COX-2 Induces Breast Cancer Stem Cells via EP4/PI3K/AKT/NOTCH/WNT Axis

Stem Cells

Volumn 34, Issue 9, 2016, Pages 2290-2305

  Majumder, Mousumi ^a   Xin, Xiping ^a   Liu, Ling ^a   Tutunea Fatan, Elena ^b   Rodriguez Torres, Mauricio ^a   Vincent, Krista ^a,d   Postovit, Lynne Marie ^a,d   Hess, David ^b,e   Lala, Peeyush K ^a,c  

^a Department of Anatomy and Cell Biology ^*  (Canada)

^b Physiology and Pharmacology   (Canada)

^c WESTERN UNIVERSITY   (Canada)

^d UNIVERSITY OF ALBERTA   (Canada)

^e ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Breast cancer; Cyclo oxygenase 2; EP4; NOTCH WNT; Stem like cell

Indexed keywords

ALDEHYDE DEHYDROGENASE; BETA CATENIN; CD24 ANTIGEN; CYCLOOXYGENASE 2; HERMES ANTIGEN; NERVE CELL ADHESION MOLECULE; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E RECEPTOR 4; PROTEIN KINASE B; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TWIST; UVOMORULIN; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN D; VIMENTIN; WNT PROTEIN;

ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER STEM CELL; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MCF 7 CELL LINE; METASTASIS; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84985994285     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2426     Document Type: Article

References (52)

1. American Cancer Society. Cancer Facts & Figures 2014. Atlanta: American Cancer Society; 2014.
2. Nahta R, Shabaya S, Ozbay T et al. Personalizing HER2-targeted therapy in metastatic breast cancer beyond HER2 status: What we have learned from clinical specimens. Curr Pharmacogenomics Person Med 2009;7:263–274.
3. Wicha M, Liu S, Dontu G. Cancer stem cells: an old idea – a paradigm shift. Cancer Res 2006;66:1883–1890.
4. Luo W, Li S, Peng B et al. Embryonic stem cells markers SOX2, OCT4 and Nanog expression and their correlations with epithelial-mesenchymal transition in nasopharyngeal carcinoma. PLoS One 2013;8:e56324. doi: 10.1371/journal.pone.0056324.
5. Majumder M, Xin X, Liu L et al. EP4 as the common target on cancer cells and macrophages to abolish angiogenesis, lymph-angiogenesis, metastasis and SLC functions. Cancer Sci 2014;105:1142–1151. doi: 10.1111/cas.12475.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A et al. Prospective identification tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983–3988. doi: 10.1073/pnas.0530291100.
7. Hwang WL, Yang MH, Tsai ML et al. SNAIL regulates interleukin-8 expression, stem cell-like activity, and tumorigenicity of human colorectal carcinoma cells. Gastroenterology 2011;141:279–291, 291.e1-5. doi: 10.1053/j.gastro.2011.
8. Vesuna F, Lisok A, Kimble B et al. Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia 2009;11:1318–1328.
9. Chaffer CL, Marjanovic ND, Lee T et al. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell 2013;154:61–74. doi: 10.1016/j.cell.2013.06.005.
10. William CS, Moss M, Dubois RN. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 1999;18:7908–7916.
11. Subbaramaiah K, Dannenberg AJ. Cyclooxygenase 2: a molecular target for cancer prevention and treatment. Trends Pharmacol Sci 2003;24:96–102.
12. Harris RE, Beebe-Donk J, Alshafie GA. Reduction in the risk of human breast cancer by selective cyclooxygenase-2 (COX-2) inhibitors. BMC Cancer 2006;6:27.
13. Ristimaki A, Sivula A, Lundin J et al. Prognostic significance of elevated cyclooxygenase-2 expression in breast cancer. Cancer Res 2002;62:632–635.
14. Lala PK, Parhar RS, Singh P. Indomethacin-therapy abrogates in prostaglandin-mediated suppression of natural killer activity in tumor bearing mice and prevents tumor metastasis. Cell Immunol 1986;99:108–118.
15. Rozic J, Chakraborty C, Lala PK. Cyclooxygenase inhibitors retard murine mammary tumor progression by reducing tumor cell migration, invasiveness and angiogenesis. Int J Cancer 2001;93:497–506.
16. Timoshenko A, Xu G, Chakrabarti S et al. Role of prostaglandin E2 receptors in migration of murine and human breast cancer cells. Exp Cell Res 2003;289:265–274.
17. Timoshenko A, Chakraborty C, Wagner G et al. COX-2-mediated upregulation of the lymphangiogenic factor VEGF-C in human breast cancer. Br J Cancer 2006;94:1154–1163.
18. Xin X, Majumder M, Girish GV et al. Targeting COX-2 and EP4 to control tumor growth, angiogenesis, lymphangiogenesis and metastasis to the lungs and lymph nodes in a breast cancer model. Lab Invest 2012;92:1115–1128. doi: 10.1038/labinvest.2012.90.
19. Majumder M, Landman E, Liu L et al. COX-2 elevates oncogenic miR-526b in breast cancer by EP4 activation. Mol Cancer Res 2015;13:1022–1033. doi: 10.1158/1541-7786 MCR-14-0543
20. Breyer RM, Bagdassarian CK, Myers SA et al. Prostanoid receptors: subtypes and signaling. Annu Rev Pharmacol Toxicol 2001;41:661–690.
21. Fujino H, Xu W, Regan J. Prostaglandin E2 induced functional expression of early growth response factor-1 by EP4, but not EP2, prostanoid receptors via the phosphatidylinositol 3-kinase and extracellular signal-regulated kinases. J Biol Chem 2003;278:12151–12156.
22. Sugimoto Y, Narumiya S. Prostaglandin E receptors. J Biol Chem 2007;282:11613–11617.
23. FitzGerald GA. Coxibs and cardiovascular disease. N Engl J Med 2004;351:1709–1711.
24. Graham DJ. COX-2 inhibitors, other NSAIDs, and cardiovascular risk: The seduction of common sense. JAMA 2006;296:1653–1666.
25. Guo Y, Tukaye DN, Wu WJ et al. The COX-2/PGI2 receptor axis plays an obligatory role in mediating the cardioprotection conferred by the late phase of ischemic preconditioning. PLoS One 2012;7:e41178. doi:10.1371/journal.pone. 0041178.
26. Stylianou S, Clarke RB, Brennan K. Aberrant activation of notch signaling in human breast cancer. Cancer Res 2006;66:1517–1525.
27. Chen J, Imanaka N, Chen J et al. Hypoxia potentiates notch signaling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion. Br J Cancer 2010;102:351–360. doi: 10.1038/sj.bjc.6605486.
28. Matsuda Y, Schlange T, Oakeley EJ et al. WNT signaling enhances breast cancer cell motility and blockade of the WNT pathway by sFRP1 suppresses MDA-MB-231 xenograft growth. Breast Cancer Res 2009;11:R32. doi: 10.1186/bcr2317.
29. Dey N, Barwick BG, Moreno CS et al. Wnt signaling in triple negative breast cancer is associated with metastasis. BMC Cancer 2013;13:537. doi: 10.1186/1471-2407-13-537.
30. Jang GB, Hong IS, Kim RJ et al. Wnt/β-catenin Small-molecule inhibitor CWP232228 preferentially inhibits the growth of breast cancer stem-like cells. Cancer Res 2015;75:1691–1702. Apr 15; doi: 10.1158/0008-5472.CAN-14-2041. Epub 2015 Feb 6.
31. Buchanan FG, DuBois RN. Connecting COX-2 and Wnt in cancer. Cancer Cell 2006;9:6–8.
32. Howe LR, Chang SH, Tolle KC et al. HER2/neu induced mammary tumorigenesis and angiogenesis are reduced in cyclooxygenase-2knockout mice. Cancer Res 2005;65:10113–10119.
33. Howe LR, Subbaramaiah K, Patel J et al. Celecoxib, a selective cyclooxygenase 2 inhibitor, protects against human epidermal growth factor receptor 2 (HER-2)/neu-induced breast cancer. Cancer Res 2002;62:5405–5407.
34. Bhattacharjee R, Timoshenko A, Cai J et al. Relationship between cyclooxygenase-2 and human epidermal growth factor receptor 2 in vascular endothelial growth factor C up-regulation and lymphangiogenesis in human breast cancer. Cancer Sci 2010;101:2026–2032.
35. Majumder M, Tutunea-Fatan E, Xin X et al. Co-expression of α9β1 integrin and VEGF-D confers lymphatic metastatic ability to a human breast cancer cell line MDA-MB-468LN. PLoS One 2012;7:e35094. doi: 10.1371/journal. pone. 0035094.
36. Dontu G, Abdallah W, Foley J et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253–1270.
37. Croker AK, Allan AL. Inhibition of aldehyde dehydrogenase (ALDH) activity reduces chemotherapy and radiation resistance of stem-like ALDHhiCD44+ human breast cancer cells. Breast Cancer Res Treat 2012;133:75–87. doi: 10.1007/s10549-011-1692-y.
38. Hess DA, Craft TP, Wirthlin L et al. Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity. Stem Cells 2008;26:611–620.
39. Quail DF, Zhang G, Walsh LA et al. Embryonic morphogen nodal promotes breast cancer growth and progression. PLoS One 2012;7:e48237. doi: 10.1371/journal.pone.0048237.
40. Jadeski LC, Lala PK. Nitric oxide synthase inhibition by N G-nitro-l-arginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am J Pathol 1999;155:1381–1390.
41. http://cancergenome.nih.gov/.
42. Singh B, Cook KR, Vincent L et al. Role of COX-2 in tumorospheres derived from a breast cancer cell Line. J Surg Res 2011;168:e39–e49. doi: 10.1016/j.jss. 2010.03.003.
43. Kundu N, Ma X, Kochel T et al. Prostaglandin E receptor EP4 is a therapeutic target in breast cancer cells with stem-like properties. Breast Cancer Res Treat 2014;143:19–31.
44. Ma X, Holt D, Kundu N et al. A prostaglandin E (PGE) receptor EP4 antagonist protects natural killer cells from PGE2-mediated immunosuppression and inhibits breast cancer metastasis. Oncoimmunology 2013;12:e22647.
45. Pozzi A, Yan X, Macias-Perez I et al. Colon carcinoma cell growth is associated with prostaglandin E2/EP4 receptor-evoked ERK activation. J Biol Chem 2004;279:29797–29804.
46. George RJ, Sturmoski MA, Anant S et al. EP4 mediates PGE2 dependent cell survival through the PI3 kinase/AKT pathway. Prostaglandins Other Lipid Mediat 2007;83:112–120.
47. Kim JI, Lakshmikanthan V, Frilot N et al. Prostaglandin E2 promotes lung cancer cell migration via EP4-betaArrestin1-c-src signalsome. Mol Cancer Res 2010;8:569–577.
48. Yu X, Zou J, Ye Z et al. Notch signaling activation in human embryonic stem cells is required for embryonic, but not trophoblastic, lineage commitment. Cell Stem Cell 2008;2:461–471. doi: 10.1016/j.stem.2008.03.001.
49. Blauwkamp TA, Nigam S, Ardehali R et al. Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 2012;3:1070. doi: 10.1038/ncomms2064.
50. Jang GB, Hong IS, Kim RJ et al. Wnt/β-catenin Small-molecule inhibitor CWP232228 preferentially inhibits the growth of breast cancer stem-like cells. Cancer Res 2015;75:1691–1702. doi: 10.1158/0008-5472.CAN-14-2041.
51. Liou JY, Ellent DP, Lee S et al. Cyclooxygenase-2-derived prostaglandin E2 protects mouse embryonic stem cells from apoptosis. Stem Cells 2007;25:1096–1103.
52. Aguirre-Ghiso JA. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 2007;7:834–846.