Activation of the ciliary neurotrophic factor (CNTF) signalling pathway in cortical neurons of multiple sclerosis patients

Brain

Volumn 130, Issue 10, 2007, Pages 2566-2576

  Dutta, Ranjan ^a   McDonough, Jennifer ^a,c   Chang, Ansi ^a   Swamy, Lakshman ^a   Siu, Alan ^a   Kidd, Grahame J ^a   Rudick, Richard ^a   Mirnics, Karoly ^b   Trapp, Bruce D ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c KENT STATE UNIVERSITY   (United States)

Author keywords

CNTF; Gene expression; Multiple sclerosis; Neuroprotection

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR RECEPTOR; GLYCOPROTEIN GP 130; PROTEIN BCL 2; STAT3 PROTEIN;

APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN CORTEX; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCLEROSIS; SIGNAL TRANSDUCTION; STRESS; UPREGULATION; WESTERN BLOTTING;

CILIARY NEUROTROPHIC FACTOR; HUMANS; MOTOR CORTEX; MULTIPLE SCLEROSIS; NERVE GROWTH FACTORS; NEURONS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 34848860192     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm206     Document Type: Article

References (62)

1. Alzheimer C, Werner S. Fibroblast growth factors and neuroprotection. Adv Exp Med Biol 2002; 513: 335-51.
2. Auernhammer CJ, Bousquet C, Melmed S. Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter. Proc Natl Acad Sci USA 1999; 96: 6964-9.
3. Cantwell CA, Sterneck E, Johnson PF. Interleukin-6-specific activation of the C/EBPdelta gene in hepatocytes is mediated by Stat3 and Sp1. Mol Cell Biol 1998; 18: 2108-17.
4. Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003; 4: 299-309.
5. Dallner C, Woods AG, Deller T, Kirsch M, Hofmann HD. CNTF and CNTF receptor alpha are constitutively expressed by astrocytes in the mouse brain. Glia 2002; 37: 374-8.
6. de Almeida LP, Zala D, Aebischer P, Deglon N. Neuroprotective effect of a CNTF-expressing lentiviral vector in the quinolinic acid rat model of Huntington's disease. Neurobiol Dis 2001; 8: 433-46.
7. DeChiara TM, Vejsada R, Poueymirou WT, et al. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell 1995; 83: 313-22.
8. Dutta R, McDonough J, Yin X, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 2006; 59: 478-89.
9. Emerich DF, Winn SR, Hantraye PM, et al. Protective effect of encapsulated cells producing neurotrophic factor CNTF in a monkey model of Huntington's disease. Nature 1997; 386: 395-9.
10. Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain 1997; 120: 393-9.
11. Gardiner NJ, Cafferty WB, Slack SE, Thompson SW. Expression of gp130 and leukaemia inhibitory factor receptor subunits in adult rat sensory neurones: regulation by nerve injury. J Neurochem 2002; 83: 100-9.
12. Giess R, Holtmann B, Braga M, et al. Early onset of severe familial amyotrophic lateral sclerosis with a SOD-1 mutation: potential impact of CNTF as a candidate modifier gene. Am J Hum Genet 2002a; 70: 1277-86.
13. Giess R, Maurer M, Linker R, et al. Association of a null mutation in the CNTF gene with early onset of multiple sclerosis. Arch Neurol 2002b; 59: 407-9.
14. Gouin F, Couillaud S, Cottrel M, Godard A, Passuti N, Heymann D. Presence of leukaemia inhibitory factor (LIF) and LIF-receptor chain (gp190) in osteoclast-like cells cultured from human giant cell tumour of bone. Ultrastructural Distribution Cytokine 1999; 11: 282-9.
15. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998; 334: 297-314.
16. Hoffmann V, Hardt C. A null mutation in the CNTF gene is not associated with early onset of multiple sclerosis. Arch Neurol 2002; 59: 1974-5.
17. Hohlfeld R, Kerschensteiner M, Stadelmann C, Lassmann H, Wekerle H. The neuroprotective effect of inflammation: implications for the therapy of multiple sclerosis. Neurol Sci 2006; 27 (Suppl 1): S1-7.
18. Ip NY, Li YP, van de Stadt I, Panayotatos N, Alderson RF, Lindsay RM. Ciliary neurotrophic factor enhances neuronal survival in embryonic rat hippocampal cultures. J Neurosci 1991; 11: 3124-34.
19. Kelly JF, Elias CF, Lee CE, et al. Ciliary neurotrophic factor and leptin induce distinct patterns of immediate early gene expression in the brain. Diabetes 2004; 53: 911-20.
20. Kerschensteiner M, Gallmeier E, Behrens L, et al. Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation? J Exp Med 1999; 189: 865-70.
21. Kuhlmann T, Remington L, Cognet I, et al. Continued administration of ciliary neurotrophic factor protects mice from inflammatory pathology in experimental autoimmune encephalomyelitis. Am J Pathol 2006; 169: 584-98.
22. Kuroda H, Sugimoto T, Horii Y, Sawada T. Signaling pathway of ciliary neurotrophic factor in neuroblastoma cell lines. Med Pediatr Oncol 2001; 36: 118-21.
23. Lassmann H, Bruck W, Lucchinetti C, Rodriguez M. Remyelination in multiple sclerosis. Mult Scler 1997; 3: 133-6.
24. Leaman DW, Leung S, Li X, Stark GR. Regulation of STAT-dependent pathways by growth factors and cytokines. FASEB J 1996; 10: 1578-88.
25. Lee MY, Deller T, Kirsch M, Frotscher M, Hofmann HD. Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor alpha expression in astrocytes and neurons of the fascia dentata after entorhinal cortex lesion. J Neurosci 1997; 17: 1137-46.
26. Linker RA, Maurer M, Gaupp S, et al. CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation. Nat Med 2002; 8: 620-4.
27. Martino G. How the brain repairs itself: new therapeutic strategies in inflammatory and degenerative CNS disorders. Lancet Neurol 2004; 3: 372-8.
28. Massaro AR. Are there indicators of remyelination in blood or CSF of multiple sclerosis patients? Mult Scler 1998; 4: 228-31.
29. Massaro AR, Soranzo C, Carnevale A. Cerebrospinal-fluid ciliary neurotrophic factor in neurological patients. Eur Neurol 1997; 37: 243-6.
30. Masu Y, Wolf E, Holtmann B, Sendtner M, Brem G, Thoenen H. Disruption of the CNTF gene results in motor neuron degeneration. Nature 1993; 365: 27-32.
31. Middleton G, Hamanoue M, Enokido Y, et al. Cytokine-induced nuclear factor kappa B activation promotes the survival of developing neurons. J Cell Biol 2000; 148: 325-32.
32. Miller RG, Bryan WW, Dietz MA, et al. Toxicity and tolerability of recombinant human ciliary neurotrophic factor in patients with amyotrophic lateral sclerosis. Neurology 1996; 47: 1329-31.
33. Mirnics K, Middleton FA, Marquez A, Lewis DA, Levitt P. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 2000; 28: 53-67.
34. Naka T, Fujimoto M, Kishimoto T. Negative regulation of cytokine signaling: STAT-induced STAT inhibitor. Trends Biochem Sci 1999; 24: 394-8.
35. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000; 343: 938-52.
36. Numata A, Shimoda K, Kamezaki K, et al. Signal transducers and activators of transcription 3 augments the transcriptional activity of CCAAT/enhancer-binding protein alpha in granulocyte colony-stimulating factor signaling pathway. J Biol Chem 2005; 280: 12621-9.
37. Pantano P, Iannetti GD, Caramia F, et al. Cortical motor reorganization after a single clinical attack of multiple sclerosis. Brain 2002; 125: 1607-15.
38. Peterson JW, Bo L, Mork S, Chang A, Trapp BD. Transected neurites, apoptotic neurons and reduced inflammation in cortical MS lesions. Ann Neurol 2001; 50: 389-400.
39. Peterson WM, Wang Q, Tzekova R, Wiegand SJ. Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J Neurosci 2000; 20: 4081-90.
40. Rajan P, Symes AJ, Fink JS. STAT proteins are activated by ciliary neurotrophic factor in cells of central nervous system origin. J Neurosci Res 1996; 43: 403-11.
41. Reddy H, Narayanan S, Arnoutelis R, et al. Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain 2000; 123: 2314-320.
42. Reuss B, Bohlen und HO. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 2003; 313: 139-57.
43. Ribeiro A, Bronk SF, Roberts PJ, Urrutia R, Gores GJ. The transforming growth factor beta(1)-inducible transcription factor TIEG1, mediates apoptosis through oxidative stress. Hepatology 1999; 30: 1490-7.
44. Rocca MA, Mezzapesa DM, Falini A, et al. Evidence for axonal pathology and adaptive cortical reorganization in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis. Neuroimage 2003; 18: 847-55.
45. Schuster B, Kovaleva M, Sun Y, et al. Signaling of human ciliary neurotrophic factor (CNTF) revisited. The interleukin-6 receptor can serve as an alpha-receptor for CTNF. J.Biol Chem 2003; 278: 9528-35.
46. Segal RA, Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 1996; 19: 463-89.
47. Stahl N, Farruggella TJ, Boulton TG, Zhong Z, Darnell JE, Jr, Yancopoulos GD. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 1995; 267: 1349-53.
48. Stockli KA, Lillien LE, Naher-Noe M, et al. Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain. J Cell Biol 1991; 115: 447-59.
49. Taga T, Hibi M, Hirata Y, et al. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 1989; 58: 573-81.
50. Taga T, Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 1997; 15: 797-819.
51. Takahashi R, Yokoji H, Misawa H, Hayashi M, Hu J, Deguchi T. A null mutation in the human CNTF gene is not causally related to neurological diseases. Nat Genet 1994; 7: 79-84.
52. Thoenen H, Sendtner M. Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nat Neurosci 2002; 5 (Suppl): 1046-50.
53. Thome J, Nara K, Foley P, et al. Ciliary neurotrophic factor (CNTF) genotypes: influence on choline acetyltransferase (ChAT) and acetylcholine esterase (AChE) activities and neurotrophin 3 (NT3) concentration in human post mortem brain tissue. J Hirnforsch 1997; 38: 443-51.
54. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998; 338: 278-85.
55. Valable S, Bellail A, Lesne S, et al. Angiopoietin-1-induced PI3-kinase activation prevents neuronal apoptosis. FASEB J 2003; 17: 443-5.
56. Waxman SG. Ions, energy and axonal injury: towards a molecular neurology of multiple sclerosis. Trends Mol Med 2006; 12: 192-5.
57. Weihua X, Hu J, Roy SK, Mannino SB, Kalvakolanu DV. Interleukin-6 modulates interferon-regulated gene expression by inducing the ISGF3 gamma gene using CCAAT/enhancer binding protein-beta(C/EBP-beta). Biochim Biophys Acta 2000; 1492: 163-71.
58. Weinshenker BG. Epidemiology of multiple sclerosis. Neurol Clin 1996; 14: 291-308.
59. Weinshenker BG, Bass B, Rice GP, et al. The natural history of multiple sclerosis: a geographically based study. I. Clinical course and disability. Brain 1989; 112: 133-46.
60. Weisenhorn DM, Roback J, Young AN, Wainer BH. Cellular aspects of trophic actions in the nervous system. Int Rev Cytol 1999; 189: 177-265.
61. Widenfalk J, Lundstromer K, Jubran M, Brene S, Olson L. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 2001; 21: 3457-75.
62. Winter CG, Saotome Y, Levison SW, Hirsh D. A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc Natl Acad Sci USA 1995; 92: 5865-9.