Snail1-dependent activation of cancer-associated fibroblast controls epithelial tumor cell invasion and metastasis

Cancer Research

Volumn 76, Issue 21, 2016, Pages 6205-6217

  Alba Castellón, Lorena ^a   Olivera Salguero, Rubén ^a   Mestre Farrera, Aida ^a   Peña, Raúl ^a   Herrera, Mercedes ^b   Bonilla, Félix ^c   Casal, J Ignacio ^d   Baulida, Josep ^a   Peña, Cristina ^b   De Herreros, Antonio García ^a,e  

^a HOSPITAL DEL MAR   (Spain)

^b HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^c Centro de Estudios Biosanitarios   (Spain)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^e UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROSTAGLANDIN E2; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; SNAI1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TUMOR INVASION; ANIMAL; NEOPLASM; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; CANCER-ASSOCIATED FIBROBLASTS; CELL LINE, TUMOR; DINOPROSTONE; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS, GLANDULAR AND EPITHELIAL; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84995608162     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0176     Document Type: Article

References (44)

1. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial to mesenchymal transitions in development and disease. Cell 2009;139:871-90.
2. Tarin D, Thompson EW, Newgreen DF. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 2005;65:5996-6001.
3. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011;147:992-1009.
4. García de Herreros A, Baulida J. Cooperation, amplification, and feed-back in epithelial-mesenchymal transition. Biochim Biophys Acta 2012;1825: 223-8.
5. Peinado H, Ballestar E, Esteller M, Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 2004;24:306-19.
6. Herranz N, Pasini D, Díaz VM, Francí C, Gutiérrez A, Dave N, et al. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol Cell Biol 2008;28:4772-81.
7. Hou Z, Peng H, Ayyanathan K, Yan KP, Langer EM, Longmore GD, et al. The LIM protein Ajuba recruits protein arginine methyltransferase 5 tomediate SNAIL-dependent transcriptional repression. Mol Cell Biol 2008;28: 3198-207.
8. Dong C, Wu Y, Yao J, Wang Y, Yu Y, Rychahou PG, et al. G9a interacts with Snail and is critical for Snail-mediated E-cadherin repression in human breast cancer. J Clin Invest 2012;122:1469-86.
9. Stanisavljevic J, Porta-de-la-Riva M, Batlle R, Garcia de Herreros A, Baulida J. The p65 subunit of NF-κB and PARP1 assist Snail1 in activating fibronectin transcription. J Cell Sci 2011;124:4161-71.
10. Hsu DSS, Wang HJ, Tai SK, Chou CH, Hsieh CH, Chiu PH, et al. Acetylation of Snail modulates the cytokinome of cancer cells to enhance the recruitment of macrophages. Cancer Cell 2014;26:534-48.
11. Lin Y, Li XY, Willis AL, Liu C, Chen G, Weiss SJ. Snail1-dependent control of embryonic stem cell pluripotency and lineage commitment. Nat Commun 2014;5:3070.
12. Rowe RG, Li XY, Hu Y, Saunders TL, Virtanen I, Garcia de Herreros A, et al. Mesenchymal cells reactivate Snail1 expression to drive three-dimensional invasion programs. J Cell Biol 2009;184:399-408.
13. Batlle R, Alba-Castellón L, Loubat-Casanovas J, Armenteros E, Francí C, Stanisavljevic J, et al. Snail1 controls TGF-β responsiveness and differentiation of mesenchymal stem cells. Oncogene 2013;32:3381-9.
14. Pietras K, Ostman A. Hallmarks or cancer: interactions with the tumor stroma. Exp Cell Res 2010;316:1324-31.
15. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Gosse R, Marshall JF, Harrington K, et al. Fibroblast-led colective invasion of carcinoma cell with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007;9:1392-400.
16. Li HJ, Reinhardt F, Herschman HR, Weinberg RA. Cancer-stimulated mesenchymal stem cells create a carcinoma stem cell niche via Prostaglandin E2 signaling. Cancer Discov 2012;2:840-55.
17. Calon A, Espinet E, Palomo-Ponce S, Tauriello DV, Iglesias M, Céspedes MV, et al. Dependency of colorectal cancer on a TGFβ-driven program in for metastasis initiation. Cancer Cell 2012;22: 571-84.
18. Herrera A, Herrera M, Alba-Castellón L, Silva J, García V, Loubat-Casanovas J, et al. Protumorigenic effects of Snail-expression fibroblasts on colon cancer cells. Int J Cancer 2014;134:2984-90.
19. Francí C, Gallén M, Alameda F, Baró T, Iglesias M, Virtanen I, et al. Snail1 protein in the stroma as a new putative prognosis marker for colon tumours. PLoS One 2009;4:e5595.
20. Stanisavljevic J, Loubat-Casanovas J, Herrera M, Luque T, Peña R, Lluch A, et al. Snail1-expressing fibroblasts in the tumor microenvironment display mechanical properties that support metastasis. Cancer Res 2015;75: 284-95.
21. Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, et al. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet 2015;47:320-9.
22. Torres S, Garcia-Palmero I, Herrera M, Bartolomé RA, Peña C, Fernandez-Aceñero MJ, et al. LOXL2 is highly expressed in cancer-associated fibroblasts and associates to poor colon cancer survival. Clin Cancer Res 2015;21:4892-902.
23. Francí C, Takkunen M, Dave N, Alameda F, Gómez S, Rodríguez R, et al. Expression of Snail protein in tumor-stroma interface. Oncogene 2006;25: 5134-44.
24. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirusmiddle T oncogene:a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;2:954-61.
25. Batlle E, Sancho E, Francí C, Domínguez D, Monfar M, Baulida J, et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000;2:84-9
26. Millanes-Romero A, Herranz N, Perrera V, Iturbide A, Loubat-Casanovas J, Gil J, et al. Regulation of heterochromatin transcription by Snail1/LOXL2 during epithelial-to-mesenchymal transition. Mol Cell 2013;52: 746-57.
27. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007;449:557-63.
28. Mishra PJ, Humeniuk R, Medina DJ, Alexe G, Mesirov JP, Ganesan S, et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 2008;68:4331-9.
29. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011;19: 257-72.
30. Galardy RE, Grobelny D, Foellmer HG, Fernandez LA. Inhibition of angiogenesis by the matrix metalloprotease inhibitor N-[2R-2-(hydroxamidocarbonymethyl)-4-methylpentanoyl)]-L-tryptophan methylamide. Cancer Res 1994;54:4715-8.
31. DaCosta Byfield S, Major C, Laping NJ, Roberts AB. SB-505124 is a selective inhibitor of transforming growth factor-beta type I receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2004;65:744-52.
32. Wang D, DuBois RN. Eicosanoids and cancer. Nat Rev Cancer 2010;10: 181-93.
33. Mann JR, Backlund MG, Buchanan FG, Daikoku T, Holla VR, Rosenberg DR, et al. Repression of prostaglandin dehydrogenase by epidermal growth factor and Snail increases Prostaglandin E2 and promotes cancer progression. Cancer Res 2006;66:6649-56.
34. Penning TD, Talley JJ, Bertenshaw SR, Carter JS, Collins PW, Docter S, et al. Synthesis and biological evaluation of the 1.5 diarylpyrazole class of cyclooxygenase-2 inhibitors: identification of 4-[5-(4-methylphenyl)-3-(trifluoromethyl)-1H-pyrazole-1-yl]benzenesulfonamide (SC-58634, celecoxib). J Med Chem 1997;40:1347-65.
35. Cherukuri DP, Chen XB, Goulet AC, Young RN, Han Y, Heimark RL, et al. The EP4 receptor antagonist, L-161,982, blocks prostaglandin E2-induced signal transduction and cell proliferation in HCA-7 colon cancer cells. Exp Cell Res 2007;313:2969-79.
36. af Forselles K, Root J, Clarke T, Davey D, Aughto K, Dack K, et al. In vitro and in vivo characterization of PF-04418948, a novel, potent and selective prostaglandin EP2 receptor antagonist. Br J Pharmacol 2011; 164:1847-56.
37. Dai J, Kong Y, Si L, Chi Z, Cui C, Sheng X, et al. Large-scale analysis of PDGFRA mutations in melanomas and evaluation of their sensitivity to tyrosine kinase inhibitors imatinib and crenolanib. Clin Cancer Res 2013;19:6935-42.
38. Herrera M, Islam AB, Herrera A, Martín P, García V, Silva J, et al. Functional heterogeneity of cancer-associated fibroblasts from human colon tumors shows specific prognostic gene expression signature. Clin Cancer Res 2013;19:5914-26.
39. Escrivà M, Peiró S, Herranz N, Villagrasa P, Dave N, Montserrat-Sentís B, et al. Repression of PTEN phosphatase by Snail1 transcriptional factor during gamma radiation-induced apoptosis. Mol Cell Biol 2008;28:1528-40.
40. Menter DG, Schilsky RL, DuBois RN. Cyclo-oxygenase and cancer treatment: understanding the risk should be worth the reward. Clin Cancer Res 2010;16:1384-90.
41. Kurtova AV, Xiao J, Mo Q, Pazhanisamy S, Krasnow R, Lerner SP, et al. Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance. Nature 2015;517:209-13.
42. Tran HD, Luitel K, Kim M, Zhang K, Longmore GD, Tran DD. Transient SNAIL1 expression is necessary formetastatic competence in breast cancer. Cancer Res 2014;74:6330-40.
43. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008;14:518-27.
44. Massagué J. TGFβ in cancer. Cell 2008;134:215-30.