MicroRNA-mediated breast cancer metastasis: From primary site to distant organs

Oncogene

Volumn 31, Issue 20, 2012, Pages 2499-2511

  Wang, L ^a,b   Wang, J ^a  

^a GUANGZHOU GENERAL HOSPITAL OF GUANGZHOU MILITARY COMMAND   (China)

^b SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

breast cancer; EMT MET; metastasis; miRNA; stemness

Indexed keywords

BETA CATENIN; MICRORNA; PROTEIN BCL 2; UVOMORULIN; VASCULOTROPIN A;

ANGIOGENESIS; APOPTOSIS; BREAST METASTASIS; CANCER CELL; CANCER INVASION; CANCER PATIENT; CELL DIFFERENTIATION; CELL MIGRATION; DISTANT METASTASIS; DISTANT METASTASIS FREE SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SENESCENCE; TUMOR MICROENVIRONMENT; UNTRANSLATED REGION;

APOPTOSIS; BREAST NEOPLASMS; CELL AGING; CELL MOVEMENT; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PREDICTIVE VALUE OF TESTS; TUMOR MARKERS, BIOLOGICAL; TUMOR MICROENVIRONMENT;

EID: 84861345640     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.444     Document Type: Review

References (138)

1. Adams BD, Cowee DM, White BA. (2009). The role of miR-206 in the epidermal growth factor (EGF) induced repression of estrogen receptor-alpha (ERalpha) signaling and a luminal phenotype in MCF-7 breast cancer cells. Mol Endocrinol 23: 1215-1230.
2. Anand S, Majeti BK, Acevedo LM, Murphy EA, Mukthavaram R, Scheppke L et al. (2010). MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 16: 909-914.
3. Baffa R, Fassan M, Volinia S, O'Hara B, Liu CG, Palazzo JP et al. (2009). MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J Pathol 219: 214-221.
4. Bartel DP. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
5. Baum B, Settleman J, Quinlan MP. (2008). Transitions between epithelial and mesenchymal states in development and disease. Semin Cell Dev Biol 19: 294-308.
6. Berezikov E, Cuppen E, Plasterk RH. (2006). Approaches to microRNA discovery. Nat Genet 38: S2-S7.
7. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366. (Pubitemid 32151243)
8. Bhaumik D, Scott GK, Schokrpur S, Patil CK, Campisi J, Benz CC. (2008). Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene 27: 5643-5647.
9. Bourguignon LY, Wong G, Earle C, Krueger K, Spevak CC. (2010). Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, MicroRNA-10b expression and RhoA/RhoC upregulation leading to Rho-kinase-associated Cytoskeleton Activation and Breast Tumor Cell Invasion. J Biol Chem 285: 36721-36735.
10. Brabletz S, Brabletz T. (2010). The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep 11: 670-677.
11. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. (2005). Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749. (Pubitemid 41486367)
12. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF et al. (2008). A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68: 7846-7854.
13. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S et al. (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. (Pubitemid 351772923)
14. Cabodi S, Taverna D. (2010). Interfering with inflammation: a new strategy to block breast cancer self-renewal and progression? Breast Cancer Res 12: 305.
15. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S et al. (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101: 2999-3004. (Pubitemid 38327724)
16. Chiang AC, Massague J. (2008). Molecular basis of metastasis. N Engl J Med 359: 2814-2823.
17. Christoffersen NR, Silahtaroglu A, Orom UA, Kauppinen S, Lund AH. (2007). miR-200b mediates post-transcriptional repression of ZFHX1B. RNA 13: 1172-1178. (Pubitemid 47080461)
18. Cicek M, Fukuyama R, Welch DR, Sizemore N, Casey G. (2005). Breast cancer metastasis suppressor 1 inhibits gene expression by targeting nuclear factor-kB activity. Cancer Res 65: 3586-3595. (Pubitemid 40616334)
19. Connolly EC, Van Doorslaer K, Rogler LE, Rogler CE. (2010). Overexpression of miR-21 promotes an in vitro metastatic phenotype by targeting the tumor suppressor RHOB. Mol Cancer Res 8: 691-700.
20. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM et al. (2009). Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J 28: 347-358.
21. Davis BN, Hilyard AC, Lagna G, Hata A. (2008). SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454: 56-61. (Pubitemid 351931982)
22. Dean M, Fojo T, Bates S. (2005). Tumour stem cells and drug resistance. Nat Rev Cancer 5: 275-284. (Pubitemid 40488633)
23. Di Leva G, Gasparini P, Piovan C, Ngankeu A, Garofalo M, Taccioli C et al. (2010). MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J Natl Cancer Inst 102: 706-721.
24. Du J, Yang S, An D, Hu F, Yuan W, Zhai C et al. (2009). BMP-6 inhibits microRNA-21 expression in breast cancer through repressing deltaEF1 and AP-1. Cell Res 19: 487-496.
25. Dykxhoorn DM, Wu Y, Xie H, Yu F, Lal A, Petrocca F et al. (2009). miR-200 Enhances Mouse Breast Cancer Cell Colonization to Form Distant Metastases. PLoS One 4: e7181.
26. Edmonds MD, Hurst DR, Vaidya KS, Stafford LJ, Chen D, Welch DR. (2009). Breast cancer metastasis suppressor 1 coordinately regulates metastasis-associated microRNA expression. Int J Cancer 125: 1778-1785.
27. Esquela-Kerscher A, Slack FJ. (2006). Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269.
28. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E et al. (2007). microRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA 104: 15805-15810. (Pubitemid 350035380)
29. Fidler IJ. (1975). Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 35: 218-224.
30. Filipowicz W, Bhattacharyya SN, Sonenberg N. (2008). Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114.
31. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD et al. (2008). miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 15: 272-284.
32. Foekens JA, Sieuwerts AM, Smid M, Look MP, de Weerd V, Boersma AW et al. (2008). Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptor-positive human breast cancer. Proc Natl Acad Sci USA 105: 13021-13026.
33. Fö rstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD. (2007). Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 130: 287-297. (Pubitemid 47086327)
34. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH. (2008). Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283: 1026-1033.
35. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS et al. (2008). MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28: 5369-5380.
36. Garzon R, Marcucci G, Croce CM. (2010). Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 9: 775-789.
37. Gebeshuber CA, Zatloukal K, Martinez J. (2009). miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 10: 400-405.
38. Gee HE, Camps C, Buffa FM, Colella S, Sheldon H, Gleadle JM et al. (2008). MicroRNA-10b and breast cancer metastasis. Nature 455: E8-E9.
39. Gibbons DL, Lin W, Creighton CJ, Rizvi ZH, Gregory PA, Goodall GJ et al. (2009). Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev 23: 2140-2151.
40. Gö tte M, Mohr C, Koo CY, Stock C, Vaske AK, Viola M et al.(2010). 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, 29.6569-6580.
41. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. (2008). The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601. (Pubitemid 351627379)
42. Grelier G, Voirin N, Ay AS, Cox DG, Chabaud S, Treilleux I et al. (2009). Prognostic value of Dicer expression in human breast cancers and association with the mesenchymal phenotype. Br J Cancer 101: 673-683.
43. Grishok A, Pasquinelli AE, Conte D, Li N, Parrish S, Ha I et al. (2001). Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106: 23-34. (Pubitemid 32709955)
44. Hanahan D, Weinberg RA. (2011). Hallmarks of cancer: the next generation. Cell 144: 646-674.
45. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ. (2008). MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 105: 1516-1521. (Pubitemid 351346546)
46. Hedley BD, Chambers AF. (2009). Tumor dormancy and metastasis. Adv Cancer Res 102: 67-101.
47. Hirschmann-Jax C, Foster AE, Wulf GG et al. (2004). A distinct 'side population' of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 101: 14228-14233. (Pubitemid 39305058)
48. Horikawa T, Yang J, Kondo S, Yoshizaki T, Joab I, Furukawa M et al. (2007). Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 67: 1970-1978. (Pubitemid 46424213)
49. Hoser M, Baader SL, Bö sl MR, Ihmer A, Wegner M, Sock E. (2007). Prolonged glial expression of Sox4 in the CNS leads to architectural cerebellar defects and ataxia. J Neurosci 27: 5495-5505. (Pubitemid 46790178)
50. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S et al. (2008). The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10: 202-210. (Pubitemid 351194050)
51. Huang TH, Wu FT, Loeb GB, Hsu R, Heidersbach A, Brincat A et al. (2009). Up-regulation of miR-21 by HER2/neu Signaling Promotes Cell Invasion. J Biol Chem 284: 18515-18524.
52. Hurst DR, Edmonds MD, Scott GK, Benz CC, Vaidya KS, Welch DR. (2009a). Breast cancer metastasis suppressor 1, BRMS1, upregulates miR-146, which suppresses breast cancer metastasis. Cancer Res 69: 1279-1283.
53. Hurst DR, Edmonds MD, Welch DR. (2009b). Metastamir: the field of metastasis-regulatory microRNA is spreading. Cancer Res 69: 7495-7498.
54. Hurst DR, Xie Y, Vaidya KS, Mehta A, Moore BP, Accavitti-Loper MA et al. (2008). Alterations of BRMS1-ARID4A interaction modify gene expression but still suppress metastasis in human breast cancer cells. J Biol Chem 283: 7438-7444.
55. Hurteau GJ, Carlson JA, Spivack SD, Brock GJ. (2007). Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of Ecadherin. Cancer Res 67: 7972-7976. (Pubitemid 47395127)
56. Hutvá gner G, McLachlan J, Pasquinelli AE, Bá lint E, Tuschl T, Zamore PD. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838. (Pubitemid 32743968)
57. Iliopoulos D, Lindahl-Allen M, Polytarchou C, Hirsch HA, Tsichlis PN, Struhl K. (2010). Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 39: 761-772.
58. Iliopoulos D, Polytarchou C, Hatziapostolou M, Kottakis F, Maroulakou IG, Struhl K et al. (2009). MicroRNAs differentially regulated by Akt isoforms control EMT and stem cell renewal in cancer cells. Sci Signal 2: ra62.
59. Iorio MV, Casalini P, Piovan C, Di Leva G, Merlo A, Triulzi T et al. (2009). microRNA-205 regulates HER3 in human breast cancer. Cancer Res 69: 2195-2200.
60. Jin Z, Xie T. (2007). Dcr-1 maintains Drosophila ovarian stem cells. Curr Biol 17: 539-544. (Pubitemid 46401374)
61. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A et al. (2005). RAS is regulated by the let-7 microRNA family. Cell 120: 635-647. (Pubitemid 40343076)
62. Kang Y, Massagué J. (2004). Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118: 277-279. (Pubitemid 39061108)
63. Karin M. (2006). Nuclear factor-kappaB in cancer development and progression. Nature 441: 431-436. (Pubitemid 44050137)
64. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW et al. (2007). Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563. (Pubitemid 47525152)
65. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R et al. (2010). Transcriptional control of gene expression by microRNAs. Cell 140: 111-122.
66. Kim DH, Saetrom P, Snøove Jr O, Rossi JJ. (2008). MicroRNAdirected transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci USA 105: 16230-16235.
67. Kondo N, Toyama T, Sugiura H, Fujii Y, Yamashita H. (2008). miR-206 Expression is down-regulated in estrogen receptor alphapositive human breast cancer. Cancer Res 68: 5004-5008.
68. Kong W, Yang H, He L, Zhao JJ, Coppola D, Dalton WS et al. (2008). MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 28: 6773-6784.
69. Korpal M, Lee ES, Hu G, Kang Y. (2008). 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 283: 14910-14914.
70. Kumar MS, Pester RE, Chen CY, Lane K, Chin C, Lu J et al. (2009). Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 23: 2700-2704.
71. Leivonen SK, Mä kelä R, Ostling P, Kohonen P, Haapa-Paananen S, Kleivi K et al. (2009). Protein lysate microarray analysis to identify microRNAs regulating estrogen receptor signaling in breast cancer cell lines. Oncogene 28: 3926-3936.
72. Li F, Tiede B, Massagué J, Kang Y. (2007). Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res 17: 3-14. (Pubitemid 46096419)
73. Li QQ, Chen ZQ, Cao XX, Xu JD, Xu JW, Chen YY et al. (2011). Involvement of NF-kappaB/miR-448 regulatory feedback loop in chemotherapy-induced epithelial-mesenchymal transition of breast cancer cells. Cell Death Differ 18: 16-25.
74. Li S, Wang Q, Wang Y, Chen X, Wang Z. (2009a). PLC-gamma1 and Rac1 coregulate EGF-induced cytoskeleton remodeling and cell migration. Mol Endocrinol 23: 901-913.
75. Li XF, Yan PJ, Shao ZM. (2009b). Downregulation of miR-193b contributes to enhance urokinase-type plasminogen activator (uPA) expression and tumor progression and invasion in human breast cancer. Oncogene 28: 3937-3948.
76. Li X, Shen Y, Ichikawa H, Antes T, Goldberg GS. (2009c). Regulation of miRNA expression by Src and contact normalization: effects on nonanchored cell growth and migration. Oncogene 28: 4272-4283.
77. Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA et al. (2011). Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res 71: 1550-1560.
78. Lin SL, Chiang A, Chang D, Ying SY. (2008). Loss of miR-146a function in hormone-refractory prostate cancer. RNA 14: 417-424. (Pubitemid 351397806)
79. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D et al. (2005). MicroRNA expression profiles classify human cancers. Nature 435: 834-838. (Pubitemid 40839735)
80. Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, Colburn NH et al. (2008). MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 27: 4373-4379. (Pubitemid 352010003)
81. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG et al. (2010a). Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol 28: 341-347.
82. Ma L, Teruya-Feldstein J, Weinberg RA. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688. (Pubitemid 47552092)
83. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D et al. (2010b). miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 12: 247-271.
84. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. (Pubitemid 351636299)
85. Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S et al. (2010). A MicroRNA targeting dicer for metastasis control. Cell 141: 1195-1207.
86. Mayr C, Hemann MT, Bartel DP. (2007). Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315: 1576-1579. (Pubitemid 46449474)
87. Moriarty CH, Pursell B, Mercurio AM. (2010). miR-10b targets Tiam1: implications for Rac activation and carcinoma migration. J Biol Chem 285: 20541-20546.
88. Nicoloso MS, Spizzo R, Shimizu M, Rossi S, Calin GA. (2009). MicroRNAs-the micro steering wheel of tumour metastases. Nat Rev Cancer 9: 293-302.
89. Ørom UA, Nielsen FC, Lund AH. (2008). MicroRNA-10a binds the 50 UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30: 460-471. (Pubitemid 351672378)
90. Pandey DP, Picard D. (2009). miR-22 inhibits estrogen signaling by directly targeting the estrogen receptor alpha mRNA. Mol Cell Biol 29: 3783-3790.
91. Park SM, Gaur AB, Lengyel E, Peter ME. (2008). The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907. (Pubitemid 351482843)
92. Patel JB, Appaiah HN, Burnett RM, Bhat-Nakshatri P, Wang G, Mehta R et al. (2011). Control of EVI-1 oncogene expression in metastatic breast cancer cells through microRNA miR-22. Oncogene 30: 1290-1301.
93. Pawelek JM, Chakraborty AK. (2008). Fusion of tumour cells with bone marrow-derived cells: a unifying explanation for metastasis. Nat Rev Cancer 8: 377-386. (Pubitemid 351589699)
94. Phadke PA, Vaidya KS, Nash KT, Hurst DR, Welch DR. (2008). BRMS1 suppresses breast cancer experimental metastasis to multiple organs by inhibiting several steps of the metastatic process. Am J Pathol 172: 809-817. (Pubitemid 351354552)
95. Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. (2008). MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci USA 105: 1608-1613. (Pubitemid 351346562)
96. Polyak K, Weinberg RA. (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
97. Reddy SD, Ohshiro K, Rayala SK, Kumar R. (2008). MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Res 68: 8195-8200.
98. Reddy SD, Pakala SB, Ohshiro K, Rayala SK, Kumar R. (2009). MicroRNA-661, a c/EBPalpha target, inhibits metastatic tumor antigen 1 and regulates its functions. Cancer Res 69: 5639-5642.
99. Reya T, Morrison SJ, Clarke MF, Weissman IL. (2001). Stem cells, cancer, and cancer stem cells. Nature 414: 105-111. (Pubitemid 33041634)
100. Sachdeva M, Mo YY. (2010). MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res 70: 378-387.
101. Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S et al. (2009). p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci USA 106: 3207-3212.
102. Schickel R, Park SM, Murmann AE, Peter ME. (2010). miR-200c regulates induction of apoptosis through CD95 by targeting FAP-1. Mol Cell 38: 908-915.
103. Selaru FM, Olaru AV, Kan T, David S, Cheng Y, Mori Y et al. (2009). MicroRNA-21 is overexpressed in human cholangiocarcinoma and regulates programmed cell death 4 and tissue inhibitor of metalloproteinase 3. Hepatology 49: 1595-1601.
104. Sempere LF, Preis M, Yezefski T, Ouyang H, Suriawinata AA, Silahtaroglu A et al. (2010). Fluorescence-based codetection with protein markers reveals distinct cellular compartments for altered MicroRNA expression in solid tumors. Clin Cancer Res 16: 4246-4255.
105. Sethi G, Sung B, Aggarwal BB. (2008). Nuclear factor-kappaB activation: from bench to bedside. Exp Biol Med 233: 21-31.
106. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D et al. (2009). Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138: 592-603.
107. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. (2007). miR-21-mediated tumor growth. Oncogene 26: 2799-2803. (Pubitemid 46663837)
108. Song G, Zhang Y, Wang L. (2009). microRNA-206 targets NOTCH3, activates apoptosis, inhibits tumor cell migration and foci formation. J Biol Chem 284: 31921-31927.
109. Spizzo R, Nicoloso MS, Lupini L, Lu Y, Fogarty J, Rossi S et al. (2010). miR-145 participates with TP53 in a death-promoting regulatory loop and targets estrogen receptor-alpha in human breast cancer cells. Cell Death Differ 17: 246-254.
110. Stark A, Lin MF, Kheradpour P, Pedersen JS, Parts L, Carlson JW et al. (2007). Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219-232. (Pubitemid 350100553)
111. Su X, Chakravarti D, Cho MS, Liu L, Gi YJ, Liu YL et al. (2010). TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 467: 986-990.
112. Talmadge JE, Fidler IJ. (2010). AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 70: 5649-5669.
113. Tavazoie SF, Alarcó n C, Oskarsson T, Padua D, Wang Q, Bos PD et al. (2008). Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451: 147-152.
114. Thiery JP. (2002). Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
115. Uhlmann S, Zhang JD, Schwä ger A, Mannsperger H, Riazalhosseini Y, Burmester S et al. (2010). miR-200bc/429 cluster targets PLCgamma1 and differentially regulates proliferation and EGFdriven invasion than miR-200a/141 in breast cancer. Oncogene 29: 4297-4306.
116. Van Waes C. (2007). Nuclear factor-kappaB in development, prevention, and therapy of cancer. Clin Cancer Res 13: 1076-1082. (Pubitemid 46424045)
117. Vaidya KS, Harihar S, Stafford LJ, Stafford LJ, Hurst DR, Hicks DG et al. (2008). Breast cancer metastasis suppressor-1 differentially modulates growth factor signaling. J Biol Chem 283: 28354-28360.
118. Valastyan S, Benaich N, Chang A, Reinhardt F, Weinberg RA. (2009a). Concomitant suppression of three target genes can explain the impact of a microRNA on metastasis. Genes Dev 23: 2592-2597.
119. Valastyan S, Chang A, Benaich N, Reinhardt F, Weinberg RA. (2010). Concurrent suppression of integrin alpha5, radixin, and RhoA phenocopies the effects of miR-31 on metastasis. Cancer Res 70: 5147-5154.
120. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szá sz AM, Wang ZC et al. (2009b). A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137: 1032-1046.
121. Vetter G, Saumet A, Moes M, Vallar L, Le Béchec A, Laurini C et al. (2010). miR-661 expression in SNAI1-induced epithelial to mesenchymal transition contributes to breast cancer cell invasion by targeting Nectin-1 and StarD10 messengers. Oncogene 29: 4436-4448.
122. Waghorne C, Thomas M, Lagarde A, Kerbel RS, Breitman ML. (1988). Genetic evidence for progressive selection and overgrowth of primary tumors by metastatic cell subpopulations. Cancer Res 48: 6109-6114. (Pubitemid 18266809)
123. Wang K, Li J, Li S, Bolund L, Wiuf C. (2009). Estimation of tumor heterogeneity using CGH array data. BMC Bioinformatics 10: 12.
124. Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, Leedman PJ. (2009). Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 284: 5731-5741.
125. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A et al. (2009). The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495.
126. Wu F, Zhu S, Ding Y, Beck WT, Mo YY. (2009a). MicroRNAmediated regulation of Ubc9 expression in cancer cells. Clin Cancer Res 15: 1550-1557.
127. Wu H, Zhu S, Mo YY. (2009b). Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 19: 439-448.
128. Xu D, Takeshita F, Hino Y, Fukunaga S, Kudo Y, Tamaki A et al. (2011). miR-22 represses cancer progression by inducing cellular senescence. J Cell Biol 193: 409-424.
129. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL et al. (2008). MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 14: 2348-2360.
130. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C et al. (2004). Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939. (Pubitemid 38798858)
131. Yang J, Weinberg RA. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14: 818-829. (Pubitemid 351757205)
132. Yu F, Deng H, Yao H, Liu Q, Su F, Song E. (2010a). miR-30 reduction maintains self-renewal and inhibits apoptosis in breast tumor-initiating cells. Oncogene 29: 4194-4204.
133. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C et al. (2007). let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131: 1109-1123. (Pubitemid 350235025)
134. Yu Z, Wang C, Wang M, Li Z, Casimiro MC, Liu M et al. (2008). A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol 182: 509-517.
135. Yu Z, Willmarth NE, Zhou J, Katiyar S, Wang M, Liu Y et al. (2010b). microRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc Natl Acad Sci USA 107: 8231-8236.
136. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z et al. (2010). Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39: 133-144.
137. Zhu S, Si ML, Wu H, Mo YY. (2007). MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 282: 14328-14336. (Pubitemid 47100416)
138. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. (2008). MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18: 350-359. (Pubitemid 351333899)