Inhibition of mTOR pathway restrains astrocyte proliferation, migration and production of inflammatory mediators after oxygen-glucose deprivation and reoxygenation

Neurochemistry International

Volumn 83-84, Issue , 2015, Pages 9-18

  Li, Chun Yu ^a   Li, Xiao ^a   Liu, Shuang Feng ^a   Qu, Wen Sheng ^a   Wang, Wei ^a   Tian, Dai Shi ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Inflammation mediator; Mammalian target of rapamycin; Migration; Oxygen glucose deprivation; Proliferation; Reactive astrogliosis

Indexed keywords

GLUCOSE; MAMMALIAN TARGET OF RAPAMYCIN; OXYGEN; MTOR PROTEIN, MOUSE; NEUROPROTECTIVE AGENT; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL CYCLE PROGRESSION; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; ISCHEMIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REOXYGENATION; SIGNAL TRANSDUCTION; STRATEGIC PLANNING; ANIMAL; AUTOPHAGY; BRAIN ISCHEMIA; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; DRUG EFFECTS; METABOLISM; MOUSE; PHYSIOLOGY;

MAMMALIA;

ANIMALS; ASTROCYTES; AUTOPHAGY; BRAIN ISCHEMIA; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; GLUCOSE; MICE; NEUROPROTECTIVE AGENTS; OXYGEN; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84926140580     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.03.001     Document Type: Article

References (58)

1. Auguste K.I., Jin S., Uchida K., Yan D., Manley G.T., and Papadopoulos M.C. Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury FASEB J. 21 1 2007 108 116
2. Berven L.A., Willard F.S., and Crouch M.F. Role of the p70(S6K) pathway in regulating the actin cytoskeleton and cell migration Exp. Cell Res 296 2 2004 183 195
3. Binder D.K., and Steinhauser C. Functional changes in astroglial cells in epilepsy Glia 54 5 2006 358 368
4. Cai Z., Pang Y., Lin S., and Rhodes P.G. Differential roles of tumor necrosis factor-alpha and interleukin-1 beta in lipopolysaccharide-induced brain injury in the neonatal rat Brain Res 975 1-2 2003 37 47
5. Capdevila J., Elez E., Macarulla T., Ramos F.J., Ruiz-Echarri M., and Tabernero J. Anti-epidermal growth factor receptor monoclonal antibodies in cancer treatment Cancer Treat. Rev 35 4 2009 354 363
6. Chen H.C., Fong T.H., Hsu P.W., and Chiu W.T. Multifaceted effects of rapamycin on functional recovery after spinal cord injury in rats through autophagy promotion, anti-inflammation, and neuroprotection J. Surg. Res 179 1 2013 e203 e210
7. Chen K.B., Uchida K., Nakajima H., Yayama T., Hirai T., and Watanabe S. Tumor necrosis factor-alpha antagonist reduces apoptosis of neurons and oligodendroglia in rat spinal cord injury Spine (Phila Pa 1976) 36 17 2011 1350 1358
8. Chiang G.G., and Abraham R.T. Targeting the mTOR signaling network in cancer Trends Mol. Med 13 10 2007 433 442
9. Codeluppi S., Svensson C.I., Hefferan M.P., Valencia F., Silldorff M.D., and Oshiro M. The Rheb-mTOR pathway is upregulated in reactive astrocytes of the injured spinal cord J. Neurosci 29 4 2009 1093 1104
10. Cory G. Scratch-wound assay Methods Mol. Biol 769 2011 25 30
11. Dazert E., and Hall M.N. mTOR signaling in disease Curr. Opin. Cell Biol 23 6 2011 744 755
12. Dzau V.J., Braun-Dullaeus R.C., and Sedding D.G. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies Nat. Med 8 11 2002 1249 1256
13. Erlich S., Alexandrovich A., Shohami E., and Pinkas-Kramarski R. Rapamycin is a neuroprotective treatment for traumatic brain injury Neurobiol. Dis 26 1 2007 86 93
14. Fingar D.C., Richardson C.J., Tee A.R., Cheatham L., Tsou C., and Blenis J. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E Mol. Cell. Biol 24 1 2004 200 216
15. Fitch M.T., Doller C., Combs C.K., Landreth G.E., and Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma J. Neurosci 19 19 1999 8182 8198
16. Fletcher L., Evans T.M., Watts L.T., Jimenez D.F., and Digicaylioglu M. Rapamycin treatment improves neuron viability in an in vitro model of stroke PLoS ONE 8 7 2013
17. Fulda S. The PI3K/Akt/mTOR pathway as therapeutic target in neuroblastoma Curr. Cancer Drug Targets 9 6 2009 729 737
18. Fuller S., Munch G., and Steele M. Activated astrocytes: a therapeutic target in Alzheimer's disease? Expert Rev. Neurother 9 11 2009 1585 1594
19. Garelick M.G., and Kennedy B.K. TOR on the brain Exp. Gerontol 46 2-3 2011 155 163
20. Hennessy B.T., Smith D.L., Ram P.T., Lu Y., and Mills G.B. Exploiting the PI3K/AKT pathway for cancer drug discovery Nat. Rev. Drug Discov 4 12 2005 988 1004
21. Holley J.E., Gveric D., Newcombe J., Cuzner M.L., and Gutowski N.J. Astrocyte characterization in the multiple sclerosis glial scar Neuropathol. Appl. Neurobiol 29 5 2003 434 444
22. Iadecola C., Zhang F., Xu S., Casey R., and Ross M.E. Inducible nitric oxide synthase gene expression in brain following cerebral ischemia J. Cereb. Blood Flow Metab 15 3 1995 378 384
23. Jin C., Zhao Y., Yu L., Xu S., and Fu G. MicroRNA-21 mediates the rapamycin-induced suppression of endothelial proliferation and migration FEBS Lett 587 4 2013 378 385
24. Kalderon N. Cell elimination as a strategy for repair in acute spinal cord injury Curr. Pharm. Des 11 10 2005 1237 1245
25. Kerr B.J., and Patterson P.H. Potent pro-inflammatory actions of leukemia inhibitory factor in the spinal cord of the adult mouse Exp. Neurol 188 2 2004 391 407
26. Kruman I.I. Why do neurons enter the cell cycle? Cell Cycle 3 6 2004 769 773
27. Laplante M., and Sabatini D.M. mTOR signaling in growth control and disease Cell 149 2 2012 274 293
28. Lee S.M., Yune T.Y., Kim S.J., Kim Y.C., Oh Y.J., and Markelonis G.J. Minocycline inhibits apoptotic cell death via attenuation of TNF-alpha expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures J. Neurochem 91 3 2004 568 578
29. Lin C.C., Lee I.T., Chi P.L., Hsieh H.L., Cheng S.E., and Hsiao L.D. C-Src/Jak2/PDGFR/PKCdelta-dependent MMP-9 induction is required for thrombin-stimulated rat brain astrocytes migration Mol. Neurobiol 49 2 2014 658 672
30. Liu H.T., Li F., Wang W.Y., Li X.J., Liu Y.M., and Wang R.A. Rapamycin inhibits re-endothelialization after percutaneous coronary intervention by impeding the proliferation and migration of endothelial cells and inducing apoptosis of endothelial progenitor cells Tex. Heart Inst. J. 37 2 2010 194 201
31. Ljungberg M.C., Bhattacharjee M.B., Lu Y., Armstrong D.L., Yoshor D., and Swann J.W. Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia Ann. Neurol 60 4 2006 420 429
32. Lucas S.M., Rothwell N.J., and Gibson R.M. The role of inflammation in CNS injury and disease Br. J. Pharmacol 147 Suppl. 1 2006 S232 S240
33. Martin D.E., and Hall M.N. The expanding TOR signaling network Curr. Opin. Cell Biol 17 2 2005 158 166
34. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., and Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth Neuron 13 4 1994 805 811
35. Miao H., Crabb A.W., Hernandez M.R., and Lukas T.J. Modulation of factors affecting optic nerve head astrocyte migration Invest. Ophthalmol. Vis. Sci 51 8 2010 4096 4103
36. Molhoek K.R., Brautigan D.L., and Slingluff C.L. Jr. Synergistic inhibition of human melanoma proliferation by combination treatment with B-Raf inhibitor BAY43-9006 and mTOR inhibitor Rapamycin J. Transl. Med 3 2005 39
37. Mori T., Tan J., Arendash G.W., Koyama N., Nojima Y., and Town T. Overexpression of human S100B exacerbates brain damage and periinfarct gliosis after permanent focal ischemia Stroke 39 7 2008 2114 2121
38. Pan Q., Xie X., Guo Y., and Wang H. Simvastatin promotes cardiac microvascular endothelial cells proliferation, migration and survival by phosphorylation of p70 S6K and FoxO3a Cell Biol. Int 38 5 2014 599 609
39. Papadopoulos M.C., and Verkman A.S. Potential utility of aquaporin modulators for therapy of brain disorders Prog. Brain Res 170 2008 589 601
40. Park J., Zhang J., Qiu J., Zhu X., Degterev A., and Lo E.H. Combination therapy targeting Akt and mammalian target of rapamycin improves functional outcome after controlled cortical impact in mice J. Cereb. Blood Flow Metab 32 2 2012 330 340
41. Pekny M., Wilhelmsson U., Bogestal Y.R., and Pekna M. The role of astrocytes and complement system in neural plasticity Int. Rev. Neurobiol 82 2007 95 111
42. Qu W.S., Tian D.S., Guo Z.B., Fang J., Zhang Q., and Yu Z.Y. Inhibition of EGFR/MAPK signaling reduces microglial inflammatory response and the associated secondary damage in rats after spinal cord injury J. Neuroinflammation 9 2012 178
43. Rolls A., Shechter R., and Schwartz M. The bright side of the glial scar in CNS repair Nat. Rev. Neurosci 10 3 2009 235 241
44. Saadoun S., Papadopoulos M.C., Watanabe H., Yan D., Manley G.T., and Verkman A.S. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation J. Cell Sci 118 Pt 24 2005 5691 5698
45. Saleh A., Schroeter M., Jonkmanns C., Hartung H.P., Modder U., and Jander S. In vivo MRI of brain inflammation in human ischaemic stroke Brain 127 Pt 7 2004 1670 1677
46. Shaw R.J., and Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth Nature 441 7092 2006 424 430
47. Silver J., and Miller J.H. Regeneration beyond the glial scar Nat. Rev. Neurosci 5 2 2004 146 156
48. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation Trends Neurosci 32 12 2009 638 647
49. Tian D.S., Yu Z.Y., Xie M.J., Bu B.T., Witte O.W., and Wang W. Suppression of astroglial scar formation and enhanced axonal regeneration associated with functional recovery in a spinal cord injury rat model by the cell cycle inhibitor olomoucine J. Neurosci. Res 84 5 2006 1053 1063
50. Tian D.S., Liu J.L., Xie M.J., Zhan Y., Qu W.S., and Yu Z.Y. Tamoxifen attenuates inflammatory-mediated damage and improves functional outcome after spinal cord injury in rats J. Neurochem 109 6 2009 1658 1667
51. Wang H.H., Hsieh H.L., and Yang C.M. Nitric oxide production by endothelin-1 enhances astrocytic migration via the tyrosine nitration of matrix metalloproteinase-9 J. Cell. Physiol 226 9 2011 2244 2256
52. Wanner I.B., Anderson M.A., Song B., Levine J., Fernandez A., and Gray-Thompson Z. Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury J. Neurosci 33 31 2013 12870 12886
53. Wu X., Kihara T., Akaike A., Niidome T., and Sugimoto H. PI3K/Akt/mTOR signaling regulates glutamate transporter 1 in astrocytes Biochem. Biophys. Res. Commun 393 2010 514 518
54. Yang Q., Wang E.Y., Huang X.J., Qu W.S., Zhang L., and Xu J.Z. Blocking epidermal growth factor receptor attenuates reactive astrogliosis through inhibiting cell cycle progression and protects against ischemic brain injury in rats J. Neurochem 119 3 2011 644 653
55. Yune T.Y., Chang M.J., Kim S.J., Lee Y.B., Shin S.W., and Rhim H. Increased production of tumor necrosis factor-alpha induces apoptosis after traumatic spinal cord injury in rats J. Neurotrauma 20 2 2003 207 219
56. Zhang Q., Chen C., Lu J., Xie M., Pan D., and Luo X. Cell cycle inhibition attenuates microglial proliferation and production of IL-1beta, MIP-1alpha, and NO after focal cerebral ischemia in the rat Glia 57 8 2009 908 920
57. Zhu Z., Zhang Q., Yu Z., Zhang L., Tian D., and Zhu S. Inhibiting cell cycle progression reduces reactive astrogliosis initiated by scratch injury in vitro and by cerebral ischemia in vivo Glia 55 5 2007 546 558
58. Zuidema J.M., Hyzinski-Garcia M.C., Van Vlasselaer K., Zaccor N.W., Plopper G.E., and Mongin A.A. Enhanced GLT-1 mediated glutamate uptake and migration of primary astrocytes directed by fibronectin-coated electrospun poly-l-lactic acid fibers Biomaterials 35 5 2014 1439 1449