Cellular migration and invasion uncoupled: Increased migration is not an inexorable consequence of epithelial-to-mesenchymal transition

Molecular and Cellular Biology

Volumn 34, Issue 18, 2014, Pages 3486-3499

  Schaeffer, Daneen ^a   Somarelli, Jason A ^a   Hanna, Gabi ^a   Palmer, Gregory M ^a   Garcia Blanco, Mariano A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 4; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; SMOOTH MUSCLE ACTIN; UVOMORULIN; VIMENTIN;

ANIMAL CELL; ARTICLE; BREAST EPITHELIUM; CARCINOGENICITY; CASTRATED MALE; CELL ADHESION; CELL CONTACT; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SPREADING; CELL SUSPENSION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; RAT; TISSUE CULTURE;

ANIMALS; CELL ADHESION; CELL LINE; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMANS; MALE; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84906052542     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00694-14     Document Type: Article

References (63)

1. Chambers AF, Naumov GN, Varghese HJ, Nadkarni KV, MacDonald IC, Groom AC. 2001. Critical steps in hematogenous metastasis: an overview. Surg. Oncol. Clin. N. Am. 10:243-255, vii.
2. Folkman J. 1992. The role of angiogenesis in tumor growth. Semin. Cancer Biol. 3:65-71.
3. Fidler IJ. 1999. Critical determinants of cancer metastasis: rationale for therapy. Cancer Chemother. Pharmacol. 43(Suppl):S3-S10.
4. Woodhouse EC, Chuaqui RF, Liotta LA. 1997. General mechanisms of metastasis. Cancer 80:1529-1537.
5. Polyak K, Weinberg RA. 2009. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9:265-273. http://dx.doi.org/10.1038/nrc2620.
6. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA. 2009. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J. Clin. Invest. 119:1438-1449. http: //dx.doi.org/10.1172/JCI38019.
7. Nakamura M, Tokura Y. 2011. Epithelial-mesenchymal transition in the skin. J. Dermatol. Sci. 61:7-13. http://dx.doi.org/10.1016/j.jdermsci.2010 .11.015.
8. De Craene B, Berx G. 2013. Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer. 13:97-110. http://dx .doi.org/10.1038/nrc3447.
9. Kalluri R, Weinberg RA. 2009. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119:1420-1428. http://dx.doi.org/10.1172 /JCI39104.
10. Tiwari N, Gheldof A, Tatari M, Christofori G. 2012. EMT as the ultimate survival mechanism of cancer cells. Semin. Cancer Biol. 22:194-207. http: //dx.doi.org/10.1016/j.semcancer.2012.02.013.
11. Horwitz R, Webb D. 2003. Cell migration. Curr. Biol. 13:R756-R759. http://dx.doi.org/10.1016/j.cub.2003.09.014.
12. Friedl P, Wolf K. 2010. Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188:11-19. http://dx.doi.org/10.1083/jcb.200909003.
13. Kedrin D, van Rheenen J, Hernandez L, Condeelis J, Segall JE. 2007. Cell motility and cytoskeletal regulation in invasion and metastasis. J. Mammary Gland Biol. Neoplasia 12:143-152. http://dx.doi.org/10.1007 /s10911-007-9046-4.
14. Friedl P, Gilmour D. 2009. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10:445-457. http://dx .doi.org/10.1038/nrm2720.
15. Kwok WK, Ling MT, Lee TW, Lau TC, Zhou C, Zhang X, Chua CW, Chan KW, Chan FL, Glackin C, Wong YC, Wang X. 2005. Upregulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res. 65:5153-5162. http://dx.doi.org/10.1158/0008-5472 .CAN-04-3785.
16. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH. 2007. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res. 67: 1979-1987. http://dx.doi.org/10.1158/0008-5472.CAN-06-1479.
17. Yang Z, Zhang X, Gang H, Li X, Li Z, Wang T, Han J, Luo T, Wen F, Wu X. 2007. Up-regulation of gastric cancer cell invasion by Twist is accompanied by N-cadherin and fibronectin expression. Biochem. Biophys. Res. Commun. 358:925-930. http://dx.doi.org/10.1016/j.bbrc.2007 .05.023.
18. Matsuo N, Shiraha H, Fujikawa T, Takaoka N, Ueda N, Tanaka S, Nishina S, Nakanishi Y, Uemura M, Takaki A, Nakamura S, Kobayashi Y, Nouso K, Yagi T, Yamamoto K. 2009. Twist expression promotes migration and invasion in hepatocellular carcinoma. BMC Cancer 9:240. http://dx.doi.org/10.1186/1471-2407-9-240.
19. Shiota M, Yokomizo A, Itsumi M, Uchiumi T, Tada Y, Song Y, Kashiwagi E, Masubuchi D, Naito S. 2011. Twist1 and Y-box-binding protein-1 promote malignant potential in bladder cancer cells. BJU Int. 108:E142-E149. http://dx.doi.org/10.1111/j.1464-410X.2010.09810.x.
20. Nakashima H, Hashimoto N, Aoyama D, Kohnoh T, Sakamoto K, Kusunose M, Imaizumi K, Takeyama Y, Sato M, Kawabe T, Hasegawa Y. 2012. Involvement of the transcription factor twist in phenotype alteration through epithelial-mesenchymal transition in lung cancer cells. Mol. Carcinog. 51:400-410. http://dx.doi.org/10.1002/mc.20802.
21. Bussemakers MJ, van Bokhoven A, Mees SG, Kemler R, Schalken JA. 1993. Molecular cloning and characterization of the human E-cadherin cDNA. Mol. Biol. Rep. 17:123-128. http://dx.doi.org/10.1007/BF00996219.
22. Vesuna F, van Diest P, Chen JH, Raman V. 2008. Twist is a transcriptional repressor of E-cadherin gene expression in breast cancer. Biochem. Biophys. Res. Commun. 367:235-241. http://dx.doi.org/10.1016/j.bbrc .2007.11.151.
23. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927-939. http://dx.doi.org/10.1016/j.cell.2004.06.006.
24. Wang W, Goswami S, Lapidus K, Wells AL, Wyckoff JB, Sahai E, Singer RH, Segall JE, Condeelis JS. 2004. Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res. 64:8585-8594. http://dx.doi.org/10.1158/0008 -5472.CAN-04-1136.
25. Shapiro IM, Cheng AW, Flytzanis NC, Balsamo M, Condeelis JS, Oktay MH, Burge CB, Gertler FB. 2011. An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype. PLoS Genet. 7:e1002218. http://dx.doi.org/10.1371/journal.pgen .1002218.
26. Kim HD, Meyer AS, Wagner JP, Alford SK, Wells A, Gertler FB, Lauffenburger DA. 2011. Signaling network state predicts twist-mediated effects on breast cell migration across diverse growth factor contexts. Mol. Cell. Proteomics 10:M111.008433. http://dx.doi.org/10.1074/mcp.M111 .008433.
27. Somarelli JA, Schaeffer D, Bosma R, Bonano VI, Sohn JW, Kemeny G, Ettyreddy A, Garcia-Blanco MA. 2013. Fluorescence-based alternative splicing reporters for the study of epithelial plasticity in vivo. RNA 19:116- 127. http://dx.doi.org/10.1261/rna.035097.112.
28. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, Popescu NC, Hahn WC, Weinberg RA. 2001. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 15:50-65. http://dx.doi.org/10.1101/gad.828901.
29. Takeichi M. 1977. Functional correlation between cell adhesive properties and some cell surface proteins. J. Cell Biol. 75:464-474. http://dx.doi.org /10.1083/jcb.75.2.464.
30. Oltean S, Sorg BS, Albrecht T, Bonano VI, Brazas RM, Dewhirst MW, Garcia-Blanco MA. 2006. Alternative inclusion of fibroblast growth factor receptor 2 exon IIIc in Dunning prostate tumors reveals unexpected epithelial mesenchymal plasticity. Proc. Natl. Acad. Sci. U. S. A. 103:14116- 14121. http://dx.doi.org/10.1073/pnas.0603090103.
31. Palmer GM, Fontanella AN, Shan S, Hanna G, Zhang G, Fraser CL, Dewhirst MW. 2011. In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters. Nat. Protoc. 6:1355-1366. http://dx.doi .org/10.1038/nprot.2011.349.
32. Bonano VI, Oltean S, Garcia-Blanco MA. 2007. A protocol for imaging alternative splicing regulation in vivo using fluorescence reporters in transgenic mice. Nat. Protoc. 2:2166-2181. http://dx.doi.org/10.1038 /nprot.2007.292.
33. Wagner EJ, Carstens RP, Garcia-Blanco MA. 1999. A novel isoform ratio switch of the polypyrimidine tract binding protein. Electrophoresis 20: 1082-1086. http://dx.doi.org/10.1002/(SICI)1522-2683(19990101)20:4 /5<1082::AID-ELPS1082>3.0.CO;2-#.
34. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA, Mani SA. 2010. Core epithelialto- mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc. Natl. Acad. Sci. U. S. A. 107:15449-15454. http://dx.doi.org/10.1073/pnas .1004900107.
35. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545-15550. http://dx.doi.org/10.1073/pnas.0506580102.
36. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelialmesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7:131-142. http://dx .doi.org/10.1038/nrm1835.
37. Feng S, Wang F, Matsubara A, Kan M, McKeehan WL. 1997. Fibroblast growth factor receptor 2 limits and receptor 1 accelerates tumorigenicity of prostate epithelial cells. Cancer Res. 57:5369-5378.
38. Yan G, Fukabori Y, McBride G, Nikolaropolous S, McKeehan WL. 1993. Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol. Cell. Biol. 13: 4513-4522.
39. Dunning WF. 1963. Prostate cancer in the rat. Natl. Cancer Inst. Monogr. 12:351-369.
40. Landstrom M, Damber JE, Bergh A. 1994. Prostatic tumor regrowth after initially successful castration therapy may be related to a decreased apoptotic cell death rate. Cancer Res. 54:4281-4284.
41. Lubaroff DM, Canfield L, Reynolds CW. 1980. The Dunning tumors. Prog. Clin. Biol. Res. 37:243-263.
42. McGrath JL. 2007. Cell spreading: the power to simplify. Curr. Biol. 17:R357-R358. http://dx.doi.org/10.1016/j.cub.2007.03.057.
43. Wu X, Jin C, Wang F, Yu C, McKeehan WL. 2003. Stromal cell heterogeneity in fibroblast growth factor-mediated stromal-epithelial cell cross-talk in premalignant prostate tumors. Cancer Res. 63:4936-4944.
44. Tennant TR, Kim H, Sokoloff M, Rinker-Schaeffer CW. 2000. The Dunning model. Prostate 43:295-302. http://dx.doi.org/10.1002/1097 -0045(20000601)43:4<295::AID-PROS9>.0.CO;2-W.
45. Oltean S, Febbo PG, Garcia-Blanco MA. 2008. Dunning rat prostate adenocarcinomas and alternative splicing reporters: powerful tools to study epithelial plasticity in prostate tumors in vivo. Clin. Exp. Metastasis 25:611-619. http://dx.doi.org/10.1007/s10585-008-9186-y.
46. Kolachala VL, Bajaj R, Wang L, Yan Y, Ritzenthaler JD, Gewirtz AT, Roman J, Merlin D, Sitaraman SV. 2007. Epithelial-derived fibronectin expression, signaling, and function in intestinal inflammation. J. Biol. Chem. 282:32965-32973. http://dx.doi.org/10.1074/jbc.M704388200.
47. Quaroni A, Isselbacher KJ, Ruoslahti E. 1978. Fibronectin synthesis by epithelial crypt cells of rat small intestine. Proc. Natl. Acad. Sci. U. S. A. 75:5548-5552. http://dx.doi.org/10.1073/pnas.75.11.5548.
48. Taylor-Papadimitriou J, Burchell J, Hurst J. 1981. Production of fibronectin by normal and malignant human mammary epithelial cells. Cancer Res. 41:2491-2500.
49. Chen P, Gupta K, Wells A. 1994. Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from mitogenesis. J. Cell Biol. 124:547-555. http://dx.doi.org /10.1083/jcb.124.4.547.
50. Xie H, Pallero MA, Gupta K, Chang P, Ware MF, Witke W, Kwiatkowski DJ, Lauffenburger DA, Murphy-Ullrich JE, Wells A. 1998. EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCgamma signaling pathway. J. Cell Sci. 111(Part 5):615-624.
51. Chen P, Xie H, Wells A. 1996. Mitogenic signaling from the EGF receptor is attenuated by a phospholipase C-gamma/protein kinase C feedback mechanism. Mol. Biol. Cell 7:871-881. http://dx.doi.org/10.1091/mbc.7 .6.871.
52. Vitorino P, Meyer T. 2008. Modular control of endothelial sheet migration. Genes Dev. 22:3268-3281. http://dx.doi.org/10.1101/gad.1725808.
53. Armstrong AJ, Marengo MS, Oltean S, Kemeny G, Bitting RL, Turnbull JD, Herold CI, Marcom PK, George DJ, Garcia-Blanco MA. 2011. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol. Cancer Res. 9:997-1007. http://dx.doi.org/10.1158/1541-7786.MCR-10-0490.
54. Tomita K, van Bokhoven A, van Leenders GJ, Ruijter ET, Jansen CF, Bussemakers MJ, Schalken JA. 2000. Cadherin switching in human prostate cancer progression. Cancer Res. 60:3650-3654.
55. Theveneau E, Mayor R. 2012. Cadherins in collective cell migration of mesenchymal cells. Curr. Opin. Cell Biol. 24:677-684. http://dx.doi.org /10.1016/j.ceb.2012.08.002.
56. Zieske JD, Takahashi H, Hutcheon AE, Dalbone AC. 2000. Activation of epidermal growth factor receptor during corneal epithelial migration. Invest. Ophthalmol. Vis. Sci. 41:1346-1355.
57. Polk DB. 1998. Epidermal growth factor receptor-stimulated intestinal epithelial cell migration requires phospholipase C activity. Gastroenterology 114:493-502. http://dx.doi.org/10.1016/S0016-5085(98)70532-3.
58. Lauand C, Rezende-Teixeira P, Cortez BA, Niero EL, Machado-Santelli GM. 2013. Independent of ErbB1 gene copy number, EGF stimulates migration but is not associated with cell proliferation in non-small cell lung cancer. Cancer Cell Int. 13:38. http://dx.doi.org/10.1186/1475-2867 -13-38.
59. Keren K, Pincus Z, Allen GM, Barnhart EL, Marriott G, Mogilner A, Theriot JA. 2008. Mechanism of shape determination in motile cells. Nature 453:475-480. http://dx.doi.org/10.1038/nature06952.
60. Friedl P, Zanker KS, Brocker EB. 1998. Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech. 43:369-378. http://dx.doi.org/10.1002 /(SICI)1097-0029(19981201)43:5<369::AID-JEMT3>3.0.CO;2-6.
61. Pankova K, Rosel D, Novotny M, Brabek J. 2010. The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell. Mol. Life Sci. 67:63-71. http://dx.doi.org/10.1007 /s00018-009-0132-1.
62. Lou Y, Preobrazhenska O, auf dem Keller U, Sutcliffe M, Barclay L, McDonald PC, Roskelley C, Overall CM, Dedhar S. 2008. Epithelialmesenchymal transition (EMT) is not sufficient for spontaneous murine breast cancer metastasis. Dev. Dyn. 237:2755-2768. http://dx.doi.org/10 .1002/dvdy.21658.
63. Dykxhoorn DM, Wu Y, Xie H, Yu F, Lal A, Petrocca F, Martinvalet D, Song E, Lim B, Lieberman J. 2009. miR-200 enhances mouse breast cancer cell colonization to form distant metastases. PLoS One 4:e7181. http://dx.doi.org/10.1371/journal.pone.0007181.