Activation of the JAK/STAT pathway following transients focal cerebral ischemia: Signaling through Jak1 and Stat3 in astrocytes

GLIA

Volumn 30, Issue 3, 2000, Pages 253-270

  Justicia, Carles ^a   Gabriel, Cecília ^a,b   Planas, Anna M ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Middle cerebral artery occlusion; Rat; Signal transduction; Stroke

Indexed keywords

DNA BINDING PROTEIN; JAK1 PROTEIN, RAT; JANUS KINASE 1; PROTEIN TYROSINE KINASE; STAT3 PROTEIN; STAT3 PROTEIN, RAT; TRANSACTIVATOR PROTEIN;

ANIMAL; ARTICLE; ASTROCYTE; BRAIN; BRAIN ISCHEMIA; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; PATHOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; ASTROCYTES; BRAIN; BRAIN ISCHEMIA; DNA-BINDING PROTEINS; IMMUNOHISTOCHEMISTRY; JANUS KINASE 1; MALE; PROTEIN-TYROSINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; STAT3 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 0034013433     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1136(200005)30:3<253::AID-GLIA5>3.0.CO;2-O     Document Type: Article

References (64)

1. Banati RB, Gehrmann J, Schubert P, Kreutzberg GW. 1993. Cytotoxicity of microglia. Glia 7:111-118.
2. Barone FC, Arvin B, White RF, Miller A, Webb CL, Willette RN, Lysko PG, Feuerstein GZ. 1997. Tumor necrosis factor-α. A mediator of focal ischemic brain injury. Stroke 28:1233-1244.
3. Berhow MT, Hiroi N, Kobierski LA, Hyman SE, Nestler EJ. 1996. Influence of cocaine on the JAK-STAT pathway in the mesolimbic dopamine system. J Neurosci 16:8019-8026.
4. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278:477-483.
5. Brunn GJ, Falls EL, Nilson AE, Abraham RT. 1995. Protein-tyrosine kinase-dependent activation of STAT transcription factors in interleukin-2- or interleukin-4-stimulated T lymphocytes. J Biol Chem 270:11628-11635.
6. Buttini M, Sauter A, Boddeke HW. 1994. Induction of interleukin-1β mRNA after focal cerebral ischemia in the rat. Mol Brain Res 23:126-134.
7. Buttini M, Appel K, Sauter A, Gebicke-Haerter PJ, Boddeke HW. 1996. Expression of tumor necrosis factor alpha after focal cerebral ischemia in the rat. Neuroscience 71:1-16.
8. Buzas B, Symes AJ, Cox BM. 1999. Regulation of nociceptin/orphanin FQ gene expression by neuropoietic cytokines and neurotrophic factors in neurons and astrocytes. J Neurochem 72:1882-1889.
9. Catlett-Falcone R, Landowski TH, Oshiro MM, Turkson J, Levitzki A, Savino R, Ciliberto G, Moscinski L, Fernández-Luna JL, Nuñez G, Dalton WS, Jove R. 1999. Consitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10:105-115.
10. Cattaneo E, Magrassi L, De-Fraja C, Conti L, Di Gennaro I, Butti G, Govoni S. 1998. Variations in the levels of the JAK/STAT and shcA proteins in human brain tumors. Anticancer Res 18:2381-2387.
11. Chomczynski P, Sacchi N. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Anal Biochem 162:156-159.
12. Darnell JE, Kerr IM, Stark GR. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421.
13. De-Fraja C, Conti L, Magrassi L, Govoni S, Cattaneo E. 1998. Members of the JAK/STAT proteins are expressed and regulated during development in the mammalian forebrain. J Neurosci Res 54:320-330.
14. Dell'Albani, P, Kahn MA, Cole R, Condorelli DF, Giuffrida-Stella AM, de Vellis J. 1998. Oligodendroglial survival factors, PDGF-AA and CNTF, activate similar JAK/STAT signaling pathways. J Neurosci Res 15:191-205.
15. Ferrer I, Barrón S, Rodríguez-Farré E, Planas AM. 1995. Ionizing radiation-induced apoptosis is associated with c-Jun expression and c-Jun/AP-1 activation in the developing cerebellum of the rat. Neurosci Lett 202:105-108.
16. Feuerstein GZ, Liu T, Barone FC. 1994. Cytokines, inflammation, and brain injury: Role of tumor necrosis factor-α. Cerebrovasc Brain Metab Rev 6:341-360.
17. Grandis JR, Drenning SD, Chakraborty A, Zhou MY, Zeng Q, Pitt AS, Tweardy DJ. 1998. Requirement of Stat3 but not Stat1 activation for epidermal growth factor receptor-mediated cell growth in vitro. J Clin Invest 102:1385-1392.
18. Guo D, Dunbar JD, Yang CH, Pfeffer LM, Donner D. 1998. Induction of Jak/STAT signaling by activation of the type 1 TNF receptor. J Immunol 160:2742-2750.
19. Guschin D, Rogers N, Briscoe J, Witthuhn B, Watling D, Horn F, Pellegrini S, Yasukawa K, Heinrich P, Stark GR, Ihle JN, Kerr IM. 1995. A major role for the protein tyrosine kinase Jak1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J 14: 1421-1429.
20. Horvath CM, Wen Z, Darnell JE. 1995. A STAT protein domain that determines DNA sequence recognition suggests a novel DNA-binding domain. Genes Dev 9:984-994.
21. Hu J, Saito T, Abe K, Deguchi T. 1997. Increase of ciliary neurotrophic factor (CNTF) in the ischemic rat brain as determined by a sensitive enzyme-linked immunoassay. Neurol Res 19:593-598.
22. Ihle JN. 1996. STATs: signal transducers and activators of transcription. Cell 84:331-334.
23. Justicia C, Planas AM. 1999. Transforming growth factor-α acting at the epidermal growth factor receptor reduces infarct volume after permanent middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 19:128-132.
24. Kahn MA, Huang CJ, Caruso A, Barresi V, Nazarian R, Condorelli DF, de Vellis J. 1997. Ciliary neurotrophic factor activates JAK/Stat signal transduction cascade and induces transcriptional expression of glial fibrillary acidic protein in glial cells. J Neurochem 68:1413-1423.
25. Kato H, Liu Y, Kogure K, Kato K. 1994. Induction of 27-kDa heat shock protein following cerebral ischemia in a rat model of ischemic tolerance. Brain Res 634:235-244.
26. Lavine SD, Hofman FM, Zlokovic BV. 1998. Circulating antibody against tumor necrosis factor-alpha protects rat brain from reperfusion injury. J Cereb Blood Flow Metab 18:52-58.
27. Lehrmann E, Christensen T, Zimmer J, Diemer NH, Finsen B. 1997. Microglial and macrophage reactions mark progressive changes and define the penumbra in the rat neocortex and striatum after transient middle cerebral artery occlusion. J Comp Neurol 386:461-476.
28. Leven RM, Clark B, Tablin F. 1997. Effect of recombinant IL-6 and thrombopoietin on isolated guinea pig bone marrow megakaryocyte protein phosphorylation and proplatelet formation. Blood Cells Mol Dis 23:252-268.
29. Lin TN, Wang PY, Chi SI, Kuo J. 1998. Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor alpha (CNTRα) expression following focal cerebral ischemia. Mol Brain Res 55:71-80.
30. Liu T, Clark RK, McDonnell PC, Young PR, White RF, Barone FC, Feuerstein GZ. 1994. Tumor necrosis factor-α expression in ischemic neurons. Stroke 25:1481-1488.
31. Loddick SA, Wong ML, Bongiorno PB, Gold PW, Licinio J, Rothwell NJ. 1997. Endogenous interleukin-1 receptor antagonist is neuroprotective. Biochem Biophys Res Commun 8:211-215.
32. Loddick SA, Turnbull AV, Rothwell NJ. 1998. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 18:176-179.
33. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T. 1999. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 282:479-482.
34. Nawashiro H, Martin D, Hallenbeck JM. 1997a. Neuroprotective effects of TNF binding protein in focal cerebral ischemia. Brain Res 778:265-271.
35. Nawashiro H, Martin D, Hallenbeck JM. 1997b. Inhibition of tumor necrosis factor and amelioration of brain infarction in mice. J Cereb Blood Flow Metab 17:229-232.
36. Nawashiro H, Tasaki K, Ruetzler CA, Hallenbeck, JM. 1997c. TNF-α pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab 17:483-490.
37. Nielsen M, Kaestel CG, Eriksen KW, Woetmann A, Stokkedal T, Kaltoft K, Geisler C, Ropke C, Odum N. 1999. Inhibition of constitutively activated Stat3 correlates with altered Bcl-2/Bax expression and induction of apoptosis in mycosis fungoides tumor cells. Leukemia 13:735-738.
38. Planas AM, Soriano MA, Ferrer I, Rodríguez-Farré E. 1995. Kainic acid-induced heat shock protein-70 mRNA and protein is inhibited by MK-801 in certain rat brain regions. Eur J Neurosci 7:293-304.
39. Planas AM, Soriano MA, Berruezo M, Estrada A, Justicia C, Pitarch S, Ferrer I. 1996. Induction of Stat3, a signal transducer and transcription factor, in reactive microglia following transient focal cerebral ischemia. Eur J Neurosci 8:2612-2618.
40. Planas AM, Berruezo M, Justicia C, Barrón S, Ferrer I. 1997a. Stat3 is present in the developing and adult rat cerebellum and participates in the formation of transcription complexes binding DNA at the sis-inducible element. J Neurochem 68:1345-1351.
41. Planas AM, Justicia C, Ferrer I. 1997b. Stall in developing and adult rat brain. Induction after transient focal ischemia. NeuroReport 8:1359-1362.
42. Planas AM, Soriano MA, Estrada A, Sanz O, Martin F, Ferrer I. 1997c. The heat shock stress response after brain lesions: induction of 72 kDa heat shock protein (cell types involved, axonal transport, transcriptional regulation) and protein synthesis inhibition. Prog Neurobiol 51:607-636.
43. Planas AM, Justicia C, Soriano MA, Ferrer I. 1998. Epidermal growth factor receptor in proliferating reactive glia following transient focal ischemia in the rat brain. Glia 23:120-129.
44. Plumier JC, Armstrong JN, Landry J, Babity JM, Robertson HA, Currie RW. 1996. Expression of the 27,000 mol. wt heat shock protein following kainic acid-induced status epilepticus in the rat. Neuroscience 75:849-856.
45. Rajan P, McKay RD. 1998. Multiple routes to astrocytic differentiation in the CNS. J Neurosci 18:3620-3629.
46. Rajan P, Stewart CL, Fink JS. 1995. LIF-mediated activation of STAT proteins after neuronal injury in vivo. NeuroReport 6:2240-2244.
47. Rajan P, Symes AJ, Fink JS. 1996. STAT proteins are activated by ciliary neurotrophic factor in cells of central nervous system origin. J Neurosci Res 43:403-411.
48. Ruff-Jamison S, Zhong Z, Wen Z, Chen K, Darnell JE, Cohen S. 1994. Epidermal growth factor and lipopolysaccharide activate Stat3 transcription factor in mouse liver. J Biol Chem 269:21933-21935.
49. Samanta A, Qian X, Greene MI. 1995. Unexpected transcriptional signals in normal and mitotically defective cells mediated through cytokine and growth factor receptors. DNA Cell Biol 14:921-930.
50. Sanz O, Estrada A, Ferrer I, Planas AM. 1997. Differential cellular distribution and dynamics of Hsp70, cyclooxygenase-2, and c-Fos in the rat brain after transient focal ischemia or kainic acid. Neuroscience 80:221-232.
51. Seidel HM, Milocco LH, Lamb P, Darnell JE Jr, Stein RB, Rosen J. 1995. Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc Natl Acad Sci USA 92: 3041-3045.
52. Shual K, Ziemiecki A, Wilks AF, Harpur AG, Sadowski HB, Gilman MZ, Darnell JE. 1993. Polypeptide signaling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature 366:580-583.
53. Sonnenberg JL, MacGregor-Leon PF, Curran T, Morgan JI. 1989. Dynamic alterations occur in the levels and composition of transcription factor AP1 complexes after seizure. Neuron 3:359-365.
54. Soriano MA, Sanz O, Ferrer I, Planas AM. 1997. Cortical infarct volume is dependent on the ischemic reduction of perifocal cerebral blood flow in a three-vessel intraluminal MCA occlusion/reperfusion model in the rat. Brain Res 747:272-278.
55. Spleiss O, Appel K, Boddeke HWGM, Berger M, Gebicke-Haerter PJ. 1998. Molecular biology of microglia cytokine and chemokine receptors and microglial activation. Life Sci 62:1707-1710.
56. Wagner BJ, Hayes TE, Hoban CJ, Cochran BH. 1990. The SJF binding element confers sis/PDGF inducibility onto the c-fos promoter. EMBO J 9:4477-4484.
57. Wang X, Yue TL, Barone FC, White RF, Gagnon RC, Feuerstein GZ. 1994. Concomitant cortical expression of TNF-α and IL-1β mRNAs follows early response gene expression in transient focal ischemia. Mol Chem Neuropathol 23:103-114.
58. Wang X, Yue TL, Young PR, Barone FC, Feuerstein GZ. 1995. Expression of interleukin-6, c-fos, and zif 268 mRNAs in rat ischemic cortex. J Cereb Blood Flow Metab 15:166-171.
59. Wang X, Barone FC, Aiyar NV, Feuerstein GZ. 1997. Interleukin-1 receptor and receptor antagonist gene expression after focal stroke in rats. Stroke 28:155-161.
60. Wang Y, Fuller GM. 1995. Interleukin-6 and ciliary neurotrophic factor trigger janus kinase activation and early gene response in rat hepatocytes. Gene 162:285-289.
61. Yamasaki Y, Matsuura N, Shozuhara H, Onodera H, Itoyama Y, Kogure K. 1995. Interleukin-1 as a pathogenic mediator of ischemic brain damage in rats. Stroke 26:676-681.
62. Yang X, Chung D, Cepko CL. 1993. Molecular cloning of the murine Jak1 protein tyrosine kinase and its expression in the mouse central nervous system. J Neurosci 13:3006-3017.
63. Yao GL, Kato H, Khalil M, Kiryu S, Kiyama H. 1997. Selective upregulation of cytokine receptor subchain and their intracellular signaling molecules after peripheral nerve injury. Eur J Neurosci 9:1047-1054.
64. Zushi S, Shinomura Y, Kiyohara T, Miyazaki Y, Kondo S, Sugimachi M, Higashimoto Y, Kanayama S, Matsuzawa Y. 1998. STAT3 mediates the survival signal in oncogenic ras-transfected intestinal epithelial cells. Int J Cancer 78:326-330.