MiR-155 promotes macroscopic tumor formation yet inhibits tumor dissemination from mammary fat pads to the lung by preventing EMT

Oncogene

Volumn 30, Issue 31, 2011, Pages 3440-3453

  Xiang, X ^a   Zhuang, X ^a   Ju, S ^a   Zhang, S ^b   Jiang, H ^a   Mu, J ^a   Zhang, L ^a   Miller, D ^a   Grizzle, W ^b   Zhang, H G ^a,c  

^a University of Louisville School of Medicine   (United States)

^b University of Alabama at Birmingham   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

epithelial tomesenchymal transition; miR 155; tumor metastasis

Indexed keywords

FAT; MICRORNA; MICRORNA 155; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST TUMOR; CANCER STAGING; CARCINOGENESIS; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HUMAN; IN VIVO STUDY; LUNG TUMOR; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

ADIPOSE TISSUE; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARCINOMA; CELL DEDIFFERENTIATION; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; LUNG NEOPLASMS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICRORNAS;

EID: 79961168650     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.54     Document Type: Article

References (45)

1. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA. (2009). Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119: 1438-1449.
2. Aokage K, Ishii G, Ohtaki Y, Yamaguchi Y, Hishida T, Yoshida J et al. (2011). Dynamic molecular changes associated with epithelial-mesenchymal transition and subsequent mesenchymal-epithelial transition in the early phase of metastatic tumor formation. Int J Cancer 128: 1585-1595.
3. Bukholm IK, Nesland JM, Borresen-Dale AL. (2000). Re-expression of E-cadherin, alpha-catenin and beta-catenin, but not of gamma-catenin, in metastatic tissue from breast cancer patients [see comments]. J Pathol 190: 15-19. (Pubitemid 30053348)
4. Chen CZ, Li L, Lodish HF, Bartel DP. (2004). MicroRNAs modulate hematopoietic lineage differentiation. Science 303: 83-86. (Pubitemid 38055775)
5. Cheng CW, Wu PE, Yu JC, Huang CS, Yue CT, Wu CW et al. (2001). Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 20: 3814-3823.
6. Chung KH, Hart CC, Al-Bassam S, Avery A, Taylor J, Patel PD et al. (2006). Polycistronic RNA polymerase II expression vectors for RNA interference based on BIC/miR-155. Nucleic Acids Res 34: e53.
7. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, Heerema N et al. (2006). Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci USA 103: 7024-7029.
8. Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF et al. (2005). Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA 102: 3627-3632. (Pubitemid 40354662)
9. Gallardo E, Navarro A, Vinolas N, Marrades RM, Diaz T, Gel B et al. (2009). miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis 30: 1903-1909.
10. 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.
11. Grizzle WE, Mountz JD, Yang PA, Xu X, Sun S, Van Zant GE et al. (2002). BXD recombinant inbred mice represent a novel T cell-mediated immune response tumor model. Int J Cancer 101: 270-279. (Pubitemid 34970896)
12. Han H-J, Russo J, Kohwi Y, Kohwi-Shigematsu T. (2008). SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452: 187-193. (Pubitemid 351380252)
13. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED et al. (2007). Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol 213: 374-383. (Pubitemid 47509716)
14. Iorio MV, Ferracin M, Liu C-G, Veronese A, Spizzo R, Sabbioni S et al. (2005). MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070. (Pubitemid 41161233)
15. Iorns E, Hnatyszyn HJ, Seo P, Clarke J, Ward T, Lippman M. (2010). The role of SATB1 in breast cancer pathogenesis. J Natl Cancer Inst 102: 1284-1296.
16. Jiang S, Zhang H-W, Lu M-H, He X-H, Li Y, Gu H et al. (2010). MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 70: 3119-3127.
17. Johnson MH. (2009). From mouse egg to mouse embryo: polarities, axes, and tissues. Annu Rev Cell Dev Biol 25: 483-512.
18. Katoh M. (2005). Epithelial-mesenchymal transition in gastric cancer (Review). Int J Oncol 27: 1677-1683.
19. Kong W, He L, Coppola M, Guo J, Esposito NN, Coppola D et al. (2010). MicroRNA-155 regulates cell survival, growth, and chemo-sensitivity by targeting FOXO3a in breast cancer. J Biol Chem 285: 17869-17879.
20. 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.
21. Li J, Huang H, Sun L, Yang M, Pan C, Chen W et al. (2009). MiR-21 indicates poor prognosis in tongue squamous cell carcinomas as an apoptosis inhibitor. Clin Cancer Res 15: 3998-4008.
22. Logullo AF, Nonogaki S, Pasini FS, Osorio CA, Soares FA, Brentani MM. (2010). Concomitant expression of epithelial-mesenchymal transition biomarkers in breast ductal carcinoma: association with progression. Oncol Rep 23: 313-320.
23. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D et al. (2010). miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 12: 247-256.
24. Nakaya Y, Kuroda S, Katagiri YT, Kaibuchi K, Takahashi Y. (2004). Mesenchymal-epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1. Dev Cell 7: 425-438. (Pubitemid 39232977)
25. Nguyen DX, Bos PD, Massague J. (2009). Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9: 274-284.
26. Park S-M, 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)
27. Peinado H, Olmeda D, Cano A. (2007). Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428. (Pubitemid 46809165)
28. Polyak K, Weinberg RA. (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
29. Pulaski BA, Ostrand-Rosenberg S. (2001). Mouse 4T1 breast tumor model. Current Protocols in Immunology, Vol. 4, Ch. 20. John Wiley: New York, p. 20.2.1.
30. Ryu JK, Hong SM, Karikari CA, Hruban RH, Goggins MG, Maitra A. (2010). Aberrant MicroRNA-155 expression is an early event in the multistep progression of pancreatic adenocarcinoma. Pancrea-tology 10: 66-73.
31. Sobrado VR, Moreno-Bueno G, Cubillo E, Holt LJ, Nieto MA, Portillo F et al. (2009). The class I bHLH factors E2-2A and E2-2B regulate EMT. J Cell Sci 122: 1014-1024.
32. Soltermann A, Tischler V, Arbogast S, Braun J, Probst-Hensch N, Weder W et al. (2008). Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer. Clin Cancer Res 14: 7430-7437.
33. Stewart TJ, Abrams SI. (2007). Altered immune function during long-term host-tumor interactions can be modulated to retard autochthonous neoplastic growth. J Immunol 179: 2851-2859.
34. Thiery JP, Acloque H, Huang RYJ, Nieto MA. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
35. Thompson EW, Williams ED. (2008). EMT and MET in carcinoma-clinical observations, regulatory pathways and new models. Clin Exp Metastasis 25: 591-592.
36. Tsuji T, Ibaragi S, Hu G-f. (2009a). Epithelial-Mesenchymal Transition and Cell Cooperativity in Metastasis. Cancer Res 69: 7135-7139.
37. Tsuji T, Ibaragi S, Hu GF. (2009b). Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res 69: 7135-7139.
38. Tsuji T, Ibaragi S, Shima K, Hu MG, Katsurano M, Sasaki A et al. (2008). Epithelial-mesenchymal transition induced by growth suppressor p12CDK2-AP1 promotes tumor cell local invasion but suppresses distant colony growth. Cancer Res 68: 10377-10386.
39. Tusher VG, Tibshirani R, Chu G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121. (Pubitemid 32397092)
40. Wang B, Majumder S, Nuovo G, Kutay H, Volinia S, Patel T et al. (2009). Role of microRNA-155 at early stages of hepatocarcinogen-esis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology 50: 1152-1161.
41. Wells A, Yates C, Shepard CR. (2008). E-cadherin as an indicator of mesenchymal to epithelial reverting transitions during the metastatic seeding of disseminated carcinomas. Clin Exp Metastasis 25: 621-628.
42. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. (2009). Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228-234.
43. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M et al. (2006). Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9: 189-198. (Pubitemid 43357945)
44. 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)
45. Zhao S, Fernald RD. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12: 1047-1064. (Pubitemid 41580022)