Notch1 induces epithelial-mesenchymal transition and the cancer stem cell phenotype in breast cancer cells and STAT3 plays a key role

International Journal of Oncology

Volumn 46, Issue 3, 2015, Pages 1141-1148

  Zhang, Xiaojin ^a   Zhao, Xiaoai ^a   Shao, Shan ^a   Zuo, Xiaoxiao ^a   Ning, Qian ^b   Luo, Minna ^a   Gu, Shanzhi ^a   Zhao, Xinhan ^a  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Cancer stem cells; Epithelial mesenchymal transition; Notch1; Signal transducer and activator of transcription 3

Indexed keywords

FIBRONECTIN; INTERLEUKIN 1BETA; NERVE CELL ADHESION MOLECULE; NOTCH1 RECEPTOR; OCCLUDIN; STAT3 PROTEIN; SYNAPTOTAGMIN I; UVOMORULIN; VIMENTIN; NOTCH1 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; BREAST EPITHELIUM CELL; CANCER STEM CELL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FILTERS AND MEMBRANES; MCF 7 CELL LINE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BREAST TUMOR; CELL CULTURE; CELL TRANSFORMATION; FEMALE; GENETIC TRANSFECTION; GENETICS; HUMAN; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; MCF-7 CELLS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; PHENOTYPE; RECEPTOR, NOTCH1; STAT3 TRANSCRIPTION FACTOR; TRANSFECTION;

EID: 84921903048     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2809     Document Type: Article

References (48)

1. Wang Z, Li Y, Banerjee S and Sarkar FH: Exploitation of the Notch signaling pathway as a novel target for cancer therapy. Anticancer Res 28: 3621-3630, 2008.
2. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B and Miele L: Rational targeting of Notch signaling in cancer. Oncogene 27: 5124-5131, 2008.
3. Gallahan D, Jhappan C and Robinson G, et al: Expression of a truncated Int3 gene in developing secretory mammary epithelium specifically retards lobular differentiation resulting in tumorigenesis. Cancer Res 56: 1775-1785, 1996.
4. Kiaris H, Politi K and Grimm LM, et al: Modulation of notch signaling elicits signature tumors and inhibits hras1-induced oncogenesis in the mouse mammary epithelium. Am J Pathol 165: 695-705, 2004.
5. Bao B, Wang Z and Ali S, et al: Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Lett 307: 26-36, 2011.
6. Artavanis-Tsakonas S, Rand MD and Lake RJ: Notch signaling: cell fate control and signal integration in development. Science 284: 770-776, 1999.
7. Shook D and Keller R: Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech Dev 120: 1351-1383, 2003.
8. Thiery JP: Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454, 2002.
9. Levayer R and Lecuit T: Breaking down EMT. Nat Cell Biol 10: 757-759, 2008.
10. Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428, 2009.
11. Duband JL, Blavet C, Jarov A and Fournier-Thibault C: Spatio-temporal control of neural epithelial cell migration and epithelium-to-mesenchyme transition during avian neural tube development. Dev Growth Differ 51: 25-44, 2009.
12. Clevers H: The cancer stem cell: premises, promises and challenges. Nat Med 17: 313-319, 2011.
13. Mani SA, Guo W and Liao MJ, et al: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715, 2008.
14. Baker SJ, Rane SG and Reddy EP: Hematopoietic cytokine receptor signaling. Oncogene 26: 6724-6737, 2007.
15. Groner B, Lucks P and Borghouts C: The function of Stat3 in tumor cells and their microenvironment. Semin Cell Dev Biol 19: 341-350, 2008.
16. Berishaj M, Gao SP and Ahmed S, et al: Stat3 is tyrosine-phosphorylated through the interleukin-6/glycoprotein 130/Janus kinase pathway in breast cancer. Breast Cancer Res 9: R32, 2007.
17. Marotta LL, Almendro V and Marusyk A, et al: The JAK2/STAT3 signaling pathway is required for growth of CD44(+) CD24(-) stem cell-like breast cancer cells in human tumors. J Clin Invest 121: 2723-2735, 2011.
18. Barnes RM and Firulli AB: A twist of insight - the role of Twist-family bHLH factors in development. Int J Dev Biol 53: 909-924, 2009.
19. Puisieux A, Valsesia-Wittmann S and Ansieau S: A twist for survival and cancer progression. Br J Cancer 94: 13-17, 2006.
20. Zeisberg M and Neilson EG: Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 119: 1429-1437, 2009.
21. Watanabe O, Imamura H and Shimizu T, et al: Expression of twist and wnt in human breast cancer. Anticancer Res 24: 3851-3856, 2004.
22. Vesuna F, Lisok A, Kimble B and Raman V: Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia 11: 1318-1328, 2009.
23. Anant S, Roy S and VijayRaghavan K: Twist and Notch negatively regulate adult muscle differentiation in Drosophila. Development 125: 1361-1369, 1998.
24. Tapanes-Castillo A and Baylies MK: Notch signaling patterns Drosophila mesodermal segments by regulating the bHLH transcription factor twist. Development 131: 2359-2372, 2004.
25. Hsu KW, Hsieh RH, Huang KH, et al: Activation of the Notch1/ STAT3/Twist signaling axis promotes gastric cancer progression. Carcinogenesis 33: 1459-1467, 2012.
26. Li Y, Wang L, Pappan L, Galliher-Beckley A and Shi J: IL-1beta promotes stemness and invasiveness of colon cancer cells through Zeb1 activation. Mol Cancer 11: 87, 2012.
27. Liu ZL, Li Y, Kong QY, et al: Immunohistochemical profiling of Wnt, NF-kappaB, Stat3 and Notch signaling in human epidermal tumors. J Dermatol Sci 52: 133-136, 2008.
28. Koch U, Lehal R and Radtke F: Stem cells living with a Notch. Development 140: 689-704, 2013.
29. Osanyingbemi-Obidi J, Dobromilskaya I, Illei PB, Hann CL and Rudin CM: Notch signaling contributes to lung cancer clonogenic capacity in vitro but may be circumvented in tumorigenesis in vivo. Mol Cancer Res 9: 1746-1754, 2011.
30. Bolos V, Mira E and Martinez-Poveda B, et al: Notch activation stimulates migration of breast cancer cells and promotes tumor growth. Breast Cancer Res 15: R54, 2013.
31. Espinoza I and Miele L: Deadly crosstalk: Notch signaling at the intersection of EMT and cancer stem cells. Cancer Lett 341: 41-45, 2013.
32. Xie M, Zhang L and He CS, et al: Activation of Notch-1 enhances epithelial-mesenchymal transition in gefitinib-acquired resistant lung cancer cells. J Cell Biochem 113: 1501-1513, 2012.
33. Ghajar CM and Bissell MJ: Extracellular matrix control of mammary gland morphogenesis and tumorigenesis: insights from imaging. Histochem Cell Biol 130: 1105-1118, 2008.
34. Park J and Schwarzbauer JE: Mammary epithelial cell interactions with fibronectin stimulate epithelial-mesenchymal transition. Oncogene 33: 1649-1657, 2014.
35. Bonnet D and Dick JE: Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737, 1997.
36. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988, 2003.
37. Li C, Heidt DG, Dalerba P, et al: Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037, 2007.
38. Mallini P, Lennard T, Kirby J and Meeson A: Epithelial-tomesenchymal transition: what is the impact on breast cancer stem cells and drug resistance. Cancer Treat Rev 40: 341-348, 2014.
39. Castellanos JA, Merchant NB and Nagathihalli NS: Emerging targets in pancreatic cancer: epithelial-mesenchymal transition and cancer stem cells. Onco Targets Ther 6: 1261-1267, 2013.
40. Takebe N, Warren RQ and Ivy SP: Breast cancer growth and metastasis: interplay between cancer stem cells, embryonic signaling pathways and epithelial-to-mesenchymal transition. Breast Cancer Res 13: 211, 2011.
41. Espinoza I, Pochampally R, Xing F, Watabe K and Miele L: Notch signaling: targeting cancer stem cells and epithelial-tomesenchymal transition. Onco Targets Ther 6: 1249-1259, 2013.
42. McGowan PM, Simedrea C and Ribot EJ, et al: Notch1 inhibition alters the CD44hi/CD24lo population and reduces the formation of brain metastases from breast cancer. Mol Cancer Res 9: 834-844, 2011.
43. Soriano JV, Uyttendaele H, Kitajewski J and Montesano R: Expression of an activated Notch4(int-3) oncoprotein disrupts morphogenesis and induces an invasive phenotype in mammary epithelial cells in vitro. Int J Cancer 86: 652-659, 2000.
44. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM and Wicha MS: Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res 6: R605-R615, 2004.
45. Bellavia D, Checquolo S, Campese AF, Felli MP, Gulino A and Screpanti I: Notch3: from subtle structural differences to functional diversity. Oncogene 27: 5092-5098, 2008.
46. Guo S, Liu M and Gonzalez-Perez RR: Role of Notch and its oncogenic signaling crosstalk in breast cancer. Biochim Biophys Acta 1815: 197-213, 2011.
47. Lin JT, Wang JY and Chen MK, et al: Colon cancer mesenchymal stem cells modulate the tumorigenicity of colon cancer through interleukin 6. Exp Cell Res 319: 2216-2229, 2013.
48. Wang H, Tian Y, Wang J, et al: Inflammatory cytokines induce NOTCH signaling in nucleus pulposus cells: implications in intervertebral disc degeneration. J Biol Chem 288: 16761-16774, 2013.