Developmental stage determines estrogen receptor alpha expression and non-genomic mechanisms that control IGF-1 signaling and mammary proliferation in mice

Journal of Clinical Investigation

Volumn 122, Issue 1, 2012, Pages 192-204

  Tian, Jie ^a   Berton, Thomas R ^a   Shirley, Stephanie H ^a,b   Lambertz, Isabel ^a   Gimenez Conti, Irma B ^a,b   DiGiovanni, John ^a,b,d   Korach, Kenneth S ^c   Conti, Claudio J ^a,b   Fuchs Young, Robin ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; ESTROGEN RECEPTOR ALPHA; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER RISK; CARCINOGENESIS; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; POSTMENOPAUSE; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE REACTION; TRANSGENIC MOUSE;

ANIMALS; BREAST NEOPLASMS; CATTLE; CELL PROLIFERATION; CYCLIN D1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-LIKE GROWTH FACTOR I; MAMMARY GLANDS, ANIMAL; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; PARACRINE COMMUNICATION; PROTO-ONCOGENE PROTEINS C-RAF; SEXUAL MATURATION; SIGNAL TRANSDUCTION;

EID: 84855417073     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI42204     Document Type: Article

References (70)

1. Yee D. The insulin-like growth factors and breast cancer - revisited. Breast Cancer Res Treat. 1998;47(3):197-199. (Pubitemid 28059816)
2. Yu H, Rohan T. Role of the insulin-like growth factor family in cancer development and progression. J Natl Cancer Inst. 2000;92(18):1472-1489.
3. Valentinis B, Baserga R. IGF-I receptor signalling in transformation and differentiation. Mol Pathol. 2001;54(3):133-137. (Pubitemid 32539602)
4. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer. 2002;2(7):489-501. (Pubitemid 37328931)
5. White MF, Yenush L. The IRS-signaling system: a network of docking proteins that mediate insulin and cytokine action. Curr Top Microbiol Immunol. 1998;228:179-208.
6. White MF. The IRS-signalling system: a network of docking proteins that mediate insulin action. Mol Cell Biochem. 1998;182(1-2):3-11. (Pubitemid 28181643)
7. Goalstone ML, Draznin B. What does insulin do to Ras? Cell Signal. 1998;10(5):297-301. (Pubitemid 28286785)
8. Hay N. The Akt-mTOR tango and its relevance to cancer. Cancer Cell. 2005;8(3):179-183. (Pubitemid 41317589)
9. Luo J, Manning BD, Cantley LC. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell. 2003;4(4):257-262. (Pubitemid 37329790)
10. Vanhaesebroeck B, Alessi DR. The PI3K-PDK1 connection: more than just a road to PKB. Biochem J. 2000;346(pt 3):561-576. (Pubitemid 30171014)
11. Creighton CJ, et al. Insulin-like growth factor-I activates gene transcription programs strongly associated with poor breast cancer prognosis. J Clin Oncol. 2008;26(25):4078-4085.
12. Mu L, et al. Peptide concentrations and mRNA expression of IGF-I, IGF-II and IGFBP-3 in breast cancer and their associations with disease characteristics. Breast Cancer Res Treat. 2009;115(1):151-162.
13. Shin A, Ren Z, Shu XO, Cai Q, Gao YT, Zheng W. Expression patterns of insulin-like growth factor 1 (IGF-I) and its receptor in mammary tissues and their associations with breast cancer survival. Breast Cancer Res Treat. 2007;105(1):55-61. (Pubitemid 47282744)
14. de Ostrovich KK, et al. Paracrine overexpression of insulin-like growth factor-1 enhances mammary tumorigenesis in vivo. Am J Pathol. 2008;173(3):824-834.
15. Hadsell DL, Greenberg NM, Fligger JM, Baumrucker CR, Rosen JM. Targeted expression of des(1-3) human insulin-like growth factor I in transgenic mice influences mammary gland development and IGF-binding protein expression. Endocrinology. 1996;137(1):321-330. (Pubitemid 26005007)
16. Weber MS, Boyle PL, Corl BA, Wong EA, Gwazdauskas FC, Akers RM. Expression of ovine insulin-like growth factor-1 (IGF-1) stimulates alveolar bud development in mammary glands of transgenic mice. Endocrine. 1998;8(3):251-259. (Pubitemid 28350815)
17. DiGiovanni J, 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(6):1561-1570. (Pubitemid 30183426)
18. Dupont J, Karas M, LeRoith D. The potentiation of estrogen on insulin-like growth factor I action in MCF-7 human breast cancer cells includes cell cycle components. J Biol Chem. 2000;275(46):35893-35901.
19. Sisci D, Surmacz E. Crosstalk between IGF signaling and steroid hormone receptors in breast cancer. Curr Pharm Des. 2007;13(7):705-717. (Pubitemid 46510746)
20. 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(8):957-972. (Pubitemid 27199876)
21. Surmacz E, Bartucci M. Role of estrogen receptor alpha in modulating IGF-I receptor signaling and function in breast cancer. J Exp Clin Cancer Res. 2004;23(3):385-394. (Pubitemid 39490622)
22. Lee AV, Weng CN, Jackson JG, Yee D. Activation of estrogen receptor-mediated gene transcription by IGF-I in human breast cancer cells. J Endocrinol. 1997;152(1):39-47. (Pubitemid 27026386)
23. Kahlert S, Nuedling S, van Eickels M, Vetter H, Meyer R, Grohe C. Estrogen receptor alpha rapidly activates the IGF-1 receptor pathway. J Biol Chem. 2000;275(24):18447-18453. (Pubitemid 30414803)
24. Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW. Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci U S A. 1999;96(5):1858-1862. (Pubitemid 29117832)
25. Chu I, et al. Src promotes estrogen-dependent estrogen receptor alpha proteolysis in human breast cancer. J Clin Invest. 2007;117(8):2205-2215. (Pubitemid 47219565)
26. Jalkanen M, Nguyen H, Rapraeger A, Kurn N, Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells: localization on the cell surface with a monoclonal antibody. J Cell Biol. 1985;101(3):976-984. (Pubitemid 16258224)
27. Sherr CJ. D-type cyclins. Trends Biochem Sci. 1995;20(5):187-190.
28. Rodriguez-Puebla ML, LaCava M, Conti CJ. Cyclin D1 overexpression in mouse epidermis increases cyclin-dependent kinase activity and cell proliferation in vivo but does not affect skin tumor development. Cell Growth Differ. 1999;10(7):467-472. (Pubitemid 29344688)
29. Morelli C, Garofalo C, Bartucci M, Surmacz E. Estrogen receptor-alpha regulates the degradation of insulin receptor substrates 1 and 2 in breast cancer cells. Oncogene. 2003;22(26):4007-4016. (Pubitemid 36819641)
30. Zimmermann S, Moelling K. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science. 1999;286(5445):1741-1744. (Pubitemid 129515882)
31. Rommel C, et al. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science. 1999;286(5445):1738-1741. (Pubitemid 129515881)
32. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A. 1993;90(23):11162-11166. (Pubitemid 23354389)
33. Bocchinfuso WP, et al. Induction of mammary gland development in estrogen receptor-alpha knockout mice. Endocrinology. 2000;141(8):2982-2994. (Pubitemid 32250463)
34. Jackson JG, White MF, Yee D. Insulin receptor substrate-1 is the predominant signaling molecule activated by insulin-like growth factor-I, insulin, and interleukin-4 in estrogen receptor-positive human breast cancer cells. J Biol Chem. 1998;273(16):9994-10003. (Pubitemid 28183101)
35. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem. 1997;272(10):6653-6662. (Pubitemid 27118151)
36. Toker A. Protein kinases as mediators of phosphoinositide 3-kinase signaling. Mol Pharmacol. 2000;57(4):652-658. (Pubitemid 30183703)
37. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsichlis PN, Rosen N. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem. 1998;273(45):29864-29872. (Pubitemid 28510001)
38. Diehl JA. Cycling to cancer with cyclin D1. Cancer Biol Ther. 2002;1(3):226-231.
39. Dufourny B, et al. Mitogenic signaling of insulin-like growth factor I in MCF-7 human breast cancer cells requires phosphatidylinositol 3-kinase and is independent of mitogen-activated protein kinase. J Biol Chem. 1997;272(49):31163-31171. (Pubitemid 27527567)
40. Dupont J, Le Roith D. Insulin-like growth factor 1 and oestradiol promote cell proliferation of MCF-7 breast cancer cells: new insights into their synergistic effects. Mol Pathol. 2001;54(3):149-154. (Pubitemid 32539605)
41. Yee D, Lee AV. Crosstalk between the insulin-like growth factors and estrogens in breast cancer. J Mammary Gland Biol Neoplasia. 2000;5(1):107-115.
42. Foster JS, Henley DC, Ahamed S, Wimalasena J. Estrogens and cell-cycle regulation in breast cancer. Trends Endocrinol Metab. 2001;12(7):320-327. (Pubitemid 33714224)
43. Hamelers IH, van Schaik RF, Sipkema J, Sussenbach JS, Steenbergh PH. Insulin-like growth factor I triggers nuclear accumulation of cyclin D1 in MCF-7S breast cancer cells. J Biol Chem. 2002;277(49):47645-47652. (Pubitemid 36159286)
44. Kawashima K, et al. The estrogen-occupied estrogen receptor functions as a negative regulator to inhibit cell proliferation induced by insulin/IGF-1: a cell context-specific antimitogenic action of estradiol on rat lactotrophs in culture. Endocrinology. 2002;143(7):2750-2758. (Pubitemid 34701339)
45. Cascio S, Bartella V, Garofalo C, Russo A, Giordano A, Surmacz E. Insulin-like growth factor 1 differentially regulates estrogen receptor-dependent transcription at estrogen response element and AP-1 sites in breast cancer cells. J Biol Chem. 2007;282(6):3498-3506. (Pubitemid 47084426)
46. Beretta L, Gingras AC, Svitkin YV, Hall MN, Sonenberg N. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 1996;15(3):658-664. (Pubitemid 26044579)
47. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell. 2006;124(3):471-484. (Pubitemid 43199434)
48. Sasaoka T, Rose DW, Jhun BH, Saltiel AR, Draznin B, Olefsky JM. Evidence for a functional role of Shc proteins in mitogenic signaling induced by insulin, insulin-like growth factor-1, and epidermal growth factor. J Biol Chem. 1994;269(18):13689-13694. (Pubitemid 24206151)
49. Skolnik EY, et al. The SH2/SH3 domain-containing protein GRB2 interacts with tyrosine-phosphorylated IRS1 and Shc: implications for insulin control of ras signalling. EMBO J. 1993;12(5):1929-1936. (Pubitemid 23157709)
50. Bol DK, Kiguchi K, Gimenez-Conti I, Rupp T, DiGiovanni J. Overexpression of insulin-like growth factor-1 induces hyperplasia, dermal abnormalities, and spontaneous tumor formation in transgenic mice. Oncogene. 1997;14(14):1725-1734. (Pubitemid 27198945)
51. Russo IH, Russo J. Mammary gland neoplasia in long-term rodent studies. Environ Health Perspect. 1996;104(9):938-967. (Pubitemid 26372400)
52. Tian J, et al. Transgenic insulin-like growth factor-1 stimulates activation of COX-2 signaling in mammary glands [published online ahead of print October 17, 2011]. Mol Carcinog. doi:10.1002/mc.20868.
53. Donovan EA, Kummar S. Role of insulin-like growth factor-1R system in colorectal carcinogenesis. Crit Rev Oncol Hematol. 2008;66(2):91-98. (Pubitemid 351446110)
54. Sugumar A, Liu YC, Xia Q, Koh YS, Matsuo K. Insulin-like growth factor (IGF)-I and IGF-binding protein 3 and the risk of premenopausal breast cancer: a meta-analysis of literature. Int J Cancer. 2004;111(2):293-297. (Pubitemid 38924709)
55. Schernhammer ES, Holly JM, Hunter DJ, Pollak MN, Hankinson SE. Insulin-like growth factor-I, its binding proteins (IGFBP-1 and IGFBP-3), and growth hormone and breast cancer risk in The Nurses Health Study II. Endocr Relat Cancer. 2006;13(2):583-592. (Pubitemid 43886678)
56. Lund MJ, et al. Race and triple negative threats to breast cancer survival: a population-based study in Atlanta, GA. Breast Cancer Res Treat. 2009;113(2):357-370.
57. Carey LA, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295(21):2492-2502. (Pubitemid 43854964)
58. Aloia JF, Mikhail M, Pagan CD, Arunachalam A, Yeh JK, Flaster E. Biochemical and hormonal variables in black and white women matched for age and weight. J Lab Clin Med. 1998;132(5):383-389. (Pubitemid 28552096)
59. D'Aloisio AA, et al. IGF-I and IGFBP-3 polymorphisms in relation to circulating levels among African American and Caucasian women. Cancer Epidemiol Biomarkers Prev. 2009;18(3):954-966.
60. Yanovski JA, Sovik KN, Nguyen TT, Sebring NG. Insulin-like growth factors and bone mineral density in African American and White girls. J Pediatr. 2000;137(6):826-832.
61. Wong WW, Copeland KC, Hergenroeder AC, Hill RB, Stuff JE, Ellis KJ. Serum concentrations of insulin, insulin-like growth factor-I and insulin-like growth factor binding proteins are different between white and African American girls. J Pediatr. 1999;135(3):296-300. (Pubitemid 30180500)
62. Baglietto L, English DR, Hopper JL, Morris HA, Tilley WD, Giles GG. Circulating insulin-like growth factor-I and binding protein-3 and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev. 2007;16(4):763-768. (Pubitemid 46650579)
63. Rinaldi S, et al. IGF-I, IGFBP-3 and breast cancer risk in women: The European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr Relat Cancer. 2006;13(2):593-605. (Pubitemid 43886679)
64. Ahn J, et al. Adiposity, adult weight change, and postmenopausal breast cancer risk. Arch Intern Med. 2007;167(19):2091-2102. (Pubitemid 350036709)
65. Li CI, Malone KE, Daling JR. Interactions between body mass index and hormone therapy and postmenopausal breast cancer risk (United States). Cancer Causes Control. 2006;17(5):695-703. (Pubitemid 43668328)
66. Morimoto LM, et al. Obesity, body size, and risk of postmenopausal breast cancer: the Women's Health Initiative (United States). Cancer Causes Control. 2002;13(8):741-751. (Pubitemid 35204050)
67. Abul-Hajj YJ. Relationship between estrogen receptors, 17 beta-hydroxysteroid dehydrogenase and estrogen content in human breast cancer. Steroids. 1979;34(2):217-225.
68. Moseson M. Estrogen receptors and response to surgical adjuvant chemotherapy for breast cancer - hypothesized relationship to tumor stroma. Oncology. 1982;39(2):83-87. (Pubitemid 12170233)
69. Cheng D, Cote J, Shaaban S, Bedford MT. The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol Cell. 2007;25(1):71-83. (Pubitemid 46049059)
70. Shirley SH, et al. Transcriptional regulation of estrogen receptor-alpha by p53 in human breast cancer cells. Cancer Res. 2009;69(8):3405-3414.