Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor: Implications for breast cancer treatment

Cancer Research

Volumn 72, Issue 13, 2012, Pages 3372-3380

  Fagan, Dedra H ^b   Uselman, Ryan R ^a   Sachdev, Deepali ^a,c   Yee, Douglas ^a,b,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEW 541; DALOTUZUMAB; INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B; PROTEIN TYROSINE KINASE INHIBITOR; SOMATOMEDIN B; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TAMOXIFEN CITRATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER RESISTANCE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RECEPTOR DOWN REGULATION; TREATMENT RESPONSE; TUMOR XENOGRAFT;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CELL ADHESION; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; HUMANS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; TAMOXIFEN;

EID: 84863584930     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0684     Document Type: Article

References (38)

1. MacGregor JI, Jordan VC. Basic guide to the mechanisms of antiestrogen action. Pharmacol Rev 1998;50:151-96. (Pubitemid 28305723)
2. Tanno S, Mitsuuchi Y, Altomare DA, Xiao GH, Testa JR. AKT activation up-regulates insulin-like growth factor I receptor expression and promotes invasiveness of human pancreatic cancer cells. Cancer Res 2001;61:589-93. (Pubitemid 32128619)
3. Ciampolillo A, De Tullio C, Giorgino F. The IGF-I/IGF-I receptor pathway: implications in the pathophysiology of thyroid cancer. Curr Med Chem 2005;12:2881-91. (Pubitemid 41613364)
4. Lee AV, Darbre P, King RJ. Processing of insulin-like growth factor-II (IGF-II) by human breast cancer cells. Mol Cell Endocrinol 1994;99:211-20.
5. Lee AV, Jackson JG, Gooch JL, Hilsenbeck SG, Coronado-Heinsohn E, Osborne CK, et al. Enhancement of insulin-like growth factor signaling in human breast cancer: estrogen regulation of insulin receptor substrate-1 expression in vitro and in vivo. Mol Endocrinol 1999;13:787-96. (Pubitemid 30645331)
6. Molloy CA, May FE, Westley BR. Insulin receptor substrate-1 expression is regulated by estrogen in the MCF-7 human breast cancer cell line. J Biol Chem 2000;275:12565-71. (Pubitemid 30241403)
7. Murphy LJ, Murphy LC, Friesen HG. Estrogen induces insulin-like growth factor-I expression in the rat uterus. Mol Endocrinol 1987;1:445-50. (Pubitemid 17165983)
8. Umayahara Y, Kawamori R, Watada H, Imano E, Iwama N, Morishima T, et al. Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer. J Biol Chem 1994;269:16433-42. (Pubitemid 24209344)
9. Becker MA, Ibrahim YH, Cui X, Lee AV, Yee D. The IGF pathway regulates ERalpha through a S6K1-dependent mechanism in breast cancer cells. Mol Endocrinol 2011;25:516-28.
10. Osborne R. Commercial interest waxes for IGF-1 blockers. Nat Biotechnol 2008;26:719-20.
11. Fagan DH, Yee D. Crosstalk between IGF1R and estrogen receptor signaling in breast cancer. J Mammary Gland Biol Neoplasia 2008;13:423-9.
12. Kaufman PA, Ferrero JM, Bourgeois H, Kennecke H, De Boer R, Jacot W, et al. A randomized, double-blind, placebo-controlled, phase 2 study of AMG 479 with Exemestane (E) or Fulvestrant (F) in postmenopausal women with hormone-receptor positive (HR+) metastatic (M) or locally advanced (LA) breast cancer (BC). Cancer Res 2010;70:76s.
13. Avnet S, Sciacca L, Salerno M, Gancitano G, Cassarino MF, Longhi A, et al. Insulin receptor isoform A and insulin-like growth factor II as additional treatment targets in human osteosarcoma. Cancer Res 2009;69:2443-52.
14. Frasca F, Pandini G, Sciacca L, Pezzino V, Squatrito S, Belfiore A, et al. The role of insulin receptors and IGF-I receptors in cancer and other diseases. Arch Physiol Biochem 2008;114:23-37. (Pubitemid 351998752)
15. 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.
16. Zhang H, Pelzer AM, Kiang DT, Yee D. Down-regulation of type I insulin-like growth factor receptor increases sensitivity of breast cancer cells to insulin. Cancer Res 2007;67:391-7. (Pubitemid 46142798)
17. Ulanet DB, Ludwig DL, Kahn CR, Hanahan D. Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF-1R targeted therapy. Proc Natl Acad Sci U S A 2010;107:10791-8.
18. Pollak M. Targeting insulin and insulin-like growth factor signalling in oncology. Curr Opin Pharmacol 2008;8:384-92.
19. Twentyman PR, Luscombe M. A study of some variables in a tetrazolium dye (MTT) based assay for cell growth and chemosensitivity. Br J Cancer 1987;56:279-85. (Pubitemid 17158816)
20. Levin-Allerhand JA, Sokol K, Smith JD. Safe and effective method for chronic 17beta-estradiol administration to mice. Contemp Top Lab Anim Sci 2003;42:33-5. (Pubitemid 37498992)
21. Goetsch L, Gonzalez A, Leger O, Beck A, Pauwels PJ, Haeuw JF, et al. A recombinant humanized anti-insulin-like growth factor receptor type I antibody (h7C10) enhances the antitumor activity of vinorelbine and anti-epidermal growth factor receptor therapy against human cancer xenografts. Int J Cancer 2005;113:316-28. (Pubitemid 39628325)
22. Pandini G, Wurch T, Akla B, Corvaia N, Belfiore A, Goetsch L. Functional responses and in vivo anti-tumour activity of h7C10: a humanised monoclonal antibody with neutralising activity against the insulin- like growth factor-1 (IGF-1) receptor and insulin/IGF-1 hybrid receptors. Eur J Cancer 2007;43:1318-27. (Pubitemid 46720250)
23. Sachdev D, Li SL, Hartell JS, Fujita-Yamaguchi Y, Miller JS, Yee D. A chimeric humanized single-chain antibody against the type I insulinlike growth factor (IGF) receptor renders breast cancer cells refractory to the mitogenic effects of IGF-I. Cancer Res 2003;63:627-35. (Pubitemid 36158140)
24. Wiseman LR, Johnson MD, Wakeling AE, Lykkesfeldt AE, May FE, Westley BR. Type I IGF receptor and acquired tamoxifen resistance in oestrogen-responsive human breast cancer cells. Eur J Cancer 1993;29A:2256-64. (Pubitemid 24053004)
25. Freiss G, Rochefort H, Vignon F. Mechanisms of 4-hydroxytamoxifen anti-growth factor activity in breast cancer cells: alterations of growth factor receptor binding sites and tyrosine kinase activity. Biochem Biophys Res Commun 1990;173:919-26.
26. Huynh H, Yang X, Pollak M. Estradiol and antiestrogens regulate a growth inhibitory insulin-like growth factor binding protein 3 autocrine loop in human breast cancer cells. J Biol Chem 1996;271:1016-21. (Pubitemid 26034960)
27. Pratt SE, Pollak MN. Estrogen and antiestrogen modulation of MCF7 human breast cancer cell proliferation is associated with specific alterations in accumulation of insulin-like growth factor-binding proteins in conditioned media. Cancer Res 1993;53:5193-8. (Pubitemid 23333387)
28. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S, et al. Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res 2008;68:826-33. (Pubitemid 351206760)
29. Pollak M. Insulin and insulin-like growth factor signalling in neoplasia. Nat Rev Cancer 2008;8:915-28.
30. Tolcher AW, Sarantopoulos J, Patnaik A, Papadopoulos K, Lin CC, Rodon J, et al. Phase I, pharmacokinetic, and pharmacodynamic study of AMG 479, a fully human monoclonal antibody to insulin-like growth factor receptor 1. J Clin Oncol 2009;27:5800-7.
31. Drury S, Detre S, Leary A, Salter J, Reis-Filho J, Barbashina V, et al. Changes in breast cancer biomarkers in the IGF1R/PI3K pathway in recurrent breast cancer after tamoxifen treatment. Endocr Relat Cancer 2011;18:565-77.
32. Gallagher EJ, LeRoith D. The proliferating role of insulin and insulinlike growth factors in cancer. Trends Endocrinol Metab 2010;21:610-8.
33. Haluska P, Shaw HM, Batzel GN, Yin D, Molina JR, Molife LR, et al. Phase I dose escalation study of the anti insulin-like growth factor-I receptor monoclonal antibody CP-751,871 in patients with refractory solid tumors. Clin Cancer Res 2007;13:5834-40. (Pubitemid 47583908)
34. Shah SP, Morin RD, Khattra J, Prentice L, Pugh T, Burleigh A, et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009;461:809-13.
35. Haluska P, Hou X, Huang F, Harrington S, Greer A, Macedo L, et al. Complete IGF signaling blockade by the dual-kinase inhibitor, BMS-754807, is sufficient to overcome tamoxifen and letrozole resistance in vitro and in vivo. Cancer Res 2009;69:402.
36. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006;66:1500-8. (Pubitemid 43259931)
37. Di Cosimo S, Bendell JC, Cervantes-Ruiperez A, Roda D, Prudkin L, Stein MN, et al. A phase I study of the oral mTOR inhibitor ridaforolimus (RIDA) in combination with the IGF-1R antibody dalotuzumab (DALO) in patients (pts) with advanced solid tumors. J Clin Oncol 28:15s, 2010 (suppl; abstr 3008).
38. Naing A, LoRusso P, Gupta S, Benjamin S, Rohren E, Chen HX, et al. Dual inhibition of IGFR andmTORpathways. J Clin Oncol 28:15s, 2010 (suppl; abstr 3007).