Early activation of STAT3 regulates reactive astrogliosis induced by diverse forms of neurotoxicity

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  O'Callaghan, James P ^a   Kelly, Kimberly A ^a   VanGilder, Reyna L ^b   Sofroniew, Michael V ^c   Miller, Diane B ^a  

^a NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 3,4 METHYLENEDIOXYAMPHETAMINE; 3,4 METHYLENEDIOXYMETHAMPHETAMINE; AMPHETAMINE; CORTICOSTERONE; DIAZEPAM; GLIAL FIBRILLARY ACIDIC PROTEIN; JANUS KINASE 2; KAINIC ACID; LIPOPOLYSACCHARIDE; METHAMPHETAMINE; NOMIFENSINE; STAT3 PROTEIN; TRIMETHYLTIN; TYROSINE; CORT 108297; FUSED HETEROCYCLIC RINGS; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; HETEROCYCLIC COMPOUND; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN REGION; CONTROLLED STUDY; GFAP GENE; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; BRAIN; CORPUS STRIATUM; DEFICIENCY; DRUG EFFECTS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GLIOSIS; HIPPOCAMPUS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; ASTROCYTES; AZA COMPOUNDS; BRAIN; CORPUS STRIATUM; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; GLIOSIS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HIPPOCAMPUS; JANUS KINASE 2; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; RATS; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84904245054     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102003     Document Type: Article

References (77)

1. Norton WT, Aquino DA, Hozumi I, Chiu FC, Brosnan CF (1992) Quantitative aspects of reactive gliosis: a review. Neurochem Res 17:877-885.
2. O'Callaghan JP (1993) Quantitative features of reactive gliosis following toxicant-induced damage of the CNS. Ann N Y Acad Sci 679:195-210.
3. Eng LF, Ghirnikar RS, Lee YL (2000) Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 25:1439-1451.
4. Norenberg MD, Rao KV, Jayakumar AR (2005) Mechanisms of ammonia-induced astrocyte swelling. Metab Brain Dis 20:303-318. (Pubitemid 43029804)
5. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, et al. (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32:6391-6410.
6. Eng LF (1985) Glial fibrillary acidic protein (GFAP): the major protein of glial intermediate filaments in the differentiated astrocytes. J Neuroimmunol 8(4- 6):203-14.
7. Penky M, Wilhelmsson U, Penka M (2014) The dual role of astrocyte activation and reactive gliosis. Neuroscience Letters 565:30-38.
8. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
9. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7-35.
10. Sosunov AA, Wu X, Tsankova NM, Guilfoyle E, McKhann GM 2nd, et al. (2014) Phenotypic heterogeneity and plasticity of isocortical and hippocampal astrocytes in the human brain. J Neurosci 34(6):2285-2298.
11. O'Callaghan JP, Sriram K (2005) Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert Opin Drug Saf 4:433-442. (Pubitemid 40723718)
12. Sriram K, Benkovic SA, Hebert MA, Miller DB, O'Callaghan JP (2004) Induction of gp130-related cytokines and activation of JAK2/STAT3 pathway in astrocytes precedes up-regulation of glial fibrillary acidic protein in the 1- methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of neurodegeneration: key signaling pathway for astrogliosis in vivo? J Biol Chem 279:19936-19947. (Pubitemid 38623436)
13. Chen E, Xu D, Lan X, Jia B, Sun L, et al. (2013) A Novel Role of the STAT3 Pathway in Brain Inflammation-induced Human Neural Progenitor Cell Differentiation. Curr Mol Med 13:1474-84.
14. O'Callaghan JP, Sriram K, Miller DB (2008) Defining " neuroinflammation". Ann N Y Acad Sci 1139:318-330.
15. Wanner IB, Anderson MA, Song B, Levine J, Fernandez A, et al. (2013) 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 33:12870-12886.
16. Oliva AA, Kang Y, Sanchez-Molano J, Furones C, Atkins CM (2012) STAT3 signaling after traumatic brain injury. J Neurochem 120:710-720.
17. Herrmann JE, Imura T, Song B, Qi J, Ao Y, et al. (2008) STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28:7231-7243.
18. Okada S, Nakamura M, Katoh H, Miyao T, Shimazaki T, et al. (2006) Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat Med 12(7):829-834. (Pubitemid 44050074)
19. Dinapoli VA, Benkovic SA, Li X, Kelly KA, Miller DB, et al. (2010) Age exaggerates proinflammatory cytokine signaling and truncates signal transducers and activators of transcription 3 signaling following ischemic stroke in the rat. Neuroscience 170:633-644.
20. Deng H, Han HS, Cheng D, Sun GH, Yenari MA (2003) Mild hypothermia inhibits inflammation after experimental stroke and brain inflammation. Stroke 34:2495-2501. (Pubitemid 37221971)
21. Bauer S, Kerr BJ, Patterson PH (2007) The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 8:221-232. (Pubitemid 46294661)
22. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46-56. (Pubitemid 350295688)
23. O'Callaghan JP, Miller DB (2010) Spinal glia and chronic pain. Metabolism 59:S21-6.
24. O'Callaghan JP (1991) Quantification of glial fibrillary acidic protein: comparison of slot-immunobinding assays with a novel sandwich ELISA. Neurotoxicol Teratol 13:275-281.
25. O'Callaghan JP (2002) Measurement of glial fibrillary acidic protein. Curr Protoc Toxicol Chapter 12:Unit12.
26. O'Callaghan JP, Miller DB, Reinhard JF, Jr. (1990) Characterization of the origins of astrocyte response to injury using the dopaminergic neurotoxicant, 1- methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Brain Res 521:73-80. (Pubitemid 20208736)
27. Sriram K, Miller DB, O'Callaghan JP (2006) Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-alpha. J Neurochem 96:706-718.
28. Takeda K, Kaisho T, Yoshida N, Takeda J, Kishimoto T, et al. (1998) Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3- deficient mice. J Immunol 161:4652-4660. (Pubitemid 28492039)
29. O'Callaghan JP, Miller DB (1994) Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 270:741-751. (Pubitemid 24271391)
30. O'Callaghan JP, Jensen KF, Miller DB (1995) Quantitative aspects of drug and toxicant-induced astrogliosis. Neurochem Int 26:115.
31. O'Callaghan JP, Sriram K (2004) Focused microwave irradiation of the brain preserves in vivo protein phosphorylation: comparison with other methods of sacrifice and analysis of multiple phosphoproteins. J Neurosci Methods 135:159- 168.
32. Scharf MT, Mackiewicz M, Naidoo N, O'Callaghan JP, Pack AI (2008) AMP-activated protein kinase phosphorylation in brain is dependent on method of killing and tissue preparation. J Neurochem 105:833-841. (Pubitemid 351562726)
33. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85. (Pubitemid 16258399)
34. Cromey DW (2007) Avoiding twisted pixels: ethical guidelines for the appropriate use of manipulation of scientific digital images. Sci Eng Ethics 16:639-667.
35. Sedgewick J (2013) Image Integrity: Scientific Do's and Don'ts. www.imagingandanalysis.com/courses-image-integrity.
36. Miller DB, O'Callaghan JP (1994) Environment-, drug- and stress-induced alterations in body temperature affect the neurotoxicity of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 270:752-760. (Pubitemid 24271392)
37. Kelly KA, Miller DB, Bowyer JF, O'Callaghan JP (2012) Chronic exposure to corticosterone enhances the neuroinflammatory and neurotoxic responses to methamphetamine. J Neurochem 122:995-1009.
38. Benkovic SA, O'Callaghan JP, Miller DB (2004) Sensitive indicators of injury reveal hippocampal damage in C57BL/6J mice treated with kainic acid in the absence of tonic-clonic seizures. Brain Res. 1024(1-2):59-76. (Pubitemid 39307088)
39. Fuller TA, Olney JW (1981) Only certain anticonvulsants protect against kainate neurotoxicity. Neurobehav Toxicol Teratol 3:355-361. (Pubitemid 12242800)
40. Murray PJ (2007) The JAK-STAT signaling pathway: Input and output integration. J Immunol 178:2623-2629.
41. Nicolas CS, Amici M, Bortolotto ZA, Doherty A, Csaa Z, et al. (2013) The role of JAK-STAT signaling in the CNS. JAK-STAT 2013; 2:e22925; http://dx.doi.org/10.4161/jkst.22925.
42. Garrido-Mesa N, Zarzuelo A, Galvez J (2013) Minocycline: far beyond an antibiotic. Br J Pharmacol 169(2):337-52.
43. Hamby ME, Coppola G, Ao Y, Geschwind DH, Khakh BS, et al. (2012) Inflammatory mediators alter the astrocyte transcriptome and calcium signaling elicited by multiple G-protein-coupled receptors. J Neurosci. 32: 14489-14510.
44. 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. (Pubitemid 24144493)
45. Dawn B, Xuan YT, Guo Y, Rezazadeh A, Stein AB, et al. (2004) IL-6 plays an obligatory role in late preconditioning via JAK-STAT signaling and upregulation of iNOS and COX-2. Cardiovasc Res 64:61-71. (Pubitemid 39208923)
46. Bengmark S (2004) Acute and "chronic" phase reaction-a mother of disease. Clin Nutr 23:1256-1266.
47. Dantzer R, Kelley KW (2007) Twenty years of research on cytokine-induced sickness behavior. Brain Behav Immun 21:153-160. (Pubitemid 46038917)
48. Gautron L, Lafon P, Chaigniau M, Tramu G, Laye S (2002) Spatiotemporal analysis of signal transducer and activator of transcription 3 activation in rat brain astrocytes and pituitary following peripheral immune challenge. Neuroscience 112:717-729. (Pubitemid 34634165)
49. Lebel E, Vallieres L, Rivest S (2000) Selective involvement of interleukin-6 in the transcriptional activation of the suppressor of cytokine signaling-3 in the brain during systemic immune challenges. Endocrinology 141:3749-3763.
50. Rivest S, Lacroix S, Vallieres L, Nadeau S, Zhang J, et al. (2000) How the blood talks to the brain parenchyma and the paraventricular nucleus of the hypothalamus during systemic inflammatory and infectious stimuli. Proc Soc Exp Biol Med 223:22-38. (Pubitemid 30182654)
51. Turner RC, Lucke-Wold B, Miller DB, O'Callaghan JP, Rosen CL, et al. (2012) Neuropoietic cytokines and neural injury: alterations in JAK2/STAT3 signaling associated with aging. In: Neurological Disorders: New Research (Thomas CE, Moore JR, eds), pp 27-48. Nova Science Publishers, Inc.
52. Darnell JE Jr (1997) STATs and gene regulation. Science 277:1630-1635.
53. Leonard WJ, O'Shea JJ (1998) Jaks and STATs: biological implications. Annu Rev Immunol 16:293-322. (Pubitemid 28183367)
54. Thomas DM, Francescutti-Verbeem DM, Liu X, Kuhn DM (2004) Identification of differentially regulated transcripts in mouse striatum following methamphetamine treatment-an oligonucleotide microarray approach. J Neurochem 88:380-393. (Pubitemid 38084554)
55. Miscia S, Marchisio M, Grilli A, Di Valerio V, Centurione L, et al. (2002) Tumor necrosis factor alpha (TNF-alpha) activates Jak1/Stat3-Stat5B signaling through TNFR-1 in human B cells. Cell Growth Differ 13(1):13-8. (Pubitemid 34106795)
56. Aguzzi A, Barres BA, Bennett ML (2013) Microglia: Scapegoat, Saboteur, or Something Else? Science 339:156-161.
57. Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J, et al. (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338:1353-1356.
58. Stella N (2012) Inflammation to Rebuild a Brain. Science 338:1303-1304.
59. Buttini M, Limonta S, Boddeke HWGM (1996) Peripheral administration of lipopolysaccharide induces activation of microglial cells in rat brain. Neurochem Int 29:25-35. (Pubitemid 26276501)
60. Datta SC, Opp MR (2008) Lipopolysaccharide-induced increases in cytokines in discrete mouse brain regions are detectable using Luminex xMAP technology. J Neurosci Methods 175:119-124.
61. Meddahi A, Bree F, Papy-Garcia D, Gautron J, Barritault D, et al. (2002) Pharmacological studies of RGTA(11), a heparan sulfate mimetic polymer, efficient on muscle regeneration. J Biomed Mater Res 62:525-531.
62. Beurel E, Jope RS (2009) Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J Neuroinflammation 6:9.
63. Al-Amri JS, Hagras MM, Mohamed IM (2013) Effect of epigallocatechin-3- gallate on inflammatory mediators release in LPS-induced Parkinson's disease in rats. Indian J Exp Biol 51:357-362.
64. Qin L, Wu X, Block ML, Liu Y, Breese GR, et al. (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453- 462.
65. Nguyen TA, Frank-Cannon T, Martinez TN, Ruhn KA, Marvin M, et al. (2013) Analysis of inflammation-related nigral degeneration and locomotor function in DJ-1(-/-) mice. J Neuroinflammation 10:50.
66. Qin L, Liu Y, Hong JS, Crews FT (2013) NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration. Glia 61:855-868.
67. Kaya M, Palanduz A, Kalayci R, Kemikler G, Simsek G, et al. (2004) Effects of lipopolysaccharide on the radiation-induced changes in the blood-brain barrier and the astrocytes. Brain Res 1019:105-112. (Pubitemid 39078616)
68. Semmler A, Okulla T, Sastre M, Dumitrescu-Ozimek L, Heneka MT (2005) Systemic inflammation induces apoptosis with variable vulnerability of different brain regions. J Chem Neuroanat 30:144-157. (Pubitemid 41338695)
69. Ifuku M, Katafuchi T, Mawatari S, Noda M, Miake K, et al. (2012) Antiinflammatory/ anti-amyloidogenic effects of plasmalogens in lipopolysaccharideinduced neuroinflammation in adult mice. J Neuroinflammation 9:197.
70. Little AR, Benkovic SA, Miller DB, O'Callaghan JP (2002) Chemically induced neuronal damage and gliosis: enhanced expression of the proinflammatory chemokine, monocyte chemoattractant protein (MCP)-1, without a corresponding increase in proinflammatory cytokines(1). Neuroscience 115:307-320. (Pubitemid 35232709)
71. Dantzer R (2004) Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500:399-411.
72. Xia H, Wang Q, Liao Y, Xu X, Baxter SM, et al. (2002) Polymerization rate and mechanism of ultrasonically initiated emulsion polymerization of n-butyl acrylate. Ultrason Sonochem 9:151-158. (Pubitemid 34722262)
73. Choi JS, Kim SY, Cha JH, Choi YS, Sung KW, et al. (2003) Upregulation of gp130 and STAT3 activation in the rat hippocampus following transient forebrain ischemia. Glia 41:237-246. (Pubitemid 36258469)
74. Tsuda M, Kohro Y, Yano T, Tsujikawa T, Kitano J, et al. (2011) JAK-STAT3 pathway regulates spinal astrocyte proliferation and neuropathic pain maintenance in rats. Brain 134:1127-1139.
75. Zhang Y, Barres BA (2010) Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 20:588-594.
76. Shigetomi E, Bushong EA, Haustein MD, Tong X, Jackson-Weaver O, et al. (2013) Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J Gen Physiol 141:633-647.
77. Brock TO, O'Callaghan JP (1987) Quantitative changes in the synaptic vesicle proteins synapsin I and p38 and the astrocyte-specific protein glial fibrillary acidic protein are associated with chemical-induced injury to the rat central nervous system. J Neurosci 7:931-942. (Pubitemid 17055338)