Regulation of Id Gene Expression by Type I Insulin-Like Growth Factor: Roles of STAT3 and the Tyrosine 950 Residue of the Receptor

REFERENCES

• Alani, R. M., J. Hasskari, M. Grace, M. C. Hernandez, M. A. Israel, and K. Munger. 1999. Immortalization of primary human keratinocytes by the helix-loop-helix protein. Id1. Proc. Natl. Acad. Sci. USA 96:9637–9641.
   PubMedGoogle Scholar
• Barone, M. V., R. Pepperkok, F. A. Peverali, and L. Philipson. 1994. Id proteins control growth induction in mammalian cells. Proc. Natl. Acad. Sci. USA 91:4985–4988.
   PubMed Web of Science ®Google Scholar
• Baserga, R., and A. Morrione. 1999. Differentiation and malignant transformation: two roads diverged in a wood. J. Cell. Biochem. 32/33:68–75.
   Google Scholar
• Baserga, R., M. Prisco, and A. Hongo. 1999. IGFs and cell growth. The IGF system. R. G. Rosenfeld, and C. T. Roberts Jr.. 329–353. Humana Press, Totowa. N.J
   Google Scholar
• Basu, T., P. H. Warne, and J. Downward. 1994. Role of Shc in the activation of Ras in response to epidermal growth factor and nerve growth factor. Oncogene 9:3483–3491.
   PubMedGoogle Scholar
• Benezra, R., R. L. Davis, D. Lockshon, D. L. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61:49–59.
   PubMed Web of Science ®Google Scholar
• Blakesley, V. A., A. A. Butler, A. P. Koval, Y. Okubo, and D. LeRoith. 1999. IGF-I receptor function: transducing the IGF-I signal into intracellular events. The IGF system.. R. G. Rosenfeld, and C. T. Roberts Jr.. 143–163. Humana Press, Totowa, N.J
   Google Scholar
• Brown, G., M. A. Choudhry, J. Durham, M. T. Drayson, and R. H. Michell. 1999. Monocytically differentiating HL60 cells proliferate rapidly before they mature. Exp. Cell Res. 253:511–518.
   PubMedGoogle Scholar
• Chaturvedi, P., S. Sharma, and P. Reddy. 1997. Abrogation of interleukin-3 dependence of myeloid cells by the v-src oncogene requires SH2 and SH3 domains which specify activation of STATs. Mol. Cell. Biol. 17:3295–3304.
   PubMed Web of Science ®Google Scholar
• Christy, B. A., L. K. Saunders, L. F. Lau, N. G. Copeland, N. A. Jenkins, and D. Mathans. 1991. An Id-related helix-loop-helix protein encoded by a growth factor inducible gene. Proc. Natl. Acad. Sci. USA 88:1815–1819.
   PubMed Web of Science ®Google Scholar
• Cooper, C. L., and P. E. Newburger. 1998. Differential expression of Id genes in multipotent myeloid progenitor cells: Id1 is induced by early- and late-acting cytokines while Id2 is selectively induced by cytokines that drive terminal granulocytic differentiation. J. Cell. Biochem. 71:277–285.
   PubMedGoogle Scholar
• Cooper, C. L., G. Brady, F. Bilia, N. N. Iscove, and P. J. Quesenberry. 1997. Expression of the Id family helix-loop-helix regulators during growth and development in the hematopoietic system. Blood 89:3155–3165.
   PubMedGoogle Scholar
• Craparo, A., T. J. O'Neill, and T. A. Gustafson. 1995. Non-SH2 domains within insulin receptor substrate-1 and SHC mediate their phosphotyrosine-dependent interaction with the NPEY motif of the insulin-like growth factor-I receptor. J. Biol. Chem. 270:15639–15643.
   PubMedGoogle Scholar
• Cristofanelli, B., B. Valentinis, S. Soddu, M. G. Rizzo, A. Marchetti, G. Bossi, A. R. Morena, M. Dews, R. Baserga, and A. Sacchi. 2000. Co-operative transformation of 32D cells by the combined expression of IRS-1 and v-Ha-Ras. Oncogene 19:3245–3255.
   PubMedGoogle Scholar
• De Koning, J. P., A. A. Soede-Bobok, A. C. Ward, A. M. Schelen, C. Antonissen, D. van Leeuwen, B. Lowenberg, and I. P. Touw. 2000. Stat-3-mediated differentiation and survival of myeloid cells in response to granulocyte colony-stimulating factor: role for the cyclin-dependent kinase inhibitor p27Kip1. Oncogene 19:3290–3298.
   PubMed Web of Science ®Google Scholar
• Desprez, P. Y., E. Hara, M. J. Bissell, and J. Campisi. 1995. Suppression of mammary epithelial cell differentiation by the helix-loop-helix protein Id-1. Mol. Cell. Biol. 15:3398–3404.
   PubMedGoogle Scholar
• Desprez, P. Y., C. Q Lin, N. Thomasset, C. J. Simpson, M. J. Bissell, and J. Campisi. 1998. A novel pathway for mammary epithelial cell invasion by the helix-loop-helix protein Id-1. Mol. Cell. Biol. 18:4577–4588.
   PubMedGoogle Scholar
• Dews, M., M. Prisco, F. Peruzzi, G. Romano, A. Morrione, and R. Baserga. 2000. Domains of the IGF-I receptor required for the activation of extracellular signal-regulated kinases. Endocrinology 141:1289–1300.
   PubMedGoogle Scholar
• Dudek, H., S. R. Datta, T. F. Franke, M. J. Birnbaum, R. Yao, G. M. Cooper, R. A. Segal, D. R. Kaplan, and M. E. Greenberg. 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661–665.
   PubMed Web of Science ®Google Scholar
• Dufner, A., and G. Thomas. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253:100–109.
   PubMed Web of Science ®Google Scholar
• Emanuelli, B., P. Peraldi, C. Filloux, D. Sawka-Verhelle, D. Hilton, and E. van Obberghen. 2000. SOCS-3 is an insulin-induced negative regulator of insulin signaling. J. Biol. Chem. 275:15985–15991.
   PubMedGoogle Scholar
• English, J., G. Pearson, J. Wilsbacher, J. Swantek, M. Karandikar, S. Xu, and M. H. Cobb. 1999. New insights into the control of MAP kinase pathways. Exp. Cell Res. 253:255–270.
   PubMed Web of Science ®Google Scholar
• Florio, M., M. C. Hernandez, H. Yang, H. K. Shu, J. L. Cleveland, and M. A. Israel. 1998. Id2 promotes apoptosis by a novel mechanism independent of dimerization to basic helix-loop-helix factors. Mol. Cell. Biol. 18:5435–5444.
   PubMedGoogle Scholar
• Garcia, R., C. L. Yu, A. Hudnall, R. Catlett, K. L. Nelson, T. Smithgall, D. J. Fujita, S. P. Ethier, and R. Jove. 1997. Constitutive activation of Stat3 in fibroblasts transformed by diverse oncoproteins and in breast carcinoma cells. Cell Growth Differentiation 8:1267–1276.
   PubMedGoogle Scholar
• Garrington, T. P., and G. L. Johnson. 1999. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell Biol. 11:211–218.
   PubMed Web of Science ®Google Scholar
• Gu, H., H. Maeda, J. J. Moon, J. D. Lord, M. Yoakim, B. H. Nelson, and B. G. Neel. 2000. New role for Shc in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol. Cell. Biol. 20:7109–7120.
   PubMed Web of Science ®Google Scholar
• Gual, P., V. Baron, V. Lequoy, and E. van Obberghen. 1998. Interaction of Janus kinases JAK-1 and JAK-2 with the insulin receptor and the insulin-like growth factor 1 receptor. Endocrinology 139:884–893.
   PubMedGoogle Scholar
• Hara, E., T. Yamaguchi, H. Nojima, T. Ide, J. Campisi, H. Okayama, and K. Oda. 1994. Id related genes encoding HLH proteins are required for G1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269:2139–2145.
   PubMed Web of Science ®Google Scholar
• Hawley, R. G., F. H. Lieu, A. Z. Fong, and T. S. Hawley. 1994. Versatile retroviral vectors for potential use in gene therapy. Gene Ther. 1:136–138.
   PubMed Web of Science ®Google Scholar
• Iavarone, A., P. Garg, A. Lasorella, J. Hsu, and M. A. Israel. 1994. The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8:1270–1284.
   PubMedGoogle Scholar
• Ishiguro, A., K. S. Spirin, M. Shioara, A. Tobler, A. F. Gombart, M. A. Israel, J. D. Norton, and H. P. Koeffler. 1996. Id2 expression increases with differentiation of human myeloid cells. Blood 87:5225–5231.
   PubMedGoogle Scholar
• Jen, Y., K. Manova, and R. Benezra. 1996. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev. Dyn. 207:235–252.
   PubMed Web of Science ®Google Scholar
• Kennedy, S. G., A. J. Wagner, S. D. Conzen, J. Jordan, A. Bellacosa, P. N. Tsichlis, and N. Hay. 1997. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11:701–713.
   PubMed Web of Science ®Google Scholar
• Khwaja, A., P. Rodriguez-Viciana, S. Wennstrom, P. H. Warne, and J. Downward. 1997. Matrix adhesion and ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/AAkt cellular survival pathway. EMBO J. 16:2783–2793.
   PubMed Web of Science ®Google Scholar
• Koval, A. P., V. A. Blakesley, C. T. Roberts Jr., V. Zick, and D. LeRoith. 1998. Interaction in vitro of the product of the c-Crk-II proto-oncogene with the insulin-like growth factor 1 receptor. Biochem. J. 330:923–932.
   PubMedGoogle Scholar
• Kreider, B. L., R. Benezra, G. Rovera, and T. Kadesch. 1992. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science 255:1700–1702.
   PubMedGoogle Scholar
• Kulik, G., and M. J. Weber. 1998. Akt-dependent and -independent survival signaling pathways utilized by insulin-like growth factor 1. Mol. Cell. Biol. 18:6711–6718.
   PubMed Web of Science ®Google Scholar
• Lasorella, A., M. Noseda, M. Beyna, and A. Iavarone. 2000. Id2 is a retinoblasoma protein target and mediates signaling by Myc oncoproteins. Nature 407:592–598.
   PubMedGoogle Scholar
• Lin, C. Q., J. Singh, K. Murata, Y. Itahana, S. Parrinello, S. H. Liang, C. E. Gillett, J. Campisi, and P. Y. Desprez. 2000. A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res. 60:1332–1340.
   PubMedGoogle Scholar
• Lister, J., W. C. Forrester, and M. H. Baron. 1995. Inhibition of an erythroid differentiation switch by the helix-loop-helix protein Id1. J. Biol. Chem. 270:17939–17946.
   PubMedGoogle Scholar
• Lyden, D., A. Z. Young, D. Zagzag, W. Yan, R. O'Reilly, B. L. Bader, R. O. Hynes, Y. Zhuang, K. Manova, and R. Benezra. 1999. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401:670–677.
   PubMed Web of Science ®Google Scholar
• Minami, M., M. Inoue, S. Wei, K. Takeda, M. Matsumoto, D. Kishimoto, and S. Akira. 1996. STAT3 activation is a critical step in gp130-mediated terminal differentiation and growth arrest of a myeloid cell line. Proc. Natl. Acad. Sci. USA 93:3963–3966.
   PubMed Web of Science ®Google Scholar
• Nakajima, K., Y. Yamanaka, K. Nakae, H. Kojima, M. Ichiba, N. Kiuchi, T. Kitaoka, T. Fukada, M. Hibi, and T. Hirano. 1996. A central role of Stat3 on IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15:3651–3658.
   PubMed Web of Science ®Google Scholar
• Navarro, M., and R. Baserga. 2001. Limited redundancy of survival signals from the type 1 insulin-like growth factor receptor. Endocrinology 142:1073–1081.
   PubMed Web of Science ®Google Scholar
• Nickoloff, B. J., V. Chaturvedi, P. Bacon, J. Z. Qin, M. F. Denning, and M. O. Diaz. 2000. Id-1 delays senescence but does not immortalize keratinocytes. J. Biol. Chem. 275:27501–27504.
   PubMed Web of Science ®Google Scholar
• Norton, J. D., R. W. Deed, G. Craggs, and F. Sablitzky. 1998. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8:58–65.
   PubMedGoogle Scholar
• Nosaka, T., T. Kawashima, K. Misawa, K. Ikuta, A. L. F. Mui, and T. Kitamura. 1999. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 18:4754–4765.
   PubMed Web of Science ®Google Scholar
• Peruzzi, F., M. Prisco, M. Dews, P. Salomoni, E. Grassilli, G. Romano, B. Calabretta, and R. Baserga. 1999. Multiple signaling pathways of the IGF-I receptor in protection from apoptosis. Mol. Cell. Biol. 19:7203–7215.
   PubMed Web of Science ®Google Scholar
• Prisco, M., G. Romano, F. Peruzzi, B. Valentinis, and R. Baserga. 1999. Insulin and IGF-I receptor signaling in protection from apoptosis. Horm. Metab. Res. 31:80–89.
   PubMedGoogle Scholar
• Raz, R., C. K. Lee, L. A. Cannizzaro, P. D'Eustachio, and D. E. Levy. 1999. Essential role of STAT3 for embryonic stem cell pluripotency. Proc. Natl. Acad. Sci. USA 96:2846–2851.
   PubMedGoogle Scholar
• Rodriguez-Tarduchy, G., M. K. L. Collins, I. Garcia, and A. Lopez-Rivas. 1992. Insulin-like growth factor I inhibits apoptosis in IL-3 dependent hemopoietic cells. J. Immunol. 149:535–540.
   PubMed Web of Science ®Google Scholar
• Sasaoka, T., B. Draznin, J. W. Leitner, W. J. Langlois, and J. M. Olefsky. 1994. Shc is the predominant signaling molecule coupling insulin receptors to activation of guanine nucleotide releasing factor and p21ras-GTP formation. J. Biol. Chem. 269:10734–10738.
   PubMed Web of Science ®Google Scholar
• Scher, C. D., R. C. Shephard, H. N. Antoniades, and C. D. Stiles. 1979. Platelet derived growth factor and the regulation of the mammalian fibroblast cell cycle. Biochim. Biophys. Acta 560:217–241.
   PubMed Web of Science ®Google Scholar
• Shimozaki, K., K. Nakajima, T. Hirano, and S. Nagata. 1997. Involvement of STAT3 in the granulocyte colony-stimulating factor-induced differentiation of myeloid cells. J. Biol. Chem. 272:25184–25189.
   PubMed Web of Science ®Google Scholar
• Soon, L., L. Flechner, J. S. Gutkind, L. H. Wang, R. Baserga, J. H. Pierce, and W. Li. 1999. Insulin-like growth factor 1 synergizes with interleukin 4 for hematopoietic cell proliferation independent of insulin receptor substrate expression. Mol. Cell. Biol. 19:3816–3828.
   PubMed Web of Science ®Google Scholar
• Steinman, R. A., and A. Iro. 1999. Suppression of G-CSF-mediated Stat signalling by IL-3. Leukemia 13:54–61.
   PubMedGoogle Scholar
• Sun, X. H., N. G. Copeland, N. A. Jenkins, and D. Baltimore. 1991. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11:5603–5611.
   PubMed Web of Science ®Google Scholar
• Tartare-Deckert, S., D. Sawka-Verhelle, J. Murdaca, and van E. Obberghen. 1996. Evidence for a differential interaction of SHC and the insulin receptor substrate-1 (IRS-1) with the insulin-like growth factor-I (IGF-I) receptor in the yeast two-hybrid system. J. Biol. Chem. 271:23456–23460.
   Google Scholar
• Valentinis, B., M. Navarro, T. Zanocco-Marani, P. Edmonds, J. McCormick, A. Morrione, A. Sacchi, G. Romano, K. Reiss, and R. Baserga. 2000. Insulin receptor substrate-1, p70S6K and cell size in transformation and differentiation of hemopoietic cells. J. Biol. Chem. 275:25451–25459.
   PubMed Web of Science ®Google Scholar
• Valentinis, B., G. Romano, F. Peruzzi, A. Morrione, M. Prisco, S. Soddu, B. Cristofanelli, A. Sacchi, and R. Baserga. 1999. Growth and differentiation signals by the insulin-like growth factor 1 receptor in hemopoietic cells are mediated through different pathways. J. Biol. Chem. 274:12423–12430.
   PubMed Web of Science ®Google Scholar
• Valtieri, M., D. J. Tweardy, D. Caracciolo, K. Johnson, F. Mavilio, S. Altmann, D. Santoli, and G. Rovera. 1987. Cytokine dependent granulocytic differentiation. J. Immunol. 138:3829–3835.
   PubMed Web of Science ®Google Scholar
• Wang, L. M., M. G. Myers Jr., X. J. Sun, S. A. Aaronson, M. White, and J. H. Pierce. 1993. IRS-1: essential for insulin- and IL-4-stimulated mitogenesis in hemopoietic cells. Science 261:1591–1594.
   PubMedGoogle Scholar
• Ward, A. C., L. Smith, J. P. de Koning, Y. van Aesch, and I. P. Touw. 1999. Multiple signals mediate proliferation, differentiation and survival from the granulocyte-colony stimulating factor receptor in myeloid 32D cells. J. Biol. Chem. 274:14956–14962.
   PubMed Web of Science ®Google Scholar
• White, M. F.. 1998. The IRS-signalling system: a network of docking proteins that mediate insulin action. Mol. Cell. Biochem. 182:3–11.
   PubMed Web of Science ®Google Scholar
• Wu, Y. Y., and R. A. Bradshaw. 2000. Activation of Stat3 signaling pathway is required for differentiation by interleukin-6 in OC12–E2 cells. J. Biol. Chem. 275:2147–2156.
   PubMedGoogle Scholar
• Yenush, L., C. Zanella, T. Uchida, D. Bernal, and M. F. White. 1998. The pleckstrin homology and phosphotyrosine binding domains of insulin receptor substrate 1 mediate inhibition of apoptosis by insulin. Mol. Cell. Biol. 18:6784–6794.
   PubMed Web of Science ®Google Scholar
• Zhang, V., J. Turkson, C. Carter-Su, T. Smithgall, A. Levitzki, A. Kraker, J. J. Krolewski, P. Medveczky, and R. Jove. 2000. Activation of Stat3 in v-src transformed fibroblasts requires cooperation of Jak1 kinase activity. J. Biol. Chem. 275:24935–24944.
   PubMed Web of Science ®Google Scholar
• Zong, C. S., J. Chan, D. E. Levy, C. Horvath, H. B. Sadowski, and L. H. Wang. 2000. Mechanism of STAT3 activation by insulin-like growth factor I receptor. J. Biol. Chem. 275:15099–15105.
   PubMed Web of Science ®Google Scholar
• Zong, C. S., L. Zong, Y. Jiang, H. B. Sadowski, and L. H. Wang. 1998. Stat3 plays an important role in oncogenic ros- and insulin-like growth factor 1 receptor-induced anchorage-independent growth. J. Biol. Chem. 273:28065–28072.
   PubMed Web of Science ®Google Scholar