The emerging molecular machinery and therapeutic targets of metastasis

Trends in Pharmacological Sciences

Volumn 36, Issue 6, 2015, Pages 349-359

  Sun, Yutong ^a   Ma, Li ^b,c  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Cancer stem cell; Circulating tumor cell; Epithelial mesenchymal plasticity; Metastasis; Therapy resistance

Indexed keywords

ANTINEOPLASTIC AGENT; CELECOXIB; DASATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FG 3019; GEMCITABINE; ILOMASTAT; MICRORNA; MICRORNA 200C; MICRORNA 205; MICRORNA 373; MRX 34; ONCOPROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; RAPAMYCIN; SCATTER FACTOR; TANESPIMYCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR YAP; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; TRANSFORMING GROWTH FACTOR BETA; TRASTUZUMAB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULAR CELL ADHESION MOLECULE 1; WNT PROTEIN;

ARTICLE; BONE METASTASIS; BREAST METASTASIS; CANCER GROWTH; CANCER MORTALITY; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CELL MIGRATION; CELL SUBPOPULATION; CIRCULATING TUMOR CELL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; LIVER CANCER; LUNG METASTASIS; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; METASTATIC MELANOMA; MOLECULARLY TARGETED THERAPY; NON SMALL CELL LUNG CANCER; NONHUMAN; PANCREAS CANCER; PDZ DOMAIN; PRIORITY JOURNAL; RADIOSENSITIVITY; TUMOR INVASION; TUMOR MICROENVIRONMENT; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; METABOLISM; NEOPLASM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR EMBOLISM;

ANIMALS; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84934890113     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2015.04.001     Document Type: Review

References (126)

1. Fidler, I.J. (2003) The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 3, 453-458
2. Brabletz, T. et al. (2013) Roadblocks to translational advances on metastasis research. Nat. Med. 19, 1104-1109
3. Wan, L. et al. (2013) Tumor metastasis: moving new biological insights into the clinic. Nat. Med. 19, 1450-1464
4. Eccles, S.A. and Welch, D.R. (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369, 1742-1757
5. Talmadge, J.E. and Fidler, I.J. (2010) AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res. 70, 5649-5669
6. Lee, Y.T. (1983) Breast carcinoma: pattern of metastasis at autopsy. J. Surg. Oncol. 23, 175-180
7. Weigelt, B. et al. (2005) Breast cancer metastasis: markers and models. Nat. Rev. Cancer 5, 591-602
8. Steeg, P.S. and Theodorescu, D. (2008) Metastasis: a therapeutic target for cancer. Nat. Clin. Pract. Oncol. 5, 206-219
9. Steeg, P.S. (2012) Perspective: the right trials. Nature 485, S58-S59
10. Lehmann, B.D. et al. (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 121, 2750-2767
11. Scheel, C. et al. (2007) Adaptation versus selection: the origins of metastatic behavior. Cancer Res. 67, 11476-11479 discussion 11479-11480
12. Thiery, J.P. (2002) Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442-454
13. Thiery, J.P. et al. (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890
14. Yang, J. and Weinberg, R.A. (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829
15. Kalluri, R. and Weinberg, R.A. (2009) The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428
16. Tsai, J.H. et al. (2012) Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22, 725-736
17. Ocana, O.H. et al. (2012) Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 22, 709-724
18. Yang, J. et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939
19. Batlle, E. et al. (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89
20. Cano, A. et al. (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83
21. Hajra, K.M. et al. (2002) The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 62, 1613-1618
22. Eger, A. et al. (2005) DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 24, 2375-2385
23. Comijn, J. et al. (2001) The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7, 1267-1278
24. Tsai, J.H. and Yang, J. (2013) Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev. 27, 2192-2206
25. Davis, F.M. et al. (2014) Targeting EMT in cancer: opportunities for pharmacological intervention. Trends Pharmacol. Sci. 35, 479-488
26. Friedl, P. and Wolf, K. (2008) Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 68, 7247-7249
27. Sabeh, F. et al. (2009) Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185, 11-19
28. Brabletz, T. et al. (2005) Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5, 744-749
29. Mani, S.A. et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715
30. Morel, A.P. et al. (2008) Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 3, e2888
31. Chaffer, C.L. et al. (2013) Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell 154, 61-74
32. Gregory, P.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
33. Park, S.M. et al. (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
34. Shimono, Y. et al. (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138, 592-603
35. Burk, U. 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
36. Korpal, M. et al. (2011) Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nat. Med. 17, 1101-1108
37. Dykxhoorn, D.M. et al. (2009) miR-200 enhances mouse breast cancer cell colonization to form distant metastases. PLoS ONE 4, e7181
38. Chua, K.N. et al. (2012) A cell-based small molecule screening method for identifying inhibitors of epithelial-mesenchymal transition in carcinoma. PLoS ONE 7, e33183
39. Reka, A.K. et al. (2011) Identifying inhibitors of epithelial-mesenchymal transition by connectivity map-based systems approach. J. Thorac. Oncol. 6, 1784-1792
40. Gupta, P.B. et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138, 645-659
41. Pegram, M.D. et al. (1998) HER-2/neu as a predictive marker of response to breast cancer therapy. Breast Cancer Res. Treat. 52, 65-77
42. Slamon, D.J. et al. (2001) Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N. Engl. J. Med. 344, 783-792
43. Kwak, E.L. et al. (2010) Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N. Engl. J. Med. 363, 1693-1703
44. Chapman, P.B. et al. (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 364, 2507-2516
45. Yu, F.X. and Guan, K.L. (2013) The Hippo pathway: regulators and regulations. Genes Dev. 27, 355-371
46. Lu, L. et al. (2010) Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc. Natl. Acad. Sci. U.S.A. 107, 1437-1442
47. Dong, J. et al. (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133
48. Chen, Q. et al. (2014) A temporal requirement for Hippo signaling in mammary gland differentiation, growth, and tumorigenesis. Genes Dev. 28, 432-437
49. Lamar, J.M. et al. (2012) The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proc. Natl. Acad. Sci. U.S.A. 109, E2441-E2450
50. Yu, F.X. et al. (2012) Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791
51. Chen, D. et al. (2012) LIFR is a breast cancer metastasis suppressor upstream of the Hippo-YAP pathway and a prognostic marker. Nat. Med. 18, 1511-1517
52. Liu-Chittenden, Y. et al. (2012) Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev. 26, 1300-1305
53. Jiao, S. et al. (2014) A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 25, 166-180
54. Dornhofer, N. et al. (2006) Connective tissue growth factor-specific monoclonal antibody therapy inhibits pancreatic tumor growth and metastasis. Cancer Res. 66, 5816-5827
55. Finger, E.C. et al. (2014) CTGF is a therapeutic target for metastatic melanoma. Oncogene 33, 1093-1100
56. Zhang, J. and Ma, L. (2012) MicroRNA control of epithelial-mesenchymal transition and metastasis. Cancer Metastasis Rev. 31, 653-662
57. Pencheva, N. and Tavazoie, S.F. (2013) Control of metastatic progression by microRNA regulatory networks. Nat. Cell Biol. 15, 546-554
58. Medina, P.P. et al. (2010) OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 467, 86-90
59. Asangani, I.A. et al. (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27, 2128-2136
60. Zhu, S. et al. (2008) MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 18, 350-359
61. Voorhoeve, P.M. et al. (2006) A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124, 1169-1181
62. Huang, Q. et al. (2008) The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat. Cell Biol. 10, 202-210
63. Ling, H. et al. (2013) MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat. Rev. Drug Discov. 12, 847-865
64. Friedl, P. and Wolf, K. (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374
65. Clark, E.A. et al. (2000) Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406, 532-535
66. Ma, L. et al. (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682-688
67. Ma, L. et al. (2010) Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat. Biotechnol. 28, 341-347
68. 1 integrin. J. Cell Biol. 199, 653-668
69. Sonoshita, M. et al. (2011) Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling. Cancer Cell 19, 125-137
70. Kallergi, G. et al. (2011) Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res. 13, R59
71. Yu, M. et al. (2013) Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580-584
72. Lu, X. and Kang, Y. (2010) Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin. Cancer Res. 16, 5928-5935
73. Rhim, A.D. et al. (2012) EMT and dissemination precede pancreatic tumor formation. Cell 148, 349-361
74. Joyce, J.A. and Pollard, J.W. (2009) Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252
75. Allinen, M. et al. (2004) Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6, 17-32
76. Karnoub, A.E. et al. (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449, 557-563
77. Dirat, B. et al. (2011) Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 71, 2455-2465
78. Wyckoff, J. et al. (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 64, 7022-7029
79. Krebs, M.G. et al. (2014) Molecular analysis of circulating tumour cells - biology and biomarkers. Nat. Rev. Clin. Oncol. 11, 129-144
80. Yap, T.A. et al. (2014) Circulating tumor cells: a multifunctional biomarker. Clin. Cancer Res. 20, 2553-2568
81. Miyamoto, D.T. et al. (2014) Circulating tumour cells - monitoring treatment response in prostate cancer. Nat. Rev. Clin. Oncol. 11, 401-412
82. Hou, J.M. et al. (2012) Clinical significance and molecular characteristics of circulating tumor cells and circulating tumor microemboli in patients with small-cell lung cancer. J. Clin. Oncol. 30, 525-532
83. Aceto, N. et al. (2014) Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158, 1110-1122
84. Hodgkinson, C.L. et al. (2014) Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer. Nat. Med. 20, 897-903
85. Yu, M. et al. (2014) Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 345, 216-220
86. Nash, G.F. et al. (2002) Platelets and cancer. Lancet Oncol. 3, 425-430
87. Gul, N. et al. (2014) Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J. Clin. Invest. 124, 812-823
88. Douma, S. et al. (2004) Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 430, 1034-1039
89. Yu, M. et al. (2012) RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 487, 510-513
90. Valastyan, S. and Weinberg, R.A. (2011) Tumor metastasis: molecular insights and evolving paradigms. Cell 147, 275-292
91. Padua, D. et al. (2008) TGFβ primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133, 66-77
92. Gupta, G.P. et al. (2007) Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446, 765-770
93. Chen, Q. et al. (2011) Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 20, 538-549
94. Zhang, X.H. et al. (2009) Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 16, 67-78
95. Kang, Y. et al. (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549
96. Minn, A.J. et al. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524
97. Bos, P.D. et al. (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1009
98. Mundy, G.R. (2002) Metastasis to bone: causes, consequences and therapeutic opportunities. Nat. Rev. Cancer 2, 584-593
99. Sosa, M.S. et al. (2014) Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat. Rev. Cancer 14, 611-622
100. Giancotti, F.G. (2013) Mechanisms governing metastatic dormancy and reactivation. Cell 155, 750-764
101. Barkan, D. et al. (2008) Inhibition of metastatic outgrowth from single dormant tumor cells by targeting the cytoskeleton. Cancer Res. 68, 6241-6250
102. Barkan, D. et al. (2010) Metastatic growth from dormant cells induced by a Col-I-enriched fibrotic environment. Cancer Res. 70, 5706-5716
103. 1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proc. Natl. Acad. Sci. U.S.A. 106, 10290-10295
104. Gao, H. et al. (2012) The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites. Cell 150, 764-779
105. Bao, S. et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760
106. + breast cancer-initiating cells to radiation. J. Natl. Cancer Inst. 98, 1777-1785
107. Baumann, M. et al. (2008) Exploring the role of cancer stem cells in radioresistance. Nat. Rev. Cancer 8, 545-554
108. Holohan, C. et al. (2013) Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 13, 714-726
109. Wang, Z. et al. (2011) Pancreatic cancer: understanding and overcoming chemoresistance. Nat. Rev. Gastroenterol. Hepatol. 8, 27-33
110. Arumugam, T. et al. (2009) Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 69, 5820-5828
111. Sui, H. et al. (2014) Epithelial-mesenchymal transition and drug resistance: role, molecular mechanisms, and therapeutic strategies. Oncol. Res. Treat. 37, 584-589
112. Dave, B. et al. (2012) Epithelial-mesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res. 14, 202
113. Adam, L. et al. (2009) miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin. Cancer Res. 15, 5060-5072
114. Siebzehnrubl, F.A. et al. (2013) The ZEB1 pathway links glioblastoma initiation, invasion and chemoresistance. EMBO Mol. Med. 5, 1196-1212
115. Ren, J. et al. (2013) Inhibition of ZEB1 reverses EMT and chemoresistance in docetaxel-resistant human lung adenocarcinoma cell line. J. Cell. Biochem. 114, 1395-1403
116. Haddad, Y. et al. (2009) Delta-crystallin enhancer binding factor 1 controls the epithelial to mesenchymal transition phenotype and resistance to the epidermal growth factor receptor inhibitor erlotinib in human head and neck squamous cell carcinoma lines. Clin. Cancer Res. 15, 532-542
117. Zhang, P. et al. (2014) ATM-mediated stabilization of ZEB1 promotes DNA damage response and radioresistance through CHK1. Nat. Cell Biol. 16, 864-875
118. Zhang, P. et al. (2014) miR-205 acts as a tumour radiosensitizer by targeting ZEB1 and Ubc13. Nat. Commun. 5, 5671
119. Liu, W. et al. (2014) Inhibition of TBK1 attenuates radiation-induced epithelial-mesenchymal transition of A549 human lung cancer cells via activation of GSK-3β and repression of ZEB1. Lab. Invest. 94, 362-370
120. Chen, W. et al. (2013) Effect of AKT inhibition on epithelial-mesenchymal transition and ZEB1-potentiated radiotherapy in nasopharyngeal carcinoma. Oncol. Lett. 6, 1234-1240
121. Cortez, M.A. et al. (2014) Therapeutic delivery of miR-200c enhances radiosensitivity in lung cancer. Mol. Ther. 22, 1494-1503
122. Wellner, U. et al. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 11, 1487-1495
123. Spaderna, S. et al. (2008) The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 68, 537-544
124. Aigner, K. et al. (2007) The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26, 6979-6988
125. Yang, Y. et al. (2014) ZEB1 sensitizes lung adenocarcinoma to metastasis suppression by PI3K antagonism. J. Clin. Invest. 124, 2696-2708
126. Zhang, P. et al. (2015) ZEB1: at the crossroads of epithelial-mesenchymal transition, metastasis and therapy resistance. Cell Cycle 14, 481-487