Stat3 mediates LIF-induced protection of astrocytes against toxic ROS by upregulating the UPC2 mRNA pool

GLIA

Volumn 62, Issue 2, 2014, Pages 159-170

  Lapp, Daniel W ^a   Zhang, Samuel S ^a,b   Barnstable, Colin J ^a,b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

Glia; Oxidative stress; Uncoupling protein 2

Indexed keywords

LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCOUPLING PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL CULTURE; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; UPREGULATION;

GLIA; OXIDATIVE STRESS; UNCOUPLING PROTEIN 2;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ION CHANNELS; LEUKEMIA INHIBITORY FACTOR; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84890131134     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22594     Document Type: Article

References (52)

1. Aaronson DS, Horvath CM. 2002. A road map for those who don't know JAK-STAT. Science 296:1653-1655.
2. Adam-Vizi V, Chinopoulos C. 2006. Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol Sci 27:639-645.
3. Azzu V, Jastroch M, Divakaruni AS, Brand MD. 2010. The regulation and turnover of mitochondrial uncoupling proteins. Biochim Biophys Acta 1797:785-791.
4. Banner LR, Moayeri NN, Patterson PH. 1997. Leukemia inhibitory factor is expressed in astrocytes following cortical brain injury. Exp Neurol 147:1-9.
5. Barreto GE, Gonzalez J, Torres Y, Morales L. 2011. Astrocytic-neuronal crosstalk: Implications for neuroprotection from brain injury. Neurosci Res 71:107-113.
6. Boengler K, Ungefug E, Heusch G, Schulz R. The STAT3 inhibitor stattic impairs cardiomyocyte mitochondrial function through increased reactive oxygen species formation. Curr Pharm Des, in press.
7. Boeuf, H, Hauss, C, Graeve, FD, Baran, N, Kedinger, C. 1997. Leukemia inhibitory factor-dependent transcriptional activation in embryonic stem cells. J Cell Biol 138:1207-1217.
8. Chan PH. 1994. Oxygen radicals in focal cerebral ischemia. Brain Pathol 4:59-65.
9. Chan SH, Wu CA, Wu KL, Ho YH, Chang AY, Chan JY. 2009. Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ Res 105:886-896.
10. Choi JS, Kim SY, Cha JH, Choi YS, Sung KW, Oh ST, Kim ON, Chung JW, Chun MH, Lee SB, Lee MY. 2003. Upregulation of gp130 and STAT3 activation in the rat hippocampus following transient forebrain ischemia. Glia 41:237-246.
11. Craig R, Wagner M, McCardle T, Craig AG, Glembotski CC. 2001. The cytoprotective effects of the glycoprotein 130 receptor-coupled cytokine, cardiotrophin-1, require activation of NF-kappa B. J Biol Chem 276:37621-37629.
12. Cui Y, Xu X, Bi H, Zhu Q, Wu J, Xia X, Qiushi Ren, Ho PC. 2008. Expression modification of uncoupling proteins and MnSOD in retinal endothelial cells and pericytes induced by high glucose: The role of reactive oxygen species in diabetic retinopathy. Exp Eye Res 83:807-816.
13. Deng-Bryant Y, Singh IN, Carrico KM, Hall ED. 2008. Neuroprotective effects of tempol, a catalytic scavenger of peroxynitrite-derived free radicals, in a mouse traumatic brain injury model. J Cereb Blood Flow Metab 28:1114-1126.
14. Desagher S, Glowinski J, Premont J. 1996. Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 16:2553-2562.
15. Dienel GA, Hertz L. Astrocytic contributions to bioenergetics of cerebral ischemia. 2005. Glia 50:362-388.
16. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD. 2002a. Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99.
17. Echtay KS, Murphy MP, Smith RA, Talbot DA, Brand MD. 2002b. Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants. J Biol Chem 277:47129-47135.
18. Fang XX, Jiang XL, Han XH, Peng YP, Qiu YH. 2013. Neuroprotection of interleukin-6 against NMDA-induced neurotoxicity is mediated by JAK/STAT3, MAPK/ERK, and PI3K/AKT signaling pathways. Cell Mol Neurobiol 33:241-251.
19. Giardina TM, Steer JH, Lo SZ, Joyce DA. 2008. Uncoupling protein-2 accumulates rapidly in the inner mitochondrial membrane during mitochondrial reactive oxygen stress in macrophages. Biochim Biophys Acta 1777:118-129.
20. Hall ED, Vaishnav RA, Mustafa AG. 2010. Antioxidant therapies for traumatic brain injury. Neurotherapeutics 7:51-61.
21. Horvath TL, Diano S, Barnstable C. 2003. Mitochondrial uncoupling protein 2 in the central nervous system: Neuromodulator and neuroprotector. Biochem Pharmacol 65:1917-1921.
22. Hurtaud C, Gelly C, Bouillaud F, Lévi-Meyrueis C. 2006. Translation control of UCP2 synthesis by the upstream open reading frame. Cell Mol Life Sci 63:1780-1789.
23. Ibarretxe G, Sánchez-Gómez MV, Campos-Esparza MR, Alberdi E, Matute C. 2006. Differential oxidative stress in oligodendrocytes and neurons after excitotoxic insults and protection by natural polyphenols. Glia 53:201-211.
24. Jacoby JJ, Kalinowski A, Liu MG, Zhang SS, Gao Q, Chai GX, Ji L, Iwamoto Y, Li E, Schneider M, Russell KS, Fu XY. 2003. Cardiomyocyte-restricted knockout of STAT3 results in higher sensitivity to inflammation, cardiac fibrosis, and heart failure with advanced age. Proc Natl Acad Sci USA 100:12929-12934.
25. Ji JZ, Elyaman W, Yip HK, Lee VW, Yick LW, Hugon J, So KF. 2004. CNTF promotes survival of retinal ganglion cells after induction of ocular hypertension in rats: The possible involvement of STAT3 pathway. Eur J Neurosci 19:265-272.
26. Jung JE, Kim GS, Narasimhan P, Song YS, Chan PH. 2009. Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci 29:7003-7014.
27. Kondrikov D, Caldwell RB, Dong Z, Su Y. 2011. Reactive oxygen species-dependent RhoA activation mediates collagen synthesis in hyperoxic lung fibrosis. Free Radic Biol Med 50:1689-1698.
28. Korshunov SS, Skulachev VP, Starkov AA. 1997. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15-18.
29. Liang Q, Smith AD, Pan S, Tyurin VA, Kagan VE, Hastings TG, Schor NF. 2005. Neuroprotective effects of TEMPOL in central and peripheral nervous system models of Parkinson's disease. Biochem Pharmacol 70:1371-1381.
30. Lucius R, Sievers J. 1996. Postnatal retinal ganglion cells in vitro: Protection against reactive oxygen species (ROS)-induced axonal degeneration by cocultured astrocytes. Brain Res 743:56-62.
31. Macauley SL, Pekny M, Sands MS. 2011. The role of attenuated astrocyte activation in infantile neuronal ceroid lipofuscinosis. J Neurosci 31:15575-15585.
32. Mronga T, Stahnke T, Goldbaum O, Richter-Landsberg C. 2004. Mitochondrial pathway is involved in hydrogen-peroxide-induced apoptotic cell death of oligodendrocytes. Glia 46:446-455.
33. Naha PC, Davoren M, Lyng FM, Byrne HJ. 2010. Reactive oxygen species (ROS) induced cytokine production and cytotoxicity of PAMAM dendrimers in J774A.1 cells. Toxicol Appl Pharmacol 246:91-99.
34. Nègre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Pénicaud L, Casteilla L. 1997. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11:809-815.
35. Niwa H, Burdon T, Chambers I, Smith A. 1998. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 12:2048-2060.
36. Otero GC, Merrill JE. 1994. Cytokine receptors on glial cells. Glia 11:117-128.
37. Panickar KS, Norenberg MD. 2005. Astrocytes in cerebral ischemic injury: Morphological and general considerations. Glia 50:287-298.
38. Park CK, Hall ED. 2004. Dose response analysis of the 21-aminosteroid tirilazad mesylate (U-74006F) upon neurological outcome and ischemic brain damage in permanent focal cerebral ischemia. Brain Res 645:157-163.
39. Pecqueur C, Couplan E, Bouillaud F, Ricquier D. 2001. Genetic and physiological analysis of the role of uncoupling proteins in human energy homeostasis. J Mol Med (Berl) 79:48-56.
40. Peterson WM, Wang Q, Tzekova R, Wiegand SJ. 2000. Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J Neurosci 20:4081-4090.
41. Ridet JL, Malhotra SK, Privat A, Gage FH. 1997. Reactive astrocytes: Cellular and molecular cues to biological function. Trends Neurosci 20:570-577.
42. Rousset S, Mozo J, Dujardin G, Emre Y, Masscheleyn S, Ricquier D, Cassard-Doulcier AM. 2007. UCP2 is a mitochondrial transporter with an unusual very short half-life. FEBS Lett 581:479-482.
43. Sarafian TA, Montes C, Imura T, Qi J, Coppola G, Geschwind DH, Sofroniew MV. 2010. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 5:e9532.
44. Siesjö BK, Agardh CD, Bengtsson F. 1989. Free radicals and brain damage. Cerebrovasc Brain Metab Rev 1:165-211.
45. Sofroniew MV. 2000. Astrocyte failure as a cause of CNS dysfunction. Mol Psychiatry 5:230-232.
46. Spence RD, Hamby ME, Umeda E, Itoh N, Du S, Wisdom AJ, Cao Y, Bondar G, Lam J, Ao Y, Sandoval F, Suriany S, Sofroniew MV, Voskuhl RR. 2011. Proc Natl Acad Sci USA 108:8867-8872.
47. Tanaka J, Toku K, Zhang B, Ishihara K, Sakanaka M, Maeda N. 1999. Astrocytes prevent neuronal death induced by reactive oxygen and nitrogen species. Glia 28:85-96.
48. Trendelenburg G, Dirnagl U. Neuroprotective role of astrocytes in cerebral ischemia: Focus on ischemic preconditioning. 2005. Glia 50:307-320.
49. Wang D, Malo D, Hekimi S. 2010. Elevated mitochondrial reactive oxygen species generation affects the immune response via hypoxia-inducible factor-1alpha in long-lived Mclk1± mouse mutants. J Immunol 184:582-590.
50. Zhang SS, Wei J, Qin H, Zhang L, Xie B, Hui P, Deisseroth A, Barnstable CJ, Fu XY. 2004. STAT3-mediated signaling in the determination of rod photoreceptor cell fate in mouse retina. Invest Ophthalmol Vis Sci 45:2407-2412.
51. Zheng Z, Chen H, Zhao H, Liu K, Luo D, Chen Y, Chen Y, Yang X, Gu Q, Xu X. 2010. Inhibition of JAK2/STAT3-mediated VEGF upregulation under high glucose conditions by PEDF through a mitochondrial ROS pathway in vitro. Invest Ophthalmol Vis Sci 51:64-71.
52. Zhong Z, Wen Z, Darnell JE Jr. 1994. Stat3: A STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264:95-98.