Crosstalk between breast cancer stem cells and metastatic niche: Emerging molecular metastasis pathway?

Tumor Biology

Volumn 34, Issue 4, 2013, Pages 2019-2030

  Fazilaty, Hassan ^a   Gardaneh, Mossa ^b   Bahrami, Tayyeb ^a   Salmaninejad, Arash ^a   Behnam, Babak ^c  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b NATIONAL INSTITUTE OF GENETIC ENGINEERING AND BIOTECHNOLOGY   (Iran)

^c IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Breast cancer metastasis; Cancer stem cell; Epithelial to mesenchymal transition; Metastatic niche; Molecular metastasis pathway; TGF

Indexed keywords

E74 LIKE FACTOR 5; HYPOXIA INDUCIBLE FACTOR; SMAD PROTEIN; TENASCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

BREAST CANCER; CANCER STEM CELL; CELL DIFFERENTIATION; CELL RENEWAL; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMAN; METASTASIS; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR CELL; TUMOR INVASION; TUMOR MICROENVIRONMENT;

EID: 84881481392     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-013-0831-y     Document Type: Review

References (129)

1. Klein CA. Cancer. The metastasis cascade. Science. 2008;321:1785-7.
2. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell. 2006;127:679-95.
3. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147:275-92.
4. Chaffer CH, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559-64.
5. Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer. 2009;9:274-84.
6. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer. 2003;3:453-8.
7. Friedl P, Wolf K. Tumor-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer. 2003;3:362-74.
8. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5:744-9.
9. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells - perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 2006;66:9339-44.
10. Korkaya H, Wicha MS. Selective targeting of cancer stem cells: a new concept in cancer therapeutics. Bio Drugs. 2007;21:299-310.
11. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009;69:1302-13.
12. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med. 2006;355:1253-61.
13. Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK, et al. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell. 2010;6:603-15.
14. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-7.
15. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumor initiating cells. Nature. 2004;432:396-401.
16. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983-8. Erratum in: Proc Natl Acad Sci USA 2003.
17. Li F, Tiede B, Massague J, Kang Y. Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res. 2007;17:3-14.
18. Velasco-Velázquez MA, Homsi N, De La Fuente M, Pestell RG. Breast cancer stem cells. Int J Biochem Cell Biol. 2012;44:573-7.
19. Sajithlal GB, Rothermund K, Zhang F, Dabbs DJ, Latimer JJ, Grant SG, et al. Permanently blocked stem cells derived from breast cancer cell lines. Stem Cells. 2010;28:1008-18.
20. Phillips TM, McBride WH, Pajonk F. The response of CD24 (-/low) /CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst. 2006;98:1777-85.
21. Chu JE, Allan AL. The role of cancer stem cells in the organ tropism of breast cancer metastasis: a mechanistic balance between the "seed" and the "soil"? Int J Breast Cancer. 2012;2012:209748.
22. Huntly BJ, Shigematsu H, Deguchi K, Lee BH, Mizuno S, Duclos N, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6:587-96.
23. Krivtsov AV, Twomey D, Feng Z, Stubbs MC, Wang Y, Faber J, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006;442:818-22.
24. 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.
25. Morel AP, Lièvre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One. 2008;3:e2888.
26. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871-90.
27. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119:1420-8.
28. 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.
29. Kong D, Li Y, Wang Z, Sarkar FH. Cancer stem cells and epithelial-to-mesenchymal transition (EMT)-phenotypic cells: are they cousins or twins? Cancers (Basel). 2011;3:716-29.
30. Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol. 2012;22:396-403.
31. Gilles C, Polette M, Mestdagt M, Nawrocki-Raby B, Ruggeri P, Birembaut P, et al. Transactivation of vimentin by β-catenin in human breast cancer cells. Cancer Res. 2003;63:2658-64.
32. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, et al. Functional interaction of β-catenin with the transcription factor LEF-1. Nature (Lond). 1996;382:638-42.
33. Bindels S, Mestdagt M, Vandewalle C, Jacobs N, Volders L, Noel A, et al. Regulation of vimentin by SIP1 in human epithelial breast tumor cells. Oncogene. 2006;25:4975-85.
34. Zhu QS, Rosenblatt K, Huang KL, Lahat G, Brobey R, Bolshakov S, et al. Vimentin is a novel AKT1 target mediating motility and invasion. Oncogene. 2011;30:457-70.
35. Jing Y, Han Z, Zhang S, Liu Y, Wei L. Epithelial-mesenchymal transition in tumor microenvironment. Cell Biosci. 2011;1:29.
36. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010;29:4741-51.
37. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia. 2010;15:117-34.
38. Piek E, Moustakas A, Kurisaki A, Heldin CH, ten Dijke P. TGF-β type I receptor/ALK-5 and smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci. 1999;112:4557-68.
39. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A. TGF-β and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymalcell transition. Mol Biol Cell. 2005;16:1987-2002.
40. Hoot KE, Lighthall J, Han G, Lu SL, Li A, Ju W, et al. Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression. J Clin Invest. 2008;118:2722-32.
41. Deckers M, van Dinther M, Buijs J, Que I, Löwik C, van der Pluijm G, et al. The tumor suppressor Smad4 is required for transforming growth factor β-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res. 2006;66:2202-9.
42. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-β1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest. 2003;112:1486-94.
43. Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, Mizel DE, et al. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol. 1999;1:260-6.
44. Kaimori A, Potter J, Kaimori JY, Wang C, Mezey E, Koteish A. Transforming growth factor-β1 induces an epithelial-to-mesenchymal transition state in mouse hepatocytes in vitro. J Biol Chem. 2007;282:22089-101.
45. Desgrosellier JS, Mundell NA, McDonnell MA, Moses HL, Barnett JV. Activin receptor-like kinase 2 and Smad6 regulate epithelial-mesenchymal transformation during cardiac valve formation. Dev Biol. 2005;280:201-10.
46. Armstrong EJ, Bischoff J. Heart valve development: endothelial cell signaling and differentiation. Circ Res. 2004;95:459-70.
47. Saika S, Ikeda K, Yamanaka O, Sato M, Muragaki Y, Ohnishi Y, et al. Transient adenoviral gene transfer of Smad7 prevents injury-induced epithelial-mesenchymal transition of lens epithelium in mice. Lab Invest. 2004;84:1259-70.
48. Dooley S, Hamzavi J, Ciuclan L, Godoy P, Ilkavets I, Ehnert S, et al. Hepatocyte-specific Smad7 expression attenuates TGF-β-mediated fibrogenesis and protects against liver damage. Gastroenterology. 2008;135:642-59.
49. Xu J, Lamouille S, Derynck R. TGF-β-induced epithelial to mesenchymal transition. Cell Res. 2009;19:156-72.
50. Cho HJ, Baek KE, Saika S, Jeong MJ, Yoo J. Snail is required for transforming growth factor-b-induced epithelial-mesenchymal transition by activating PI3 kinase/Akt signal pathway. Biochem Biophys Res Commun. 2007;353:337-43.
51. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-β employs HMGA2 to elicit epithelial- mesenchymal transition. J Cell Biol. 2006;174:175-83.
52. Thuault S, Tan EJ, Peinado H, Cano A, Heldin CH, Moustakas A. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to- mesenchymal transition. J Cell Biol. 2008;283:33437-46.
53. Tan EJ, Thuault S, Caja L, Carletti T, Heldin CH, Moustakas A. Regulation of transcription factor twist expression by the DNA architectural protein high mobility group A2 during epithelial-to-mesenchymal transition. J Biol Chem. 2012;287:7134-45.
54. Barrallo-Gimeno A, Nieto MA. The snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 2005;132:3151-61.
55. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature. 2003;425:577-84.
56. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL. Regulation of the polarity protein Par6 by TGF-β receptors controls epithelial cell plasticity. Science. 2005;307:1603-9.
57. Viloria-Petit AM, David L, Jia JY, Erdemir T, Bane AL, Pinnaduwage D, et al. A role for the TGFβ-Par6 polarity pathway in breast cancer progression. Proc Natl Acad Sci U S A. 2009;106:14028-33.
58. Kim ES, Sohn YW, Moon A. TGF-β-induced transcriptional activation of MMP-2 is mediated by activating transcription factor (ATF) 2 in human breast epithelial cells. Cancer Lett. 2007;252:147-56.
59. Kim JY, Kim YM, Yang CH, Cho SK, Lee JW, Cho M. Functional regulation of SlugSnail2 is dependent on GSK-3β-mediated phosphorylation. FEBS J. 2012;279:2929-39.
60. Byun HJ, Hong IK, Kim E, Jin YJ, Jeoung DI, Hahn JH, et al. A splice variant of CD99 increases motility and MMP-9 expression of human breast cancer cells through the AKT-, ERK-, and JNK-dependent AP-1 activation signaling pathways. J Biol Chem. 2006;281:34833-47.
61. Craene BD, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer. 2013;13:97-110.
62. Ouyang G, Wang Z, Fang X, Liu J, Yang CJ. Molecular signaling of the epithelial to mesenchymal transition in generating and maintaining cancer stem cells. Cell Mol Life Sci. 2010;67:2605-18.
63. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 2009;11:1487-95.
64. Thiery JP. Epithelial-mesenchymal transitions in tumor progression. Nat Rev Cancer. 2002;2:442-54.
65. Zhang J, Liang Q, Lei Y, Yao M, Li L, Gao X, et al. SOX4 induces epithelial-mesenchymal transition and contributes to breast cancer progression. Cancer Res. 2012;72:4597-608.
66. Ocaña OH, Córcoles R, Fabra A, Moreno-Bueno G, Acloque H, Vega S, et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer prrx1. Cancer Cell. 2012;22:709-24.
67. 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.
68. Brabletz T. To differentiate or not - routes towards metastasis? Nat Rev Cancer. 2012;12:425-36.
69. Brabletz T. EMT and MET in metastasis: where are the cancer stem cells? Cancer Cell. 2012;22:699-701.
70. Nieto MA. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol. 2011;27:347-76.
71. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008;14:818-29.
72. Kim NH, Kim HS, Li XY, Lee I, Choi HS, Kang SE, et al. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol. 2011;195:417-33.
73. Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U, et al. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle. 2011;10:4256-71.
74. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10:593-601.
75. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008;9:582-9.
76. Chang CJ, Chao CH, Xia W, Yang JY, Xiong Y, Li CW, et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol. 2011;13:317-23.
77. Kim T, Veronese A, Pichiorri F, Lee TJ, Jeon YJ, Volinia S, et al. p53 regulates epithelial to mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J Exp Med. 2011;208:875-83.
78. Yamakuchi M, Lowenstein CJ. MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle. 2009;8:712-5.
79. Samavarchi-Tehrani P, Golipour A, David L, Sung HK, Beyer TA, Datti A, et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell. 2010;7:64-77.
80. Scheel C, Eaton EN, Li SHJ, Chaffer CL, Reinhardt F, Kah KJ, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell. 2011;145:926-40.
81. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial mesenchymal transition is essential for squamous cell carcinomametastasis. Cancer Cell. 2012;22:725-36.
82. Frisch SM. The epithelial cell default-phenotype hypothesis and its implications for cancer. Bioessays. 1997;19:705-9.
83. Mullen AC, Orlando DA, Newman JJ, Lovén J, Kumar RM, Bilodeau S, et al. Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell. 2011;147:565-76.
84. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell. 2013;153:307-19.
85. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005;122:947-56.
86. Lu X, Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res. 2010;16:5928-35.
87. Semenza GL. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci. 2012;33:207-14.
88. Wang Y, Liu Y, Malek SN, Zheng P, Liu Y. Targeting HIF1a eliminates cancer stem cells in hematological malignancies. Cell Stem Cell. 2011;8:399-411.
89. Keith B, Simon MC. Hypoxia inducible factors, stem cells and cancer. Cell. 2007;129:465-72.
90. Imai T, Horiuchi A, Wang C, Oka K, Ohira S, Nikaido T, et al. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am J Pathol. 2003;163:1437-47.
91. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, et al. Direct regulation of TWIST by HIF-1α promotes metastasis. Nat Cell Biol. 2008;10:295-305.
92. Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, Baek JH, et al. 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. 2006;66:2725-31.
93. Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1 (HIF-1): implications in metastasis and development. Cell Cycle. 2008;7:2090-6.
94. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res. 2003;63:1138-43.
95. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117:927-39.
96. Casas E, Kim J, Bendesky A, Ohno-Machado L, Wolfe CJ, Yang J. Snail2 is an essential mediator of Twist1-induced epithelial mesenchymal transition and metastasis. Cancer Res. 2011;71:245-54.
97. McKean DM, Sisbarro L, Ilic D, Kaplan-Alburquerque N, Nemenoff R, Weiser-Evans M, et al. FAK induces expression of Prx1 to promote tenascin-C-dependent fibroblast migration. J Cell Biol. 2003;161:393-402.
98. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 2002;3:155-66.
99. Savagner P, Yamada KM, Thiery JP. The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J Cell Biol. 1997;137:1403-19.
100. Medici D, Hay ED, Olsen BR. Snail and slug promote epithelial-mesenchymal transition through β-catenin-T-cell factor-4-dependent expression of transforming growth factor-β 3. Mol Biol Cell. 2008;19:4875-87.
101. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012;148:1015-28.
102. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861-72.
103. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663-76.
104. Zhou J, Ng AY, Tymms MJ, Jermiin LS, Seth AK, Thomas RS, et al. A novel transcription factor, ELF5, belongs to the ELF subfamily of ETS genes and maps to human chromosome 11p13-15, a region subject to LOH and rearrangement in human carcinoma cell lines. Oncogene. 1998;17:2719-32.
105. Zhou J, Chehab R, Tkalcevic J, Naylor MJ, Harris J, Wilson TJ, et al. Elf5 is essential for early embryogenesis and mammary gland development during pregnancy and lactation. EMBO J. 2005;24:635-44.
106. Oakes SR, Naylor MJ, Asselin-Labat ML, Blazek KD, Gardiner-Garden M, Hilton HN, et al. The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev. 2008;22:581-6.
107. Choi YS, Chakrabarti R, Escamilla-Hernandez R, Sinha S. Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev Biol. 2009;329:227-41.
108. Chakrabarti R, Wei Y, Romano RA, DeCoste C, Kang Y, Sinha S. Elf5 regulates mammary gland stem/progenitor cell fate by influencing notch signaling. Stem Cells. 2012;30:1496-508.
109. Chakrabarti R, Hwang J, Andres Blanco M, Wei Y, Lukačišin M, Romano RA, et al. Elf5 inhibits the epithelial-mesenchymal transition in mammary gland development and breast cancer metastasis by transcriptionally repressing Snail2. Nat Cell Biol. 2012;14:1212-22.
110. Mathsyaraja H, Ostrowski MC. Setting Snail2's pace during EMT. Nat Cell Biol. 2012;14:1122-3.
111. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer. 2009;9:285-93.
112. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74.
113. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell. 2009;15:35-44.
114. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive hematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820-7.
115. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006;25:9-34.
116. Mason SD, Joyce JA. Proteolytic networks in cancer. Trends Cell Biol. 2011;21:228-37.
117. Hildenbrand R, Jansen C, Wolf G, Bohme B, Berger S, von Minckwitz G, et al. Transforming growth factor-β stimulates urokinase expression in tumor-associated macrophages of the breast. Lab Invest. 1998;78:59-71.
118. + stroma cells in the breast cancer microenvironment. Clin Cancer Res. 2012;18:1004-14.
119. Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr HA, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481:85-9.
120. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17:867-74.
121. Kii I, Nishiyama T, Li M, Matsumoto K, Saito M, Amizuka N, et al. Incorporation of Tenascin-C into the extracellular matrix by Periostin underlies an extracellular meshwork architecture. J Biol Chem. 2010;285:2028-39.
122. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436:518-24.
123. Oskarsson T, Massague J. Extracellular matrix players in metastatic niches. EMBO J. 2012;31:254-6.
124. Serrano I, McDonald PC, Lock FE, Dedhar S. Role of the integrin-linked kinase (ILK)/Rictor complex in TGFβ-1-induced epithelial-mesenchymal transition (EMT). Oncogene. 2013;32:50-60.
125. Massague J. TGF-β signaling in context. Nat Rev Mol Cell Biol. 2012;13:616-30.
126. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339:580-4.
127. Ikushima H, Miyazono K. TGFβ signalling: a complex web in cancer progression. Nat Rev Cancer. 2010;10:415-24.
128. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011;20:576-90.
129. Li L, Neaves WB. Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 2006;66:4553-7.