Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination

Journal of Neuroscience

Volumn 23, Issue 20, 2003, Pages 7710-7718

  Mason, Jeffrey L ^a   Xuan, Shouhong ^a   Dragatsis, Ioannis ^a,b   Efstratiadis, Argiris ^a   Goldman, James E ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Apoptosis; Demyelination; Macrophages; Oligodendrocyte; Progenitors; Transgenic

Indexed keywords

CUPRIZONE; SOMATOMEDIN; SOMATOMEDIN C RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; GENETIC CODE; GENETIC RECOMBINATION; MACROPHAGE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR INTRINSIC ACTIVITY; REMYELINIZATION; SIBLING; SIGNAL TRANSDUCTION; STEM CELL;

EID: 0042922772     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-20-07710.2003     Document Type: Article

References (46)

1. Arnett HA, Mason JL, Marino M, Suzuki K, Matsushima GK, Ting JP-Y (2001) TNF α promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 4:1116-1122.
2. Ashkenazi A, Dixit VM (1999) Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11:255-260.
3. Barres BA, Schmid R, Sendnter M, Raff MC (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118:283-295.
4. Blakemore WF, Keirstead HS (1999) The origin of remyelinating cells in the central nervous system. J Neuroimmunol 98:69-76.
5. Cannella B, Pitt D, Capello E, Raine CS (2000) Insulin-like growth factor-1 fails to enhance central nervous system myelin repair during autoimmune demyelination. Am J Pathol 157:933-943.
6. Chang A, Tourtellotte WW, Rudick R, Trapp BD (2002) Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 346:165-173.
7. Cheng CM, Joncas G, Reinhardt RR, Farrer R, Quarles R, Janssen J, McDonald MP, Crawley JN, Powell-Braxton L, Bondy CA (1998) Biochemical and morphometric analyses show that myelination in the insulin-like growth factor 1 null brain is proportionate to its neuronal composition. J Neurosci 18:5673-5681.
8. Di Cola G, Cool MH, Accili D (1997) Hypoglycemic effect of insulin-like growth factor-1 in mice lacking insulin receptors. J Clin Invest 99:2538-2544.
9. Dietrich P, Dragatsis I, Xuan S, Zeitlin S, Efstratiadis A (2000) A conditional mutagenesis in mice with heat shock promoter-driven cre transgenes. Mamm Genome 11:196-205.
10. Dopp JM, Mackenzie-Graham A, Otero GC, Merrill JE (1997) Differential expression, cytokine modulation, and specific functions of type-1 and type-2 tumor necrosis factor receptors in rat glia. J Neuroimmunol 75:104-112.
11. Dragatsis I, Zeitlin S (2000) CamKIIα-cre transgene expression and recombination patterns in the mouse brain. Genesis 26:133-135.
12. Gensert JM, Goldman JE (1997) Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19:197-203.
13. Gensert JM, Goldman JE (2001) Heterogeneity of cycling progenitors in the adult mammalian cortex and white matter. J Neurobiol 48:75-86.
14. Haridas V, Darnay BG, Natarajan K, Heller R, Aggarwal BB (1998) Overexpression the p80 TNF receptor leads to TNF-dependent apoptosis, nuclear factor-κB activation, and c-Jun kinase activation. J Immunol 160:3152-3162.
15. Hinks GL, Franklin RJ (1999) Distinctive patterns of PDGF-A, FGF-2, IGF-I, and TGF-β1 gene expression during remyelination of experimentally-induced spinal cord demyelination. Mol Cell Neurosci 14:153-168.
16. Hiremath MM, Saito Y, Knapp GW, Ting JP-Y, Suzuki K, Matsushima GK (1998) Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol 92:38-49.
17. Li W, Quigley L, Yao D-L, Hudson LD, Brenner M, Zhang BJ, Brocke S, McFarland HF, Webster HD (1998) Chronic relapsing experimental autoimmune encephalomyelitis: effects of insulin-like growth factor-I treatment on clinical deficits, lesion severity, glial responses, and blood brain barrier defects. J Neuropathol Exp Neurol 57:426-438.
18. Liu J-P, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) Mice carrying null mutations of the genes encoding the insulin-like growth factor 1 (igf1) and type-1 IGF receptor (igf1r). Cell 75:59-72.
19. Liu X, Yao D-L, Bondy CA, Brenner M, Hudson LD, Zhou J, Webster Hd (1994) Astrocytes express insulin-like growth factor-1 (IGF-1) and its binding protein, IGFBP-2, during demyelination induced by experimental autoimmune encephalomyelitis. Mol Cell Neurosci 5:418-430.
20. Liu X, Linnington C, Webster HD, Lassmann S, Yao DL, Hudson LD, Wekerle H, Kreutzberg GW (1997) Insulin-like growth factor-I treatment reduces immune cell responses in acute non-demyelinative experimental autoimmune encephalomyelitis. J Neurosci 47:531-538.
21. Lucchinetti CF, Bruck W, Rodriguez M, Lassmann H (1996) Distinct patterns of multiple sclerosis pathology indicates heterogeneity in pathogenesis. Brain Pathol 6:259-274.
22. Ludwin SK (1978) Central nervous system demyelination and remyelination in the mouse. Lab Invest 39:597-612.
23. + cycling progenitors in the adult forebrain white matter respond differentially to PDGF-AA, FGF-2 and IGF-1. Mol Cell Neurosci 20:30-42.
24. Mason JL, Jones JJ, Taniike M, Suzuki K, Morell P, Matsushima GK (2000a) Mature oligodendrocyte apoptosis precedes IGF-1 production and oligodendrocyte progenitor accumulation and differentiation during demyelination/remyelination. J Neurosci Res 61:251-262.
25. Mason JL, Ye P, Suzuki K, D'Ercole AJ, Matsushima GK (2000b) Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J Neurosci 20:5703-5708.
26. Mason JL, Suzuki K, Chaplin DD, Matsushima GK (2001a) Interleukin-1beta promotes repair of the CNS. J Neurosci 21:7046-7052.
27. Mason JL, Langaman C, Morell P, Suzuki K, Matsushima GK (2001b) Episodic demyelination and subsequent remyelination within the murine central nervous system: changes in axonal calibre. Neuropathol Appl Neurobiol 27:50-58.
28. Matsushima GK, Morell P (2001) The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 11:107-116.
29. McMorris FA, Dubois-Dalq M (1988) Insulin-like growth factor 1 promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. J Neurosci Res 21:199-209.
30. Messersmith DJ, Murtie JC, Le TQ, Frost EE, Armstrong RC (2000) Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J Neurosci Res 62:241-256.
31. Mozell RL, McMorris FA (1991) Insulin-like growth factor I stimulates oligodendrocyte development and myelination in rat aggregate cultures. J Neurosci Res 30:382-390.
32. Ness JK, Wood TL (2002) Insulin-like growth factor I, but not neurotrophin-3, sustains Akt activation and provides long-term protection of immature oligodendrocytes from glutamate-mediated apoptosis. Mol Cell Neurosci 20:476-488.
33. Nishiyama A, Lin X-H, Giese N, Heldin C-H, Stallcup WB (1996) Colocalization of NG2 proteoglycan and PDGF α-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314.
34. + glial cells are distinct from resting and activated microglia. J Neurosci Res 48:299-312.
35. O'Leary MT, Hinks GL, Charlton HM, Franklin RJM (2002) Increasing local levels of IGF-1 mRNA expression using adenoviral vectors does not alter oligodendrocyte remyelination in the CNS of aged rats. Mol Cell Neurosci 19:32-42.
36. Redwine JM, Armstrong RC (1998) In vivo proliferation of oligodendrocyte progenitors expressing PDGFαR during early remyelination. J Neurobiol 37:413-428.
37. Rossant J, McMahon A (1999) "Cre"-ating mouse mutants-a meeting review on conditional mouse genetics. Genes Dev 13:142-145.
38. Sauer B (1998) Inducible gene targeting in mice using the Cre/lox system. Methods 14:381-392.
39. Sidman RL, Abervine JB, Pierce ET (1971) Atlas of the mouse brain and spinal cord. Cambridge, MA: Harvard UP.
40. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
41. Tchelingerian JL, Monge M, Le Saux F, Zalc B, Jacque C (1995) Differential oligodendroglial expression of the tumor necrosis factor receptors in vivo and in vitro. J Neurochem 65:2377-2380.
42. Vallano ML, Beaman-Hall CM, Mathur A, Chen Q (2000) Astrocytes express specific variants of CaM KII delta and gamma, but not alpha and beta, that determine their cellular localizations. Glia 30:154-164.
43. Weiss T Grell M, Siemienski K, Muhlenbeck F, Durkop H, Pfizenmaier K, Scheurich P, Wajant H (1998) TNFR80-dependent enhancement of TNFR60-induced cell death is mediated by TNFR-associated factor 2 and is specific for TNFR60. J Immunol 161:3136-3142.
44. Wolswijk G (1998) Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 18:601-609.
45. Yao D-L, West NR, Bondy CA Brenner M, Hudson LD, Zhou J, Collins GH, Webster HD (1995) Cryogenic spinal cord injury induces astrocytic gene expression of insulin-like growth factor 1 and insulin-like growth factor binding protein 2 during myelin regeneration. J Neurosci Res 40:647-659.
46. Ye P, D'Ercole AJ (1999) Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-α-induced injury. Endocrinology 140:3063-3072.