Hypoxia induces epithelial-mesenchymal transition in follicular thyroid cancer: Involvement of regulation of twist by hypoxia inducible factor-1α

Yonsei Medical Journal

Volumn 56, Issue 6, 2015, Pages 1503-1514

  Yang, Yeon Ju ^a   Na, Hwi Jung ^a   Suh, Michelle J ^a   Ban, Myung Jin ^a   Byeon, Hyung Kwon ^a   Kim, Won Shik ^a   Kim, Jae Wook ^b   Choi, Eun Chang ^a   Kwon, Hyeong Ju ^a   Chang, Jae Won ^a   Koh, Yoon Woo ^a  

^a Yonsei University College of Medicine   (South Korea)

^b Soonchunhyang University College of Medicine   (South Korea)

Author keywords

Epithelial mesenchymal transition; Follicular thyroid cancer; Hypoxia; Hypoxia inducible factor 1 ; Orthotopic thyroid cancer model; Twist

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; CADHERIN; LYMPHOKINE; TUMOR MIGRATION INHIBITION FACTOR; TWIST RELATED PROTEIN 1; VIMENTIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; THYROID CANCER; TISSUE MICROARRAY; WESTERN BLOTTING; WOUND HEALING; ADENOCARCINOMA; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; THYROID TUMOR; TRANSCRIPTION INITIATION; TUMOR INVASION;

ADENOCARCINOMA, FOLLICULAR; ANIMALS; CADHERINS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LYMPHOKINES; MICE; NEOPLASM INVASIVENESS; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYROID NEOPLASMS; TRANSCRIPTIONAL ACTIVATION; TWIST-RELATED PROTEIN 1; VIMENTIN;

EID: 84944040597     PISSN: 05135796     EISSN: None     Source Type: Journal    
DOI: 10.3349/ymj.2015.56.6.1503     Document Type: Article

References (48)

1. Phay JE, Ringel MD. Metastatic mechanisms in follicular cell-derived thyroid cancer. Endocr Relat Cancer 2013;20:R307-19
2. Carling T, Udelsman R. Thyroid cancer. Annu Rev Med 2014;65: 125-37
3. Chang JW, Kang SU, Shin YS, Kim KI, Seo SJ, Yang SS, et al. Nonthermal atmospheric pressure plasma inhibits thyroid papillary cancer cell invasion via cytoskeletal modulation, altered MMP- 2/-9/uPA activity. PLoS One 2014;9:e92198
4. Rahmani N, Abbas Hashemi S, Fazli M, Raisian M. Clinical management and outcomes of papillary, follicular and medullary thyroid cancer surgery. Med Glas (Zenica) 2013;10:164-7
5. Zhao JH, Luo Y, Jiang YG, He DL, Wu CT. Knockdown of β-Catenin through shRNA cause a reversal of EMT and metastatic phenotypes induced by HIF-1α. Cancer Invest 2011;29:377-82
6. Xiao W, Jiang M, Li H, Li C, Su R, Huang K. Knockdown of FAK inhibits the invasion and metastasis of Tca8113 cells in vitro. Mol Med Rep 2013;8:703-7
7. Marie-Egyptienne DT, Lohse I, Hill RP. Cancer stem cells, the epithelial to mesenchymal transition (EMT) and radioresistance: potential role of hypoxia. Cancer Lett 2013;341:63-72
8. De Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013;13:97-110
9. Cavallaro U, Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 2004;4:118-32
10. Burrows N, Resch J, Cowen RL, von Wasielewski R, Hoang-Vu C, West CM, et al. Expression of hypoxia-inducible factor 1 alpha in thyroid carcinomas. Endocr Relat Cancer 2010;17:61-72
11. Kim DH, Hossain MA, Kim MY, Kim JA, Yoon JH, Suh HS, et al. A novel resveratrol analogue, HS-1793, inhibits hypoxia-induced HIF- 1α and VEGF expression, and migration in human prostate cancer cells. Int J Oncol 2013;43:1915-24
12. Melstrom LG, Salabat MR, Ding XZ, Strouch MJ, Grippo PJ, Mirzoeva S, et al. Apigenin down-regulates the hypoxia response genes: HIF-1α, GLUT-1, and VEGF in human pancreatic cancer cells. J Surg Res 2011;167:173-81
13. Kockar F, Yildrim H, Sagkan RI, Hagemann C, Soysal Y, Anacker J, et al. Hypoxia and cytokines regulate carbonic anhydrase 9 expression in hepatocellular carcinoma cells in vitro. World J Clin Oncol 2012;3:82-91
14. Sendoel A, Kohler I, Fellmann C, Lowe SW, Hengartner MO. HIF- 1 antagonizes p53-mediated apoptosis through a secreted neuronal tyrosinase. Nature 2010;465:577-83
15. Culver C, Melvin A, Mudie S, Rocha S. HIF-1α depletion results in SP1-mediated cell cycle disruption and alters the cellular response to chemotherapeutic drugs. Cell Cycle 2011;10:1249-60
16. Burrows N, Babur M, Resch J, Williams KJ, Brabant G. Hypoxiainducible factor in thyroid carcinoma. J Thyroid Res 2011;2011: 762905
17. Li H, Liang CZ, Chen QX. Regulatory role of hypoxia inducible factor in the biological behavior of nucleus pulposus cells. Yonsei Med J 2013;54:807-12
18. Semenza GL. HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 2010;20:51-6
19. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32
20. Warfel NA, El-Deiry WS. HIF-1 signaling in drug resistance to chemotherapy. Curr Med Chem 2014;21:3021-8
21. Zerilli M, Zito G, Martorana A, Pitrone M, Cabibi D, Cappello F, et al. BRAF(V600E) mutation influences hypoxia-inducible factor- 1alpha expression levels in papillary thyroid cancer. Mod Pathol 2010;23:1052-60
22. Kim CH, Kwon S, Bahn JH, Lee K, Jun SI, Rack PD, et al. Effects of atmospheric nonthermal plasma on invasion of colorectal cancer cells. Appl Phys Lett 2010;96:243701
23. Chang JW, Kang SU, Choi JW, Shin YS, Baek SJ, Lee SH, et al. Tolfenamic acid induces apoptosis and growth inhibition in anaplastic thyroid cancer: involvement of nonsteroidal anti-inflammatory drug-activated gene-1 expression and intracellular reactive oxygen species generation. Free Radic Biol Med 2014;67:115-30
24. 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;117:927-39
25. Carpenter RL, Paw I, Dewhirst MW, Lo HW. Akt phosphorylates and activates HSF-1 independent of heat shock, leading to Slug overexpression and epithelial-mesenchymal transition (EMT) of HER2- overexpressing breast cancer cells. Oncogene 2015;34:546-57
26. Chen L, Shi Y, Yuan J, Han Y, Qin R, Wu Q, et al. HIF-1 alpha overexpression correlates with poor overall survival and disease-free survival in gastric cancer patients post-gastrectomy. PLoS One 2014;9: e90678
27. Friday BB, Adjei AA. Advances in targeting the Ras/Raf/MEK/Erk mitogen-activated protein kinase cascade with MEK inhibitors for cancer therapy. Clin Cancer Res 2008;14:342-6
28. Vasko V, Ferrand M, Di Cristofaro J, Carayon P, Henry JF, de Micco C. Specific pattern of RAS oncogene mutations in follicular thyroid tumors. J Clin Endocrinol Metab 2003;88:2745-52
29. Nikiforova MN, Lynch RA, Biddinger PW, Alexander EK, Dorn GW 2nd, Tallini G, et al. RAS point mutations and PAX8-PPAR gamma rearrangement in thyroid tumors: evidence for distinct molecular pathways in thyroid follicular carcinoma. J Clin Endocrinol Metab 2003;88:2318-26
30. Burrows N, Babur M, Resch J, Ridsdale S, Mejin M, Rowling EJ, et al. GDC-0941 inhibits metastatic characteristics of thyroid carcinomas by targeting both the phosphoinositide-3 kinase (PI3K) and hypoxia- inducible factor-1α (HIF-1α) pathways. J Clin Endocrinol Metab2011;96:E1934-43
31. Sandrini F, Matyakhina L, Sarlis NJ, Kirschner LS, Farmakidis C, Gimm O, et al. Regulatory subunit type I-alpha of protein kinase A (PRKAR1A): a tumor-suppressor gene for sporadic thyroid cancer. Genes Chromosomes Cancer 2002;35:182-92
32. Jubb AM, Pham TQ, Hanby AM, Frantz GD, Peale FV, Wu TD, et al. Expression of vascular endothelial growth factor, hypoxia inducible factor 1alpha, and carbonic anhydrase IX in human tumours. J Clin Pathol 2004;57:504-12
33. Zundel W, Schindler C, Haas-Kogan D, Koong A, Kaper F, Chen E, et al. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev 2000;14:391-6
34. Maxwell PJ, Coulter J, Walker SM, McKechnie M, Neisen J, McCabe N, et al. Potentiation of inflammatory CXCL8 signalling sustains cell survival in PTEN-deficient prostate carcinoma. Eur Urol 2013;64:177-88
35. Franco-Chuaire ML, Magda Carolina SC, Chuaire-Noack L. Epithelial- mesenchymal transition (EMT): principles and clinical impact in cancer therapy. Invest Clin 2013;54:186-205
36. Gravdal K, Halvorsen OJ, Haukaas SA, Akslen LA. A switch from Ecadherin to N-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin Cancer Res 2007;13:7003-11
37. Fan M, Liu Y, Xia F, Wang Z, Huang Y, Li J, et al. Increased expression of EphA2 and E-N cadherin switch in primary hepatocellular carcinoma. Tumori 2013;99:689-96
38. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, et al. The transcription factor snail controls epithelialmesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000;2:76-83
39. Hajra KM, Chen DY, Fearon ER. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002;62:1613-8
40. Grooteclaes ML, Frisch SM. Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 2000;19:3823-8
41. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001;7:1267-78
42. Perez-Moreno MA, Locascio A, Rodrigo I, Dhondt G, Portillo F, Nieto MA, et al. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J Biol Chem 2001;276:27424-31
43. Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1 (HIF-1): implications in metastasis and development. Cell Cycle 2008;7:2090-6
44. Khan MA, Chen HC, Zhang D, Fu J. Twist: a molecular target in cancer therapeutics. Tumour Biol 2013;34:2497-506
45. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, et al. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 2008;10:295-305
46. Stoletov K, Kato H, Zardouzian E, Kelber J, Yang J, Shattil S, et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci 2010;123(Pt 13):2332-41
47. Eckert MA, Yang J. Targeting invadopodia to block breast cancer metastasis. Oncotarget 2011;2:562-8
48. Hung JJ, Yang MH, Hsu HS, Hsu WH, Liu JS, Wu KJ. Prognostic significance of hypoxia-inducible factor-1alpha, TWIST1 and Snail expression in resectable non-small cell lung cancer. Thorax 2009; 64:1082-9