Tumor Biology

, Volume 37, Issue 1, pp 185–197 | Cite as

The role of TWIST1 in epithelial-mesenchymal transition and cancers

Review

Abstract

TWIST1 is a basic helix-loop-helix (bHLH) transcription factor which plays essential and pivotal roles in multiple stages of embryonic development, and significantly contributes to tumor metastasis, even tumor initiation and primary tumor growth. It is well recognized that TWIST1 is overexpressed in a variety of tumors. Overexpression of TWIST1 induces epithelial-mesenchymal transition (EMT), a key process in the metastases formation of cancer. TWIST1 also promotes the formation of cancer stem cells and facilitates the process of tumorigenesis. Numerous studies have shown that targeting TWIST1 or TWIST1-related molecules significantly inhibits tumor growth, restricts tumor metastasis, reverses drug resistance, and thus improves the survival of cancer patients. Therefore, it is important to provide a better understanding of the context-dependent regulation of TWIST1 in each individual epithelial tumor, which might reveal new therapeutic targets in cancer treatment.

Keywords

TWIST1 Role Epithelial-mesenchymal transition (EMT) Cancers 

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (no. 81302032) and the Natural Science Foundation of Jiangsu Province (no. BK20140736).

Compliance with ethical standards

Conflicts of interest

None

References

  1. 1.
    Piccinin S et al. A “twist box” code of p53 inactivation: twist box: p53 interaction promotes p53 degradation. Cancer Cell. 2012;22(3):404–15.PubMedGoogle Scholar
  2. 2.
    Castanon I et al. Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development. 2001;128(16):3145–59.PubMedGoogle Scholar
  3. 3.
    Connerney J et al. Twist1 homodimers enhance FGF responsiveness of the cranial sutures and promote suture closure. Dev Biol. 2008;318(2):323–34.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Xue G, Hemmings BA. Phosphorylation of basic helix-loop-helix transcription factor Twist in development and disease. Biochem Soc Trans. 2012;40(1):90–3.PubMedGoogle Scholar
  5. 5.
    Fackler MJ et al. DNA methylation of RASSF1A, HIN-1, RAR-beta, Cyclin D2 and Twist in situ and invasive lobular breast carcinoma. Int J Cancer. 2003;107(6):970–5.PubMedGoogle Scholar
  6. 6.
    Li B et al. Down-regulation of miR-214 contributes to intrahepatic cholangiocarcinoma metastasis by targeting Twist. FEBS J. 2012;279(13):2393–8.PubMedGoogle Scholar
  7. 7.
    Yu J et al. miR-300 inhibits epithelial to mesenchymal transition and metastasis by targeting Twist in human epithelial cancer. Mol Cancer. 2014;13:121.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Qiang L et al. Regulation of cell proliferation and migration by p62 through stabilization of Twist1. Proc Natl Acad Sci U S A. 2014;111(25):9241–6.PubMedPubMedCentralGoogle Scholar
  9. 9.
    El Ghouzzi V et al. Mutations within or upstream of the basic helix-loop-helix domain of the TWIST gene are specific to Saethre-Chotzen syndrome. Eur J Hum Genet. 1999;7(1):27–33.PubMedGoogle Scholar
  10. 10.
    Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell. 2004;118(3):277–9.PubMedGoogle Scholar
  11. 11.
    Morel AP et al. EMT inducers catalyze malignant transformation of mammary epithelial cells and drive tumorigenesis towards claudin-low tumors in transgenic mice. PLoS Genet. 2012;8(5), e1002723.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Pallier K et al. TWIST1 a new determinant of epithelial to mesenchymal transition in EGFR mutated lung adenocarcinoma. PLoS One. 2012;7(1), e29954.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Pinho AV, Rooman I, Real FX. p53-dependent regulation of growth, epithelial-mesenchymal transition and stemness in normal pancreatic epithelial cells. Cell Cycle. 2011;10(8):1312–21.PubMedGoogle Scholar
  14. 14.
    Thiery JP et al. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871–90.PubMedGoogle Scholar
  15. 15.
    Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008;14(6):818–29.PubMedGoogle Scholar
  16. 16.
    Duan J et al. Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J. 2012;31(2):429–42.PubMedGoogle Scholar
  17. 17.
    Balli D et al. Foxm1 transcription factor is required for lung fibrosis and epithelial-to-mesenchymal transition. EMBO J. 2013;32(2):231–44.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Bednarz-Knoll N, Alix-Panabieres C, Pantel K. Plasticity of disseminating cancer cells in patients with epithelial malignancies. Cancer Metastasis Rev. 2012;31(3-4):673–87.PubMedGoogle Scholar
  19. 19.
    Chao Y et al. Partial mesenchymal to epithelial reverting transition in breast and prostate cancer metastases. Cancer Microenviron. 2012;5(1):19–28.PubMedGoogle Scholar
  20. 20.
    Schwitalla S et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell. 2013;152(1-2):25–38.PubMedGoogle Scholar
  21. 21.
    Tsai JH et al. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 2012;22(6):725–36.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med. 2013;19(11):1438–49.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Taube JH et al. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A. 2010;107(35):15449–54.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Gradilone A et al. Circulating tumour cells lacking cytokeratin in breast cancer: the importance of being mesenchymal. J Cell Mol Med. 2011;15(5):1066–70.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Ledford H. Cancer theory faces doubts. Nature. 2011;472(7343):273.PubMedGoogle Scholar
  26. 26.
    Yu M et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339(6119):580–4.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Brabletz T et al. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci U S A. 2001;98(18):10356–61.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Ocana OH et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell. 2012;22(6):709–24.PubMedGoogle Scholar
  29. 29.
    Celia-Terrassa T et al. Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J Clin Invest. 2012;122(5):1849–68.PubMedPubMedCentralGoogle Scholar
  30. 30.
    De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer. 2013;13(2):97–110.PubMedGoogle Scholar
  31. 31.
    Puisieux A, Brabletz T, Caramel J. Oncogenic roles of EMT-inducing transcription factors. Nat Cell Biol. 2014;16(6):488–94.PubMedGoogle Scholar
  32. 32.
    Sun T et al. Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry. Hepatology. 2010;51(2):545–56.PubMedGoogle Scholar
  33. 33.
    Eckert MA et al. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell. 2011;19(3):372–86.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Renard I et al. Identification and validation of the methylated TWIST1 and NID2 genes through real-time methylation-specific polymerase chain reaction assays for the noninvasive detection of primary bladder cancer in urine samples. Eur Urol. 2010;58(1):96–104.PubMedGoogle Scholar
  35. 35.
    Mehrotra J et al. Very high frequency of hypermethylated genes in breast cancer metastasis to the bone, brain, and lung. Clin Cancer Res. 2004;10(9):3104–9.PubMedGoogle Scholar
  36. 36.
    Yang MH et al. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol. 2010;12(10):982–92.PubMedGoogle Scholar
  37. 37.
    Nieto MA. Epithelial plasticity: a common theme in embryonic and cancer cells. Science. 2013;342(6159):1234850.PubMedGoogle Scholar
  38. 38.
    Nairismagi ML et al. The proto-oncogene TWIST1 is regulated by microRNAs. PLoS One. 2013;8(5), e66070.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Li LZ et al. miR-720 inhibits tumor invasion and migration in breast cancer by targeting TWIST1. Carcinogenesis. 2014;35(2):469–78.PubMedGoogle Scholar
  40. 40.
    Hong J et al. Phosphorylation of serine 68 of Twist1 by MAPKs stabilizes Twist1 protein and promotes breast cancer cell invasiveness. Cancer Res. 2011;71(11):3980–90.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1 (HIF-1): implications in metastasis and development. Cell Cycle. 2008;7(14):2090–6.PubMedGoogle Scholar
  42. 42.
    Satoh K et al. Up-regulation of MSX2 enhances the malignant phenotype and is associated with twist 1 expression in human pancreatic cancer cells. Am J Pathol. 2008;172(4):926–39.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Howe LR et al. Twist is up-regulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res. 2003;63(8):1906–13.PubMedGoogle Scholar
  44. 44.
    Cheng GZ et al. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem. 2008;283(21):14665–73.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Hsu KW et al. Activation of the Notch1/STAT3/Twist signaling axis promotes gastric cancer progression. Carcinogenesis. 2012;33(8):1459–67.PubMedGoogle Scholar
  46. 46.
    Mani SA et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704–15.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Vesuna F et al. Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia. 2009;11(12):1318–28.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Xu Y et al. SRC-1 and Twist1 expression positively correlates with a poor prognosis in human breast cancer. Int J Biol Sci. 2014;10(4):396–403.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Ai L et al. TRIM29 suppresses TWIST1 and invasive breast cancer behavior. Cancer Res. 2014;74(17):4875–87.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Yang J et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927–39.PubMedGoogle Scholar
  51. 51.
    Watson MA et al. Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients. Clin Cancer Res. 2007;13(17):5001–9.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Papadaki MA et al. Co-expression of putative stemness and epithelial-to-mesenchymal transition markers on single circulating tumour cells from patients with early and metastatic breast cancer. BMC Cancer. 2014;14:651.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Kallergi G et al. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res. 2011;13(3):R59.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Li QQ et al. Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clin Cancer Res. 2009;15(8):2657–65.PubMedGoogle Scholar
  55. 55.
    Shen J et al. Simultaneous inhibition of metastasis and growth of breast cancer by co-delivery of twist shRNA and paclitaxel using pluronic P85-PEI/TPGS complex nanoparticles. Biomaterials. 2013;34(5):1581–90.PubMedGoogle Scholar
  56. 56.
    Xue G et al. Akt/PKB-mediated phosphorylation of Twist1 promotes tumor metastasis via mediating cross-talk between PI3K/Akt and TGF-beta signaling axes. Cancer Discov. 2012;2(3):248–59.PubMedGoogle Scholar
  57. 57.
    Banerjee A et al. ARTEMIN synergizes with TWIST1 to promote metastasis and poor survival outcome in patients with ER negative mammary carcinoma. Breast Cancer Res. 2011;13(6):R112.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Haga CL, Phinney DG. MicroRNAs in the imprinted DLK1-DIO3 region repress the epithelial-to-mesenchymal transition by targeting the TWIST1 protein signaling network. J Biol Chem. 2012;287(51):42695–707.PubMedPubMedCentralGoogle Scholar
  59. 59.
    Zhang H et al. MiR-7, inhibited indirectly by lincRNA HOTAIR, directly inhibits SETDB1 and reverses the EMT of breast cancer stem cells by downregulating the STAT3 pathway. Stem Cells. 2014;32(11):2858–68.PubMedGoogle Scholar
  60. 60.
    Chen D et al. miR-100 induces epithelial-mesenchymal transition but suppresses tumorigenesis, migration and invasion. PLoS Genet. 2014;10(2):e1004177.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Lin Y et al. MicroRNA-33b inhibits breast cancer metastasis by targeting HMGA2, SALL4 and Twist1. Sci Rep. 2015;5:9995.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Nairismagi ML et al. Translational control of TWIST1 expression in MCF-10A cell lines recapitulating breast cancer progression. Oncogene. 2012;31(47):4960–6.PubMedGoogle Scholar
  63. 63.
    Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449(7163):682–8.PubMedGoogle Scholar
  64. 64.
    Li CW et al. Epithelial-mesenchymal transition induced by TNF-alpha requires NF-kappaB-mediated transcriptional upregulation of Twist1. Cancer Res. 2012;72(5):1290–300.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Sullivan NJ et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene. 2009;28(33):2940–7.PubMedGoogle Scholar
  66. 66.
    Li S et al. TWIST1 associates with NF-kappaB subunit RELA via carboxyl-terminal WR domain to promote cell autonomous invasion through IL8 production. BMC Biol. 2012;10:73.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Low-Marchelli JM et al. Twist1 induces CCL2 and recruits macrophages to promote angiogenesis. Cancer Res. 2013;73(2):662–71.PubMedPubMedCentralGoogle Scholar
  68. 68.
    D’Angelo RC et al. TIMP-1 via TWIST1 induces EMT phenotypes in human breast epithelial cells. Mol Cancer Res. 2014;12(9):1324–33.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Yin X et al. ATF3, an adaptive-response gene, enhances TGF{beta} signaling and cancer-initiating cell features in breast cancer cells. J Cell Sci. 2010;123(Pt 20):3558–65.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Liang Y et al. Epigenetic activation of TWIST1 by MTDH promotes cancer stem-like cell traits in breast cancer. Cancer Res. 2015;75(17):3672–80.PubMedGoogle Scholar
  71. 71.
    Shi J et al. Disrupting the interaction of BRD4 with diacetylated Twist suppresses tumorigenesis in basal-like breast cancer. Cancer Cell. 2014;25(2):210–25.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Yang F et al. SET8 promotes epithelial-mesenchymal transition and confers TWIST dual transcriptional activities. EMBO J. 2012;31(1):110–23.PubMedGoogle Scholar
  73. 73.
    Kwok WK et al. Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res. 2005;65(12):5153–62.PubMedGoogle Scholar
  74. 74.
    Gajula RP et al. The twist box domain is required for Twist1-induced prostate cancer metastasis. Mol Cancer Res. 2013;11(11):1387–400.PubMedGoogle Scholar
  75. 75.
    Cho KH et al. STAT3 mediates TGF-beta1-induced TWIST1 expression and prostate cancer invasion. Cancer Lett. 2013;336(1):167–73.PubMedGoogle Scholar
  76. 76.
    Cho KH et al. A ROS/STAT3/HIF-1alpha signaling cascade mediates EGF-induced TWIST1 expression and prostate cancer cell invasion. Prostate. 2014;74(5):528–36.PubMedGoogle Scholar
  77. 77.
    Shiota M et al. Clusterin mediates TGF-beta-induced epithelial-mesenchymal transition and metastasis via Twist1 in prostate cancer cells. Cancer Res. 2012;72(20):5261–72.PubMedGoogle Scholar
  78. 78.
    van den Hoogen C et al. Integrin alphav expression is required for the acquisition of a metastatic stem/progenitor cell phenotype in human prostate cancer. Am J Pathol. 2011;179(5):2559–68.PubMedPubMedCentralGoogle Scholar
  79. 79.
    van der Horst G et al. Targeting of alpha(v)-integrins in stem/progenitor cells and supportive microenvironment impairs bone metastasis in human prostate cancer. Neoplasia. 2011;13(6):516–25.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Alexander NR et al. N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res. 2006;66(7):3365–9.PubMedGoogle Scholar
  81. 81.
    Ezponda T et al. The histone methyltransferase MMSET/WHSC1 activates TWIST1 to promote an epithelial-mesenchymal transition and invasive properties of prostate cancer. Oncogene. 2013;32(23):2882–90.PubMedGoogle Scholar
  82. 82.
    Kogan-Sakin I et al. Mutant p53(R175H) upregulates Twist1 expression and promotes epithelial-mesenchymal transition in immortalized prostate cells. Cell Death Differ. 2011;18(2):271–81.PubMedGoogle Scholar
  83. 83.
    Kwok WK et al. Role of p14ARF in TWIST-mediated senescence in prostate epithelial cells. Carcinogenesis. 2007;28(12):2467–75.PubMedGoogle Scholar
  84. 84.
    Ru P et al. miRNA-29b suppresses prostate cancer metastasis by regulating epithelial-mesenchymal transition signaling. Mol Cancer Ther. 2012;11(5):1166–73.PubMedGoogle Scholar
  85. 85.
    Shiota M et al. Castration resistance of prostate cancer cells caused by castration-induced oxidative stress through Twist1 and androgen receptor overexpression. Oncogene. 2010;29(2):237–50.PubMedGoogle Scholar
  86. 86.
    Dey P et al. Estrogen receptors beta1 and beta2 have opposing roles in regulating proliferation and bone metastasis genes in the prostate cancer cell line PC3. Mol Endocrinol. 2012;26(12):1991–2003.PubMedPubMedCentralGoogle Scholar
  87. 87.
    Ju X et al. Identification of a cyclin D1 network in prostate cancer that antagonizes epithelial-mesenchymal restraint. Cancer Res. 2014;74(2):508–19.PubMedGoogle Scholar
  88. 88.
    Yuen HF et al. TWIST modulates prostate cancer cell-mediated bone cell activity and is upregulated by osteogenic induction. Carcinogenesis. 2008;29(8):1509–18.PubMedGoogle Scholar
  89. 89.
    Ardiani A et al. Combination therapy with a second-generation androgen receptor antagonist and a metastasis vaccine improves survival in a spontaneous prostate cancer model. Clin Cancer Res. 2013;19(22):6205–18.PubMedGoogle Scholar
  90. 90.
    Yang MH et al. Comprehensive analysis of the independent effect of twist and snail in promoting metastasis of hepatocellular carcinoma. Hepatology. 2009;50(5):1464–74.PubMedGoogle Scholar
  91. 91.
    Li YM et al. Epithelial-mesenchymal transition markers expressed in circulating tumor cells in hepatocellular carcinoma patients with different stages of disease. Cell Death Dis. 2013;4, e831.PubMedPubMedCentralGoogle Scholar
  92. 92.
    Okabe H et al. CD44s signals the acquisition of the mesenchymal phenotype required for anchorage-independent cell survival in hepatocellular carcinoma. Br J Cancer. 2014;110(4):958–66.PubMedGoogle Scholar
  93. 93.
    Na DC et al. Invasion and EMT-associated genes are up-regulated in B viral hepatocellular carcinoma with high expression of CD133-human and cell culture study. Exp Mol Pathol. 2011;90(1):66–73.PubMedGoogle Scholar
  94. 94.
    Liu AY et al. Twist2 promotes self-renewal of liver cancer stem-like cells by regulating CD24. Carcinogenesis. 2014;35(3):537–45.PubMedGoogle Scholar
  95. 95.
    Sun T et al. Promotion of tumor cell metastasis and vasculogenic mimicry by way of transcription coactivation by Bcl-2 and Twist1: a study of hepatocellular carcinoma. Hepatology. 2011;54(5):1690–706.PubMedGoogle Scholar
  96. 96.
    Zhao N et al. Changes in microRNAs associated with Twist-1 and Bcl-2 overexpression identify signaling pathways. Exp Mol Pathol. 2015;99(3):524–32.PubMedGoogle Scholar
  97. 97.
    Chang TM, Hung WC. Transcriptional repression of TWIST1 gene by Prospero-related homeobox 1 inhibits invasiveness of hepatocellular carcinoma cells. FEBS Lett. 2012;586(20):3746–52.PubMedGoogle Scholar
  98. 98.
    Chang TM, Hung WC. The homeobox transcription factor Prox1 inhibits proliferation of hepatocellular carcinoma cells by inducing p53-dependent senescence-like phenotype. Cancer Biol Ther. 2013;14(3):222–9.PubMedPubMedCentralGoogle Scholar
  99. 99.
    Wang YP et al. Lipocalin-2 negatively modulates the epithelial-to-mesenchymal transition in hepatocellular carcinoma through the epidermal growth factor (TGF-beta1)/Lcn2/Twist1 pathway. Hepatology. 2013;58(4):1349–61.PubMedGoogle Scholar
  100. 100.
    Fu J et al. p28GANK overexpression accelerates hepatocellular carcinoma invasiveness and metastasis via phosphoinositol 3-kinase/AKT/hypoxia-inducible factor-1alpha pathways. Hepatology. 2011;53(1):181–92.PubMedGoogle Scholar
  101. 101.
    Tan EJ et al. Regulation of transcription factor Twist expression by the DNA architectural protein high mobility group A2 during epithelial-to-mesenchymal transition. J Biol Chem. 2012;287(10):7134–45.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Wang D et al. SOX5 promotes epithelial-mesenchymal transition and cell invasion via regulation of Twist1 in hepatocellular carcinoma. Med Oncol. 2015;32(2):461.PubMedGoogle Scholar
  103. 103.
    Huang W et al. Sox12, a direct target of FoxQ1, promotes hepatocellular carcinoma metastasis through up-regulating Twist1 and FGFBP1. Hepatology. 2015;61(6):1920–33.PubMedGoogle Scholar
  104. 104.
    Zhao XL et al. Promotion of hepatocellular carcinoma metastasis through matrix metalloproteinase activation by epithelial-mesenchymal transition regulator Twist1. J Cell Mol Med. 2011;15(3):691–700.PubMedGoogle Scholar
  105. 105.
    Meng F et al. Functional analysis of microRNAs in human hepatocellular cancer stem cells. J Cell Mol Med. 2012;16(1):160–73.PubMedGoogle Scholar
  106. 106.
    Yan-Qi Z et al. Expression and significance of TWIST basic helix-loop-helix protein over-expression in gastric cancer. Pathology. 2007;39(5):470–5.PubMedGoogle Scholar
  107. 107.
    Feng MY et al. Metastasis-induction and apoptosis-protection by TWIST in gastric cancer cells. Clin Exp Metastasis. 2009;26(8):1013–23.PubMedGoogle Scholar
  108. 108.
    Sung CO et al. Twist1 is up-regulated in gastric cancer-associated fibroblasts with poor clinical outcomes. Am J Pathol. 2011;179(4):1827–38.PubMedPubMedCentralGoogle Scholar
  109. 109.
    Zheng HX et al. Fas signaling promotes motility and metastasis through epithelial-mesenchymal transition in gastrointestinal cancer. Oncogene. 2013;32(9):1183–92.PubMedGoogle Scholar
  110. 110.
    Cho SJ et al. Peroxisome proliferator-activated receptor gamma upregulates galectin-9 and predicts prognosis in intestinal-type gastric cancer. Int J Cancer. 2014;136(4):810–20.PubMedGoogle Scholar
  111. 111.
    Toubal A et al. SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation. J Clin Invest. 2013;123(1):362–79.PubMedGoogle Scholar
  112. 112.
    Zha L et al. HMGA2 elicits EMT by activating the Wnt/beta-catenin pathway in gastric cancer. Dig Dis Sci. 2013;58(3):724–33.PubMedGoogle Scholar
  113. 113.
    Zheng Q et al. Trefoil factor 3 peptide regulates migration via a Twist-dependent pathway in gastric cell. Biochem Biophys Res Commun. 2013;438(1):6–12.PubMedGoogle Scholar
  114. 114.
    Feng MY et al. Gene expression profiling in TWIST-depleted gastric cancer cells. Anat Rec (Hoboken). 2009;292(2):262–70.Google Scholar
  115. 115.
    Qian J et al. Twist1 promotes gastric cancer cell proliferation through up-regulation of FoxM1. PLoS One. 2013;8(10), e77625.PubMedPubMedCentralGoogle Scholar
  116. 116.
    Luo GQ et al. Activator protein-1 involvement in proliferation inhibition by gene silencing of Twist in gastric cancer cells. Pathology. 2011;43(7):697–701.PubMedGoogle Scholar
  117. 117.
    Li X et al. miRNA-223 promotes gastric cancer invasion and metastasis by targeting tumor suppressor EPB41L3. Mol Cancer Res. 2011;9(7):824–33.PubMedGoogle Scholar
  118. 118.
    Liu Z et al. miR-10b promotes cell invasion through RhoC-AKT signaling pathway by targeting HOXD10 in gastric cancer. Int J Oncol. 2012;40(5):1553–60.PubMedGoogle Scholar
  119. 119.
    <Twist1-mediated 4E-BP1 re [PMIDY26360779].pdf>.Google Scholar
  120. 120.
    Hung JJ et al. Prognostic significance of hypoxia-inducible factor-1alpha, TWIST1 and Snail expression in resectable non-small cell lung cancer. Thorax. 2009;64(12):1082–9.PubMedGoogle Scholar
  121. 121.
    Merikallio H et al. Zeb1 and twist are more commonly expressed in metastatic than primary lung tumours and show inverse associations with claudins. J Clin Pathol. 2011;64(2):136–40.PubMedGoogle Scholar
  122. 122.
    Tran PT et al. Twist1 suppresses senescence programs and thereby accelerates and maintains mutant Kras-induced lung tumorigenesis. PLoS Genet. 2012;8(5), e1002650.PubMedPubMedCentralGoogle Scholar
  123. 123.
    Jin HO et al. Silencing of Twist1 sensitizes NSCLC cells to cisplatin via AMPK-activated mTOR inhibition. Cell Death Dis. 2012;3, e319.PubMedPubMedCentralGoogle Scholar
  124. 124.
    Azuma K et al. FGFR1 activation is an escape mechanism in human lung cancer cells resistant to afatinib, a pan-EGFR family kinase inhibitor. Oncotarget. 2014;5(15):5908–19.PubMedPubMedCentralGoogle Scholar
  125. 125.
    Yoshimatsu M et al. Dysregulation of PRMT1 and PRMT6, type I arginine methyltransferases, is involved in various types of human cancers. Int J Cancer. 2011;128(3):562–73.PubMedGoogle Scholar
  126. 126.
    Avasarala S et al. PRMT1 is a novel regulator of epithelial-mesenchymal-transition in non-small cell lung cancer. J Biol Chem. 2015;290(21):13479–89.PubMedPubMedCentralGoogle Scholar
  127. 127.
    Smith PW et al. Breast cancer metastasis suppressor 1 (BRMS1) suppresses metastasis and correlates with improved patient survival in non-small cell lung cancer. Cancer Lett. 2009;276(2):196–203.PubMedGoogle Scholar
  128. 128.
    Liu Y et al. Loss of BRMS1 promotes a mesenchymal phenotype through NF-kappaB-dependent regulation of Twist1. Mol Cell Biol. 2015;35(1):303–17.PubMedGoogle Scholar
  129. 129.
    Pino I et al. Altered patterns of expression of members of the heterogeneous nuclear ribonucleoprotein (hnRNP) family in lung cancer. Lung Cancer. 2003;41(2):131–43.PubMedGoogle Scholar
  130. 130.
    Tauler J et al. hnRNP A2/B1 modulates epithelial-mesenchymal transition in lung cancer cell lines. Cancer Res. 2010;70(18):7137–47.PubMedGoogle Scholar
  131. 131.
    Yang L et al. MircoRNA-33a inhibits epithelial-to-mesenchymal transition and metastasis and could be a prognostic marker in non-small cell lung cancer. Sci Rep. 2015;5:13677.PubMedPubMedCentralGoogle Scholar
  132. 132.
    Pirozzi G et al. Epithelial to mesenchymal transition by TGFbeta-1 induction increases stemness characteristics in primary non small cell lung cancer cell line. PLoS One. 2011;6(6), e21548.PubMedPubMedCentralGoogle Scholar
  133. 133.
    Kumar M et al. NF-kappaB regulates mesenchymal transition for the induction of non-small cell lung cancer initiating cells. PLoS One. 2013;8(7), e68597.PubMedPubMedCentralGoogle Scholar
  134. 134.
    Zhuo WL et al. Short interfering RNA directed against TWIST, a novel zinc finger transcription factor, increases A549 cell sensitivity to cisplatin via MAPK/mitochondrial pathway. Biochem Biophys Res Commun. 2008;369(4):1098–102.PubMedGoogle Scholar
  135. 135.
    Wang X et al. Identification of a novel function of TWIST, a bHLH protein, in the development of acquired taxol resistance in human cancer cells. Oncogene. 2004;23(2):474–82.PubMedGoogle Scholar
  136. 136.
    Pham CG et al. Upregulation of Twist-1 by NF-kappaB blocks cytotoxicity induced by chemotherapeutic drugs. Mol Cell Biol. 2007;27(11):3920–35.PubMedPubMedCentralGoogle Scholar
  137. 137.
    Li QQ et al. Involvement of NF-kappaB/miR-448 regulatory feedback loop in chemotherapy-induced epithelial-mesenchymal transition of breast cancer cells. Cell Death Differ. 2011;18(1):16–25.PubMedGoogle Scholar
  138. 138.
    Shiota M et al. Interaction between docetaxel resistance and castration resistance in prostate cancer: implications of Twist1, YB-1, and androgen receptor. Prostate. 2013;73(12):1336–44.PubMedGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2015

Authors and Affiliations

  1. 1.Department of Respiratory MedicineJinling Hospital, Medical School of Nanjing UniversityNanjingChina
  2. 2.Department of Respiratory MedicineJiangsu Province Hospital of Chinese Medicine, Affiliated Hospital of Nanjing University of Chinese MedicineNanjingChina

Personalised recommendations