Forcing through Tumor Metastasis: The Interplay between Tissue Rigidity and Epithelial-Mesenchymal Transition

Trends in Cell Biology

Volumn 26, Issue 2, 2016, Pages 111-120

  Wei, Spencer C ^a,c   Yang, Jing ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

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

Author keywords

EMT; Extracellular matrix; Matrix stiffness; Metastasis; Tissue rigidity

Indexed keywords

FIBRONECTIN; NERVE CELL ADHESION MOLECULE; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN; VIMENTIN;

CELL PLASTICITY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; HUMAN; MECHANOTRANSDUCTION; METASTASIS; METASTASIS POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; RIGIDITY; TISSUE RIGIDITY; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; BIOMECHANICS; METABOLISM; PATHOLOGY; PERMEABILITY; PHYSIOLOGY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ANIMALS; BIOMECHANICAL PHENOMENA; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; NEOPLASM METASTASIS; PERMEABILITY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR MICROENVIRONMENT;

EID: 84957591326     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2015.09.009     Document Type: Review

References (90)

1. Jaalouk D.E., Lammerding J. Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 2009, 10:63-73.
2. Butcher D.T., et al. A tense situation: forcing tumour progression. Nat. Rev. Cancer 2009, 9:108-122.
3. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 2011, 17:320-329.
4. Conklin M.W., et al. Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am. J. Pathol. 2011, 178:1221-1232.
5. Provenzano P.P., et al. Collagen density promotes mammary tumor initiation and progression. BMC Med. 2008, 6:11.
6. Yu H., et al. Forcing form and function: biomechanical regulation of tumor evolution. Trends Cell Biol. 2011, 21:47-56.
7. Levental K.R., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
8. Paszek M.J., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
9. Van den Eynden G.G., et al. A fibrotic focus is a prognostic factor and a surrogate marker for hypoxia and (lymph)angiogenesis in breast cancer: review of the literature and proposal on the criteria of evaluation. Histopathology 2007, 51:440-451.
10. Colpaert C., et al. The presence of a fibrotic focus is an independent predictor of early metastasis in lymph node-negative breast cancer patients. Am. J. Surg. Pathol. 2001, 25:1557-1558.
11. Hasebe T., et al. Prognostic significance of fibrotic focus in invasive ductal carcinoma of the breast: a prospective observational study. Modern Pathol. 2002, 15:502-516.
12. Lopez J.I., et al. In situ force mapping of mammary gland transformation. Integr. Biol. (Camb.) 2011, 3:910-921.
13. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat. (Basel) 1995, 154:8-20.
14. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
15. Tsai J.H., et al. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 2012, 22:725-736.
16. Yang J., et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
17. Tsai J.H., Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev. 2013, 27:2192-2206.
18. Ocana O.H., et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer prrx1. Cancer Cell 2012, 22:709-724.
19. Leight J.L., et al. Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial-mesenchymal transition. Mol. Biol. Cell 2012, 23:781-791.
20. Wei S.C., et al. Matrix stiffness drives epithelial-mesenchymal transition and tumour metastasis through a TWIST1-G3BP2 mechanotransduction pathway. Nat. Cell Biol. 2015, 17:678-688.
21. Gomez E.W., et al. Tissue geometry patterns epithelial-mesenchymal transition via intercellular mechanotransduction. J. Cell. Biochem. 2010, 110:44-51.
22. Dupont S., et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474:179-183.
23. Shao D.D., et al. KRAS and YAP1 converge to regulate EMT and tumor survival. Cell 2014, 158:171-184.
24. Lamar J.M., et al. The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E2441-E2450.
25. Zhao B., et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 2008, 22:1962-1971.
26. Wang Y.C., et al. Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature 2012, 484:390-393.
27. le Duc Q., et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 2010, 189:1107-1115.
28. Scarpa E., et al. Cadherin switch during EMT in neural crest cells leads to contact inhibition of locomotion via repolarization of forces. Dev. Cell 2015, 34:421-434.
29. Samuel M.S., et al. Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 2011, 19:776-791.
30. Das T., et al. A molecular mechanotransduction pathway regulates collective migration of epithelial cells. Nat. Cell Biol. 2015, 17:276-287.
31. Nguyen-Ngoc K.V., et al. ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E2595-E2604.
32. Butler L.C., et al. Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat. Cell Biol. 2009, 11:859-864.
33. Plodinec M., et al. The nanomechanical signature of breast cancer. Nat. Nanotechnol. 2012, 7:757-765.
34. Provenzano P.P., et al. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 2006, 4:38.
35. Brabletz T., et al. Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and beta-catenin. Cells Tissues Organs. 2005, 179:56-65.
36. Plotnikov S.V., et al. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 2012, 151:1513-1527.
37. Xu W., et al. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS ONE 2012, 7:e46609.
38. Physical Sciences - Oncology Centers Network, et al. A physical sciences network characterization of non-tumorigenic and metastatic cells. Sci. Rep. 2013, 3:1449.
39. Davidson P.M., et al. Nuclear deformability constitutes a rate-limiting step during cell migration in 3-D environments. Cell. Mol. Bioeng. 2014, 7:293-306.
40. Denais C., Lammerding J. Nuclear mechanics in cancer. Adv. Exp. Med. Biol. 2014, 773:435-470.
41. Yang W.H., et al. RAC1 activation mediates Twist1-induced cancer cell migration. Nat. Cell Biol. 2012, 14:366-374.
42. Martin A.C., et al. Integration of contractile forces during tissue invagination. J. Cell Biol. 2010, 188:735-749.
43. Riaz M., et al. High TWIST1 mRNA expression is associated with poor prognosis in lymph node-negative and estrogen receptor-positive human breast cancer and is co-expressed with stromal as well as ECM related genes. Breast Cancer Res. 2012, 14:R123.
44. Kirschmann D.A., et al. A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res. 2002, 62:4478-4483.
45. El-Haibi C.P., et al. Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:17460-17465.
46. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
47. Nieto M.A. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 2011, 27:347-376.
48. Baldwin A.K., et al. Epithelial-mesenchymal status influences how cells deposit fibrillin microfibrils. J. Cell Sci. 2014, 127:158-171.
49. Maschler S., et al. Enhanced tenascin-C expression and matrix deposition during Ras/TGF-beta-induced progression of mammary tumor cells. Oncogene 2004, 23:3622-3633.
50. Pickup M.W., et al. Stromally derived lysyl oxidase promotes metastasis of transforming growth factor-beta-deficient mouse mammary carcinomas. Cancer Res. 2013, 73:5336-5346.
51. Goetz J.G., et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
52. Calvo F., et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat. Cell Biol. 2013, 15:637-646.
53. Prager-Khoutorsky M., et al. Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat. Cell Biol. 2011, 13:1457-1465.
54. Hasebe T., et al. Atypical tumor-stromal fibroblasts in invasive ductal carcinoma of the breast. Am. J. Surg. Pathol. 2011, 35:325-336.
55. Maschler S., et al. Tumor cell invasiveness correlates with changes in integrin expression and localization. Oncogene 2005, 24:2032-2041.
56. Jiang G., et al. Rigidity sensing at the leading edge through alphavbeta3 integrins and RPTPalpha. Biophys. J. 2006, 90:1804-1809.
57. Ehrlicher A.J., et al. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 2011, 478:260-263.
58. Kang J., et al. Structurally governed cell mechanotransduction through multiscale modeling. Sci. Rep. 2015, 5:8622.
59. Geiger B., et al. Transmembrane crosstalk between the extracellular matrix--cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2001, 2:793-805.
60. Johnson C.P., et al. Forced unfolding of proteins within cells. Science 2007, 317:663-666.
61. Friedland J.C., et al. Mechanically activated integrin switch controls alpha5beta1 function. Science 2009, 323:642-644.
62. Zhu J., et al. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol. Cell 2008, 32:849-861.
63. Valiathan R.R., et al. Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev. 2012, 31:295-321.
64. Zhang K., et al. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat. Cell Biol. 2013, 15:677-687.
65. Walsh L.A., et al. Discoidin domain receptor 2 is a critical regulator of epithelial-mesenchymal transition. Matrix Biol. 2011, 30:243-247.
66. Xu H., et al. Discoidin domain receptors promote alpha1beta1- and alpha2beta1-integrin mediated cell adhesion to collagen by enhancing integrin activation. PLoS ONE 2012, 7:e52209.
67. Luzzi K.J., et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153:865-873.
68. Chambers A.F., et al. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2:563-572.
69. Erler J.T., 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.
70. Lu P., et al. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 2012, 196:395-406.
71. Erler J.T., et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006, 440:1222-1226.
72. Barry-Hamilton V., et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat. Med. 2010, 16:1009-1017.
73. Cox T.R., et al. The hypoxic cancer secretome induces pre-metastatic bone lesions through lysyl oxidase. Nature 2015, 522:106-110.
74. Wong C.C., et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:16369-16374.
75. Gilkes D.M., et al. Hypoxia and the extracellular matrix: drivers of tumour metastasis. Nat. Rev. Cancer 2014, 14:430-439.
76. Gort E.H., et al. The TWIST1 oncogene is a direct target of hypoxia-inducible factor-2alpha. Oncogene 2008, 27:1501-1510.
77. Yang M.H., et al. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 2008, 10:295-305.
78. Lester R.D., et al. uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J. Cell Biol. 2007, 178:425-436.
79. Kaplan R.N., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
80. Korpal M., et al. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nat. Med. 2011, 17:1101-1108.
81. Townley A.K., et al. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 2008, 121:3025-3034.
82. Wang H., et al. The osteogenic niche promotes early-stage bone colonization of disseminated breast cancer cells. Cancer Cell 2015, 27:193-210.
83. Mani S.A., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
84. Morel A.P., et al. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008, 3:e2888.
85. Oskarsson T., et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 2011, 17:867-874.
86. Malanchi I., et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2011, 481:85-89.
87. Norris R.A., et al. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J. Cell. Biochem. 2007, 101:695-711.
88. Kii I., et al. Incorporation of tenascin-C into the extracellular matrix by periostin underlies an extracellular meshwork architecture. J. Biol. Chem. 2010, 285:2028-2039.
89. Hoffman B.D., et al. Dynamic molecular processes mediate cellular mechanotransduction. Nature 2011, 475:316-323.
90. Eyckmans J., et al. A hitchhiker's guide to mechanobiology. Dev. Cell 2011, 21:35-47.