Loss of JunB Activity Enhances Stromelysin 1 Expression in a Model of the Epithelial-to-Mesenchymal Transition of Mouse Skin Tumors

REFERENCES

• Bakiri, L., D. Lallemand, E. Bossy-Wetzel, and M. Yaniv. 2000. Cell cycle-dependent variations in c-Jun and JunB phosphorylation: a role in the control of cyclin D1 expression. EMBO J. 19:2056–2068.
   PubMedGoogle Scholar
• Batlle, E., E. Sancho, C. Franci, D. Dominguez, M. Monfar, J. Baulida, and D. H. Garcia. 2000. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2:84–89.
   PubMed Web of Science ®Google Scholar
• Birchmeier, C., W. Birchmeier, and B. Brand-Saberi. 1996. Epithelial-mesenchymal transitions in cancer progression. Acta Anat. (Basel) 156:217–226.
   PubMedGoogle Scholar
• Boulikas, T.. 1995. Phosphorylation of transcription factors and control of the cell cycle. Crit. Rev. Eukaryot. Gene Expr. 5:1–77.
   PubMed Web of Science ®Google Scholar
• Bremner, R., and A. Balmain. 1990. Genetic changes in skin tumor progression: correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell 61:407–417.
   PubMedGoogle Scholar
• Brown, K., and A. Balmain. 1995. Transgenic mice and squamous multistage skin carcinogenesis. Cancer Metastasis Rev. 14:113–124.
   PubMedGoogle Scholar
• Burns, P. A., C. J. Kemp, J. V. Gannon, D. P. Lane, R. Bremner, and A. Balmain. 1991. Loss of heterozygosity and mutational alterations of the p53 gene in skin tumors of interspecific hybrid mice. Oncogene 6:2363–2369.
   PubMedGoogle Scholar
• Cano, A., M. A. Perez-Moreno, I. Rodrigo, A. Locascio, M. J. Blanco, M. G. del Barrio, F. Portillo, and M. A. Nieto. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2:76–83.
   PubMed Web of Science ®Google Scholar
• Caulin, C., F. G. Scholl, P. Frontelo, C. Gamallo, and M. Quintanilla. 1995. Chronic exposure of cultured transformed mouse epidermal cells to transforming growth factor-beta 1 induces an epithelial-mesenchymal transdifferentiation and a spindle tumoral phenotype. Cell Growth Differ. 6:1027–1035.
   PubMedGoogle Scholar
• Chambers, A. F., and L. M. Matrisian. 1997. Changing views of the role of matrix metalloproteinases in metastasis. J. Natl. Cancer Inst. 89:1260–1270.
   PubMed Web of Science ®Google Scholar
• Chiu, R., P. Angel, and M. Karin. 1989. Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell 59:979–986.
   PubMed Web of Science ®Google Scholar
• Crawford, H. C., and L. M. Matrisian. 1996. Mechanisms controlling the transcription of matrix metalloproteinase genes in normal and neoplastic cells. Enzyme Protein 49:20–37.
   PubMedGoogle Scholar
• Cui, W., D. J. Fowlis, S. Bryson, E. Duffie, H. Ireland, A. Balmain, and R. J. Akhurst. 1996. TGFbeta1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell 86:531–542.
   PubMed Web of Science ®Google Scholar
• D'Armiento, J., T. DiColandrea, S. S. Dalal, Y. Okada, M. T. Huang, A. H. Conney, and K. Chada. 1995. Collagenase expression in transgenic mouse skin causes hyperkeratosis and acanthosis and increases susceptibility to tumorigenesis. Mol. Cell. Biol. 15:5732–5739.
   PubMedGoogle Scholar
• De Groot, R. P., J. Auwerx, M. Bourouis, and P. Sassone-Corsi. 1993. Negative regulation of Jun/AP-1: conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy. Oncogene 8:841–847.
   PubMed Web of Science ®Google Scholar
• Deng, T., and M. Karin. 1993. JunB differs from c-Jun in its DNA-binding and dimerization domains, and represses c-Jun by formation of inactive heterodimers. Genes Dev. 7:479–490.
   PubMed Web of Science ®Google Scholar
• Dong, Z. G., H. C. Crawford, V. Lavrovsky, D. Taub, R. Watts, L. M. Matrisian, and N. H. Colburn. 1997. A dominant negative mutant of jun blocking 12-o-tetradecanoylphorbol-13-acetate-induced invasion in mouse keratinocytes. Mol. Carcinog. 19:204–212.
   PubMed Web of Science ®Google Scholar
• Engel, M. E., M. A. McDonnell, B. K. Law, and H. L. Moses. 1999. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J. Biol. Chem. 274:37413–37420.
   PubMed Web of Science ®Google Scholar
• Gaire, M., Z. Magbanua, S. McDonnell, L. McNeil, D. H. Lovett, and L. M. Matrisian. 1994. Structure and expression of the human gene for the matrix metalloproteinase matrilysin. J. Biol. Chem. 269:2032–2040.
   PubMed Web of Science ®Google Scholar
• Gandarillas, A., and F. M. Watt. 1995. Changes in expression of members of the fos and jun families and myc network during terminal differentiation of human keratinocytes. Oncogene 11:1403–1407.
   PubMedGoogle Scholar
• Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7:2135–2148.
   PubMed Web of Science ®Google Scholar
• Joseloff, E., and G. T. Bowden. 1997. Regulation of the transcription factor AP-1 in benign and malignant mouse keratinocyte cells. Mol. Carcinog. 18:26–36.
   PubMedGoogle Scholar
• Kerr, L. D., D. B. Miller, and L. M. Matrisian. 1990. TGF-beta 1 inhibition of transin-stromelysin gene expression is mediated through a fos binding sequence. Cell 61:267–278.
   PubMed Web of Science ®Google Scholar
• Kirstein, M., L. Sanz, S. Quinones, J. Moscat, M. T. Diaz-Meco, and J. Saus. 1996. Cross-talk between different enhancer elements during mitogenic induction of the human stromelysin-1 gene. J. Biol. Chem. 271:18231–18236.
   PubMed Web of Science ®Google Scholar
• Leppa, S., R. Saffrich, W. Ansorge, and D. Bohmann. 1998. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 17:4404–4413.
   PubMed Web of Science ®Google Scholar
• Li, B., C. Tournier, R. J. Davis, and R. A. Flavell. 1999. Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J. 18:420–432.
   PubMed Web of Science ®Google Scholar
• Lochter, A., S. Galosy, J. Muschler, N. Freedman, Z. Werb, and M. J. Bissell. 1997. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol. 139:1861–1872.
   PubMed Web of Science ®Google Scholar
• Majmudar, G., B. R. Nelson, T. C. Jensen, J. J. Voorhees, and T. M. Johnson. 1994. Increased expression of stromelysin-3 in basal cell carcinomas. Mol. Carcinog. 9:17–23.
   PubMedGoogle Scholar
• Matrisian, L. M., and G. T. Bowden. 1990. Stromelysin/transin and tumor progression. Semin. Cancer Biol. 1:107–115.
   PubMedGoogle Scholar
• Matsui, M., M. Tokuhara, Y. Konuma, N. Nomura, and R. Ishizaki. 1990. Isolation of human fos-related genes and their expression during monocyte-macrophage differentiation. Oncogene 5:249–255.
   PubMed Web of Science ®Google Scholar
• Mendelson, K. G., L. R. Contois, S. G. Tevosian, R. J. Davis, and K. E. Paulson. 1996. Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc. Natl. Acad. Sci. USA 93:12908–12913.
   PubMed Web of Science ®Google Scholar
• Nikolakaki, E., P. J. Coffer, R. Hemelsoet, J. R. Woodgett, and L. H. Defize. 1993. Glycogen synthase kinase 3 phosphorylates Jun family members in vitro and negatively regulates their transactivating potential in intact cells. Oncogene 8:833–840.
   PubMedGoogle Scholar
• Ostrowski, L. E., J. Finch, P. Krieg, L. M. Matrisian, G. Patskan, J. F. O'Connell, J. Philips, T. J. Slaga, R. Breathnach, and G. T. Bowden. 1988. Expression pattern of a gene for a secreted metalloproteinase during late stages of tumor progression. Mol. Carcinog. 1:13–19.
   PubMed Web of Science ®Google Scholar
• Papavassiliou, A. G., M. Treier, and D. Bohmann. 1995. Intramolecular signal transduction in c-Jun. EMBO J. 14:2014–2019.
   PubMedGoogle Scholar
• Pertovaara, L., L. Sistonen, T. J. Bos, P. K. Vogt, J. Keski-Oja, and K. Alitalo. 1989. Enhanced jun gene expression is an early genomic response to transforming growth factor beta stimulation. Mol. Cell. Biol. 9:1255–1262.
   PubMed Web of Science ®Google Scholar
• Portella, G., S. A. Cumming, J. Liddell, W. Cui, H. Ireland, R. J. Akhurst, and A. Balmain. 1998. Transforming growth factor beta is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion. Cell Growth Differ. 9:393–404.
   PubMedGoogle Scholar
• Portella, G., J. Liddell, R. Crombie, S. Haddow, M. Clarke, A. B. Stoler, and A. Balmain. 1994. Molecular mechanisms of invasion and metastasis during mouse skin tumour progression. Invasion Metastasis 14:7–16.
   PubMedGoogle Scholar
• Rosenberger, S. F., J. S. Finch, A. Gupta, and G. T. Bowden. 1999. Extracellular signal-regulated kinase 1/2-mediated phosphorylation of JunD and FosB is required for okadaic acid-induced activator protein 1 activation. J. Biol. Chem. 274:1124–1130.
   PubMedGoogle Scholar
• Rutberg, S. E., T. L. Adams, A. Glick, M. T. Bonovich, C. Vinson, and S. H. Yuspa. 2000. Activator protein 1 transcription factors are fundamental to v-rasHa-induced changes in gene expression in neoplastic keratinocytes. Cancer Res. 60:6332–6338.
   PubMedGoogle Scholar
• Rutberg, S. E., E. Saez, A. Glick, A. A. Dlugosz, B. M. Spiegelman, and S. H. Yuspa. 1996. Differentiation of mouse keratinocytes is accompanied by PKC-dependent changes in AP-1 proteins. Oncogene 13:167–176.
   PubMedGoogle Scholar
• Ryder, K., A. Lanahan, E. Perez-Albuerne, and D. Nathans. 1989. jun-D: a third member of the jun gene family. Proc. Natl. Acad. Sci. USA 86:1500–1503.
   PubMed Web of Science ®Google Scholar
• Ryder, K., L. F. Lau, and D. Nathans. 1988. A gene activated by growth factors is related to the oncogene v-jun. Proc. Natl. Acad. Sci. USA 85:1487–1491.
   PubMed Web of Science ®Google Scholar
• Savagner, P., K. M. Yamada, and J. P. Thiery. 1997. The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J. Cell Biol. 137:1403–1419.
   PubMed Web of Science ®Google Scholar
• Schreiber, E., P. Matthias, M. M. Muller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with ‘mini-extracts,’ prepared from a small number of cells. Nucleic Acids Res. 17:6419
   PubMed Web of Science ®Google Scholar
• Stoler, A. B., F. Stenback, and A. Balmain. 1993. The conversion of mouse skin squamous cell carcinomas to spindle cell carcinomas is a recessive event. J. Cell Biol. 122:1103–1117.
   PubMedGoogle Scholar
• Suzuki, T., H. Okuno, T. Yoshida, T. Endo, H. Nishina, and H. Iba. 1991. Difference in transcriptional regulatory function between c-Fos and Fra-2. Nucleic Acids Res. 19:5537–5542.
   PubMedGoogle Scholar
• Szabowski, A., N. Maas-Szabowski, S. Andrecht, A. Kolbus, M. Schorpp-Kistner, N. E. Fusenig, and P. Angel. 2000. c-Jun and JunB antagonistically control cytokine-regulated mesenchymal-epidermal interaction in skin. Cell 103:745–755.
   PubMed Web of Science ®Google Scholar
• Wilkinson, D. G., S. Bhatt, R. P. Ryseck, and R. Bravo. 1989. Tissue-specific expression of c-jun and junB during organogenesis in the mouse. Development 106:465–471.
   PubMed Web of Science ®Google Scholar
• Wright, J. H., S. McDonnell, G. Portella, G. T. Bowden, A. Balmain, and L. M. Matrisian. 1994. A switch from stromal to tumor cell expression of stromelysin-1 mRNA associated with the conversion of squamous to spindle carcinomas during mouse skin tumor progression. Mol. Carcinog. 10:207–215.
   PubMedGoogle Scholar
• Young, M. R., J. J. Li, M. Rincon, R. A. Flavell, B. K. Sathyanarayana, R. Hunziker, and N. Colburn. 1999. Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc. Natl. Acad. Sci. USA 96:9827–9832.
   PubMed Web of Science ®Google Scholar
• Zoumpourlis, V., P. Papassava, S. Linardopoulos, D. Gillespie, A. Balmain, and A. Pintzas. 2000. High levels of phosphorylated c-Jun, Fra-1, Fra-2 and ATF-2 proteins correlate with malignant phenotypes in the multistage mouse skin carcinogenesis model. Oncogene 19:4011–4021.
   PubMed Web of Science ®Google Scholar