MicroRNA regulation of epithelial plasticity in cancer

Cancer Letters

Volumn 341, Issue 1, 2013, Pages 46-55

  D'Amato, Nicholas C ^a   Howe, Erin N ^a,b   Richer, Jennifer K ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Cancer; EMT; MET; Metastasis; MicroRNA; Plasticity

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 155; MICRORNA 200; MICRORNA 203; MICRORNA 296; MICRORNA 34A; MICRORNA 7; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG; UVOMORULIN;

CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; CELL RENEWAL; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIAL PLASTICITY; EPITHELIUM CELL; FEEDBACK SYSTEM; GENE TARGETING; HUMAN; MESENCHYME CELL; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SHORT SURVEY;

EID: 84887156288     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.11.054     Document Type: Review

References (156)

1. Aigner K., Dampier B., Descovich L., Mikula M., Sultan A., Schreiber M., Mikulits W., Brabletz T., Strand D., Obrist P., Sommergruber W., Schweifer N., Wernitznig A., Beug H., Foisner R., Eger A. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007, 26:6979-6988.
2. Alvarez-Garcia I., Miska E.A. MicroRNA functions in animal development and human disease. Development 2005, 132:4653-4662.
3. Ando T., Yoshida T., Enomoto S., Asada K., Tatematsu M., Ichinose M., Sugiyama T., Ushijima T. DNA methylation of microRNA genes in gastric mucosae of gastric cancer patients: its possible involvement in the formation of epigenetic field defect, international journal of cancer. J. Int. Cancer 2009, 124:2367-2374.
4. Asangani I.A., Rasheed S.A., Nikolova D.A., Leupold J.H., Colburn N.H., Post S., Allgayer H. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008, 27:2128-2136.
5. Asirvatham A.J., Gregorie C.J., Hu Z., Magner W.J., Tomasi T.B. MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components. Mol. Immunol. 2008, 45:1995-2006.
6. Babiarz J.E., Ruby J.G., Wang Y., Bartel D.P., Blelloch R. Mouse ES cells express endogenous shRNAs, siRNAs, and other microprocessor-independent, Dicer-dependent small RNAs. Gene. Dev. 2008, 22:2773-2785.
7. Bahri S., Wang S., Conder R., Choy J., Vlachos S., Dong K., Merino C., Sigrist S., Molnar C., Yang X., Manser E., Harden N. The leading edge during dorsal closure as a model for epithelial plasticity: pak is required for recruitment of the Scribble complex and septate junction formation. Development 2010, 137:2023-2032.
8. Berezikov E., Chung W.J., Willis J., Cuppen E., Lai E.C. Mammalian mirtron genes. Mol. Cell 2007, 28:328-336.
9. Bommer G.T., Gerin I., Feng Y., Kaczorowski A.J., Kuick R., Love R.E., Zhai Y., Giordano T.J., Qin Z.S., Moore B.B., MacDougald O.A., Cho K.R., Fearon E.R. P53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol.: CB 2007, 17:1298-1307.
10. Bornachea O., Santos M., Martinez-Cruz A.B., Garcia-Escudero R., Duenas M., Costa C., Segrelles C., Lorz C., Buitrago A., Saiz-Ladera C., Agirre X., Grande T., Paradela B., Maraver A., Ariza J.M., Prosper F., Serrano M., Sanchez-Cespedes M., Paramio J.M. EMT and induction of miR-21 mediate metastasis development in Trp53-deficient tumours. Sci. Rep. 2012, 2:434.
11. Brabletz T. To differentiate or not-routes towards metastasis. Nat. Rev. Cancer 2012, 12:425-436.
12. Burk U., Schubert J., Wellner U., Schmalhofer O., Vincan E., Spaderna S., Brabletz T. 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.
13. Calin G.A., Croce C.M. MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006, 6:857-866.
14. Calin G.A., Dumitru C.D., Shimizu M., Bichi R., Zupo S., Noch E., Aldler H., Rattan S., Keating M., Rai K., Rassenti L., Kipps T., Negrini M., Bullrich F., Croce C.M. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Nat. Acad. Sci. USA 2002, 99:15524-15529.
15. Carvalho J., van Grieken N.C., Pereira P.M., Sousa S., Tijssen M., Buffart T.E., Diosdado B., Grabsch H., Santos M.A., Meijer G., Seruca R., Carvalho B., Oliveira C. Lack of microRNA-101 causes E-cadherin functional deregulation through EZH2 up-regulation in intestinal gastric cancer. J. Pathol. 2012.
16. Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., Lee K.H., Feldmann G., Yamakuchi M., Ferlito M., Lowenstein C.J., Arking D.E., Beer M.A., Maitra A., Mendell J.T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell. 2007, 26:745-752.
17. Chekulaeva M., Mathys H., Zipprich J.T., Attig J., Colic M., Parker R., Filipowicz W. MiRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 2011, 18:1218-1226.
18. Cheloufi S., Dos Santos C.O., Chong M.M., Hannon G.J. A Dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465:584-589.
19. Chen J., Wang L., Matyunina L.V., Hill C.G., McDonald J.F. Overexpression of miR-429 induces mesenchymal-to-epithelial transition (MET) in metastatic ovarian cancer cells. Gynecol. Oncol. 2011, 121:200-205.
20. Cochrane D.R., Cittelly D.M., Howe E.N., Spoelstra N.S., McKinsey E.L., LaPara K., Elias A., Yee D., Richer J.K. MicroRNAs link estrogen receptor alpha status and Dicer levels in breast cancer. Horm. Cancer 2010, 1:306-319.
21. Coppola V., Musumeci M., Patrizii M., Cannistraci A., Addario A., Maugeri-Sacca M., Biffoni M., Francescangeli F., Cordenonsi M., Piccolo S., Memeo L., Pagliuca A., Muto G., Zeuner A., De Maria R., Bonci D. BTG2 loss and miR-21 upregulation contribute to prostate cell transformation by inducing luminal markers expression and epithelial-mesenchymal transition. Oncogene 2012.
22. Corney D.C., Flesken-Nikitin A., Godwin A.K., Wang W., Nikitin A.Y. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res. 2007, 67:8433-8438.
23. Creighton C.J., Li X., Landis M., Dixon J.M., Neumeister V.M., Sjolund A., Rimm D.L., Wong H., Rodriguez A., Herschkowitz J.I., Fan C., Zhang X., He X., Pavlick A., Gutierrez M.C., Renshaw L., Larionov A.A., Faratian D., Hilsenbeck S.G., Perou C.M., Lewis M.T., Rosen J.M., Chang J.C. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Nat. Acad. Sci. USA 2009, 106:13820-13825.
24. Davalos V., Moutinho C., Villanueva A., Boque R., Silva P., Carneiro F., Esteller M. Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 2012, 31:2062-2074.
25. Davis B.N., Hilyard A.C., Lagna G., Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008, 454:56-61.
26. de Antonellis P., Medaglia C., Cusanelli E., Andolfo I., Liguori L., De Vita G., Carotenuto M., Bello A., Formiggini F., Galeone A., De Rosa G., Virgilio A., Scognamiglio I., Sciro M., Basso G., Schulte J.H., Cinalli G., Iolascon A., Zollo M. MiR-34a targeting of Notch ligand delta-like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS ONE 2011, 6:e24584.
27. Deng Y., Deng H., Bi F., Liu J., Bemis L.T., Norris D., Wang X.J., Zhang Q. MicroRNA-137 targets carboxyl-terminal binding protein 1 in melanoma cell lines. Int. J. Biol. Sci. 2011, 7:133-137.
28. DeSano J.T., Xu L. MicroRNA regulation of cancer stem cells and therapeutic implications. AAPS J. 2009, 11:682-692.
29. Dong P., Karaayvaz M., Jia N., Kaneuchi M., Hamada J., Watari H., Sudo S., Ju J., Sakuragi N. Mutant p53 gain-of-function induces epithelial-mesenchymal transition through modulation of the miR-130b-ZEB1 axis. Oncogene 2012.
30. Douma S., Van Laar T., Zevenhoven J., Meuwissen R., Van Garderen E., Peeper D.S. Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 2004, 430:1034-1039.
31. Du J., Yang S., An D., Hu F., Yuan W., Zhai C., Zhu T. BMP-6 inhibits microRNA-21 expression in breast cancer through repressing deltaEF1 and AP-1. Cell Res. 2009, 19:487-496.
32. Dykxhoorn D.M., Wu Y., Xie H., Yu F., Lal A., Petrocca F., Martinvalet D., Song E., Lim B., Lieberman J. MiR-200 enhances mouse breast cancer cell colonization to form distant metastases. PLoS ONE 2009, 4:e7181.
33. Eger A., Aigner K., Sonderegger S., Dampier B., Oehler S., Schreiber M., Berx G., Cano A., Beug H., Foisner R. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005, 24:2375-2385.
34. Eis P.S., Tam W., Sun L., Chadburn A., Li Z., Gomez M.F., Lund E., Dahlberg J.E. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Nat. Acad. Sci. USA 2005, 102:3627-3632.
35. Engels B.M., Hutvagner G. Principles and effects of microRNA-mediated post-transcriptional gene regulation. Oncogene 2006, 25:6163-6169.
36. Etienne-Manneville S. Polarity proteins in migration and invasion. Oncogene 2008, 27:6970-6980.
37. Forman J.J., Legesse-Miller A., Coller H.A. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Nat. Acad. Sci. USA 2008, 105:14879-14884.
38. Fujita S., Ito T., Mizutani T., Minoguchi S., Yamamichi N., Sakurai K., Iba H. MiR-21 Gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J. Mol. Biol. 2008, 378:492-504.
39. Gebeshuber C.A., Zatloukal K., Martinez J. MiR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep. 2009, 10:400-405.
40. Gibbons D.L., Lin W., Creighton C.J., Rizvi Z.H., Gregory P.A., Goodall G.J., Thilaganathan N., Du L., Zhang Y., Pertsemlidis A., Kurie J.M. Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Gene. Dev. 2009, 23:2140-2151.
41. Gotte M., Mohr C., Koo C.Y., Stock C., Vaske A.K., Viola M., Ibrahim S.A., Peddibhotla S., Teng Y.H., Low J.Y., Ebnet K., Kiesel L., Yip G.W. MiR-145-dependent targeting of junctional adhesion molecule A and modulation of fascin expression are associated with reduced breast cancer cell motility and invasiveness. Oncogene 2010, 29:6569-6580.
42. Greene S.B., Gunaratne P.H., Hammond S.M., Rosen J.M. A putative role for microRNA-205 in mammary epithelial cell progenitors. J. Cell Sci. 2010, 123:606-618.
43. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008, 10:593-601.
44. Gregory P.A., Bracken C.P., Bert A.G., Goodall G.J. MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 2008, 7:3112-3118.
45. Grelier G., Voirin N., Ay A.S., Cox D.G., Chabaud S., Treilleux I., Leon-Goddard S., Rimokh R., Mikaelian I., Venoux C., Puisieux A., Lasset C., Moyret-Lalle C. Prognostic value of Dicer expression in human breast cancers and association with the mesenchymal phenotype. Br. J. Cancer 2009, 101:673-683.
46. Guo L., Lu Z. The fate of miRNA* strand through evolutionary analysis: implication for degradation as merely carrier strand or potential regulatory molecule?. PLoS ONE 2010, 5:e11387.
47. Gupta S., Read D.E., Deepti A., Cawley K., Gupta A., Oommen D., Verfaillie T., Matus S., Smith M.A., Mott J.L., Agostinis P., Hetz C., Samali A. Perk-dependent repression of miR-106b-25 cluster is required for ER stress-induced apoptosis. Cell Death Disease 2012, 3:e333.
48. Han M., Wang Y., Liu M., Bi X., Bao J., Zeng N., Zhu Z., Mo Z., Wu C., Chen X. MiR-21 regulates epithelial-mesenchymal transition phenotype and hypoxia-inducible factor-1alpha expression in third-sphere forming breast cancer stem cell-like cells. Cancer Sci. 2012, 103:1058-1064.
49. Hansen T.B., Wiklund E.D., Bramsen J.B., Villadsen S.B., Statham A.L., Clark S.J., Kjems J. MiRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J. 2011, 30:4414-4422.
50. He L., Thomson J.M., Hemann M.T., Hernando-Monge E., Mu D., Goodson S., Powers S., Cordon-Cardo C., Lowe S.W., Hannon G.J., Hammond S.M. A microRNA polycistron as a potential human oncogene. Nature 2005, 435:828-833.
51. Herranz H., Cohen S.M. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Gene. Dev. 2010, 24:1339-1344.
52. Howe E.N., Cochrane D.R., Richer J.K. Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res. : BCR 2011, 13:R45.
53. Howe E.N., Cochrane D.R., Richer J.K. The miR-200 and miR-221/222 microRNA families: opposing effects on epithelial identity. J. Mammary Gland Biol. Neoplasia 2012, 17:65-77.
54. Huang Q., Gumireddy K., Schrier M., le Sage C., Nagel R., Nair S., Egan D.A., Li A., Huang G., Klein-Szanto A.J., Gimotty P.A., Katsaros D., Coukos G., Zhang L., Pure E., Agami R. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat. Cell Biol. 2008, 10:202-210.
55. Iliopoulos D., Hirsch H.A., Wang G., Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc. Nat. Acad. Sci. USA 2011, 108:1397-1402.
56. Iliopoulos D., Lindahl-Allen M., Polytarchou C., Hirsch H.A., Tsichlis P.N., Struhl K. Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol. Cell 2010, 39:761-772.
57. Iorio M.V., Ferracin M., Liu C.G., Veronese A., Spizzo R., Sabbioni S., Magri E., Pedriali M., Fabbri M., Campiglio M., Menard S., Palazzo J.P., Rosenberg A., Musiani P., Volinia S., Nenci I., Calin G.A., Querzoli P., Negrini M., Croce C.M. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005, 65:7065-7070.
58. Jechlinger M., Grunert S., Tamir I.H., Janda E., Ludemann S., Waerner T., Seither P., Weith A., Beug H., Kraut N. Expression profiling of epithelial plasticity in tumor progression. Oncogene 2003, 22:7155-7169.
59. Ji Q., Hao X., Zhang M., Tang W., Yang M., Li L., Xiang D., Desano J.T., Bommer G.T., Fan D., Fearon E.R., Lawrence T.S., Xu L. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS ONE 2009, 4:e6816.
60. Jiang L., Dai Y., Liu X., Wang C., Wang A., Chen Z., Heidbreder C.E., Kolokythas A., Zhou X. Identification and experimental validation of G protein alpha inhibiting activity polypeptide 2 (GNAI2) as a microRNA-138 target in tongue squamous cell carcinoma. Hum. Genet. 2011, 129:189-197.
61. Jurmeister S., Baumann M., Balwierz A., Keklikoglou I., Ward A., Uhlmann S., Zhang J.D., Wiemann S., Sahin O. MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol. Cell. Biol. 2012, 32:633-651.
62. Kim N.H., Kim H.S., Li X.Y., Lee I., Choi H.S., Kang S.E., Cha S.Y., Ryu J.K., Yoon D., Fearon E.R., Rowe R.G., Lee S., Maher C.A., Weiss S.J., Yook J.I. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J. Cell Biol. 2011, 195:417-433.
63. Kim T., Veronese A., Pichiorri F., Lee T.J., Jeon Y.J., Volinia S., Pineau P., Marchio A., Palatini J., Suh S.S., Alder H., Liu C.G., Dejean A., Croce C.M. P53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J. Exp. Med. 2011, 208:875-883.
64. Kim Y.J., Hwang S.J., Bae Y.C., Jung J.S. MiR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells 2009, 27:3093-3102.
65. Kong D., Banerjee S., Ahmad A., Li Y., Wang Z., Sethi S., Sarkar F.H. Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells. PLoS ONE 2010, 5:e12445.
66. Kong W., Yang H., He L., Zhao J.J., Coppola D., Dalton W.S., Cheng J.Q. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol. Cell. Biol. 2008, 28:6773-6784.
67. Korpal M., Lee E.S., Hu G., Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 2008, 283:14910-14914.
68. Kumarswamy R., Mudduluru G., Ceppi P., Muppala S., Kozlowski M., Niklinski J., Papotti M., Allgayer H. MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer, International journal of cancer. J. Int. Cancer 2012, 130:2044-2053.
69. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
70. Lau N.C., Lim L.P., Weinstein E.G., Bartel D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001, 294:858-862.
71. Lee J.M., Dedhar S., Kalluri R., Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 2006, 172:973-981.
72. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294:862-864.
73. Lee Y., Kim M., Han J., Yeom K.H., Lee S., Baek S.H., Kim V.N. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004, 23:4051-4060.
74. Li B., Han Q., Zhu Y., Yu Y., Wang J., Jiang X. Down-regulation of miR-214 contributes to intrahepatic cholangiocarcinoma metastasis by targeting Twist. FEBS J. 2012, 279:2393-2398.
75. Li X., Cassidy J.J., Reinke C.A., Fischboeck S., Carthew R.W. A microRNA imparts robustness against environmental fluctuation during development. Cell 2009, 137:273-282.
76. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
77. Liu C., Kelnar K., Liu B., Chen X., Calhoun-Davis T., Li H., Patrawala L., Yan H., Jeter C., Honorio S., Wiggins J.F., Bader A.G., Fagin R., Brown D., Tang D.G. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat. Med. 2011, 17:211-215.
78. Liu C., Tang D.G. MicroRNA regulation of cancer stem cells. Cancer Res. 2011, 71:5950-5954.
79. Liu P., Wilson M.J. MiR-520c and miR-373 upregulate MMP9 expression by targeting mTOR and SIRT1, and activate the Ras/Raf/MEK/Erk signaling pathway and NF-kappaB factor in human fibrosarcoma cells. J. Cell. Physiol. 2012, 227:867-876.
80. Liu X., Jiang L., Wang A., Yu J., Shi F., Zhou X. MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer Lett. 2009, 286:217-222.
81. Liu X., Wang C., Chen Z., Jin Y., Wang Y., Kolokythas A., Dai Y., Zhou X. MicroRNA-138 suppresses epithelial-mesenchymal transition in squamous cell carcinoma cell lines. Biochem. J. 2011, 440:23-31.
82. Liu Y.N., Yin J.J., Abou-Kheir W., Hynes P.G., Casey O.M., Fang L., Yi M., Stephens R.M., Seng V., Sheppard-Tillman H., Martin P., Kelly K. MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 2012.
83. Lodygin D., Tarasov V., Epanchintsev A., Berking C., Knyazeva T., Korner H., Knyazev P., Diebold J., Hermeking H. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008, 7:2591-2600.
84. Lopez-Serra P., Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 2012, 31:1609-1622.
85. Lu J., Getz G., Miska E.A., Alvarez-Saavedra E., Lamb J., Peck D., Sweet-Cordero A., Ebert B.L., Mak R.H., Ferrando A.A., Downing J.R., Jacks T., Horvitz H.R., Golub T.R. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
86. Lujambio A., Calin G.A., Villanueva A., Ropero S., Sanchez-Cespedes M., Blanco D., Montuenga L.M., Rossi S., Nicoloso M.S., Faller W.J., Gallagher W.M., Eccles S.A., Croce C.M., Esteller M. A microRNA DNA methylation signature for human cancer metastasis. Proc. Nat. Acad. Sci. USA 2008, 105:13556-13561.
87. Lujambio A., Ropero S., Ballestar E., Fraga M.F., Cerrato C., Setien F., Casado S., Suarez-Gauthier A., Sanchez-Cespedes M., Git A., Spiteri I., Das P.P., Caldas C., Miska E., Esteller M. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 2007, 67:1424-1429.
88. Ma L., Young J., Prabhala H., Pan E., Mestdagh P., Muth D., Teruya-Feldstein J., Reinhardt F., Onder T.T., Valastyan S., Westermann F., Speleman F., Vandesompele J., Weinberg R.A. MiR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol. 2010, 12:247-256.
89. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., Campbell L.L., Polyak K., Brisken C., Yang J., Weinberg R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
90. Martello G., Rosato A., Ferrari F., Manfrin A., Cordenonsi M., Dupont S., Enzo E., Guzzardo V., Rondina M., Spruce T., Parenti A.R., Daidone M.G., Bicciato S., Piccolo S. A MicroRNA targeting Dicer for metastasis control. Cell 2010, 141:1195-1207.
91. Meng F., Henson R., Wehbe-Janek H., Ghoshal K., Jacob S.T., Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007, 133:647-658.
92. Micalizzi D.S., Farabaugh S.M., Ford H.L. epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J. Mammary Gland Biol. Neoplasia 2010, 15:117-134.
93. Micalizzi D.S., Wang C.A., Farabaugh S.M., Schiemann W.P., Ford H.L. Homeoprotein Six1 increases TGF-beta type I receptor and converts TGF-beta signaling from suppressive to supportive for tumor growth. Cancer Res. 2010, 70:10371-10380.
94. Moes M., Le Bechec A., Crespo I., Laurini C., Halavatyi A., Vetter G., Del Sol A., Friederich E. A novel network integrating a miRNA-203/SNAI1 feedback loop which regulates epithelial to mesenchymal transition. PLoS ONE 2012, 7:e35440.
95. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008, 3:e2888.
96. Mraz M., Dolezalova D., Plevova K., Stano Kozubik K., Mayerova V., Cerna K., Musilova K., Tichy B., Pavlova S., Borsky M., Verner J., Doubek M., Brychtova Y., Trbusek M., Hampl A., Mayer J., Pospisilova S. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood 2012, 119:2110-2113.
97. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S., Weinberg R.A. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 2008, 68:3645-3654.
98. Ozdamar B., Bose R., Barrios-Rodiles M., Wang H.R., Zhang Y., Wrana J.L. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 2005, 307:1603-1609.
99. Papadimitriou E., Vasilaki E., Vorvis C., Iliopoulos D., Moustakas A., Kardassis D., Stournaras C. Differential regulation of the two RhoA-specific GEF isoforms Net1/Net1A by TGF-beta and miR-24: role in epithelial-to-mesenchymal transition. Oncogene 2012, 31:2862-2875.
100. Papagiannakopoulos T., Shapiro A., Kosik K.S. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 2008, 68:8164-8172.
101. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Gene. Dev. 2008, 22:894-907.
102. Petrie R.J., Doyle A.D., Yamada K.M. Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 2009, 10:538-549.
103. Piao X., Zhang X., Wu L., Belasco J.G. CCR4-NOT deadenylates mRNA associated with RNA-induced silencing complexes in human cells. Mol. Cell. Biol. 2010, 30:1486-1494.
104. Place R.F., Li L.C., Pookot D., Noonan E.J., Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc. Nat. Acad. Sci. USA 2008, 105:1608-1613.
105. Polytarchou C., Iliopoulos D., Struhl K. An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. Proc. Nat. Acad. Sci. USA 2012, 109:14470-14475.
106. Qian B., Katsaros D., Lu L., Preti M., Durando A., Arisio R., Mu L., Yu H. High miR-21 expression in breast cancer associated with poor disease-free survival in early stage disease and high TGF-beta1. Breast Cancer Res. Treat. 2009, 117:131-140.
107. Reddy S.D., Ohshiro K., Rayala S.K., Kumar R. MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Res. 2008, 68:8195-8200.
108. Rokavec M., Wu W., Luo J.L. IL6-mediated suppression of miR-200c directs constitutive activation of inflammatory signaling circuit driving transformation and tumorigenesis. Mol. Cell. 2012, 45:777-789.
109. Rosati J., Spallotta F., Nanni S., Grasselli A., Antonini A., Vincenti S., Presutti C., Colussi C., D'Angelo C., Biroccio A., Farsetti A., Capogrossi M.C., Illi B., Gaetano C. Smad-interacting protein-1 and microRNA 200 family define a nitric oxide-dependent molecular circuitry involved in embryonic stem cell mesendoderm differentiation. Arterioscler. Thromb. Vasc. Biol. 2011, 31:898-907.
110. Ru P., Steele R., Newhall P., Phillips N.J., Toth K., Ray R.B. MiRNA-29b suppresses prostate cancer metastasis by regulating epithelial-mesenchymal transition signaling. Mol. Cancer Ther. 2012, 11:1166-1173.
111. Saini S., Majid S., Yamamura S., Tabatabai L., Suh S.O., Shahryari V., Chen Y., Deng G., Tanaka Y., Dahiya R. Regulatory Role of mir-203 in Prostate Cancer Progression and Metastasis. Clin. Cancer Res. : Official J. Am. Assoc. Cancer Res. 2011, 17:5287-5298.
112. Sayed D., He M., Hong C., Gao S., Rane S., Yang Z., Abdellatif M. MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J. Biol. Chem. 2010, 285:20281-20290.
113. Sayed D., Rane S., Lypowy J., He M., Chen I.Y., Vashistha H., Yan L., Malhotra A., Vatner D., Abdellatif M. MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol. Biol. Cell 2008, 19:3272-3282.
114. Shimono Y., Zabala M., Cho R.W., Lobo N., Dalerba P., Qian D., Diehn M., Liu H., Panula S.P., Chiao E., Dirbas F.M., Somlo G., Pera R.A., Lao K., Clarke M.F. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009, 138:592-603.
115. Silber J., Lim D.A., Petritsch C., Persson A.I., Maunakea A.K., Yu M., Vandenberg S.R., Ginzinger D.G., James C.D., Costello J.F., Bergers G., Weiss W.A., Alvarez-Buylla A., Hodgson J.G. MiR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 2008, 6:14.
116. Small E.M., Frost R.J., Olson E.N. MicroRNAs add a new dimension to cardiovascular disease. Circulation 2010, 121:1022-1032.
117. Smit M.A., Geiger T.R., Song J.Y., Gitelman I., Peeper D.S. A Twist-Snail axis critical for TrkB-induced epithelial-mesenchymal transition-like transformation, anoikis resistance, and metastasis. Mol. Cell. Biol. 2009, 29:3722-3737.
118. Smith A.L., Iwanaga R., Drasin D.J., Micalizzi D.S., Vartuli R.L., Tan A.C., Ford H.L. The miR-106b-25 cluster targets Smad7 activates TGF-beta signaling and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 2012.
119. Song B., Wang C., Liu J., Wang X., Lv L., Wei L., Xie L., Zheng Y., Song X. MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. J. Exp. Clin. Cancer Res. : CR 2010, 29:29.
120. Sossey-Alaoui K., Bialkowska K., Plow E.F. The miR200 family of microRNAs regulates WAVE3-dependent cancer cell invasion. J. Biol. Chem. 2009, 284:33019-33029.
121. Spaderna S., Schmalhofer O., Wahlbuhl M., Dimmler A., Bauer K., Sultan A., Hlubek F., Jung A., Strand D., Eger A., Kirchner T., Behrens J., Brabletz T. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 2008, 68:537-544.
122. Sullivan N.J., Sasser A.K., Axel A.E., Vesuna F., Raman V., Ramirez N., Oberyszyn T.M., Hall B.M. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009, 28:2940-2947.
123. Suzuki H., Yamamoto E., Nojima M., Kai M., Yamano H.O., Yoshikawa K., Kimura T., Kudo T., Harada E., Sugai T., Takamaru H., Niinuma T., Maruyama R., Yamamoto H., Tokino T., Imai K., Toyota M., Shinomura Y. Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect. Carcinogenesis 2010, 31:2066-2073.
124. Takamizawa J., Konishi H., Yanagisawa K., Tomida S., Osada H., Endoh H., Harano T., Yatabe Y., Nagino M., Nimura Y., Mitsudomi T., Takahashi T. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004, 64:3753-3756.
125. Tellez C.S., Juri D.E., Do K., Bernauer A.M., Thomas C.L., Damiani L.A., Tessema M., Leng S., Belinsky S.A. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res. 2011, 71:3087-3097.
126. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
127. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 2006, 7:131-142.
128. Tokumaru S., Suzuki M., Yamada H., Nagino M., Takahashi T. Let-7 regulates Dicer expression and constitutes a negative feedback loop. Carcinogenesis 2008, 29:2073-2077.
129. Toyota M., Suzuki H., Sasaki Y., Maruyama R., Imai K., Shinomura Y., Tokino T. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 2008, 68:4123-4132.
130. Truscott M., Islam A.B., Lopez-Bigas N., Frolov M.V. Mir-11 limits the proapoptotic function of its host gene, dE2f1. Genes Dev. 2011, 25:1820-1834.
131. Tsang J., Zhu J., van Oudenaarden A. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell 2007, 26:753-767.
132. Vaira V., Faversani A., Dohi T., Montorsi M., Augello C., Gatti S., Coggi G., Altieri D.C., Bosari S. MiR-296 regulation of a cell polarity-cell plasticity module controls tumor progression. Oncogene 2012, 31:27-38.
133. Vallejo D.M., Caparros E., Dominguez M. Targeting Notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells. EMBO J. 2011, 30:756-769.
134. Vetter G., Saumet A., Moes M., Vallar L., Le Bechec A., Laurini C., Sabbah M., Arar K., Theillet C., Lecellier C.H., Friederich E. MiR-661 expression in SNAI1-induced epithelial to mesenchymal transition contributes to breast cancer cell invasion by targeting Nectin-1 and StarD10 messengers. Oncogene 2010, 29:4436-4448.
135. Vrba L., Garbe J.C., Stampfer M.R., Futscher B.W. Epigenetic regulation of normal human mammary cell type-specific miRNAs. Genome Res. 2011, 21:2026-2037.
136. Vrba L., Jensen T.J., Garbe J.C., Heimark R.L., Cress A.E., Dickinson S., Stampfer M.R., Futscher B.W. Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS ONE 2010, 5:e8697.
137. Wahid F., Shehzad A., Khan T., Kim Y.Y. MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim. Biophys. Acta 1803, 2010:1231-1243.
138. Wang B., Li S., Qi H.H., Chowdhury D., Shi Y., Novina C.D. Distinct passenger strand and mRNA cleavage activities of human Argonaute proteins. Nat. Struct. Mol. Biol. 2009, 16:1259-1266.
139. Wang H.R., Zhang Y., Ozdamar B., Ogunjimi A.A., Alexandrova E., Thomsen G.H., Wrana J.L. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 2003, 302:1775-1779.
140. Wang P., Zou F., Zhang X., Li H., Dulak A., Tomko R.J., Lazo J.S., Wang Z., Zhang L., Yu J. MicroRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res. 2009, 69:8157-8165.
141. Weigelt B., Peterse J.L. L.J. van 't Veer, Breast cancer metastasis: markers and models. Nat. Rev. Cancer 2005, 5:591-602.
142. Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., Waldvogel B., Vannier C., Darling D., zur Hausen A., Brunton V.G., Morton J., Sansom O., Schuler J., Stemmler M.P., Herzberger C., Hopt U., Keck T., Brabletz S., Brabletz T. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 2009, 11:1487-1495.
143. Wiklund E.D., Gao S., Hulf T., Sibbritt T., Nair S., Costea D.E., Villadsen S.B., Bakholdt V., Bramsen J.B., Sorensen J.A., Krogdahl A., Clark S.J., Kjems J. MicroRNA alterations and associated aberrant DNA methylation patterns across multiple sample types in oral squamous cell carcinoma. PLoS ONE 2011, 6:e27840.
144. Wilting S.M., van Boerdonk R.A., Henken F.E., Meijer C.J., Diosdado B., Meijer G.A., le Sage C., Agami R., Snijders P.J., Steenbergen R.D. Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol. Cancer 2010, 9:167.
145. Xie G., Yao Q., Liu Y., Du S., Liu A., Guo Z., Sun A., Ruan J., Chen L., Ye C., Yuan Y. IL-6-induced epithelial-mesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int. J. Oncol. 2012, 40:1171-1179.
146. Xu Q., Wang L., Li H., Han Q., Li J., Qu X., Huang S., Zhao R.C. Mesenchymal stem cells play a potential role in regulating the establishment and maintenance of epithelial-mesenchymal transition in MCF7 human breast cancer cells by paracrine and induced autocrine TGF-beta. Int. J. Oncol. 2012.
147. Yan G.R., Xu S.H., Tan Z.L., Liu L., He Q.Y. Global identification of miR-373-regulated genes in breast cancer by quantitative proteomics. Proteomics 2011, 11:912-920.
148. Yang C.H., Yue J., Pfeffer S.R., Handorf C.R., Pfeffer L.M. MicroRNA miR-21 regulates the metastatic behavior of B16 melanoma cells. J. Biol. Chem. 2011, 286:39172-39178.
149. Yang J.S., Maurin T., Robine N., Rasmussen K.D., Jeffrey K.L., Chandwani R., Papapetrou E.P., Sadelain M., O'Carroll D., Lai E.C. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc. Nat. Acad. Sci. USA 2010, 107:15163-15168.
150. Yu F., Deng H., Yao H., Liu Q., Su F., Song E. Mir-30 reduction maintains self-renewal and inhibits apoptosis in breast tumor-initiating cells. Oncogene 2010, 29:4194-4204.
151. Yu F., Jiao Y., Zhu Y., Wang Y., Zhu J., Cui X., Liu Y., He Y., Park E.Y., Zhang H., Lv X., Ma K., Su F., Park J.H., Song E. MicroRNA 34c gene down-regulation via DNA methylation promotes self-renewal and epithelial-mesenchymal transition in breast tumor-initiating cells. J. Biol. Chem. 2012, 287:465-473.
152. Zekri L., Huntzinger E., Heimstadt S., Izaurralde E. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol. Cell. Biol. 2009, 29:6220-6231.
153. Zhang J., Zhang H., Liu J., Tu X., Zang Y., Zhu J., Chen J., Dong L. MiR-30 inhibits TGF-beta1-induced epithelial-to-mesenchymal transition in hepatocyte by targeting Snail1. Biochem. Biophys. Res. Commun. 2012, 417:1100-1105.
154. Zhao X., Dou W., He L., Liang S., Tie J., Liu C., Li T., Lu Y., Mo P., Shi Y., Wu K., Nie Y., Fan D. MicroRNA-7 functions as an anti-metastatic microRNA in gastric cancer by targeting insulin-like growth factor-1 receptor. Oncogene 2012.
155. Zheng F., Liao Y.J., Cai M.Y., Liu Y.H., Liu T.H., Chen S.P., Bian X.W., Guan X.Y., Lin M.C., Zeng Y.X., Kung H.F., Xie D. The putative tumour suppressor microRNA-124 modulates hepatocellular carcinoma cell aggressiveness by repressing ROCK2 and EZH2. Gut 2012, 61:278-289.
156. Zhu S., Wu H., Wu F., Nie D., Sheng S., Mo Y.Y. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 2008, 18:350-359.