Molecular profiling of tumour budding implicates TGFβ-mediated epithelial-mesenchymal transition as a therapeutic target in oral squamous cell carcinoma

Journal of Pathology

Volumn 236, Issue 4, 2015, Pages 505-516

  Jensen, D H ^a   Dabelsteen, E ^a   Specht, L ^a   Fiehn, A M K ^a   Therkildsen, M H ^a   Jonson L ^a   Vikesaa, J ^a   Nielsen, F C ^a   Von Buchwald, C ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

epithelial mesenchymal transition; lymph node metastasis; oral squamous cell carcinoma; TGF ; tumour budding

Indexed keywords

KRUPPEL LIKE FACTOR; MICRORNA 200; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PRRX1; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; MICRORNA; TUMOR MARKER;

ADULT; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; MOUTH SQUAMOUS CELL CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; RNA SEQUENCE; TUMOR BUDDING; UPREGULATION; CARCINOMA, SQUAMOUS CELL; DISEASE FREE SURVIVAL; DNA MICROARRAY; DRUG DESIGN; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; HEAD AND NECK NEOPLASMS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MOLECULARLY TARGETED THERAPY; MORTALITY; MOUTH NEOPLASMS; PATHOLOGY; PHENOTYPE; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE; PROCEDURES; REPRODUCIBILITY; RETROSPECTIVE STUDY; SIGNAL TRANSDUCTION; TIME;

ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; DISEASE-FREE SURVIVAL; DRUG DESIGN; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KAPLAN-MEIER ESTIMATE; LASER CAPTURE MICRODISSECTION; LYMPHATIC METASTASIS; MALE; MICRORNAS; MIDDLE AGED; MOLECULAR TARGETED THERAPY; MOUTH NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE OF TESTS; REPRODUCIBILITY OF RESULTS; RETROSPECTIVE STUDIES; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MARKERS, BIOLOGICAL;

EID: 84937412521     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4550     Document Type: Article

References (51)

1. Ross G, Soutar D, Gordon MacDonald D, et al., Sentinel node biopsy in head and neck cancer: preliminary results of a multicenter trial. Ann Surgical Oncol 2004; 11: 690-696.
2. Onken MD, Winkler AE, Kanchi KL, et al., A surprising cross-species conservation in the genomic landscape of mouse and human oral cancer identifies a transcriptional signature predicting metastatic disease. Clin Cancer Res 2014; 20: 2873-2884.
3. Vogelstein B, Papadopoulos N, Velculescu VE, et al., Cancer genome landscapes. Science 2013; 339: 1546-1558.
4. van Hooff SR, Leusink FKJ, Roepman P, et al., Validation of a gene expression signature for assessment of lymph node metastasis in oral squamous cell carcinoma. J Clin Oncol 2012; 30: 4104-4110.
5. Glasgow S, Bleier JS, Burgart L, et al., Meta-analysis of histopathological features of primary colorectal cancers that predict lymph node metastases. J Gastrointest Surg 2012; 16: 1019-1028.
6. Kye BH, Jung JH, Kim HJ, et al., Tumor budding as a risk factor of lymph node metastasis in submucosal invasive T1 colorectal carcinoma: a retrospective study. BMC Surg 2012; 12: 16.
7. Wang C, Huang H, Huang Z, et al., Tumor budding correlates with poor prognosis and epithelial-mesenchymal transition in tongue squamous cell carcinoma. J Oral Pathol Med 2011; 40: 545-551.
8. Brabletz T., To differentiate or not-routes towards metastasis. Nat Rev Cancer 2012; 12: 425-436.
9. Thiery JP,. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002; 2: 442-454.
10. Bronsert P, Enderle-Ammour K, Bader M, et al., Cancer cell invasion and EMT marker expression: a three-dimensional study of the human cancer-host interface. J Pathol 2014; 234: 410-422.
11. Gregory PA, Bert AG, Paterson EL, et al., The MIR-200 family and MIR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
12. Park SM, Gaur AB, Lengyel E, et al., The MIR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008; 22: 894-907.
13. Taube JH, Herschkowitz JI, Komurov K, 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 USA 2010; 107: 15449-15454.
14. Díaz-Martín J, Díaz-Lõpez A, Moreno-Bueno G, et al., A core microRNA signature associated with inducers of the epithelial-to-mesenchymal transition. J Pathol 2014; 232: 319-329.
15. McDonald OG, Maitra A, Hruban RH,. Human correlates of provocative questions in pancreatic pathology. Adv Anat Pathol 2012; 19: 351.
16. Bastid J., EMT in carcinoma progression and dissemination: facts, unanswered questions, and clinical considerations. Cancer Metast Rev 2012; 31: 277-283.
17. Ledford H., Cancer theory faces doubts. Nature 2011; 472: 273-273.
18. Altman DG, McShane LM, Sauerbrei W, et al., Reporting recommendations for tumor marker prognostic studies (REMARK): explanation and elaboration. BMC Med 2012; 10: 51.
19. Moore HM, Kelly AB, Jewell SD, et al., Biospecimen reporting for improved study quality (BRISQ). J Proteome Res 2011; 10: 3429-3438.
20. Robinson MD, McCarthy DJ, Smyth GK,. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26: 139-140.
21. Dvinge H, Bertone P,. HTqPCR: high-throughput analysis and visualization of quantitative real-time PCR data in R. Bioinformatics 2009; 25: 3325-3326.
22. Subramanian A, Tamayo P, Mootha VK, et al., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Academy Sci USA 2005; 102: 15545-15550.
23. Hedbäck N, Jensen DH, Specht L, et al., MiR-21 expression in the tumor stroma of oral squamous cell carcinoma: an independent biomarker of disease free survival. PloS One 2014; 9: e95193.
24. Wang Z, Gerstein M, Snyder M,. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009; 10: 57-63.
25. Presland RB, Dale BA,. Epithelial structural proteins of the skin and oral cavity: function in health and disease. Crit Rev Oral Biol Med 2000; 11: 383-408.
26. Ocaña OH, Cõrcoles R, Fabra Á, et al., Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 2012; 22: 709-724.
27. Burk U, Schubert J, Wellner U, et al., A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008; 9: 582-589.
28. Roca H, Hernandez J, Weidner S, et al., Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer. PloS One 2013; 8: e76773.
29. Li S, Yang J,. Ovol proteins: guardians against EMT during epithelial differentiation. Dev Cell 2014; 29: 1-2.
30. Anastassiou D, Rumjantseva V, Cheng W, et al., Human cancer cells express Slug-based epithelial-mesenchymal transition gene expression signature obtained in vivo. BMC Cancer 2011; 11: 529.
31. Puisieux A, Brabletz T, Caramel J,. Oncogenic roles of EMT-inducing transcription factors. Nat Cell Biol 2014; 16: 488-494.
32. Xie N, Wang C, Liu X, et al., Tumor budding correlates with occult cervical lymph node metastasis and poor prognosis in clinical early-stage tongue squamous cell carcinoma. J Oral Pathol Med 2014; 44: 266-272.
33. De Craene B, Berx G,. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013; 13: 97-110.
34. Pan C, Kumar C, Bohl S, et al., Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteom 2009; 8: 443-450.
35. Gillet J-P, Calcagno AM, Varma S, et al., Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci USA 2011; 108: 18708-18713.
36. Loboda A, Nebozhyn MV, Watters JW, et al., EMT is the dominant program in human colon cancer. BMC Med Genom 2011; 4: 9.
37. Tan TZ, Miow QH, Miki Y, et al., Epithelial-mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer patients. EMBO Mol Med 2014: e201404208.
38. Betge J, Kornprat P, Pollheimer MJ, et al., Tumor budding is an independent predictor of outcome in AJCC/UICC stage II colorectal cancer. Ann Surg Oncol 2012; 19: 3706-3712.
39. Rogers AC, Gibbons D, Hanly AM, et al., Prognostic significance of tumor budding in rectal cancer biopsies before neoadjuvant therapy. Mod Pathol 2014; 27: 156-162.
40. Khalil N., TGFβ: from latent to active. Microbes Infect 1999; 1: 1255-1263.
41. Seliger C, Leukel P, Moeckel S, et al., Lactate-modulated induction of THBS-1 activates transforming growth factor (TGF)-β2 and migration of glioma cells in vitro. PloS One 2013; 8: e78935.
42. Liborio TN, Acquafreda T, Matizonkas-Antonio LF, et al., In situ hybridization detection of homeobox genes reveals distinct expression patterns in oral squamous cell carcinomas. Histopathology 2011; 58: 225-233.
43. Giampieri S, Manning C, Hooper S, et al., Localized and reversible TGFβ signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009; 11: 1287-1296.
44. Matise LA, Palmer TD, Ashby WJ, et al., Lack of transforming growth factor-β signaling promotes collective cancer cell invasion through tumor-stromal crosstalk. Breast Cancer Res 2012; 14: R98.
45. Weston BS, Wahab NA, Mason RM,. CTGF mediates TGF-β-induced fibronectin matrix deposition by upregulating active α5β1 integrin in human mesangial cells. J Am Soc Nephrol 2003; 14: 601-610.
46. Frisch SM,. The epithelial cell default phenotype hypothesis and its implications for cancer. Bioessays 1997; 19: 705-709.
47. Tiwari N, Meyer-Schaller N, Arnold P, et al., Klf4 is a transcriptional regulator of genes critical for EMT, including Jnk1 (Mapk8). PloS One 2013; 8: e57329.
48. Liu Y-N, Abou-Kheir W, Yin JJ, et al., Critical and reciprocal regulation of KLF4 and SLUG in transforming growth factor β-initiated prostate cancer epithelial-mesenchymal transition. Mol Cell Biol 2012; 32: 941-953.
49. Zhang H-F, Xu L-Y, Li E-M,. A family of pleiotropically acting microRNAs in cancer progression, miR-200: potential cancer therapeutic targets. Curr Pharmaceut Design 2014; 20: 1896-1903.
50. Paterson EL, Kazenwadel J, Bert AG, et al., Down-regulation of the miRNA-200 family at the invasive front of colorectal cancers with degraded basement membrane indicates EMT is involved in cancer progression. Neoplasia 2013; 15: 180-IN122.
51. Rickman DS, Millon R, De Reynies A, et al., Prediction of future metastasis and molecular characterization of head and neck squamous-cell carcinoma based on transcriptome and genome analysis by microarrays. Oncogene 2008; 27: 6607-6622.