Home LiteratureArticle Details
PMID: 15713641 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Role for Akt3/protein kinase Bgamma in attainment of normal brain size.

Molecular and cellular biology ·Vol. 25 ·No. 5 ·2005-03-00 ·Pages 1869-78

Easton RM, Cho H, Roovers K, Shineman DW, Mizrahi M, Forman MS, Lee VM, Szabolcs M, de Jong R, Oltersdorf T, Ludwig T, Efstratiadis A, Birnbaum MJ

Abstract

Studies of Drosophila and mammals have revealed the importance of insulin signaling through phosphatidylinositol 3-kinase and the serine/threonine kinase Akt/protein kinase B for the regulation of cell, organ, and organismal growth. In mammals, three highly conserved proteins, Akt1, Akt2, and Akt3, comprise the Akt family, of which the first two are required for normal growth and metabolism, respectively. Here we address the function of Akt3. Like Akt1, Akt3 is not required for the maintenance of normal carbohydrate metabolism but is essential for the attainment of normal organ size. However, in contrast to Akt1-/- mice, which display a proportional decrease in the sizes of all organs, Akt3-/- mice present a selective 20% decrease in brain size. Moreover, although Akt1- and Akt3-deficient brains are reduced in size to approximately the same degree, the absence of Akt1 leads to a reduction in cell number, whereas the lack of Akt3 results in smaller and fewer cells. Finally, mammalian target of rapamycin signaling is attenuated in the brains of Akt3-/- but not Akt1-/- mice, suggesting that differential regulation of this pathway contributes to an isoform-specific regulation of cell growth.

MeSH Terms
Animals Blood Glucose/analysis Body Weight/genetics,physiology Brain/cytology,enzymology,growth & development Female Glucose/metabolism Glucose Tolerance Test Insulin/blood,metabolism Male Mice Mice, Knockout Myocardium/cytology Oncogene Proteins/genetics,physiology Organ Size/genetics,physiology Phosphorylation Protein Serine-Threonine Kinases/genetics,physiology Proto-Oncogene Proteins/genetics,physiology Proto-Oncogene Proteins c-akt Ribosomal Protein S6 Kinases/metabolism
Chemicals
Blood Glucose Insulin Oncogene Proteins Proto-Oncogene Proteins Akt2 protein, mouse Akt3 protein, mouse Protein Serine-Threonine Kinases Proto-Oncogene Proteins c-akt Ribosomal Protein S6 Kinases Glucose
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Easton Rachael M
Department of Medicine, University of Pennsylvania School of Medicine, Clinical Research Building 322, 415 Curie Blvd., Philadelphia, PA 19104, USA.
Cho Han
Roovers Kristin
Shineman Diana W
Mizrahi Moshe
Forman Mark S
Lee Virginia M-Y
Szabolcs Matthias
de Jong Ron
Oltersdorf Tilman
Ludwig Thomas
Efstratiadis Argiris
Birnbaum Morris J
References (73)
73 references, click to expand
  1. Role of insulin-like growth factors in embryonic and postnatal growth.
    Cell. 1993 Oct 8;75(1):73-82 PMID: 8402902
  2. IGF-I is required for normal embryonic growth in mice.
    Genes Dev. 1993 Dec;7(12B):2609-17 PMID: 8276243
  3. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene.
    Nature. 1994 Nov 10;372(6502):186-90 PMID: 7526222
  4. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons.
    Neuron. 1995 Apr;14(4):717-30 PMID: 7718235
  5. The Drosophila insulin receptor is required for normal growth.
    Endocrinology. 1996 Mar;137(3):846-56 PMID: 8603594
  6. Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1 and identification of insulin receptor substrate-2.
    Diabet Med. 1996 Sep;13(9 Suppl 6):S103-8 PMID: 8894493
  7. Regulation of neuronal survival by the serine-threonine protein kinase Akt.
    Science. 1997 Jan 31;275(5300):661-5 PMID: 9005851
  8. Insulin-like growth factor I gene deletion causing intrauterine growth retardation and severe short stature.
    Acta Paediatr Suppl. 1997 Nov;423:39-45 PMID: 9401537
  9. Protein kinase C modulates the insulin-stimulated increase in Akt1 and Akt3 activity in 3T3-L1 adipocytes.
    Biochem Biophys Res Commun. 1998 Feb 13;243(2):509-13 PMID: 9480839
  10. Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation.
    J Neurosci. 2003 Aug 6;23(18):7084-92 PMID: 12904469
  11. Protein kinase B alpha/Akt1 regulates placental development and fetal growth.
    J Biol Chem. 2003 Aug 22;278(34):32124-31 PMID: 12783884
  12. Deficiency of PDK1 in cardiac muscle results in heart failure and increased sensitivity to hypoxia.
    EMBO J. 2003 Sep 15;22(18):4666-76 PMID: 12970179
  13. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer.
    Cancer Cell. 2003 Sep;4(3):209-21 PMID: 14522255
  14. mTor is required for hypertrophy of Pten-deficient neuronal soma in vivo.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12923-8 PMID: 14534328
  15. Schizophrenia.
    N Engl J Med. 2003 Oct 30;349(18):1738-49 PMID: 14585943
  16. Body building: regulation of shape and size by PI3K/TOR signaling during development.
    Mech Dev. 2003 Nov;120(11):1283-96 PMID: 14623438
  17. Isoform-specific regulation of insulin-dependent glucose uptake by Akt/protein kinase B.
    J Biol Chem. 2003 Dec 5;278(49):49530-6 PMID: 14522993
  18. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB.
    Nat Cell Biol. 1999 Dec;1(8):500-6 PMID: 10587646
  19. Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration.
    J Neurosci. 2000 Apr 15;20(8):2875-86 PMID: 10751440
  20. The conserved phosphoinositide 3-kinase pathway determines heart size in mice.
    EMBO J. 2000 Jun 1;19(11):2537-48 PMID: 10835352
  21. The conserved PI3'K/PTEN/Akt signaling pathway regulates both cell size and survival in Drosophila.
    Oncogene. 2000 Aug 17;19(35):3971-7 PMID: 10962553
  22. Genetic control of cell size.
    Curr Opin Genet Dev. 2000 Oct;10(5):529-35 PMID: 10980431
  23. Increased number of cardiomyocytes in cross-sections from tachycardia-induced cardiomyopathic hearts.
    Int J Mol Med. 1999 Feb;3(2):153-5 PMID: 9917522
  24. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth.
    Dev Biol. 2001 Jan 1;229(1):141-62 PMID: 11133160
  25. Hypoinsulinaemia, glucose intolerance and diminished beta-cell size in S6K1-deficient mice.
    Nature. 2000 Dec 21-28;408(6815):994-7 PMID: 11140689
  26. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta).
    Science. 2001 Jun 1;292(5522):1728-31 PMID: 11387480
  27. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene.
    Genes Dev. 2001 Sep 1;15(17):2203-8 PMID: 11544177
  28. The tumor suppressor gene PTEN can regulate cardiac hypertrophy and survival.
    J Biol Chem. 2001 Sep 21;276(38):35786-93 PMID: 11448956
  29. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala.
    Neuron. 2001 Sep 13;31(5):841-51 PMID: 11567621
  30. PKB/AKT: functional insights from genetic models.
    Nat Rev Mol Cell Biol. 2001 Oct;2(10):760-8 PMID: 11584303
  31. Regulation of pancreatic beta-cell growth and survival by the serine/threonine protein kinase Akt1/PKBalpha.
    Nat Med. 2001 Oct;7(10):1133-7 PMID: 11590437
  32. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice.
    J Biol Chem. 2001 Oct 19;276(42):38349-52 PMID: 11533044
  33. Disruption of IRS-2 causes type 2 diabetes in mice.
    Nature. 1998 Feb 26;391(6670):900-4 PMID: 9495343
  34. Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons.
    J Neurosci. 1998 Apr 15;18(8):2933-43 PMID: 9526010
  35. Polyoma middle T antigen activates the Ser/Thr kinase Akt in a PI3-kinase-dependent manner.
    Biochem Biophys Res Commun. 1998 May 8;246(1):76-81 PMID: 9600071
  36. Biochemical and morphometric analyses show that myelination in the insulin-like growth factor 1 null brain is proportionate to its neuronal composition.
    J Neurosci. 1998 Aug 1;18(15):5673-81 PMID: 9671658
  37. Genetics of mouse growth.
    Int J Dev Biol. 1998;42(7):955-76 PMID: 9853827
  38. Size control in animal development.
    Cell. 1999 Jan 22;96(2):235-44 PMID: 9988218
  39. A human protein kinase Bgamma with regulatory phosphorylation sites in the activation loop and in the C-terminal hydrophobic domain.
    J Biol Chem. 1999 Apr 2;274(14):9133-6 PMID: 10092583
  40. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4.
    Cell. 1999 Jun 25;97(7):865-75 PMID: 10399915
  41. Drosophila S6 kinase: a regulator of cell size.
    Science. 1999 Sep 24;285(5436):2126-9 PMID: 10497130
  42. Raf and akt mediate distinct aspects of sensory axon growth.
    Neuron. 2002 Jul 3;35(1):65-76 PMID: 12123609
  43. The Drosophila insulin/IGF receptor controls growth and size by modulating PtdInsP(3) levels.
    Development. 2002 Sep;129(17):4103-9 PMID: 12163412
  44. Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland.
    Development. 2002 Sep;129(17):4159-70 PMID: 12163417
  45. PTEN overexpression suppresses proliferation and differentiation and enhances apoptosis of the mouse mammary epithelium.
    J Clin Invest. 2002 Sep;110(6):815-25 PMID: 12235113
  46. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways.
    Cell. 2002 Sep 20;110(6):737-49 PMID: 12297047
  47. PTEN regulation of neural development and CNS stem cells.
    J Cell Biochem. 2003 Jan 1;88(1):24-8 PMID: 12461771
  48. Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation.
    Mol Psychiatry. 2003 Feb;8(2):217-24 PMID: 12610654
  49. The insulin-like growth factor system and cancer.
    Cancer Lett. 2003 Jun 10;195(2):127-37 PMID: 12767520
  50. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2.
    Genes Dev. 2003 Jun 1;17(11):1352-65 PMID: 12782654
  51. Insulin-like growth factor 1 is essential for normal dendritic growth.
    J Neurosci Res. 2003 Jul 1;73(1):1-9 PMID: 12815703
  52. Control of synaptic strength, a novel function of Akt.
    Neuron. 2003 Jun 19;38(6):915-28 PMID: 12818177
  53. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7841-6 PMID: 12799464
  54. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression.
    Cell Cycle. 2003 Jul-Aug;2(4):339-45 PMID: 12851486
  55. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta.
    J Clin Invest. 2003 Jul;112(2):197-208 PMID: 12843127
  56. In vivo ethanol decreases phosphorylated MAPK and p70S6 kinase in the developing rat brain.
    Neuroreport. 2003 Jul 18;14(10):1395-9 PMID: 12876481
  57. Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease.
    Nat Genet. 2001 Dec;29(4):396-403 PMID: 11726926
  58. Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease.
    Nat Genet. 2001 Dec;29(4):404-11 PMID: 11726927
  59. Distinct and overlapping functions of insulin and IGF-I receptors.
    Endocr Rev. 2001 Dec;22(6):818-35 PMID: 11739335
  60. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo.
    Science. 2001 Dec 7;294(5549):2186-9 PMID: 11691952
  61. Akt/protein kinase B promotes organ growth in transgenic mice.
    Mol Cell Biol. 2002 Apr;22(8):2799-809 PMID: 11909972
  62. Genetic analysis of insulin signaling in Drosophila.
    Trends Endocrinol Metab. 2002 May-Jun;13(4):156-62 PMID: 11943559
  63. The phosphoinositide 3-kinase pathway.
    Science. 2002 May 31;296(5573):1655-7 PMID: 12040186
  64. The IGF-1/Akt pathway is neuroprotective in Huntington's disease and involves Huntingtin phosphorylation by Akt.
    Dev Cell. 2002 Jun;2(6):831-7 PMID: 12062094
  65. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart.
    J Biol Chem. 2002 Jun 21;277(25):22896-901 PMID: 11943770
  66. Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia.
    Nat Genet. 2004 Feb;36(2):131-7 PMID: 14745448
  67. How are the sizes of cells, organs, and bodies controlled?
    PLoS Biol. 2003 Dec;1(3):E86 PMID: 14691557
  68. Advances in protein kinase B signalling: AKTion on multiple fronts.
    Trends Biochem Sci. 2004 May;29(5):233-42 PMID: 15130559
  69. Phosphoinositide 3-kinase and its targets in B-cell and T-cell signaling.
    Curr Opin Immunol. 2004 Jun;16(3):314-20 PMID: 15134780
  70. Comparative aspects of the brain growth spurt.
    Early Hum Dev. 1979 Mar;3(1):79-83 PMID: 118862
  71. Relative brain size and basal metabolic rate in terrestrial vertebrates.
    Nature. 1981 Sep 3;293(5827):57-60 PMID: 7266659
  72. Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice.
    Neuron. 1993 Apr;10(4):729-40 PMID: 8386530
  73. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r).
    Cell. 1993 Oct 8;75(1):59-72 PMID: 8402901
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-03-00
Pages
1869-78
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC549378
Subset
IM
Grants
NCI NIH HHS · P01 CA097403 · United States
NIDDK NIH HHS · DK50306 · United States
NIDDK NIH HHS · P30 DK050306 · United States
NIDDK NIH HHS · R01 DK056886 · United States
NIDDK NIH HHS · T32 DK7314 · United States
NIDDK NIH HHS · R01 DK56886 · United States
NIDDK NIH HHS · DK19525 · United States
NIDDK NIH HHS · T32 DK007314 · United States
NIDDK NIH HHS · P30 DK019525 · United States
NCI NIH HHS · P01 CA97403 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com