Insulin receptor phosphorylation by endogenous insulin or the insulin analog AspB10 promotes mammary tumor growth independent of the IGF-I receptor

Diabetes

Volumn 62, Issue 10, 2013, Pages 3553-3560

  Gallagher, Emily Jane ^a   Alikhani, Nyosha ^a   Tobin Hess, Aviva ^a   Blank, Jeffrey ^a   Buffin, Nicholas J ^a   Zelenko, Zara ^a   Tennagels, Norbert ^b   Werner, Ulrich ^b   LeRoith, Derek ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INSULIN DERIVATIVE; INSULIN RECEPTOR; PROTEIN KINASE B; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; ANTIDIABETIC AGENT; DRUG DERIVATIVE; INSULIN, ASP(B10); INSULIN, ASP(B10)-; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST TUMOR; CONTROLLED STUDY; FEMALE; HYPERINSULINEMIA; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TUMOR GROWTH; ANIMAL; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; EXPERIMENTAL MAMMARY NEOPLASM; HUMAN; HYPERINSULINISM; METABOLIC SYNDROME X; METABOLISM; MOLECULARLY TARGETED THERAPY; OBESITY; PATHOLOGY; PHOSPHORYLATION; PROGNOSIS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TUMOR CELL CULTURE; TUMOR CELL LINE; ANALOGS AND DERIVATIVES; BREAST NEOPLASMS; COMPLICATION; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; TRENDS;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; HUMANS; HYPERINSULINISM; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MAMMARY NEOPLASMS, EXPERIMENTAL; METABOLIC SYNDROME X; MICE; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; OBESITY; PHOSPHORYLATION; PROGNOSIS; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84890191760     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0249     Document Type: Article

References (46)

1. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348:1625-1638
2. Campbell PT, Newton CC, Patel AV, Jacobs EJ, Gapstur SM. Diabetes and cause-specific mortality in a prospective cohort of one million U.S. adults. Diabetes Care 2012;35:1835-1844
3. Esposito K, Chiodini P, Colao A, Lenzi A, Giugliano D. Metabolic syndrome and risk of cancer: a systematic review and meta-analysis. Diabetes Care 2012;35:2402-2411
4. Lipscombe LL, Goodwin PJ, Zinman B, McLaughlin JR, Hux JE. Increased prevalence of prior breast cancer in women with newly diagnosed diabetes. Breast Cancer Res Treat 2006;98:303-309
5. Gunter MJ, Hoover DR, Yu H, et al. Insulin, insulin-like growth factor-I, and risk of breast cancer in postmenopausal women. J Natl Cancer Inst 2009; 101:48-60
6. Del Giudice ME, Fantus IG, Ezzat S, McKeown-Eyssen G, Page D, Goodwin PJ. Insulin and related factors in premenopausal breast cancer risk. Breast Cancer Res Treat 1998;47:111-120
7. Kabat GC, Kim M, Caan BJ, et al. Repeated measures of serum glucose and insulin in relation to postmenopausal breast cancer. Int J Cancer 2009;125: 2704-2710
8. Goodwin PJ, Ennis M, Pritchard KI, et al. Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 2002;20:42-51
9. Novosyadlyy R, Lann DE, Vijayakumar A, et al. Insulin-mediated acceleration of breast cancer development and progression in a nonobese model of type 2 diabetes. Cancer Res 2010;70:741-751
10. Rose DP, Vona-Davis L. The cellular and molecular mechanisms by which insulin influences breast cancer risk and progression. Endocr Relat Cancer 2012;19:R225-R241
11. Gonullu G, Ersoy C, Ersoy A, et al. Relation between insulin resistance and serum concentrations of IL-6 and TNF-alpha in overweight or obese women with early stage breast cancer. Cytokine 2005;31:264-269
12. Law JH, Habibi G, Hu K, et al. Phosphorylated insulin-like growth factor-i/ insulin receptor is present in all breast cancer subtypes and is related to poor survival. Cancer Res 2008;68:10238-10246
13. Fierz Y, Novosyadlyy R, Vijayakumar A, Yakar S, LeRoith D. Insulinsensitizing therapy attenuates type 2 diabetes-mediated mammary tumor progression. Diabetes 2010;59:686-693
14. Ferguson RD, Novosyadlyy R, Fierz Y, et al. Hyperinsulinemia enhances c-Myc-mediated mammary tumor development and advances metastatic progression to the lung in a mouse model of type 2 diabetes. Breast Cancer Res 2012;14:R8
15. Lu S, Lee WM, Archer MC. Insulin does not promote rat mammary carcinogenesis. Carcinogenesis 1998;19:699-702
16. Stammberger I, Bube A, Durchfeld-Meyer B, Donaubauer H, Troschau G. Evaluation of the carcinogenic potential of insulin glargine (LANTUS) in rats and mice. Int J Toxicol 2002;21:171-179
17. Dideriksen L, Jorgensen L, Drejer K. Carcinogenic effect of the human insulin analogue B10 Asp in female rats (Abstract). Diabetologia 1992;35: A3
18. Hansen BF, Kurtzhals P, Jensen AB, Dejgaard A, Russell-Jones D. Insulin X10 revisited: a super-mitogenic insulin analogue. Diabetologia 2011;54: 2226-2231
19. Sciacca L, Cassarino MF, Genua M, et al. Insulin analogues differently activate insulin receptor isoforms and post-receptor signalling. Diabetologia 2010;53:1743-1753
20. Milazzo G, Sciacca L, Papa V, Goldfine ID, Vigneri R. ASPB10 insulin induction of increased mitogenic responses and phenotypic changes in human breast epithelial cells: evidence for enhanced interactions with the insulin-like growth factor-I receptor. Mol Carcinog 1997;18:19-25
21. Oleksiewicz MB, Bonnesen C, Hegelund AC, et al. Comparison of intracellular signalling by insulin and the hypermitogenic AspB10 analogue in MCF-7 breast adenocarcinoma cells. J Appl Toxicol 2011;31:329-341
22. Kurtzhals P, Schäffer L, Sørensen A, et al. Correlations of receptor binding and metabolic and mitogenic potencies of insulin analogs designed for clinical use. Diabetes 2000;49:999-1005
23. Sommerfeld MR, Müller G, Tschank G, et al. In vitro metabolic and mitogenic signaling of insulin glargine and its metabolites. PLoS One 2010;5:e9540
24. Glendorf T, Knudsen L, Stidsen CE, et al. Systematic evaluation of the metabolic to mitogenic potency ratio for B10-substituted insulin analogues. PLoS One 2012;7:e29198
25. Hamel FG, Siford GL, Fawcett J, Chance RE, Frank BH, Duckworth WC. Differences in the cellular processing of AspB10 human insulin compared with human insulin and LysB28ProB29 human insulin. Metabolism 1999;48: 611-617
26. Fernández AM, Kim JK, Yakar S, et al. Functional inactivation of the IGF-I and insulin receptors in skeletal muscle causes type 2 diabetes. Genes Dev 2001;15:1926-1934
27. Pei XF, Noble MS, Davoli MA, et al. Explant-cell culture of primary mammary tumors from MMTV-c-Myc transgenic mice. In Vitro Cell Dev Biol Anim 2004;40:14-21
28. Borowsky AD, Namba R, Young LJ, et al. Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior. Clin Exp Metastasis 2005;22:47-59
29. Johansson GS, Arnqvist HJ. Insulin and IGF-I action on insulin receptors, IGF-I receptors, and hybrid insulin/IGF-I receptors in vascular smooth muscle cells. Am J Physiol Endocrinol Metab 2006;291:E1124-E1130
30. Pandini G, Vigneri R, Costantino A, et al. Insulin and insulin-like growth factor-I (IGF-I) receptor overexpression in breast cancers leads to insulin/ IGF-I hybrid receptor overexpression: evidence for a second mechanism of IGF-I signaling. Clin Cancer Res 1999;5:1935-1944
31. Osborne CK, Bolan G, Monaco ME, Lippman ME. Hormone responsive human breast cancer in long-term tissue culture: effect of insulin. Proc Natl Acad Sci USA 1976;73:4536-4540
32. 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;29:2517-2527
33. Zhang H, Pelzer AM, Kiang DT, Yee D. Down-regulation of type I insulinlike growth factor receptor increases sensitivity of breast cancer cells to insulin. Cancer Res 2007;67:391-397
34. Yee D. Insulin-like growth factor receptor inhibitors: baby or the bathwater? J Natl Cancer Inst 2012;104:975-981
35. Vølund A, Brange J, Drejer K, et al. In vitro and in vivo potency of insulin analogues designed for clinical use. Diabet Med 1991;8:839-847
36. Rakatzi I, Ramrath S, Ledwig D, et al. A novel insulin analog with unique properties: LysB3,GluB29 insulin induces prominent activation of insulin receptor substrate 2, but marginal phosphorylation of insulin receptor substrate 1. Diabetes 2003;52:2227-2238
37. Qiao D, Meyer K, Friedl A. Glypican-1 stimulates Skp2 autoinduction loop and G1/S transition in endothelial cells. J Biol Chem 2012;287:5898-5909
38. Velpula KK, Dasari VR, Tsung AJ, Dinh DH, Rao JS. Transcriptional repression of Mad-Max complex by human umbilical cord blood stem cells downregulates extracellular signal-regulated kinase in glioblastoma. Stem Cells Dev 2012;21:1779-1793
39. Marshall GM, Liu PY, Gherardi S, et al. SIRT1 promotes N-Myc oncogenesis through a positive feedback loop involving the effects of MKP3 and ERK on N-Myc protein stability. PLoS Genet 2011;7:e1002135
40. Lin CJ, Cencic R, Mills JR, Robert F, Pelletier J. c-Myc and eIF4F are components of a feedforward loop that links transcription and translation. Cancer Res 2008;68:5326-5334
41. Wu Y, Yakar S, Zhao L, Hennighausen L, LeRoith D. Circulating insulin-like growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res 2002;62:1030-1035
42. Frasca F, Pandini G, Scalia P, et al. Insulin receptor isoform A, a newly recognized, high-affinity insulin-like growth factor II receptor in fetal and cancer cells. Mol Cell Biol 1999;19:3278-3288
43. Sciacca L, Prisco M, Wu A, Belfiore A, Vigneri R, Baserga R. Signaling differences from the A and B isoforms of the insulin receptor (IR) in 32D cells in the presence or absence of IR substrate-1. Endocrinology 2003;144: 2650-2658
44. Kalla Singh S, Brito C, Tan QW, De León M, De León D. Differential expression and signaling activation of insulin receptor isoforms A and B: a link between breast cancer and diabetes. Growth Factors 2011;29:278-289
45. Leibiger B, Leibiger IB, Moede T, et al. Selective insulin signaling through A and B insulin receptors regulates transcription of insulin and glucokinase genes in pancreatic beta cells. Mol Cell 2001;7:559-570
46. Harrington SC, Weroha SJ, Reynolds C, Suman VJ, Lingle WL, Haluska P. Quantifying insulin receptor isoform expression in FFPE breast tumors. Growth Horm IGF Res 2012;22:108-115