TWIST1 and TWIST2 promoter methylation and protein expression in tumor stroma influence the epithelial-mesenchymal transition-like tumor budding phenotype in colorectal cancer

Oncotarget

Volumn 6, Issue 2, 2015, Pages 874-885

  Galván, José A ^a   Helbling, Melina ^a   Koelzer, Viktor H ^a   Tschan, Mario P ^a   Berger, Martin D ^b   Hädrich, Marion ^b   Schnüriger, Beat ^b   Karamitopoulou, Eva ^a   Dawson, Heather ^a   Inderbitzin, Daniel ^b,c   Lugli, Alessandro ^a   Zlobec, Inti ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c Spital Bern Tiefenau   (Switzerland)

Author keywords

Budding; Methylation; Pyrosequencing; Tumor microenvironment; Twist

Indexed keywords

TRANSCRIPTION FACTOR TWIST; TWIST1 PROTEIN; TWIST2 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; BETA CATENIN; CADHERIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; TWIST1 PROTEIN, HUMAN; TWIST2 PROTEIN, HUMAN; ZEB1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL LINE; CANCER GRADING; CANCER PROGNOSIS; COHORT ANALYSIS; COLORECTAL CANCER; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LASER CAPTURE MICRODISSECTION; LYMPH NODE METASTASIS; LYMPH VESSEL METASTASIS; MAJOR CLINICAL STUDY; MALE; ONCOGENESIS AND MALIGNANT TRANSFORMATION; PERINEURAL INVASION; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; STROMA CELL; SURVIVAL TIME; TUMOR BUDDING; TUMOR INVASION; UPREGULATION; ADULT; AGED; COLORECTAL TUMOR; DNA SEQUENCE; GENETICS; HCT116 CELL LINE; HT 29 CELL LINE; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOLOGY; PROCEDURES; PROGNOSIS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BETA CATENIN; CADHERINS; COHORT STUDIES; COLORECTAL NEOPLASMS; DNA METHYLATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HCT116 CELLS; HOMEODOMAIN PROTEINS; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NUCLEAR PROTEINS; PROGNOSIS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; STROMAL CELLS; TRANSCRIPTION FACTORS; TWIST TRANSCRIPTION FACTOR;

EID: 84921825783     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2716     Document Type: Article

References (40)

1. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002; 2:442-454.
2. Perez-Moreno M, Jamora C, Fuchs E. Sticky business: orchestrating cellular signals at adherens junctions. Cell. 2003; 112:535-548.
3. Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 2009; 28:151-166.
4. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D, van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell. 2001; 7:1267-1278.
5. Risinger JI, Berchuck A, Kohler MF, Boyd J. Mutations of the E-cadherin gene in human gynecologic cancers. Nat Genet. 1994; 7:98-102.
6. Singh AB, Sharma A, Smith JJ, Krishnan M, Chen X, Eschrich S, Washington MK, Yeatman TJ, Beauchamp RD, Dhawan P. Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology. 2011; 141:2140-2153.
7. Wheeler JM, Kim HC, Efstathiou JA, Ilyas M, Mortensen NJ, Bodmer WF. Hypermethylation of the promoter region of the E-cadherin gene (CDH1) in sporadic and ulcerative colitis associated colorectal cancer. Gut. 2001; 48:367-371.
8. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004; 117:927-939.
9. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2000; 2:84-89.
10. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci. 2003; 116:499-511.
11. Celesti G, Di Caro G, Bianchi P, Grizzi F, Basso G, Marchesi F, Doni A, Marra G, Roncalli M, Mantovani A, et al. Presence of Twist1-positive neoplastic cells in the stroma of chromosome-unstable colorectal tumors. Gastroenterology. 2013; 145:647-657e615.
12. Hur K, Toiyama Y, Takahashi M, Balaguer F, Nagasaka T, Koike J, Hemmi H, Koi M, Boland CR, Goel A. MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut. 2013; 62:1315-1326.
13. Jass JR, Barker M, Fraser L, Walsh MD, Whitehall VL, Gabrielli B, Young J, Leggett BA. APC mutation and tumour budding in colorectal cancer. J Clin Pathol. 2003; 56:69-73.
14. Karamitopoulou E, Zlobec I, Kolzer V, Kondi-Pafiti A, Patsouris ES, Gennatas K, Lugli A. Proposal for a 10-high-power-fields scoring method for the assessment of tumor budding in colorectal cancer. Mod Pathol. 2013; 26:295-301.
15. Zlobec I, Lugli A. Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: tumor budding as oncotarget. Oncotarget. 2010; 1:651-661.
16. Nakamura T, Mitomi H, Kikuchi S, Ohtani Y, Sato K. Evaluation of the usefulness of tumor budding on the prediction of metastasis to the lung and liver after curative excision of colorectal cancer. Hepatogastroenterology. 2005; 52:1432-1435.
17. Ueno H, Mochizuki H, Hashiguchi Y, Hatsuse K, Fujimoto H, Hase K. Predictors of extrahepatic recurrence after resection of colorectal liver metastases. Br J Surg. 2004; 91:327-333.
18. Ueno H, Murphy J, Jass JR, Mochizuki H, Talbot IC. Tumour 'budding' as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology. 2002; 40:127-132.
19. Wang HS, Liang WY, Lin TC, Chen WS, Jiang JK, Yang SH, Chang SC, Lin JK. Curative resection of T1 colorectal carcinoma: risk of lymph node metastasis and long-term prognosis. Dis Colon Rectum. 2005; 48:1182-1192.
20. Wang LM, Kevans D, Mulcahy H, O'Sullivan J, Fennelly D, Hyland J, O'Donoghue D, Sheahan K. Tumor budding is a strong and reproducible prognostic marker in T3N0 colorectal cancer. Am J Surg Pathol. 2009; 33:134-141.
21. Pino MS, Chung DC. The chromosomal instability pathway in colon cancer. Gastroenterology. 2010; 138:2059-2072.
22. Brabletz T, Spaderna S, Kolb J, Hlubek F, Faller G, Bruns CJ, Jung A, Nentwich J, Duluc I, Domon-Dell C, et al. Down-regulation of the homeodomain factor Cdx2 in colorectal cancer by collagen type I: an active role for the tumor environment in malignant tumor progression. Cancer Res. 2004; 64:6973-6977.
23. Gomez I, Pena C, Herrera M, Munoz C, Larriba MJ, Garcia V, Dominguez G, Silva J, Rodriguez R, Garcia de Herreros A, et al. TWIST1 is expressed in colorectal carcinomas and predicts patient survival. PLoS One. 2011; 6:e18023.
24. Kim YH, Kim G, Kwon CI, Kim JW, Park PW, Hahm KB. TWIST1 and SNAI1 as markers of poor prognosis in human colorectal cancer are associated with the expression of ALDH1 and TGF-beta1. Oncol Rep. 2014; 31:1380-1388.
25. Okada T, Suehiro Y, Ueno K, Mitomori S, Kaneko S, Nishioka M, Okayama N, Sakai K, Higaki S, Hazama S, et al. TWIST1 hypermethylation is observed frequently in colorectal tumors and its overexpression is associated with unfavorable outcomes in patients with colorectal cancer. Genes Chromosomes Cancer. 2010; 49:452-462.
26. Padin-Iruegas ME, Herranz-Carnero M, Aguin-Losada S, Brozos-Vazquez E, Anido-Herranz U, Antunez-Lopez JR, Ruibal-Morell A, Lopez-Lopez R. Prognostic value of changes in the expression of stem cell markers in the peripheral blood of patients with colon cancer. Oncol Rep. 2013; 29:2467-2472.
27. Ishikawa T, Shimizu T, Ueki A, Yamaguchi SI, Onishi N, Sugihara E, Kuninaka S, Miyamoto T, Morioka H, Nakayama R, et al. Twist2 functions as a tumor suppressor in murine osteosarcoma cells. Cancer Sci. 2013; 104: 880-888.
28. Yu H, Jin GZ, Liu K, Dong H, Duan JC, Li Z, Dong W, Cong WM, Yang JH. Twist2 is a valuable prognostic biomarker for colorectal cancer. World J Gastroenterol. 2013; 19:2404-2411.
29. Wang T, Li Y, Wang W, Tuerhanjiang A, Wu Z, Yang R, Yuan M, Ma D, Wang S. Twist2, the key Twist isoform related to prognosis, promotes invasion of cervical cancer by inducing epithelial-mesenchymal transition and blocking senescence. Hum Pathol. 2014; 45:1839-46.
30. Mao Y, Xu J, Li Z, Zhang N, Yin H, Liu Z. The role of nuclear beta-catenin accumulation in the Twist2-induced ovarian cancer EMT. PLoS One. 2013; 8:e78200.
31. Ashktorab H, Rahi H, Wansley D, Varma S, Shokrani B, Lee E, Daremipouran M, Laiyemo A, Goel A, Carethers JM, et al. Toward a comprehensive and systematic methylome signature in colorectal cancers. Epigenetics. 2013; 8:807-815.
32. Oster B, Thorsen K, Lamy P, Wojdacz TK, Hansen LL, Birkenkamp-Demtroder K, Sorensen KD, Laurberg S, Orntoft TF, Andersen CL. Identification and validation of highly frequent CpG island hypermethylation in colorectal adenomas and carcinomas. Int J Cancer. 2011; 129:2855-2866.
33. Ruppenthal RD, Nicolini C, Filho AF, Meurer R, Damin AP, Rohe A, Alexandre CO, Damin DC. TWIST1 promoter methylation in primary colorectal carcinoma. Pathol Oncol Res. 2011; 17:867-872.
34. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M, Xu LM, Costanzo C, Cheng JQ, Wang LH. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem. 2008; 283:14665-14673.
35. Sosic D, Olson EN. A new twist on twist-modulation of the NF-kappa B pathway. Cell Cycle. 2003; 2:76-78.
36. Sun S, Ning X, Zhang Y, Lu Y, Nie Y, Han S, Liu L, Du R, Xia L, He L, et al. Hypoxia-inducible factor-1alpha induces Twist expression in tubular epithelial cells subjected to hypoxia, leading to epithelial-to-mesenchymal transition. Kidney Int. 2009; 75:1278-1287.
37. Moreno-Bueno G, Peinado H, Molina P, Olmeda D, Cubillo E, Santos V, Palacios J, Portillo F, Cano A. The morphological and molecular features of the epithelial-to-mesenchymal transition. Nat Protoc. 2009; 4:1591-1613.
38. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene. 2005; 24:5764-5774.
39. Dong P, Kaneuchi M, Watari H, Sudo S, Sakuragi N. MicroRNA-106b modulates epithelial-mesenchymal transition by targeting TWIST1 in invasive endometrial cancer cell lines. Mol Carcin. 2014; 53:349-359.
40. Zlobec I, Koelzer VH, Dawson H, Perren A, Lugli A. Next-generation tissue microarray (ngTMA) increases the quality of biomarker studies: an example using CD3, CD8, and CD45RO in the tumor microenvironment of six different solid tumor types. J Transl Med. 2013; 11:104.