PHLDA1 expression is controlled by an estrogen receptor-NFκB-miR-181 regulatory loop and is essential for formation of ER+ mammospheres

Oncogene

Volumn 34, Issue 18, 2015, Pages 2309-2316

  Kastrati, I ^a   Canestrari, E ^a   Frasor, J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MIRN181 MICRORNA, HUMAN; PHLDA1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

BREAST TUMOR; CANCER STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; MICRORNAS; NEOPLASTIC STEM CELLS; NF-KAPPA B; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84939890767     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.180     Document Type: Article

References (50)

1. Zhou Y, Eppenberger-Castori S, Marx C, Yau C, Scott GK, Eppenberger U et al. Activation of nuclear factor-kappaB (NFkappaB) identifies a high-risk subset of hormone-dependent breast cancers. Int J Biochem Cell Biol 2005; 37: 1130-1144.
2. Zhou Y, Yau C, Gray JW, Chew K, Dairkee SH, Moore DH et al. Enhanced NF kappa B and AP-1 transcriptional activity associated with antiestrogen resistant breast cancer. BMC Cancer 2007; 7: 59.
3. Jones RL, Rojo F, A'Hern R, Villena N, Salter J, Corominas JM et al. Nuclear NF-kappaB/p65 expression and response to neoadjuvant chemotherapy in breast cancer. J Clin Pathol 2011; 64: 130-135.
4. deGraffenried LA, Chandrasekar B, Friedrichs WE, Donzis E, Silva J, Hidalgo M et al. NF-kappa B inhibition markedly enhances sensitivity of resistant breast cancer tumor cells to tamoxifen. Ann Oncol 2004; 15: 885-890.
5. Riggins RB, Zwart A, Nehra R, Clarke R. The nuclear factor kappa B inhibitor parthenolide restores ICI 182,780 (Faslodex; fulvestrant)-induced apoptosis in antiestrogen-resistant breast cancer cells. Mol Cancer Ther 2005; 4: 33-41.
6. Frasor J, Weaver A, Pradhan M, Dai Y, Miller LD, Lin CY et al. Positive cross-talk between estrogen receptor and NF-kappaB in breast cancer. Cancer Res 2009; 69: 8918-8925.
7. Stanculescu A, Bembinster LA, Borgen K, Bergamaschi A, Wiley E, Frasor J. Estrogen promotes breast cancer cell survival in an inhibitor of apoptosis (IAP)-dependent manner. Horm Cancer 2010; 1: 127-135.
8. Toyoshima Y, Karas M, Yakar S, Dupont J, Lee H, LeRoith D. TDAG51 mediates the effects of insulin-like growth factor I (IGF-I) on cell survival. J Biol Chem 2004; 279: 25898-25904.
9. Sakthianandeswaren A, Christie M, D'Andreti C, Tsui C, Jorissen RN, Li S et al. PHLDA1 expression marks the putative epithelial stem cells and contributes to intestinal tumorigenesis. Cancer Res 2011; 71: 3709-3719.
10. Van Laere S, Limame R, Van Marck EA, Vermeulen PB, Dirix LY. Is there a role for mammary stem cells in inflammatory breast carcinoma?: A review of evidence from cell line, animal model, and human tissue sample experiments. Cancer 2010; 116: 2794-2805.
11. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
12. Choi WY, Giraldez AJ, Schier AF. Target protectors reveal dampening and balancing of Nodal agonist and antagonist by miR-430. Science 2007; 318: 271-274.
13. Bridge G, Monteiro R, Henderson S, Emuss V, Lagos D, Georgopoulou D et al. The microRNA-30 family targets DLL4 to modulate endothelial cell behavior during angiogenesis. Blood 2012; 120: 5063-5072.
14. Kim K, Madak-Erdogan Z, Ventrella R, Katzenellenbogen BS. A MicroRNA196a2∗and TP63 circuit regulated by estrogen receptor-alpha and ERK2 that controls breast cancer proliferation and invasiveness properties. Horm Cancer 2013; 4: 78-91.
15. Knauss JL, Bian S, Sun T. Plasmid-based target protectors allow specific blockade of miRNA silencing activity in mammalian developmental systems. Front Cell Neurosci 2013; 7: 163.
16. Makino K, Jinnin M, Aoi J, Hirano A, Kajihara I, Makino T et al. Discoidin domain receptor 2-microRNA 196a-mediated negative feedback against excess type I collagen expression is impaired in scleroderma dermal fibroblasts. J Invest Dermatol 2013; 133: 110-119.
17. Ouyang YB, Lu Y, Yue S, Giffard RG. miR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion 2012; 12: 213-219.
18. Maillot G, Lacroix-Triki M, Pierredon S, Gratadou L, Schmidt S, Benes V et al. Widespread estrogen-dependent repression of micrornas involved in breast tumor cell growth. Cancer Res 2009; 69: 8332-8340.
19. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65: 5506-5511.
20. Charafe-Jauffret E, Monville F, Ginestier C, Dontu G, Birnbaum D, Wicha MS. Cancer stem cells in breast: Current opinion and future challenges. Pathobiology 2008; 75: 75-84.
21. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008; 100: 672-679.
22. O'Brien CS, Howell SJ, Farnie G, Clarke RB. Resistance to endocrine therapy: Are breast cancer stem cells the culprits? J Mammary Gland Biol Neoplasia 2009; 14: 45-54.
23. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-9344.
24. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009; 458: 780-783.
25. Murohashi M, Hinohara K, Kuroda M, Isagawa T, Tsuji S, Kobayashi S et al. Gene set enrichment analysis provides insight into novel signalling pathways in breast cancer stem cells. Br J Cancer 2010; 102: 206-212.
26. Cao Y, Luo JL, Karin M. IkappaB kinase alpha kinase activity is required for selfrenewal of ErbB2/Her2-transformed mammary tumor-initiating cells. Proc Natl Acad Sci USA 2007; 104: 15852-15857.
27. Iliopoulos D, Hirsch HA, Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 2009; 139: 693-706.
28. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010; 16: 45-55.
29. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc Natl Acad Sci USA 2010; 107: 21737-21742.
30. Baumgarten SC, Frasor J. Inflammation: An instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol Endocrinol 2012; 26: 360-371.
31. Pradhan M, Baumgarten SC, Bembinster LA, Frasor J. CBP mediates NF-kappaB-dependent histone acetylation and estrogen receptor recruitment to an estrogen response element in the BIRC3 promoter. Mol Cell Biol 2012; 32: 569-575.
32. Pradhan M, Bembinster LA, Baumgarten SC, Frasor J. Proinflammatory cytokines enhance estrogen-dependent expression of the multidrug transporter gene ABCG2 through estrogen receptor and NF{kappa}B cooperativity at adjacent response elements. J Biol Chem 2010; 285: 31100-31106.
33. Frasor J, Weaver AE, Pradhan M, Mehta K. Synergistic up-regulation of prostaglandin E synthase expression in breast cancer cells by 17beta-estradiol and proinflammatory cytokines. Endocrinology 2008; 149: 6272-6279.
34. Meier-Noorden M, Flindt S, Kalinke U, Hinz T. A CpG-rich bidirectional promoter induces the T-cell death-associated gene 51 and downregulates an inversely oriented transcript during early T-cell activation. Gene 2004; 338: 197-207.
35. Croker AK, Allan AL. Cancer stem cells: Implications for the progression and treatment of metastatic disease. J Cell Mol Med 2008; 12: 374-390.
36. Velasco-Velazquez MA, Popov VM, Lisanti MP, Pestell RG. The role of breast cancer stem cells in metastasis and therapeutic implications. Am J Pathol 2011; 179: 2-11.
37. Hollier BG, Evans K, Mani SA. The epithelial-to-mesenchymal transition and cancer stem cells: A coalition against cancer therapies. J Mammary Gland Biol Neoplasia 2009; 14: 29-43.
38. Johnson EO, Chang KH, de Pablo Y, Ghosh S, Mehta R, Badve S et al. PHLDA1 is a crucial negative regulator and effector of Aurora A kinase in breast cancer. J Cell Sci 2011; 124: 2711-2722.
39. Taylor MA, Sossey-Alaoui K, Thompson CL, Danielpour D, Schiemann WP. TGF-beta upregulates miR-181a expression to promote breast cancer metastasis. J Clin Invest 2013; 123: 150-163.
40. Neel JC, Lebrun JJ. Activin and TGFbeta regulate expression of the microRNA-181 family to promote cell migration and invasion in breast cancer cells. Cell Signal 2013; 25: 1556-1566.
41. Bisso A, Faleschini M, Zampa F, Capaci V, De Santa J, Santarpia L et al. Oncogenic miR-181a/b affect the DNA damage response in aggressive breast cancer. Cell Cycle 2013; 12: 1679-1687.
42. Lobry C, Oh P, Mansour MR, Look AT, Aifantis I. Notch signaling: Switching an oncogene to a tumor suppressor. Blood 2014; 123: 2451-2459.
43. Thorner AR, Parker JS, Hoadley KA, Perou CM. Potential tumor suppressor role for the c-Myb oncogene in luminal breast cancer. PLoS ONE 2010; 5: E13073.
44. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17: 1253-1270.
45. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138: 645-659.
46. Seiler CY, Park JG, Sharma A, Hunter P, Surapaneni P, Sedillo C et al. DNASU plasmid and PSI:Biology-Materials repositories: Resources to accelerate biological research. Nucleic Acids Res 2014; 42: D1253-D1260.
47. Cormier CY, Park JG, Fiacco M, Steel J, Hunter P, Kramer J et al. PSI:Biologymaterials repository: A biologist's resource for protein expression plasmids. J Struct Funct Genomics 2011; 12: 55-62.
48. Cormier CY, Mohr SE, Zuo D, Hu Y, Rolfs A, Kramer J et al. Protein Structure Initiative Material Repository: An open shared public resource of structural genomics plasmids for the biological community. Nucleic Acids Res 2010; 38: D743-D749.
49. Yang X, Boehm JS, Yang X, Salehi-Ashtiani K, Hao T, Shen Y et al. A public genome-scale lentiviral expression library of human ORFs. Nat Methods 2011; 8: 659-661.
50. Gyorffy B, Lanczky A, Szallasi Z. Implementing an online tool for genome-wide validation of survival-associated biomarkers in ovarian-cancer using microarray data from 1287 patients. Endocr Relat Cancer 2012; 19: 197-208.