Snail1 induced in breast cancer cells in 3D collagen I gel environment suppresses cortactin and impairs effective invadopodia formation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 9, 2014, Pages 2037-2054

  Lee, Mi Sook ^a   Kim, Sudong ^a   Kim, Baek Gil ^b   Won, Cheolhee ^a   Nam, Seo Hee ^a   Kang, Suki ^b   Kim, Hye Jin ^a   Kang, Minkyung ^a   Ryu, Jihye ^a   Song, Haeng Eun ^a   Lee, Doohyung ^a   Ye, Sang Kyu ^a   Jeon, Noo Li ^a   Kim, Tai Young ^a   Cho, Nam Hoon ^b   Lee, Jung Weon ^a  

^a Seoul National University   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

3D collagen; Cortactin; Invasion; JNK; Snail 1

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; COLLAGEN GEL; COLLAGEN TYPE 1; CORTACTIN; DACTINOMYCIN; F ACTIN; MATRIGEL; MATRIX METALLOPROTEINASE 14; PROTEIN C JUN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; SNAIL1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UVOMORULIN;

ACIDITY; ARTICLE; BREAST CANCER CELL LINE; CELL DENSITY; CELL MEMBRANE; CELL SHAPE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; COLLAGEN DEGRADATION; CONTROLLED STUDY; E BOX ELEMENT; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOBLOTTING; INVADOPODIA FORMATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

3D COLLAGEN; CORTACTIN; INVASION; JNK; SNAIL1;

ACTINS; ANIMALS; BREAST NEOPLASMS; CATTLE; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CELL NUCLEUS; COLLAGEN TYPE I; CORTACTIN; FEMALE; GELS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MATRIX METALLOPROTEINASE 14; NEOPLASM INVASIVENESS; PHOSPHOSERINE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-JUN; PSEUDOPODIA; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MICROENVIRONMENT;

EID: 84902477423     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.05.007     Document Type: Article

References (52)

1. Friedl P., Wolf K. Proteolytic interstitial cell migration: a five-step process. Cancer Metastasis Rev. 2009, 28:129-135.
2. Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 2007, 17:107-117.
3. Destaing O., Block M.R., Planus E., Albiges-Rizo C. Invadosome regulation by adhesion signaling. Curr. Opin. Cell Biol. 2011, 23:1-10.
4. Albiges-Rizo C., Destaing O., Fourcade B., Planus E., Block M.R. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 2009, 122:3037-3049.
5. Yamada K.M., Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007, 130:601-610.
6. Friedl P., Sahai E., Weiss S., Yamada K.M. New dimensions in cell migration. Nat. Rev. Mol. Cell Biol. 2012, 13:743-747.
7. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
8. Box C., Rogers S.J., Mendiola M., Eccles S.A. Tumour-microenvironmental interactions: paths to progression and targets for treatment. Semin. Cancer Biol. 2010, 20:128-138.
9. Taddei M.L., Giannoni E., Comito G., Chiarugi P. Microenvironment and tumor cell plasticity: an easy way out. Cancer Lett. 2013, 341(1):80-96.
10. Dunn C., Wiltshire C., MacLaren A., Gillespie D.A. Molecular mechanism and biological functions of c-Jun N-terminal kinase signalling via the c-Jun transcription factor. Cell. Signal. 2002, 14:585-593.
11. Haeusgen W., Herdegen T., Waetzig V. The bottleneck of JNK signaling: molecular and functional characteristics of MKK4 and MKK7. Eur. J. Cell Biol. 2011, 90:536-544.
12. Derijard B., Hibi M., Wu I.-H., Barrett T., Su B., Deng T., Karin M., Davis R.J. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-JUN activation domain. Cell 1994, 76:1025-1037.
13. Musti A.M., Treier M., Bohmann D. Reduced ubiquitin-dependent degradation of c-Jun after phosphorylation by MAP kinases. Science 1997, 275:400-402.
14. Ebelt N.D., Cantrell M.A., Van Den Berg C.L. c-Jun N-terminal kinases mediate a wide range of targets in the metastatic cascade. Genes Cancer 2013, 4:378-387.
15. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
16. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000, 2:84-89.
17. Villarejo A., Cortes-Cabrera A., Molina-Ortiz P., Portillo F., Cano A. Differential role of Snail1 and Snail2 zinc fingers in E-cadherin repression and epithelial to mesenchymal transition. J. Biol. Chem. 2014, 289:930-941.
18. Lee M.S., Kim H.P., Kim T.Y., Lee J.W. Gefitinib resistance of cancer cells correlated with TM4SF5-mediated epithelial-mesenchymal transition. Biochim. Biophys. Acta 2012, 1823:514-523.
19. Kim B.G., An H.J., Kang S., Choi Y.P., Gao M.Q., Park H., Cho N.H. Laminin-332-rich tumor microenvironment for tumor invasion in the interface zone of breast cancer. Am. J. Pathol. 2011, 178:373-381.
20. Klemke R.L. Trespassing cancer cells: 'fingerprinting' invasive protrusions reveals metastatic culprits. Curr. Opin. Cell Biol. 2012, 24:662-669.
21. Kenny P.A., Lee G.Y., Myers C.A., Neve R.M., Semeiks J.R., Spellman P.T., Lorenz K., Lee E.H., Barcellos-Hoff M.H., Petersen O.W., Gray J.W., Bissell M.J. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol. Oncol. 2007, 1:84-96.
22. Hemavathy K., Ashraf S.I., Ip Y.T. Snail/slug family of repressors: slowly going into the fast lane of development and cancer. Gene 2000, 257:1-12.
23. Kim H., Kang M., Lee S.A., Kwak T.K., Jung O., Lee H.J., Kim S.H., Lee J.W. TM4SF5 accelerates G1/S phase progression via cytosolic p27(Kip1) expression and RhoA activity. Biochim. Biophys. Acta 2010, 1803:975-982.
24. Lundgren K., Nordenskjold B., Landberg G. Hypoxia, Snail and incomplete epithelial-mesenchymal transition in breast cancer. Br. J. Cancer 2009, 101:1769-1781.
25. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
26. Blanco M.J., Moreno-Bueno G., Sarrio D., Locascio A., Cano A., Palacios J., Nieto M.A. Correlation of snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 2002, 21:3241-3246.
27. Sou P.W., Delic N.C., Halliday G.M., Lyons J.G. Snail transcription factors in keratinocytes: enough to make your skin crawl. Int. J. Biochem. Cell Biol. 2010, 42:1940-1944.
28. Condeelis J., Segall J.E. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 2003, 3:921-930.
29. Giampieri S., Manning C., Hooper S., Jones L., Hill C.S., Sahai E. Localized and reversible TGFβ signalling switches breast cancer cells from cohesive to single cell motility. Nat. Cell Biol. 2009, 11:1287-1296.
30. Wu S., Kasisomayajula K., Peng J., Bancalari E. Inhibition of JNK enhances TGF-β1-activated Smad2 signaling in mouse embryonic lung. Pediatr. Res. 2009, 65:381-386.
31. Pessah M., Marais J., Prunier C., Ferrand N., Lallemand F., Mauviel A., Atfi A. c-Jun associates with the oncoprotein Ski and suppresses Smad2 transcriptional activity. J. Biol. Chem. 2002, 277:29094-29100.
32. Liu Q., Zhang Y., Mao H., Chen W., Luo N., Zhou Q., Yu X. A crosstalk between the Smad and JNK signaling in the TGF-β-induced epithelial-mesenchymal transition in rat peritoneal mesothelial cells. PLoS One 2012, 7:e32009.
33. Dennler S., Prunier C., Ferrand N., Gauthier J.M., Atfi A. c-Jun inhibits transforming growth factor β-mediated transcription by repressing Smad3 transcriptional activity. J. Biol. Chem. 2000, 275:28858-28865.
34. Ventura J.J., Kennedy N.J., Flavell R.A., Davis R.J. JNK regulates autocrine expression of TGF-beta1. Mol. Cell 2004, 15:269-278.
35. Olmeda D., Moreno-Bueno G., Flores J.M., Fabra A., Portillo F., Cano A. SNAI1 is required for tumor growth and lymph node metastasis of human breast carcinoma MDA-MB-231 cells. Cancer Res. 2007, 67:11721-11731.
36. Zhang K., Corsa C.A., Ponik S.M., Prior J.L., Piwnica-Worms D., Eliceiri K.W., Keely P.J., Longmore G.D. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat. Cell Biol. 2013, 15:677-687.
37. Shields M.A., Dangi-Garimella S., Krantz S.B., Bentrem D.J., Munshi H.G. Pancreatic cancer cells respond to type I collagen by inducing snail expression to promote membrane type 1 matrix metalloproteinase-dependent collagen invasion. J. Biol. Chem. 2011, 286:10495-10504.
38. Garcia de Herreros A., Baulida J. Cooperation, amplification, and feed-back in epithelial-mesenchymal transition. Biochim. Biophys. Acta 2012, 1825:223-228.
39. Chiang C., Ayyanathan K. Snail/Gfi-1 (SNAG) family zinc finger proteins in transcription regulation, chromatin dynamics, cell signaling, development, and disease. Cytokine Growth Factor Rev. 2013, 24:123-131.
40. Lu C., Sun X., Sun L., Sun J., Lu Y., Yu X., Zhou L., Gao X. Snail mediates PDGF-BB-induced invasion of rat bone marrow mesenchymal stem cells in 3D collagen and chick chorioallantoic membrane. J. Cell. Physiol. 2013, 228:1827-1833.
41. Ota I., Li X.Y., Hu Y., Weiss S.J. Induction of a MT1-MMP and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20318-20323.
42. Rowe R.G., Li X.Y., Hu Y., Saunders T.L., Virtanen I., Garcia de Herreros A., Becker K.F., Ingvarsen S., Engelholm L.H., Bommer G.T., Fearon E.R., Weiss S.J. Mesenchymal cells reactivate Snail1 expression to drive three-dimensional invasion programs. J. Cell Biol. 2009, 184:399-408.
43. Buday L., Downward J. Roles of cortactin in tumor pathogenesis. Biochim. Biophys. Acta 2007, 1775:263-273.
44. Weaver A.M., Heuser J.E., Karginov A.V., Lee W.L., Parsons J.T., Cooper J.A. Interaction of cortactin and N-WASp with Arp2/3 complex. Curr. Biol. 2002, 12:1270-1278.
45. Magalhaes M.A., Larson D.R., Mader C.C., Bravo-Cordero J.J., Gil-Henn H., Oser M., Chen X., Koleske A.J., Condeelis J. Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J. Cell Biol. 2011, 195:903-920.
46. Beaty B.T., Sharma V.P., Bravo-Cordero J.J., Simpson M.A., Eddy R.J., Koleske A.J., Condeelis J. β1 integrin regulates Arg to promote invadopodial maturation and matrix degradation. Mol. Biol. Cell 2013, 24:1661-1675. (S1661-1611).
47. Wolf K., Wu Y.I., Liu Y., Geiger J., Tam E., Overall C., Stack M.S., Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 2007, 9:893-904.
48. Tolde O., Rosel D., Vesely P., Folk P., Brabek J. The structure of invadopodia in a complex 3D environment. Eur. J. Cell Biol. 2010, 89:674-680.
49. Yu X., Machesky L.M. Cells assemble invadopodia-like structures and invade into matrigel in a matrix metalloprotease dependent manner in the circular invasion assay. PLoS One 2012, 7:e30605.
50. Vaskovicova K., Zarsky V., Rosel D., Nikolic M., Buccione R., Cvrckova F., Brabek J. Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life. Biol. Direct 2013, 8:8.
51. Yamaguchi H. Pathological roles of invadopodia in cancer invasion and metastasis. Eur. J. Cell Biol. 2012, 91:902-907.
52. Kovacs A., Dhillon J., Walker R.A. Expression of P-cadherin, but not E-cadherin or N-cadherin, relates to pathological and functional differentiation of breast carcinomas. Mol. Pathol. 2003, 56:318-322.