Mesenchymal-epithelial transition in sarcomas is controlled by the combinatorial expression of microRNA 200s and GRHL2

Molecular and Cellular Biology

Volumn 36, Issue 19, 2016, Pages 2503-2513

  Somarelli, Jason A ^a   Shetler, Samantha ^a   Jolly, Mohit K ^b,c   Wang, Xueyang ^d   Bartholf Dewitt, Suzanne ^d   Hish, Alexander J ^a   Gilja, Shivee ^a   Eward, William C ^d   Ware, Kathryn E ^a   Levine, Herbert ^b,c   Armstrong, Andrew J ^a,d   Garcia Blanco, Mariano A ^d,e,f  

^a DUKE CANCER INSTITUTE   (United States)

^b RICE UNIVERSITY   (United States)

^c Rice University   (United States)

^d DUKE UNIVERSITY   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN; GRAINYHEAD LIKE TRANSCRIPTION FACTOR 2; MICRORNA 200; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; GRHL2 PROTEIN, HUMAN; MICRORNA; MIRN200 MICRORNA, HUMAN; ZEB1 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOMA; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; METASTASIS; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS; THEORETICAL MODEL; TUMOR INVASION;

DNA-BINDING PROTEINS; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MODELS, THEORETICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROGNOSIS; SARCOMA; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS; UP-REGULATION; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 84990036789     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00373-16     Document Type: Article

References (54)

1. Nakaya Y, Sheng G. 2013. EMT in developmental morphogenesis. Cancer Lett 341:9-15. http://dx.doi.org/10.1016/j.canlet.2013.02.037.
2. Lim J, Thiery JP. 2012. Epithelial-mesenchymal transitions: insights from development. Development 139:3471-3486. http://dx.doi.org/10.1242/dev.071209.
3. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890. http://dx.doi.org/10.1016/j.cell.2009.11.007.
4. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelialmesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142. http://dx.doi.org/10.1038/nrm1835.
5. Weber CE, Li NY, Wai PY, Kuo PC. 2012. Epithelial-mesenchymal transition, TGF-beta, and osteopontin in wound healing and tissue remodeling after injury. J Burn Care Res 33:311-318. http://dx.doi.org/10.1097/BCR.0b013e318240541e.
6. Galichon P, Finianos S, Hertig A. 2013. EMT-MET in renal disease: should we curb our enthusiasm? Cancer Lett 341:24-29. http://dx.doi.org/10.1016/j.canlet.2013.04.018.
7. Carew RM, Wang B, Kantharidis P. 2012. The role of EMT in renal fibrosis. Cell Tissue Res 347:103-116. http://dx.doi.org/10.1007/s00441-011-1227-1.
8. Willis BC, Borok Z. 2007. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 293:L525-L534. http://dx.doi.org/10.1152/ajplung.00163.2007.
9. Ye X, Weinberg RA. 2015. Epithelial-mesenchymal plasticity: a central regulator of cancer progression. Trends Cell Biol 25:675-686. http://dx.doi.org/10.1016/j.tcb.2015.07.012.
10. Li L, Li W. 2015. Epithelial-mesenchymal transition in human cancer: comprehensive reprogramming of metabolism, epigenetics, and differentiation. Pharmacol Ther 150:33-46. http://dx.doi.org/10.1016/j.pharmthera.2015.01.004.
11. Tsai JH, Yang J. 2013. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev 27:2192-2206. http://dx.doi.org/10.1101/gad.225334.113.
12. Bitting RL, Schaeffer D, Somarelli JA, Garcia-Blanco MA, Armstrong AJ. 2014. The role of epithelial plasticity in prostate cancer dissemination and treatment resistance. Cancer Metastasis Rev 33:441-468. http://dx.doi.org/10.1007/s10555-013-9483-z.
13. Schaeffer D, Somarelli JA, Hanna G, Palmer GM, Garcia-Blanco MA. 2014 Cellular migration and invasion uncoupled: increased migration is not an inexorable consequence of epithelial-to-mesenchymal transition. Mol Cell Biol 34:3486-3499. http://dx.doi.org/10.1128/MCB.00694-14.
14. Mathow D, Chessa F, Rabionet M, Kaden S, Jennemann R, Sandhoff R, Grone HJ, Feuerborn A. 2015. Zeb1 affects epithelial cell adhesion by diverting glycosphingolipid metabolism. EMBO Rep 16:321-331. http://dx.doi.org/10.15252/embr.201439333.
15. Ware KE, Hinz TK, Kleczko E, Singleton KR, Marek LA, Helfrich BA, Cummings CT, Graham DK, Astling D, Tan AC, Heasley LE. 2013. A mechanism of resistance to gefitinib mediated by cellular reprogramming and the acquisition of an FGF2-FGFR1 autocrine growth loop. Oncogenesis 2:e39. http://dx.doi.org/10.1038/oncsis.2013.4.
16. Yauch RL, Januario T, Eberhard DA, Cavet G, Zhu W, Fu L, Pham TQ, Soriano R, Stinson J, Seshagiri S, Modrusan Z, Lin CY, O'Neill V, Amler LC. 2005. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin Cancer Res 11:8686-8698. http://dx.doi.org/10.1158/1078-0432.CCR-05-1492.
17. Jolly MK, Huang B, Lu M, Mani SA, Levine H, Ben-Jacob E. 2014. Towards elucidating the connection between epithelial-mesenchymal transitions and stemness. J R Soc Interface 11:20140962. http://dx.doi.org/10.1098/rsif.2014.0962.
18. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. 2008. The epithelial-mesenchymal transition gen-erates cells with properties of stem cells. Cell 133:704-715. http://dx.doi.org/10.1016/j.cell.2008.03.027.
19. Chen L, Gibbons DL, Goswami S, Cortez MA, Ahn YH, Byers LA, Zhang X, Yi X, Dwyer D, Lin W, Diao L, Wang J, Roybal JD, Patel M, Ungewiss C, Peng D, Antonia S, Mediavilla-Varela M, Robertson G, Jones S, Suraokar M, Welsh JW, Erez B, Wistuba II, Chen L, Peng D, Wang S, Ullrich SE, Heymach JV, Kurie JM, Qin FX. 2014. Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression. Nat Commun 5:5241. http://dx.doi.org/10.1038/ncomms6241.
20. Vega S, Morales AV, Ocana OH, Valdes F, Fabregat I, Nieto MA. 2004. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev 18:1131-1143. http://dx.doi.org/10.1101/gad.294104.
21. Huang SS, Huang JS. 2005. TGF-beta control of cell proliferation. J Cell Biochem 96:447-462. http://dx.doi.org/10.1002/jcb.20558.
22. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. 2012. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22:725-736. http://dx.doi.org/10.1016/j.ccr.2012.09.022.
23. Armstrong AJ, Marengo MS, Oltean S, Kemeny G, Bitting RL, Turnbull JD, Herold CI, Marcom PK, George DJ, Garcia-Blanco MA. 2011. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol Cancer Res 9:997-1007. http://dx.doi.org/10.1158/1541-7786.MCR-10-0490.
24. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, Concannon KF, Donaldson MC, Sequist LV, Brachtel E, Sgroi D, Baselga J, Ramaswamy S, Toner M, Haber DA, Maheswaran S. 2013. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339:580-584. http://dx.doi.org/10.1126/science.1228522.
25. Jolly MK, Boareto M, Huang B, Jia D, Lu M, Ben-Jacob E, Onuchic JN, Levine H. 2015. Implications of the hybrid epithelial/mesenchymal phenotype in metastasis. Front Oncol 5:155.
26. Alba-Castellón L, Batlle R, Franci C, Fernandez-Acenero MJ, Mazzolini R, Pena R, Loubat J, Alameda F, Rodriguez R, Curto J, Albanell J, Munoz A, Bonilla F, Ignacio Casal J, Rojo F, Garcia de Herreros A. 2014 Snail1 expression is required for sarcomagenesis. Neoplasia 16:413-421 http://dx.doi.org/10.1016/j.neo.2014.05.002.
27. Shen A, Zhang Y, Yang H, Xu R, Huang G. 2012. Overexpression of ZEB1 relates to metastasis and invasion in osteosarcoma. J Surg Oncol 105:830-834. http://dx.doi.org/10.1002/jso.23012.
28. Wang N, He YL, Pang LJ, Zou H, Liu CX, Zhao J, Hu JM, Zhang WJ, Qi Y, Li F. 2015. Down-regulated E-cadherin expression is associated with poor five-year overall survival in bone and soft tissue sarcoma: results of a meta-analysis. PLoS One 10:e0121448. http://dx.doi.org/10.1371/journal.pone.0121448.
29. Lu M, Jolly MK, Levine H, Onuchic JN, Ben-Jacob E. 2013. MicroRNAbased regulation of epithelial-hybrid-mesenchymal fate determination. Proc Natl Acad Sci U S A 110:18144-18149. http://dx.doi.org/10.1073/pnas.1318192110.
30. Dhooge A, Govaerts W, Kuznetsov YA. 2003. MATCONT: a MATLAB package for numerical bifurcation analysis of ODEs. ACM Trans Math Softw 29:141-164. http://dx.doi.org/10.1145/779359.779362.
31. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ. 2008. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68:7846-7854. http://dx.doi.org/10.1158/0008-5472.CAN-08-1942.
32. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T. 2008. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9:582-589. http://dx.doi.org/10.1038/embor.2008.74.
33. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U, Hermeking H. 2011. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10:4256-4271 http://dx.doi.org/10.4161/cc.10.24.18552.
34. Guaita S, Puig I, Franci C, Garrido M, Dominguez D, Batlle E, Sancho E, Dedhar S, De Herreros AG, Baulida J. 2002. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J Biol Chem 277:39209-39216. http://dx.doi.org/10.1074/jbc.M206400200.
35. Gill JG, Langer EM, Lindsley RC, Cai M, Murphy TL, Kyba M, Murphy KM. 2011. Snail and the microRNA-200 family act in opposition to regulate epithelial-to-mesenchymal transition and germ layer fate restriction in differentiating ESCs. Stem Cells 29:764-776. http://dx.doi.org/10.1002/stem.628.
36. Ahn YH, Gibbons DL, Chakravarti D, Creighton CJ, Rizvi ZH, Adams HP, Pertsemlidis A, Gregory PA, Wright JA, Goodall GJ, Flores ER, Kurie JM. 2012. ZEB1 drives prometastatic actin cytoskeletal remodeling by downregulating miR-34a expression. J Clin Invest 122:3170-3183. http://dx.doi.org/10.1172/JCI63608.
37. Hurteau GJ, Carlson JA, Roos E, Brock GJ. 2009. Stable expression of miR-200c alone is sufficient to regulate TCF8 (ZEB1) and restore Ecadherin expression. Cell Cycle 8:2064-2069. http://dx.doi.org/10.4161/cc.8.13.8883.
38. Hill L, Browne G, Tulchinsky E. 2013. ZEB/miR-200 feedback loop: at the crossroads of signal transduction in cancer. Int J Cancer 132:745-754. http://dx.doi.org/10.1002/ijc.27708.
39. Preca BT, Bajdak K, Mock K, Sundararajan V, Pfannstiel J, Maurer J, Wellner U, Hopt UT, Brummer T, Brabletz S, Brabletz T, Stemmler MP. 2015. A self-enforcing CD44s/ZEB1 feedback loop maintains EMT and stemness properties in cancer cells. Int J Cancer 137:2566-2577. http://dx.doi.org/10.1002/ijc.29642.
40. Varma S, Cao Y, Tagne JB, Lakshminarayanan M, Li J, Friedman TB, Morell RJ, Warburton D, Kotton DN, Ramirez MI. 2012. The transcription factors Grainyhead-like 2 and NK2-homeobox 1 form a regulatory loop that coordinates lung epithelial cell morphogenesis and differentiation. J Biol Chem 287:37282-37295. http://dx.doi.org/10.1074/jbc.M112.408401.
41. Cieply B, Riley P, Pifer PM, Widmeyer J, Addison JB, Ivanov AV, Denvir J, Frisch SM. 2012. Suppression of the epithelial-mesenchymal transition by Grainyhead-like-2. Cancer Res 72:2440-2453. http://dx.doi.org/10.1158/0008-5472.CAN-11-4038.
42. Cieply B, Farris J, Denvir J, Ford HL, Frisch SM. 2013. Epithelialmesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and Grainyhead-like-2. Cancer Res 73:6299-6309. http://dx.doi.org/10.1158/0008-5472.CAN-12-4082.
43. Werth M, Walentin K, Aue A, Schonheit J, Wuebken A, Pode-Shakked N, Vilianovitch L, Erdmann B, Dekel B, Bader M, Barasch J, Rosenbauer F, Luft FC, Schmidt-Ott KM. 2010. The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex. Development 137:3835-3845. http://dx.doi.org/10.1242/dev.055483.
44. Sánchez-Tilló E, Lazaro A, Torrent R, Cuatrecasas M, Vaquero EC, Castells A, Engel P, Postigo A. 2010. ZEB1 represses E-cadherin and induces an EMT by recruiting the SWI/SNF chromatin-remodeling protein BRG1. Oncogene 29:3490-3500. http://dx.doi.org/10.1038/onc.2010.102.
45. Schmalhofer O, Brabletz S, Brabletz T. 2009. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 28: 151-166. http://dx.doi.org/10.1007/s10555-008-9179-y.
46. Werner S, Frey S, Riethdorf S, Schulze C, Alawi M, Kling L, Vafaizadeh V, Sauter G, Terracciano L, Schumacher U, Pantel K, Assmann V. 2013. Dual roles of the transcription factor grainyhead-like 2 (GRHL2) in breast cancer. J Biol Chem 288:22993-23008. http://dx.doi.org/10.1074/jbc.M113.456293.
47. Oltean S, Febbo PG, Garcia-Blanco MA. 2008. Dunning rat prostate adenocarcinomas and alternative splicing reporters: powerful tools to study epithelial plasticity in prostate tumors in vivo. Clin Exp Metastasis 25:611-619. http://dx.doi.org/10.1007/s10585-008-9186-y.
48. Salt MB, Bandyopadhyay S, McCormick F. 2014. Epithelial-tomesenchymal transition rewires the molecular path to PI3K-dependent proliferation. Cancer Discov 4:186-199. http://dx.doi.org/10.1158/2159-8290.CD-13-0520.
49. Kuijjer ML, Rydbeck H, Kresse SH, Buddingh EP, Lid AB, Roelofs H, Burger H, Myklebost O, Hogendoorn PC, Meza-Zepeda LA, Cleton-Jansen AM. 2012. Identification of osteosarcoma driver genes by integrative analysis of copy number and gene expression data. Genes Chromosomes Cancer 51:696-706. http://dx.doi.org/10.1002/gcc.21956.
50. Crago AM, Singer S. 2011. Clinical and molecular approaches to well differentiated and dedifferentiated liposarcoma. Curr Opin Oncol 23: 373-378. http://dx.doi.org/10.1097/CCO.0b013e32834796e6.
51. Eid JE, Garcia CB. 2015. Reprogramming of mesenchymal stem cells by oncogenes. Semin Cancer Biol 32:18-31. http://dx.doi.org/10.1016/j.semcancer.2014.05.005.
52. Yin K, Liao Q, He H, Zhong D. 2012. Prognostic value of Twist and E-cadherin in patients with osteosarcoma. Med Oncol 29:3449-3455. http://dx.doi.org/10.1007/s12032-012-0317-6.
53. Tian W, Wang G, Yang J, Pan Y, Ma Y. 2013. Prognostic role of E-cadherin and Vimentin expression in various subtypes of soft tissue leiomyosarcomas. Med Oncol 30:401. http://dx.doi.org/10.1007/s12032-012-0401-y.
54. Tam WL, Weinberg RA. 2013. The epigenetics of epithelial-mesenchymal plasticity in cancer. NatMed 19:1438-1449. http://dx.doi.org/10.1038/nm.3336.