Twist2 contributes to breast cancer progression by promoting an epithelial-mesenchymal transition and cancer stem-like cell self-renewal

Oncogene

Volumn 30, Issue 47, 2011, Pages 4707-4720

  Fang, X ^a   Cai, Y ^a   Liu, J ^a   Wang, Z ^a   Wu, Q ^b   Zhang, Z ^b   Yang, C J ^a   Yuan, L ^a   Ouyang, G ^a  

^a XIAMEN UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

Author keywords

Breast cancer; Cancer stem cell; Epithelial mesenchymal transition; Metastasis; Twist2

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BETA ACTIN; BETA CATENIN; BIOCHEMICAL MARKER; CD24 ANTIGEN; FIBRONECTIN; HERMES ANTIGEN; NERVE CELL ADHESION MOLECULE; PROTEIN TWIST2; STAT3 PROTEIN; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER STEM CELL; CELL MIGRATION; CELL RENEWAL; CELL SIZE; CELL SUBPOPULATION; COLONY FORMING UNIT; CONTROLLED STUDY; DOWN REGULATION; E CADHERIN GENE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; MORPHOLOGY; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TWIST2 GENE; UPREGULATION;

ANTIGENS, CD24; ANTIGENS, CD44; BREAST NEOPLASMS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; NEOPLASTIC STEM CELLS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; STAT3 TRANSCRIPTION FACTOR; TWIST TRANSCRIPTION FACTOR;

EID: 81855182066     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.181     Document Type: Article

References (57)

1. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA. (2009). Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119: 1438-1449.
2. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. (2003). Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988.
3. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C et al. (2008). Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 14: 79-89.
4. Ansieau S, Morel AP, Hinkal G, Bastid J, Puisieux A. (2010). TWISTing an embryonic transcription factor into an oncoprotein. Oncogene 29: 3173-3184.
5. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M et al. (2004). Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5: 329-339.
6. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
7. Battula VL, Evans KW, Hollier BG, Shi Y, Marini FC, Ayyanan A et al. (2010). Epithelial-mesenchymal transition-derived cells exhibit multilineage differentiation potential similar to mesenchymal stem cells. Stem Cells 28: 1435-1445.
8. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. (2005). Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749.
9. Bromberg J. (2002). Stat proteins and oncogenesis. J Clin Invest 109: 1139-1142.
10. Chan KS, Sano S, Kiguchi K, Anders J, Komazawa N, Takeda J et al. (2004). Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis. J Clin Invest 114: 720-728.
11. Chen ZF, Behringer RR. (1995). Twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev 9: 686-699.
12. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M et al. (2008). Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 283: 14665-14673.
13. Debnath J, Muthuswamy SK, Brugge JS. (2003). Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in threedimensional basement membrane cultures. Methods 30: 256-268.
14. Dimri GP, Martinez JL, Jacobs JJ, Keblusek P, Itahana K, Van Lohuizen M et al. (2002). The Bmi-1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res 62: 4736-4745.
15. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ et al. (2003). In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17: 1253-1270.
16. Evdokimova V, Tognon C, Ng T, Ruzanov P,Melnyk N, Fink D et al. (2009). Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelialmesenchymal transition. Cancer Cell 15: 402-415.
17. Fernando RI, Litzinger M, Trono P, Hamilton DH, Schlom J, Palena C. (2010). The T-box transcription factor Brachyury promotes epithelial-mesenchymal transition in human tumor cells. J Clin Invest 120: 533-544.
18. Franco HL, Casasnovas J, Rodríguez-Medina JR, Cadilla CL. (2011). Redundant or separate entities?-Roles of Twist1 and Twist2 as molecular switches during gene transcription. Nucleic Acids Res 39: 1177-1186.
19. Gong XQ, Li L. (2002). Dermo-1, a multifunctional basic helix-loophelix protein, represses MyoD transactivation via the HLH domain, MEF2 interaction, and chromatin deacetylation. J Biol Chem 277: 12310-12317.
20. Gupta PB, Chaffer CL, Weinberg RA. (2009a). Cancer stem cells: mirage or reality? Nat Med 15: 1010-1012.
21. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA et al. (2009b). Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
22. Hanahan D, Weinberg RA. (2011). Hallmarks of cancer: the next generation. Cell 144: 646-674.
23. Iliopoulos D, Polytarchou C, Hatziapostolou M, Kottakis F, Maroulakou IG, Struhl K et al. (2009). MicroRNAs differentially regulated by Akt isoforms control EMT and stem cell renewal in cancer cells. Sci Signal 2: ra62.
24. Isenmann S, Arthur A, Zannettino AC, Turner JL, Shi S, Glackin CA et al. (2009). TWIST family of basic helix-loop-helix transcription factors mediate human mesenchymal stem cell growth and commitment. Stem Cells 27: 2457-2468.
25. Kalluri R, Weinberg RA. (2009). The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428.
26. Lee MS, Lowe G, Flanagan S, Kuchler K, Glackin CA. (2000). Human Dermo-1 has attributes similar to twist in early bone development. Bone 27: 591-602.
27. Levy DE, Darnell Jr JE. (2002). Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3: 651-662.
28. Li L, Cserjesi P, Olson EN. (1995). Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Dev Biol 172: 280-292.
29. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW et al. (2006). Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 66: 6063-6071.
30. Liu S, Dontu G, Wicha MS. (2005). Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res 7: 86-95.
31. Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y et al. (2007). Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 67: 9066-9076.
32. Maeda M, Johnson KR, Wheelock MJ. (2005). Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J Cell Sci 118: 873-887.
33. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
34. McCoy EL, Iwanaga R, Jedlicka P, Abbey NS, Chodosh LA, Heichman KA et al. (2009). Six1 expands the mouse mammary epithelial stem/progenitor cell pool and induces mammary tumors that undergo epithelial-mesenchymal transition. J Clin Invest 119: 2663-2677.
35. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. (2008). Generation of breast cancer stem cells through epithelialmesenchymal transition. PLoS One 3: e2888.
36. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. (2008). Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68: 3645-3654.
37. Ouyang G, Wang Z, Fang X, Liu J, Yang CJ. (2010). Molecular signaling of the epithelial to mesenchymal transition in generating and maintaining cancer stem cells. Cell Mol Life Sci 67: 2605-2618.
38. Peinado H, Olmeda D, Cano A. (2007). Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428.
39. Polyak K, Weinberg RA. (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
40. Ruan K, Bao S, Ouyang G. (2009). The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66: 2219-2230.
41. Singh A, Settleman J. (2010). EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29: 4741-4751.
42. Song G, Ouyang G, Mao Y, Ming Y, Bao S, Hu T. (2009a). Osteopontin promotes gastric cancer metastasis by augmenting cell survival and invasion through Akt-mediated HIF-1alpha upregulation and MMP9 activation. J Cell Mol Med 13: 1706-1718.
43. Song LB, Li J, Liao WT, Feng Y, Yu CP, Hu LJ et al. (2009b). The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest 119: 3626-3636.
44. Sullivan NJ, Sasser AK, Axel AE, Vesuna F, Raman V, Ramirez N et al. (2009). Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 28: 2940-2947.
45. Thiery JP, Acloque H, Huang RY, Nieto MA. (2009). Epithelialmesenchymal transitions in development and disease. Cell 139: 871-890.
46. Thiery JP, Sleeman JP. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
47. Thisse B, el Messal M, Perrin-Schmitt F. (1987). The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern. Nucleic Acids Res 15: 3439-3453.
48. Tsuji T, Ibaragi S, Shima K, Hu MG, Katsurano M, Sasaki A et al. (2008). Epithelial-mesenchymal transition induced by growth suppressor p12CDK2-AP1 promotes tumor cell local invasion but suppresses distant colony growth. Cancer Res 68: 10377-10386.
49. Vesuna F, Lisok A, Kimble B, Raman V. (2009). Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia 11: 1318-1328.
50. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A et al. (2009). The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495.
51. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C et al. (2004). Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939.
52. Yang J, Weinberg RA. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14: 818-829.
53. Yang MH, Hsu DS, Wang HW, Wang HJ, Lan HY, Yang WH et al. (2010). Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol 12: 982-992.
54. Yang Y, Pan X, Lei W, Wang J, Shi J, Li F et al. (2006). Regulation of transforming growth factor-beta 1-induced apoptosis and epithelial-to- mesenchymal transition by protein kinase A and signal transducers and activators of transcription 3. Cancer Res 66: 8617-8624.
55. Yin G, Chen R, Alvero AB, Fu HH, Holmberg J, Glackin C et al. (2010). TWISTing stemness, inflammation and proliferation of epithelial ovarian cancer cells through MIR199A2/214. Oncogene 29: 3545-3553.
56. Yu M, Smolen GA, Zhang J, Wittner B, Schott BJ, Brachtel E et al. (2009). A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression. Genes Dev 23: 1737-1742.
57. Zhou J, Wulfkuhle J, Zhang H, Gu P, Yang Y, Deng J et al. (2007). Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci USA 104: 16158-16163.