J Neurochem. 2011; 120(4):477-94. DOI: 10.1111/j.1471-4159.2011.07596.x. View

Wu J, Duan R, Cao H, Field D, Newnham C, Koehler D . Regulation of epithelium-specific Ets-like factors ESE-1 and ESE-3 in airway epithelial cells: potential roles in airway inflammation. Cell Res. 2008; 18(6):649-63. PMC: 4494831. DOI: 10.1038/cr.2008.57. View

Cai Y, Cho G, Ju C, Wang S, Ryu J, Shin C . Activated microglia are less vulnerable to hemin toxicity due to nitric oxide-dependent inhibition of JNK and p38 MAPK activation. J Immunol. 2011; 187(3):1314-21. DOI: 10.4049/jimmunol.1002925. View

Depino A . Peripheral and central inflammation in autism spectrum disorders. Mol Cell Neurosci. 2012; 53:69-76. DOI: 10.1016/j.mcn.2012.10.003. View

Ellwardt E, Zipp F . Molecular mechanisms linking neuroinflammation and neurodegeneration in MS. Exp Neurol. 2014; 262 Pt A:8-17. DOI: 10.1016/j.expneurol.2014.02.006. View

Zhu X, Wang K, Zhang K, Tan X, Wu Z, Sun S . Tetramethylpyrazine Protects Retinal Capillary Endothelial Cells (TR-iBRB2) against IL-1β-Induced Nitrative/Oxidative Stress. Int J Mol Sci. 2015; 16(9):21775-90. PMC: 4613279. DOI: 10.3390/ijms160921775. View

10.

Zhan Y, Yuan L, Kondo M, Oettgen P . The counter-regulatory effects of ESE-1 during angiotensin II-mediated vascular inflammation and remodeling. Am J Hypertens. 2010; 23(12):1312-7. PMC: 3715883. DOI: 10.1038/ajh.2010.164. View

11.

Gao H, Zhou H, Zhang F, Wilson B, Kam W, Hong J . HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci. 2011; 31(3):1081-92. PMC: 3046932. DOI: 10.1523/JNEUROSCI.3732-10.2011. View

12.

Morales I, Guzman-Martinez L, Cerda-Troncoso C, Farias G, Maccioni R . Neuroinflammation in the pathogenesis of Alzheimer's disease. A rational framework for the search of novel therapeutic approaches. Front Cell Neurosci. 2014; 8:112. PMC: 4001039. DOI: 10.3389/fncel.2014.00112. View

13.

Grall F, Prall W, Wei W, Gu X, Cho J, Choy B . The Ets transcription factor ESE-1 mediates induction of the COX-2 gene by LPS in monocytes. FEBS J. 2005; 272(7):1676-87. DOI: 10.1111/j.1742-4658.2005.04592.x. View

14.

Kuan C, Whitmarsh A, Yang D, Liao G, Schloemer A, Dong C . A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci U S A. 2003; 100(25):15184-9. PMC: 299947. DOI: 10.1073/pnas.2336254100. View

15.

Grall F, Gu X, Tan L, Cho J, Inan M, Pettit A . Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1. Arthritis Rheum. 2003; 48(5):1249-60. DOI: 10.1002/art.10942. View

16.

Miyamoto A, Wake H, Moorhouse A, Nabekura J . Microglia and synapse interactions: fine tuning neural circuits and candidate molecules. Front Cell Neurosci. 2013; 7:70. PMC: 3654203. DOI: 10.3389/fncel.2013.00070. View

17.

Choi W, Klintworth H, Xia Z . JNK3-mediated apoptotic cell death in primary dopaminergic neurons. Methods Mol Biol. 2011; 758:279-92. PMC: 3490420. DOI: 10.1007/978-1-61779-170-3_19. View

18.

Akhter R, Sanphui P, Das H, Saha P, Biswas S . The regulation of p53 up-regulated modulator of apoptosis by JNK/c-Jun pathway in β-amyloid-induced neuron death. J Neurochem. 2015; 134(6):1091-103. DOI: 10.1111/jnc.13128. View

19.

Ren D, Tu H, Kim H, Wang G, Bean G, Takeuchi O . BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science. 2010; 330(6009):1390-3. PMC: 3163443. DOI: 10.1126/science.1190217. View

20.

Whitfield J, Neame S, Paquet L, Bernard O, Ham J . Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron. 2001; 29(3):629-43. DOI: 10.1016/s0896-6273(01)00239-2. View