IRS-2 branch of IGF-1 receptor signaling is essential for appropriate timing of myelination

Journal of Neurochemistry

Volumn 107, Issue 4, 2008, Pages 907-917

  Freude, Susanna ^a   Leeser, Uschi ^a   Müller, Marita ^a   Hettich, Moritz M ^a   Udelhoven, Michael ^a   Schilbach, Katharina ^a   Tobe, Kazuyuki ^b   Kadowaki, Takashi ^b   Köhler, Christoph ^a   Schröder, Hannsjörg ^a   Krone, Wilhelm ^a   Brüning, Jens C ^a   Schubert, Markus ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Brain; Insulin receptor substrate 2; Insulin like growth factor 1; Mice; Myelin development

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 2; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MOTOR COORDINATION; MOUSE; MYELINATION; NEUROMUSCULAR FUNCTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAND STRENGTH; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; MYELIN BASIC PROTEINS; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; PSYCHOMOTOR PERFORMANCE; RECEPTOR, IGF TYPE 1; RNA, MESSENGER; ROTAROD PERFORMANCE TEST; SIGNAL TRANSDUCTION; SILVER STAINING; UP-REGULATION;

MUS;

EID: 54349085910     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05631.x     Document Type: Article

References (45)

1. Araki E., Lipes M. A., Patti M. E., Bruning J. C., Haag III. B., Johnson R. S. Kahn C. R. (1994) Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372, 186 190.
2. Barres B. A., Schmid R., Sendnter M. Raff M. C. (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118, 283 295.
3. Bartsch U. (1996) Myelination and axonal regeneration in the central nervous system of mice deficient in the myelin-associated glycoprotein. J. Neurocytol. 25, 303 313.
4. Benjamins J. A. Morell P. (1978) Proteins of myelin and their metabolism. Neurochem. Res. 3, 137 174.
5. Bjornholm M., He A. R., Attersand A., Lake S., Liu S. C., Lienhard G. E., Taylor S., Arner P. Zierath J. R. (2002) Absence of functional insulin receptor substrate-3 (IRS-3) gene in humans. Diabetologia 45, 1697 1702.
6. Brunet A., Bonni A., Zigmond M. J., Lin M. Z., Juo P., Hu L. S., Anderson M. J., Arden K. C., Blenis J. Greenberg M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857 868.
7. Bruning J. C., Gautam D., Burks D. J., Gillette J., Schubert M., Orban P. C., Klein R., Krone W., Muller-Wieland D. Kahn C. R. (2000) Role of brain insulin receptor in control of body weight and reproduction. Science 289, 2122 2125.
8. Cross D. A., Alessi D. R., Cohen P., Andjelkovich M. Hemmings B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785 789.
9. Cui Q. L. Almazan G. (2007) IGF-I-induced oligodendrocyte progenitor proliferation requires PI3K/Akt, MEK/ERK, and Src-like tyrosine kinases. J. Neurochem. 100, 1480 1493.
10. Cui Q. L., Zheng W. H., Quirion R. Almazan G. (2005) Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J. Biol. Chem. 280, 8918 8928.
11. D'Ercole A. J., Ye P. O'Kusky J. R. (2002) Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 36, 209 220.
12. Dangata Y. Y. Kaufman M. H. (1997) Myelinogenesis in the optic nerve of (C57BL × CBA) F1 hybrid mice: a morphometric analysis. Eur. J. Morphol. 35, 3 17.
13. Fantin V. R., Keller S. R., Lienhard G. E. Wang L. M. (1999) Insulin receptor substrate 4 supports insulin- and interleukin 4-stimulated proliferation of hematopoietic cells. Biochem. Biophys. Res. Commun. 260, 718 723.
14. Fantin V. R., Wang Q., Lienhard G. E. Keller S. R. (2000) Mice lacking insulin receptor substrate 4 exhibit mild defects in growth, reproduction, and glucose homeostasis. Am. J. Physiol. Endocrinol. Metab. 278, E127 E133.
15. Garbay B., Heape A. M., Sargueil F. Cassagne C. (2000) Myelin synthesis in the peripheral nervous system. Prog. Neurobiol. 61, 267 304.
16. Hsieh J., Aimone J. B., Kaspar B. K., Kuwabara T., Nakashima K. Gage F. H. (2004) IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J. Cell Biol. 164, 111 122.
17. Kubota N., Tobe K., Terauchi Y. et al. (2000) Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory beta-cell hyperplasia. Diabetes 49, 1880 1889.
18. Lagarde W. H., Benjamin R., Heerens A. T., Ye P., Cohen R. I., Moats-Staats B. M. D'Ercole A. J. (2007) A non-transformed oligodendrocyte precursor cell line, OL-1, facilitates studies of insulin-like growth factor-I signaling during oligodendrocyte development. Int. J. Dev. Neurosci. 25, 95 105.
19. Lavan B. E., Lane W. S. Lienhard G. E. (1997) The 60-kDa phosphotyrosine protein in insulin-treated adipocytes is a new member of the insulin receptor substrate family. J. Biol. Chem. 272, 11439 11443.
20. Liu J. P., Baker J., Perkins A. S., Robertson E. J. Efstratiadis A. (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75, 59 72.
21. Liu S. C., Wang Q., Lienhard G. E. Keller S. R. (1999) Insulin receptor substrate 3 is not essential for growth or glucose homeostasis. J. Biol. Chem. 274, 18093 18099.
22. Luzi P., Zaka M., Rao H. Z., Curtis M., Rafi M. A. Wenger D. A. (2004) Generation of transgenic mice expressing insulin-like growth factor-1 under the control of the myelin basic protein promoter: increased myelination and potential for studies on the effects of increased IGF-1 on experimentally and genetically induced demyelination. Neurochem. Res. 29, 881 889.
23. Mason J. L., Ye P., Suzuki K., D'Ercole A. J. Matsushima G. K. (2000) Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J. Neurosci. 20, 5703 5708.
24. McMorris F. A., Mozell R. L., Carson M. J., Shinar Y., Meyer R. D. Marchetti N. (1993) Regulation of oligodendrocyte development and central nervous system myelination by insulin-like growth factors. Ann. N Y Acad. Sci. 692, 321 334.
25. Nave K. A. (1994) Neurological mouse mutants and the genes of myelin. J. Neurosci. Res. 38, 607 612.
26. Norton W. T. Poduslo S. E. (1973) Myelination in rat brain: method of myelin isolation. J. Neurochem. 21, 749 757.
27. Readhead C. Hood L. (1990) The dysmyelinating mouse mutations shiverer (shi) and myelin deficient (shimld). Behav. Genet. 20, 213 234.
28. Saltiel A. R. (2001) New perspectives into the molecular pathogenesis and treatment of type 2 diabetes. Cell 104, 517 529.
29. Salvati S., Attorri L., Avellino C., Di Biase A. Sanchez M. (2000) Diet, lipids and brain development. Dev. Neurosci. 22, 481 487.
30. Schubert M., Brazil D. P., Burks D. J. et al. (2003) Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 23, 7084 7092.
31. Shinar Y. McMorris F. A. (1995) Developing oligodendroglia express mRNA for insulin-like growth factor-I, a regulator of oligodendrocyte development. J. Neurosci. Res. 42, 516 527.
32. Sun X. J., Miralpeix M., Myers Jr. M. G., Glasheen E. M., Backer J. M., Kahn C. R. White M. F. (1992) Expression and function of IRS-1 in insulin signal transmission. J. Biol. Chem. 267, 22662 22672.
33. Sun X. J., Wang L. M., Zhang Y., Yenush L., Myers Jr. M. G., Glasheen E., Lane W. S., Pierce J. H. White M. F. (1995) Role of IRS-2 in insulin and cytokine signalling. Nature 377, 173 177.
34. Tamemoto H., Kadowaki T., Tobe K., Yagi T., Sakura H., Hayakawa T., Terauchi Y., Ueki K., Kaburagi Y. Satoh S. (1994) Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature 372, 182 186.
35. Tennekoon G. I., Cohen S. R., Price D. L. McKhann G. M. (1977) Myelinogenesis in optic nerve. A morphological, autoradiographic, and biochemical analysis. J. Cell Biol. 72, 604 616.
36. Uchida T., Myers Jr. M. G. White M. F. (2000) IRS-4 mediates protein kinase B signaling during insulin stimulation without promoting antiapoptosis. Mol. Cell. Biol. 20, 126 138.
37. White M. F. (2003) Insulin signaling in health and disease. Science 302, 1710 1711.
38. Withers D. J., Gutierrez J. S., Towery H. et al. (1998) Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391, 900 904.
39. Yamada M., Ohnishi H., Sano S., Nakatani A., Ikeuchi T. Hatanaka H. (1997) Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272, 30334 30339.
40. Ye P., Carson J. D'Ercole A. J. (1995) In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein-1 (IGFBP-1) transgenic mice. J. Neurosci. 15, 7344 7356.
41. Ye P., Li L., Lund P. K. D'Ercole A. J. (2002a) Deficient expression of insulin receptor substrate-1 (IRS-1) fails to block insulin-like growth factor-I (IGF-I) stimulation of brain growth and myelination. Brain Res. Dev. Brain Res. 136, 111 121.
42. Ye P., Li L., Richards R. G., DiAugustine R. P. D'Ercole A. J. (2002b) Myelination is altered in insulin-like growth factor-I null mutant mice. J. Neurosci. 22, 6041 6051.
43. Yenush L. White M. F. (1997) The IRS-signalling system during insulin and cytokine action. Bioessays 19, 491 500.
44. Zaka M., Rafi M. A., Rao H. Z., Luzi P. Wenger D. A. (2005) Insulin-like growth factor-1 provides protection against psychosine-induced apoptosis in cultured mouse oligodendrocyte progenitor cells using primarily the PI3K/Akt pathway. Mol. Cell. Neurosci. 30, 398 407.
45. Zeger M., Popken G., Zhang J., Xuan S., Lu Q. R., Schwab M. H., Nave K. A., Rowitch D., D'Ercole A. J. Ye P. (2007) Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 55, 400 411.