Activation of STAT3 signaling in axotomized neurons and reactive astrocytes after fimbria-fornix transection

Experimental Brain Research

Volumn 165, Issue 4, 2005, Pages 520-531

  Schubert, Klaus Oliver ^a   Naumann, Thomas ^a   Schnell, Oliver ^a   Zhi, Qixia ^a   Steup, Andreas ^a   Hofmann, Hans Dieter ^a   Kirsch, Matthias ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Axotomy; Ciliary neurotrophic factor; Cytokine signaling; Leukemia inhibitory factor; Stat3

Indexed keywords

CILIARY NEUROTROPHIC FACTOR RECEPTOR; CYTOKINE RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; LEUKEMIA INHIBITORY FACTOR RECEPTOR; RECEPTOR SUBUNIT; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN FORNIX; BRAIN INJURY; CELL TYPE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; GABAERGIC SYSTEM; HIPPOCAMPAL FIMBRIA; IMMUNOCYTOCHEMISTRY; MOUSE; MUTANT; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SEPTUM PELLUCIDUM; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; AXOTOMY; CILIARY NEUROTROPHIC FACTOR; CYTOKINES; DENERVATION; DNA PRIMERS; FORNIX (BRAIN); GAMMA-AMINOBUTYRIC ACID; IN SITU HYBRIDIZATION; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; MICE; MICE, KNOCKOUT; NEURAL CELL ADHESION MOLECULES; NEURONS; PARASYMPATHETIC NERVOUS SYSTEM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEPTUM OF BRAIN; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 24044469059     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-005-2330-x     Document Type: Article

References (60)

1. Acarin L, Gonzalez B, Castellano B (2000) STAT3 and NFkappaB activation precedes glial reactivity in excitotoxically injured young cortex but not in the corresponding distal thalamic nuclei. J Neuropathol Exp Neurol 59:151-163
2. Banner IR, Moayeri NN, Patterson PH (1997) Leukemia inhibitory factor is expressed in astrocytes following cortical brain injury. Exp Neurol 14:1-9
3. 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
4. Bugga L, Gadient RA, Kwan K, Stewart CL, Patterson PH (1997) Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor. J Neurobiol 36:509-524
5. Cheema SS, Arumugam D, Murray SS, Bartlett PF (1998) Leukemia inhibitory factor maintains choline acetyltransferase in vivo. Neuroreport 9:363-366
6. Choi J-S, Kim SY, Cha J-H, Choi Y-S, Sung K-W, Oh ST, Kim ON, Chung J-W, Chun M-H, Lee SB, Lee M-Y (2003) Upregulation of gp130 and STAT3 activation in the rat hippocampus following transient forebrain ischemia. Glia 41:237-246
7. Deller T, Frotscher M (1997) Lesion-induced plasticity of central neurons: sprouting of single fibres in the rat hippocampus after unilateral entorhinal cortex lesion. Prog Neurobiol 53:687-727
8. Derouet D, Rousseau F, Alfonis F, Froger J, Hermann J, Barbier F, Perret D, Diveu C, Guillet C, Preisser L, Dumont A, Barbado M, Morel A, deLapeyriere O, Gascan H, Chevalier S (2004) Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc Natl Acad Sci USA 101:4827-4832
9. Eddleston M, Mucke L (1993) Molecular profile of reactive astrocytes-implications for their role in neurological disease. Neuroscience 54:15-36
10. Escary JL, Perreau J, Dumenil D, Ezine S, Brulet P (1993) Leukaemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation. Nature 363:361-364
11. Freund TF (1989) GABAergic septohippocampal neurons contain parvalbumin. Brain Res 478:375-381
12. Gaykema RPA, van der Kuil LB, Hersh LB, Luiten PGM (1991) Patterns of direct projections from the hippocampus to the medial septum-diagonal band complex. Anterograde tracing with Phaseolus vulgaris leuco-agglutinin combined with immunohistochemistry of choline acetyltransferase. Neuroscience 43:349-360
13. Guthrie KM, Woods AG, Nguyen T, Gall CM (1997) Astroglial ciliary neurotrophic factor mRNA expression is increased in fields of axonal sprouting in deafferented hippocampus. J Comp Neurol 386:137-148
14. Haas CA, Hofmann H-D, Kirsch M (1998) Expression of CNTF/ LIF receptor components and activation of STAT3 signaling in axotomized facial motoneurons: evidence for a sequential postlesional function of the cytokines. J Neurobiol 41:559-571
15. Hagg T, Quon D, Higaki J, Varon S (1992) Ciliary neurotrophic factor prevents neuronal degeneration and promotes low affinity NGF receptor expression in the adult rat CNS. Neuron 8:145-158
16. Hefti F (1986) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6:2155-2162
17. Heinrich PC, Behrmann I, Müller-Newen G, Schaper F, Graeve L (1998) Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 334:297-314
18. Hollerbach E, Haas CA, Hildebrandt H, Frotscher M, Naumann T (1998) Region-specific activation of microglial cells in the rat septal complex following fimbria-fornix transection. J Comp Neurol 390:481-496
19. Hudgins SN, Levison SW (1998) Ciliary neurotrophic factor stimulates astroglial hypertrophy in vivo and in vitro. Exp Neurol 150:171-182
20. Ip NY, Wiegand SJ, Morse J, Rudge JS (1993) Injury-induced regulation of ciliary neurotrophic factor mRNA in the adult rat brain. Eur J Neurosci 5:25-33
21. Justicia C, Gabriel C, Planas AM (2000) Activation of the JAK/STAT pathway following transient focal cerebral ischemia: signaling through JAK1 and Stat3 in astrocytes. Glia 30:253-270
22. Kahn MA, Ellison JA, Speight GJ, de Vellis J (1995) CNTF regulation of astrogliosis and the activation of microglia in the developing rat central nervous system. Brain Res 685:55-67
23. Kahn MA, Huang CJ, Caruso A, Barresi V, Nazarian R, Condorelli DF, DeVellis 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
24. Kermer P, Naumann T, Bender R, Frotscher M (1995) Fate of GABAergic neurons after fimbria-fornix transection as revealed by in situ hybridization for glutamate decarboxylase mRNA and parvalbumin immunocytochemistry. J Comp Neurol 362:385-399
25. Kirsch M, Terheggen U, Hofmann H-D (2003) Ciliary neurotrophic factor is an early lesion-induced retrograde signal for axotomized facial motoneurons. Mol Cell Neurosci 24:130-138
26. Koblar SA, Turnley AM, Classon BJ, Reid KL, Ware CB, Cheema SS, Murphy M, Bartlett PF (1998) Neural precursor cell differentiation requires signaling through the leukemia inhibitory factor receptor. Proc Natl Acad Sci USA 95:3178-3181
27. Lee M-Y, Naumann T, Kirsch M, Frotscher M, Hofmann H-D (1997a) Transient upregulation of ciliary neurotrophic factor receptor a mRNA in axotomized rat septal neurons. Eur J Neurosci 9:622-626
28. Lee M-Y, Deller T, Kirsch M, Frotscher M, Hofmann H-D (1997b). Differential regulation of CNTF and CNTF receptor a expression in astrocytes and neurons of the fascia dentata following entorhinal cortex lesion. J Neurosci 17:1137-1146
29. Levison SW, Ducceschi MH, Young GM, Wood TL (1996) Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp Neurol 141:256-268
30. Levison SW, Hudgins SN, Crawford J (1998) Ciliary neurotrophic factor stimulates nuclear hypertrophy and GFAP content of cultured astrocytes. Brain Res 803:189-193
31. Levy DE, Lee C-K (2002) What does Stat3 do?. J Clin Invest 109:1143-1148
32. Linker RA, Mäurer M, Gaupp S, Martini R, Holtmann B, Giess R, Rieckmann P, Lassmann H, Toyka KV, Sendtner M, Gold R (2002) CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat Med 8:620-624
33. Lisovoski F, Akli S, Peltekian E, Vigne E, Haase G, Perricaudet M, Dreyfus PA, Kahn A, Peschanski M (1997) Phenotypic alteration of astrocytes induced by ciliary neurotrophic factor in the intact adult brain, as revealed by adenovirus-mediated gene transfer. J Neurosci 17:7228-7236
34. Manthorpe M, Louis J-L, Hagg T, Varon S (1993) Ciliary neuronotrophic factor. In: Loughlin SE, Fallon JH (eds) Neurotrophic factors. Academic, New York, pp 443-473
35. Martin A, Hofmann H-D, Kirsch M (2003) Glial reactivity in ciliary neurotrophic factor-deficient mice after optic nerve lesion. J Neurosci 23:5416-5424
36. Masu Y, Wolf E, Holtmann B, Sendtner M, Brem G, Thoenen H (1993) Disruption of the CNTF gene results in motor neuron degeneration. Nature 365:27-32
37. Moon C, Yoo JY, Matarazzo V, Sung YK, Kim EJ, Ronnett GV (2002) Leukemia inhibitory factor inhibits neuronal terminal differentiation through STAT3 activation. Proc Natl Acad Sci USA 99:9015-9020
38. Nakashima K, Wiese S, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Yoshida K, Kishimoto T, Sendtner M, Taga T (1999a) Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J Neurosci 19:5429-5434
39. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T (1999b) Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479-482
40. Naumann T, Peterson GM, Frotscher M (1992) Fine structure of rat septohippocampal neurons: II A time course analysis following axotomy. J Comp Neurol 325:219-242
41. Naumann T, Kermer P, Frotscher M (1994) Fine structure of rat hippocampal neurons: III Recovery of choline acetyltransferase immunoreactivity after fimbria-fornix transection. J Comp Neurol 348:1-10
42. Naumann T, Straube A, Frotscher M (1997) Recovery of ChAT immunoreactivity in axotomized rat cholinergic septal neurons despite reduced NGF receptor expression. Eur J Neurosci 9:1340-1349
43. NTR leads to long-lasting increases in the number of basal forebrain cholinergic neurons. J Neurosci 22:2409-2418
44. Naumann T, Schnell O, Zhi Q, Kirsch M, Schubert O, Sendtner M, Hofmann H-D (2003) Endogenous ciliary neurotrophic factor protects GABAergic, but not cholinergic, septohippocampal neurons following fimbria-fornix transection. Brain Pathol 13:309-321
45. Oyesiku NM, Wilcox JN, Wigston DJ (1997) Changes in expression of ciliary neurotrophic factor (CNTF) and CNTF-receptor a after spinal cord injury. J Neurobiol 32:251-261
46. Panni MK, Atkinson J, Sofroniew MV (1998) Leukemia inhibitory factor prevents loss of p75-nerve growth factor receptor immunoreactivity in medial septal neurons following fimbria-fornix lesion. Neuroscience 89:1113-1121
47. Rajan P, McKay RDG (1998) Multiple routes to astrocytic differentiation in the CNS. J Neurosci 18:3620-3629
48. Rajan P, Stewart CL, Fink JS (1995) LIF-mediated activation of STAT proteins after neural injury in vivo. Neuroreport 6:2240-2244
49. Schwaiger F-W, Hager G, Schmitt AB, Horvat A, Streif R, Spitzer C, Gamal S, Breuer S, Brook GA, Naciemiento W, Kreutzberg GW (2000) Peripheral but not central axotomy induces changes in Janus kinase (JAK) and signal transducers and activators of transcription (STAT). Eur J Neurosci 12:1165-1176
50. Schweizer U, Gunnersen J, Karch C, Wiese S, Holtmann B, Takeda K, Akira S, Sendtner M (2002) Conditional gene ablation of Stat3 reveals differential signaling requirements for survival of motoneurons during development and after nerve injury in the adult. J Cell Biol 156:287-297
51. Sendtner M, Carroll P, Holtmann B, Hughes RA, Thoenen H (1994) Ciliary neurotrophic factor. J Neurobiol 25:1436-1453
52. Sendtner M, Götz R, Holtmann B, Escary JL, Masu Y, Carroll P, Wolf E, Brem G, Brulet P, Thoenen H (1996) Cryptic physiological trophic support of motoneurons by LIF revealed by double gene targeting of CNTF and LIF. Curr Biol 6:686-694
53. Sofroniew MV, Galletly NP, Isacson O, Svendsen CN (1990) Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science 247:338-342
54. Sofroniew MV, Howe CL, Mobley WC (2001) Nerve growth factor signalling, neuroprotection, and neural repair. Ann Rev Neurosci 24:1217-1281
55. 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. J Biol Chem 279:19936-19947
56. Steward O, Kelly MS, Torre ER (1993) The process of reinnervation in the dendate gyrus of adult rats: temporal relationship between changes in the levels of glial fibrillary acidic protein (GFAP) and GFAP mRNA in reactive astrocytes. Exp Neurol 124:167-183
57. Suzuki S, Tanaka K, Nogawa S, Dembo T, Fukuuchi Y (2001) Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rat. Exp Neurol 170:63-71
58. Turnley AM, Bartlett PF (2000) Cytokines that signal through the leukemia inhibitory factor receptor-beta complex in the nervous system. J Neurochem 74:889-899
59. NTR -deficient mice. Neuroscience 110:641-651
60. Xia X, Hofmann H-D, Deller T, Kirsch M (2002) Induction of STAT3 signaling in activated astrocytes and sprouting neurons following entorhinal cortex lesion in adult rats. Mol Cell Neurosci 21:379-392