Skip to main content
Top
Published in: Journal of Neuroinflammation 1/2015

Open Access 01-12-2015 | Research

Role of high-mobility group box 1 in methamphetamine-induced activation and migration of astrocytes

Authors: Yuan Zhang, Tiebing Zhu, Xiaotian Zhang, Jie Chao, Gang Hu, Honghong Yao

Published in: Journal of Neuroinflammation | Issue 1/2015

Login to get access

Abstract

Background

Mounting evidence has indicated that high-mobility group box 1 (HMGB1) is involved in cell activation and migration. Our previous study demonstrated that methamphetamine mediates activation of astrocytes via sigma-1 receptor (σ-1R). However, the elements downstream of σ-1R in this process remain poorly understood. Thus, we examined the molecular mechanisms involved in astrocyte activation and migration induced by methamphetamine.

Methods

The expression of HMGB1, σ-1R, and glial fibrillary acidic protein (GFAP) was examined by western blot and immunofluorescent staining. The phosphorylation of cell signaling pathways was detected by western blot, and cell migration was examined using a wound-healing assay in rat C6 astroglia-like cells transfected with lentivirus containing red fluorescent protein (LV-RFP) as well as in primary human astrocytes. The role of HMGB1 in astrocyte activation and migration was validated using a siRNA approach.

Results

Exposure of C6 cells to methamphetamine increased the expression of HMGB1 via the activation of σ-1R, Src, ERK mitogen-activated protein kinase, and downstream NF-κB p65 pathways. Moreover, methamphetamine treatment resulted in increased cell activation and migration in C6 cells and primary human astrocytes. Knockdown of HMGB1 in astrocytes transfected with HMGB1 siRNA attenuated the increased cell activation and migration induced by methamphetamine, thereby implicating the role of HMGB1 in the activation and migration of C6 cells and primary human astrocytes.

Conclusions

This study demonstrated that methamphetamine-mediated activation and migration of astrocytes involved HMGB1 up-regulation through an autocrine mechanism. Targeting HMGB1 could provide insights into the development of a potential therapeutic approach for alleviation of cell activation and migration of astrocytes induced by methamphetamine.
Literature
1.
go back to reference Schepers RJ, Oyler JM, Joseph Jr RE, Cone EJ, Moolchan ET, Huestis MA. Methamphetamine and amphetamine pharmacokinetics in oral fluid and plasma after controlled oral methamphetamine administration to human volunteers. Clin Chem. 2003;49(1):121–32.CrossRefPubMed Schepers RJ, Oyler JM, Joseph Jr RE, Cone EJ, Moolchan ET, Huestis MA. Methamphetamine and amphetamine pharmacokinetics in oral fluid and plasma after controlled oral methamphetamine administration to human volunteers. Clin Chem. 2003;49(1):121–32.CrossRefPubMed
3.
go back to reference Zhang Y, Lv X, Bai Y, Zhu X, Wu X, Chao J, et al. Involvement of sigma-1 receptor in astrocyte activation induced by methamphetamine via up-regulation of its own expression. J Neuroinflammation. 2015;12(1):250. doi:10.1186/s12974-015-0250-7. Zhang Y, Lv X, Bai Y, Zhu X, Wu X, Chao J, et al. Involvement of sigma-1 receptor in astrocyte activation induced by methamphetamine via up-regulation of its own expression. J Neuroinflammation. 2015;12(1):250. doi:10.​1186/​s12974-015-0250-7.
5.
go back to reference Shirakawa H, Sakimoto S, Nakao K, Sugishita A, Konno M, Iida S, et al. Transient receptor potential canonical 3 (TRPC3) mediates thrombin-induced astrocyte activation and upregulates its own expression in cortical astrocytes. J Neurosci. 2010;30(39):13116–29. doi:10.1523/JNEUROSCI.1890-10.2010.CrossRefPubMed Shirakawa H, Sakimoto S, Nakao K, Sugishita A, Konno M, Iida S, et al. Transient receptor potential canonical 3 (TRPC3) mediates thrombin-induced astrocyte activation and upregulates its own expression in cortical astrocytes. J Neurosci. 2010;30(39):13116–29. doi:10.​1523/​JNEUROSCI.​1890-10.​2010.CrossRefPubMed
12.
go back to reference Aschner M. Immune and inflammatory responses in the CNS: modulation by astrocytes. Toxicol Lett. 1998;102–103:283–7.CrossRefPubMed Aschner M. Immune and inflammatory responses in the CNS: modulation by astrocytes. Toxicol Lett. 1998;102–103:283–7.CrossRefPubMed
14.
go back to reference Pu C, Vorhees CV. Developmental dissociation of methamphetamine-induced depletion of dopaminergic terminals and astrocyte reaction in rat striatum. Brain Res Dev Brain Res. 1993;72(2):325–8.CrossRefPubMed Pu C, Vorhees CV. Developmental dissociation of methamphetamine-induced depletion of dopaminergic terminals and astrocyte reaction in rat striatum. Brain Res Dev Brain Res. 1993;72(2):325–8.CrossRefPubMed
16.
go back to reference Shah A, Silverstein PS, Singh DP, Kumar A. Involvement of metabotropic glutamate receptor 5, AKT/PI3K signaling and NF-kappaB pathway in methamphetamine-mediated increase in IL-6 and IL-8 expression in astrocytes. J Neuroinflammation. 2012;9:52. doi:10.1186/1742-2094-9-52.PubMedCentralCrossRefPubMed Shah A, Silverstein PS, Singh DP, Kumar A. Involvement of metabotropic glutamate receptor 5, AKT/PI3K signaling and NF-kappaB pathway in methamphetamine-mediated increase in IL-6 and IL-8 expression in astrocytes. J Neuroinflammation. 2012;9:52. doi:10.​1186/​1742-2094-9-52.PubMedCentralCrossRefPubMed
17.
go back to reference Sharkey J, Glen KA, Wolfe S, Kuhar MJ. Cocaine binding at sigma receptors. Eur J Pharmacol. 1988;149(1–2):171–4. 0014-2999(88)90058-1.CrossRefPubMed Sharkey J, Glen KA, Wolfe S, Kuhar MJ. Cocaine binding at sigma receptors. Eur J Pharmacol. 1988;149(1–2):171–4. 0014-2999(88)90058-1.CrossRefPubMed
18.
go back to reference Su TP, London ED, Jaffe JH. Steroid binding at sigma receptors suggests a link between endocrine, nervous, and immune systems. Science. 1988;240(4849):219–21.CrossRefPubMed Su TP, London ED, Jaffe JH. Steroid binding at sigma receptors suggests a link between endocrine, nervous, and immune systems. Science. 1988;240(4849):219–21.CrossRefPubMed
19.
go back to reference Bustin M. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol. 1999;19(8):5237–46.PubMedCentralPubMed Bustin M. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol. 1999;19(8):5237–46.PubMedCentralPubMed
25.
go back to reference Hayakawa K, Miyamoto N, Seo JH, Pham LD, Kim KW, Lo EH, et al. High-mobility group box 1 from reactive astrocytes enhances the accumulation of endothelial progenitor cells in damaged white matter. J Neurochem. 2012. doi:10.1111/jnc.12120. Hayakawa K, Miyamoto N, Seo JH, Pham LD, Kim KW, Lo EH, et al. High-mobility group box 1 from reactive astrocytes enhances the accumulation of endothelial progenitor cells in damaged white matter. J Neurochem. 2012. doi:10.​1111/​jnc.​12120.
29.
32.
go back to reference Zhao N, Chen Y, Zhu J, Wang L, Cao G, Dang Y, et al. Levo-tetrahydropalmatine attenuates the development and expression of methamphetamine-induced locomotor sensitization and the accompanying activation of ERK in the nucleus accumbens and caudate putamen in mice. Neuroscience. 2014;258:101–10. doi:10.1016/j.neuroscience.2013.11.025.CrossRefPubMed Zhao N, Chen Y, Zhu J, Wang L, Cao G, Dang Y, et al. Levo-tetrahydropalmatine attenuates the development and expression of methamphetamine-induced locomotor sensitization and the accompanying activation of ERK in the nucleus accumbens and caudate putamen in mice. Neuroscience. 2014;258:101–10. doi:10.​1016/​j.​neuroscience.​2013.​11.​025.CrossRefPubMed
33.
go back to reference Hayakawa K, Arai K, Lo EH. Role of ERK map kinase and CRM1 in IL-1beta-stimulated release of HMGB1 from cortical astrocytes. Glia. 2010;58(8):1007–15. doi:10.1002/glia.20982.PubMed Hayakawa K, Arai K, Lo EH. Role of ERK map kinase and CRM1 in IL-1beta-stimulated release of HMGB1 from cortical astrocytes. Glia. 2010;58(8):1007–15. doi:10.​1002/​glia.​20982.PubMed
35.
go back to reference Aradhya S, Nelson DL. NF-kappaB signaling and human disease. Curr Opin Genet Dev. 2001;11(3):300–6. S0959-437X(00)00194-5.CrossRefPubMed Aradhya S, Nelson DL. NF-kappaB signaling and human disease. Curr Opin Genet Dev. 2001;11(3):300–6. S0959-437X(00)00194-5.CrossRefPubMed
40.
go back to reference Wang HL, Peng LP, Chen WJ, Tang SH, Sun BZ, Wang CL, et al. HMGB1 enhances smooth muscle cell proliferation and migration in pulmonary artery remodeling. Int J Clin Exp Pathol. 2014;7(7):3836–44.PubMedCentralPubMed Wang HL, Peng LP, Chen WJ, Tang SH, Sun BZ, Wang CL, et al. HMGB1 enhances smooth muscle cell proliferation and migration in pulmonary artery remodeling. Int J Clin Exp Pathol. 2014;7(7):3836–44.PubMedCentralPubMed
42.
go back to reference Zuo Z, Che X, Wang Y, Li B, Li J, Dai W, et al. High mobility group box-1 inhibits cancer cell motility and metastasis by suppressing activation of transcription factor CREB and nWASP expression. Oncotarget. 2014;5(17):7458–70. 2150.PubMedCentralPubMed Zuo Z, Che X, Wang Y, Li B, Li J, Dai W, et al. High mobility group box-1 inhibits cancer cell motility and metastasis by suppressing activation of transcription factor CREB and nWASP expression. Oncotarget. 2014;5(17):7458–70. 2150.PubMedCentralPubMed
44.
Metadata
Title
Role of high-mobility group box 1 in methamphetamine-induced activation and migration of astrocytes
Authors
Yuan Zhang
Tiebing Zhu
Xiaotian Zhang
Jie Chao
Gang Hu
Honghong Yao
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2015
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-015-0374-9

Other articles of this Issue 1/2015

Journal of Neuroinflammation 1/2015 Go to the issue