Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Kong, Dejuan ^a   Banerjee, Sanjeev ^a   Ahmad, Aamir ^a   Li, Yiwei ^a   Wang, Zhiwei ^a   Sethi, Seema ^a   Sarkar, Fazlul H ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 200; NOTCH1 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN LET 7; PROTEIN LIN28B; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TUMOR PROTEIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; LIN28B PROTEIN, HUMAN; LYMPHOKINE; MIRN200 MICRORNA, HUMAN; MIRNLET7 MICRORNA, HUMAN; NANOG PROTEIN, HUMAN; PDGFD PROTEIN, HUMAN; PLATELET DERIVED GROWTH FACTOR; POU5F1 PROTEIN, HUMAN; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER STEM CELL; CANCER TISSUE; CARCINOGENICITY; CELL RENEWAL; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENETIC TRANSFECTION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PROSTATE CANCER; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; EPITHELIUM CELL; GENETICS; HUMAN; MESODERM; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

MUS;

ANIMALS; BASE SEQUENCE; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DNA-BINDING PROTEINS; DOWN-REGULATION; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; HOMEODOMAIN PROTEINS; HUMANS; LYMPHOKINES; MALE; MESODERM; MICE; MICRORNAS; NEOPLASTIC STEM CELLS; OCTAMER TRANSCRIPTION FACTOR-3; PHENOTYPE; PLATELET-DERIVED GROWTH FACTOR; PROSTATIC NEOPLASMS; RECEPTOR, NOTCH1; SOXB1 TRANSCRIPTION FACTORS;

EID: 77957902732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012445     Document Type: Article

References (47)

1. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768.
2. Wang X, Kruithof-de JM, Economides KD, Walker D, Yu H, et al. (2009) A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 461: 495-500.
3. Roudier MP, True LD, Higano CS, Vesselle H, Ellis W, et al. (2003) Phenotypic heterogeneity of end-stage prostate carcinoma metastatic to bone. Hum Pathol 34: 646-653.
4. Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, et al. (2008) Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321: 699-702.
5. Yu J, Vodyanik MA, Smuga-Otto K, ntosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
6. Gu G, Yuan J, Wills M, Kasper S (2007) Prostate cancer cells with stem cell characteristics reconstitute the original human tumor in vivo. Cancer Res 67: 4807-4815.
7. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507.
8. Jeter CR, Badeaux M, Choy G, Chandra D, Patrawala L, et al. (2009) Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells 27: 993-1005.
9. Sotomayor P, Godoy A, Smith GJ, Huss WJ (2009) Oct4A is expressed by a subpopulation of prostate neuroendocrine cells. Prostate 69: 401-410.
10. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
11. Kasper S (2009) Identification, characterization, and biological relevance of prostate cancer stem cells from clinical specimens. Urol Oncol 27: 301-303.
12. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
13. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, et al. (2009) Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 69: 2887-2895.
14. Cano A, Nieto MA (2008) Non-coding RNAs take centre stage in epithelial-to-mesenchymal transition. Trends Cell Biol 18: 357-359.
15. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, 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.
16. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, et al. (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138: 592-603.
17. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, et al. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495.
18. Yu F, Yao H, Zhu P, Zhang X, Pan Q, et al. (2007) let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131: 1109-1123.
19. Viswanathan SR, Daley GQ, Gregory RI (2008) Selective blockade of microRNA processing by Lin28. Science 320: 97-100.
20. Kasper S (2008) Stem cells: The root of prostate cancer? J Cell Physiol 216: 332-336.
21. Marian CO, Shay JW (2009) Prostate tumor-initiating cells: a new target for telomerase inhibition therapy? Biochim Biophys Acta 1792: 289-296.
22. Hollier BG, Evans K, Mani SA (2009) The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. J Mammary Gland Biol Neoplasia 14: 29-43.
23. Peter ME (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8: 843-852.
24. Fischer AN, Fuchs E, Mikula M, Huber H, Beug H, et al. (2007) PDGF essentially links TGF-beta signaling to nuclear beta-catenin accumulation in hepatocellular carcinoma progression. Oncogene 26: 3395-3405.
25. Yang L, Lin C, Liu ZR (2006) P68 RNA helicase mediates PDGF-induced epithelial mesenchymal transition by displacing Axin from beta-catenin. Cell 127: 139-155.
26. Kong D, Wang Z, Sarkar SH, Li Y, Banerjee S, et al. (2008) Platelet-derived growth factor-D overexpression contributes to epithelial-mesenchymal transition of PC3 prostate cancer cells. Stem Cells 26: 1425-1435.
27. Kong D, Banerjee S, Huang W, Li Y, Wang Z, et al. (2008) Mammalian target of rapamycin repression by 3,3′-diindolylmethane inhibits invasion and angiogenesis in platelet-derived growth factor-D-overexpressing PC3 cells. Cancer Res 68: 1927-1934.
28. Kong D, Li Y, Wang Z, Banerjee S, Ahmad A, et al. (2009) miR-200 Regulates PDGF-D-Mediated Epithelial-Mesenchymal Transition, Adhesion, and Invasion of Prostate Cancer Cells. Stem Cells 27: 1712-1721.
29. Li H, Fredriksson L, Li X, Eriksson U (2003) PDGF-D is a potent transforming and angiogenic growth factor. Oncogene 22: 1501-1510.
30. Wang Z, Kong D, Banerjee S, Li Y, Adsay NV, et al. (2007) Down-regulation of platelet-derived growth factor-D inhibits cell growth and angiogenesis through inactivation of Notch-1 and nuclear factor-kappaB signaling. Cancer Res 67: 11377-11385.
31. Ustach CV, Kim HR (2005) Platelet-derived growth factor D is activated by urokinase plasminogen activator in prostate carcinoma cells. Mol Cell Biol 25: 6279-6288.
32. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
33. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
34. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
35. Fox V, Gokhale PJ, Walsh JR, Matin M, Jones M, et al. (2008) Cell-cell signaling through NOTCH regulates human embryonic stem cell proliferation. Stem Cells 26: 715-723.
36. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, et al. (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442: 823-826.
37. Bussing I, Slack FJ, Grosshans H (2008) let-7 microRNAs in development, stem cells and cancer. Trends Mol Med 14: 400-409.
38. Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, et al. (2009) Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis 26: 433-446.
39. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, et al. (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
40. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, 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.
41. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, 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.
42. Melton C, Judson RL, Blelloch R (2010) Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463: 621-626.
43. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
44. Ali S, Ahmad A, Banerjee S, Padhye S, Dominiak K, et al. (2010) Gemcitabine sensitivity can be induced in pancreatic cancer cells through modulation of miR-200 and miR-21 expression by curcumin or its analogue CDF. Cancer Res 70: 3606-3617.
45. Li Y, VandenBoom TG, Kong D, Wang Z, Ali S, et al. (2009) Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 69: 6704-6712.
46. Xu J, Wang R, Xie ZH, Odero-Marah V, Pathak S, et al. (2006) Prostate cancer metastasis: role of the host microenvironment in promoting epithelial to mesenchymal transition and increased bone and adrenal gland metastasis. Prostate 66: 1664-1673.
47. Kong D, Li Y, Wang Z, Banerjee S, Sarkar FH (2007) Inhibition of angiogenesis and invasion by 3,3′-diindolylmethane is mediated by the nuclear factor-kappaB downstream target genes MMP-9 and uPA that regulated bioavailability of vascular endothelial growth factor in prostate cancer. Cancer Res 67: 3310-3319.