Contribution of epithelial-to-mesenchymal transition and cancer stem cells to pancreatic cancer progression

Journal of Surgical Research

Volumn 173, Issue 1, 2012, Pages 105-112

  Krantz, Seth B ^a   Shields, Mario A ^a   Dangi Garimella, Surabhi ^a   Munshi, Hidayatullah G ^a,b   Bentrem, David J ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

drug resistance; epithelial mesenchymal transition; microRNA; pancreatic cancer; stem cells

Indexed keywords

3,3' DIINDOLYLMETHANE; ALDEHYDE DEHYDROGENASE; ANTINEOPLASTIC AGENT; CEDIRANIB; CYCLOPAMINE; ERLOTINIB; GEMCITABINE; IPI 926; ISOFLAVONE; MATRIX METALLOPROTEINASE 14; MK 0752; MONOCLONAL ANTIBODY; NOTCH RECEPTOR; OMP 21M 18; PACLITAXEL; PRI 724; PROTEIN TYROSINE KINASE; RO 4929097; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR SLUG; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; VISMODEGIB; WNT PROTEIN; ZEB1 PROTEIN;

ADVANCED CANCER; CANCER GROWTH; CANCER INVASION; CANCER MORTALITY; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURGERY; CANCER SURVIVAL; CELL MATURATION; CELL POPULATION; CLINICAL TRIAL (TOPIC); DISEASE SEVERITY; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; GENE MUTATION; HUMAN; MESENCHYME CELL; METASTASIS; MORBIDITY; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREAS DUCT ADENOCARCINOMA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR;

ADENOCARCINOMA; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; HEDGEHOG PROTEINS; HUMANS; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84857052013     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2011.09.020     Document Type: Review

References (102)

1. J.P. Thiery, H. Acloque, and R.Y.J. Huang Epithelial-mesenchymal transitions in development and disease Cell 139 2009 871
2. A.D. Yang, E.R. Camp, and F. Fan Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells Cancer Res 66 2006 46
3. K. Polyak, and R.A. Weinberg Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits Nat Rev Cancer 9 2009 265
4. J.M. Lee, S. Dedhar, and R. Kalluri The epithelial-mesenchymal transition: New insights in signaling, development, and disease J Cell Biol 172 2006 973
5. R. Kalluri, and R.A. Weinberg The basics of epithelial-mesenchymal transition J Clin Invest 119 2009 1420
6. M.A. Shields, S. Dangi-Garimella, and S.B. Krantz Pancreatic cancer cells respond to type I collagen by inducing snailexpression to promote membrane type 1-matrix metalloproteinase dependent collagen invasion J Biol Chem 286 2011 10495
7. J. Fuxe, T. Vincent, and A.G. de Herreros Transcriptional crosstalk between TGFβ and stem cell pathways in tumor cell invasion: Role of EMT promoting Smad complexes Cell Cycle 9 2010 2363
8. S. Dangi-Garimella, S.B. Krantz, and M.R. Barron Three-dimensional collagen I promotes gemcitabine resistance in pancreatic cancer through MT1-MMP-mediated expression of HMGA2 Cancer Res 71 2011 1019
9. M. Santisteban, J.M. Reiman, and M.K. Asiedu Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells Cancer Res 69 2009 2887
10. S.A. Mani, W. Guo, and M.-J. Liao The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704
11. A.-P. Morel, M. Livre, and C. Thomas Generation of breast cancer stem cells through epithelial-mesenchymal transition PLoS ONE 3 2008 e2888
12. J. Yanagawa, T.C. Walser, and L.X. Zhu Snail promotes CXCR2 ligand-dependent tumor progression in non-small cell lung carcinoma Clin Cancer Res 15 2009 6820
13. Z.A. Rasheed, J. Yang, and Q. Wang Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma J Natl Cancer Inst 102 2010 340
14. C. van den Hoogen, G. van der Horst, and H. Cheung High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer Cancer Res 70 2010 5163
15. A.T. Collins, P.A. Berry, and C. Hyde Prospective identification of tumorigenic prostate cancer stem cells Cancer Res 5 2005 10946
16. E. Giannoni, F. Bianchini, and L. Masieri Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness Cancer Res 70 2010 6945
17. J.E. Carpentino, M.J. Hynes, and H.D. Appelman Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer Cancer Res 69 2009 8208
18. F. Varnat, A. Duquet, and M. Malerba Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion EMBO Mol Med 1 2009 338
19. N.K. Kurrey, S.P. Jalgaonkar, and A.V. Joglekar Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells Stem Cells 27 2009 2059
20. S.-M. Park, A.B. Gaur, and E. Lengyel The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2 Genes Dev 22 2008 894
21. M.E. Prince, R. Sivanandan, and A. Kaczorowski Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc Nat Acad Sci USA 104 2007 973
22. G. Feldmann, S. Dhara, and V. Fendrich Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: A new paradigm for combination therapy in solid cancers Cancer Res 67 2007 2187
23. D. Tarin, E.W. Thompson, and D.F. Newgreen The fallacy of epithelial mesenchymal transition in neoplasia Cancer Res 65 2005 5996 discussion 6000
24. A.J. Trimboli, K. Fukino, A. de Bruin, G. Wei, and L. Shen Direct evidence for epithelial-mesenchymal transitions in breast cancer Cancer Res 68 2008 937
25. S.N. Flier, H. Tanjore, and E.G. Kokkotou Identification of epithelial to mesenchymal transition as a novel source of fibroblasts in intestinal fibrosis J Biol Chem 285 2010 20202
26. A. Jemal, R. Siegel, and J. Xu Cancer statistics, 2010 CA Cancer J Clin 60 2010 277
27. K.Y. Bilimoria, D.J. Bentrem, and C.Y. Ko Validation of the 6th edition AJCC Pancreatic Cancer Staging System: Report from the National Cancer Database Cancer 110 2007 738
28. S. Altekruse, C. Kosary, and M. Krapcho SEER Cancer Statistics Review, 1975-2007, National Cancer Institute 2010
29. A. Stojadinovic, A. Hoos, and M.F. Brennan Randomized clinical trials in pancreatic cancer Surg Oncol Clin N Am 11 2002 207 x
30. J.M. Winter, J.L. Cameron, and K.A. Campbell 1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience J Gastrointest Surg 10 2006 1199 discussion 1210
31. M. Hidalgo Pancreatic cancer N Engl J Med 362 2010 1605
32. A.J. Ottaviano, L. Sun, and V. Ananthanarayanan Extracellular matrix-mediated membrane-type 1 matrix metalloproteinase expression in pancreatic ductal cells is regulated by transforming growth factor-β1 Cancer Res 66 2006 7032
33. K.P. Olive, M.A. Jacobetz, and C.J. Davidson Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457
34. M.M. Javle, J.F. Gibbs, and K.K. Iwata Epithelial-mesenchymal transition (EMT) and activated extracellular signal-regulated kinase (p-Erk) in surgically resected pancreatic cancer Ann Surg Oncol 14 2007 3527
35. B. Hotz, M. Arndt, and S. Dullat Epithelial to mesenchymal transition: Expression of the regulators snail, slug, and twist in pancreatic cancer Clin Cancer Res 13 2007 4769
36. E. Buck, A. Eyzaguirre, and S. Barr Loss of homotypic cell adhesion by epithelial-mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition Mol Cancer Ther 6 2007 532
37. T. Arumugam, V. Ramachandran, and K.F. Fournier Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer Cancer Res 69 2009 5820
38. H.J. Maier, U. Schmidt-Strassburger, and M.A. Huber NF-κB promotes epithelial-mesenchymal transition, migration and invasion of pancreatic carcinoma cells Cancer Lett 295 2010 214
39. S. Ali, A. Ahmad, and S. Banerjee 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 2010 3606
40. Z. Wang, Y. Li, and D. Kong Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway Cancer Res 69 2009 2400
41. R. Derynck, and Y.E. Zhang Smad-dependent and Smad-independent pathways in TGF-β family signalling Nature 425 2003 577
42. Y. Shi, and J. Massagué Mechanisms of TGF-β signaling from cell membrane to the nucleus Cell 113 2003 685
43. J. Massagué How cells read TGF-β signals Nat Rev Mol Cell Biol 1 2000 169
44. R. Derynck, R.J. Akhurst, and A. Balmain TGF-β signaling in tumor suppression and cancer progression Nat Genet 29 2001 117
45. K.A. Brown, J.A. Pietenpol, and H.L. Moses A tale of two proteins: Differential roles and regulation of Smad2 and Smad3 in TGF-β signaling J Cell Biochem 101 2007 9
46. M. Schutte, R.H. Hruban, and L. Hedrick DPC4 gene in various tumor types Cancer Res 56 1996 2527
47. K. Izeradjene, C. Combs, and M. Best Kras(G12D) and Smad4/Dpc4 haploinsufficiency cooperate to induce mucinous cystic neoplasms and invasive adenocarcinoma of the pancreas Cancer Cell 11 2007 229
48. N. Bardeesy, K.-H. Cheng, and J.H. Berger Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer Genes Dev 20 2006 3130
49. L. Devy, L. Huang, and L. Naa Selective inhibition of matrix metalloproteinase-14 blocks tumor growth, invasion, and angiogenesis Cancer Res 69 2009 1517
50. A. Singh, P. Greninger, and D. Rhodes A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival Cancer Cell 15 2009 489
51. K.G. Leong, K. Niessen, and I. Kulic Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through slug-induced repression of E-cadherin J Exp Med 204 2007 2935
52. C. Sahlgren, M.V. Gustafsson, and S. Jin Notch signaling mediates hypoxia-induced tumor cell migration and invasion Proc Nat Acad Sci USA 105 2008 6392
53. S. Brabletz, K. Bajdak, and S. Meidhof The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells EMBO J 30 2011 770
54. Z. Wang, Y. Li, and D. Kong Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway Cancer Res 69 2009 2400
55. R. Plentz, J.-S. Park, A.D. Rhim, and D. Abravanel Inhibition of gamma-secretase activity inhibits tumor progression in a mouse model of pancreatic ductal adenocarcinoma Gastroenterology 136 2009 1741
56. M. Katoh Network of WNT and other regulatory signaling sascades in pluripotent stem cells and cancer stem cells Curr Pharm Biotechnol 12 2011 160
57. B.P. Zhou, and C. Hung M- Wnt, hedgehog and snail: Sister pathways that control by GSK-3β and β-Trcp in the regulation of metastasis Cell Cycle 4 2005 772
58. P.B. Gupta, T.T. Onder, and G. Jiang Identification of selective inhibitors of cancer stem cells by high-throughput screening Cell 138 2009 645
59. M. Al-Hajj, M.S. Wicha, and A. Benito-Hernandez Prospective identification of tumorigenic breast cancer cells Proc Nat Acad Scie USA 100 2003 3983
60. H. Korkaya, and M.S. Wicha Cancer stem cells: Nature versus nurture Nat Cell Biol 12 2010 419
61. S. Riethdorf, and K. Pantel Disseminated tumor cells in bone marrow and circulating tumor cells in blood of breast cancer patients: Current state of detection and characterization Pathobiology 75 2008 140
62. P. Neth, C. Ries, and M. Karow The Wnt signal transduction pathway in stem cells and cancer cells: Influence on cellular invasion Stem Cell Rev 3 2007 18
63. A. Singh, and J. Settleman EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer Oncogene 29 2010 4741
64. C. Li, D.G. Heidt, and P. Dalerba Identification of pancreatic cancer stem cells Cancer Res 67 2007 1030
65. S.P. Hong, J. Wen, and S. Bang CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells Int J Cancer 125 2009 2323
66. R.L. Brown, L.M. Reinke, and M.S. Damerow CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression J Clini Invest 121 2011 1064
67. W. Rudy, M. Hofmann, and R. Schwartz-Albiez The two major CD44 proteins expressed on a metastatic rat tumor cell line are derived from different splice variants: Each one individually suffices to confer metastatic behavior Cancer Res 53 1993 1262
68. M. Hofmann, W. Rudy, and U. Günthert A link between ras and metastatic behavior of tumor cells: Ras induces CD44 promoter activity and leads to low-level expression of metastasis-specific variants of CD44 in CREF cells Cancer Res 53 1993 1516
69. F. Gansauge, S. Gansauge, and A. Zobywalski Differential expression of CD44 splice variants in human pancreatic adenocarcinoma and in normal pancreas Cancer Res 55 1995 5499
70. S.P. Thayer, M.P. di Magliano, and P.W. Heiser Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis Nature 425 2003 851
71. D.M. Berman, S.S. Karhadkar, and A. Maitra Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours Nature 425 2003 846
72. R.L. Yauch, S.E. Gould, and S.J. Scales A paracrine requirement for hedgehog signalling in cancer Nature 455 2008 406
73. W.-K. Syn, Y. Jung, and A. Omenetti Hedgehog-mediated epithelial-to-mesenchymal transition and fibrogenic repair in nonalcoholic fatty liver disease Gastroenterology 137 2009 1478
74. N. Isohata, K. Aoyagi, and T. Mabuchi Hedgehog and epithelial-mesenchymal transition signaling in normal and malignant epithelial cells of the esophagus Int J Cancer 125 2009 1212
75. H. Ohta, K. Aoyagi, and M. Fukaya Cross talk between hedgehog and epithelial-mesenchymal transition pathways in gastric pit cells and in diffuse-type gastric cancers Br J Cancer 100 2009 389
76. S.S. Choi, W.-K. Syn, and G.F. Karaca Leptin promotes the myofibroblastic phenotype in hepatic stellate cells by activating the hedgehog pathway J Biol Chem 285 2010 36551
77. M.Y. Maitah, S. Ali, and A. Ahmad Up-regulation of sonic hedgehog contributes to TGF-β1-induced epithelial to mesenchymal transition in NSCLC cells PLoS ONE 6 2011 e16068
78. M. Katoh, and M. Katoh Integrative genomic analyses of ZEB2: Transcriptional regulation of ZEB2 based on SMADs, ETS1, HIF1alpha, POU/OCT, and NF-kappaB Int J Oncol 34 2009 1737
79. K. Taura, K. Miura, and K. Iwaisako Hepatocytes do not undergo epithelial-mesenchymal transition in liver fibrosis in mice Hepatology 51 2010 1027
80. D. Scholten, C.H. Osterreicher, and A. Scholten Genetic labeling does not detect epithelial-to-mesenchymal transition of cholangiocytes in liver fibrosis in mice Gastroenterology 139 2010 987
81. R.G. Rowe, Y. Lin, and R. Shimizu-Hirota Hepatocyte-derived snail1 propagates liver fibrosis progression Mol Cell Biol 31 2011 2392
82. A. Boutet, C.A. De Frutos, and P.H. Maxwell Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney EMBO J 25 2006 5603
83. X. Chen, S. Lingala, and S. Khoobyari Epithelial mesenchymal transition and hedgehog signaling activation are associated with chemoresistance and invasion of hepatoma subpopulations J Hepatol 55 2011 838
84. J.L. Dembinski, and S. Krauss Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma Clin Exp Metastasis 26 2009 611
85. M. Dillhoff, S.E. Wojcik, and M. Bloomston MicroRNAs in solid tumors J Surg Res 154 2009 349
86. B.P. Lewis, C.B. Burge, and D.P. Bartel Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets Cell 120 2005 15
87. L.P. Lim, N.C. Lau, and P. Garrett-Engele Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs Nature 433 2005 769
88. M.T. McManus, and P.A. Sharp Gene silencing in mammals by small interfering RNAs Nat Rev Genet 3 2002 737
89. J. Yu, K. Ohuchida, and K. Mizumoto MicroRNA, hsa-miR-200c, is an independent prognostic factor in pancreatic cancer and its upregulation inhibits pancreatic cancer invasion but increases cell proliferation Mol Cancer 9 2010 169
90. U. Wellner, J. Schubert, and U.C. Burk The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs Nat Cell Biol 11 2009 1487
91. M.E. Peter Let-7 and miR-200 microRNAs: Guardians against pluripotency and cancer progression Cell Cycle 8 2009 843
92. Y. Shimono, M. Zabala, and R.W. Cho Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells Cell 138 2009 592
93. Y. Li, T.G. VandenBoom, and D. Kong 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 2009 6704
94. U. Burk, J. Schubert, and U. Wellner A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells EMBO Rep 9 2008 582
95. P.A. Gregory, A.G. Bert, and E.L. Paterson The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1 Nat Cell Biol 10 2008 593
96. M. Dillhoff, J. Liu, and W. Frankel MicroRNA-21 is overexpressed in pancreatic cancer and a potential predictor of survival J Gastrointest Surg 12 2008 2171
97. O.A. Kent, M. Mullendore, and E.A. Wentzel A resource for analysis of microRNA expression and function in pancreatic ductal adenocarcinoma cells Cancer Biol Ther 8 2009 2013
98. S. Dangi-Garimella, M.J. Strouch, and P.J. Grippo Collagen regulation of let-7 in pancreatic cancer involves TGF-β1-mediated membrane type 1-matrix metalloproteinase expression Oncogene 30 2011 1002
99. B.D. Brown, and L. Naldini Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications Nat Rev Genet 10 2009 578
100. A.L. Jackson, and P.S. Linsley Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application Nat Rev Drug Discov 9 2010 57
101. K. Wu, J. Zeng, and L. Li Silibinin reverses epithelial-to-mesenchymal transition in metastatic prostate cancer cells by targeting transcription factors Oncol Rep 23 2010 1545
102. A. Vazquez-Martin, C. Oliveras-Ferraros, and S. Cufí Metformin regulates breast cancer stem cell ontogeny by transcriptional regulation of the epithelial-mesenchymal transition (EMT) status Cell Cycle 9 2010 3807