Repression of malignant tumor progression upon pharmacologic IGF1R blockade in a mouse model of insulinoma

Molecular Cancer Research

Volumn 10, Issue 6, 2012, Pages 800-809

  Zumsteg, Adrian ^a,c   Caviezel, Christoph ^a   Pisarsky, Laura ^a   Strittmatter, Karin ^a   Garciá Echeverría, Carlos ^b,d   Hofmann, Francesco ^b   Christofori, Gerhard ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NOVARTIS PHARMA AG   (Switzerland)

^c HARVARD UNIVERSITY   (United States)

^d SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOMEDIN C RECEPTOR;

ADENOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER INHIBITION; CANCER SURVIVAL; CARCINOGENESIS; CONTROLLED STUDY; DISEASE MODEL; DRUG EFFICACY; GROWTH INHIBITION; HUMAN; HUMAN CELL; INSULINOMA; INVASIVE CARCINOMA; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TUMOR CELL; TUMOR GROWTH; TUMOR VOLUME;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; IMMUNOBLOTTING; IN SITU NICK-END LABELING; INSULINOMA; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PYRIMIDINES; PYRROLES; RECEPTOR, IGF TYPE 1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR BURDEN;

EID: 84862576877     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0522     Document Type: Article

References (42)

1. Pollak M. Insulin and insulin-like growth factor signalling in neoplasia. Nat Rev Cancer 2008;8:915-28.
2. Maki RG. Small is beautiful: insulin-like growth factors and their role in growth, development, and cancer. J Clin Oncol 2010;28:4985-95.
3. Gualberto A, Pollak M. Emerging role of insulin-like growth factor receptor inhibitors in oncology: early clinical trial results and future directions. Oncogene 2009;28:3009-21.
4. Baserga R. Customizing the targeting of IGF-1 receptor. Future Oncol 2009;5:43-50.
5. Hofmann F, Garcia-Echeverria C. Blocking the insulin-like growth factor-I receptor as a strategy for targeting cancer. Drug Discov Today 2005;10:1041-7. (Pubitemid 41074142)
6. Brown J, Jones EY, Forbes BE. Keeping IGF-II under control: lessons from the IGF-II-IGF2R crystal structure. Trends Biochem Sci 2009;34:612-9.
7. Ullrich A, Gray A, Tam AW, Yang-Feng T, Tsubokawa M, Collins C, et al. Insulin-like growth factor I receptor primary structure: comparison with insulin receptor suggests structural determinants that define functional specificity. EMBO J 1986;5:2503-12.
8. Chitnis MM, Yuen JS, Protheroe AS, Pollak M, Macaulay VM. The type 1 insulin-like growth factor receptor pathway. Clin Cancer Res 2008;14:6364-70.
9. Swenne I. Pancreatic beta-cell growth and diabetes mellitus. Diabetologia 1992;35:193-201.
10. Hugl SR, White MF, Rhodes CJ. Insulin-like growth factor I (IGF-I)-stimulated pancreatic beta-cell growth is glucose-dependent. Synergistic activation of insulin receptor substrate-mediated signal transduction pathways by glucose and IGF-I in INS-1 cells. J Biol Chem 1998;273:17771-9. (Pubitemid 28355120)
11. Lingohr MK, Dickson LM, McCuaig JF, Hugl SR, Twardzik DR, Rhodes CJ. Activation of IRS-2-mediated signal transduction by IGF-1, but not TGF-alpha or EGF, augments pancreatic beta-cell proliferation. Diabetes 2002;51:966-76. (Pubitemid 34438338)
12. Arany E, Hill DJ. Ontogeny of fibroblast growth factors in the early development of the rat endocrine pancreas. Pediatr Res 2000;48:389-403. (Pubitemid 30637344)
13. Hill DJ, Petrik J, Arany E, McDonald TJ, Delovitch TL. Insulin-like growth factors prevent cytokine-mediated cell death in isolated islets of Langerhans from pre-diabetic non-obese diabetic mice. J Endocrinol 1999;161:153-65. (Pubitemid 29170202)
14. Liu W, Chin-Chance C, Lee EJ, Lowe WL Jr. Activation of phosphatidylinositol 3-kinase contributes to insulin-like growth factor I-mediated inhibition of pancreatic beta-cell death. Endocrinology 2002;143:3802-12. (Pubitemid 35244359)
15. Lu Y, Herrera PL, Guo Y, Sun D, Tang Z, LeRoith D, et al. Pancreatic-specific inactivation of IGF-I gene causes enlarged pancreatic islets and significant resistance to diabetes. Diabetes 2004;53:3131-41. (Pubitemid 39564488)
16. Kulkarni RN, Holzenberger M, Shih DQ, Ozcan U, Stoffel M, Magnuson MA, et al. beta-cell-specific deletion of the Igf1 receptor leads to hyperinsulinemia and glucose intolerance but does not alter beta-cell mass. Nat Genet 2002;31:111-5.
17. Sell C, Rubini M, Rubin R, Liu JP, Efstratiadis A, Baserga R. Simian virus 40 large tumor antigen is unable to transform mouse embryonic fibroblasts lacking type 1 insulin-like growth factor receptor. Proc Natl Acad Sci U S A 1993;90:11217-21. (Pubitemid 23354400)
18. Yakar S, Leroith D, Brodt P. The role of the growth hormone/insulin-like growth factor axis in tumor growth and progression: lessons from animal models. Cytokine Growth Factor Rev 2005;16:407-20. (Pubitemid 41022011)
19. DiGiovanni J, Bol DK, Wilker E, Beltran L, Carbajal S, Moats S, et al. Constitutive expression of insulin-like growth factor-1 in epidermal basal cells of transgenic mice leads to spontaneous tumor promotion. Cancer Res 2000;60:1561-70. (Pubitemid 30183426)
20. DiGiovanni J, Kiguchi K, Frijhoff A, Wilker E, Bol DK, Beltran L, et al. Deregulated expression of insulin-like growth factor 1 in prostate epithelium leads to neoplasia in transgenic mice. Proc Natl Acad Sci U S A 2000;97:3455-60. (Pubitemid 30183324)
21. Rogler CE, Yang D, Rossetti L, Donohoe J, Alt E, Chang CJ, et al. Altered body composition and increased frequency of diverse malignancies in insulin-like growth factor-II transgenic mice. J Biol Chem 1994;269:13779-84. (Pubitemid 24191120)
22. Renehan AG, Zwahlen M, Minder C, O'Dwyer ST, Shalet SM, Egger M. Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet 2004;363:1346-53. (Pubitemid 38529873)
23. Jenkins PJ, Mukherjee A, Shalet SM. Does growth hormone cause cancer? Clin Endocrinol (Oxf) 2006;64:115-21.
24. Burtscher I, Christofori G. The IGF/IGF-1 receptor signaling pathway as a potential target for cancer therapy. Drug Resist Updat 1999;2:3-8. (Pubitemid 29217088)
25. Hanahan D. Heritable formation of pancreatic beta-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 1985;315:115-22. (Pubitemid 15064530)
26. Christofori G, Naik P, Hanahan D. A second signal supplied by insulin-like growth factor II in oncogene-induced tumorigenesis. Nature 1994;369:414-8.
27. Christofori G, Naik P, Hanahan D. Deregulation of both imprinted and expressed alleles of the insulin-like growth factor 2 gene during beta-cell tumorigenesis. Nat Genet 1995;10:196-201.
28. Lopez T, Hanahan D. Elevated levels of IGF-1 receptor convey invasive and metastatic capability in a mouse model of pancreatic islet tumorigenesis. Cancer Cell 2002;1:339-53. (Pubitemid 41039136)
29. Tanno B, Mancini C, Vitali R, Mancuso M, McDowell HP, Dominici C, et al. Down-regulation of insulin-like growth factor I receptor activity by NVP-AEW541 has an antitumor effect on neuroblastoma cells in vitro and in vivo. Clin Cancer Res 2006;12:6772-80. (Pubitemid 44876847)
30. Manara MC, Landuzzi L, Nanni P, Nicoletti G, Zambelli D, Lollini PL, et al. Preclinical in vivo study of new insulin-like growth factor-I receptor-specific inhibitor in Ewing's sarcoma. Clin Cancer Res 2007;13:1322-30. (Pubitemid 46424074)
31. Garcia-Echeverria C, Pearson MA, Marti A, Meyer T, Mestan J, Zimmermann J, et al. In vivo antitumor activity of NVP-AEW541-A novel, potent, and selective inhibitor of the IGF-IR kinase. Cancer Cell 2004;5:231-9. (Pubitemid 38402115)
32. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, Akiyama M, et al. Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiplemyeloma, other hematologic malignancies, and solid tumors. Cancer Cell 2004;5:221-30. (Pubitemid 38402114)
33. Warshamana-Greene GS, Litz J, Buchdunger E, Garcia-Echeverria C, Hofmann F, Krystal GW. The insulin-like growth factor-I receptor kinase inhibitor, NVP-ADW742, sensitizes small cell lung cancer cell lines to the effects of chemotherapy. Clin Cancer Res 2005;11:1563-71. (Pubitemid 40315241)
34. Gotlieb WH, Bruchim I, Gu J, Shi Y, Camirand A, Blouin MJ, et al. Insulin-like growth factor receptor I targeting in epithelial ovarian cancer. Gynecol Oncol 2006;100:389-96. (Pubitemid 43075275)
35. Hopfner M, Sutter AP, Huether A, Ahnert-Hilger G, Scherubl H. A novel approach in the treatment of neuroendocrine gastrointestinal tumors: additive antiproliferative effects of interferon-gamma and meta-iodobenzylguanidine. BMC Cancer 2004;4:23.
36. Efrat S, Linde S, Kofod H, Spector D, Delannoy M, Grant S, et al. Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene. Proc Natl Acad Sci U S A 1988;85:9037-41. (Pubitemid 19001836)
37. Inoue M, Hager JH, Ferrara N, Gerber HP, Hanahan D. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell 2002;1:193-202. (Pubitemid 41039165)
38. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007;117:1155-66. (Pubitemid 46718400)
39. Ulanet DB, Ludwig DL, Kahn CR, Hanahan D. Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF1R targeted therapy. Proc Natl Acad Sci U S A 2010;107:10791-8.
40. Menu E, Jernberg-Wiklund H, Stromberg T, De Raeve H, Girnita L, Larsson O, et al. Inhibiting the IGF-1 receptor tyrosine kinase with the cyclolignan PPP: an in vitro and in vivo study in the 5T33MM mouse model. Blood 2006;107:655-60. (Pubitemid 43076391)
41. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998;392:190-3. (Pubitemid 28162793)
42. Zhang H, Fagan DH, Zeng X, Freeman KT, Sachdev D, Yee D. Inhibition of cancer cell proliferation and metastasis by insulin receptor downregulation. Oncogene 2010;29:2517-27.