Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 964842, 8 pages
http://dx.doi.org/10.1155/2015/964842
Review Article

Wnt/β-Catenin Signaling Pathway in Skin Carcinogenesis and Therapy

1Institute of Tropical Medicine, Third Military Medical University, 30 Gaotanyan Street, Chongqing 400038, China
2Department of Hematology, Southwest Hospital, Third Military Medical University, 30 Gaotanyan Street, Chongqing 400038, China
3Center for Engineering in Medicine, Department of Surgery, Massachusetts General Hospital, Harvard Medical School, 51 Blossom Street, Boston, MA 02114, USA

Received 9 January 2015; Revised 6 April 2015; Accepted 21 April 2015

Academic Editor: Pascale Quatresooz

Copyright © 2015 Jing Li 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. R. Nusse and H. E. Varmus, “Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome,” Cell, vol. 31, no. 1, pp. 99–109, 1982. View at Publisher · View at Google Scholar · View at Scopus
  2. J. D. Holland, A. Klaus, A. N. Garratt, and W. Birchmeier, “Wnt signaling in stem and cancer stem cells,” Current Opinion in Cell Biology, vol. 25, no. 2, pp. 254–264, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Wend, J. D. Holland, U. Ziebold, and W. Birchmeier, “Wnt signaling in stem and cancer stem cells,” Seminars in Cell & Developmental Biology, vol. 21, no. 8, pp. 855–863, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. R. T. Moon, A. D. Kohn, G. V. De Ferrari, and A. Kaykas, “Wnt and β-catenin signalling: diseases and therapies,” Nature Reviews Genetics, vol. 5, no. 9, pp. 691–701, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Nusse, “Wnt signaling and stem cell control,” Cell Research, vol. 18, no. 5, pp. 523–527, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. S. M. An, Q. P. Ding, and L.-S. Li, “Stem cell signaling as a target for novel drug discovery: recent progress in the WNT and Hedgehog pathways,” Acta Pharmacologica Sinica, vol. 34, no. 6, pp. 777–783, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. F. M. Watt, C. L. Celso, and V. Silva-Vargas, “Epidermal stem cells: an update,” Current Opinion in Genetics & Development, vol. 16, no. 5, pp. 518–524, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. D. D. Bikle, “Vitamin D and the skin: physiology and pathophysiology,” Reviews in Endocrine & Metabolic Disorders, vol. 13, no. 1, pp. 3–19, 2012. View at Publisher · View at Google Scholar
  9. H. J. Snippert, A. Haegebarth, M. Kasper et al., “Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin,” Science, vol. 327, no. 5971, pp. 1385–1389, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Huelsken, R. Vogel, B. Erdmann, G. Cotsarelis, and W. Birchmeier, “β-catenin controls hair follicle morphogenesis and stem cell differentiation in the skin,” Cell, vol. 105, no. 4, pp. 533–545, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Wend, J. D. Holland, U. Ziebold, and W. Birchmeier, “Wnt signaling in stem and cancer stem cells,” Seminars in Cell and Developmental Biology, vol. 21, no. 8, pp. 855–863, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Huelsken, R. Vogel, B. Erdmann, G. Cotsarelis, and W. Birchmeier, “β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin,” Cell, vol. 105, no. 4, pp. 533–545, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Grigoryan, P. Wend, A. Klaus, and W. Birchmeier, “Deciphering the function of canonical Wnt signals in development and disease: Conditional loss- and gain-of-function mutations of beta-catenin in mice,” Genes & Development, vol. 22, no. 17, pp. 2308–2341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Posthaus, L. Williamson, D. Baumann et al., “β-catenin is not required for proliferation and differentiation of epidemal mouse keratinocytes,” Journal of Cell Science, vol. 115, no. 23, pp. 4587–4595, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Alonso and E. Fuchs, “Stem cells in the skin: waste not, Wnt not,” Genes & Development, vol. 17, no. 10, pp. 1189–1200, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Blanpain and E. Fuchs, “Epidermal homeostasis: a balancing act of stem cells in the skin,” Nature Reviews Molecular Cell Biology, vol. 10, no. 3, pp. 207–217, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Maretto, M. Cordenonsi, S. Dupont et al., “Mapping Wnt/β-catenin signaling during mouse development and in colorectal tumors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 6, pp. 3299–3304, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Reddy, T. Andl, A. Bagasra et al., “Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis,” Mechanisms of Development, vol. 107, no. 1-2, pp. 69–82, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. O. Shakhova, “Neural crest stem cells in melanoma development,” Current Opinion in Oncology, vol. 26, no. 2, pp. 215–221, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. G. M. Kruger, J. T. Mosher, S. Bixby, N. Joseph, T. Iwashita, and S. J. Morrison, “Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness,” Neuron, vol. 35, no. 4, pp. 657–669, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. J. G. Toma, M. Akhavan, K. J. L. Fernandes et al., “Isolation of multipotent adult stem cells from the dermis of mammalian skin,” Nature Cell Biology, vol. 3, no. 9, pp. 778–784, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. K. J. L. Fernandes, I. A. McKenzie, P. Mill et al., “A dermal niche for multipotent adult skin-derived precursor cells,” Nature Cell Biology, vol. 6, no. 11, pp. 1082–1093, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Sieber-Blum, M. Grim, Y. F. Hu, and V. Szeder, “Pluripotent neural crest stem cells in the adult hair follicle,” Developmental Dynamics, vol. 231, no. 2, pp. 258–269, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Belicchi, F. Pisati, R. Lopa et al., “Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain,” Journal of Neuroscience Research, vol. 77, no. 4, pp. 475–486, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. J. G. Toma, I. A. McKenzie, D. Bagli, and F. D. Miller, “Isolation and characterization of multipotent skin-derived precursors from human skin,” Stem Cells, vol. 23, no. 6, pp. 727–737, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. C. E. Wong, C. Paratore, M. T. Dours-Zimmermann et al., “Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin,” Journal of Cell Biology, vol. 175, no. 6, pp. 1005–1015, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. A. P. W. Johnston, S. Naska, K. Jones, H. Jinno, D. R. Kaplan, and F. D. Miller, “Sox2-mediated regulation of adult neural crest precursors and skin repair,” Stem Cell Reports, vol. 1, no. 1, pp. 38–45, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Kumar and J. P. Brockes, “Nerve dependence in tissue, organ, and appendage regeneration,” Trends in Neurosciences, vol. 35, no. 11, pp. 691–699, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. J. F. Crane and P. A. Trainor, “Neural crest stem and progenitor cells,” Annual Review of Cell and Developmental Biology, vol. 22, pp. 267–286, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. K. W. Vance and C. R. Goding, “The transcription network regulating melanocyte development and melanoma,” Pigment Cell Research, vol. 17, no. 4, pp. 318–325, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Larue, M. Kumasaka, and C. R. Goding, “β-catenin in the melanocyte lineage,” Pigment Cell Research, vol. 16, no. 3, pp. 312–317, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. R. I. Dorsky, D. W. Raible, and R. T. Moon, “Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway,” Genes and Development, vol. 14, no. 2, pp. 158–162, 2000. View at Google Scholar · View at Scopus
  33. I. M. Bachmann, O. Straume, H. E. Puntervoll, M. B. Kalvenes, and L. A. Akslen, “Importance of P-cadherin, β-catenin, and Wnt5a/Frizzled for progression of melanocytic tumors and prognosis in cutaneous melanoma,” Clinical Cancer Research, vol. 11, no. 24, pp. 8606–8614, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Kageshita, C. V. Hamby, T. Ishihara, K. Matsumoto, T. Saida, and T. Ono, “Loss of β-catenin expression associated with disease progression in malignant melanoma,” British Journal of Dermatology, vol. 145, no. 2, pp. 210–216, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. G. M. Mælandsmo, R. Holm, J. M. Nesland, Ø. Fodstad, and V. A. Flørenes, “Reduced β-catenin expression in the cytoplasm of advanced-stage superficial spreading malignant melanoma,” Clinical Cancer Research, vol. 9, no. 9, pp. 3383–3388, 2003. View at Google Scholar · View at Scopus
  36. S. Vauclair, M. Nicolas, Y. Barrandon, and F. Radtke, “Notch1 is essential for postnatal hair follicle development and homeostasis,” Developmental Biology, vol. 284, no. 1, pp. 184–193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. V. Devgan, C. Mammucari, S. E. Millar, C. Brisken, and G. P. Dotto, “p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation,” Genes and Development, vol. 19, no. 12, pp. 1485–1495, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Shah, M. N. Islam, S. Dakshanamurthy et al., “The molecular basis of vitamin D receptor and β-catenin crossregulation,” Molecular Cell, vol. 21, no. 6, pp. 799–809, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. F. M. Watt, C. L. Celso, and V. Silva-Vargas, “Epidermal stem cells: an update,” Current Opinion in Genetics and Development, vol. 16, no. 5, pp. 518–524, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. F. M. Watt and C. A. Collins, “Role of β-catenin in epidermal stem cell expansion, lineage selection, and cancer,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 73, pp. 503–512, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. V. Silva-Vargas, C. Lo Celso, A. Giangreco et al., “β-catenin and hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells,” Developmental Cell, vol. 9, no. 1, pp. 121–131, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. V. P. I. Vidal, M.-C. Chaboissier, S. Lützkendorf et al., “Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment,” Current Biology, vol. 15, no. 15, pp. 1340–1351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Niemann and F. M. Watt, “Designer skin: Lineage commitment in postnatal epidermis,” Trends in Cell Biology, vol. 12, no. 4, pp. 185–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. E. Fuchs, T. Tumbar, and G. Guasch, “Socializing with the neighbors: stem cells and their niche,” Cell, vol. 116, no. 6, pp. 769–778, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Muranushi, C. M. Olsen, N. Pandeya, and A. C. Green, “Aspirin and nonsteroidal anti-inflammatory drugs can prevent cutaneous squamous cell carcinoma: a systematic review and meta-analysis,” Journal of Investigative Dermatology, vol. 135, no. 4, pp. 975–983, 2014. View at Publisher · View at Google Scholar
  46. I. Malanchi, H. Peinado, D. Kassen et al., “Cutaneous cancer stem cell maintenance is dependent on β-catenin signalling,” Nature, vol. 452, no. 7187, pp. 650–653, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Liu, S. Pan, M. H. Hsieh et al., “Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 50, pp. 20224–20229, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Larue and V. Delmas, “The WNT/beta-catenin pathway in melanoma,” Frontiers in Bioscience, vol. 11, no. 1, pp. 733–742, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Hecht, K. Vleminckx, M. P. Stemmler, F. Van Roy, and R. Kemler, “The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates,” The EMBO Journal, vol. 19, no. 8, pp. 1839–1850, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Kramps, O. Peter, E. Brunner et al., “Wnt/Wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear β-catenin-TCF complex,” Cell, vol. 109, no. 1, pp. 47–60, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Hoffmans, R. Städeli, and K. Basler, “Pygopus and legless provide essential transcriptional coactivator functions to Armadillo/β-catenin,” Current Biology, vol. 15, no. 13, pp. 1207–1211, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. K. H. Emami, C. Nguyen, H. Ma et al., “A small molecule inhibitor of β-catenin/CREB-binding protein transcription,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 34, pp. 12682–12687, 2004. View at Publisher · View at Google Scholar
  53. M. McMillan and M. Kahn, “Investigating Wnt signaling: a chemogenomic safari,” Drug Discovery Today, vol. 10, no. 21, pp. 1467–1474, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Takahashi-Yanaga and M. Kahn, “Targeting Wnt signaling: can we safely eradicate cancer stem cells?” Clinical Cancer Research, vol. 16, no. 12, pp. 3153–3162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Tataroglu, T. Karabacak, and D. D. Apa, “β-catenin and CD44 expression in keratoacanthoma and squamous cell carcinoma of the skin,” Tumori, vol. 93, no. 3, pp. 284–289, 2007. View at Google Scholar · View at Scopus
  56. C. Doglioni, S. Piccinin, S. Demontis et al., “Alterations of beta-catenin pathway in non-melanoma skin tumors: loss of α-ABC nuclear reactivity correlates with the presence of β-catenin gene mutation,” The American Journal of Pathology, vol. 163, no. 6, pp. 2277–2287, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. M. El-Bahrawy, N. El-Masry, M. Alison, R. Poulsom, and M. Fallowfield, “Expression of beta-catenin in basal cell carcinoma,” British Journal of Dermatology, vol. 148, no. 5, pp. 964–970, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. M. C. Clouser, D. J. Roe, J. A. Foote, and R. B. Harris, “Effect of non-steroidal anti-inflammatory drugs on non-melanoma skin cancer incidence in the SKICAP-AK trial,” Pharmacoepidemiology and Drug Safety, vol. 18, no. 4, pp. 276–283, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. C. Curiel-Lewandrowski, T. Nijsten, M. L. Gomez, L. M. Hollestein, M. B. Atkins, and R. S. Stern, “Long-term use of nonsteroidal anti-inflammatory drugs decreases the risk of cutaneous melanoma: results of a united states case–control study,” Journal of Investigative Dermatology, vol. 131, no. 7, pp. 1460–1468, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. D. J. Bjorkman, “Current status of nonsteroidal anti-inflammatory drug (NSAID) use in the United States: risk factors and frequency of complications,” The American Journal of Medicine, vol. 107, no. 6, pp. 3S–8S, 1999. View at Google Scholar · View at Scopus
  61. G. A. FitzGerald, “Coxibs and cardiovascular disease,” The New England Journal of Medicine, vol. 351, no. 17, pp. 1709–1711, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. J. M. Scheiman and A. M. Fendrick, “Summing the risk of NSAID therapy,” The Lancet, vol. 369, no. 9573, pp. 1580–1581, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. N. M. Davies, A. G. Roøseth, C. B. Appleyard et al., “NO-naproxen vs. naproxen: ulcerogenic, analgesic and anti-inflammatory effects,” Alimentary Pharmacology and Therapeutics, vol. 11, no. 1, pp. 69–79, 1997. View at Publisher · View at Google Scholar · View at Scopus
  64. J. L. Wallace, B. Reuter, C. Cicala, W. McKnight, M. B. Grisham, and G. Cirino, “Novel nonsteroidal anti-inflammatory drug derivatives with markedly reduced ulcerogenic properties in the rat,” Gastroenterology, vol. 107, no. 1, pp. 173–179, 1994. View at Google Scholar · View at Scopus
  65. S. Fiorucci, L. Santucci, P. Gresele, R. M. Faccino, P. Del Soldato, and A. Morelli, “Gastrointestinal safety of NO-aspirin (NCX-4016) in healthy human volunteers: a proof of concept endoscopic study,” Gastroenterology, vol. 124, no. 3, pp. 600–607, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Fiorucci, L. Santucci, J. L. Wallace et al., “Interaction of a selective cyclooxygenase-2 inhibitor with aspirin and NO-releasing aspirin in the human gastric mucosa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 19, pp. 10937–10941, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Reinau, C. Surber, S. S. Jick, and C. R. Meier, “Nonsteroidal anti-inflammatory drugs and the risk of nonmelanoma skin cancer,” International Journal of Cancer, vol. 137, no. 1, pp. 144–153, 2015. View at Publisher · View at Google Scholar
  68. D. D. Bikle, Y. Oda, C.-L. Tu, and Y. Jiang, “Novel mechanisms for the vitamin D receptor (VDR) in the skin and in skin cancer,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 148, pp. 47–51, 2015. View at Publisher · View at Google Scholar
  69. L. Hu, D. D. Bikle, and Y. Oda, “Reciprocal role of vitamin D receptor on β-catenin regulated keratinocyte proliferation and differentiation,” The Journal of Steroid Biochemistry & Molecular Biology, vol. 144, pp. 237–241, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. Y. Jiang, C. Prunier, and P. H. Howe, “The inhibitory effects of Disabled-2 (Dab2) on Wnt signaling are mediated through Axin,” Oncogene, vol. 27, no. 13, pp. 1865–1875, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. N. Pendás-Franco, Ó. Aguilera, F. Pereira, J. M. González-Sancho, and A. Muñoz, “Vitamin D and Wnt/β-catenin pathway in colon cancer: role and regulation of DICKKOPF genes,” Anticancer Research, vol. 28, no. 5, pp. 2613–2623, 2008. View at Google Scholar · View at Scopus
  72. D. N. Syed, F. Afaq, N. Maddodi et al., “Inhibition of human melanoma cell growth by the dietary flavonoid fisetin is associated with disruption of Wnt/β-catenin signaling and decreased mitf levels,” Journal of Investigative Dermatology, vol. 131, no. 6, pp. 1291–1299, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Larue and F. Beermann, “Cutaneous melanoma in genetically modified animals,” Pigment Cell Research, vol. 20, no. 6, pp. 485–497, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. G. J. Walker, H. P. Soyer, T. Terzian, and N. F. Box, “Modelling melanoma in mice,” Pigment Cell & Melanoma Research, vol. 24, no. 6, pp. 1158–1176, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. D. Dankort, D. P. Curley, R. A. Cartlidge et al., “Braf(V600E) cooperates with Pten loss to induce metastatic melanoma,” Nature Genetics, vol. 41, no. 5, pp. 544–552, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. W. E. Damsky, D. P. Curley, M. Santhanakrishnan et al., “β-catenin signaling controls metastasis in Braf-activated Pten-deficient melanomas,” Cancer Cell, vol. 20, no. 6, pp. 741–754, 2011. View at Publisher · View at Google Scholar · View at Scopus