Loss of AP-2 results in downregulation of c-KIT and enhancement of melanoma tumorigenicity and metastasis

EMBO Journal

Volumn 17, Issue 15, 1998, Pages 4358-4369

  Huang, Suyun ^a   Jean, Didier ^a   Luca, Mario ^a   Tainsky, Michael A ^a   Bar Eli, Menashe ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Apoptosis; Malignant melanoma; Metastasis; Transcription factor; Tyrosine kinase

Indexed keywords

MESSENGER RNA; STEM CELL FACTOR; TRANSCRIPTION FACTOR AP 2; TYROSINE KINASE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; GENE LOSS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE;

ANIMALS; APOPTOSIS; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION; HUMANS; LUNG NEOPLASMS; MALE; MELANOMA; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM TRANSPLANTATION; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-KIT; REPRESSOR PROTEINS; STEM CELL FACTOR; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR AP-2; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR CELLS, CULTURED; UP-REGULATION;

ANIMALIA; MUS MUSCULUS;

EID: 0032479996     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.15.4358     Document Type: Article

References (80)

1. Ariizumi, K., Bergstresser, P.R. and Takashima, A. (1996) Wavelength-specific induction of immediate early genes by ultraviolet radiation. J. Dermatol. Sci., 12, 147-155.
2. Bar-Eli, M. (1997) Molecular mechanisms of melanoma metastasis. J. Cell Physiol., 173, 275-278.
3. Bauer, R., Imhof, A., Pscherer, A., Kopp, H., Moser, M., Seagers, S., Kerscher, M., Tainsky, M.A., Hofstaedter, F. and Buettner, R. (1994) The genomic structure of the human AP-2 transcription factor. Nucleic Acids Res., 22, 1413-1420.
4. Bosher, J.M., Williams, T. and Hurst, H.C. (1995) The developmentally regulated transcription factor AP-2 is involved in c-erbB-2 overexpression in human mammary carcinoma. Proc. Natl Acad. Sci. USA, 92, 744-747.
5. Brannan, C.I., Lyman, S.D., Williams, D.E., Eisenman, J., Anderson, D., Cosman, D., Bedell, M.A., Jenkins, N.A. and Coopeland, N.G. (1991) Steel-Dickie mutation encodes a c-KIT ligand lacking transmembrane and cytoplasmic domains. Proc. Natl Acad. Sci. USA, 88, 4671-4674.
6. Buettner, R., Kannan, P., Imhof, A., Bauer, R., Yim, S.O., Glackshuber, R., van Dyke, M.W. and Tainsky, M.A. (1993) An alternatively spliced mRNA from the AP-2 gene encodes a negative regulator of transcriptional activation of AP-2. Mol. Cell. Biol., 13, 4174-4185.
7. Carthew, R.W., Codosh, L.A. and Sharp, P.A. (1985) An RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell. 43, 439-148.
8. Chabot, B., Stephenson, D.A., Chapman, V.M., Besmer, P. and Bernstein, A. (1988) The protooncogene c-kit encoding a trans-membrane tyrosine kinase receptor maps to the mouse W locus. Nature, 335, 88-89.
9. Copeman, M.C. (1992) The putative melanoma tumor-suppressor gene on human chromosome 6q. Pathology, 24, 307-309.
10. Cowley, G.P. and Smith, M.E. (1996) Cadherin expression in melanocytic naevi and malignant melanomas. Am. J. Pathol., 179, 183-187.
11. Descheemaeker, K.A., Wyns, S., Nelles, L., Auwerx, J., Ny, T. and Collen, D. (1992) Interaction of AP-1-like, AP-2-like and SP-1-like proteins with two distinct sties in the upstream regulatory region of the plasminogen activator inhibitor-1 gene mediates the phorbol 12-myristate 13-acetate response. J. Biol. Chem., 267, 15086-15091.
12. Duan, C. and Clemmons, D.R. (1995) Transcription factor AP-2 regulates human insulin-like growth factor binding protein-5 gene expression. J. Biol. Chem., 270, 24844-24851.
13. Fidler, I.J. (1990) Critical factors in the biology of human cancer metastasis. Cancer Res., 50, 6130-6138.
14. Fidler, I.J. (1992) The biology of melanoma metastasis. In Balch, C.M., Houghton, A.N., Milton, G.W., Sober, A.J. and Soong, S.J. (eds) Cutaneous Melanoma. J.B. Lippincott Company, Philadelphia, PA, pp. 112-129.
15. d mutant. Cell. 64, 1025-1035.
16. Fleischman, R.A. (1992) Human piebald trait resulting from a dominant negative mutant allele of the c-KIT membrane receptor gene. J. Clin. Invest., 89, 1713-1717.
17. Fleischman, R.A., Saltman, K.L., Stastny, V. and Zneimer, S. (1991) Deletion of the c-kit protooncogene in the human development defect piebald trait. Proc. Natl Acad. Sci. USA, 88, 10885-10889.
18. Fort, P., Marty. L., Piechaczyh, M., Sabrouty, S.E., Dani, C., Jeanteur, P. and Blanchard, J.M. (1985) Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res., 13, 1431-1442.
19. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S.A. (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J. Cell Biol., 119, 493-501.
20. Gaynor, R.B., Muchardt, C., Xia, Y.R., Klisak, I., Mohandas, T., Sparkes, R.S. and Lusis, A.J. (1991) Localization of the gene for the DNA-binding protein AP-2 to human chromosome 6p 22.3-pter. Genomics, 10, 1100-1102.
21. Geisler, E.N., Ryan, M.A. and Housman, D.E. (1988) The dominant white spotting (W) locus of the mouse encodes the c-KIT protooncogene. Cell, 55, 185-192.
22. Giebel, L.B. and Spritz, R.A. (1991) Mutation of the KIT (mast/stem cell growth factor receptor) proto-oncogene in human piebaldism. Proc. Natl Acad. Sci. USA, 88, 8696-8699.
23. Grether-Beck, S., Olaizola-Horn, S., Schmitt, H., Grewe, M., Jahnke, A., Johnson, J.P. Briviba, K., Sies, H. and Krutmann, J. (1996) Activation of transcription factor Ap-2 mediates UVA radiation- and singlet oxygen-induced expression of the human intercellular adhesion molecule gene. Proc. Natl Acad. Sci. USA, 93, 14586-14591.
24. Grover, R. and Wilson, G.D. (1996) Bcl-2 expression in malignant melanoma. Eur. J. Surg. Oncol., 22, 347-349.
25. Gutman, M., Singh, R.K., Radinsky, R. and Bar-Eli, M. (1994) Intertumoral heterogeneity of receptor-tyrosine kinases expression in human melanoma cell lines with different metastatic capabilities. Anticancer Res., 14, 1759-1766.
26. Haslinger, A. and Karin, M. (1985) Upstream promoter element of the human metallothionein-IIA gene can act like an enhancer element. Proc. Natl Acad. Sci. USA, 82, 8572-8576.
27. Healy, E., Rehman, I., Angus, B. and Rees, J.L. (1995) Loss of heterozygosity in sporadic primary cutaneous melanoma. Genes Chromosom. Cancer, 12, 152-156.
28. Holman, C.D.J., Mulroney, C.D. and Armstrong, B.K. (1980) Epidemiology of preinvasive and invasive malignant melanoma in Western Australia. Int. J. Cancer, 25, 317-323.
29. Huang, S., Luca, M. Gutman, M., McConkey, D.J., Langley, K.E., Lyman, S.D. and Bar-Eli, M. (1996) Enforced c-KIT expression renders highly metastatic human melanoma cells susceptible to stem cell factor-induced apoptosis and inhibits their tumorigenic and metastatic potential. Oncogene, 13, 2339-2347.
30. Hudson, J.M. Frade, R. and Bar-Eli, M. (1995) Wild-type p53 regulates its own transcription in a cell-type-specific manner. DNA Cell Biol., 14, 759-766.
31. Hyman, S.E., Comb, M. Pearlberg, J. and Goodman, H.M. (1989) An AP-2 element acts synergistically with the cyclic AMP and phorbol ester-inducible enhancer of the human proenkephalin gene. Mol. Cell. Biol., 9, 321-324.
32. Janknecht, R. and Hunter, T. (1997) Convergence of MAP-kinase pathways on the ternary complex factor Sap-1a. EMBO J., 16, 1620-1627.
33. Jean, D., Gershenwald, J.E., Huang, S., Luca, M., Hudson, M.J., Tainsky, A.M. and Bar-Eli, M. (1998) Loss of AP-2 results in upregulation of MCAM/MUC18 and an increase in tumor growth and metastasis of human melanoma cells. J. Biol. Chem., 273, 16501-16508.
34. Jiang, H., Lin, J., Su, Z.Z., Herlyn, M., Kerbel, R.S., Weissman, B.E., Welch, D.R. and Fisher, P.B. (1995) The melanoma differentiation-associated gene mda-6. which encodes the cyclin-dependent kinase inhibitor p21, is differentially expressed during growth, differentiation and progression in human melanoma cells. Oncogene, 10, 1855-1864.
35. Kannan, P., Buettner, R., Chiao, P.J., Yim, S.O., Sarkiss, M. and Tainksy, M.A. (1994) N-ras oncogene causes AP-2 transcriptional self-interference which leads to transformation. Genes Dev., 8, 1258-1269.
36. Kopf, A.W., Salopek, T.G., Slade, J., Marghoob, A.A. and Bart, R.S. (1995) Techniques of cutaneous examination for the detection of skin cancer. Cancer, 75, 684-690.
37. Kozlowski, J.M., Hart, I.R., Fidler, I.J. and Hanna, N. (1984) A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J. Natl Cancer Inst., 72, 913-917.
38. Lassam, N. and Bickford, S. (1992) Loss of c-KIT expression in cultured melanoma cells. Oncogene, 7, 51-56.
39. Leask, A., Byrne, C. and Fuchs, E. (1991) Transcriptional factor AP-2 and its role in epidermal-specific gene expression. Proc. Natl Acad. Sci. USA, 88, 7948-7952.
40. Lee, W., Haslinger, A., Karin, M. and Tjian, R. (1987) Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40. Nature, 325, 368-372.
41. Lehmann, J.M., Holzmann, B., Breitbart, E.W., Schmiegelow, P., Riethmüller, G. and Johnson, J.P. (1989) MUC18, a marker of tumor progression in human melanoma, shows sequence similarity to the neural cell adhesion molecule of the immunoglobulin superfamily. Proc. Natl Acad. Sci. USA, 89, 9891-9895.
42. Li, L., Price, J.E., Fan, D., Zhang, R.D., Bucana, C.D. and Fidler, I.J. (1989) Correlation of growth capacity of human tumor cells in hard agarose with their in vivo proliferative capacity at specific metastatic sites. J. Natl Cancer Inst., 81, 1406-1412.
43. Luca, M., Huang, S., Gershenwald, J.E., Singh, R.K., Reich, R. and BarEli, M. (1997) Expression of interleukin-8 by human melanoma cells upregulates MMP-2 activity and increases tumor growth and metastasis. Am. J. Pathol., 151, 1105-1113.
44. Luca, M., Hunt, B., Bucana, C.D., Johnson, J.P., Fidler, I.J. and Bar-Eli, M. (1993) Direct correlation between MUC18 expression and metastatic potential of human melanoma cells. Melanoma Res., 3, 35-41.
45. INK4/mts-1) gene in human melanoma cells: Relevance to tumor growth and metastasis. Oncogene, 11, 1399-1402.
46. Lüscher, B., Mitchell, P.J., Williams. T. and Tjian, R. (1989) Regulation of transcription factor AP-2 by the morphogen retinoic acid and by second messengers. Genes Dev., 3, 1507-1517.
47. Mitchell, P.J., Timmons, P.M., Hebert, J.M., Rigby, P.W. and Tjian, R. (1991) Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev., 5, 105-119.
48. Mitchell, P.J., Wang, C. and Tjian, R. (1987) Positive and negative regulation of transcription in vitro: Enhancer-binding protein AP-2 is inhibited by SV40 antigen. Cell, 50, 847-861.
49. Naeve, G.S., Sharma, A. and Lee, A.S. (1992) Identification of a 10-base pair protein binding site in the promoter of the hamster h3.2 gene required tor the S-phase-dependent increase in transcription and its interaction with a jun-like nuclear factor. Cell Growth Differ., 3, 919-928.
50. Natali, P.G., Nicotra, M.R., Digiesi, G., Cavaliere, R., Bigotti, A., Trizio, D. and Segatto, O. (1994) Expression of gp185 HER-2 in human cutaneous melanoma: Implications for experimental immunotherapeutics. Int. J. Cancer, 56, 341-346.
51. Natali, P.G., Nicotra, M.R., Winkler, A.B., Cavaliere, R., Bigotti, A. and Ullrich, A. (1992) Progression of human cutaneous melanoma is associated with loss of expression of c-KIT protooncogene receptor. Int. J. Cancer, 52, 197-201.
52. Nishikawa, S., Kusakabe, M., Yoshingaga, K., Ogawa, M., Hayashi, S.I., Kunisada, T., Era, T., Sakakura, T. and Nishikawa, S.I. (1991) In vitro manipulation of coat color formation by a monoclonal anti-c-KIT antibody: two distinct waves of c-KIT dependency during melanocyte development. EMBO J., 10, 2111-2118.
53. Nocka, K., Majumder, S., Chabot, B., Ray, P., Cervone, M., Bernstein, A. and Besmer, P. (1989) Expression of the c-kit gene products in known cellular targets of W mutations in normal and W mutant mice: Evidence for impaired c-kit kinase in mutant mice. Genes Dev., 3, 816-826.
54. 41. EMBO J., 9, 1805-1813.
55. Nyborg, J.K. and Dynan, W.S. (1990) Interaction of cellular proteins with the human T cell leukemia virus type 1 transcriptional control region. J. Biol. Chem., 265, 8230-8236.
56. Orr-Urtreger, A., Avivi, A., Zimmer, Y., Givol, D., Yarden, Y. and Lonai, P. (1990) Developmental expression of c-kit, a proto-oncogene encoded by the W locus. Development, 109, 911-923.
57. Pathak, S., Drwinga, H.L. and Hsu, T.C. (1983) Involvement of chromosome 6 in the rearrangement of human malignant melanomas. Cytogenet. Cell Genet., 36, 573-579.
58. Radinsky, R., Fidler, I.J., Price, J.E., Esumi, N., Tsan, R., Petty, C.M., Bucana, C.D. and Bar-Eli, M. (1994) Terminal differentiation and apoptosis in experimental lung metastases of human osteogenic sarcoma cells by wild-type p53. Oncogene, 9, 1877-1883.
59. Reith, A.D., Rotapel, R., Giddens, E., Brady, C., Forrester, L. and Bernstein, A. (1990) W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c-KIT transmembrane receptor. Genes Dev., 4, 390-400.
60. Romerdahl, C.A., Donawho, C., Fidler, I.J. and Kripke, M.L. (1988) Effect of UV-B radiation on the in vivo growth of murine melanoma cells. Cancer Res., 48, 4007-4010.
61. Schorle, H., Meier, P., Buchert, M., Jaenisch, R. and Mitchell, P.J. (1996) Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature, 381, 235-238.
62. Singh, R.K., Gutman, M., Reich, R. and Bar-Eli, M. (1995) Ultraviolet B irradiation promotes tumorigenic and metastatic properties in primary cutaneous melanoma via induction of interleukin 8. Cancer Res., 55, 3669-3674.
63. 42 spotting phenotype results from a missense mutation in the c-KIT receptor kinase. Science, 247, 209-212.
64. Trent, J.M., Stanbridge, E.J., McBride, H.L., Meese, E.U., Casey, G. and Araujo, D.E. (1990) Tumorigenicity in human melanoma cell lines controlled by introduction of human chromosome 6. Science, 247, 569-571.
65. Trent, J.M., Thompson, F.H. and Meyskens, F.L. (1983) Identification of a recurring translocation site involving chromosome 6 in human malignant melanoma. Cancer Res., 49, 420-423.
66. van den Oord, J.J., Vandeghinste, N., De Ley, M. and De Wolf-Peeters, C. (1994) Bc1-2 expression in human melanocytes and melanocytic tumors. Am. J. Pathol. 145, 294-300.
67. Vidal, M.J., Loganzo, F., Jr, de Oliveira, A.R., Hayward, N.K. and Albino, A.P. (1995) Mutations and defective expression of the WAF-1 p21 tumor-suppressor gene in malignant melanomas. Melanoma Res., 5, 243-250.
68. Walker, G.J., Nancarrow, D.J., Walters, M.K., Palmer, J.M., Weber, J.L. and Hayward, N.K. (1994) Linkage analysis in familial melanoma kindreds to markers on chromosome 6p. Int. J. Cancer, 59, 771-775.
69. Welch, D.R., Chen, P, Miele, M.E., McGary, C.T., Bower, J.M. and Weissman, B.E. (1994) Microcell-mediated transfer of chromosome 6 into metastatic human C8161 melanoma cells suppresses metastasis but does not inhibit tumorigenicity. Oncogene, 9, 255-262.
70. Williams, T. and Tjian, R. (1991) Characterization of a dimerization motif in AP-2 and its function in heterologous DNA-binding proteins. Science, 251, 1067-1071.
71. Williams, T., Admon, A., Luscher, B. and Tjian, R. (1988) Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev., 2, 1557-1569.
72. Xie, S., Huang, S., Luca, M., Gutman, M., Reich, R., Johnson, J.P. and BarEli, M. (1997a) Expression of MCAM/MUC18 by human melanoma cells leads to increased tumor growth and metastasis. Cancer Res., 57, 2295-2303.
73. Xie, S., Price, J.E., Luca, M., Jean, D., Ronai, Z. and Bar-Eli, M. (1997b) Dominant-negative CREB inhibits tumor growth and metastasis of human melanoma cells. Oncogene, 15, 2069-2075.
74. Yamamoto, K., Tojo, A., Aoki, N. and Shibuya, A. (1993) Characterization of the promoter region of the human c-KIT protooncogene. Jpn. J. Cancer Res., 84, 1136-1144.
75. Yarden, Y. et al. (1987) A human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J., 6, 3342-3351.
76. Zakut, R., Perlis, R., Eliyahu, S., Yarden, Y., Givol, D., Lyman, S.D. and Halaban, R. (1993) KIT ligand (mast cell growth factor) inhibits the growth of KIT-expressing melanoma cells. Oncogene, 8, 2221-2229.
77. WAF1/CIP1 expression. Nature Genet., 15, 78-82.
78. Zhang, J., Cui, P., Glatfelter, A.A., Cummings, L.M., Meltzer, P.S. and Trent, J.M. (1995) Microdissection-based cloning of a translocation breakpoint in a human malignant melanoma. Cancer Res., 55, 4640-4645.
79. Zhang, J., Hagopian-Donaldson, S., Serbedzija, G., Elsemore, J., Plehn-Dujowich, D., McMahon, A.P. Flavell, R.A. and Williams, T. (1996) Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature, 381, 238-241.
80. Zsebo, K.M. et al. (1990) Stem cell factor is encoded at the SL locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell, 63, 213-224.