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Journal of Oncology
Volume 2009 (2009), Article ID 963209, 12 pages
http://dx.doi.org/10.1155/2009/963209
Review Article

PAI-1 Regulates the Invasive Phenotype in Human Cutaneous Squamous Cell Carcinoma

1Center for Cell Biology & Cancer Research, Albany Medical College, 47 New Scotland Avenue, Albany, NY 12208, USA
2Department of Pathology, Albany Medical College, 47 New Scotland Avenue, Albany, NY 12208, USA
3Laboratory of Tumor and Developmental Biology, Groupe Interdisciplinaire de Génoprotéomique Appliqué-Cancer, University of Liège, Avenue de l'Hôpital 3, 4000 Liège, Belgium

Received 26 August 2009; Accepted 24 November 2009

Academic Editor: Guus A. M. S. Van Dongen

Copyright © 2009 Jennifer Freytag et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. J. Eide and M. A. Weinstock, “Epidemiology of skin cancer,” in Cancer of the Skin, D. S. Rigel, R. J. Friedman, L. M. Dzubow, D. S. Reintgen, J.-C. Bystryn, and R. Marks, Eds., pp. 47–60, Elsevier, Philadelphia, Pa, USA, 2005. View at Google Scholar
  2. P. G. Lang and J. C. Maize, “Basal cell carcinoma,” in Cancer of the Skin, D. S. Rigel, R. J. Friedman, L. M. Dzubow, D. S. Reintgen, J.-C. Bystryn, and R. Marks, Eds., pp. 101–132, Elsevier, Philadelphia, Pa, USA, 2005. View at Google Scholar
  3. A. Dlugosz, G. Merlino, and S. H. Yuspa, “Progress in cutaneous cancer research,” Journal of Investigative Dermatology Symposium Proceedings, vol. 7, no. 1, pp. 17–26, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. M. P. Staples, M. Elwood, R. C. Burton, J. L. Williams, R. Marks, and G. G. Giles, “Non-melanoma skin cancer in Australia: the 2002 national survey and trends since 1985,” Medical Journal of Australia, vol. 184, no. 1, pp. 6–10, 2006. View at Google Scholar · View at Scopus
  5. T. H. Nguyen and J. Yoon, “Squamous cell carcinoma,” in Cancer of the Skin, D. S. Rigel, R. J. Friedman, L. M. Dzubow, D. S. Reintgen, J.-C. Bystryn, and R. Marks, Eds., pp. 133–150, Elsevier, Philadelphia, Pa, USA, 2005. View at Google Scholar
  6. P. Boukamp, “UV-induced skin cancer: similarities—variations,” Journal of the German Society of Dermatology, vol. 3, no. 7, pp. 493–503, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Boukamp, W. Peter, U. Pascheberg et al., “Step-wise progression in human skin carcinogenesis in vitro involves mutational inactivation of p53, ras(H) oncogene activation and additional chromosome loss,” Oncogene, vol. 11, no. 5, pp. 961–969, 1995. View at Google Scholar · View at Scopus
  8. G. Giglia-Mari and A. Sarasin, “TP53 mutations in human skin cancers,” Human Mutation, vol. 21, no. 3, pp. 217–228, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Dans and S. S. Fakharzadeh, “Genetic basis of skin cancer,” in Cancer of the Skin, D. S. Rigel, R. J. Friedman, L. M. Dzubow, D. S. Reintgen, J.-C. Bystryn, and R. Marks, Eds., pp. 15–27, Elsevier, Philadelphia, Pa, USA, 2005. View at Google Scholar
  10. B. R. Smoller, “Squamous cell carcinoma: from precursor lesions to high-risk variants,” Modern Pathology, vol. 19, supplement 2, pp. S88–S92, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Y. Tsai and H. Tsao, “The genetics of skin cancer,” American Journal of Medical Genetics, vol. 131C, no. 1, pp. 82–92, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Boukamp, “Non-melanoma skin cancer: what drives tumor development and progression?” Carcinogenesis, vol. 26, no. 10, pp. 1657–1667, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. S. H. Yuspa, “The pathogenesis of squamous cell cancer: lessons learned from studies of skin carcinogenesis,” Journal of Dermatological Science, vol. 17, no. 1, pp. 1–7, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Frame, R. Crombie, J. Liddell et al., “Epithelial carcinogenesis in the mouse: correlating the genetics and the biology,” Philosophical Transactions of the Royal Society B, vol. 353, no. 1370, pp. 839–845, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. P. K. Tsantoulis, N. G. Kastrinakis, A. D. Tourvas, G. Laskaris, and V. G. Gorgoulis, “Advances in the biology of oral cancer,” Oral Oncology, vol. 43, no. 6, pp. 523–534, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Brown, D. Strathdee, S. Bryson, W. Lambie, and A. Balmain, “The malignant capacity of skin tumours induced by expression of a mutant H-ras transgene depends on the cell type targeted,” Current Biology, vol. 8, no. 9, pp. 516–524, 1998. View at Google Scholar · View at Scopus
  17. R. J. Akhurst and A. Balmain, “Genetic events and the role of TGFβ in epithelial tumour progression,” Journal of Pathology, vol. 187, no. 1, pp. 82–90, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Caulin, T. Nguyen, G. A. Lang et al., “An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations,” Journal of Clinical Investigation, vol. 117, no. 7, pp. 1893–1901, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. W. Cui, D. J. Fowlis, S. Bryson et al., “TGFß1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice,” Cell, vol. 86, no. 4, pp. 531–542, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Portella, S. A. Cumming, J. Liddell et al., “Transforming growth factor ß is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion,” Cell Growth and Differentiation, vol. 9, no. 5, pp. 393–404, 1998. View at Google Scholar · View at Scopus
  21. R. Derynck, R. J. Akhurst, and A. Balmain, “TGF-β signaling in tumor suppression and cancer progression,” Nature Genetics, vol. 29, no. 2, pp. 117–129, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Moreno-Bueno, F. Portillo, and A. Cano, “Transcriptional regulation of cell polarity in EMT and cancer,” Oncogene, vol. 27, no. 55, pp. 6958–6969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Han, S.-L. Lu, A. G. Li et al., “Distinct mechanisms of TGF-ß1-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis,” Journal of Clinical Investigation, vol. 115, no. 7, pp. 1714–1723, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Kalluri and R. A. Weinberg, “The basics of epithelial-mesenchymal transition,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1420–1428, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Bierie and H. L. Moses, “Tumour microenvironment: TGFβ: the molecular Jekyll and Hyde of cancer,” Nature Reviews Cancer, vol. 6, no. 7, pp. 506–520, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. N. Moghal and P. W. Sternberg, “Multiple positive and negative regulators of signaling by the EGF-receptor,” Current Opinion in Cell Biology, vol. 11, no. 2, pp. 190–196, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. O. Rho, L. M. Beltran, I. B. Gimenez-Conti, and J. DiGiovanni, “Altered expression of the epidermal growth factor receptor and transforming growth factor-α during multistage skin carcinogenesis in SENCAR mice,” Molecular Carcinogenesis, vol. 11, no. 1, pp. 19–28, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Samarakoon, C. E. Higgins, S. P. Higgins, and P. J. Higgins, “TGF-β1-induced expression of the poor prognosis SERPINE1/PAI-1 gene requires EGFR signaling: a new target for anti-EGFR therapy,” Journal of Oncology, vol. 2009, Article ID 342391, 6 pages, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. M. M. Murillo, G. del Castillo, A. Sánchez, M. Fernández, and I. Fabregat, “Involvement of EGF receptor and c-Src in the survival signals induced by TGF-β1 in hepatocytes,” Oncogene, vol. 24, no. 28, pp. 4580–4587, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-K. Joo, H.-S. Kim, J.-Y. Park, Y. Seomun, M.-J. Son, and J.-T. Kim, “Ligand release-independent transactivation of epidermal growth factor receptor by transforming growth factor-β involves multiple signaling pathways,” Oncogene, vol. 27, no. 5, pp. 614–628, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. P. O-Charoenrat, P. Rhys-Evans, H. Modjtahedi, W. Court, G. Box, and S. Eccles, “Overexpression of epidermal growth factor receptor in human head and neck squamous carcinoma cell lines correlates with matrix metalloproteinase-9 expression and in vitro invasion,” International Journal of Cancer, vol. 89, no. 2, pp. 307–317, 2000. View at Google Scholar · View at Scopus
  32. P. O-charoenrat, P. H. Rhys-Evans, D. J. Archer, and S. A. Eccles, “C-erbB receptors in squamous cell carcinomas of the head and neck: clinical significance and correlation with matrix metalloproteinases and vascular endothelial growth factors,” Oral Oncology, vol. 38, no. 1, pp. 73–80, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Zavadil and E. P. Böttinger, “TGF-β and epithelial-to-mesenchymal transitions,” Oncogene, vol. 24, no. 37, pp. 5764–5774, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Zavadil, M. Bitzer, D. Liang et al., “Genetic programs of epithelial cell plasticity directed by transforming growth factor-ß,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 12, pp. 6686–6691, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. C. E. Wilkins-Port, Q. Ye, J. E. Mazurkiewicz, and P. J. Higgins, “TGF-β1 + EGF-initiated invasive potential in transformed human keratinocytes is coupled to a plasmin/MMP-10/MMP-1-dependent collagen remodeling axis: role for PAI-1,” Cancer Research, vol. 69, no. 9, pp. 4081–4091, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. S. A. Mani, W. Guo, M.-J. Liao et al., “The epithelial-mesenchymal transition generates cells with properties of stem cells,” Cell, vol. 133, no. 4, pp. 704–715, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Yang and R. A. Weinberg, “Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis,” Developmental Cell, vol. 14, no. 6, pp. 818–829, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Nindl, C. Dang, T. Forschner et al., “Identification of differentially expressed genes in cutaneous squamous cell carcinoma by microarray expression profiling,” Molecular Cancer, vol. 5, pp. 1–17, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Dang, M. Gottschling, K. Manning et al., “Identification of dysregulated genes in cutaneous squamous cell carcinoma.,” Oncology Reports, vol. 16, no. 3, pp. 513–519, 2006. View at Google Scholar · View at Scopus
  40. S. Akiyoshi, M. Ishii, N. Nemoto, M. Kawabata, H. Aburatani, and K. Miyazono, “Targets of transcriptional regulation by transforming growth factor-β: expression profile analysis using oligonucleotide arrays,” Japanese Journal of Cancer Research, vol. 92, no. 3, pp. 257–268, 2001. View at Google Scholar · View at Scopus
  41. G. Moreno-Bueno, E. Cubillo, D. Sarrió et al., “Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelial- mesenchymal transition,” Cancer Research, vol. 66, no. 19, pp. 9543–9556, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. P. A. Andreasen, L. Kjøller, L. Christensen, and M. J. Duffy, “The urokinase-type plasminogen activator system in cancer metastasis: a review,” International Journal of Cancer, vol. 72, no. 1, pp. 1–22, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Hundsdorfer, H. F. Zeilhofer, K. P. Bock, P. Dettmar, M. Schmitt, and H. H. Horch, “The prognostic importance of urinase type plasminogen activators (uPA) and plasminogen activator inhibitors (PAI-1) in the primary resection of oral squamous cell carcinoma,” Mund-, Kiefer- und Gesichtschirurgie, vol. 8, no. 3, pp. 173–179, 2004. View at Google Scholar · View at Scopus
  44. K. Annecke, M. Schmitt, U. Euler et al., “uPA and PAI-1 in breast cancer: review of their clinical utility and current validation in the prospective NNBC-3 trial,” Advances in Clinical Chemistry, vol. 45, pp. 31–45, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Harbeck, M. Schmitt, S. Paepke, H. Allgayer, and R. E. Kates, “Tumor-associated proteolytic factors uPA and PAI-1: critical appraisal of their clinical relevance in breast cancer and their integration into decision-support algorithms,” Critical Reviews in Clinical Laboratory Sciences, vol. 44, no. 2, pp. 179–201, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Vairaktaris, C. Yapijakis, Z. Serefoglou et al., “Plasminogen activator inhibitor-1 polymorphism is associated with increased risk for oral cancer,” Oral Oncology, vol. 42, no. 9, pp. 888–892, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. K. Bajou, V. Masson, R. D. Gerard et al., “The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin: implications for antiangiogenic strategies,” Journal of Cell Biology, vol. 152, no. 4, pp. 777–784, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Bajou, A. Noel, R. D. Gerard et al., “Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization,” Nature Medicine, vol. 4, no. 8, pp. 923–928, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. G. E. Davis, K. A. Pintar Allen, R. Salazar, and S. A. Maxwell, “Matrix metalloproteinase-1 and -9 activation by plasmin regulates a novel endothelial cell-mediated mechanism of collagen gel contraction and capillary tube regression in three-dimensional collagen matrices,” Journal of Cell Science, vol. 114, no. 5, pp. 917–930, 2001. View at Google Scholar · View at Scopus
  50. S. P. Higgins, R. Samarakoon, C. E. Higgins, J. Freytag, C. Wilkins-Port, and P. J. Higgins, “TGF-β1-induced expression of the anti-apoptotic PAI-1 protein requires EGFR signaling,” Cell Communication Insights, vol. 2, pp. 1–11, 2009. View at Google Scholar
  51. C. Maillard, M. Jost, M. U. Rømer et al., “Host plasminogen activator inhibitor-1 promotes human skin carcinoma progression in a stage-dependent manner,” Neoplasia, vol. 7, no. 1, pp. 57–66, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Bacharach, A. Itin, and E. Keshet, “Apposition-dependent induction of plasminogen activator inhibitor type 1 expression: a mechanism for balancing pericellular proteolysis during angiogenesis,” Blood, vol. 92, no. 3, pp. 939–945, 1998. View at Google Scholar · View at Scopus
  53. K. M. Providence, S. P. Higgins, A. Mullen, A. Battista, C. E. Higgins, and P. J. Higgins, “SERPINE1 (PAI-1) is deposited into keratinocyte migration “trails” and required for optimal monolayer wound repair,” Archives of Dermatological Research, vol. 300, no. 6, pp. 303–310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. C. E. Wilkins-Port, C. E. Higgins, J. Freytag, S. P. Higgins, J. A. Carlson, and P. J. Higgins, “PAI-1 is a critical upstream regulator of the TGF-β1/EGF-induced invasive phenotype in mutant p53 human cutaneous squamous cell carcinoma,” Journal of Biomedicine and Biotechnology, vol. 2007, pp. 1–8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Illemann, U. Hansen, H. J. Nielsen et al., “Leading-edge myofibroblasts in human colon cancer express plasminogen activator inhibitor-1,” American Journal of Clinical Pathology, vol. 122, no. 2, pp. 256–265, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. B. V. Offersen, B. S. Nielsen, G. Høyer-Hansen et al., “The myofibroblast is the predominant plasminogen activator inhibitor-1-expressing cell type in human breast carcinomas,” American Journal of Pathology, vol. 163, no. 5, pp. 1887–1899, 2003. View at Google Scholar · View at Scopus
  57. F. Maquerlot, S. Galiacy, M. Malo et al., “Dual role for plasminogen activator inhibitor type 1 as soluble and as matricellular regulator of epithelial alveolar cell wound healing,” American Journal of Pathology, vol. 169, no. 5, pp. 1624–1632, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Parrinello, J.-P. Coppe, A. Krtolica, and J. Campisi, “Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation,” Journal of Cell Science, vol. 118, no. 3, pp. 485–496, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Giannopoulou, S. C. Iszkula, C. Dai et al., “Distinctive role of Stat3 and Erk-1/2 activation in mediating interferon-? inhibition of TGF-ß1 action,” American Journal of Physiology, vol. 290, no. 5, pp. F1234–F1240, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Freytag, C. E. Wilkins-Port, C. E. Higgins, S. P. Higgins, R. Samarakoon, and P. J. Higgins, “PAI-1 mediates the TGF-β1+EGF-induced “scatter”-response in transformed human keratinocytes,” Journal of Investigative Dermatology. In press.
  61. M. Davies, M. Robinson, E. Smith, S. Huntley, S. Prime, and I. Paterson, “Induction of an epithelial to mesenchymal transition in human immortal and malignant keratinocytes by TGF-β1 involves MAPK, Smad and AP-1 signalling pathways,” Journal of Cellular Biochemistry, vol. 95, no. 5, pp. 918–931, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. D. Chin, G. M. Boyle, P. G. Parsons, and W. B. Coman, “What is transforming growth factor-beta (TGF-β)?” British Journal of Plastic Surgery, vol. 57, no. 3, pp. 215–221, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. C. H. Streuli, C. Schmidhauser, M. Kobrin, M. J. Bissell, and R. Derynck, “Extracellular matrix regulates expression of the TGF-β1 gene,” Journal of Cell Biology, vol. 120, no. 1, pp. 253–260, 1993. View at Publisher · View at Google Scholar · View at Scopus
  64. T. M. Vollberg Sr., M. D. George, and A. M. Jetten, “Induction of extracellular matrix gene expression in normal human keratinocytes by transforming growth factor β is altered by cellular differentiation,” Experimental Cell Research, vol. 193, no. 1, pp. 93–100, 1991. View at Google Scholar · View at Scopus
  65. N. E. Wikner, J. T. Elder, K. A. Persichitte, P. Mink, and R. A. F. Clark, “Transforming growth factor-β modulates plasminogen activator activity and plasminogen activator inhibitor type-1 expression in human keratinocytes in vitro,” Journal of Investigative Dermatology, vol. 95, no. 5, pp. 607–613, 1990. View at Google Scholar · View at Scopus
  66. K. Ahokas, J. Lohi, S. A. Illman et al., “Matrix metalloproteinase-21 is expressed epithelially during development and in cancer and is up-regulated by transforming growth factor-ß1 in keratinocytes,” Laboratory Investigation, vol. 83, no. 12, pp. 1887–1899, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Johansson, J. Westermarck, S. Leppä et al., “Collagenase 3 (matrix metalloproteinase 13) gene expression by HaCaT keratinocytes is enhanced by tumor necrosis factor a and transforming growth factor ß1,” Cell Growth and Differentiation, vol. 8, no. 2, pp. 243–250, 1997. View at Google Scholar · View at Scopus
  68. E. S. Kim, M. S. Kim, and A. Moon, “TGF-beta-induced upregulation of MMP-2 and MMP-9 depends on p38 MAPK, but not ERK signaling in MCF10A human breast epithelial cells.,” International Journal of Oncology, vol. 25, no. 5, pp. 1375–1382, 2004. View at Google Scholar · View at Scopus
  69. E.-S. Kim, M.-S. Kim, and A. Moon, “Transforming growth factor (TGF)-β in conjunction with H-ras activation promotes malignant progression of MCF10A breast epithelial cells,” Cytokine, vol. 29, no. 2, pp. 84–91, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. H.-S. Kim, T. Shang, Z. Chen, S. C. Pflugfelder, and D.-Q. Li, “TGF-β1 stimulates production of gelatinase (MMP-9), collagenases (MMP-1, -13) and stromelysins (MMP-3, -10, -11) by human corneal epithelial cells,” Experimental Eye Research, vol. 79, no. 2, pp. 263–274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. H. G. Munshi, Y. I. Wu, S. Mukhopadhyay et al., “Differential regulation of membrane type 1-matrix metalloproteinase activity by ERK 1/2- and p38 MAPK-modulated tissue inhibitor of metalloproteinases 2 expression controls transforming growth factor-ß1-induced pericellular collagenolysis,” Journal of Biological Chemistry, vol. 279, no. 37, pp. 39042–39050, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. L. J. Windsor, H. Grenett, B. Birkedal-Hansen, M. K. Bodden, J. A. Engler, and H. Birkedal-Hansen, “Cell type-specific regulation of SL-1 and SL-2 genes. Induction of the SL- 2 gene but not the SL-1 gene by human keratinocytes in response to cytokines and phorbolesters,” Journal of Biological Chemistry, vol. 268, no. 23, pp. 17341–17347, 1993. View at Google Scholar · View at Scopus
  73. M. Madlener, C. Mauch, W. Conca, M. Brauchle, W. C. Parks, and S. Werner, “Regulation of the expression of stromelysin-2 by growth factors in keratinocytes: implications for normal and impaired wound healing,” Biochemical Journal, vol. 320, no. 2, pp. 659–664, 1996. View at Google Scholar · View at Scopus
  74. S. Chakraborti, M. Mandal, S. Das, A. Mandal, and T. Chakraborti, “Regulation of matrix metalloproteinases. An overview,” Molecular and Cellular Biochemistry, vol. 253, no. 1-2, pp. 269–285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. P. O-charoenrat, P. H. Rhys-Evans, and S. A. Eccles, “Expression of matrix metalloproteinases and their inhibitors correlates with invasion and metastasis in squamous cell carcinoma of the head and neck,” Archives of Otolaryngology, vol. 127, no. 7, pp. 813–820, 2001. View at Google Scholar · View at Scopus
  76. U. Impola, V. J. Uitto, J. Hietanen et al., “Differential expression of matrilysin-I (MMP-7), 92 kD gelatinase (MMP-9), and metalloelastase (MMP-12) in oral verrucous and squamous cell cancer,” Journal of Pathology, vol. 202, no. 1, pp. 14–22, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. E. Kerkelä, R. Ala-aho, L. Jeskanen et al., “Differential patterns of stromelysin-2 (MMP-10) and MT1-MMP (MMP-14) expression in epithelial skin cancers,” British Journal of Cancer, vol. 84, no. 5, pp. 659–669, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. R. Mathew, R. Khanna, R. Kumar, M. Mathur, N. K. Shukla, and R. Ralhan, “Stromelysin-2 overexpression in human esophageal squamous cell carcinoma: potential clinical implications,” Cancer Detection and Prevention, vol. 26, no. 3, pp. 222–228, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Krampert, W. Bloch, T. Sasaki et al., “Activities of the matrix metalloproteinase stromelysin-2 (MMP-10) in matrix degradation and keratinocyte organization in wounded skin,” Molecular Biology of the Cell, vol. 15, no. 12, pp. 5242–5254, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Uttamsingh, X. Bao, K. T. Nguyen et al., “Synergistic effect between EGF and TGF-ß1 in inducing oncogenic properties of intestinal epithelial cells,” Oncogene, vol. 27, no. 18, pp. 2626–2634, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. F.-C. Hsieh, G. Cheng, and J. Lin, “Evaluation of potential Stat3-regulated genes in human breast cancer,” Biochemical and Biophysical Research Communications, vol. 335, no. 2, pp. 292–299, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Itoh, T. Murata, T. Suzuki et al., “Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells,” Oncogene, vol. 25, no. 8, pp. 1195–1204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. N. Sumita, T. Bito, K. Nakajima, and C. Nishigori, “Stat3 activation is required for cell proliferation and tumorigenesis but not for cell viability in cutaneous squamous cell carcinoma cell lines,” Experimental Dermatology, vol. 15, no. 4, pp. 291–299, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Suiqing, Z. Min, and C. Lirong, “Overexpression of phosphorylated-STAT3 correlated with the invasion and metastasis of cutaneous squamous cell carcinoma,” Journal of Dermatology, vol. 32, no. 5, pp. 354–360, 2005. View at Google Scholar · View at Scopus
  85. S. M. Kutz, C. E. Higgins, R. Samarakoon et al., “TGF-ß1-induced PAI-1 expression is E box/USF-dependent and requires EGFR signaling,” Experimental Cell Research, vol. 312, no. 7, pp. 1093–1105, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. R. Samarakoon, C. E. Higgins, S. P. Higgins, S. M. Kutz, and P. J. Higgins, “Plasminogen activator inhibitor type-1 gene expression and induced migration in TGF-β1-stimulated smooth muscle cells is pp60csrc/MEK-dependent,” Journal of Cellular Physiology, vol. 204, no. 1, pp. 236–246, 2005. View at Publisher · View at Google Scholar · View at Scopus
  87. P. P.-C. Hu, X. Shen, D. Huang, Y. Liu, C. Counter, and X.-F. Wang, “The MEK pathway is required for stimulation of p21(WAF1/CIP1) by transforming growth factor-β,” Journal of Biological Chemistry, vol. 274, no. 50, pp. 35381–35387, 1999. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Sato, K. Kawai-Kowase, H. Sato et al., “c-Src and hydrogen peroxide mediate transforming growth factor-ß1-induced smooth muscle cell-gene expression in 10T1/2 cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 2, pp. 341–347, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Oft, J. Peli, C. Rudaz, H. Schwarz, H. Beug, and E. Reichmann, “TGF-β1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells,” Genes and Development, vol. 10, no. 19, pp. 2462–2477, 1996. View at Google Scholar · View at Scopus
  90. M. Oft, R. J. Akhurst, and A. Balmain, “Metastasis is driven by sequential elevation of H-ras and Smad2 levels,” Nature Cell Biology, vol. 4, no. 7, pp. 487–494, 2002. View at Google Scholar · View at Scopus
  91. J. S. Biscardi, M. C. Maa, D. A. Tice, M. E. Cox, T. H. Leu, and S. J. Parsons, “c-Src-mediated phosphorylation of the epidermal growth factor receptor on tyr 845 and tyr 1101 is associated with modulation of receptor function,” Journal of Biological Chemistry, vol. 274, pp. 8335–8343, 1999. View at Google Scholar
  92. L. M. Beaulieu, B. R. Whitley, T. F. Wiesner et al., “Breast cancer and metabolic syndrome linked through the plasminogen activator inhibitor-1 cycle,” BioEssays, vol. 29, no. 10, pp. 1029–1038, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Moro, L. Dolce, S. Cabodi et al., “Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines,” Journal of Biological Chemistry, vol. 277, no. 11, pp. 9405–9414, 2002. View at Publisher · View at Google Scholar · View at Scopus
  94. C. K. Miranti and J. S. Brugge, “Sensing the environment: a historical perspective on integrin signal transduction,” Nature Cell Biology, vol. 4, no. 4, pp. E83–E90, 2002. View at Publisher · View at Google Scholar · View at Scopus
  95. J.-T. Kim and C.-K. Joo, “Involvement of cell-cell interactions in the rapid stimulation of Cas tyrosine phosphorylation and Src kinase activity by transforming growth factor-β1,” Journal of Biological Chemistry, vol. 277, no. 35, pp. 31938–31948, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. F. W. Khwaja, P. Svoboda, M. Reed, J. Pohl, B. Pyrzynska, and E. G. Van Meir, “Proteomic identification of the wt-p53-regulated tumor cell secretome,” Oncogene, vol. 25, no. 58, pp. 7650–7661, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Piccolo, “p53 regulation orchestrates the TGF-β response,” Cell, vol. 133, no. 5, pp. 767–769, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Cordenonsi, S. Dupont, S. Maretto, A. Insinga, C. Imbriano, and S. Piccolo, “Links between tumor suppressors: p53 is required for TGF-β gene responses by cooperating with Smads,” Cell, vol. 113, no. 3, pp. 301–314, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. M. Cordenonsi, M. Montagner, M. Adorno et al., “Integration of TGF-ß and Ras/MAPK signaling through p53 phosphorylation,” Science, vol. 315, no. 5813, pp. 840–843, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Dupont, L. Zacchigna, M. Adorno et al., “Convergence of p53 and TGFß signaling networks,” Cancer Letters, vol. 213, no. 2, pp. 129–138, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. C. Kunz, S. Pebler, J. Otte, and D. von der Ahe, “Differential regulation of plasminogen activator and inhibitor gene transcription by the tumor suppressor p53,” Nucleic Acids Research, vol. 23, no. 18, pp. 3710–3717, 1995. View at Google Scholar · View at Scopus
  102. T. Riley, E. Sontag, P. Chen, and A. Levine, “Transcriptional control of human p53-regulated genes,” Nature Reviews Molecular Cell Biology, vol. 9, no. 5, pp. 402–412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Shetty, P. Shetty, S. Idell, T. Velusamy, Y. P. Bhandary, and R. S. Shetty, “Regulation of plasminogen activator inhibitor-1 expression by tumor suppressor protein p53,” Journal of Biological Chemistry, vol. 283, no. 28, pp. 19570–19580, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. R. R. Allen, L. Qi, and P. J. Higgins, “Upstream stimulatory factor regulates E box-dependent PAI-1 transcription in human epidermal keratinocytes,” Journal of Cellular Physiology, vol. 203, no. 1, pp. 156–165, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. D. E. Fisher, L. A. Parent, and P. A. Sharp, “Myc/Max and other helix-loop-helix/leucine zipper proteins bend DNA toward the minor groove,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 24, pp. 11779–11783, 1992. View at Publisher · View at Google Scholar · View at Scopus
  106. N. Scheinfeld and V. DeLeo, “Etiological factors in skin cancers: environmental and biological,” in Cancer of the Skin, D. S. Rigel, R. J. Friedman, L. M. Dzubow, D. S. Reintgen, J.-C. Bystryn, and R. Marks, Eds., pp. 61–70, Elsevier, Philadelphia, Pa, USA, 2005. View at Google Scholar
  107. R. M. Kortlever, P. J. Higgins, and R. Bernards, “Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence,” Nature Cell Biology, vol. 8, no. 8, pp. 878–884, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. R. D. Balsara, F. J. Castellino, and V. A. Ploplis, “A novel function of plasminogen activator inhibitor-1 in modulation of the AKT pathway in wild-type and plasminogen activator inhibitor-1-deficient endothelial cells,” Journal of Biological Chemistry, vol. 281, no. 32, pp. 22527–22536, 2006. View at Publisher · View at Google Scholar · View at Scopus
  109. R. M. Kortlever, J. H. Nijwening, and R. Bernards, “Transforming growth factor-β requires its target plasminogen activator inhibitor-1 for cytostatic activity,” Journal of Biological Chemistry, vol. 283, no. 36, pp. 24308–24313, 2008. View at Publisher · View at Google Scholar · View at Scopus