AXL induces epithelial-to-mesenchymal transition and regulates the function of breast cancer stem cells

Oncogene

Volumn 33, Issue 10, 2014, Pages 1316-1324

  Asiedu, M K ^a   Beauchamp Perez, F D ^a   Ingle, J N ^b   Behrens, M D ^a   Radisky, D C ^a   Knutson, K L ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

AXL; BCSCs; CSCs; EMT; tyrosine kinase

Indexed keywords

AMUVATINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN;

ANIMAL CELL; ARTICLE; BREAST CANCER; BREAST CANCER STEM CELL; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER CHEMOTHERAPY; CANCER STEM CELL; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; CHEMOSENSITIVITY; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MARKER GENE; METASTASIS; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR INVASION;

MURINAE;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CARCINOGENESIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; MICE; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS; PYRIMIDINES; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TUMOR BURDEN; UP-REGULATION;

EID: 84895922043     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.57     Document Type: Article

References (47)

1. Han JS, Crowe DL. Tumor initiating cancer stem cells from human breast cancer cell lines. Int J Oncol 2009; 34: 1449-1453
2. Vermeulen L, Sprick MR, Kemper K, Stassi G, Medema JP. Cancer stem cells-old concepts, new insights. Cell Death Differ 2008; 15: 947-958
3. Vicente-Duenas C, Cobaleda C, Perez-Losada J, Sanchez-Garcia I. The evolution of cancer modeling: The shadow of stem cells. Dis Model Mech 2010; 3: 149-155
4. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR et al. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 2009; 69: 2887-2895
5. 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
6. Radisky DC. Epithelial-mesenchymal transition. J Cell Sci 2005; 118: 4325-4326
7. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008; 3: E2888
8. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in Development and disease. Cell 2009; 139: 871-890
9. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002; 2: 442-454
10. Cowin P, Welch DR. Breast cancer progression: Controversies and consensus in the molecular mechanisms of metastasis and EMT. J Mammary Gland Biol Neoplasia 2007; 12: 99-102
11. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: New insights in signaling, development, and disease. J Cell Biol 2006; 172: 973-981
12. O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C et al. Axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol 1991; 11: 5016-5031
13. Bose R, Molina H, Patterson AS, Bitok JK, Periaswamy B, Bader JS et al. Phosphoproteomic analysis of Her2/neu signaling and inhibition. Proc Natl Acad Sci USA 2006; 103: 9773-9778
14. Hafizi S, Dahlback B. Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J 2006; 273: 5231-5244
15. Hutterer M, Knyazev P, Abate A, Reschke M, Maier H, Stefanova N et al. Axl and growth arrest-specific gene 6 are frequently overexpressed in human gliomas and predict poor prognosis in patients with glioblastoma multiforme. Clin Cancer Res 2008; 14: 130-138
16. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J et al. Axl as a potential therapeutic target in cancer: Role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009; 28: 3442-3455
17. Zhang YX, Knyazev PG, Cheburkin YV, Sharma K, Knyazev YP, Orfi L et al. AXL is a potential target for therapeutic intervention in breast cancer progression. Cancer Res 2008; 68: 1905-1915
18. Gjerdrum C, Tiron C, Høiby T, Stefansson I, Haugen H, Sandal T et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci USA 2010; 107: 1124-1129
19. Liu L, Greger J, Shi H, Liu Y, Greshock J, Annan R et al. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: Activation of AXL. Cancer Res 2009; 69: 6871-6878
20. 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
21. Asiedu MK, Ingle JN, Behrens MD, Radisky DC, Knutson KL. TGF{beta}/TNF{alpha}-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Res 2011; 71: 4707-4719
22. Qi W, Cooke LS, Stejskal A, Riley C, Croce KD, Saldanha JW et al. MP470, a novel receptor tyrosine kinase inhibitor, in combination with Erlotinib inhibits the HER family/PI3K/Akt pathway and tumor growth in prostate cancer. BMC Cancer 2009; 9: 142
23. Welsh JW, Mahadevan D, Ellsworth R, Cooke L, Bearss D, Stea B. The c-Met receptor tyrosine kinase inhibitor MP470 radiosensitizes glioblastoma cells. Radiat Oncol 2009; 4: 69
24. Meng F, Liu L, Chin PC, D'Mello SR. Akt is a downstream target of NF-kappa B. J Biol Chem 2002; 277: 29674-29680
25. Tai KY, Shieh YS, Lee CS, Shiah SG, Wu CW. Axl promotes cell invasion by inducing MMP-9 activity through activation of NF-kappaB and Brg-1. Oncogene 2008; 27: 4044-4055
26. Chen W, Li Z, Bai L, Lin Y. NF-kappaB in lung cancer, a carcinogenesis mediator and a prevention and therapy target. Front Biosci 2011; 16: 1172-1185
27. Shipitsin M, Polyak K. The cancer stem cell hypothesis: In search of definitions, markers, and relevance. Lab Invest 2008; 88: 459-463
28. Wicha MS. Cancer stem cells and metastasis: Lethal seeds. Clin Cancer Res 2006; 12: 5606-5607
29. Gangemi R, Paleari L, Orengo AM, Cesario A, Chessa L, Ferrini S et al. Cancer stem cells: A new paradigm for understanding tumor growth and progression and drug resistance. Curr Med Chem 2009; 16: 1688-1703
30. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: Mirage or reality?. Nat Med 2009; 15: 1010-1012
31. Blick T, Hugo H, Widodo E, Waltham M, Pinto C, Mani SA et al. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia 2010; 15: 235-252
32. Rankin EB, Fuh KC, Taylor TE, Krieg AJ, Musser M, Yuan J et al. AXL is an essential factor and therapeutic target for metastatic ovarian cancer. Cancer Res 2010; 70: 7570-7579
33. Nakano T, Tani M, Ishibashi Y, Kimura K, Park YB, Imaizumi N et al. Biological properties and gene expression associated with metastatic potential of human osteosarcoma. Clin Exp Metast 2003; 20: 665-674
34. Vajkoczy P, Knyazev P, Kunkel A, Capelle HH, Behrndt S, von Tengg-Kobligk H et al. Dominant-negative inhibition of the Axl receptor tyrosine kinase suppresses brain tumor cell growth and invasion and prolongs survival. Proc Natl Acad Sci USA 2006; 103: 5799-5804
35. Shieh YS, Lai CY, Kao YR, Shiah SG, Chu YW, Lee HS et al. Expression of axl in lung adenocarcinoma and correlation with tumor progression. Neoplasia 2005; 7: 1058-1064
36. Chung BI, Malkowicz SB, Nguyen TB, Libertino JA, McGarvey TW. Expression of the proto-oncogene Axl in renal cell carcinoma. DNA Cell Biol 2003; 22: 533-540
37. van Ginkel PR, Gee RL, Shearer RL, Subramanian L, Walker TM, Albert DM et al. Expression of the receptor tyrosine kinase Axl promotes ocular melanoma cell survival. Cancer Res 2004; 64: 128-134
38. Craven RJ, Xu LH, Weiner TM, Fridell YW, Dent GA, Srivastava S et al. Receptor tyrosine kinases expressed in metastatic colon cancer. Int J Cancer 1995; 60: 791-797
39. Song X, Wang H, Logsdon CD, Rashid A, Fleming JB, Abbruzzese JL et al. Overexpression of receptor tyrosine kinase Axl promotes tumor cell invasion and survival in pancreatic ductal adenocarcinoma. Cancer 117: 734-743
40. Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi JP, Nevo J, Gjerdrum C et al. Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 2011; 30: 1436-1448
41. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7: 131-142
42. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004; 117: 927-939
43. Koorstra JB, Karikari CA, Feldmann G, Bisht S, Rojas PL, Offerhaus GJ et al. The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target. Cancer Biol Ther 2009; 8: 618-626
44. Lee WP, Liao Y, Robinson D, Kung HJ, Liu ET, Hung MC. Axl-gas6 interaction counteracts E1A-mediated cell growth suppression and proapoptotic activity. Mol Cell Biol 1999; 19: 8075-8082
45. Holland SJ, Pan A, Franci C, Hu Y, Chang B, Li W et al. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res 2010; 70: 1544-1554
46. Keating AK, Kim GK, Jones AE, Donson AM, Ware K, Mulcahy JM et al. Inhibition of Mer and Axl receptor tyrosine kinases in astrocytoma cells leads to increased apoptosis and improved chemosensitivity. Mol Cancer Ther 2010; 9: 1298-1307
47. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, Chiapero-Stanke L et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 2008; 10: R52