Subcellular Localization of IRS-1 in Cell Proliferation and Differentiation

X. Tu; A. Wu; A. Maiorana; R. Baserga

doi:10.1055/s-2004-814155

Hormone and Metabolic Research, Table of Contents

Horm Metab Res 2003; 35(11/12): 734-739
DOI: 10.1055/s-2004-814155

Original

Subcellular Localization of IRS-1 in Cell Proliferation and Differentiation

X. Tu¹ , A. Wu¹ , A. Maiorana¹ , R. Baserga¹

¹ Kimmel Cancer Center, Thomas Jefferson University, Philadelphia

Abstract

The type 1 insulin-like growth factor receptor (IGF-IR) and its docking protein, insulin receptor substrate-1 (IRS-1), play important roles in cell transformation, cell differentiation and aging. IRS-1 and other IRS proteins can, under certain conditions, localize to the nuclei of cells, where they undergo interactions with nuclear and nucleolar proteins. In this study, we confirm and extend these observations, demonstrating that IRS-1 is preferentially nuclear in growing cells. Differentiation and inhibition of ribosomal RNA synthesis cause subcellular redistribution of IRS-1 and other nuclear proteins to the cytoplasm.

Key words

IGF-I receptor - Nuclear IRS-1 - Differentiation

Full Text

References

1 Blakesley V A, Butler A A, Koval A P, Okubo Y, LeRoith D. IGF-I receptor function: transducing the IGF-I signal into intracellular events. In: Rosenfeld RG, Roberts CT Jr (eds) The IGF System. Totowa, NJ; Humana Press 1999: 143-163
2 Rosenfeld R G, Roberts C T Jr (eds). The IGF System. Totowa, NJ; Humana Press 1999: 787
3 Baserga R. The contradictions of the insulin-like growth factor 1 receptor. Oncogene. 2000; 19 5574-5581
4 LeRoith D, Zumkeller W, Baxter R (ed). Insulin-like Growth Factors. Georgetown, TX; Landes Bioscience, EUREKA.com 2003
5 White M F. The IRS-signalling system: a network of docking proteins that mediate insulin action. Mol Cell Bioch. 1998; 182 3-11
6 Zhou-Li F, Xu S-Q, Dews M, Baserga R. Co-operation of simian virus 40 T antigen and insulin receptor substrate-1 in protection from apoptosis induced by interleukin-3 withdrawal. Oncogene. 1997; 15 961-970
7 Wang L M, Myers M G Jr, Sun X J, Aaronson S A, White M, Pierce J H. IRS-1: essential for insulin- and IL-4-stimulated mitogenesis in hemopoietic cells. Science. 1993; 261 1591-1594
8 Valentinis B, Romano G, Peruzzi F, Morrione A, Prisco M, Soddu S, Cristofanelli B, Sacchi A, Baserga R. Growth and differentiation signals by the insulin-like growth factor 1 receptor in hemopoietic cells are mediated through different pathways. J Biol Chem. 1999; 274 12 423-12 430
9 Valentinis B, Navarro M, Zanocco-Marani T, Edmonds P, McCormick J, Morrione A, Sacchi A, Romano G, Reiss K, Baserga R. Insulin receptor substrate-1, p70S6K and cell size in transformation and differentiation of hemopoietic cells. J Biol Chem. 2000; 275 25 451-25 459
10 Zamorano J, Wang H Y, Wang L-M, Pierce J H, Keegan A D. IL-4 protects cells from apoptosis via the insulin receptor substrate pathway and a second independent signaling pathway. J Immunol. 1996; 157 4926-4934
11 Sun X J, Pons S, Wang L M, Zhang Y, Yenush L, Burks D, Myers M G Jr, Glasheen E, Jenkins N A, White M F. The IRS-2 gene on murine chromosome 8 encodes a unique signaling adapter for insulin and cytokine action. Mol Endocr. 1997; 11 251-262
12 Kim B, Cheng H-L, Margolis B, Feldman E L. Insulin receptor substrate 2 and Shc play different roles in insulin-like growth factor I signaling. J Biol Chem. 1998; 273 34 543-34 550
13 Sadowski C L, Choi T S, Le M, Wheeler T T, Wang L H, Sadowski H B. Insulin induction of SOCS-2 and SOCS-3 mRNA expression in C2C12 skeletal muscle cells is mediated by Stat5. J Biol Chem. 2001; 276 20 703-20 710
14 Chang Q, Li Y, White M F, Fletcher J A, Xiao S. Constitutive activation of insulin receptor substrate-1 is a frequent event in human tumors: therapeutic implications. Cancer Res. 2002; 62 6035-6038
15 Bohni R, Riesco-Escovar J, Oldham S, Brogiolo W, Stocker H, Andruss B F, Beckingham K, Hafen E. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS-1. Cell. 1999; 97 865-875
16 Montagne J, Stewart M J, Stocker H, Hafen E, Kozma S C, Thomas G. Drosophila 6 kinase: a regulator of cell size. Science. 1999; 285 2126-2129
17 Verdu J, Buratovich M A, Wilder E L, Birnbaum M J. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nature Cell Biol. 1999; 1 500-506
18 Pete G, Fuller G R, Oldham J M, Smith D R, D’Ercole A J, Kahn C R, Lund P K. Postnatal growth responses to insulin-like growth factor 1 in insulin receptor substrate-1 mice. Endocrinology. 1999; 140 5478-5487
19 Shima H, Pende M, Chen Y, Fumagalli S, Thomas G, Kozma S C. Disruption of the p70S6K/p85S6K gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J. 1998; 17 6649-6659
20 Ludwig T, Eggenschwiler J, Fisher P, D'Ercole J P, Davenport M L, Efstratiadis A. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Develop Biol. 1996; 177 517-535
21 Baserga R. Growth in size and cell DNA replication. Exp Cell Res. 1984; 151 -5
22 Jorgensen P, Nishikawa J L, Breitkreutz B J, Tyers M. Systematic identification of pathways that couple cell growth and division in yeast. Science. 2002; 297 395-400
23 Moss T, Stefanovsky V Y. Promotion and regulation of ribosomal transcription in eukaryotes by RNA polymerase I. Progr Nucleic Acid Res Mol Biol. 1995; 50 25-66
24 Grummt I. Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Progr Nucl Acid Res Mol Biol. 1999; 62 109-153
25 Larson D E, Xie W Q, Glibetic M, O’Mahony D, Sells B H, Rothblum L I. Coordinated decrease in rRNA gene transcription factors and rRNA synthesis during muscle differentiation. Proc Natl Acad Sci. 1993; 90 7933-7936
26 Comai L, Song Y, Tan C, Bui T. Inhibition of RNA polymerase I transcription in differentiated myeloid leukemia cells by inactivation of Selectivity Factor^-1. Cell Growth & Diff. 2000; 11 63-70
27 Reeder R H. Regulation of RNA polymerase transcription in yeast and vertebrates. Progr. Nucl Acid Res Mol Biol. 1999; 62 293-327
28 Tu X, Batta P, Innocent N, Prisco M, Casaburi , I , Belletti B, Baserga R. Nuclear translocation of insulin receptor substrate-1 by oncogenes and IGF-I: effect on ribosomal RNA synthesis. J Biol Chem. 2002; 277 44 357-44 365
29 Sun H Z, Tu X, Prisco M, Wu A, Casiburi I, Baserga R. IGF-I receptor signaling and nuclear translocation of insulin receptor substrates-1 and -2. Mol Endocrinol. 2003; 17 472-486
30 Liu J-P, Baker J, Perkins A S, Robertson E J, Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 1993; 75 59-72
31 Sell C, Rubini M, Rubin R, Liu J-P, Efstratiadis A, Baserga R. Simian virus 40 large tumor antigen is unable to transform mouse embryonic fibroblasts lacking type-1 IGF receptor. Proc Natl Acad Sci USA. 1993; 90 11 217-11 221
32 Radna R L, Caton Y, Jha K K, Kaplan P, Li G, Traganos , Ozer H L. Growth of immortal simian virus 40 tsA-transformed human fibroblasts is temperature-dependent. Mol Cell Biol. 1989; 9 3093-309 632
33 Wu A, Sciacca L, Baserga R. Nuclear translocation of insulin receptor substrate-1 by the insulin receptor in mouse embryo fibroblasts. J Cell Physiol. 2003; 195 453-460
34 Prisco M, Santini F, Baffa R, Liu M, Drakas R, Wu A, Baserga R. Nuclear translocation of IRS-1 by the SV40 T antigen and the activated IGF-I receptor. J Biol Chem. 2002; 277 32 078-32 085
35 Lassak A, DelValle L, Peruzzi F, Wang J Y, Enam S, Croul S, Khalili K, Reiss K. Insulin receptor substrate-1 translocation to the nucleus by the human JC virus T antigen. J Biol Chem. 2002; 277 17 231-17 238
36 Sciacca L, Prisco M, Wu A, Belfiore A, Vigneri R, Baserga R. Signaling differences from the A and B isoforms of the insulin receptor (IR) in 32D cells in the preence or absence of IR substrate-1. Endocrinology. 2003; 144 2550-2658
37 Politz J C, Lewandowski L B, Pederson T. Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis. J Cell Biol. 2002; 159 411-418
38 Ringertz N R, Savage R E. Cell Hybrids. New York; Academic Press 1976
39 Hannan K M, Kennedy B K, Cavanaugh A H, Hannan R D, Hirschler-Laszkiewicz I, Jefferson L S, Rothblum L I. RNA polymerase I transcription in confluent cells: Rb down regulates rDNA transcription during confluence-induced cell cycle arrest. Oncogene. 2000; 19 3487-3497
40 Tu X, Baffa R, Luke S, Prisco M, Baserga R. Intracellular redistribution of nuclear and nucleolar proteins during differentiation of 32D murine hemopoietic cells. Exp Cell Res. 2003; 288 119-130
41 Lieberman I, Abrams R, Ove P. Changes in the metabolism of ribonucleic acid preceding the synthesis of deoxyribonucleic acid in mammalian cells cultured from the animal. J Biol Chem. 1963; 238 2141-2149
42 Jacobs A R, LeRoith D, Taylor S I. Insulin receptor substrate-1 pleckstrin homology and phosphotyrosine-binding domains are both involved in plasma membrane targeting. J Biol Chem. 2001; 276 40 795-40 802
43 Kreider B L, Benezra R, Rovera G, Kadesch T. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science. 1992; 255 1700-1702

R. Baserga

Kimmel Cancer Center, Thomas Jefferson University

233 S. 10th Street · 624 BLSB · Philadelphia, PA 19107

Phone: +1(215)5034507

Fax: +1(215)9230249

Email: R_baserga@lac.tju.edu