TGF-β-Induced Transcription Sustains Amoeboid Melanoma Migration and Dissemination

Current Biology

Volumn 25, Issue 22, 2015, Pages 2899-2914

  Cantelli, Gaia ^a   Orgaz, Jose L ^a   Rodriguez Hernandez, Irene ^a   Karagiannis, Panagiotis ^b,c   Maiques, Oscar ^d   Matias Guiu, Xavier ^d   Nestle, Frank O ^b   Marti, Rosa M ^d   Karagiannis, Sophia N ^b   Sanz Moreno, Victoria ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b ST THOMAS HOSPITAL   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d HOSPITAL UNIVERSITARI ARNAU DE VILANOVA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CITED1 PROTEIN, HUMAN; MYOSIN ADENOSINE TRIPHOSPHATASE; NUCLEAR PROTEIN; SMAD2 PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; CELL MOTION; CELL SHAPE; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; HUMAN; KERATINOCYTE; MELANOCYTE; MELANOMA; METABOLISM; METASTASIS; MOUSE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TRANSCRIPTION INITIATION; TUMOR CELL LINE; UPREGULATION;

ACTOMYOSIN; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; KERATINOCYTES; MELANOCYTES; MELANOMA; MICE; MICE, NUDE; NEOPLASM METASTASIS; NUCLEAR PROTEINS; SMAD2 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84960811071     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2015.09.054     Document Type: Article

References (48)

1. J.P. Thiery Epithelial-mesenchymal transitions in tumour progression Nat. Rev. Cancer 2 2002 442 454
2. S. Giampieri, C. Manning, S. Hooper, L. Jones, C.S. Hill, and E. Sahai Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility Nat. Cell Biol. 11 2009 1287 1296
3. A. Bruna, R.S. Darken, F. Rojo, A. Ocaña, S. Peñuelas, A. Arias, R. Paris, A. Tortosa, J. Mora, J. Baselga, and J. Seoane High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene Cancer Cell 11 2007 147 160
4. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, M. Shipitsin, and et al. The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
5. D.A. Thomas, and J. Massagué TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance Cancer Cell 8 2005 369 380
6. A. Nakao, T. Imamura, S. Souchelnytskyi, M. Kawabata, A. Ishisaki, E. Oeda, K. Tamaki, J. Hanai, C.H. Heldin, K. Miyazono, and P. ten Dijke TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4 EMBO J. 16 1997 5353 5362
7. S. Abdollah, M. Macías-Silva, T. Tsukazaki, H. Hayashi, L. Attisano, and J.L. Wrana TbetaRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling J. Biol. Chem. 272 1997 27678 27685
8. J. Massagué TGFβ signalling in context Nat. Rev. Mol. Cell Biol. 13 2012 616 630
9. T. Shioda, M.H. Fenner, and K.J. Isselbacher msg1, a novel melanocyte-specific gene, encodes a nuclear protein and is associated with pigmentation Proc. Natl. Acad. Sci. USA 93 1996 12298 12303
10. T. Yahata, M.P. de Caestecker, R.J. Lechleider, S. Andriole, A.B. Roberts, K.J. Isselbacher, and T. Shioda The MSG1 non-DNA-binding transactivator binds to the p300/CBP coactivators, enhancing their functional link to the Smad transcription factors J. Biol. Chem. 275 2000 8825 8834
11. A.J. Murphy, C. de Caestecker, J. Pierce, S.C. Boyle, G.D. Ayers, Z. Zhao, J.M. Libes, H. Correa, T. Walter, S.S. Huppert, and et al. CITED1 expression in liver development and hepatoblastoma Neoplasia 14 2012 1153 1163
12. A.J. Murphy, J. Pierce, C. de Caestecker, G.D. Ayers, A. Zhao, J.R. Krebs, V.K. Saito-Diaz, E. Lee, A.O. Perantoni, M.P. de Caestecker, and H.N. Lovvorn 3rd CITED1 confers stemness to Wilms tumor and enhances tumorigenic responses when enriched in the nucleus Oncotarget 5 2014 386 402
13. A.J. Murphy, J. Pierce, C. de Caestecker, C. Taylor, J.R. Anderson, A.O. Perantoni, M.P. de Caestecker, and H.N. Lovvorn 3rd SIX2 and CITED1, markers of nephronic progenitor self-renewal, remain active in primitive elements of Wilms' tumor J. Pediatr. Surg. 47 2012 1239 1249
14. J. McBryan, J. Howlin, P.A. Kenny, T. Shioda, and F. Martin ERalpha-CITED1 co-regulated genes expressed during pubertal mammary gland development: implications for breast cancer prognosis Oncogene 26 2007 6406 6419
15. M. Sassa, Y. Hayashi, R. Watanabe, T. Kikumori, T. Imai, J. Kurebayashi, T. Kiuchi, and Y. Murata Aberrant promoter methylation in overexpression of CITED1 in papillary thyroid cancer Thyroid 21 2011 511 517
16. J. Caramel, E. Papadogeorgakis, L. Hill, G.J. Browne, G. Richard, A. Wierinckx, G. Saldanha, J. Osborne, P. Hutchinson, G. Tse, and et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma Cancer Cell 24 2013 466 480
17. R.W. Keane, L.A. Lipsich, and J.S. Brugge Differentiation and transformation of neural plate cells Dev. Biol. 103 1984 38 52
18. P.M. Kulesa, J.C. Kasemeier-Kulesa, J.M. Teddy, N.V. Margaryan, E.A. Seftor, R.E. Seftor, and M.J. Hendrix Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment Proc. Natl. Acad. Sci. USA 103 2006 3752 3757
19. V. Sanz-Moreno, G. Gadea, J. Ahn, H. Paterson, P. Marra, S. Pinner, E. Sahai, and C.J. Marshall Rac activation and inactivation control plasticity of tumor cell movement Cell 135 2008 510 523
20. J.L. Orgaz, and V. Sanz-Moreno Emerging molecular targets in melanoma invasion and metastasis Pigment Cell Melanoma Res. 26 2013 39 57
21. A. Lorentzen, J. Bamber, A. Sadok, I. Elson-Schwab, and C.J. Marshall An ezrin-rich, rigid uropod-like structure directs movement of amoeboid blebbing cells J. Cell Sci. 124 2011 1256 1267
22. V. Ruprecht, S. Wieser, A. Callan-Jones, M. Smutny, H. Morita, K. Sako, V. Barone, M. Ritsch-Marte, M. Sixt, R. Voituriez, and C.P. Heisenberg Cortical contractility triggers a stochastic switch to fast amoeboid cell motility Cell 160 2015 673 685
23. Y.J. Liu, M. Le Berre, F. Lautenschlaeger, P. Maiuri, A. Callan-Jones, M. Heuzé, T. Takaki, R. Voituriez, and M. Piel Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells Cell 160 2015 659 672
24. E. Sahai, and C.J. Marshall Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis Nat. Cell Biol. 5 2003 711 719
25. J.L. Orgaz, P. Pandya, R. Dalmeida, P. Karagiannis, B. Sanchez-Laorden, A. Viros, J. Albrengues, F.O. Nestle, A.J. Ridley, C. Gaggioli, and et al. Diverse matrix metalloproteinase functions regulate cancer amoeboid migration Nat. Commun. 5 2014 4255
26. V. Sanz-Moreno, C. Gaggioli, M. Yeo, J. Albrengues, F. Wallberg, A. Viros, S. Hooper, R. Mitter, C.C. Féral, M. Cook, and et al. ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma Cancer Cell 20 2011 229 245
27. M. Tozluoʇlu, A.L. Tournier, R.P. Jenkins, S. Hooper, P.A. Bates, and E. Sahai Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions Nat. Cell Biol. 15 2013 751 762
28. S.W. Tobin, K. Douville, U. Benbow, C.E. Brinckerhoff, V.A. Memoli, and B.A. Arrick Consequences of altered TGF-beta expression and responsiveness in breast cancer: evidence for autocrine and paracrine effects Oncogene 21 2002 108 118
29. N.A. Bhowmick, A. Chytil, D. Plieth, A.E. Gorska, N. Dumont, S. Shappell, M.K. Washington, E.G. Neilson, and H.L. Moses TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia Science 303 2004 848 851
30. M. Adorno, M. Cordenonsi, M. Montagner, S. Dupont, C. Wong, B. Hann, A. Solari, S. Bobisse, M.B. Rondina, V. Guzzardo, and et al. A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis Cell 137 2009 87 98
31. M.J. Goumans, G. Valdimarsdottir, S. Itoh, F. Lebrin, J. Larsson, C. Mummery, S. Karlsson, and P. ten Dijke Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling Mol. Cell 12 2003 817 828
32. F. Liu, A. Hata, J.C. Baker, J. Doody, J. Cárcamo, R.M. Harland, and J. Massagué A human Mad protein acting as a BMP-regulated transcriptional activator Nature 381 1996 620 623
33. J. Howlin, J. McBryan, S. Napoletano, T. Lambe, E. McArdle, T. Shioda, and F. Martin CITED1 homozygous null mice display aberrant pubertal mammary ductal morphogenesis Oncogene 25 2006 1532 1542
34. Z. Lin, R. Feng, J. Li, Y. Meng, L. Yuan, Z. Fu, J. Guo, F.R. Bringhurst, and D. Yang Nuclear translocation of CBP/p300-interacting protein CITED1 induced by parathyroid hormone requires serine phosphorylation at position 79 in its 63-84 domain Cell. Signal. 26 2014 2436 2445
35. N.J. Laping, E. Grygielko, A. Mathur, S. Butter, J. Bomberger, C. Tweed, W. Martin, J. Fornwald, R. Lehr, J. Harling, and et al. Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542 Mol. Pharmacol. 62 2002 58 64
36. R.Y. Bai, C. Koester, T. Ouyang, S.A. Hahn, M. Hammerschmidt, C. Peschel, and J. Duyster SMIF, a Smad4-interacting protein that functions as a co-activator in TGFbeta signalling Nat. Cell Biol. 4 2002 181 190
37. N. Reymond, B.B. d'Água, and A.J. Ridley Crossing the endothelial barrier during metastasis Nat. Rev. Cancer 13 2013 858 870
38. J. Zavadil, and E.P. Böttinger TGF-beta and epithelial-to-mesenchymal transitions Oncogene 24 2005 5764 5774
39. R. Derynck, and R.J. Akhurst Differentiation plasticity regulated by TGF-beta family proteins in development and disease Nat. Cell Biol. 9 2007 1000 1004
40. Y. Kang, W. He, S. Tulley, G.P. Gupta, I. Serganova, C.R. Chen, K. Manova-Todorova, R. Blasberg, W.L. Gerald, and J. Massagué Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway Proc. Natl. Acad. Sci. USA 102 2005 13909 13914
41. E.A. Clark, T.R. Golub, E.S. Lander, and R.O. Hynes Genomic analysis of metastasis reveals an essential role for RhoC Nature 406 2000 532 535
42. A. Sadok, and C.J. Marshall Rho GTPases: masters of cell migration Small GTPases 5 2014 e29710
43. T.R. Gershon, O. Oppenheimer, S.S. Chin, and W.L. Gerald Temporally regulated neural crest transcription factors distinguish neuroectodermal tumors of varying malignancy and differentiation Neoplasia 7 2005 575 584
44. N.M. Shah, A.K. Groves, and D.J. Anderson Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members Cell 85 1996 331 343
45. R. Watanabe, Y. Hayashi, M. Sassa, T. Kikumori, T. Imai, T. Kiuchi, and Y. Murata Possible involvement of BRAFV600E in altered gene expression in papillary thyroid cancer Endocr. J. 56 2009 407 414
46. H. Blaser, M. Reichman-Fried, I. Castanon, K. Dumstrei, F.L. Marlow, K. Kawakami, L. Solnica-Krezel, C.P. Heisenberg, and E. Raz Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow Dev. Cell 11 2006 613 627
47. J. Jacobelli, R.S. Friedman, M.A. Conti, A.M. Lennon-Dumenil, M. Piel, C.M. Sorensen, R.S. Adelstein, and M.F. Krummel Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions Nat. Immunol. 11 2010 953 961
48. C.M. Balch, J.E. Gershenwald, S.J. Soong, J.F. Thompson, M.B. Atkins, D.R. Byrd, A.C. Buzaid, A.J. Cochran, D.G. Coit, S. Ding, and et al. Final version of 2009 AJCC melanoma staging and classification J. Clin. Oncol. 27 2009 6199 6206