The mitotic kinase aurora-A promotes distant metastases by inducing epithelial-to-mesenchymal transition in ER + breast cancer cells

Oncogene

Volumn 33, Issue 5, 2014, Pages 599-610

  D'Assoro, A B ^a,b   Liu, T ^a   Quatraro, C ^a   Amato, A ^a,c   Opyrchal, M ^b   Leontovich, A ^b   Ikeda, Y ^b   Ohmine, S ^b   Lingle, W ^b   Suman, V ^b   Ecsedy, J ^d   Iankov, I ^b   Di Leonardo, A ^c   Ayers Inglers, J ^a   Degnim, A ^b   Billadeau, D ^b   McCubrey, J ^e   Ingle, J ^b   Salisbury, J L ^a   Galanis, E ^b  

^a MAYO GRADUATE SCHOOL   (United States)

^b Mayo Clinic   (United States)

^c Millennium Pharmaceuticals Inc ^*  (Italy)

^d MILLENNIUM PHARMACEUTICALS INC   (United States)

^e EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Breast Cancer; Metastases; Stemness

Indexed keywords

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIGENS, CD24; AURORA KINASE A; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MCF-7 CELLS; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-RAF; RECEPTOR, ERBB-2; RNA INTERFERENCE; RNA, SMALL INTERFERING; SMAD5 PROTEIN; SOXB1 TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84895067936     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.628     Document Type: Article

References (44)

1. Basaran G, Devrim C, Caglar HB, Gulluoglu B, Kaya H, Seber S et al. Clinical outcome of breast cancer patients with N3a (4/10 positive lymph nodes) disease: Has it changed over years Med Oncol 2010; 28: 726-732.
2. Chang H, Rha SY, Jeung HC, Im CK, Ahn JB, Kwon WS et al. Association of the ABCB1 gene polymorphisms 2677G4T/A and 3435C4T with clinical outcomes of paclitaxel monotherapy in metastatic breast cancer patients. Ann Oncol 2009; 20: 272-277.
3. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
4. Hwang-Verslues WW, Kuo WH, Chang PH, Pan CC, Wang HH, Tsai ST et al. Multiple lineages of human breast cancer stem/progenitor cells identified by profiling with stem cell markers. PLoS One 2009; 4: E8377.
5. DAssoro AB, Leontovich A, Amato A, Ayers-Ringler JR, Quatraro C, Hafner K et al. Abrogation of p53 function leads to metastatic transcriptome networks that typify tumor progression in human breast cancer xenografts. Int J Oncol 2010; 37: 1167-1176.
6. Guarino M, Rubino B, Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007; 39: 305-318.
7. Beavon IR. The E-cadherin-catenin complex in tumour metastasis: Structure, function and regulation. Eur J Cancer 2000; 36: 1607-1620.
8. Strathdee G. Epigenetic versus genetic alterations in the inactivation of E-cadherin. Semin Cancer Biol 2002; 12: 373-379.
9. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
10. Turley EA, Veiseh M, Radisky DC, Bissell MJ. Mechanisms of disease: Epithelial-mesenchymal transition-does cellular plasticity fuel neoplastic progression Nat Clin Pract Oncol 2008; 5: 280-290.
11. Wicha MS, Liu S, Dontu G. Cancer stem cells: An old idea-A paradigm shift. Cancer Res 2006; 66: 1883-1890, discussion 95-96.
12. Abraham BK, Fritz P, McClellan M, Hauptvogel P, Athelogou M, Brauch H. Prevalence of CD44/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin Cancer Res 2005; 11: 1154-1159.
13. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988.
14. Honeth G, Bendahl PO, Ringner M, Saal LH, Gruvberger-Saal SK, Lovgren K et al. The CD44/CD24-phenotype is enriched in basal-like breast tumors. Breast Cancer Res 2008; 10: R53.
15. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI. The CD44/CD24-phenotype relates to triple-negative state and unfavorable prognosis in breast cancer patients. Med Oncol 2011; 28: 745-752.
16. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007; 11: 259-273.
17. Wendt MK, Smith JA, Schiemann WP. Transforming growth factor-beta-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression. Oncogene 2010; 29: 6485-6498.
18. 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 2009; 102: 206-212.
19. Eralp Y, Derin D, Ozluk Y, Yavuz E, Guney N, Saip P et al. MAPK overexpression is associated with anthracycline resistance and increased risk for recurrence in patients with triple-negative breast cancer. Ann Oncol 2008; 19: 669-674.
20. Jin W, Wu L, Liang K, Liu B, Lu Y, Fan Z. Roles of the PI-3K and MEK pathways in Ras-mediated chemoresistance in breast cancer cells. Br J Cancer 2003; 89: 185-191.
21. Ghayad SE, Vendrell JA, Larbi SB, Dumontet C, Bieche I, Cohen PA. Endocrine resistance associated with activated ErbB system in breast cancer cells is reversed by inhibiting MAPK or PI3K/Akt signaling pathways. Int J Cancer 2010; 126: 545-562.
22. Whyte J, Bergin O, Bianchi A, McNally S, Martin F. Key signalling nodes in mammary gland development and cancer. Mitogen-activated protein kinase signalling in experimental models of breast cancer progression and in mammary gland development. Breast Cancer Res 2009; 11: 209.
23. Wang F, Weaver VM, Petersen OW, Larabell CA, Dedhar S, Briand P et al. Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: A different perspective in epithelial biology. Proc Natl Acad Sci USA 1998; 95: 14821-14826.
24. Marampon F, Ciccarelli C, Zani BM. Down-regulation of c-Myc following MEK/ERK inhibition halts the expression of malignant phenotype in rhabdomyosarcoma and in non muscle-derived human tumors. Mol Cancer 2006; 5: 31.
25. Kim ES, Kim MS, Moon A. Transforming growth factor (TGF)-beta in conjunction with H-ras activation promotes malignant progression of MCF10A breast epithelial cells. Cytokine 2005; 29: 84-91.
26. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith De et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244: 707-712.
27. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001; 3: 785-792.
28. Aranda V, Haire T, Nolan ME, Calarco JP, Rosenberg AZ, Fawcett JP et al. Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat Cell Biol 2006; 8: 1235-1245.
29. Kim IY, Yong HY, Kang KW, Moon A. Overexpression of ErbB2 induces invasion of MCF10A human breast epithelial cells via MMP-9. Cancer Lett 2009; 275: 227-233.
30. Korkaya H, Paulson A, Iovino F, Wicha MS. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 2008; 27: 6120-6130.
31. Roesler R, Cornelio DB, Abujamra AL, Schwartsmann G. HER2 as a cancer stem-cell target. Lancet Oncol 2010; 11: 225-226.
32. Korkaya H, Wicha MS. Cancer stem cells: Nature versus nurture. Nat Cell Biol 2010; 12: 419-421.
33. Basto R, Brunk K, Vinadogrova T, Peel N, Franz A, Khodjakov A et al. Centrosome amplification can initiate tumorigenesis in flies. Cell 2008; 133: 1032-1042.
34. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
35. Kerkhoff E, Fedorov LM, Siefken R, Walter AO, Papadopoulos T, Rapp UR. Lungtargeted expression of the c-Raf-1 kinase in transgenic mice exposes a novel oncogenic character of the wild-type protein. Cell Growth Differ 2000; 11: 185-190.
36. Chang CJ, Yang JY, Xia W, Chen CT, Xie X, Chao CH et al. EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-beta-catenin signaling. Cancer Cell 2011; 19: 86-100.
37. Yu D, Hung MC. Overexpression of ErbB2 in cancer and ErbB2-targeting strategies. Oncogene 2000; 19: 6115-6121.
38. Yu D, Hung MC. Role of erbB2 in breast cancer chemosensitivity. BioEssays 2000; 22: 673-680.
39. Lu J, Guo H, Treekitkarnmongkol W, Li P, Zhang J, Shi B et al. 14-3-3zeta Cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell 2009; 16: 195-207.
40. Yu X, Minter-Dykhouse K, Malureanu L, Zhao WM, Zhang D, Merkle CJ et al. Chfr is required for tumor suppression and Aurora A regulation. Nat Genet 2005; 37: 401-406.
41. Davis JM, Navolanic PM, Weinstein-Oppenheimer CR, Steelman LS, Hu W, Konopleva M et al. Raf-1 and Bcl-2 induce distinct and common pathways that contribute to breast cancer drug resistance. Clin Cancer Res 2003; 9: 1161-1170.
42. DAssoro AB, Barrett SL, Folk C, Negron VC, Boeneman K, Busby R et al. Amplified centrosomes in breast cancer: A potential indicator of tumor aggressiveness. Breast Cancer Res Treat 2002; 75: 25-34.
43. DAssoro AB, Busby R, Suino K, Delva E, Almodovar-Mercado GJ, Johnson H et al. Genotoxic stress leads to centrosome amplification in breast cancer cell lines that have an inactive G1/S cell cycle checkpoint.. Oncogene 2004; 23: 4068-4075.
44. DAssoro AB, Busby R, Acu ID, Quatraro C, Reinholz MM, Farrugia DJ et al. Impaired p53 function leads to centrosome amplification, acquired ERalpha phenotypic heterogeneity and distant metastases in breast cancer MCF-7 xenografts. Oncogene 2008; 27: 3901-3911.