Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation

Journal of Neuroscience

Volumn 23, Issue 18, 2003, Pages 7084-7092

  Schubert, Markus ^a   Brazil, Derek P ^a   Burks, Deborah J ^a   Kushner, Jake A ^a   Ye, Jing ^a   Flint, Carrie L ^a   Farhang Fallah, Janet ^a   Dikkes, Pieter ^a   Warot, Xavier M ^a   Rio, Carlos ^a   Corfas, Gabriel ^a   White, Morris F ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Alzheimer's disease; Brain size; Diabetes; Growth factors; Insulin receptor substrates; Irs2; Neuron survival; Tau phosphorylation

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 2; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY GROWTH; BRAIN DEVELOPMENT; BRAIN GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DIABETES MELLITUS; FEMALE; GENE DISRUPTION; HIPPOCAMPUS; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0043127453     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-18-07084.2003     Document Type: Article

References (86)

1. Aberg M, Aberg N, Hedbacker H, Oscarsson J, Eriksson P (2000) Peripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20:2896-2903.
2. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF (2002) Phosphorylation of ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277:1531-1537.
3. Airey DC, Lu L, Williams RW (2001) Genetic control of the mouse cerebellum: identification of quantitative trait loci modulating size and architecture. J Neurosci 21:5099-5109.
4. Anlar B, Sullivan KA, Feldman EL (1999) Insulin-like growth factor-I and central nervous system development. Horm Metab Res 31:120-125.
5. Bektas A, Warram JH, White MF, Krolewski AS, Doria A (1999) Exclusion of insulin receptor substrate 2 (IRS-2) as a major locus for early-onset autosomal dominant type 2 diabetes. Diabetes 48:640-642.
6. Bernal D, Almind K, Yenush L, Ayoub M, Zhang Y, Rosshani L, Larsson C, Pedersen O, White MF (1998) IRS-2 amino acid polymorphisms are not associated with random type 2 diabetes among Caucasians. Diabetes 47:976-979.
7. Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371-1378.
8. Birnbaum MJ (2002) RhoGAP: the next big thing for small mice? Dev Cell 2:521-523.
9. Bjornholm M, He AR, Attersand A, Lake S, Liu SC, Lienhard GE, Taylor S, Arner P, Zierath JR (2002) Absence of functional insulin receptor substrate-3 (IRS-3) gene in humans. Diabetologia 45:1697-1702.
10. Blass JP, Gibson GE, Hoyer S (2002) The role of the metabolic lesion in Alzheimer's disease. J Alzheimers Dis 4:225-232.
11. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating inhibiting a Forkhead transcription factor. Cell 96:857-868.
12. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Good-year LJ, Kahn CR (1998) A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2:559-569.
13. Burks DJ, de Mora JF, Schubert M, Withers DJ, Myers MG, Towery HH, Altamuro SL, Flint CL, White MF (2000) IRS-2 pathways integrate female reproduction and energy homeostasis. Nature 407:377-382.
14. Carantoni M, Zuliani G, Munari MR, D'Elia K, Palmieri E, Fellin R (2000) Alzheimer disease and vascular dementia: relationships with fasting glucose and insulin levels. Dement Geriatr Cogn Disord 11:176-180.
15. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369.
16. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
17. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
18. Dentremont KD, Ye P, D'Ercole AJ, O'Kusky JR (1999) Increased insulin-like growth factor-I (IGF-I) expression during early postnatal development differentially increases neuron number and growth in medullary nuclei of the mouse. Brain Res Dev Brain Res 114:135-141.
19. DiCicco-Bloom E, Black IB (1998) Insulin growth factors regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Proc Natl Acad Sci USA 85:4066-4070.
20. Drechsel DN, Hyman AA, Cobb MH, Kirschner MW (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141-1154.
21. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, Greenberg ME (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661-665.
22. Dutta S, Gannon M, Peers B, Wright C, Bonner-Weir S, Montminy M (2001) PDX:PBX complexes are required for normal proliferation of pancreatic cells during development. Proc Natl Acad Sci USA 98:1065-1070.
23. Fantin VR, Lavan BE, Wang Q, Jenkins NA, Gilbert DJ, Copeland NG, Keller SR, Lienhard GE (1999) Cloning, tissue expression, and chromosomal location of the mouse insulin receptor substrate 4 gene. Endocrinology 140:1329-1337.
24. Fernyhough P, Mill JF, Roberts JL, Ishii DN (1989) Stabilization of tubulin mRNAs by insulin and insulin-like growth factor I during neurite formation. Brain Res Mol Brain Res 6:109-120.
25. Finch CE, Cohen DM (1997) Aging, metabolism, and Alzheimer disease: review and hypotheses. Exp Neurol 143:82-102.
26. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578-1584.
27. Frolich L, Blum-Degen D, Riederer P, Hoyer S (1999) A disturbance in the neuronal insulin receptor signal transduction in sporadic Alzheimer's disease. Ann NY Acad Sci 893:290-293.
28. Garcia A, Cereghini S, Sontag E (2000) Protein phosphatase 2A and phosphatidylinositol 3-kinase regulate the activity of Sp1-responsive promoters. J Biol Chem 275:9385-9389.
29. Gasparini L, Gouras GK, Wang R, Gross RS, Beal MF, Greengard P, Xu H (2001) Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J Neurosci 21:2561-2570.
30. Gasparini L, Netzer WJ, Greengard P, Xu H (2002) Does insulin dysfunction play a role in Alzheimer's disease? Trends Pharmacol Sci 23:288-293.
31. Goldowitz D, Hamre K (1998) The cells and molecules that make a cerebellum. Trends Neurosci 21:375-382.
32. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.
33. Heidenreich KA, Toledo SP (1989) Insulin receptors mediate growth effects in cultured fetal neurons. I. Rapid stimulation of protein synthesis. Endocrinology 125:1451-1457.
34. Hong M, Lee VM (1997) Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J Biol Chem 272:19547-19553.
35. Horner PJ, Gage FH (2000) Regenerating the damaged central nervous system. Nature 407:963-969.
36. Hoyer S (2002) The aging brain. Changes in the neuronal insulin/insulin receptor signal transduction cascade trigger late-onset sporadic Alzheimer disease (SAD). A mini-review. J Neural Transm 109:991-1002.
37. Kaytor MD, Orr HT (2002) The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol 12:275-278.
38. Kulkarni RN, Bruning JC, Winnay JN, Postic C, Magnuson MA, Kahn CR (1999) Tissue-specific knockout of the insulin receptor in pancreatic β cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 96:329-339.
39. Kushner JA, Ye J, Schubert M, Burks DJ, Dow MA, Flint CL, Dutta S, Wright CV, Montminy MR, White MF (2002) Pdxl restores beta cell function in Irs2 knockout mice. J Clin Invest 109:1193-1201.
40. Lavan BE, Lane WS, Lienhard GE (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.
41. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405:360-364.
42. Liolitsa D, Powell J, Lovestone S (2002) Genetic variability in the insulin signalling pathway may contribute to the risk of late onset Alzheimer's disease. J Neurol Neurosurg Psychiatry 73:261-266.
43. Liu JP, Baker J, Perkins JA, Robertson EJ, 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.
44. Lovestone S (1999) Diabetes and dementia: is the brain another site of end-organ damage? Neurology 53:1907-1909.
45. Lovestone S, Reynolds CH (1997) The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78:309-324.
46. Lu L, Airey DC, Williams RW (2001) Complex trait analysis of the hippocampus: mapping and biometric analysis of two novel gene loci with specific effects on hippocampal structure in mice. J Neurosci 21:3503-3514.
47. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 20:27-39.
48. Ludwig T, Eggenschwiler J, Fisher P, D'Ercole AJ, Davenport ML, Efstratiadis A (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 177:517-535.
49. Luo J, Balkin N, Stewart J, Sarwark J, Charrow J, Nye J (2000) Neural tube defects and the 13q deletion syndrome: evidence for a critical region in 13q33-34. Am J Med Genet 91:227-230.
50. Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A (2001) Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev Biol 229:141-162.
51. Ma XH, Zhong P, Gu Z, Feng J, Yan Z (2003) Muscarinic potentiation of GABA(A) receptor currents is gated by insulin signaling in the prefrontal cortex. J Neurosci 23:1159-1168.
52. Michael MD, Kulkarni RN, Postic C, Previs S, Shulman GI, Magnuson MA, Kahn CR (2000) Loss of insulin signaling in hepatocyte leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 6:87-97.
53. Mill JF, Chao MV, Ishii DN (1985) Insulin, insulin-like growth factor II, and nerve growth factor effects on tubulin mRNA levels and neurite formation. Proc Natl Acad Sci USA 82:7126-7130.
54. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM (1999) Diabetes mellitus and the risk of dementia: the Rotterdam Study. Neurology 53:1937-1942.
55. Pixley SK, Danogoria NS, Odoms KK, Hastings L (2000) Effects of insulin-like growth factor 1 on olfactory neurogensis in vivo and in vitro. Ann NY Acad Sci 855:244-247.
56. Previs SF, Withers DJ, Ren JM, White MF, Shulman GI (2000) Contrasting effects of IRS-1 vs IRS-2 gene disruption on carbohydrate and lipid metabolism in vivo. J Biol Chem 275:38990-38994.
57. Recio-Pinto E, Lang FF, Ishii DN (1984) Insulin and insulin-like growth factor II permit nerve growth factor binding and the neurite formation response in cultured human neuroblastoma cells. Proc Natl Acad Sci USA 81:2562-2566.
58. Rodgers EE, Theibert AB (2002) Functions of PI 3-kinase in development of the nervous system. Int J Dev Neurosci 20:187-197.
59. Rui L, Yuan M, Frantz D, Shoelson S, White MF (2002) SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem 277:42394-42398.
60. Russell JW, Windebank AJ, Schenone A, Feldman EL (1998) Insulin-like growth factor-I prevents apopstis in neurons after nerve growth factor withdrawal. J Neurobiol 36:455-467.
61. Saltiel AR (2001) New perspectives into the molecular pathogenesis and treatment of type 2 diabetes. Cell 104:517-529.
62. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766.
63. Selkoe DJ, Podlisny MB (2002) Deciphering the genetic basis of Alzheimer's disease. Annu Rev Genomics Hum Genet 3:67-99.
64. Sharma J, Bakshi R, Lee D, Hachinski V, Chan RKT (2003) Cerebral atrophy in young, otherwise healthy patients with type 1 diabetes mellitus. Neurology [Suppl] 35:3-29.
65. Solano DC, Sironi M, Bonfini C, Solerte SB, Govoni S, Racchi M (2000) Insulin regulates soluble amyloid precursor protein release via phosphatidyl inositol 3 kinase-dependent pathway. FASEB J 14:1015-1022.
66. Sontag E, Nunbhakdi-Craig V, Lee G, Bloom GS, Mumby MC (1996) Regulation of the phosphorylation state and microtubule-binding activity of tau by protein phosphatase 2A. Neuron 17:1201-1207.
67. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White III CL, Mumby MC, Bloom GS (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 274:25490-25498.
68. Sordella R, Classon M, Hu KQ, Matheson SF, Brouns MR, Fine B, Zhang L, Takami H, Yamada Y, Settleman J (2002) Modulation of CREB activity by the Rho GTPase regulates cell and organism size during mouse embryonic development. Dev Cell 2:553-565.
69. Spillantini MG, Goedert M (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci 21:428-433.
70. Stein TD, Johnson JA (2002) Lack of neurodegeneration intransgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J Neurosci 22:7380-7388.
71. Stolk RP, Breteler MM, Ott A, Pols HA, Lamberts SW, Grobbee DE, Hofman A (1997) Insulin and cognitive function in an elderly population. The Rotterdam Study. Diabetes Care 20:792-795.
72. Strom RC, Williams RW (1998) Cell production and cell death in the generation of variation in neuron number. J Neurosci 18:9948-9953.
73. Sun XJ, Miralpeix M, Myers Jr MG, Glasheen EM, Backer JM, Kahn CR, White MF (1992) The expression and function of IRS-1 in insulin signal transmission. J Biol Chem 267:22662-22672.
74. Sun XJ, Wang LM, Zhang Y, Yenush L, Myers Jr MG, Glasheen EM, Lane WS, Pierce JH, White MF (1995) Role of IRS-2 in insulin and cytokine signalling. Nature 377:173-177.
75. Towfighi J, Ladda RL, Sharkey FE (1987) Purkinje cell inclusions and "atelencephaly" in 13q-chromosomal syndrome. Arch Pathol Lab Med 11I:146-150.
76. Uchida T, Myers Jr MG, White MF (2000) IRS-4 mediates activation of PKB/Akt during insulin stimulation without inhibition of apoptosis. Mol Cell Biol 20:126-138.
77. Vaccarino F, Schwartz ML, Raballo R, Rhee L, Rhee J, Zhou M, Doetschman TC, Coffin J, Wyland J, Hung Y (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2:246-253.
78. Weggen S, Eriksen JL, Das P, Sagi SA, Wang R, Pietrzik CU, Findlay KA, Smith TE, Murphy MP, Bulter T, Kang DE, Marquez-Sterling N, Golde TE, Koo EH (2001) A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity. Nature 414:212-216.
79. White MF (2002) IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 283:E413-E422.
80. Withers DJ, Gutierrez JS, Towery H, Burks DJ, Ren JM, Previs S, Zhang Y, Bernal D, Pons S, Shulman GI, Bonner-Weir S, White MF (1998) Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391:900-904.
81. Withers DJ, Burks DJ, Towery HH, Altamuro SL, Flint CL, White MF (1999) Irs-2 coordinates Igf-1 receptor-mediated beta-cell development and peripheral insulin signalling. Nat Genet 23:32-40.
82. Woods KA, Camacho-Hubner C, Savage MO, Clark AJL (1996) Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med 335:1363-1367.
83. Yamada M, Ohnishi O, 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 cultured cerebral cortical neurons. J Biol Chem 272:30334-30339.
84. Ye P, Xing Y, Dai Z, D'Ercole AJ (1996) In vivo actions of insulin-growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-1 increases proliferation of granule cell progenitors. Brain Res Dev Brain Res 95:44-54.
85. Yenush L, White MF (1997) The IRS-signaling system during insulin and cytokine action. BioEssays 19:491-500.
86. Zackenfels K, Oppenheim RW, Rohrer H (1995) Evidence for an important role of IGF-I and IGF-II for the early development of chick sympathetic neurons. Neuron 14:731-741.