Activation of the PI3K/Akt signal transduction pathway and increased levels of insulin receptor in protein repair-deficient mice

Aging Cell

Volumn 4, Issue 1, 2005, Pages 1-12

  Farrar, Christine ^a   Houser, Carolyn R ^a,b,c   Clarke, Steven ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^d 637 Paul D Boyer Hall ^*  (United States)

Author keywords

Akt; Enlarged brain; IGF I receptor; Iisoaspartate; Insulin receptor; PCMT1

Indexed keywords

ACTIN; BRAIN PROTEIN; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; METHYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN; PROTEIN KINASE B; PROTEIN LEVO ISOASPARTATE(DEXTRO ASPARTATE)O METHYLTRANSFERASE; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; 3 PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE; 3-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INSULIN RECEPTOR SUBSTRATE 1 PROTEIN; INSULIN RECEPTOR SUBSTRATE-1 PROTEIN; ONCOPROTEIN; PROTEIN DEXTRO ASPARTATE METHYLTRANSFERASE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE PHOSPHATASE; PTEN PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; BRAIN WEIGHT; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; HEART; HIPPOCAMPUS; HYPOINSULINEMIA; IMMUNOHISTOCHEMISTRY; INSULIN BLOOD LEVEL; LIVER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TESTIS; WESTERN BLOTTING; ANIMAL; BLOOD; BRAIN; BRAIN CORTEX; C57BL MOUSE; GENETICS; METABOLISM; MOUSE MUTANT; ORGAN SIZE; PATHOLOGY; PHOSPHORYLATION;

ANIMALIA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOOD GLUCOSE; BRAIN; CEREBRAL CORTEX; FEMALE; GLUCOSE TOLERANCE TEST; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SIZE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN D-ASPARTATE-L-ISOASPARTATE METHYLTRANSFERASE; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 23844547049     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9728.2004.00136.x     Document Type: Article

References (61)

1. Abel ED, Kaulbach HC, Tian R, Hopkins JC, Duffy J, Doetschman T, Minnemann T, Boers ME, Hadro E, Oberste-Berghaus C, Quist W, Lowell BB, Ingwall JS, Kahn BB (1999) Cardiac hypertrophy with preserved contractile function after selective deletion of GLUT4 from the heart. J. Clin. Invest. 104, 1703-1714.
2. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 20, 2896-2903.
3. Adams S, DasGupta G, Chalovich JM, Reisler E (1990) Immunological evidence for the binding of caldesmon to the NH2-terminal segment of actin. J. Biol. Chem. 265, 19652-19657.
4. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, Cohen P (1997) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 7, 261-269.
5. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319-335.
6. Baserga R (1999) The IGF-I receptor in cancer research. Exp. Cell. Res. 253, 1-6.
7. Baskin DG, Figlewicz DP, Woods SC, Porte D Jr, Dorsa DM (1987) Insulin in the brain. Annu. Rev. Physiol. 49, 335-347.
8. Brennan TV, Anderson JW, Jia Z, Waygood EB, Clarke S (1994) Repair of spontaneously deamidated HPr phosphocarrier protein catalyzed by the 1-isoaspartate-(D-aspartate)O-methyltransferase. J. Biol. Chem. 269, 24586-24595.
9. Carson MJ, Behringer RR, Brinster RL, McMorris FA (1993) Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 10, 729-740.
10. Casamayor A, Morrice NA, Alessi DR (1999) Phosphorylation of Ser-241 is essential for the activity of 3-phosphoinositide-dependent protein kinase-1: identification of five sites of phosphorylation in vivo. Biochem. J. 342, 287-292.
11. Chavous DA, Jackson FR, O'Connor CM (2001) Extension of the Drosophila lifespan by overexpression of a protein repair methyltransferase. Proc. Natl. Acad. Sci. USA 98, 14814-14818.
12. Cheng X, Ma Y, Moore M, Hemmings BA, Taylor SS (1998) Phosphorylation and activation of cAMP-dependent protein kinase by phosphoinositide-dependent protein kinase. Proc. Natl Acad. Sci. USA 95, 9849-9854.
13. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369.
14. 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.
15. Datta SR, Brunet A, Greenberg ME (1999) Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927.
16. Davidson MB (1987) Effect of growth hormone on carbohydrate and lipid metabolism. Endocr. Rev. 8, 115-131.
17. Diliberto EJ Jr, Axelrod J (1974) Characterization and substrate specificity of a protein carboxymethylase in the pituitary gland. Proc. Natl Acad. Sci. USA 71, 1701-1704.
18. Dominici FP, Hauck S, Argentino DP, Bartke A, Turyn D (2002) Increased insulin sensitivity and upregulation of insulin receptor, insulin receptor substrate (IRS)-1 and IRS-2 in liver of Ames dwarf mice. J. Endocrinol. 173, 81-94.
19. Doyle HA, Gee RJ, Mamula MJ (2003) A failure to repair self-proteins leads to T cell hyperproliferation and autoantibody production. J. Immunol. 171, 2840-2847.
20. Fero ML, Rivkin M, Tasch M, Porter P, Carow CE, Firpo E, Polyak K, Tsai LH, Broudy V, Perlmutter RM, Kaushansky K, Roberts JM (1996) A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27 (Kip1)-deficient mice. Cell 85, 733-744.
21. Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J (1998) Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36, 249-266.
22. Gavin JR, 3rd, Roth J, Neville DM Jr, de Meyts P, Buell DN (1974) Insulin-dependent regulation of insulin receptor concentrations: a direct demonstration in cell culture. Proc. Natl Acad. Sci. USA 71, 84-88.
23. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, Kornblum HI, Liu X, Wu H (2001) Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186-2189.
24. Havrankova J, Roth J, Brownstein M (1978) Insulin receptors are widely distributed in the central nervous system of the rat. Nature 272, 827-829.
25. He XP, Minichiello L, Klein R, McNamara JO (2002) Immunohistochemical evidence of seizure-induced activation of trkB receptors in the mossy fiber pathway of adult mouse hippocampus. J. Neurosci. 22, 7502-7508.
26. Hernandez-Sanchez C, Blakesley V, Kalebic T, Helman L, LeRoith D (1995) The role of the tyrosine kinase domain of the insulin-like growth factor-I receptor in intracellular signaling, cellular proliferation, and tumorigenesis. J. Biol. Chem. 270, 29176-29181.
27. Huebscher KJ, Lee J, Rovelli G, Ludin B, Matus A, Stauffer D, Furst P (1999) Protein isoaspartyl methyltransferase protects from Bax-induced apoptosis. Gene 240, 333-341.
28. Ikegaya Y, Yamada M, Fukuda T, Kuroyanagi H, Shirasawa T, Nishiyama N (2001) Aberrant synaptic transmission in the hippocampal CA3 region and cognitive deterioration in protein-repair enzyme-deficient mice. Hippocampus 11, 287-298.
29. Ingrosso D, D'Angelo S, di Carlo E, Perna AF, Zappia V, Galletti P (2000) Increased methyl esterification of altered aspartyl residues in erythrocyte membrane proteins in response to oxidative stress. Eur. J. Biochem. 267, 4397-4405.
30. Johnson BA, Murray ED Jr, Clarke S, Glass DB, Aswad DW (1987) Protein carboxyl methyltransferase facilitates conversion of atypical 1-isoaspartyl peptides to normal 1-aspartyl peptides. J. Biol. Chem. 262, 5622-5629.
31. Kahn CR, Goldfine ID, Neville DM Jr, De Meyts P (1978) Alterations in insulin binding induced by changes in vivo in the levels of glucocorticoids and growth hormone. Endocrinology 103, 1054-1066.
32. Kim E, Lowenson JD, Clarke S, Young SG (1999) Phenotypic analysis of seizure-prone mice lacking 1-isoaspartate (D-aspartate) O-methyltransferase. J. Biol. Chem. 274, 20671-20678.
33. Kim E, Lowenson JD, MacLaren DC, Clarke S, Young SG (1997) Deficiency of a protein-repair enzyme results in the accumulation of altered proteins, retardation of growth, and fatal seizures in mice. Proc. Natl Acad. Sci. USA 94, 6132-6137.
34. Klepper J, Wang D, Fischbarg J, Vera JC, Jarjour IT, O'Driscoll KR, De Vivo DC (1999) Defective glucose transport across brain tissue barriers: a newly recognized neurological syndrome. Neurochem. Res. 24, 587-594.
35. Kozma SC, Thomas G (2002) Regulation of cell size in growth, development and human disease: PI3K, PKB and S6K. Bioessays 24, 65-71.
36. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P, Flavell RA (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325-337.
37. Landgraf R, Landraf-Leurs MM, Weissmann A, Horl R, von Werder K, Scriba PC (1977) Prolactin: a diabetogenic hormone. Diabetologia 13, 99-104.
38. Lanthier J, Desrosiers RR (2004) Protein 1-isoaspartyl methyltransferase repairs abnormal aspartyl residues accumulated in vivo in type-1 collagen and restores cell migration. Exp. Cell Res. 293, 96-105.
39. Lopaczynski W, Terry C, Nissley P (2000) Autophosphorylation of the insulin-like growth factor I receptor cytoplasmic domain. Biochem. Biophys. Res. Commun. 279, 955-960.
40. Lowenson JD, Kim E, Young SG, Clarke S (2001) Limited accumulation of damaged proteins in 1-isoaspartyl (D-aspartyl) O-methyltransferase-deficient mice. J. Biol. Chem. 276, 20695-20702.
41. Maehama T, Dixon JE (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 13375-13378.
42. McFadden PN, Clarke S (1987) Conversion of isoaspartyl peptides to normal peptides: implications for the cellular repair of damaged proteins. Proc. Natl Acad. Sci. USA 84, 2595-2599.
43. Miller SJ, Lou DY, Seldin DC, Lane WS, Neel BG (2002) Direct identification of PTEN phosphorylation sites. FEBS Lett. 528, 145-153.
44. Ozes ON, Akca H, Mayo LD, Gustin JA, Maehama T, Dixon JE, Donner DB (2001) A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc. Natl Acad. Sci. USA 98, 4640-4645.
45. Scheid MP, Woodgett JR (2003) Unravelling the activation mechanisms of protein kinase B/Akt. FEBS Lett. 546, 108-112.
46. Srivastava AK, Pandey SK (1998) Potential mechanism(s) involved in the regulation of glycogen synthesis by insulin. Mol. Cell Biochem. 182, 135-141.
47. Steinberg RA, Cauthron RD, Symcox MM, Shuntoh H (1993) Autoactivation of catalytic (C alpha) subunit of cyclic AMP-dependent protein kinase by phosphorylation of threonine 197. Mol. Cell Biol. 13, 2332-2341.
48. Stephens L, Anderson K, Stokoe D, Erdjument-Bromage H, Painter GF, Holmes AB, Gaffney PR, Reese CB, McCormick F, Tempst P, Coadwell J, Hawkins PT (1998) Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate- dependent activation of protein kinase B. Science 279, 710-714.
49. Torres J, Pulido R (2001) The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J. Biol. Chem. 276, 993-998.
50. Uhlmann EJ, Wong M, Baldwin RL, Bajenaru ML, Onda H, Kwiatkowski DJ, Yamada K, Gutmann DH (2002) Astrocyte-specific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann. Neurol. 52, 285-296.
51. Unger J, McNeill TH, Moxley RT, 3rd, White M, Moss A, Livingston JN (1989) Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31, 143-157.
52. Unger JW, Moss AM, Livingston JN (1991) Immunohistochemical localization of insulin receptors and phosphotyrosine in the brainstem of the adult rat. Neuroscience 42, 853-861.
53. Vazquez F, Grossman SR, Takahashi Y, Rokas MV, Nakamura N, Sellers WR (2001) Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J. Biol. Chem. 276, 48627-48630.
54. White MF (1998) The IRS-signaling system: a network of docking proteins that mediate insulin action. Mol. Cell. Biochem. 182, 3-11.
55. White MF, Shoelson SE, Keutmann H, Kahn CR (1988) A cascade of tyrosine autophosphorylation in the beta-subunit activates the phosphotransferase of the insulin receptor. J. Biol. Chem. 263, 2969-2980.
56. White MF, Takayama S, Kahn CR (1985) Differences in the sites of phosphorylation of the insulin receptor in vivo and in vitro. J. Biol. Chem. 260, 9470-9478.
57. White MF, Yenush L (1998) The IRS-signaling system: a network of docking proteins that mediate insulin and cytokine action. Curr. Top. Microbiol. Immunol. 228, 179-208.
58. Xu B, Bird VG, Miller WT (1995) Substrate specificities of the insulin and insulin-like growth factor 1 receptor tyrosine kinase catalytic domains. J. Biol. Chem. 270, 29825-29830.
59. Yamamoto A, Takagi H, Kitamura D, Tatsuoka H, Nakano H, Kawano H, Kuroyanagi H, Yahagi Y, Kobayashi S, Koizumi K, Sakai T, Saito K, Chiba T, Kawamura K, Suzuki K, Watanabe T, Mori H, Shirasawa T (1998) Deficiency in protein 1-isoaspartyl methyltransferase results in a fatal progressive epilepsy. J. Neurosci. 18, 2063-2074.
60. Ye P, Carson J, D'Ercole AJ (1995a) 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.
61. Ye P, Carson J, D'Ercole AJ (1995b) Insulin-like growth factor-I influences the initiation of myelination: studies of the anterior commissure of transgenic mice. Neurosci. Lett. 201, 235-238.