IGF1R inhibition in mammary epithelia promotes canonical Wnt signaling and Wnt1-driven tumors

Cancer Research

Volumn 74, Issue 19, 2014, Pages 5668-5679

  Rota, Lauren M ^a   Albanito, Lidia ^a   Shin, Marcus E ^a   Goyeneche, Corey L ^a   Shushanov, Sain ^a   Gallagher, Emily J ^b   Le Roith, Derek ^b   Lazzarino, Deborah A ^a   Wood, Teresa L ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOMEDIN C RECEPTOR; WNT1 PROTEIN;

ANIMAL; ANTAGONISTS AND INHIBITORS; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; GENETICS; LUNG TUMOR; METABOLISM; MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SECONDARY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UDDER;

ANIMALS; FEMALE; LUNG NEOPLASMS; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; WNT1 PROTEIN;

EID: 84907482281     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0970     Document Type: Article

References (65)

1. Lehmann BD, Pietenpol JA. Identification and use of biomarkers in treatment strategies for triple-negative breast cancer subtypes. J Pathol 2014;232:142-50.
2. O'Toole SA, Beith JM, Millar EK, West R, McLean A, Cazet A, et al. Therapeutic targets in triple negative breast cancer. J Clin Pathol 2013;66:530-42.
3. Rakha EA, Reis-Filho JS, Ellis IO. Basal-like breast cancer: a critical review. J Clin Oncol 2008;26:2568-81.
4. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009;15:907-13.
5. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007;8:R76.
6. Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982;31:99-109.
7. Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammaryglandhyperplasia and adenocarcinomasin male and female mice. Cell 1988;55:619-25.
8. Khramtsov AI, Khramtsova GF, Tretiakova M, Huo D, Olopade OI, Goss KH. Wnt/βeta-catenin pathway activation is enriched in basallike breast cancers and predicts poor outcome. Am J Pathol 2010;176:2911-20.
9. Dey N, Barwick BG, Moreno CS, Ordanic-Kodani M, Chen Z, Oprea-Ilies G, et al. Wnt signaling in triple negative breast cancer is associated with metastasis. BMC Cancer 2013;13:537.
10. Litzenburger BC, Creighton CJ, Tsimelzon A, Chan BT, Hilsenbeck SG, Wang T, et al. High IGF-IR activity in triple-negative breast cancer cell lines and tumorgrafts correlates with sensitivity to anti-IGF-IR therapy. Clin Cancer Res 2011;17:2314-27.
11. Davison Z, de Blacquiere GE, Westley BR, May FE. Insulin-like growth factor-dependent proliferation and survival of triple-negative breast cancer cells: implications for therapy. Neoplasia 2011;13:504-15.
12. Zhang H, Yee D. The therapeutic potential of agents targeting the type I insulin-like growth factor receptor. Expert Opin Investig Drugs 2004;13:1569-77.
13. Le Roith D, Werner H, Neuenschwander S, Kalebic T, Helman LJ. The role of the insulin-like growth factor-I receptor in cancer. Ann N Y Acad Sci 1995;766:402-8.
14. Baserga R. The IGF-I receptor in cancer research. Exp Cell Res 1999;253:1-6.
15. Carboni JM, Lee AV, Hadsell DL, Rowley BR, Lee FY, Bol DK, et al. Tumor development by transgenic expression of a constitutively active insulin-like growth factor I receptor. Cancer Res 2005;65:3781-7.
16. Jones RA, Campbell CI, Gunther EJ, Chodosh LA, Petrik JJ, Khokha R, et al. Transgenic overexpression of IGF-IR disrupts mammary ductal morphogenesis and induces tumor formation. Oncogene 2007;26:1636-44.
17. Louvi A, Accili D, Efstratiadis A. Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev Biol 1997;189:33-48.
18. Frasca F, Pandini G, Scalia P, Sciacca L, Mineo R, Costantino A, 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;19:3278-88.
19. Sciacca L, Costantino A, Pandini G, Mineo R, Frasca F, Scalia P, et al. Insulin receptor activation by IGF-II in breast cancers: evidence for a new autocrine/paracrine mechanism. Oncogene 1999;18:2471-9.
20. Vella V, Pandini G, Sciacca L, Mineo R, Vigneri R, Pezzino V, et al. A novel autocrine loop involving IGF-II and the insulin receptor isoform-A stimulates growth of thyroid cancer. J Clin Endocrinol Metab 2002;87:245-54.
21. Huang J, Morehouse C, Streicher K, Higgs BW, Gao J, Czapiga M, et al. Altered expression of insulin receptor isoforms in breast cancer. PLoS ONE 2011;6:e26177.
22. Belfiore A, Frasca F, Pandini G, Sciacca L, Vigneri R. Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev 2009;30:586-623.
23. Law JH, Habibi G, Hu K, Masoudi H, Wang MY, Stratford AL, 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;68:10238-46.
24. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res 2001;10:545-53.
25. Fernandez AM, Dupont J, Farrar RP, Lee S, Stannard B, Le Roith D. Muscle-specific inactivation of the IGF-I receptor induces compensatory hyperplasia in skeletal muscle. J Clin Invest 2002;109:347-55.
26. Kato H, Faria TN, Stannard B, Roberts CT Jr, Le Roith D. Role of tyrosine kinase activity in signal transduction by the insulin-like growth factor-I (IGF-I) receptor. Characterization of kinase-deficient IGF-I receptors and the action of an IGF-I-mimetic antibody (alpha IR-3). J Biol Chem 1993;268:2655-61.
27. Smalley MJ, Kendrick H, Sheridan JM, Regan JL, Prater MD, Lindeman GJ, et al. Isolation of mouse mammary epithelial subpopulations: a comparison of leading methods. J Mammary Gland Biol Neoplasia 2012;17:91-7.
28. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-8.
29. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-7.
30. La Marca HL, Visbal AP, Creighton CJ, Liu H, Zhang Y, Behbod F, et al. CCAAT/enhancer binding protein beta regulates stem cell activity and specifies luminal cell fate in the mammary gland. Stem Cells 2010;28:535-44.
31. Rota LM, Lazzarino DA, Ziegler AN, Le Roith D, Wood TL. Determining mammosphere-forming potential: application of the limiting dilution analysis. J Mammary Gland Biol Neoplasia 2012;17:119-23.
32. Rowzee AM, Ludwig DL, Wood TL. Insulin-like growth factor type 1 receptor and insulin receptor isoform expression and signaling in mammary epithelial cells. Endocrinology 2009;150:3611-9.
33. Sun Z, Shushanov S, Le Roith D, Wood TL. Decreased IGF type 1 receptor signaling in mammary epithelium during pregnancy leads to reduced proliferation, alveolar differentiation, and expression of insulin receptor substrate (IRS)-1 and IRS-2. Endocrinology 2011;152:3233-45.
34. Miura M, Surmacz E, Burgaud JL, Baserga R. Different effects on mitogenesis and transformation of a mutation at tyrosine 1251 of the insulin-like growth factor I receptor. J Biol Chem 1995;270:22639-44.
35. Morcavallo A, Gaspari M, Pandini G, Palummo A, Cuda G, Larsen MR, et al. Research resource: new and diverse substrates for the insulin receptor isoform A revealed by quantitative proteomics after stimulation with IGF-II or insulin. Mol Endocrinol 2011;25:1456-68.
36. Sell C, Dumenil G, Deveaud C, Miura M, Coppola D, De Angelis T, et al. Effect of a null mutation of the insulin-like growth factor I receptor gene on growth and transformation of mouse embryo fibroblasts. Mol Cell Biol 1994;14:3604-12.
37. Li Y, Hively WP, Varmus HE. Use of MMTV-Wnt-1 transgenic mice for studying the genetic basis of breast cancer. Oncogene 2000;19:1002-9.
38. Pond AC, Herschkowitz JI, Schwertfeger KL, Welm B, Zhang Y, York B, et al. Fibroblast growth factor receptor signaling dramatically accelerates tumorigenesis and enhances oncoprotein translation in the mouse mammary tumor virus-Wnt-1 mouse model of breast cancer. Cancer Res 2010;70:4868-79.
39. Miyoshi K, Shillingford JM, Le Provost F, Gounari F, Bronson R, von Boehmer H, et al. Activation of beta-catenin signaling in differentiated mammary secretory cells induces transdifferentiation into epidermis and squamousmetaplasias. Proc Natl Acad Sci USA 2002;99:219-24.
40. Miyoshi K, Rosner A, Nozawa M, Byrd C, Morgan F, Landesman-Bollag E, et al. Activation of different Wnt/βeta-catenin signaling components in mammary epithelium induces transdifferentiation and the formation of pilar tumors. Oncogene 2002;21:5548-56.
41. Bu W, Chen J, Morrison GD, Huang S, Creighton CJ, Huang J, et al. Keratin 6a marks mammary bipotential progenitor cells that can give rise to a unique tumor model resembling human normal-like breast cancer. Oncogene 2011;30:4399-409.
42. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci U S A 2003;100:15853-8.
43. Macias H, Moran A, Samara Y, Moreno M, Compton JE, Harburg G, et al. SLIT/ROBO1 signaling suppresses mammary branching morphogenesis by limiting basal cell number. Dev Cell 2011;20:827-40.
44. Kaanta AS, Virtanen C, Selfors LM, Brugge JS, Neel BG. Evidence for a multipotent mammary progenitor with pregnancy-specific activity. Breast Cancer Res 2013;15:R65.
45. Liu BY, Kim YC, Leatherberry V, Cowin P, Alexander CM. Mammary gland development requires syndecan-1 to create a beta-catenin/TCF-responsive mammary epithelial subpopulation. Oncogene 2003;22:9243-53.
46. Kim S, Goel S, Alexander CM. Differentiation generates paracrine cell pairs that maintain basaloid mouse mammary tumors: proof of concept. PLoS ONE 2011;6:e19310.
47. Molyneux G, Geyer FC, Magnay FA, McCarthy A, Kendrick H, Natrajan R, et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010;7:403-17.
48. Bouras T, Pal B, Vaillant F, Harburg G, Asselin-Labat ML, Oakes SR, et al. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 2008;3:429-41.
49. Ayyanan A, Civenni G, Ciarloni L, Morel C, Mueller N, Lefort K, et al. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc Natl Acad Sci U S A 2006;103:3799-804.
50. Teissedre B, Pinderhughes A, Incassati A, Hatsell SJ, Hiremath M, Cowin P. MMTV-Wnt1 and -DeltaN89beta-catenin induce canonical signaling in distinct progenitors and differentially activate Hedgehog signaling within mammary tumors. PLoS ONE 2009;4:e4537.
51. Alexander CM, Goel S, Fakhraldeen SA, Kim S. Wnt signaling in mammary glands: plastic cell fates and combinatorial signaling. Cold Spring Harb Perspect Biol 2012;4:a008037.
52. Chakrabarti R, Wei Y, Romano RA, De Coste C, Kang Y, Sinha S. Elf5 regulates mammary gland stem/progenitor cell fate by influencing notch signaling. Stem Cells 2012;30:1496-508.
53. Chakrabarti R, Hwang J, Andres Blanco M, Wei Y, Lukacisin M, Romano RA, et al. Elf5 inhibits the epithelial-mesenchymal transition in mammary gland development and breast cancer metastasis by transcriptionally repressing Snail2. Nat Cell Biol 2012;14:1212-22.
54. Katoh M. Network of WNT and other regulatory signaling cascades in pluripotent stem cells and cancer stem cells. Curr Pharm Biotechnol 2011;12:160-70.
55. Kim S, Alexander CM. Tumorsphere assay provides more accurate prediction of in vivo responses to chemotherapeutics. Biotechnol Lett 2013.
56. Liu JC, Deng T, Lehal RS, Kim J, Zacksenhaus E. Identification of tumorsphere- and tumor-initiating cells in HER2/Neu-induced mammary tumors. Cancer Res 2007;67:8671-81.
57. Shaw FL, Harrison H, Spence K, Ablett MP, Simoes BM, Farnie G, et al. A detailed mammosphere assay protocol for the quantification of breast stem cell activity. J Mammary Gland Biol Neoplasia 2012;17:111-7.
58. 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.
59. Dunlap SM, Chiao LJ, Nogueira L, Usary J, Perou CM, Varticovski L, et al. Dietary energy balance modulates epithelial-to-mesenchymal transition and tumor progression in murine claudin-low and basal-like mammary tumor models. Cancer Prev Res 2012;5:930-42.
60. Andres SF, Simmons JG, Mah AT, Santoro MA, Van Landeghem L, Lund PK. Insulin receptor isoform switching in intestinal stem cells, progenitors, differentiated lineages and tumors: evidence that IR-B limits proliferation. J Cell Sci 2013;126:5645-56.
61. Schnarr B, Strunz K, Ohsam J, Benner A, Wacker J, Mayer D. Downregulation of insulin-like growth factor-I receptor and insulin receptor substrate-1 expression in advanced human breast cancer. Int J Cancer 2000;89:506-13.
62. Heni M, Hennenlotter J, Scharpf M, Lutz SZ, Schwentner C, Todenhofer T, et al. Insulin receptor isoforms A and B as well as insulin receptor substrates-1 and -2 are differentially expressed in prostate cancer. PLoS ONE 2012;7:e50953.
63. Brisken C, Ayyannan A, Nguyen C, Heineman A, Reinhardt F, Tan J, et al. IGF-2 is a mediator of prolactin-induced morphogenesis in the breast. Dev Cell 2002;3:877-87.
64. Pandini G, Conte E, Medico E, Sciacca L, Vigneri R, Belfiore A. IGF-II binding to insulin receptor isoform A induces a partially different gene expression profile from insulin binding. Ann N Y Acad Sci 2004;1028:450-6.
65. 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.