Inflammation linking EMT and cancer stem cells

Oral Oncology

Volumn 48, Issue 11, 2012, Pages 1068-1075

  Zhou, Chenchen ^a   Liu, Jeffrey ^a,b   Tang, Yaling ^a   Liang, Xinhua ^a  

^a SICHUAN UNIVERSITY   (China)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

Cancer stem cells (CSCs); Epithelial mesenchymal transition (EMT); Inflammation microenvironment

Indexed keywords

ALDEHYDE DEHYDROGENASE; BETA CATENIN; DEXAMETHASONE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MICRORNA; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UVOMORULIN; WNT PROTEIN;

CAENORHABDITIS ELEGANS; CANCER CELL; CANCER GROWTH; CANCER INVASION; CANCER STEM CELL; CARCINOGENICITY; CELL ADHESION; CELL DIFFERENTIATION; DROSOPHILA; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENETIC TRANSCRIPTION; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; INFLAMMATION; MACROPHAGE; METASTASIS; MICROENVIRONMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; WOUND HEALING;

CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; INFLAMMATION; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; TUMOR MARKERS, BIOLOGICAL; TUMOR MICROENVIRONMENT;

EID: 84867886641     PISSN: 13688375     EISSN: 18790593     Source Type: Journal    
DOI: 10.1016/j.oraloncology.2012.06.005     Document Type: Review

References (203)

1. D.J. Moskovic, J.R. Smolarz, D. Stanley, C. Jimenez, M.D. Williams, and E.Y. Hanna Malignant head and neck paragangliomas: is there an optimal treatment strategy? Head Neck Oncol 2 2010 23
2. I.J. Fidler The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited Nat Rev Cancer 3 6 2003 453 458
3. A. Mantovani Cancer: inflaming metastasis Nature 457 7225 2009 36 37
4. M.J. Bissell, and W.C. Hines Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression Nat Med 17 3 2011 320 329
5. G. Lorusso, and C. Ruegg The tumor microenvironment and its contribution to tumor evolution toward metastasis Histochem Cell Biol 130 6 2008 1091 1103
6. A. Mantovani, P. Allavena, A. Sica, and F. Balkwill Cancer-related inflammation Nature 454 7203 2008 436 444
7. F. Balkwill, and A. Mantovani Inflammation and cancer: back to Virchow? Lancet 357 9255 2001 539 545
8. A. Mantovani Molecular pathways linking inflammation and cancer Curr Mol Med 10 4 2010 369 373
9. P. Allavena, C. Garlanda, M.G. Borrello, A. Sica, and A. Mantovani Pathways connecting inflammation and cancer Curr Opin Genet Dev 18 1 2008 3 10
10. S.I. Grivennikov, F.R. Greten, and M. Karin Immunity, inflammation, and cancer Cell 140 6 2010 883 899
11. S. Kim, H. Takahashi, W.W. Lin, P. Descargues, S. Grivennikov, and Y. Kim Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis Nature 457 7225 2009 102 106
12. R.N. Kaplan, R.D. Riba, S. Zacharoulis, A.H. Bramley, L. Vincent, and C. Costa VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche Nature 438 7069 2005 820 827
13. K.E. de Visser, A. Eichten, and L.M. Coussens Paradoxical roles of the immune system during cancer development Nat Rev Cancer 6 1 2006 24 37
14. M.M. Markiewski, R.A. DeAngelis, F. Benencia, S.K. Ricklin-Lichtsteiner, A. Koutoulaki, and C. Gerard Modulation of the antitumor immune response by complement Nat Immunol 9 11 2008 1225 1235
15. P. Andreu, M. Johansson, N.I. Affara, F. Pucci, T. Tan, and S. Junankar FcRgamma activation regulates inflammation-associated squamous carcinogenesis Cancer Cell 17 2 2010 121 134
16. R. Kalluri EMT: when epithelial cells decide to become mesenchymal-like cells J Clin Invest 119 6 2009 1417 1419
17. A. Singh, and J. Settleman EMT, cancer stem cells and drug resistance. an emerging axis of evil in the war on cancer Oncogene 29 34 2010 4741 4751
18. P. Sansone, and J. Bromberg Environment, inflammation, and cancer Curr Opin Genet Dev 21 1 2011 80 85
19. J.M. Lopez-Novoa, and M.A. Nieto Inflammation and EMT: an alliance towards organ fibrosis and cancer progression EMBO Mol Med 1 6-7 2009 303 314
20. A. Stockinger, A. Eger, J. Wolf, H. Beug, and R. Foisner E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity J Cell Biol 154 6 2001 1185 1196
21. R. Kalluri, and R.A. Weinberg The basics of epithelial-mesenchymal transition J Clin Invest 119 6 2009 1420 1428
22. H. Acloque, M.S. Adams, K. Fishwick, M. Bronner-Fraser, and M.A. Nieto Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease J Clin Invest 119 2009 1438 1449
23. D.C. Radisky, and M.A. LaBarge Epithelial-mesenchymal transition and the stem cell phenotype Cell Stem Cell 2 6 2008 511 512
24. J.P. Thiery, and J.P. Sleeman Complex networks orchestrate epithelial-mesenchymal transitions Nat Rev Mol Cell Biol 7 2 2006 131 142
25. J.P. Thiery, H. Acloque, R.Y. Huang, and M.A. Nieto Epithelial- mesenchymal transitions in development and disease Cell 139 5 2009 871 890
26. T. Brabletz, A. Jung, S. Spaderna, F. Hlubek, and T. Kirchner Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression Nat Rev Cancer 5 9 2005 744 749
27. R. Reuter, B. Grunewald, and M. Leptin A role for the mesoderm in endodermal migration and morphogenesis in Drosophila Development 119 4 1993 1135 1145
28. C. LaBonne, and M. Bronner-Fraser Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration Dev Biol 221 1 2000 195 205
29. K.W. Cho, B. Blumberg, H. Steinbeisser, and E.M. De Robertis Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid Cell 67 6 1991 1111 1120
30. C. Scheel, E.N. Eaton, S.H. Li, C.L. Chaffer, F. Reinhardt, and K.J. Kah Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast Cell 145 6 2011 926 940
31. M. Oft, J. Peli, C. Rudaz, H. Schwarz, H. Beug, and E. Reichmann TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells Genes Dev 10 19 1996 2462 2477
32. R.C. Bates, and A.M. Mercurio Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids Mol Biol Cell 14 5 2003 1790 1800
33. J. Zavadil, L. Cermak, N. Soto-Nieves, and E.P. Bottinger Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition EMBO J 23 5 2004 1155 1165
34. S.S. Karhadkar, G.S. Bova, N. Abdallah, S. Dhara, D. Gardner, and A. Maitra Hedgehog signalling in prostate regeneration, neoplasia and metastasis Nature 431 7009 2004 707 712
35. J.I. Yook, X.Y. Li, I. Ota, C. Hu, H.S. Kim, and N.H. Kim A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells Nat Cell Biol 8 12 2006 1398 1406
36. J. Condeelis, and J.W. Pollard Macrophages: obligate partners for tumor cell migration, invasion, and metastasis Cell 124 2 2006 263 266
37. C.L. Chaffer, and R.A. Weinberg A perspective on cancer cell metastasis Science 331 6024 2011 1559 1564
38. A. Lochter, S. Galosy, J. Muschler, N. Freedman, Z. Werb, and M.J. Bissell Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells J Cell Biol 139 7 1997 1861 1872
39. J.P. Thiery Epithelial-mesenchymal transitions in tumour progression Nat Rev Cancer 2 6 2002 442 454
40. R. Kalluri, and M. Zeisberg Fibroblasts in cancer Nat Rev Cancer 6 5 2006 392 401
41. S.C. Lebret, D.F. Newgreen, E.W. Thompson, and M.L. Ackland Induction of epithelial to mesenchymal transition in PMC42-LA human breast carcinoma cells by carcinoma-associated fibroblast secreted factors Breast Cancer Res 9 1 2007 R19
42. E. Giannoni, F. Bianchini, L. Calorini, and P. Chiarugi Cancer associated fibroblasts exploit reactive oxygen species through a proinflammatory signature leading to epithelial mesenchymal transition and stemness Antioxid Redox Signal 14 12 2011 2361 2371
43. F.R. Greten, L. Eckmann, T.F. Greten, J.M. Park, Z.W. Li, and L.J. Egan IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer Cell 118 3 2004 285 296
44. E. Pikarsky, R.M. Porat, I. Stein, R. Abramovitch, S. Amit, and S. Kasem NF-kappaB functions as a tumour promoter in inflammation-associated cancer Nature 431 7007 2004 461 466
45. S. Maeda, L.C. Hsu, H. Liu, L.A. Bankston, M. Iimura, and M.F. Kagnoff Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing Science 307 5710 2005 734 738
46. M. Karin NF-kappaB and cancer: mechanisms and targets Mol Carcinog 45 6 2006 355 361
47. R.E. Bachelder, S.O. Yoon, C. Franci, A.G. de Herreros, and A.M. Mercurio Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition J Cell Biol 168 1 2005 29 33
48. S. Julien, I. Puig, E. Caretti, J. Bonaventure, L. Nelles, and F. van Roy Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition Oncogene 26 53 2007 7445 7456
49. Y. Wu, J. Deng, P.G. Rychahou, S. Qiu, B.M. Evers, and B.P. Zhou Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion Cancer Cell 15 5 2009 416 428
50. T.D. Tlsty, and L.M. Coussens Tumor stroma and regulation of cancer development Annu Rev Pathol 1 2006 119 150
51. H. Yu, D. Pardoll, and R. Jove STATs in cancer inflammation and immunity: a leading role for STAT3 Nat Rev Cancer 9 11 2009 798 809
52. A.O. Rehman Wang CY.CXCL12/SDF-1 alpha activates NF-kappaB and promotes oral cancer invasion through the Carma3/Bcl10/Malt1 complex. Int J Oral Sci 1 3 2009 105 118
53. R. Strippoli, I. Benedicto, M.L. Perez Lozano, A. Cerezo, M. Lopez-Cabrera, and M.A. del Pozo Epithelial-to-mesenchymal transition of peritoneal mesothelial cells is regulated by an ERK/NF-kappaB/Snail1 pathway Dis Model Mech 1 4-5 2008 264 274
54. K. Lin, S. Baritaki, L. Militello, G. Malaponte, Y. Bevelacqua, and B. Bonavida The role of B-RAF mutations in melanoma and the induction of EMT via dysregulation of the NF-kappaB/Snail/RKIP/PTEN circuit Genes Cancer 1 5 2010 409 420
55. A.J. Pantuck, J. An, H. Liu, and M.B. Rettig NF-kappaB-dependent plasticity of the epithelial to mesenchymal transition induced by Von Hippel-Lindau inactivation in renal cell carcinomas Cancer Res 70 2 2010 752 761
56. S. Baritaki, A. Chapman, K. Yeung, D.A. Spandidos, M. Palladino, and B. Bonavida Inhibition of epithelial to mesenchymal transition in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: pivotal roles of Snail repression and RKIP induction Oncogene 28 40 2009 3573 3585
57. Q.Q. Li, Z.Q. Chen, X.X. Cao, J.D. Xu, J.W. Xu, and Y.Y. Chen Involvement of NF-kappaB/miR-448 regulatory feedback loop in chemotherapy-induced epithelial-mesenchymal transition of breast cancer cells Cell Death Differ 18 1 2011 16 25
58. N. Gavert, A. Vivanti, J. Hazin, T. Brabletz, and A. Ben-Ze'ev L1-mediated colon cancer cell metastasis does not require changes in EMT and cancer stem cell markers Mol Cancer Res 9 1 2011 14 24
59. M. de Graauw, M.H. van Miltenburg, M.K. Schmidt, C. Pont, R. Lalai, and J. Kartopawiro Annexin A1 regulates TGF-beta signaling and promotes metastasis formation of basal-like breast cancer cells Proc Natl Acad Sci USA 107 14 2010 6340 6345
60. J. Yang, and R.A. Weinberg Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis Dev Cell 14 6 2008 818 829
61. D.L. Franco, J. Mainez, S. Vega, P. Sancho, M.M. Murillo, and C.A. de Frutos Snail1 suppresses TGF-beta-induced apoptosis and is sufficient to trigger EMT in hepatocytes J Cell Sci 123 Pt 20 2010 3467 3477
62. K.E. Hoot, J. Lighthall, G. Han, S.L. Lu, A. Li, and W. Ju Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression J Clin Invest 118 8 2008 2722 2732
63. H. Peinado, M. Quintanilla, and A. Cano Transforming growth factor beta-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions J Biol Chem 278 23 2003 21113 21123
64. N. Bardeesy, K.H. Cheng, J.H. Berger, G.C. Chu, J. Pahler, and P. Olson Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer Genes Dev 20 22 2006 3130 3146
65. U. Valcourt, M. Kowanetz, H. Niimi, C.H. Heldin, and A. Moustakas TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition Mol Biol Cell 16 4 2005 1987 2002
66. S. Dooley, J. Hamzavi, L. Ciuclan, P. Godoy, I. Ilkavets, and S. Ehnert Hepatocyte-specific Smad7 expression attenuates TGF-beta-mediated fibrogenesis and protects against liver damage Gastroenterology 135 2 2008 642 659
67. P. Papageorgis, A.W. Lambert, S. Ozturk, F. Gao, H. Pan, and U. Manne Smad signaling is required to maintain epigenetic silencing during breast cancer progression Cancer Res 70 3 2010 968 978
68. A.V. Bakin, C. Rinehart, A.K. Tomlinson, and C.L. Arteaga P38 mitogen-activated protein kinase is required for TGFbeta-mediated fibroblastic transdifferentiation and cell migration J Cell Sci 115 Pt 15 2002 3193 3206
69. R. Perlman, W.P. Schiemann, M.W. Brooks, H.F. Lodish, and R.A. Weinberg TGF-beta-induced apoptosis is mediated by the adapter protein Daxx that facilitates JNK activation Nat Cell Biol 3 8 2001 708 714
70. J. Zavadil, M. Bitzer, D. Liang, Y.C. Yang, A. Massimi, and S. Kneitz Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta Proc Natl Acad Sci USA 98 12 2001 6686 6691
71. M. Arsura, G.R. Panta, J.D. Bilyeu, L.G. Cavin, M.A. Sovak, and A.A. Oliver Transient activation of NF-kappaB through a TAK1/IKK kinase pathway by TGF-beta1 inhibits AP-1/SMAD signaling and apoptosis: implications in liver tumor formation Oncogene 22 3 2003 412 425
72. J.I. Park, M.G. Lee, K. Cho, B.J. Park, K.S. Chae, and D.S. Byun Transforming growth factor-beta1 activates interleukin-6 expression in prostate cancer cells through the synergistic collaboration of the Smad2, p38-NF-kappaB, JNK, and Ras signaling pathways Oncogene 22 28 2003 4314 4332
73. J.R. Neil, and W.P. Schiemann Altered TAB1:I kappaB kinase interaction promotes transforming growth factor beta-mediated nuclear factor-kappaB activation during breast cancer progression Cancer Res 68 5 2008 1462 1470
74. A. Chaudhury, G.S. Hussey, P.S. Ray, G. Jin, P.L. Fox, and P.H. Howe TGF-beta-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI Nat Cell Biol 12 3 2010 286 293
75. S.A. Rajasekaran, T.P. Huynh, D.G. Wolle, C.E. Espineda, L.J. Inge, and A. Skay Na, K-ATPase subunits as markers for epithelial-mesenchymal transition in cancer and fibrosis Mol Cancer Ther 9 6 2010 1515 1524
76. M. Natsuizaka, S. Ohashi, G.S. Wong, A. Ahmadi, R.A. Kalman, and D. Budo Insulin-like growth factor-binding protein-3 promotes transforming growth factor-{beta}1-mediated epithelial-to-mesenchymal transition and motility in transformed human esophageal cells Carcinogenesis 31 8 2010 1344 1353
77. B. Kong, C.W. Michalski, X. Hong, N. Valkovskaya, S. Rieder, and I. Abiatari AZGP1 is a tumor suppressor in pancreatic cancer inducing mesenchymal-to-epithelial transdifferentiation by inhibiting TGF-beta-mediated ERK signaling Oncogene 29 37 2010 5146 5158
78. D.S. Micalizzi, C.A. Wang, S.M. Farabaugh, W.P. Schiemann, and H.L. Ford Homeoprotein Six1 increases TGF-beta type I receptor and converts TGF-beta signaling from suppressive to supportive for tumor growth Cancer Res 70 24 2010 10371 10380
79. G. Moreno-Bueno, F. Portillo, and A. Cano Transcriptional regulation of cell polarity in EMT and cancer Oncogene 27 55 2008 6958 6969
80. H. Peinado, D. Olmeda, and A. Cano Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7 6 2007 415 428
81. J. Braun, C. Hoang-Vu, H. Dralle, and S. Huttelmaier Downregulation of microRNAs directs the EMT and invasive potential of anaplastic thyroid carcinomas Oncogene 29 29 2010 4237 4244
82. P.A. Gregory, A.G. Bert, E.L. Paterson, S.C. Barry, A. Tsykin, and G. Farshid The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1 Nat Cell Biol 10 5 2008 593 601
83. M. Korpal, E.S. Lee, G. Hu, and Y. Kang 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 22 2008 14910 14914
84. W. Kong, H. Yang, L. He, J.J. Zhao, D. Coppola, and W.S. Dalton 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 22 2008 6773 6784
85. S. Zhu, M.L. Si, H. Wu, and Y.Y. Mo MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1) J Biol Chem 282 19 2007 14328 14336
86. S. Zhu, H. Wu, F. Wu, D. Nie, S. Sheng, and Y.Y. Mo MicroRNA-21 targets tumor suppressor genes in invasion and metastasis Cell Res 18 3 2008 350 359
87. N. Dumont, M.B. Wilson, Y.G. Crawford, P.A. Reynolds, M. Sigaroudinia, and T.D. Tlsty Sustained induction of epithelial to mesenchymal transition activates DNA methylation of genes silenced in basal-like breast cancers Proc Natl Acad Sci USA 105 39 2008 14867 14872
88. C. Yan, W.A. Grimm, W.L. Garner, L. Qin, T. Travis, and N. Tan Epithelial to mesenchymal transition in human skin wound healing is induced by tumor necrosis factor-alpha through bone morphogenic protein-2 Am J Pathol 176 5 2010 2247 2258
89. B. Baran, I. Bechyne, M. Siedlar, K. Szpak, B. Mytar, and J. Sroka Blood monocytes stimulate migration of human pancreatic carcinoma cells in vitro: the role of tumour necrosis factor-alpha Eur J Cell Biol 88 12 2009 743 752
90. E. Takahashi, O. Nagano, T. Ishimoto, T. Yae, Y. Suzuki, and T. Shinoda Tumor necrosis factor-alpha regulates transforming growth factor-beta-dependent epithelial-mesenchymal transition by promoting hyaluronan-CD44-moesin interaction J Biol Chem 285 6 2010 4060 4073
91. J.L. Luo, W. Tan, J.M. Ricono, O. Korchynskyi, M. Zhang, and S.L. Gonias Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin Nature 446 7136 2007 690 694
92. J.L. Luo, S. Maeda, L.C. Hsu, H. Yagita, and M. Karin Inhibition of NF-kappaB in cancer cells converts inflammation- induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression Cancer cell 6 3 2004 297 305
93. Q. Zhang, B.T. Helfand, T.L. Jang, L.J. Zhu, L. Chen, and X.J. Yang Nuclear factor-kappaB-mediated transforming growth factor-beta-induced expression of vimentin is an independent predictor of biochemical recurrence after radical prostatectomy Clin Cancer Res 15 10 2009 3557 3567
94. M.A. Huber, N. Azoitei, B. Baumann, S. Grunert, A. Sommer, and H. Pehamberger NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression J Clin Invest 114 4 2004 569 581
95. J.R. Neil, K.M. Johnson, R.A. Nemenoff, and W.P. Schiemann Cox-2 inactivates Smad signaling and enhances EMT stimulated by TGF-beta through a PGE2-dependent mechanisms Carcinogenesis 29 11 2008 2227 2235
96. H.J. You, T. How, and G.C. Blobe The type III transforming growth factor-beta receptor negatively regulates nuclear factor kappa B signaling through its interaction with beta-arrestin2 Carcinogenesis 30 8 2009 1281 1287
97. J.R. Neil, M. Tian, and W.P. Schiemann X-linked inhibitor of apoptosis protein and its E3 ligase activity promote transforming growth factor-{beta}-mediated nuclear factor-{kappa}B activation during breast cancer progression J Biol Chem 284 32 2009 21209 21217
98. H.L. Chua, P. Bhat-Nakshatri, S.E. Clare, A. Morimiya, S. Badve, and H. Nakshatri NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2 Oncogene 26 5 2007 711 724
99. M. Musteanu, L. Blaas, M. Mair, M. Schlederer, M. Bilban, and S. Tauber Stat3 is a negative regulator of intestinal tumor progression in Apc(Min) mice Gastroenterology 138 3 2010 1003 1011 e1-5
100. A.J. Evans, R.C. Russell, O. Roche, T.N. Burry, J.E. Fish, and V.W. Chow VHL promotes E2 box-dependent E-cadherin transcription by HIF-mediated regulation of SIP1 and snail Mol Cell Biol 27 1 2007 157 169
101. M.H. Yang, M.Z. Wu, S.H. Chiou, P.M. Chen, S.Y. Chang, and C.J. Liu Direct regulation of TWIST by HIF-1alpha promotes metastasis Nat Cell Biol 10 3 2008 295 305
102. B. Krishnamachary, D. Zagzag, H. Nagasawa, K. Rainey, H. Okuyama, and J.H. Baek Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B Cancer Res 66 5 2006 2725 2731
103. H. Peinado, M. Del Carmen Iglesias-de la Cruz, D. Olmeda, K. Csiszar, K.S. Fong, and S. Vega A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression EMBO J 24 19 2005 3446 3458
104. C. Min, K.H. Kirsch, Y. Zhao, S. Jeay, A.H. Palamakumbura, and P.C. Trackman The tumor suppressor activity of the lysyl oxidase propeptide reverses the invasive phenotype of Her-2/neu-driven breast cancer Cancer Res 67 3 2007 1105 1112
105. C.A. Gebeshuber, K. Zatloukal, and J. Martinez MiR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis EMBO Rep 10 4 2009 400 405
106. L. Ma, J. Young, H. Prabhala, E. Pan, P. Mestdagh, and D. Muth MiR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis Nat Cell Biol 12 3 2010 247 256
107. F. Bazzoni, M. Rossato, M. Fabbri, D. Gaudiosi, M. Mirolo, and L. Mori Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals Proc Natl Acad Sci USA 106 13 2009 5282 5287
108. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, and A.Y. Zhou The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 4 2008 704 715
109. A.P. Morel, M. Lievre, C. Thomas, G. Hinkal, S. Ansieau, and A. Puisieux Generation of breast cancer stem cells through epithelial-mesenchymal transition PLoS One 3 8 2008 e2888
110. C. Tang, B.T. Ang, and S. Pervaiz Cancer stem cell: target for anti-cancer therapy FASEB J 21 14 2007 3777 3785
111. M.F. Clarke, J.E. Dick, P.B. Dirks, C.J. Eaves, C.H. Jamieson, and D.L. Jones Cancer stem cells - perspectives on current status and future directions: AACR workshop on cancer stem cells Cancer Res 66 19 2006 9339 9344
112. N.Y. Frank, T. Schatton, and M.H. Frank The therapeutic promise of the cancer stem cell concept J Clin Invest 120 1 2010 41 50
113. J.E. Visvader, and G.J. Lindeman Cancer stem cells in solid tumours: accumulating evidence and unresolved questions Nat Rev Cancer 8 10 2008 755 768
114. M.H. Tabor, M.R. Clay, J.H. Owen, C.R. Bradford, T.E. Carey, and G.T. Wolf Head and neck cancer stem cells: the side population Laryngoscope 121 3 2011 527 533
115. M.E. Prince, R. Sivanandan, A. Kaczorowski, G.T. Wolf, M.J. Kaplan, and P. Dalerba Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc Natl Acad Sci USA 104 3 2007 973 978
116. A. Okamoto, K. Chikamatsu, K. Sakakura, K. Hatsushika, G. Takahashi, and K. Masuyama Expansion and characterization of cancer stem-like cells in squamous cell carcinoma of the head and neck Oral Oncol 45 7 2009 633 639
117. Y.C. Chen, Y.W. Chen, H.S. Hsu, L.M. Tseng, P.I. Huang, and K.H. Lu Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer Biochem Biophys Res Commun 385 3 2009 307 313
118. M.R. Clay, M. Tabor, J.H. Owen, T.E. Carey, C.R. Bradford, and G.T. Wolf Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase Head Neck 32 9 2010 1195 1201
119. A.L. Tang, S.J. Hauff, J.H. Owen, M.P. Graham, M.J. Czerwinski, and J.J. Park UM-SCC-104: A New human papillomavirus-16-positive cancer stem cell-containing head and neck squamous cell carcinoma cell line Head Neck December 2011 10.1002/hed.21962
120. S.J. Davis, V. Divi, J.H. Owen, C.R. Bradford, T.E. Carey, and S. Papagerakis Metastatic potential of cancer stem cells in head and neck squamous cell carcinoma Arch Otolaryngol Head Neck Surg 136 12 2010 1260 1266
121. J. Song, I. Chang, Z. Chen, M. Kang, and C.Y. Wang Characterization of side populations in HNSCC: highly invasive, chemoresistant and abnormal Wnt signaling PLoS One 5 7 2010 e11456
122. S.J. Goldie, K.W. Mulder, D.W. Tan, S.K. Lyons, A.H. Sims, and F.M. Watt FRMD4A upregulation in human squamous cell carcinoma promotes tumor growth and metastasis and is associated with poor prognosis Cancer Res May 7 2012 [Epub ahead of print]
123. M. Greaves Cancer stem cells: back to Darwin? Semin Cancer Biol 20 2 2010 65 70
124. C.F. Kim, E.L. Jackson, A.E. Woolfenden, S. Lawrence, I. Babar, and S. Vogel Identification of bronchioalveolar stem cells in normal lung and lung cancer Cell 121 6 2005 823 835
125. M. Shackleton, F. Vaillant, K.J. Simpson, J. Stingl, G.K. Smyth, and M.L. Asselin-Labat Generation of a functional mammary gland from a single stem cell Nature 439 7072 2006 84 88
126. T. Miyamoto, I.L. Weissman, and K. Akashi AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation Proc Natl Acad Sci USA 97 13 2000 7521 7526
127. A.L. Welm, S. Kim, B.E. Welm, and J.M. Bishop MET and MYC cooperate in mammary tumorigenesis Proc Natl Acad Sci USA 102 12 2005 4324 4329
128. J. Houghton, C. Stoicov, S. Nomura, A.B. Rogers, J. Carlson, and H. Li Gastric cancer originating from bone marrow-derived cells Science 306 5701 2004 1568 1571
129. A.M. Eastham, H. Spencer, F. Soncin, S. Ritson, C.L. Merry, and P.L. Stern Epithelial-mesenchymal transition events during human embryonic stem cell differentiation Cancer Res 67 23 2007 11254 11262
130. C.H. Jamieson, L.E. Ailles, S.J. Dylla, M. Muijtjens, C. Jones, and J.L. Zehnder Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML New Engl J Med 351 7 2004 657 667
131. S. Jaiswal, D. Traver, T. Miyamoto, K. Akashi, E. Lagasse, and I.L. Weissman Expression of BCR/ABL and BCL-2 in myeloid progenitors leads to myeloid leukemias Proc Natl Acad Sci USA 100 17 2003 10002 10007
132. A.V. Krivtsov, D. Twomey, Z. Feng, M.C. Stubbs, Y. Wang, and J. Faber Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9 Nature 442 7104 2006 818 822
133. A.L. Vescovi, R. Galli, and B.A. Reynolds Brain tumour stem cells Nat Rev Cancer 6 6 2006 425 436
134. R. Bjerkvig, B.B. Tysnes, K.S. Aboody, J. Najbauer, and A.J. Terzis Opinion: the origin of the cancer stem cell: current controversies and new insights Nat Rev Cancer 5 11 2005 899 904
135. J.M. Pawelek, and A.K. Chakraborty Fusion of tumour cells with bone marrow-derived cells: a unifying explanation for metastasis Nat Rev Cancer 8 5 2008 377 386
136. J.M. Pawelek, and A.K. Chakraborty The cancer cell-leukocyte fusion theory of metastasis Adv Cancer Res 101 2008 397 444
137. M. Santisteban, J.M. Reiman, M.K. Asiedu, M.D. Behrens, A. Nassar, and K.R. Kalli Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells Cancer Res 69 7 2009 2887 2895
138. J.M. Pawelek Tumour-cell fusion as a source of myeloid traits in cancer Lancet Oncol 6 12 2005 988 993
139. U. Wellner, J. Schubert, U.C. Burk, O. Schmalhofer, F. Zhu, and A. Sonntag The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs Nat Cell Biol 11 12 2009 1487 1495
140. A. Biddle, X. Liang, L. Gammon, B. Fazil, L.J. Harper, and H. Emich Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative Cancer Res 71 15 2011 5317 5326
141. D. Basu, K.T. Montone, L.P. Wang, P.A. Gimotty, R. Hammond, and J.A. Diehl Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas Cell Cycle 10 12 2011 2008 2016
142. J.B. Sunwoo A cisplatin-resistant subpopulation of mesenchymal-like cells in head and neck squamous cell carcinoma Cell Cycle 10 17 2011 2834 2835
143. N.P. Judd, A.E. Winkler, O. Murillo-Sauca, J.J. Brotman, J.H. Law, and J.S. Lewis Jr. ERK1/2 regulation of CD44 modulates oral cancer aggressiveness Cancer Res 72 1 2012 365 374
144. C. Chen, Y. Wei, M. Hummel, T.K. Hoffmann, M. Gross, and A.M. Kaufmann Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma PLoS One 6 1 2011 e16466
145. Z. Zhang, M.S. Filho, and J.E. Nör The biology of head and neck cancer stem cells Oral Oncol 48 1 2012 1 9
146. C. Scheel, T. Onder, A. Karnoub, and R.A. Weinberg Adaptation versus selection: the origins of metastatic behavior Cancer Res 67 24 2007 11476 11479 [discussion 9-80]
147. A. Biddle, and I.C. Mackenzie Cancer stem cells and EMT in carcinoma Cancer Metastasis Rev Feb 3 2012 [Epub ahead of print]
148. K.A. Moore, and I.R. Lemischka Stem cells and their niches Science 311 5769 2006 1880 1885
149. L. Li, and T. Xie Stem cell niche: structure and function Annu Rev Cell Dev Biol 21 2005 605 631
150. D.T. Scadden The stem-cell niche as an entity of action Nature 441 7097 2006 1075 1079
151. T. Xie, and A.C. Spradling A niche maintaining germ line stem cells in the Drosophila ovary Science 290 5490 2000 328 330
152. H. Lin The stem-cell niche theory: lessons from flies Nat Rev Genet 3 12 2002 931 940
153. L. Li, and H. Clevers Coexistence of quiescent and active adult stem cells in mammals Science 327 5965 2010 542 545
154. M.P. Lutolf, P.M. Gilbert, and H.M. Blau Designing materials to direct stem-cell fate Nature 462 7272 2009 433 441
155. D.J. Rossi, C.H. Jamieson, and I.L. Weissman Stems cells and the pathways to aging and cancer Cell 132 4 2008 681 696
156. N.Z. Kuhn, and R.S. Tuan Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis J Cell Physiol 222 2 2010 268 277
157. P.M. Gilbert, K.L. Havenstrite, K.E. Magnusson, A. Sacco, N.A. Leonardi, and P. Kraft Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture Science 329 5995 2010 1078 1081
158. M.H. Stewart, S.C. Bendall, and M. Bhatia Deconstructing human embryonic stem cell cultures: niche regulation of self-renewal and pluripotency J Mol Med (Berl) 86 8 2008 875 886
159. T. Schroeder Hematopoietic stem cell heterogeneity: subtypes, not unpredictable behavior Cell Stem Cell 6 3 2010 203 207
160. M. Bhatia Developmental biology. Microenvironment mimicry Science 329 5995 2010 1024 1025
161. R.J. Gilbertson, and D.H. Gutmann Tumorigenesis in the brain: location, location, location Cancer Res 67 12 2007 5579 5582
162. R.J. Gilbertson, and J.N. Rich Making a tumour's bed: glioblastoma stem cells and the vascular niche Nat Rev Cancer 7 10 2007 733 736
163. L.A. Johnston Competitive interactions between cells: death, growth, and geography Science 324 5935 2009 1679 1682
164. A. Spradling, D. Drummond-Barbosa, and T. Kai Stem cells find their niche Nature 414 6859 2001 98 104
165. J.T. Connelly, J.E. Gautrot, B. Trappmann, D.W. Tan, G. Donati, and W.T. Huck Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions Nat Cell Biol 12 7 2010 711 718
166. R. Iglesias-Bartolome, and J.S. Gutkind Keeping the epidermal stem cell niche in shape Cell Stem Cell 7 2 2010 143 145
167. R.M. Castilho, C.H. Squarize, K. Leelahavanichkul, Y. Zheng, T. Bugge, and J.S. Gutkind Rac1 is required for epithelial stem cell function during dermal and oral mucosal wound healing but not for tissue homeostasis in mice PLoS One 5 5 2010 e10503
168. R. Iglesias-Bartolome, and J.S. Gutkind Signaling circuitries controlling stem cell fate: to be or not to be Curr Opin Cell Biol 23 6 2011 716 723
169. A.A. Kiger, D.L. Jones, C. Schulz, M.B. Rogers, and M.T. Fuller Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue Science 294 5551 2001 2542 2545
170. C. Schulz, A.A. Kiger, S.I. Tazuke, Y.M. Yamashita, L.C. Pantalena-Filho, and D.L. Jones A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage Genetics 167 2 2004 707 723
171. X. Song, M.D. Wong, E. Kawase, R. Xi, B.C. Ding, and J.J. McCarthy Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary Development 131 6 2004 1353 1364
172. N. Tulina, and E. Matunis Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling Science 294 5551 2001 2546 2549
173. S.J. Morrison, and J. Kimble Asymmetric and symmetric stem-cell divisions in development and cancer Nature 441 7097 2006 1068 1074
174. E. Charafe-Jauffret, C. Ginestier, F. Iovino, J. Wicinski, N. Cervera, and P. Finetti Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature Cancer Res 69 4 2009 1302 1313
175. Z.T. Schafer, and J.S. Brugge IL-6 involvement in epithelial cancers J Clin Invest 117 12 2007 3660 3663
176. M. Todaro, M.P. Alea, A.B. Di Stefano, P. Cammareri, L. Vermeulen, and F. Iovino Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4 Cell Stem Cell 1 4 2007 389 402
177. P. Sansone, G. Storci, S. Tavolari, T. Guarnieri, C. Giovannini, and M. Taffurelli IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland J Clin Invest 117 12 2007 3988 4002
178. E. Charafe-Jauffret, C. Ginestier, F. Iovino, C. Tarpin, M. Diebel, and B. Esterni Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer Clin Cancer Res 16 1 2010 45 55
179. E.N. Arwert, R. Lal, S. Quist, I. Rosewell, N. van Rooijen, and F.M. Watt Tumor formation initiated by nondividing epidermal cells via an inflammatory infiltrate Proc Natl Acad Sci USA 107 46 2010 19903 19908
180. N. Fortunel, J. Hatzfeld, L. Aoustin, P. Batard, K. Ducos, and M.N. Monier Specific dose-response effects of TGF-beta1 on developmentally distinct hematopoietic stem/progenitor cells from human umbilical cord blood Hematol J 1 2 2000 126 135
181. A. Chabanon, C. Desterke, E. Rodenburger, D. Clay, B. Guerton, and L. Boutin A cross-talk between stromal cell-derived factor-1 and transforming growth factor-beta controls the quiescence/cycling switch of CD34(+) progenitors through FoxO3 and mammalian target of rapamycin Stem Cells 26 12 2008 3150 3161
182. T. Watabe, A. Nishihara, K. Mishima, J. Yamashita, K. Shimizu, and K. Miyazawa TGF-beta receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells J Cell Biol 163 6 2003 1303 1311
183. T. Kokudo, Y. Suzuki, Y. Yoshimatsu, T. Yamazaki, T. Watabe, and K. Miyazono Snail is required for TGFbeta-induced endothelial-mesenchymal transition of embryonic stem cell-derived endothelial cells J Cell Sci 121 Pt 20 2008 3317 3324
184. G.A. Challen, N.C. Boles, S.M. Chambers, and M.A. Goodell Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1 Cell Stem Cell 6 3 2010 265 278
185. K. Oguma, H. Oshima, M. Aoki, R. Uchio, K. Naka, and S. Nakamura Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells EMBO J 27 12 2008 1671 1681
186. S. Umar, S. Sarkar, Y. Wang, and P. Singh Functional cross-talk between beta-catenin and NFkappaB signaling pathways in colonic crypts of mice in response to progastrin J Biol Chem 284 33 2009 22274 22284
187. F.H. Chen, and R.S. Tuan Mesenchymal stem cells in arthritic diseases Arthritis Res Ther 10 5 2008 223
188. C. Yu, A.J. Kastin, and W. Pan TNF reduces LIF endocytosis despite increasing NFkappaB-mediated gp130 expression J Cell Physiol 213 1 2007 161 166
189. C.H. Squarize, R.M. Castilho, V. Sriuranpong, D.S. Pinto Jr., and J.S. Gutkind Molecular cross-talk between the NFkappaB and STAT3 signaling pathways in head and neck squamous cell carcinoma Neoplasia 8 9 2006 733 746
190. S.L. Bhave, T.N. Teknos, and Q. Pan Molecular parameters of head and neck cancer metastasis Crit Rev Eukaryot Gene Expr 21 2 2011 143 153
191. V. Sriuranpong, J.I. Park, P. Amornphimoltham, V. Patel, B.D. Nelkin, and J.S. Gutkind Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system Cancer Res 63 11 2003 2948 2956
192. T.E. North, W. Goessling, C.R. Walkley, C. Lengerke, K.R. Kopani, and A.M. Lord Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis Nature 447 7147 2007 1007 1011
193. N.J. Maitland, and A.T. Collins Inflammation as the primary aetiological agent of human prostate cancer: a stem cell connection? J Cell Biochem 105 4 2008 931 939
194. P. Lee, D.J. Lee, C. Chan, S.W. Chen, I. Ch'en, and C. Jamora Dynamic expression of epidermal caspase 8 simulates a wound healing response Nature 458 7237 2009 519 523
195. M.A. Rieger, P.S. Hoppe, B.M. Smejkal, A.C. Eitelhuber, and T. Schroeder Hematopoietic cytokines can instruct lineage choice Science 325 5937 2009 217 218
196. S.C. Bendall, M.H. Stewart, P. Menendez, D. George, K. Vijayaragavan, and T. Werbowetski-Ogilvie IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro Nature 448 7157 2007 1015 1021
197. M. Shipitsin, L.L. Campbell, P. Argani, S. Weremowicz, N. Bloushtain-Qimron, and J. Yao Molecular definition of breast tumor heterogeneity Cancer Cell 11 3 2007 259 273
198. I. Ben-Porath, M.W. Thomson, V.J. Carey, R. Ge, G.W. Bell, and A. Regev An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors Nat Genet 40 5 2008 499 507
199. S. Cufi, A. Vazquez-Martin, C. Oliveras-Ferraros, B. Martin-Castillo, J. Joven, and J.A. Menendez Metformin against TGFbeta-induced epithelial-to- mesenchymal transition (EMT): from cancer stem cells to aging-associated fibrosis Cell Cycle 9 22 2010 4461 4468
200. Z. Chng, A. Teo, R.A. Pedersen, and L. Vallier SIP1 mediates cell-fate decisions between neuroectoderm and mesendoderm in human pluripotent stem cells Cell Stem Cell 6 1 2010 59 70
201. G. Yin, R. Chen, A.B. Alvero, H.H. Fu, J. Holmberg, and C. Glackin TWISTing stemness, inflammation and proliferation of epithelial ovarian cancer cells through MIR199A2/214 Oncogene 29 24 2010 3545 3553
202. C. Liu, and D.G. Tang MicroRNA regulation of cancer stem cells Cancer Res 71 18 2011 5950 5954
203. G. Pani, T. Galeotti, and P. Chiarugi Metastasis: cancer cell's escape from oxidative stress Cancer Metastasis Rev 29 2 2010 351 378