Oncogenic transformation by the signaling adaptor proteins insulin receptor substrate (IRS)-1 and IRS-2

Cell Cycle

Volumn 6, Issue 6, 2007, Pages 705-713

  Dearth, Robert K ^a   Cui, Xiaojiang ^a   Kim, Hyun Jung ^a   Hadsell, Darryl L ^a   Lee, Adrian V ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Breast cancer; Cancer; Insulin receptor substrate; IRS 1; IRS 2; Mammary gland; Oncogene; Transformation; Transgenic mouse

Indexed keywords

ADAPTOR PROTEIN; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; SMALL INTERFERING RNA;

BREAST CANCER; BREAST DEVELOPMENT; BREAST METASTASIS; CARCINOGENESIS; CARCINOGENICITY; CELL DIFFERENTIATION; CELL GROWTH; CELL METABOLISM; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECT; HUMAN; MAMMARY GLAND; MOLECULAR CLONING; NONHUMAN; ONCOGENE; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW;

MUS MUSCULUS;

EID: 34047198390     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6.6.4035     Document Type: Review

References (153)

1. Ambrogio C, Voena C, Manazza AD, Piva R, Riera L, Barberis L, Costa C, Tarone G, Defilippi P, Hirsch E, Erba EB, Mohammed S, Jensen ON, Palestro G, Inghirami G, Chiarle R. p130Cas mediates the transforming properties of the anaplastic lymphoma kinase. Blood 2005; 106:3907-16.
2. Senechal K, Halpern J, Sawyers CL. The CRKL adaptor protein transforms fibroblasts and functions in transformation by the BCR-ABL oncogene. J Biol Chem 1996; 271:23255-61.
3. Singer CF, Hudelist G, Lamm W, Mueller R, Handl C, Kubista E, Czerwenka K. Active (p)CrkL is overexpressed in human malignancies: Potential role as a surrogate parameter for therapeutic tyrosine kinase inhibition. Oncol Rep 2006; 15:353-9.
4. Mood K, Saucier C, Bong YS, Lee HS, Park M, Daar IO. Gab1 is required for cell cycle transition, cell proliferation, and transformation induced by an oncogenic met receptor. Mol Biol Cell 2006; 17:3717-28.
5. Saucier C, Papavasiliou V, Palazzo A, Naujokas MA, Kremer R, Park M. Use of signal specific receptor tyrosine kinase oncoproteins reveals that pathways downstream from Grb2 or Shc are sufficient for cell transformation and metastasis. Oncogene 2002; 21:1800-11.
6. Fixman ED, Fournier TM, Kamikura DM, Naujokas MA, Park M. Pathways downstream of Shc and Grb2 are required for cell transformation by the tpr-Met oncoprotein. J Biol Chem 1996; 271:13116-22.
7. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003; 4:915-25.
8. Ma PC, Kijima T, Maulik G, Fox EA, Sattler M, Griffin JD, Johnson BE, Salgia R. c-MET mutational analysis in small cell lung cancer: Novel juxtamembrane domain mutations regulating cytoskeletal functions. Cancer Res 2003; 63:6272-81.
9. Zhang YW, Vande Woude GF. HGF/SF-met signaling in the control of branching morphogenesis and invasion. J Cell Biochem 2003; 88:408-17.
10. Terui E, Matsunaga T, Yoshida H, Kouchi K, Kuroda H, Hishiki T, Saito T, Yamada S, Shirasawa H, Ohnuma N. Shc family expression in neuroblastoma: High expression of shcC is associated with a poor prognosis in advanced neuroblastoma. Clin Cancer Res 2005; 11:3280-7.
11. Hynes NE, Stern DF. The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim Biophys Acta 1994; 1198:165-84.
12. Yamasaki S, Nishida K, Yoshida Y, Itoh M, Hibi M, Hirano T. Gab1 is required for EGF receptor signaling and the transformation by activated ErbB2. Oncogene 2003; 22:1546-56.
13. Bentires-Alj M, Gil SG, Chan R, Wang ZC, Wang Y, Imanaka N, Harris LN, Richardson A, Neel BG, Gu H. A role for the scaffolding adapter GAB2 in breast cancer. Nat Med 2006; 12:114-21.
14. van der Flier S, Brinkman A, Look MP, Kok EM, Meijer-van Gelder ME, Klijn JG, Dorssers LC, Foekens JA. Bcar1/p130Cas protein and primary breast cancer: Prognosis and response to tamoxifen treatment. J Natl Cancer Inst 2000; 92:120-7.
15. Cabodi S, Tinnirello A, Di Stefano P, Bisaro B, Ambrosino E, Castellano I, Sapino A, Arisio R, Cavallo F, Forni G, Glukhova M, Silengo L, Altruda F, Turco E, Tarone G, Defilippi P. p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis. Cancer Res 2006; 66:4672-80.
16. Kao J, Pollack JR. RNA interference-based functional dissection of the 17q12 amplicon in breast cancer reveals contribution of coamplified genes. Genes Chromosomes Cancer 2006; 45:761-9.
17. Lee YH, White MF. Insulin receptor substrate proteins and diabetes. Arch Pharm Res 2004; 27:361-70.
18. Sun XJ, Rothenberg P, Kahn CR, Backer JM, Araki E, Wilden PA, Cahill DA, Goldstein BJ, White MF. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 1991; 352:73-7.
19. Sun XJ, Wang LM, Zhang Y, Yenush L, Myers Jr MG, Glasheen E, Lane WS, Pierce JH, White MF. Role of IRS-2 in insulin and cytokine signalling. Nature 1995; 377:173-7.
20. Smith-Hall J, Pons S, Patti ME, Burks DJ, Yenush L, Sun XJ, Kahn CR, White MF. The 60 kDa insulin receptor substrate functions like an IRS protein (pp60IRS3) in adipose cells. Biochemistry 1997; 36:8304-10.
21. Lavan BE, Fantin VR, Chang ET, Lane WS, Keller SR, Lienhard GE. A novel 160-kDa phosphotyrosine protein in insulin-treated embryonic kidney cells is a new member of the insulin receptor substrate family. Journal of Biological Chemistry 1997; 272:21403-7.
22. Cai D, Dhe-Paganon S, Melendez PA, Lee J, Shoelson SE. Two new substrates in insulin signaling, IRS5/DOK4 and IRS6/DOK5. J Biol Chem 2003; 278:25323-30.
23. Surmacz E. Function of the IGF-I receptor in breast cancer. J Mammary Gland Biol Neoplasia 2000; 5:95-105.
24. Myers Jr MG, Sun XJ, Cheatham B, Jachna BR, Glasheen EM, Backer JM, White MF. IRS-1 is a common element in insulin and insulin-like growth factor-I signaling to the phosphatidylinositol 3'-kinase. Endocrinology 1993; 132:1421-30.
25. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: Insights into insulin action. Nat Rev Mol Cell Biol 2006; 7:85-96.
26. Ridderstrale M, Degerman E, Tornqvist H. Growth hormone stimulates the tyrosine phosphorylation of the insulin receptor substrate-1 and its association with phosphatidylinositol 3-kinase in primary adipocytes. J Biol Chem 1995; 270:3471-4.
27. Cui X, Lazard Z, Zhang P, Hopp TA, Lee AV. Progesterone crosstalks with insulin-like growth factor signaling in breast cancer cells via induction of insulin receptor substrate-2. Oncogene 2003; 22:6937-41.
28. Cui X, Kim HJ, Kuiatse I, Kim H, Brown PH, Lee AV. Epidermal growth factor induces insulin receptor substrate-2 in breast cancer cells via c-Jun NH(2)-terminal kinase/activator protein-1 signaling to regulate cell migration. Cancer Res 2006; 66:5304-13.
29. Platanias LC, Fish EN. Signaling pathways activated by interferons. Exp Hematol 1999; 27:1583-92.
30. White MF, Yenush L. The IRS-signaling system: A network of docking proteins that mediate insulin and cytokine action. Curr Top Microbiol Immunol 1998; 228:179-208.
31. Yamauchi T, Kaburagi Y, Ueki K, Tsuji Y, Stark GR, Kerr IM, Tsushima T, Akanuma Y, Komuro I, Tobe K, Yazaki Y, Kadowaki T. Growth hormone and prolactin stimulate tyrosine phosphorylation of insulin receptor substrate-1, -2, and -3, their association with p85 phosphatidylinositol 3-kinase (PI3-kinase), and concomitantly PI3- kinase activation via JAK2 kinase. J Biol Chem 1998; 273:15719-26.
32. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 2002; 283:E413-22.
33. Yamauchi T, Tobe K, Tamemoto H, Ueki K, Kaburagi Y, Yamamoto-Honda R, Takahashi Y, Yoshizawa F, Aizawa S, Akanuma Y, Sonenberg N, Yazaki Y, Kadowaki T. Insulin signalling and insulin actions in the muscles and livers of insulin-resistant, insulin receptor substrate 1-deficient mice. Mol Cell Biol 1996; 16:3074-84.
34. Withers DJ, Gutierrez JS, Towery H, Burks DJ, Ren JM, Previs S, Zhang Y, Bernal D, Pons S, Shulman GI, Bonner-Weir S, White MF. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 1998; 391:900-4.
35. Tanaka S, Wands JR. A carboxy-terminal truncated insulin receptor substrate-1 dominant negative protein reverses the human hepatocellular carcinoma malignant phenotype. J Clin Invest 1996; 98:2100-8.
36. Bergmann U, Funatomi H, Kornmann M, Beger HG, Korc M. Increased expression of insulin receptor substrate-1 in human pancreatic cancer. Biochem Biophys Res Commun 1996; 220:886-90.
37. Chang Q, Li Y, White MF, Fletcher JA, Xiao S. Constitutive activation of insulin receptor substrate 1 is a frequent event in human tumors: Therapeutic implications. Cancer Res 2002; 62:6035-8.
38. Sun XJ, Miralpeix M, Myers Jr MG, Glasheen EM, Backer JM, Kahn CR, White MF. Expression and function of IRS-1 in insulin signal transmission. J Biol Chem 1992; 267:22662-72.
39. Myers Jr MG, White MF. The new elements of insulin signaling: Insulin receptor substrate-1 and proteins with SH2 domains. Diabetes 1993; 42:643-50.
40. Hadsell DL, Alexeenko T, Klemintidis Y, Torres D, Lee AV. Inability of overexpressed des(1-3)human insulin-like growth factor I (IGF-I) to inhibit forced mammary gland involution is associated with decreased expression of IGF signaling molecules. Endocrinology 2001; 142:1479-88.
41. Wu X, Sallinen K, Anttila L, Makinen M, Luo C, Pollanen P, Erkkola R. Expression of insulin-receptor substrate-1 and -2 in ovaries from women with insulin resistance and from controls. Fertil Steril 2000; 74:564-72.
42. Lee AV, Jackson JG, Gooch JL, Hilsenbeck SG, Coronado-Heinsohn E, Osborne CK, Yee D. Enhancement of insulin-like growth factor signaling in human breast cancer: Estrogen regulation of insulin receptor substrate-1 expression in vitro and in vivo. Molecular Endocrinology 1999; 13:787-96.
43. Oesterreich S, Zhang P, Guler RL, Sun X, Curran E, Welshons WV, Lee AV. Reexpression of estrogen receptor α in estrogen receptror α-negative MCF-7 cells results in restoration of estrogen and IGF-mediated signaling and proliferation. Cancer Research 2001, (In press August 1st).
44. Sisci D, Morelli C, Garofalo C, Romeo F, Morabito L, Casaburi F, Middea E, Cascio S, Brunelli E, Ando S, Surmacz E. Expression of nuclear insulin receptor substrate 1 (IRS-1) in breast cancer. J Clin Pathol 2006.
45. Jager J, Gremeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-indu ced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007; 148:241-51.
46. Bjornholm M, Zierath JR. Insulin signal transduction in human skeletal muscle: Identifying the defects in Type II diabetes. Biochem Soc Trans 2005; 33:354-7.
47. Araki E, Lipes MA, Patti ME, Bruning JC, Haag IIIrd B, Johnson RS, Kahn CR. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 1994; 372:186-90.
48. Vassen L, Wegrzyn W, Klein-Hitpass L. Human insulin receptor substrate-2: Gene organization and promoter characterization. Diabetes 1999; 48:1877-80, [In Process Citation].
49. He W, Craparo A, Zhu Y, O'Neill TJ, Wang LM, Pierce JH, Gustafson TA. Interaction of insulin receptor substrate-2 (IRS-2) with the insulin and insulin-like growth factor I receptors: Evidence for two distinct phosphotyrosine-dependent interaction domains within IRS-2, [In Process Citation]. J Biol Chem 1996; 271:11641-5.
50. Sawka-Verhelle D, Tartare-Deckert S, White MF, Van Obberghen E. Insulin receptor substrate-2 binds to the insulin receptor through its phosphotyrosine-binding domain and through a newly identified domain comprising amino acids 591-786. J Biol Chem 1996; 271:5980-3.
51. Araki E, Lipes MA, Patti M, Bruning JC, Haag IIIrd B, Johnson RS, Kahn CR. Alternative pathway of insulin-signaling in mice with targeted disruption of the IRS-1 gene. Nature 1994; 372:186-90.
52. Liu SC, Wang Q, Lienhard GE, Keller SR. Insulin receptor substrate 3 is not essential for growth or glucose homeostasis. J Biol Chem 1999; 274:18093-9.
53. Fantin VR, Wang Q, Lienhard GE, Keller SR. Mice lacking insulin receptor substrate 4 exhibit mild defects in growth, reproduction, and glucose homeostasis. Am J Physiol Endocrinol Metab 2000; 278:E127-33.
54. Shepherd PR. Mechanisms regulating phosphoinositide 3-kinase signalling in insulin-sensitive tissues. Acta Physiol Scand 2005; 183:3-12.
55. Shepherd PR, Withers DJ, Siddle K. Phosphoinositide 3-kinase: The key switch mechanism in insulin signalling. Biochem J 1998; 333(Pt 3):471-90.
56. Cantley LC. The role of phosphoinositide 3-kinase in human disease. Harvey Lect 2004; 100:103-22.
57. White MF. The IRS-signaling system: A network of docking proteins that mediate insulin and cytokine action. Recent Prog Horm Res 1998; 53:119-38.
58. Myers Jr MG, Wang LM, Sun XJ, Zhang Y, Yenush L, Schlessinger J, Pierce JH, White MF. Role of IRS-1-GRB-2 complexes in insulin signaling. Mol Cell Biol 1994; 14:3577-87.
59. Skolnik EY, Batzer A, Li N, Lee CH, Lowenstein E, Mohammadi M, Margolis B, Schlessinger J. The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science 1993; 260:1953-5.
60. Torii S, Yamamoto T, Tsuchiya Y, Nishida E. ERK MAP kinase in G cell cycle progression and cancer. Cancer Sci 2006; 97:697-702.
61. Xiao S, Rose DW, Sasaoka T, Maegawa H, Burke Jr TR, Roller PP, Shoelson SE, Olefsky JM. Syp (SH-PTP2) is a positive mediator of growth factor-stimulated mitogenic signal transduction. J Biol Chem 1994; 269:21244-8.
62. Kuhne MR, Pawson T, Lienhard GE, Feng GS. The insulin receptor substrate 1 associates with the SH2-containing phosphotyrosine phosphatase Syp. J Biol Chem 1993; 268:11479-81.
63. Amoui M, Craddock BP, Miller WT. Differential phosphorylation of IRS-1 by insulin and insulin-like growth factor I receptors in Chinese hamster ovary cells. J Endocrinol 2001; 171:153-62.
64. Sasaoka T, Rose DW, Jhun BH, Saltiel AR, Draznin B, Olefsky JM. Evidence for a functional role of Shc proteins in mitogenic signaling induced by insulin, insulin-like growth factor-1, and epidermal growth factor. J Biol Chem 1994; 269:13689-94.
65. Noguchi T, Matozaki T, Horita K, Fujioka Y, Kasuga M. Role of SH-PTP2, a protein-tyrosine phosphatase with Src homology 2 domains, in insulin-stimulated Ras activation. Molecular and Cellular Biology 1994; 14:6674-82.
66. Yamauchi K, Milarski KL, Saltiel AR, Pessin JE. Protein-tyrosine- phosphatase SHPTP2 is a required positive effector for insulin downstream signaling. Proc Natl Acad Sci USA 1995; 92:664-8.
67. Sun XJ, Pons S, Asano T, Myers Jr MG, Glasheen E, White MF. The Fyn tyrosine kinase binds Irs-1 and forms a distinct signaling complex during insulin stimulation. J Biol Chem 1996; 271:10583-7.
68. Beitner-Johnson D, Blakesley VA, Shen-Orr Z, Jimenez M, Stannard B, Wang LM, Pierce J, LeRoith D. The proto-oncogene product c-Crk associates with insulin receptor substrate-1 and 4PS: Modulation by insulin growth factor-I (IGF) and enhanced IGF-I signaling. J Biol Chem 1996; 271:9287-90.
69. Lee CH, Li W, Nishimura R, Zhou M, Batzer AG, Myers Jr MG, White MF, Schlessinger J, Skolnik EY. Nck associates with the SH2 domain-docking protein IRS-1 in insulin-stimulated cells. Proc Natl Acad Sci USA 1993; 90:11713-7.
70. Bruning JC, Winnay J, Cheatham B, Kahn CR. Differential signaling by insulin receptor substrate 1 (IRS-1) and IRS-2 in IRS-1-deficient cells. Molecular and Cellular Biology 1997; 17:1513-21.
71. Burfoot MS, Rogers NC, Watling D, Smith JM, Pons S, Paonessaw G, Pellegrini S, White MF, Kerr IM. Janus kinase-dependent activation of insulin receptor substrate 1 in response to interleukin-4, oncostatin M, and the interferons. J Biol Chem 1997; 272:24183-90.
72. Jiang H, Harris MB, Rothman P. IL-4/IL-13 signaling beyond JAK/STAT. J Allergy Clin Immunol 2000; 105:1063-70.
73. Knoops L, Renauld JC. IL-9 and its receptor: From signal transduction to tumorigenesis. Growth Factors 2004; 22:207-15.
74. Yenush L, White MF. The IRS-signalling system during insulin and cytokine action. Bioessays 1997; 19:491-500.
75. Izuhara K, Harada N. Interleukin-4 activates two distinct pathways of phosphatidylinositol-3 kinase in the same cells. Biochem Biophys Res Commun 1996; 229:624-9.
76. Chilton BS, Hewetson A. Prolactin and growth hormone signaling. Curr Top Dev Biol 2005; 68:1-23.
77. Liang L, Jiang J, Frank SJ. Insulin receptor substrate-1-mediated enhancement of growth hormone-induced mitogen-activated protein kinase activation. Endocrinology 2000; 141:3328-36.
78. Berlanga JJ, Gualillo O, Buteau H, Applanat M, Kelly PA, Edery M. Prolactin activates tyrosyl phosphorylation of insulin receptor substrate 1 and phosphatidylinositol-3-OH kinase. J Biol Chem 1997; 272:2050-2.
79. Myers Jr MG, Leptin receptor signaling and the regulation of mammalian physiology. Recent Prog Horm Res 2004; 59:287-304.
80. Ueno H, Kondo E, Yamamoto-Honda R, Tobe K, Nakamoto T, Sasaki K, Mitani K, Furusaka A, Tanaka T, Tsujimoto Y, Kadowaki T, Hirai H. Association of insulin receptor substrate proteins with Bcl-2 and their effects on its phosphorylation and antiapoptotic function. Mol Biol Cell 2000; 11:735-46.
81. D'Ambrosio C, Keller SR, Morrione A, Lienhard GE, Baserga R, Surmacz E. Transforming potential of the insulin receptor substrate 1. Cell Growth and Differentiation 1995; 6:557-62.
82. Ogihara T, Isobe T, Ichimura T, Taoka M, Funaki M, Sakoda H, Onishi Y, Inukai K, Anai M, Fukushima Y, Kikuchi M, Yazaki Y, Oka Y, Asano T. 14-3-3 protein binds to insulin receptor substrate-1, one of the binding sites of which is in the phosphotyrosine binding domain. Journal of Biological Chemistry 1997; 272:25267-74.
83. Kosaki A, Yamada K, Suga J, Otaka A, Kuzuya H. 14-3-3beta protein associates with insulin receptor substrate 1 and decreases insulin-stimulated phosphatidylinositol 3'-kinase activity in 3T3L1 adipocytes. Journal of Biological Chemistry 1998; 273:940-4.
84. Lebrun P, Mothe-Satney I, Delahaye L, Van Obberghen E, Baron V. Insulin receptor substrate-1 as a signaling molecule for focal adhesion kinase pp125(FAK) and pp60(src). J Biol Chem 1998; 273:32244-53.
85. Lebrun P, Baron V, Hauck CR, Schlaepfer DD, Van Obberghen E. Cell adhesion and focal adhesion kinase regulate insulin receptor substrate-1 expression. J Biol Chem 2000; 275:38371-7.
86. Li Z, Joyal JL, Sacks DB. Binding of IRS proteins to calmodulin is enhanced in insulin resistance. Biochemistry 2000; 39:5089-96.
87. Algenstaedt P, Antonetti DA, Yaffe MB, Kahn CR. Insulin receptor substrate proteins create a link between the tyrosine phosphorylation cascade and the Ca2+-ATPases in muscle and heart. J Biol Chem 1997; 272:23696-702.
88. Prisco M, Santini F, Baffa R, Liu M, Drakas R, Wu A, Baserga R. Nuclear translocation of insulin receptor substrate-1 by the simian virus 40 T antigen and the activated type 1 insulin-like growth factor receptor. J Biol Chem 2002; 277:32078-85.
89. 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; 277:44357-65.
90. 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; 195:453-60.
91. Sun H, Tu X, Prisco M, Wu A, Casiburi I, Baserga R. Insulin-like growth factor I receptor signaling and nuclear translocation of insulin receptor substrates 1 and 2. Mol Endocrinol 2003; 17:472-86.
92. Del Valle L, Wang JY, Lassak A, Peruzzi F, Croul S, Khalili K, Reiss K. Insulin-like growth factor I receptor signaling system in JC virus T antigen-induced primitive neuroectodermal tumors-medulloblastomas. J Neurovirol 2002; 8(Suppl 2):138-47.
93. Chen J, Wu A, Sun H, Drakas R, Garofalo C, Cascio S, Surmacz E, Baserga R. Functional significance of type 1 insulin-like growth factor-mediated nuclear translocation of the insulin receptor substrate-1 and beta-catenin. J Biol Chem 2005; 280:29912-20.
94. Morelli C, Garofalo C, Sisci D, del Rincon S, Cascio S, Tu X, Vecchione A, Sauter ER, Miller Jr WH, Surmacz E. Nuclear insulin receptor substrate 1 interacts with estrogen receptor alpha at ERE promoters. Oncogene 2004; 23:7517-26.
95. Trojanek J, Ho T, Del Valle L, Nowicki M, Wang JY, Lassak A, Peruzzi F, Khalili K, Skorski T, Reiss K. Role of the insulin-like growth factor I/insulin receptor substrate 1 axis in Rad51 trafficking and DNA repair by homologous recombination. Mol Cell Biol 2003; 23:7510-24.
96. Ueki K, Kondo T, Kahn CR. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 2004; 24:5434-46.
97. Inaba M, Saito H, Fujimoto M, Sumitani S, Ohkawara T, Tanaka T, Kouhara H, Kasayama S, Kawase I, Kishimoto T, Naka T. Suppressor of cytokine signaling 1 suppresses muscle differentiation through modulation of IGF-I receptor signal transduction. Biochem Biophys Res Commun 2005; 328:953-61.
98. Alexander WS, Hilton DJ. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol 2004; 22:503-29.
99. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 1996; 271:665-8.
100. Folli F, Kahn CR, Hansen H, Bouchie JL, Feener EP. Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels: A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. Journal of Clinical Investigation 1997; 100:2158-69.
101. Paz K, Hemi R, LeRoith D, Kanety H, Zick Y. The p-tyr binding (PTB) domain of insulin receptor substrate (IRS) proteins serves as a substrate for protein kinase B (PKB): Possible involvement of PKB in insulin-resistance induced by hyperinsulinemia. Proceddings of the Endocrine Society 1998; OR17-2:75.
102. De Fea K, Roth RA. Protein kinase C modulation of insulin receptor substrate-1 tyrosine phosphorylation requires serine 612. Biochemistry 1997; 36:12939-47.
103. Tanasijevic MJ, Myers Jr MG, Thoma RS, Crimmins DL, White MF, Sacks DB. Phosphorylation of the insulin receptor substrate IRS-1 by casein kinase II. Journal of Biological Chemistry 1993; 268:18157-66.
104. De Fea K, Roth RA. Modulation of insulin receptor substrate-1 tyrosine phosphorylation and function by mitogen-activated protein kinase. Journal of Biological Chemistry 1997; 272:31400-6.
105. Aguirre V, Uchida T, Yenush L, Davis R, White MF. The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 2000; 275:9047-54.
106. Begum N, Sandu OA, Ito M, Lohmann SM, Smolenski A. Active Rho kinase (ROK-alpha) associates with insulin receptor substrate-1 and inhibits insulin signaling in vascular smooth muscle cells. J Biol Chem 2002; 277:6214-22.
107. Freund GG, Wittig JG, Mooney RA. The PI3-kinase serine kinase phosphorylates its p85 subunit and IRS-1 in PI3-kinase/IRS-1 complexes. Biochemical and Biophysical Research Communications 1995; 206:272-8.
108. Lam K, Carpenter CL, Ruderman NB, Friel JC, Kelly KL. The phosphatidylinositol 3-kinase serine kinase phosphorylates IRS-1: Stimulation by insulin and inhibition by Wortmannin. Journal of Biological Chemistry 1994; 269:20648-52.
109. Tanti JF, Gremeaux T, Van Obberghen E, Le Marchand-Brustel Y. Insulin receptor substrate 1 is phosphorylated by the serine kinase activity of phosphatidylinositol 3-kinase. Biochemical Journal 1994; 304:17-21.
110. Lee AV, Gooch JL, Oesterreich S, Guler RL, Yee D. Insulin-like growth factor I-induced degradation of insulin receptor substrate 1 is mediated by the 26S proteasome and blocked by phosphatidylinositol 3'-kinase inhibition. Mol Cell Biol 2000; 20:1489-96.
111. Sun XJ, Goldberg JL, Qiao LY, Mitchell JJ. Insulin-induced insulin receptor substrate-1 degradation is mediated by the proteasome degradation pathway. Diabetes 1999; 48:1359-64.
112. Haruta T, Uno T, Kawahara J, Takano A, Egawa K, Sharma PM, Olefsky JM, Kobayashi M. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1, [In Process Citation]. Mol Endocrinol 2000; 14:783-94.
113. Shi Y, Yan H, Frost P, Gera J, Lichtenstein A. Mammalian target of rapamycin inhibitors activate the AKT kinase in multiple myeloma cells by up-regulating the insulin-like growth factor receptor/insulin receptor substrate-1/phosphatidylinositol 3-kinase cascade. Mol Cancer Ther 2005; 4:1533-40.
114. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, Baselga J, Rosen N. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006; 66:1500-8.
115. Lee AV, Zhang P, Ivanova M, Bonnette S, Oesterreich S, Rosen JM, Grimm S, Hovey RC, Vonderhaar BK, Kahn CR, Torres D, George J, Mohsin S, Allred DC, Hadsell DL. Developmental and hormonal signals dramatically alter the localization and abundance of insulin receptor substrate proteins in the mammary gland. Endocrinology 2003; 144:2683-94.
116. Hovey RC, Harris J, Hadsell DL, Lee AV, Ormandy CJ, Vonderhaar BK. Local insulin-like growth factor-II mediates prolactin-induced mammary gland development. Molecular Endocrinology 2002, (Published December 23, 2002 as doi:10.1210/me.2002-0214).
117. Green KA, Naylor MJ, Lowe ET, Wang P, Marshman E, Streuli CH. Caspase-mediated cleavage of insulin receptor substrate. J Biol Chem 2004; 279:25149-56.
118. Lee AV, Taylor ST, Greenall J, Mills JD, Tonge DW, Zhang P, George J, Fiorotto ML, Hadsell DL. Rapid induction of IGF-IR signaling in normal and tumor tissue following intravenous injection of IGF-I in mice. Horm Metab Res 2003; 35:651-5.
119. Ito T, Sasaki Y, Wands JR. Overexpression of human insulin receptor substrate 1 induces cellular transformation with activation of mitogen-activated protein kinases. Mol Cell Biol 1996; 16:943-51.
120. Tanaka S, Ito T, Wands JR. Neoplastic transformation induced by insulin receptor substrate-1 overexpression requires an interaction with both Grb2 and Syp signaling molecules. J Biol Chem 1996; 271:14610-6.
121. DeAngelis T, Chen J, Wu A, Prisco M, Baserga R. Transformation by the simian virus 40 T antigen is regulated by IGF-I receptor and IRS-1 signaling. Oncogene 2006; 25:32-42.
122. Cristofanelli B, Valentinis B, Soddu S, Rizzo MG, Marchetti A, Bossi G, Morena AR, Dews M, Baserga R, Sacchi A. Cooperative transformation of 32D cells by the combined expression of IRS-1 and V-Ha-Ras. Oncogene 2000; 19:3245-55.
123. Khalili K, Del Valle L, Wang JY, Darbinian N, Lassak A, Safak M, Reiss K. T-antigen of human polyomavirus JC cooperates with IGF-IR signaling system in cerebellar tumors of the childhood-medulloblastomas. Anticancer Res 2003; 23:2035-41.
124. Fei ZL, D'Ambrosio C, Li S, Surmacz E, Baserga R. Association of insulin receptor substrate 1 with simian virus 40 large T antigen. Mol Cell Biol 1995; 15:4232-39.
125. Melillo RM, Carlomagno F, De Vita G, Formisano P, Vecchio G, Fusco A, Billaud M, Santoro M. The insulin receptor substrate (IRS)-1 recruits phosphatidylinositol 3-kinase to Ret: Evidence for a competition between Shc and IRS-1 for the binding to Ret. Oncogene 2001; 20:209-18.
126. Hennige AM, Lammers R, Arlt D, Hoppner W, Strack V, Niederfellner G, Seif FJ, Haring HU, Kellerer M. Ret oncogene signal transduction via a IRS-2/PI 3-kinase/PKB and a SHC/Grb-2 dependent pathway: Possible implication for transforming activity in NIH3T3 cells. Mol Cell Endocrinol 2000; 167:69-76.
127. Lannon CL, Martin MJ, Tognon CE, Jin W, Kim SJ, Sorensen PH. A highly conserved NTRK3 C-terminal sequence in the ETV6-NTRK3 oncoprotein binds the phosphotyrosine binding domain of insulin receptor substrate-1: An essential interaction for transformation. J Biol Chem 2004; 279:6225-34.
128. Reiss K, Khalili K, Giordano A, Trojanek J. JC virus large T-antigen and IGF-I signaling system merge to affect DNA repair and genomic integrity. J Cell Physiol 2006; 206:295-300.
129. Nishiyama M, Wands JR. Cloning and increased expression of an insulin receptor substrate-1- like gene in human hepatocellular carcinoma. Biochem Biophys Res Commun 1992; 183:280-5.
130. Nehrbass D, Klimek F, Bannasch P. Overexpression of insulin receptor substrate-1 emerges early in hepatocarcinogenesis and elicits preneoplastic hepatic glycogenosis. Am J Pathol 1998; 152:341-5.
131. Boissan M, Beurel E, Wendum D, Rey C, Lecluse Y, Housset C, Lacombe ML, Desbois-Mouthon C. Overexpression of insulin receptor substrate-2 in human and murine hepatocellular carcinoma. Am J Pathol 2005; 167:869-77.
132. Tanaka S, Wands JR. Insulin receptor substrate 1 overexpression in human hepatocellular carcinoma cells prevents transforming growth factor beta1-induced apoptosis. Cancer Res 1996; 56:3391-4.
133. Kornmann M, Maruyama H, Bergmann U, Tangvoranuntakul P, Beger HG, White MF, Korc M. Enhanced expression of the insulin receptor substrate-2 docking protein in human pancreatic cancer. Cancer Res 1998; 58:4250-4.
134. Han CH, Cho JY, Moon JT, Kim HJ, Kim SK, Shin DH, Chang J, Ahn CM, Kim SK, Chang YS. Clinical significance of insulin receptor substrate-I down-regulation in nonsmall cell lung cancer. Oncol Rep 2006; 16:1205-10.
135. Jackson JG, White MF, Yee D. Insulin receptor substrate-1 is the predominant signaling molecule activated by insulin-like growth factor-I, insulin, and interleukin-4 in estrogen receptor-positive human breast cancer cells. J Biol Chem 1998; 273:9994-10003.
136. Dunn SE, Ehrlich M, Sharp NJ, Reiss K, Solomon G, Hawkins R, Baserga R, Barrett JC. A dominant negative mutant of the insulin-like growth factor-I receptor inhibits the adhesion, invasion, and metastasis of breast cancer. Cancer Research 1998; 58:3353-61.
137. Surmacz E, Burgard JL. Overexpression of IRS-1 in the human breast cancer cell line MCF-7 induces loss of estrogen requirements for growth and transformation. Clinical Cancer Research 1995; 1:1429-36.
138. Nolan MK, Jankowska L, Prisco M, Xu S, Guvakova MA, Surmacz E. Differential roles of IRS-1 and SHC signaling pathways in breast cancer cells. International Journal of Cancer 1997; 72:828-34.
139. Cesarone G, Garofalo C, Abrams MT, Igoucheva O, Alexeev V, Yoon K, Surmacz E, Wickstrom E. RNAi-mediated silencing of insulin receptor substrate 1 (IRS-1) enhances tamoxifen-induced cell death in MCF-7 breast cancer cells. J Cell Biochem 2006; 98:440-50.
140. Jackson JG, Yoneda T, Yee D. Increased insulin receptor substrate-2 (IRS-2) signaling correlates with high metastati phenotype in human breast cancer cells. Proceeding of the Endocrine Society 1999, (81st Annual Meeting:P3-193).
141. Nagle JA, Ma Z, Byrne MA, White MF, Shaw LM. Involvement of insulin receptor substrate 2 in mammary tumor metastasis. Mol Cell Biol 2004; 24:9726-35.
142. Ma Z, Gibson SL, Byrne MA, Zhang J, White MF, Shaw LM. Suppression of insulin receptor substrate-1 (lRS-1) promotes mammary tumor metastasis. Mol Cell Biol 2006.
143. Byron SA, Horwitz KB, Richer JK, Lange CA, Zhang X, Yee D. Insulin receptor substrates mediate distinct biological responses to insulin-like growth factor receptor activation in breast cancer cells. Br J Cancer 2006; 95:1220-8.
144. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 2005; 5:675-88.
145. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001; 3:785-92.
146. Dearth RK, Cui X, Kim HJ, Kuiatse I, Lawrence NA, Zhang X, Divisova J, Britton OL, Mohsin S, Allred DC, Hadsell DL, Lee AV. Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate 1 (IRS-1) or IRS-2. Mol Cell Biol 2006; 26:9302-14.
147. Rosner A, Miyoshi K, Landesman-Bollag E, Xu X, Seldin DC, Moser AR, MacLeod CL, Shyamala G, Gillgrass AE, Cardiff RD. Pathway pathology: Histological differences between ErbB/Ras and Wnt pathway transgenic mammary tumors. Am J Pathol 2002; 161:1087-97.
148. Hemmeryckx B, van Wijk A, Reichert A, Kaartinen V, de Jong R, Pattengale PK, Gonzalez-Gomez I, Groffen J, Heisterkamp N. Crkl enhances leukemogenesis in BCR/ABL P190 transgenic mice. Cancer Res 2001; 61:1398-405.
149. Webster MA, Hutchinson JN, Rauh MJ, Muthuswamy SK, Anton M, Tortorice CG, Cardiff RD, Graham FL, Hassell JA, Muller WJ. Requirement for both Shc and phosphatidylinositol 3' kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol Cell Biol 1998; 18:2344-59.
150. Green JE, Hudson T. The promise of genetically engineered mice for cancer prevention studies. Nat Rev Cancer 2005; 5:184-98.
151. Rocha RL, Hilsenbeck SG, Jackson JG, VanDenBerg CL, Weng C, Lee AV, Yee D. Insulin-like growth factor binding protein-3 and insulin receptor substrate-1 in breast cancer: Correlation with clinical parameters and disease-free survival. Clin Cancer Res 1997; 3:103-9.
152. Koda M, Sulkowska M, Kanczuga-Koda L, Sulkowski S. Expression of insulin
153. Schnarr B, Strunz K, Ohsam J, Benner A, Wacker J, Mayer D. Down-regulation of insulinlike growth factor-I receptor and insulin receptor substrate-1 expression in advanced human breast cancer. Int J Cancer 2000; 89:506-13.