HMGA1 controls transcription of insulin receptor to regulate cyclin D1 translation in pancreatic cancer cells

Cancer Research

Volumn 67, Issue 10, 2007, Pages 4679-4686

  Kolb, Sebastian ^a   Fritsch, Ralph ^a   Saur, Dieter ^a   Reichert, Maximilian ^a   Schmid, Roland M ^a   Schneider, Günter ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; HIGH MOBILITY GROUP A PROTEIN; INITIATION FACTOR 4E; INSULIN RECEPTOR; SMALL INTERFERING RNA;

ARTICLE; CANCER CELL; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; HUMAN; HUMAN CELL; PANCREAS CANCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING;

CELL GROWTH PROCESSES; CELL LINE, TUMOR; CYCLIN D1; GENE EXPRESSION REGULATION, NEOPLASTIC; HMGA1A PROTEIN; HUMANS; PANCREATIC NEOPLASMS; PROTEIN BIOSYNTHESIS; RECEPTOR, INSULIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 34250311157     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-3308     Document Type: Article

References (46)

1. Reeves R, Beckerbauer LM. HMGA proteins as therapeutic drug targets. Prog Cell Cycle Res 2003;5:279-86.
2. Sgarra R, Rustighi A, Tessari MA, et al. Nuclear phosphoproteins HMGA and their relationship with chromatin structure and cancer. FEBS Lett 2004;574:1-8.
3. Reeves R. Molecular biology of HMGA proteins: hubs of nuclear function. Gene 2001;277:63-81.
4. Wood LJ, Maher JF, Bunton TE, Resar LM. The oncogenic properties of the HMG-I gene family. Cancer Res 2000;60:4256-61.
5. Treff NR, Pouchnik D, Dement GA, Britt RL, Reeves R. High-mobility group A1a protein regulates Ras/ERK signaling in MCF-7 human breast cancer cells. Oncogene 2004;23:777-85.
6. Xu Y, Sumter TF, Bhattacharya R, et al. The HMG-I oncogene causes highly penetrant, aggressive lymphoid malignancy in transgenic mice and is overexpressed in human leukemia. Cancer Res 2004;64:3371-5.
7. Fedele M, Pentimalli F, Baldassarre G, et al. Transgenic mice overexpressing the wild-type form of the HMGA1 gene develop mixed growth hormone/prolactin cell pituitary adenomas and natural killer cell lymphomas. Oncogene 2005;24:3427-35.
8. Abe N, Watanabe T, Masaki T, et al. Pancreatic duct cell carcinomas express high levels of high mobility group I(Y) proteins. Cancer Res 2000;60:3117-22.
9. Tarbe N, Evtimova V, Burtscher H, Jarsch M, Alves F, Weidle UH. Transcriptional profiling of cell lines derived from an orthotopic pancreatic tumor model reveals metastasis-associated genes. Anticancer Res 2001;21: 3221-8.
10. Trapasso F, Sarti M, Cesari R, et al. Therapy of human pancreatic carcinoma based on suppression of HMGA1 protein synthesis in preclinical models. Cancer Gene Ther 2004;11:633-41.
11. Rozenblum E, Schutte M, Goggins M, et al. Tumor-suppressive pathways in pancreatic carcinoma. Cancer Res 1997;57:1731-4.
12. Huang L, Lang D, Geradts J, et al. Molecular and immunochemical analyses of RB1 and cyclin D1 in human ductal pancreatic carcinomas and cell lines. Mol Carcinog 1996;15:85-95.
13. Gansauge S, Gansauge F, Ramadani M, et al. Overexpression of cyclin D1 in human pancreatic carcinoma is associated with poor prognosis. Cancer Res 1997;57:1634-7.
14. Kornmann M, Ishiwata T, Itakura J, Tangvoranuntakul P, Beger HG, Korc M. Increased cyclin D1 in human pancreatic cancer is associated with decreased postoperative survival. Oncology 1998;55:363-9.
15. Alt JR, Cleveland JL, Hannink M, Diehl JA. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev 2000;14:3102-14.
16. Diehl JA, Zindy F, Sherr CJ. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 1997;11:957-72.
17. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998;12:3499-511.
18. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsichlis P, Rosen N. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 1998;273:29864-72.
19. Koziczak M, Hynes NE. Cooperation between fibroblast growth factor receptor-4 and ErbB2 in regulation of cyclin D1 translation. J Biol Chem 2004; 279:50004-11.
20. Rosenwald IB, Kaspar R, Rousseau D, et al. Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and posttranscriptional levels. J Biol Chem 1995;270:21176-80.
21. Rousseau D, Kaspar R, Rosenwald I, Gehrke L, Sonenberg N. Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc Natl Acad Sci U S A 1996;93: 1065-70.
22. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004;18:1926-45.
23. Foti D, Iuliano R, Chiefari E, Brunetti A. A nucleoprotein complex containing Sp1, C/EBP β, and HMGI-Y controls human insulin receptor gene transcription. Mol Cell Biol 2003;23:2720-32.
24. Paonessa F, Foti D, Costa V, et al. Activator protein-2 overexpression accounts for increased insulin receptor expression in human breast cancer. Cancer Res 2006;66: 5085-93.
25. 1- to S-phase progression. EMBO J 2006;25:3801-12.
26. Johnson KR, Disney JE, Wyatt CR, Reeves R. Expression of mRNAs encoding mammalian chromosomal proteins HMG-I and HMG-Y during cellular proliferation. Exp Cell Res 1990;187:69-76.
27. Thanos D, Du W, Maniatis T. The high mobility group protein HMG I(Y) is an essential structural component of a virus-inducible enhancer complex. Cold Spring Harb Symp Quant Biol 1993;58:73-81.
28. Reeves R, Edberg DD, Li Y. Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol Cell Biol 2001;21:575-94.
29. Diehl JA, Benzeno S. Cyclin D1 and pancreatic carcinoma: a proliferative agonist and chemotherapeutic antagonist. Clin Cancer Res 2005;11:5665-7.
30. Nissen MS, Langan TA, Reeves R. Phosphorylation by cdc2 kinase modulates DNA binding activity of high mobility group I nonhistone chromatin protein. J Biol Chem 1991;266:19945-52.
31. Gingras AC, Raught B, Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 1999; 68:913-63.
32. Dever TE. Gene-specific regulation by general translation factors. Cell 2002;108:545-56.
33. Gingras AC, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001; 15:807-26.
34. Mamane Y, Petroulakis E, Rong L, Yoshida K, Ler LW, Sonenberg N. eIF4E-from translation to transformation. Oncogene 2004;23:3172-9.
35. Gingras AC, Gygi SP, Raught B, et al. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 1999;13:1422-37.
36. Massague J, Blinderman LA, Czech MP. The high affinity insulin receptor mediates growth stimulation in rat hepatoma cells. J Biol Chem 1982;257:13958-63.
37. Straus DS. Growth-stimulatory actions of insulin in vitro and in vivo. Endocr Rev 1984;5:356-69.
38. Giorgino F, Belfiore A, Milazzo G, et al. Overexpression of insulin receptors in fibroblast and ovary cells induces a ligand-mediated transformed phenotype. Mol Endocrinol 1991;5:452-9.
39. Milazzo G, Giorgino F, Damante G, et al. Insulin receptor expression and function in human breast cancer cell lines. Cancer Res 1992;52:3924-30.
40. Fisher WE, Boros LG, Schirmer WJ. Insulin promotes pancreatic cancer: evidence for endocrine influence on exocrine pancreatic tumors. J Surg Res 1996;63:310-3.
41. Kornmann M, Maruyama H, Bergmann U, et al. Enhanced expression of the insulin receptor substrate-2 docking protein in human pancreatic cancer. Cancer Res 1998;58:4250-4.
42. 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.
43. Asano T, Yao Y, Shin S, McCubrey J, Abbruzzese JL, Reddy SA. Insulin receptor substrate is a mediator of phosphoinositide 3-kinase activation in quiescent pancreatic cancer cells. Cancer Res 2005;65:9164-8.
44. Lawrence JC, Jr., Abraham RT. PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem Sci 1997;22:345-9.
45. Brunetti A, Manfioletti G, Chiefari E, Goldfine ID, Foti D. Transcriptional regulation of human insulin receptor gene by the high-mobility group protein HMGI(Y). FASEB J 2001;15:492-500.
46. Foti D, Chiefari E, Fedele M, et al. Lack of the architectural factor HMGA1 causes insulin resistance and diabetes in humans and mice. Nat Med 2005;11: 765-73.