Growth hormone potentiates 17β-estradiol-dependent breast cancer cell proliferation independently of IGF-I receptor signaling

Endocrinology

Volumn 154, Issue 9, 2013, Pages 3219-3227

  Felice, Dana L ^a   El Shennawy, Lamiaa ^a   Zhao, Shuangping ^a   Lantvit, Daniel L ^a   Shen, Qi ^a   Unterman, Terry G ^a   Swanson, Steven M ^a   Frasor, Jonna ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; GROWTH HORMONE; GROWTH HORMONE RECEPTOR; JANUS KINASE 2; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ARTICLE; BREAST CANCER; CANCER CELL; CELL PROLIFERATION; EARLY RESPONSE GENE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; UPREGULATION;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; ESTRADIOL; FEMALE; HUMAN GROWTH HORMONE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; JANUS KINASE 2; MAP KINASE SIGNALING SYSTEM; NEOPLASM PROTEINS; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, IGF TYPE 1; RECEPTORS, SOMATOTROPIN; RECOMBINANT PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84883156145     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2208     Document Type: Article

References (65)

1. Kahlert S, Nuedling S, van Eickels M, Vetter H, Meyer R, Grohe C. Estrogen receptor α rapidly activates the IGF-1 receptor pathway. J Biol Chem. 2000;275:18447-18453.
2. 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;152:39-47.
3. Song RX, Barnes CJ, Zhang Z, Bao Y, Kumar R, Santen RJ. The role of Shc and insulin-like growth factor 1 receptor in mediating the translocation of estrogen receptor α to the plasma membrane. Proc Natl Acad Sci USA. 2004;101:2076-2081.
4. Cullen KJ, Yee D, Bates SE, et al. Regulation of human breast cancer by secreted growth factors. Acta Oncol. 1989;28:835-839.
5. Lee AV, Jackson JG, Gooch JL, 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;13:787-796.
6. Yee D, Lee AV. Cross talk between the insulin-like growth factors and estrogens in breast cancer. J Mammary Gland Biol Neoplasia. 2000;5:107-115.
7. 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;275:12565-12571.
8. Knowlden JM, Hutcheson IR, Barrow D, Gee JM, Nicholson RI. Insulin-like growth factor-I receptor signaling in tamoxifen-resistant breast cancer: a supporting role to the epidermal growth factor receptor. Endocrinology. 2005;146:4609-4618.
9. Massarweh S, Osborne CK, Creighton CJ, 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;68:826-833.
10. Zhang Y, Moerkens M, Ramaiahgari S, et al. Elevated insulin-like growth factor 1 receptor signaling induces antiestrogen resistance through the MAPK/ERK and PI3K/Akt signaling routes. Breast Cancer Res. 2011;13:R52.
11. Creighton CJ, Casa A, Lazard Z, et al. Insulin-like growth factor-I activates gene transcription programs strongly associated with poor breast cancer prognosis. J Clin Oncol. 2008;26:4078-4085.
12. Chakraborty AK, Welsh A, Digiovanna MP. Co-targeting the insulin-like growth factor I receptor enhances growth-inhibitory and pro-apoptotic effects of anti-estrogens in human breast cancer cell lines. Breast Cancer Res Treat. 2010;120:327-335.
13. Sachdev D, Yee D. Disrupting insulin-like growth factor signaling as a potential cancer therapy. Mol Cancer Ther. 2007;6:1-12.
14. Lee AV, Yee D. Targeting IGF-1R: at a crossroad. Oncology (Williston Park). 2011;25:535-536; discussion 551.
15. Yee D. Insulin-like growth factor receptor inhibitors: baby or the bathwater? J Natl Cancer Inst. 2012;104:975-981.
16. Kaufman P, Ferrero J, Bourgeois H, et al. Abstract S1-4 : 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. Cancer Res. 2010;70:S1-S4.
17. Fagan DH, Uselman RR, Sachdev D, Yee D. Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor: implications for breast cancer treatment. Cancer Res. 2012;72:3372-3380.
18. Weroha SJ, Haluska P. IGF-1 receptor inhibitors in clinical trials - early lessons. J Mammary Gland Biol Neoplasia. 2008;13:471-483.
19. Tolcher AW, Sarantopoulos J, Patnaik A, 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;27:5800-5807.
20. BerelowitzM,SzaboM,Frohman LA, Firestone S, Chu L, Hintz RL. Somatomedin-C mediates growth hormone negative feedback by effects on both the hypothalamus and the pituitary. Science. 1981; 212:1279-1281.
21. Guevara-Aguirre J, Balasubramanian P, Guevara-Aguirre M, et al. Growth hormone receptor deficiency is associated with a major reduction in pro-aging signaling, cancer, and diabetes in humans. Sci Transl Med. 2011;3:70ra13.
22. Menashe I, Maeder D, Garcia-Closas M, et al. Pathway analysis of breast cancer genome-wide association study highlights three pathways and one canonical signaling cascade. Cancer Res. 2010;70: 4453-4459.
23. Gebre-Medhin M, Kindblom LG, Wennbo H, Tornell J, Meis-Kindblom JM. Growth hormone receptor is expressed in human breast cancer. Am J Pathol. 2001;158:1217-1222.
24. Wu ZS, Yang K, Wan Y, et al. Tumor expression of human growth hormone and human prolactin predict a worse survival outcome in patients with mammary or endometrial carcinoma. J Clin Endocrinol Metab. 2011;96:E1619-E1629.
25. Kleinberg DL, Ruan W. IGF-I, GH, and sex steroid effects in normal mammary gland development. J Mammary Gland Biol Neoplasia. 2008;13:353-360.
26. Kleinberg DL, Wood TL, Furth PA, Lee AV. Growth hormone and insulin-like growth factor-I in the transition from normal mammary development to preneoplastic mammary lesions. Endocr Rev. 2009; 30:51-74.
27. Lin X, Yu Y, Zhao H, Zhang Y, Manela J, Tonetti DA. Overex-pression of PKCα is required to impart estradiol inhibition and tamoxifen-resistance in a T47D human breast cancer tumor model. Carcinogenesis. 2006;27:1538-1546.
28. Felice D, Sun J, Liu R. A modified methylene blue assay for accurate cell counting. J Funct Foods. 2009;1:109-118.
29. Labarca C, Paigen K. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980;102:344-352.
30. κB in breast cancer. Cancer Res. 2009; 69:8918-8925.
31. Lisztwan J, Pornon A, Chen B, Chen S, Evans DB. The aromatase inhibitor letrozole and inhibitors of insulin-like growth factor I receptor synergistically induce apoptosis in in vitro models of estrogen-dependent breast cancer. Breast Cancer Res. 2008;10:R56.
32. Huang Y, Kim SO, Jiang J, Frank SJ. Growth hormone-induced phosphorylation of epidermal growth factor (EGF) receptor in 3T3-F442A cells. Modulation of EGF-induced trafficking and signaling. J Biol Chem. 2003;278:18902-18913.
33. Yamauchi T, Ueki K, Tamemoto H, et al Tyrosine phosphorylation of the EGF receptor by the kinase Jak2 is induced by growth hormone. Nature. 1997;390:91-96.
34. Yamauchi T, Ueki K, Tobe K, et al. Growth hormone-induced tyrosine phosphorylation of EGF receptor as an essential element leading to MAP kinase activation and gene expression. Endocr J. 1998; 45(suppl):S27-S31.
35. Jin H, Lanning NJ, Carter-Su C. JAK2, but not Src family kinases, is required for STAT, ERK, and Akt signaling in response to growth hormone in preadipocytes and hepatoma cells. Mol Endocrinol. 2008;22:1825-1841.
36. Alvarez JV, Frank DA. Genome-wide analysis of STAT target genes: elucidating the mechanism of STAT-mediated oncogenesis. Cancer Biol Ther. 2004;3:1045-1050.
37. Fox EM, Bernaciak TM, Wen J, Weaver AM, Shupnik MA, Silva CM. Signal transducer and activator of transcription 5b, c-Src, and epidermal growth factor receptor signaling play integral roles in estrogen-stimulated proliferation of estrogen receptor-positive breast cancer cells. Mol Endocrinol. 2008;22:1781-1796.
38. Cui TX, Lin G, LaPensee CR, et al. C/EBPβmediates growth hormone-regulated expression of multiple target genes. Mol Endocrinol. 2011;25:681-693.
39. Avraham R, Sas-Chen A, Manor O, et al. EGF decreases the abundance of microRNAs that restrain oncogenic transcription factors. Sci Signal. 2010;3:ra43.
40. Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev Biol. 2001;229:141-162.
41. Vijayakumar A, Novosyadlyy R, Wu Y, Yakar S, LeRoith D. Biological effects of growth hormone on carbohydrate and lipid metabolism. Growth Horm IGF Res. 2010;20:1-7.
42. DiGirolamo DJ, Mukherjee A, Fulzele K, et al. Mode of growth hormone action in osteoblasts. J Biol Chem. 2007;282:31666-31674.
43. Huang Y, Kim SO, Yang N, Jiang J, Frank SJ. Physical and functional interaction of growth hormone and insulin-like growth factor-I signaling elements. Mol Endocrinol. 2004;18:1471-1485.
44. Gan Y, Zhang Y, Digirolamo DJ, et al. Deletion of IGF-I receptor (IGF-IR) in primary osteoblasts reduces GH-induced STAT5 signaling. Mol Endocrinol. 2010;24:644-656.
45. Ma F, Wei Z, Shi C, et al. Signaling cross talk between growth hormone (GH) and insulin-like growth factor-I (IGF-I) in pancreatic islet β-cells. Mol Endocrinol. 2011;25:2119-2133.
46. Hughes JP, Friesen HG. The nature and regulation of the receptors for pituitary growth hormone. Annu Rev Physiol. 1985;47:469-482.
47. Cunningham BC, Bass S, Fuh G, Wells JA. Zinc mediation of the binding of human growth hormone to the human prolactin receptor. Science. 1990;250:1709-1712.
48. Somers W, Ultsch M, De Vos AM, Kossiakoff AA. The X-ray structure of a growth hormone-prolactin receptor complex. Nature. 1994;372:478-481.
49. XuJ, Zhang Y, Berry PA, et al. Growth hormone signaling in human T47D breast cancer cells: potential role for a growth hormone receptor-prolactin receptor complex. Mol Endocrinol. 2011;25:597-610.
50. Xu J, Sun D, Jiang J, et al. The role of prolactin receptor in GH signaling in breast cancer cells. Mol Endocrinol. 2013;27(2):266-279.
51. Rasmussen LM, Frederiksen KS, Din N, et al. Prolactin and oestrogen synergistically regulate gene expression and proliferation of breast cancer cells. Endocr Relat Cancer. 2010;17:809-822.
52. Li X, Huang Y, Jiang J, Frank SJ. Synergy in ERK activation by cytokine receptors and tyrosine kinase growth factor receptors. Cell Signal. 2011;23:417-424.
53. Huo JS, McEachin RC, Cui TX, et al. Profiles of growth hormone (GH)-regulated genes reveal time-dependent responses and identify a mechanism for regulation of activating transcription factor 3 by GH. J Biol Chem. 2006;281:4132-4141.
54. Gong TW, Meyer DJ, Liao J, et al. Regulation of glucose transport and c-fos and egr-1 expression in cells with mutated or endogenous growth hormone receptors. Endocrinology. 1998;139:1863-1871.
55. Hodge C, Liao J, Stofega M, Guan K, Carter-Su C, Schwartz J. Growth hormone stimulates phosphorylation and activation of elk-1 and expression of c-fos, egr-1, and junB through activation of extracellular signal-regulated kinases 1 and 2. J Biol Chem. 1998; 273:31327-31336.
56. Cui TX, Piwien-Pilipuk G, Huo JS, Kaplani J, Kwok R, Schwartz J. Endogenous CCAAT/enhancer binding proteinβ and p300 are both regulated by growth hormone to mediate transcriptional activation. Mol Endocrinol. 2005;19:2175-2186.
57. Cui TX, Kwok R, Schwartz J. Cooperative regulation of endogenous cAMP-response element binding protein and CCAAT/enhancer-binding protein β in GH-stimulated c-fos expression. J Endocrinol. 2008;196:89-100.
58. Milde-Langosch K. The Fos family of transcription factors and their role in tumourigenesis. Eur J Cancer. 2005;41:2449-2461.
59. Yin X, Dewille JW, Hai T. A potential dichotomous role of ATF3, an adaptive-response gene, in cancer development. Oncogene. 2008;27:2118-2127.
60. Wang A, Arantes S, Yan L, et al. The transcription factor ATF3 acts as an oncogene in mouse mammary tumorigenesis. BMC Cancer. 2008;8:268.
61. Madden SL, Rauscher FJ 3rd. Positive and negative regulation of transcription and cell growth mediated by the EGR family of zinc-finger gene products. Ann NY Acad Sci. 1993;684: 75-84.
62. Gashler A, Sukhatme VP. Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol. 1995;50:191-224.
63. Mitchell A, Dass CR, Sun LQ, Khachigian LM. Inhibition of human breast carcinoma proliferation, migration, chemoinvasion and solid tumour growth by DNAzymes targeting the zinc finger transcription factor EGR-1. Nucleic Acids Res. 2004;32:3065-3069.
64. DuBois RN, McLane MW, Ryder K, Lau LF, Nathans D. A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem. 1990;265:19185-19191.
65. Carballo E, Lai WS, Blackshear PJ. Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science. 1998;281:1001-1005.