Loss of SNAIL regulated miR-128-2 on chromosome 3p22.3 targets multiple stem cell factors to promote transformation of mammary epithelial cells

Cancer Research

Volumn 72, Issue 22, 2012, Pages 6036-6050

  Qian, PengXu ^a   Banerjee, Arindam ^d   Wu, Zheng Sheng ^a,b,c   Zhang, Xiao ^a   Wang, Hong ^a   Pandey, Vijay ^e   Zhang, Wei Jie ^a   Lv, Xue Fei ^a   Tan, Sheng ^a   Lobie, Peter E ^e   Zhu, Tao ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; CELL PROTEIN; KRUPPEL LIKE FACTOR 4; MICRORNA; MICRORNA 128 2; PROTEIN CSF1; PROTEIN KINASE B; PROTEIN LIN28A; STAT3 PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARPP21 GENE; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; BREAST EPITHELIUM; CANCER INVASION; CANCER MORPHOLOGY; CANCER SURVIVAL; CELL MIGRATION; CELLULAR DISTRIBUTION; CHROMOSOME 3P; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE DELETION; GENE DOSAGE; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOME ABERRATIONS; CHROMOSOMES, HUMAN, PAIR 3; DOWN-REGULATION; FEMALE; HUMANS; LOSS OF HETEROZYGOSITY; MICE; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; ONCOGENE PROTEIN V-AKT; STAT3 TRANSCRIPTION FACTOR; STEM CELL FACTOR; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS;

EID: 84869212635     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1507     Document Type: Article

References (50)

1. Albertson DG, Collins C, McCormick F, Gray JW. Chromosome aberrations in solid tumors. Nat Genet 2003;34:369-76.
2. Stratton MR. Exploring the genomes of cancer cells: progress and promise. Science 2011;331:1553-8.
3. Yang X, Lippman ME. BRCA1 and BRCA2 in breast cancer. Breast Cancer Res Treat 1999;54:1-10.
4. Yang Q, Yoshimura G, Mori I, Sakurai T, Kakudo K. Chromosome 3p and breast cancer. J Hum Genet 2002;47:453-9.
5. Maitra A, Wistuba II, Washington C, Virmani AK, Ashfaq R, Milchgrub S, et al. High-resolution chromosome 3p allelotyping of breast carcinomas and precursor lesions demonstrates frequent loss of heterozygosity and a discontinuous pattern of allele loss. Am J Pathol 2001;159:119-30.
6. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-33.
7. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006;6:857-66.
8. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, et al.Human microRNAgenes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A 2004;101:2999-3004.
9. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-8.
10. Qian P, Zuo Z, Wu Z, Meng X, Li G, Zhang W, et al. Pivotal role of reduced let-7g expression in breast cancer invasion and metastasis. Cancer Res 2011;71:6463-74.
11. Chen LC, Matsumura K, Deng G, Kurisu W, Ljung BM, Lerman MI, et al. Deletion of two separate regions on chromosome 3p in breast cancers. Cancer Res 1994;54:3021-4.
12. Matsumoto S, Kasumi F, Sakamoto G, Onda M, Nakamura Y, Emi M. Detailed deletion mapping of chromosome arm 3p in breast cancers: a 2-cM region on 3p14.3-21.1 and a 5-cM region on 3p24.3-25.1 commonly deleted in tumors. Genes Chromosomes Cancer 1997;20:268-74.
13. Pandey V, Perry JK, Mohankumar KM, Kong XJ, Liu SM, Wu ZS, et al. Autocrine human growth hormone stimulates oncogenicity of endometrial carcinoma cells. Endocrinology 2008;149:3909-19.
14. Tang JZ, Zuo ZH, Kong XJ, Steiner M, Yin Z, Perry JK, et al. Signal transducer and activator of transcription (STAT)-5A and STAT5B differentially regulate human mammary carcinoma cell behavior. Endocrinology 2010;151:43-55.
15. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucl Acids Res 2011;39:D152-7.
16. Sinha S, Singh RK, Alam N, Roy A, Roychoudhury S, Panda CK. Frequent alterations of hMLH1 and RBSP3/HYA22 at chromosomal 3p22.3 region in early and late-onset breast carcinoma: clinical and prognostic significance. Cancer Sci 2008;99:1984-91.
17. Trujillo KA, Hines WC, Vargas KM, Jones AC, Joste NE, Bisoffi M, et al. Breast field cancerization: isolation and comparison of telomerase-expressing cells in tumor and tumor adjacent, histologically normal breast tissue. Mol Cancer Res 2011;9:1209-21.
18. Gentner B, Schira G, Giustacchini A, Amendola M, Brown BD, Ponzoni M, et al. Stable knockdown of microRNA in vivo by lentiviral vectors. Nat Methods 2009;6:63-6.
19. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, McGrath CM, et al. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 1990;50:6075-86.
20. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
21. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-67.
22. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol 2004;2:e363.
23. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet 2005;37:495-500.
24. Jaenisch R, Young R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 2008;132:567-82.
25. Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G, et al. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res 2008;68:9125-30.
26. Lukacs RU, Memarzadeh S, Wu H, Witte ON. Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell Stem Cell 2010;7:682-93.
27. Papakonstanti EA, Zwaenepoel O, Bilancio A, Burns E, Nock GE, Houseman B, et al. Distinct roles of class IA PI3K isoforms in primary and immortalised macrophages. J Cell Sci 2008;121:4124-33.
28. Huang J, Chen T, Liu X, Jiang J, Li J, Li D, et al. More synergetic cooperation of Yamanaka factors in induced pluripotent stem cells than in embryonic stem cells. Cell Res 2009;19:1127-38.
29. Okita K, Yamanaka S. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr Stem Cell Res Ther 2006;1:103-11.
30. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-28.
31. Dang H, Ding W, Emerson D, Rountree CB. Snail1 induces epithelial-to-mesenchymal transition and tumor initiating stem cell characteristics. BMC Cancer 2011;11:396.
32. Loots GG, Ovcharenko I. rVISTA 2.0: evolutionary analysis of transcription factor binding sites. Nucl Acids Res 2004;32:W217-21.
33. Miettinen PJ, Ebner R, Lopez AR, Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994;127:2021-36.
34. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
35. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2002;62:65-74.
36. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
37. Afanasyeva EA, Mestdagh P, Kumps C, Vandesompele J, Ehemann V, Theissen J, et al. MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival. Cell Death Differ 2011;18:974-84.
38. Elyakim E, Sitbon E, Faerman A, Tabak S, Montia E, Belanis L, et al. hsa-miR-191 is a candidate oncogene target for hepatocellular carcinoma therapy. Cancer Res 2010;70:8077-87.
39. Shi X, Su S, Long J, Mei B, Chen Y. MicroRNA-191 targets N-deacetylase/N-sulfotransferase 1 and promotes cell growth in human gastric carcinoma cell line MGC803. Acta Biochim Biophys Sin (Shanghai) 2011;43:849-56.
40. Kent OA, Mullendore M, Wentzel EA, Lopez-Romero P, Tan AC, Alvarez H, et al. A resource for analysis of microRNA expression and function in pancreatic ductal adenocarcinoma cells. Cancer Biol Ther 2009;8:2013-24.
41. Tsuda H. Gene and chromosomal alterations in sporadic breast cancer: correlation with histopathological features and implications for genesis and progression. Breast Cancer 2009;16:186-201.
42. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG. Regulation of miRNA expression during neural cell specification. Eur J Neurosci 2005;21:1469-77.
43. Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X, et al. MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J Mol Med (Berl) 2009;87:43-51.
44. Adlakha YK, Saini N. MicroRNA-128 downregulates Bax and induces apoptosis in human embryonic kidney cells. Cell Mol Life Sci 2011;68:1415-28.
45. Evangelisti C, Florian MC, Massimi I, Dominici C, Giannini G, Galardi S, et al. MiR-128 up-regulation inhibits Reelin and DCX expression and reduces neuroblastoma cell motility and invasiveness. FASEB J 2009;23:4276-87.
46. Zhu Y, Yu F, Jiao Y, Feng J, Tang W, Yao H, et al. Reduced miR-128 in breast tumor-initiating cells induces chemotherapeutic resistance via Bmi-1 and ABCC5. Clin Cancer Res 2011;17:7105-15.
47. Wu Y, Zhou BP. Snail: more than EMT. Cell Adh Migr 2010;4:199-203.
48. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, van Roy F, et al. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 2007;26:7445-56.
49. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 2003;63:2172-8.
50. Yadav A, Kumar B, Datta J, Teknos TN, Kumar P. IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 2011;9:1658-67.