Specific roles of akt iso forms in apoptosis and axon growth regulation in neurons

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Diez, Hector ^a   Garrido, Juan Jose ^a,b   Wandosell, Francisco ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN AKT3; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN S6; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ISOENZYME; MTORC1 COMPLEX, HUMAN; PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; GROWTH REGULATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVE ELONGATION; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; CELL PROLIFERATION; CELL STRAIN HEK293; CELL SURVIVAL; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE FIBER; SIGNAL TRANSDUCTION;

APOPTOSIS; AXONS; CELL PROLIFERATION; CELL SURVIVAL; CEREBRAL CORTEX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HIPPOCAMPUS; HUMANS; ISOENZYMES; PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84859609280     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032715     Document Type: Article

References (96)

1. Pearce LR, Komander D, Alessi DR, (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11: 9-22.
2. Staal SP, (1987) Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma. Proc Natl Acad Sci U S A 84: 5034-5037.
3. Manning BD, Cantley LC, (2007) AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274.
4. Dummler B, Hemmings BA, (2007) Physiological roles of PKB/Akt isoforms in development and disease. Biochem Soc Trans 35: 231-235.
5. Yang ZZ, Tschopp O, Baudry A, Dummler B, Hynx D, et al. (2004) Physiological functions of protein kinase B/Akt. Biochem Soc Trans 32: 350-354.
6. Huang H, Tindall DJ, (2007) Dynamic FoxO transcription factors. J Cell Sci 120: 2479-2487.
7. Rayasam GV, Tulasi VK, Sodhi R, Davis JA, Ray A, (2009) Glycogen synthase kinase 3: more than a namesake. Br J Pharmacol 156: 885-898.
8. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC, (2002) Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 10: 151-162.
9. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, et al. (2007) PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25: 903-915.
10. Gonzalez E, McGraw TE, (2009) The Akt kinases: isoform specificity in metabolism and cancer. Cell Cycle 8: 2502-2508.
11. Yang ZZ, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, et al. (2003) Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem 278: 32124-32131.
12. Cho H, Thorvaldsen JL, Chu Q, Feng F, Birnbaum MJ, (2001) Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem 276: 38349-38352.
13. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, et al. (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292: 1728-1731.
14. Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, et al. (2003) Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 112: 197-208.
15. Easton RM, Cho H, Roovers K, Shineman DW, Mizrahi M, et al. (2005) Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol Cell Biol 25: 1869-1878.
16. Tschopp OYZ, Brodbeck D, Dummler BA, Hemmings-Mieszczak M, Watanabe T, et al. (2005) Essential role of protein kinase B gamma (PKB gamma/Akt3) in postnatal brain development but not in glucose homeostasis. Development 132: 2943-2954.
17. Crowder RJ, Freeman RS, (2000) Glycogen synthase kinase-3 beta activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J Biol Chem 275: 34266-34271.
18. Ohba N, Kiryu-Seo S, Maeda M, Muraoka M, Ishii M, et al. (2004) Transgenic mouse overexpressing the Akt reduced the volume of infarct area after middle cerebral artery occlusion. Neurosci Lett 359: 159-162.
19. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, et al. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661-665.
20. Cardona-Gomez GP, Mendez P, DonCarlos LL, Azcoitia I, Garcia-Segura LM, (2002) Interactions of estrogen and insulin-like growth factor-I in the brain: molecular mechanisms and functional implications. J Steroid Biochem Mol Biol 83: 211-217.
21. Mendez P, Wandosell F, Garcia-Segura LM, (2006) Cross-talk between estrogen receptors and insulin-like growth factor-I receptor in the brain: cellular and molecular mechanisms. Front Neuroendocrinol 27: 391-403.
22. 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.
23. Fishwick KJ, Li RA, Halley P, Deng P, Storey KG, (2010) Initiation of neuronal differentiation requires PI3-kinase/TOR signalling in the vertebrate neural tube. Dev Biol 338: 215-225.
24. Menager C, Arimura N, Fukata Y, Kaibuchi K, (2004) PIP3 is involved in neuronal polarization and axon formation. J Neurochem 89: 109-118.
25. Jiang H, Guo W, Liang X, Rao Y, (2005) Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120: 123-135.
26. Yoshimura T, Arimura N, Kawano Y, Kawabata S, Wang S, et al. (2006) Ras regulates neuronal polarity via the PI3-kinase/Akt/GSK-3beta/CRMP-2 pathway. Biochem Biophys Res Commun 340: 62-68.
27. Yan D, Guo L, Wang Y, (2006) Requirement of dendritic Akt degradation by the ubiquitin-proteasome system for neuronal polarity. J Cell Biol 174: 415-424.
28. Guo W, Jiang H, Gray V, Dedhar S, Rao Y, (2007) Role of the integrin-linked kinase (ILK) in determining neuronal polarity. Dev Biol 306: 457-468.
29. Warby SC, Doty CN, Graham RK, Shively J, Singaraja RR, et al. (2009) Phosphorylation of huntingtin reduces the accumulation of its nuclear fragments. Mol Cell Neurosci 40: 121-127.
30. Zala D, Colin E, Rangone H, Liot G, Humbert S, et al. (2008) Phosphorylation of mutant huntingtin at S421 restores anterograde and retrograde transport in neurons. Hum Mol Genet 17: 3837-3846.
31. Liao FF, Xu H, (2009) Insulin signaling in sporadic Alzheimer's disease. Sci Signal 2: pe36.
32. Chen HK, Fernandez-Funez P, Acevedo SF, Lam YC, Kaytor MD, et al. (2003) Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113: 457-468.
33. Emamian ES, Hall D, Birnbaum MJ, Karayiorgou M, Gogos JA, (2004) Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 36: 131-137.
34. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, et al. (2006) Pten regulates neuronal arborization and social interaction in mice. Neuron 50: 377-388.
35. Endersby R, Zhu X, Hay N, Ellison DW, Baker SJ, (2011) Nonredundant functions for Akt isoforms in astrocyte growth and gliomagenesis in an orthotopic transplantation model. Cancer Res 71: 4106-4116.
36. Foster KG, Fingar DC, (2010) Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J Biol Chem 285: 14071-14077.
37. Li YH, Werner H, Puschel AW, (2008) Rheb and mTOR regulate neuronal polarity through Rap1B. J Biol Chem 283: 33784-33792.
38. Morita T, Sobue K, (2009) Specification of neuronal polarity regulated by local translation of CRMP2 and Tau via the mTOR-p70S6K pathway. J Biol Chem 284: 27734-27745.
39. Park KK, Liu K, Hu Y, Smith PD, Wang C, et al. (2008) Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322: 963-966.
40. Han J, Wang B, Xiao Z, Gao Y, Zhao Y, et al. (2008) Mammalian target of rapamycin (mTOR) is involved in the neuronal differentiation of neural progenitors induced by insulin. Mol Cell Neurosci 39: 118-124.
41. Ruvinsky I, Meyuhas O, (2006) Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem Sci 31: 342-348.
42. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, et al. (1999) Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13: 1422-1437.
43. Kaech S, Banker G, (2006) Culturing hippocampal neurons. Nat Protoc 1: 2406-2415.
44. Barnes AP, Polleux F, (2009) Establishment of Axon-Dendrite Polarity in Developing Neurons. Annu Rev Neurosci.
45. Frias MA, Thoreen CC, Jaffe JD, Schroder W, Sculley T, et al. (2006) mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s. Curr Biol 16: 1865-1870.
46. Sandsmark DK, Pelletier C, Weber JD, Gutmann DH, (2007) Mammalian target of rapamycin: master regulator of cell growth in the nervous system. Histol Histopathol 22: 895-903.
47. Priya S, Sudhakaran PR, (2008) Cell survival, activation and apoptosis of hepatic stellate cells: modulation by extracellular matrix proteins. Hepatol Res 38: 1221-1232.
48. Calleja V, Laguerre M, Parker PJ, Larijani B, (2009) Role of a novel PH-kinase domain interface in PKB/Akt regulation: structural mechanism for allosteric inhibition. PLoS Biol 7: e17.
49. Dotti CG, Sullivan CA, Banker GA, (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468.
50. Mandell JW, Banker GA, (1996) A spatial gradient of tau protein phosphorylation in nascent axons. J Neurosci 16: 5727-5740.
51. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22: 153-183.
52. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, et al. (2005) Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 19: 2199-2211.
53. Pullen N, Thomas G, (1997) The modular phosphorylation and activation of p70s6k. FEBS Lett 410: 78-82.
54. Heron-Milhavet L, Khouya N, Fernandez A, Lamb NJ, (2011) Akt1 and Akt2: differentiating the aktion. Histol Histopathol 26: 651-662.
55. Fayard E, Xue G, Parcellier A, Bozulic L, Hemmings BA, (2010) Protein kinase B (PKB/Akt), a key mediator of the PI3K signaling pathway. Curr Top Microbiol Immunol 346: 31-56.
56. Schultze SM, Jensen J, Hemmings BA, Tschopp O, Niessen M, (2011) Promiscuous affairs of PKB/AKT isoforms in metabolism. Arch Physiol Biochem 117: 70-77.
57. Pap M, Cooper GM, (1998) Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J Biol Chem 273: 19929-19932.
58. Slee EA, Adrain C, Martin SJ, (1999) Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 6: 1067-1074.
59. Parcellier A, Tintignac LA, Zhuravleva E, Hemmings BA, (2008) PKB and the mitochondria: AKTing on apoptosis. Cell Signal 20: 21-30.
60. Santi SA, Lee H, The Akt isoforms are present at distinct subcellular locations. Am J Physiol Cell Physiol 298: C580-591.
61. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, et al. (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16: 819-830.
62. Datta SR, Dudek H, Tao X, Masters S, Fu H, et al. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241.
63. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G, (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278: 687-689.
64. Yamaguchi H, Wang HG, (2001) The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 20: 7779-7786.
65. Kops GJ, de Ruiter ND, De Vries-Smits AM, Powell DR, Bos JL, et al. (1999) Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398: 630-634.
66. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868.
67. Du K, Montminy M, (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273: 32377-32379.
68. Gottlieb TM, Leal JF, Seger R, Taya Y, Oren M, (2002) Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene 21: 1299-1303.
69. Shi SH, Jan LY, Jan YN, (2003) Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112: 63-75.
70. Sosa L, Dupraz S, Laurino L, Bollati F, Bisbal M, et al. (2006) IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity. Nat Neurosci 9: 993-995.
71. Garrido JJ, Simon D, Varea O, Wandosell F, (2007) GSK3 alpha and GSK3 beta are necessary for axon formation. FEBS Lett 581: 1579-1586.
72. Arimura N, Kaibuchi K, (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8: 194-205.
73. Shi SH, Cheng T, Jan LY, Jan YN, (2004) APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr Biol 14: 2025-2032.
74. Choi YJ, Di Nardo A, Kramvis I, Meikle L, Kwiatkowski DJ, et al. (2008) Tuberous sclerosis complex proteins control axon formation. Genes Dev 22: 2485-2495.
75. Wildonger J, Jan LY, Jan YN, (2008) The Tsc1-Tsc2 complex influences neuronal polarity by modulating TORC1 activity and SAD levels. Genes Dev 22: 2447-2453.
76. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, et al. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371: 762-767.
77. Pullen N, Dennis PB, Andjelkovic M, Dufner A, Kozma SC, et al. (1998) Phosphorylation and activation of p70s6k by PDK1. Science 279: 707-710.
78. Papst PJ, Sugiyama H, Nagasawa M, Lucas JJ, Maller JL, et al. (1998) Cdc2-cyclin B phosphorylates p70 S6 kinase on Ser411 at mitosis. J Biol Chem 273: 15077-15084.
79. Hou Z, He L, Qi RZ, (2007) Regulation of s6 kinase 1 activation by phosphorylation at ser-411. J Biol Chem 282: 6922-6928.
80. Fenton TR, (2010) Gout IT Functions and regulation of the 70 kDa ribosomal S6 kinases. Int J Biochem Cell Biol 43: 47-59.
81. Pende M, Um SH, Mieulet V, Sticker M, Goss VL, et al. (2004) S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 24: 3112-3124.
82. Meyuhas O, (2008) Physiological roles of ribosomal protein S6: one of its kind. Int Rev Cell Mol Biol 268: 1-37.
83. Lee-Fruman KK, Kuo CJ, Lippincott J, Terada N, Blenis J, (1999) Characterization of S6K2, a novel kinase homologous to S6K1. Oncogene 18: 5108-5114.
84. Poot M, Kroes HY, Hochstenbach R, (2008) AKT3 as a candidate gene for corpus callosum anomalies in patients with 1q44 deletions. Eur J Med Genet 51: 689-690.
85. Boland E, Clayton-Smith J, Woo VG, McKee S, Manson FD, et al. (2007) Mapping of deletion and translocation breakpoints in 1q44 implicates the serine/threonine kinase AKT3 in postnatal microcephaly and agenesis of the corpus callosum. Am J Hum Genet 81: 292-303.
86. Andrieux J, Cuvellier JC, Duban-Bedu B, Joriot-Chekaf S, Dieux-Coeslier A, et al. (2008) A 6.9 Mb 1qter deletion/4.4 Mb 18pter duplication in a boy with extreme microcephaly with simplified gyral pattern, vermis hypoplasia and corpus callosum agenesis. Eur J Med Genet 51: 87-91.
87. Gericke A, Munson M, Ross AH, (2006) Regulation of the PTEN phosphatase. Gene 374: 1-9.
88. Chalhoub N, Zhu G, Zhu X, Baker SJ, (2009) Cell type specificity of PI3K signaling in Pdk1- and Pten-deficient brains. Genes Dev 23: 1619-1624.
89. Chalhoub N, Kozma SC, Baker SJ, (2006) S6k1 is not required for Pten-deficient neuronal hypertrophy. Brain Res 1100: 32-41.
90. Lintas C, Persico AM, (2009) Autistic phenotypes and genetic testing: state-of-the-art for the clinical geneticist. J Med Genet 46: 1-8.
91. Robinson S, Cohen AR, (2006) Cowden disease and Lhermitte-Duclos disease: an update. Case report and review of the literature. Neurosurg Focus 20: E6.
92. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM, (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101.
93. Naldini L, Blomer U, Gage FH, Trono D, Verma IM, (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A 93: 11382-11388.
94. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
95. Garcia-Martinez JM, Alessi DR, (2008) mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem J 416: 375-385.
96. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, et al. (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58: 167-176.