PAX3 and FOXD3 promote CXCR4 expression in melanoma

Journal of Biological Chemistry

Volumn 290, Issue 36, 2015, Pages 21901-21914

  Kubic, Jennifer D ^a   Lui, Jason W ^a   Little, Elizabeth C ^a   Ludvik, Anton E ^a   Konda, Sasank ^a   Salgia, Ravi ^a   Aplin, Andrew E ^b   Lang, Deborah ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOLOGY;

CELL MIGRATION; MELANOMA CELLS; MELANOMA METASTASIS; THERAPEUTIC STRATEGY;

DERMATOLOGY;

CHEMOKINE RECEPTOR CXCR4; FORKHEAD BOX D3 PROTEIN; ISOPROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG; CXCR4 PROTEIN, HUMAN; FORKHEAD TRANSCRIPTION FACTOR; FOXD3 PROTEIN, HUMAN; PAIRED BOX TRANSCRIPTION FACTOR; PAX3 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BINDING SITE; CANCER GROWTH; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; CXCR4 GENE; ENHANCER REGION; EXON; GENE ACTIVATION; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; INTRON; MELANOMA CELL LINE; MELANOMA METASTASIS; MIGRATION INHIBITION; MOLECULAR PATHOLOGY; MOUSE; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; 3T3 CELL LINE; ANIMAL; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; MELANOMA; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

3T3 CELLS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; ENHANCER ELEMENTS, GENETIC; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; INTRONS; MELANOMA; MICE; PAIRED BOX TRANSCRIPTION FACTORS; PAX3 TRANSCRIPTION FACTOR; PROTEIN BINDING; RECEPTORS, CXCR4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84941348266     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.670976     Document Type: Article

References (56)

1. Thompson, J. A. (2012) Ten years of progress in melanoma. J. Natl. Compr. Canc. Netw. 10, 932-935.
2. Longo-Imedio, M. I., Longo, N., Treviño, I., Lázaro, P., and Sánchez-Mateos, P. (2005) Clinical significance of CXCR3 and CXCR4 expression in primary melanoma. Int. J. Cancer 117, 861-865.
3. Scala, S., Giuliano, P., Ascierto, P. A., Ieranò, C., Franco, R., Napolitano, M., Ottaiano, A., Lombardi, M. L., Luongo, M., Simeone, E., Castiglia, D., Mauro, F., De Michele, I., Calemma, R., Botti, G., Caracò, C., Nicoletti, G., Satriano, R. A., and Castello, G. (2006) Human melanoma metastases express functional CXCR4. Clin. Cancer Res. 12, 2427-2433.
4. Bartolomé, R. A., Gálvez, B. G., Longo, N., Baleux, F., Van Muijen, G. N., Sánchez-Mateos, P., Arroyo, A. G., and Teixidó, J. (2004) Stromal cellderived factor-1-promotes melanoma cell invasion across basement membranes involving stimulation of membrane-type 1 matrix metalloproteinase and Rho GTPase activities. Cancer Res. 64, 2534-2543.
5. Cardones, A. R., Murakami, T., and Hwang, S. T. (2003) CXCR4 enhances adhesion of B16 tumor cells to endothelial cells in vitro and in vivo via -1 integrin. Cancer Res. 63, 6751-6757.
6. Murakami, T., Maki, W., Cardones, A. R., Fang, H., Tun Kyi, A., Nestle, F. O., and Hwang, S. T. (2002) Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16 melanoma cells. Cancer Res. 62, 7328-7334.
7. Robledo, M. M., Bartolome, R. A., Longo, N., Rodríguez-Frade, J. M., Mellado, M., Longo, I., van Muijen, G. N., Sánchez-Mateos, P., and Teixidó, J. (2001) Expression of functional chemokine receptors CXCR3 and CXCR4 on human melanoma cells. J. Biol. Chem. 276, 45098-45105.
8. Vianello, F., Papeta, N., Chen, T., Kraft, P., White, N., Hart, W. K., Kircher, M. F., Swart, E., Rhee, S., Palù, G., Irimia, D., Toner, M., Weissleder, R., and Poznansky, M. C. (2006) Murine B16 melanomas expressing high levels of the chemokine stromal-derived factor-1/CXCL12 induce tumor-specific T cell chemorepulsion and escape from immune control. J. Immunol. 176, 2902-2914.
9. Kim, M., Koh, Y. J., Kim, K. E., Koh, B. I., Nam, D. H., Alitalo, K., Kim, I., and Koh, G. Y. (2010) CXCR4 signaling regulates metastasis of chemoresistant melanoma cells by a lymphatic metastatic niche. Cancer Res. 70, 10411-10421.
10. O'Boyle, G., Swidenbank, I., Marshall, H., Barker, C. E., Armstrong, J., White, S. A., Fricker, S. P., Plummer, R., Wright, M., and Lovat, P. E. (2013) Inhibition of CXCR4-CXCL12 chemotaxis in melanoma by AMD11070. Br. J. Cancer 108, 1634-1640.
11. Lee, C. H., Kakinuma, T., Wang, J., Zhang, H., Palmer, D. C., Restifo, N. P., and Hwang, S. T. (2006) Sensitization of B16 tumor cells with a CXCR4 antagonist increases the efficacy of immunotherapy for established lung metastases. Mol. Cancer Ther. 5, 2592-2599.
12. Takekoshi, T., Ziarek, J. J., Volkman, B. F., and Hwang, S. T. (2012) A locked, dimeric CXCL12 variant effectively inhibits pulmonary metastasis of CXCR4-expressing melanoma cells due to enhanced serum stability. Mol. Cancer Ther. 11, 2516-2525.
13. Javelaud, D., Mohammad, K. S., McKenna, C. R., Fournier, P., Luciani, F., Niewolna, M., André, J., Delmas, V., Larue, L., Guise, T. A., and Mauviel, A. (2007) Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res. 67, 2317-2324.
14. Kubic, J. D., Mascarenhas, J. B., Iizuka, T., Wolfgeher, D., and Lang, D. (2012) GSK-3 promotes cell survival, growth, and PAX3 levels in human melanoma cells. Mol. Cancer Res. 10, 1065-1076.
15. Mascarenhas, J. B., Littlejohn, E. L., Wolsky, R. J., Young, K. P., Nelson, M., Salgia, R., and Lang, D. (2010) PAX3 and SOX10 activate MET receptor expression in melanoma. Pigment Cell Melanoma Res. 23, 225-237.
16. Plummer, R. S., Shea, C. R., Nelson, M., Powell, S. K., Freeman, D. M., Dan, C. P., and Lang, D. (2008) PAX3 expression in primary melanomas and nevi. Mod. Pathol. 21, 525-530.
17. Scholl, F. A., Kamarashev, J., Murmann, O. V., Geertsen, R., Dummer, R., and Schäfer, B. W. (2001) PAX3 is expressed in human melanomas and contributes to tumor cell survival. Cancer Res. 61, 823-826.
18. Bonvin, E., Falletta, P., Shaw, H., Delmas, V., and Goding, C. R. (2012) A phosphatidylinositol 3-kinase-Pax3 axis regulates Brn-2 expression in melanoma. Mol. Cell. Biol. 32, 4674-4683.
19. Liu, F., Cao, J., Lv, J., Dong, L., Pier, E., Xu, G. X., Wang, R. A., Xu, Z., Goding, C., and Cui, R. (2013) TBX2 expression is regulated by PAX3 in the melanocyte lineage. Pigment Cell Melanoma Res. 26, 67-77.
20. Chalepakis, G., Jones, F. S., Edelman, G. M., and Gruss, P. (1994) Pax-3 contains domains for transcription activation and transcription inhibition. Proc. Natl. Acad. Sci. U.S.A. 91, 12745-12749.
21. Kubic, J. D., Little, E. C., Lui, J. W., Iizuka, T., and Lang, D. (2014) PAX3 and ETS1 synergistically activate MET expression in melanoma cells. Oncogene 10.1038/onc.2014.420.
22. Kubic, J. D., Young, K. P., Plummer, R. S., Ludvik, A. E., and Lang, D. (2008) Pigmentation PAX-ways: The role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res. 21, 627-645.
23. Lang, D., and Epstein, J. A. (2003) Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum. Mol. Genet. 12, 937-945.
24. Abel, E. V., and Aplin, A. E. (2010) FOXD3 is a mutant B-RAF-regulated inhibitor of G1-S progression in melanoma cells. Cancer Res. 70, 2891-2900.
25. Basile, K. J., Abel, E. V., and Aplin, A. E. (2012) Adaptive upregulation of FOXD3 and resistance to PLX4032/4720-induced cell death in mutant B-RAF melanoma cells. Oncogene 31, 2471-2479.
26. Katiyar, P., and Aplin, A. E. (2011) FOXD3 regulates migration properties and Rnd3 expression in melanoma cells. Mol. Cancer Res. 9, 545-552.
27. Sutton, J., Costa, R., Klug, M., Field, L., Xu, D., Largaespada, D. A., Fletcher, C. F., Jenkins, N. A., Copeland, N. G., Klemsz, M., and Hromas, R. (1996) Genesis, a winged helix transcriptional repressor with expression restricted to embryonic stem cells. J. Biol. Chem. 271, 23126-23133.
28. Hayashi, H., and Kume, T. (2008) Forkhead transcription factors regulate expression of the chemokine receptor CXCR4 in endothelial cells and CXCL12-induced cell migration. Biochem. Biophys. Res. Commun. 367, 584-589.
29. Li, D., Yan, D., Liu, W., Li, M., Yu, J., Li, Y., Qu, Z., and Ruan, Q. (2011) Foxc2 overexpression enhances benefit of endothelial progenitor cells for inhibiting neointimal formation by promoting CXCR4-dependent homing. J. Vasc. Surg. 53, 1668-1678.
30. Fredericks, W. J., Galili, N., Mukhopadhyay, S., Rovera, G., Bennicelli, J., Barr, F. G., and Rauscher, F. J. 3rd. (1995) The PAX3-FKHR fusion protein created by the t(2;13) translocation in alveolar rhabdomyosarcomas is a more potent transcriptional activator than PAX3. Mol. Cell. Biol. 15, 1522-1535.
31. Galili, N., Davis, R. J., Fredericks, W. J., Mukhopadhyay, S., Rauscher, F. J. 3rd, Emanuel, B. S., Rovera, G., and Barr, F. G. (1993) Fusion of a forkhead domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat. Genet. 5, 230-235.
32. Tarnowski, M., Grymula, K., Reca, R., Jankowski, K., Maksym, R., Tarnowska, J., Przybylski, G., Barr, F. G., Kucia, M., and Ratajczak, M. Z. (2010) Regulation of expression of stromal-derived factor-1 receptors: CXCR4 and CXCR7 in human rhabdomyosarcomas. Mol. Cancer Res. 8, 1-14.
33. Tomescu, O., Xia, S. J., Strezlecki, D., Bennicelli, J. L., Ginsberg, J., Pawel, B., and Barr, F. G. (2004) Inducible short-term and stable long-term cell culture systems reveal that the PAX3-FKHR fusion oncoprotein regulates CXCR4, PAX3, and PAX7 expression. Lab. Invest. 84, 1060-1070.
34. Nelms, B. L., Pfaltzgraff, E. R., and Labosky, P. A. (2011) Functional interaction between Foxd3 and Pax3 in cardiac neural crest development. Genesis 49, 10-23.
35. Thomas, A. J., and Erickson, C. A. (2009) FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136, 1849-1858.
36. Wilson, D., Sheng, G., Lecuit, T., Dostatni, N., and Desplan, C. (1993) Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 7, 2120-2134.
37. Chalepakis, G., Goulding, M., Read, A., Strachan, T., and Gruss, P. (1994) Molecular basis of splotch and Waardenburg Pax-3 mutations. Proc. Natl. Acad. Sci. U.S.A. 91, 3685-3689.
38. Chalepakis, G., and Gruss, P. (1995) Identification of DNA recognition sequences for the Pax3 paired domain. Gene 162, 267-270.
39. Epstein, J. A., Shapiro, D. N., Cheng, J., Lam, P. Y., and Maas, R. L. (1996) Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc. Natl. Acad. Sci. U.S.A. 93, 4213-4218.
40. Jun, S., and Desplan, C. (1996) Cooperative interactions between paired domain and homeodomain. Development 122, 2639-2650.
41. Overdier, D. G., Porcella, A., and Costa, R. H. (1994) The DNA-binding specificity of the hepatocyte nuclear factor 3/forkhead domain is influenced by amino-acid residues adjacent to the recognition helix. Mol. Cell. Biol. 14, 2755-2766.
42. Caruz, A., Samsom, M., Alonso, J. M., Alcami, J., Baleux, F., Virelizier, J. L., Parmentier, M., and Arenzana-Seisdedos, F. (1998) Genomic organization and promoter characterization of human CXCR4 gene. FEBS Lett. 426, 271-278.
43. Labosky, P. A., and Kaestner, K. H. (1998) The winged helix transcription factor Hfh2 is expressed in neural crest and spinal cord during mouse development. Mech. Dev. 76, 185-190.
44. Zhu, Z. B., Makhija, S. K., Lu, B., Wang, M., Kaliberova, L., Liu, B., Rivera, A. A., Nettelbeck, D. M., Mahasreshti, P. J., Leath, C. A. 3rd, Yamamoto, M., Yamaoto, M., Alvarez, R. D., and Curiel, D. T. (2004) Transcriptional targeting of adenoviral vector through the CXCR4 tumor-specific promoter. Gene Ther. 11, 645-648.
45. Wegner, S. A., Ehrenberg, P. K., Chang, G., Dayhoff, D. E., Sleeker, A. L., and Michael, N. L. (1998) Genomic organization and functional characterization of the chemokine receptor CXCR4, a major entry co-receptor for human immunodeficiency virus type 1. J. Biol. Chem. 273, 4754-4760.
46. Gupta, S. K., and Pillarisetti, K. (1999) Cutting edge: CXCR4-Lo: Molecular cloning and functional expression of a novel human CXCR4 splice variant. J. Immunol. 163, 2368-2372.
47. Duquenne, C., Psomas, C., Gimenez, S., Guigues, A., Carles, M. J., Barbuat, C., Lavigne, J. P., Sotto, A., Reynes, J., Guglielmi, P., Mettling, C., François, V., and Corbeau, P. (2014) The two human CXCR4 isoforms display different HIV receptor activities: consequences for the emergence of X4strains. J. Immunol. 193, 4188-4194.
48. Sloane, A. J., Raso, V., Dimitrov, D. S., Xiao, X., Deo, S., Muljadi, N., Restuccia, D., Turville, S., Kearney, C., Broder, C. C., Zoellner, H., Cunningham, A. L., Bendall, L., and Lynch, G. W. (2005) Marked structural and functional heterogeneity in CXCR4: separation of HIV-1 and SDF-1-responses. Immunol. Cell Biol. 83, 129-143.
49. Vasyutina, E., Stebler, J., Brand-Saberi, B., Schulz, S., Raz, E., and Birchmeier, C. (2005) CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev. 19, 2187-2198.
50. Sasai, N., Mizuseki, K., and Sasai, Y. (2001) Requirement of FoxD3-class signaling for neural crest determination in Xenopus. Development 128, 2525-2536.
51. He, S., Li, C. G., Slobbe, L., Glover, A., Marshall, E., Baguley, B. C., and Eccles, M. R. (2011) PAX3 knockdown in metastatic melanoma cell lines does not reduce MITF expression. Melanoma Res. 21, 24-34.
52. Izraely, S., Klein, A., Sagi-Assif, O., Meshel, T., Tsarfaty, G., Hoon, D. S., and Witz, I. P. (2010) Chemokine-chemokine receptor axes in melanoma brain metastasis. Immunol. Lett. 130, 107-114.
53. Widmer, D. S., Cheng, P. F., Eichhoff, O. M., Belloni, B. C., Zipser, M. C., Schlegel, N. C., Javelaud, D., Mauviel, A., Dummer, R., and Hoek, K. S. (2012) Systematic classification of melanoma cells by phenotype-specific gene expression mapping. Pigment Cell Melanoma Res. 25, 343-353.
54. Liedtke, D., Erhard, I., Abe, K., Furutani-Seiki, M., Kondoh, H., and Schartl, M. (2014) Xmrk-induced melanoma progression is affected by Sdf1 signals through Cxcr7. Pigment Cell Melanoma Res. 27, 221-233.
55. Lee, E., Han, J., Kim, K., Choi, H., Cho, E. G., and Lee, T. R. (2013) CXCR7 mediates SDF1-induced melanocyte migration. Pigment Cell Melanoma Res. 26, 58-66.
56. Ueno, Y., Sakurai, H., Tsunoda, S., Choo, M. K., Matsuo, M., Koizumi, K., and Saiki, I. (2008) Heregulin-induced activation of ErbB3 by EGFR tyrosine kinase activity promotes tumor growth and metastasis in melanoma cells. Int. J. Cancer 123, 340-347.