Cellular and molecular mechanisms controlling the migration of melanocytes and melanoma cells

Pigment Cell and Melanoma Research

Volumn 26, Issue 3, 2013, Pages 316-325

  Bonaventure, Jacky ^a,b   Domingues, Melanie J ^a,b   Larue, Lionel ^a,b  

^a INSTITUT CURIE   (France)

^b Centre National de la Recherche Scientifique   (France)

Author keywords

Blebs; Invadopodia; Melanoblast; Melanoma; Migration

Indexed keywords

CANCER CELL CULTURE; CELL LINEAGE; CELL MATURATION; CELL MIGRATION; CYTOGENETICS; GENE IDENTIFICATION; GENETIC ENGINEERING; IN VITRO STUDY; MELANOCYTE; MELANOMA CELL; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; TUMOR INVASION;

ANIMALS; CELL MOVEMENT; EMBRYONIC DEVELOPMENT; HUMANS; MELANOCYTES; MELANOMA; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS;

VERTEBRATA;

EID: 84876804339     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12080     Document Type: Review

References (80)

1. Abercrombie, M., Heaysman, J.E., and Pegrum, S.M. (1970). The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp. Cell Res. 59, 393-398.
2. Adameyko, I., Lallemend, F., Aquino, J.B. et al. (2009). Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139, 366-379.
3. Ahn, J., Sanz-Moreno, V., and Marshall, C.J. (2012). The metastasis gene NEDD9 product acts through integrin beta3 and Src to promote mesenchymal motility and inhibit amoeboid motility. J. Cell Sci. 125, 1814-1826.
4. Bailey, C.M., Morrison, J.A., and Kulesa, P.M. (2012). Melanoma revives an embryonic migration program to promote plasticity and invasion. Pigment Cell Melanoma Res. 25, 573-583.
5. Berlin, I., Denat, L., Steunou, A.L. et al. (2012). Phosphorylation of BRN2 modulates its interaction with the Pax3 promoter to control melanocyte migration and proliferation. Mol. Cell. Biol. 32, 1237-1247.
6. Boyle, G.M., Woods, S.L., Bonazzi, V.F., Stark, M.S., Hacker, E., Aoude, L.G., Dutton-Regester, K., Cook, A.L., Sturm, R.A., and Hayward, N.K. (2011). Melanoma cell invasiveness is regulated by miR-211 suppression of the BRN2 transcription factor. Pigment Cell Melanoma Res. 24, 525-537.
7. Buccione, R., Caldieri, G., and Ayala, I. (2009). Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Can. Metastasis Rev. 28, 137-149.
8. Carreira, S., Goodall, J., Denat, L., Rodriguez, M., Nuciforo, P., Hoek, K.S., Testori, A., Larue, L., and Goding, C.R. (2006). Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev. 20, 3426-3439.
9. Charras, G., and Paluch, E. (2008). Blebs lead the way: how to migrate without lamellipodia. Nature reviews. Mol. Cell. Biol. 9, 730-736.
10. Chen, W.T. (1989). Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 251, 167-185.
11. Chesarone, M.A., and Goode, B.L. (2009). Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28-37.
12. Chudnovsky, Y., Khavari, P.A., and Adams, A.E. (2005). Melanoma genetics and the development of rational therapeutics. J. Clin. Investig. 115, 813-824.
13. Clark, E.S., Whigham, A.S., Yarbrough, W.G., and Weaver, A.M. (2007). Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67, 4227-4235.
14. Colombo, S., Berlin, I., Delmas, V., and Larue, L. (2011). Classical and non-classical melanocytes in vertebrates. In Melanins and Melanosomes, P.A. Riley, and J. Borovansky, eds. (Weinheim: Wiley-VCH Verlag & Co), pp. 21-51.
15. Delmas, V., Beermann, F., Martinozzi, S. et al. (2007). Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev. 21, 2923-2935.
16. Deng, J., Liu, Y., Lee, H. et al. (2012). S1PR1-STAT3 signaling is crucial for myeloid cell colonization at future metastatic sites. Cancer Cell 21, 642-654.
17. Faix, J., and Rottner, K. (2006). The making of filopodia. Curr. Opin. Cell Biol. 18, 18-25.
18. Friedl, P., and Wolf, K. (2009). Proteolytic interstitial cell migration: a five-step process. Cancer Metastasis Rev. 28, 129-135.
19. Friedl, P., and Wolf, K. (2010). Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188, 11-19.
20. Gaggioli, C., and Sahai, E. (2007). Melanoma invasion - current knowledge and future directions. Pigment Cell Res. 20, 161-172.
21. Gallagher, S.J., Rambow, F., Kumasaka, M., Champeval, D., Bellacosa, A., Delmas, V., and Larue, L. (2012). Beta-catenin inhibits melanocyte migration but induces melanoma metastasis. Oncogene. doi: 10.1038/onc.2012.229.
22. Goodall, J., Martinozzi, S., Dexter, T.J., Champeval, D., Carreira, S., Larue, L., and Goding, C.R. (2004). Brn-2 expression controls melanoma proliferation and is directly regulated by beta-catenin. Mol. Cell. Biol. 24, 2915-2922.
23. Goodall, J., Carreira, S., Denat, L., Kobi, D., Davidson, I., Nuciforo, P., Sturm, R.A., Larue, L., and Goding, C.R. (2008). Brn-2 represses microphthalmia-associated transcription factor expression and marks a distinct subpopulation of microphthalmia-associated transcription factor-negative melanoma cells. Cancer Res. 68, 7788-7794.
24. Hamburger, V., and Hamilton, H.L. (1992). A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 195, 231-272.
25. Hegerfeldt, Y., Tusch, M., Brocker, E.B., and Friedl, P. (2002). Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, beta1-integrin function, and migration strategies. Cancer Res. 62, 2125-2130.
26. Hirata, M., Nakamura, K., and Kondo, S. (2005). Pigment cell distributions in different tissues of the zebrafish, with special reference to the striped pigment pattern. Dev. Dyn. 234, 293-300.
27. Hoek, K.S., Schlegel, N.C., Brafford, P. et al. (2006). Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res. 19, 290-302.
28. Jordan, S.A., and Jackson, I.J. (2000). A late wave of melanoblast differentiation and rostrocaudal migration revealed in patch and rump-white embryos. Mech. Dev. 92, 135-143.
29. Joyce, J.A., and Pollard, J.W. (2009). Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
30. Kelsh, R.N., Harris, M.L., Colanesi, S., and Erickson, C.A. (2009). Stripes and belly-spots - a review of pigment cell morphogenesis in vertebrates. Semin. Cell Dev. Biol. 20, 90-104.
31. Kim, M., Gans, J.D., Nogueira, C. et al. (2006). Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 125, 1269-1281.
32. Kirkbride, K.C., Sung, B.H., Sinha, S., and Weaver, A.M. (2011). Cortactin: a multifunctional regulator of cellular invasiveness. Cell Adh. Migr. 5, 187-198.
33. Kobi, D., Steunou, A.L., Dembele, D., Legras, S., Larue, L., Nieto, L., and Davidson, I. (2010). Genome-wide analysis of POU3F2/BRN2 promoter occupancy in human melanoma cells reveals Kitl as a novel regulated target gene. Pigment Cell Melanoma Res. 23, 404-418.
34. Krauthammer, M., Kong, Y., Ha, B.H. et al. (2012). Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat. Genet. 44, 1006-1014.
35. Lammermann, T., and Sixt, M. (2009). Mechanical modes of 'amoeboid' cell migration. Curr. Opin. Cell Biol. 21, 636-644.
36. Lamoreux, M.L., Delmas, V., Larue, L., and Bennett, D. (2010). The Colors of Mice: A Model Genetic Network. (Chichester: Wiley-Blackwell).
37. Larue, L., and Beermann, F. (2007). Cutaneous melanoma in genetically modified animals. Pigment Cell Res. 20, 485-497.
38. Larue, L., Kumasaka, M., and Goding, C.R. (2003). Beta-catenin in the melanocyte lineage. Pigment Cell Res. 16, 312-317.
39. Larue, L., De Vuyst, F., and Delmas, V. (2012). Modeling melanoblast development. Cell. Mol. Life Sci. 70, 1067-1079.
40. Lecoin, L., Sakurai, T., Ngo, M.T., Abe, Y., Yanagisawa, M., and Le Douarin, N.M. (1998). Cloning and characterization of a novel endothelin receptor subtype in the avian class. Proc. Natl Acad. Sci. USA 95, 3024-3029.
41. Lee, H.O., Levorse, J.M., and Shin, M.K. (2003). The endothelin receptor-B is required for the migration of neural crest-derived melanocyte and enteric neuron precursors. Dev. Biol. 259, 162-175.
42. Lee, H., Deng, J., Kujawski, M. et al. (2010). STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat. Med. 16, 1421-1428.
43. Li, A., and Machesky, L.M. (2012). Melanoblasts on the move: Rac1 sets the pace. Small GTPases 3, 115-119.
44. Li, A., Dawson, J.C., Forero-Vargas, M., Spence, H.J., Yu, X., Konig, I., Anderson, K., and Machesky, L.M. (2010). The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr. Biol. 20, 339-345.
45. Li, A., Ma, Y., Yu, X. et al. (2011). Rac1 drives melanoblast organization during mouse development by orchestrating pseudopod- driven motility and cell-cycle progression. Dev. Cell 21, 722-734.
46. Lindsay, C.R., Lawn, S., Campbell, A.D. et al. (2011). P-Rex1 is required for efficient melanoblast migration and melanoma metastasis. Nat. Commun. 2, 555.
47. Luciani, F., Champeval, D., Herbette, A. et al. (2011). Biological and mathematical modeling of melanocyte development. Development 138, 3943-3954.
48. Machesky, L.M. (2008). Lamellipodia and filopodia in metastasis and invasion. FEBS Lett. 582, 2102-2111.
49. McGill, G.G., Haq, R., Nishimura, E.K., and Fisher, D.E. (2006). c-Met expression is regulated by Mitf in the melanocyte lineage. J. Biol. Chem. 281, 10365-10373.
50. Mort, R.L., Hay, L., and Jackson, I.J. (2010). Ex vivo live imaging of melanoblast migration in embryonic mouse skin. Pigment Cell Melanoma Res. 23, 299-301.
51. Muralidharan-Chari, V., Hoover, H., Clancy, J., Schweitzer, J., Suckow, M.A., Schroeder, V., Castellino, F.J., Schorey, J.S., and D'souza-Schorey, C. (2009). ADP-ribosylation factor 6 regulates tumorigenic and invasive properties in vivo. Cancer Res. 69, 2201-2209.
52. Oser, M., and Condeelis, J. (2009). The cofilin activity cycle in lamellipodia and invadopodia. J. Cell. Biochem. 108, 1252-1262.
53. Parichy, D.M., Rawls, J.F., Pratt, S.J., Whitfield, T.T., and Johnson, S.L. (1999). Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development 126, 3425-3436.
54. Petrie, R.J., Gavara, N., Chadwick, R.S., and Yamada, K.M. (2012). Nonpolarized signaling reveals two distinct modes of 3D cell migration. J. Cell Biol. 197, 439-455.
55. Pichot, C.S., Arvanitis, C., Hartig, S.M., Jensen, S.A., Bechill, J., Marzouk, S., Yu, J., Frost, J.A., and Corey, S.J. (2010). Cdc42-interacting protein 4 promotes breast cancer cell invasion and formation of invadopodia through activation of N-WASp. Cancer Res. 70, 8347-8356.
56. Pinner, S., Jordan, P., Sharrock, K., Bazley, L., Collinson, L., Marais, R., Bonvin, E., Goding, C., and Sahai, E. (2009). Intravital imaging reveals transient changes in pigment production and Brn2 expression during metastatic melanoma dissemination. Cancer Res. 69, 7969-7977.
57. Pla, P., and Larue, L. (2003). Involvement of endothelin receptors in normal and pathological development of neural crest cells. Int. J. Dev. Biol. 47, 315-325.
58. Pla, P., Alberti, C., Solov'eva, O., Pasdar, M., Kunisada, T., and Larue, L. (2005). Ednrb2 orients cell migration towards the dorsolateral neural crest pathway and promotes melanocyte differentiation. Pigment Cell Res. 18, 181-187.
59. Poincloux, R., Lizarraga, F., and Chavrier, P. (2009). Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122, 3015-3024.
60. Raftopoulou, M., and Hall, A. (2004). Cell migration: rho GTPases lead the way. Dev. Biol. 265, 23-32.
61. Rawls, J.F., and Johnson, S.L. (2003). Temporal and molecular separation of the kit receptor tyrosine kinase's roles in zebrafish melanocyte migration and survival. Dev. Biol. 262, 152-161.
62. Reid, K., Turnley, A.M., Maxwell, G.D., Kurihara, Y., Kurihara, H., Bartlett, P.F., and Murphy, M. (1996). Multiple roles for endothelin in melanocyte development: regulation of progenitor number and stimulation of differentiation. Development 122, 3911-3919.
63. Ridley, A.J. (2011). Life at the leading edge. Cell 145, 1012-1022.
64. Sabeh, F., Shimizu-Hirota, R., and Weiss, S.J. (2009). Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185, 11-19.
65. Sahai, E., and Marshall, C.J. (2003). Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5, 711-719.
66. Sanchez-Martin, M., Rodriguez-Garcia, A., Perez-Losada, J., Sagrera, A., Read, A.P., and Sanchez-Garcia, I. (2002). SLUG (SNAI2) deletions in patients with Waardenburg disease. Hum. Mol. Genet. 11, 3231-3236.
67. Santiago, A., and Erickson, C.A. (2002). Ephrin-B ligands play a dual role in the control of neural crest cell migration. Development 129, 3621-3632.
68. Sanz-Moreno, V., and Marshall, C.J. (2010). The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr. Opin. Cell Biol. 22, 690-696.
69. Sanz-Moreno, V., Gadea, G., Ahn, J., Paterson, H., Marra, P., Pinner, S., Sahai, E., and Marshall, C.J. (2008). Rac activation and inactivation control plasticity of tumor cell movement. Cell 135, 510-523.
70. Schoumacher, M., Goldman, R.D., Louvard, D., and Vignjevic, D.M. (2010). Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 189, 541-556.
71. Schouwey, K., Delmas, V., Larue, L., Zimber-Strobl, U., Strobl, L.J., Radtke, F., and Beermann, F. (2007). Notch1 and Notch2 receptors influence progressive hair graying in a dose-dependent manner. Dev. Dyn. 236, 282-289.
72. Shackleton, M., and Quintana, E. (2010). Progress in understanding melanoma propagation. Mol. Oncol. 4, 451-457.
73. Sixt, M. (2012). Cell migration: fibroblasts find a new way to get ahead. J. Cell Biol. 197, 347-349.
74. Spiering, D., and Hodgson, L. (2011). Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh. Migr. 5, 170-180.
75. Theveneau, E., Marchant, L., Kuriyama, S., Gull, M., Moepps, B., Parsons, M., and Mayor, R. (2010). Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell 19, 39-53.
76. Tsao, H., Chin, L., Garraway, L.A., and Fisher, D.E. (2012). Melanoma: from mutations to medicine. Genes Dev. 26, 1131-1155.
77. Virchow, R.L.K. (1859). Cellular Pathology. (London: John Churchill).
78. Wellbrock, C., Rana, S., Paterson, H., Pickersgill, H., Brummelkamp, T., and Marais, R. (2008). Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS ONE 3, e2734.
79. Whiteman, D.C., Pavan, W.J., and Bastian, B.C. (2011). The melanomas: a synthesis of epidemiological, clinical, histopathological, genetic, and biological aspects, supporting distinct subtypes, causal pathways, and cells of origin. Pigment Cell Melanoma Res. 24, 879-897.
80. Yoshida, K., and Soldati, T. (2006). Dissection of amoeboid movement into two mechanically distinct modes. J. Cell Sci. 119, 3833-3844.