About this Journal Submit a Manuscript Table of Contents
Journal of Skin Cancer
Volume 2011 (2011), Article ID 614097, 10 pages
http://dx.doi.org/10.1155/2011/614097
Review Article

Tumor Suppressor Function of CYLD in Nonmelanoma Skin Cancer

Molecular Tumor Pathology, Department of Laboratory Medicine, Lund University, Skåne University Hospital, 205 02 Malmö, Sweden

Received 13 July 2011; Revised 15 September 2011; Accepted 21 September 2011

Academic Editor: Giuseppe Argenziano

Copyright © 2011 K. C. Masoumi 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. A. M. Weissman, “Themes and variations on ubiquitylation,” Nature Reviews Molecular Cell Biology, vol. 2, no. 3, pp. 169–178, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. C. M. Pickart, “Mechanisms underlying ubiquitination,” Annual Review of Biochemistry, vol. 70, pp. 503–533, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. F. E. Reyes-Turcu, K. H. Ventii, and K. D. Wilkinson, “Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes,” Annual Review of Biochemistry, vol. 78, pp. 363–397, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. P. J. Biggs, R. Wooster, D. Ford et al., “Familial cylindromatosis (turban tumour syndrome) gene localised to chromosome 16q12-q13: evidence for its role as a tumour suppressor gene,” Nature Genetics, vol. 11, no. 4, pp. 441–443, 1995. View at Scopus
  5. G. R. Bignell, W. Warren, S. Seal et al., “Identification of the familial cylindromatosis tumour-suppressor gene,” Nature Genetics, vol. 25, no. 2, pp. 160–165, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. J. P. Welch, R. S. Wells, and C. B. Kerr, “Ancell-Spiegler cylindromas (turban tumours) and Brooke-Fordyce Trichoepitheliomas: evidence for a single genetic entity,” Journal of Medical Genetics, vol. 5, no. 1, pp. 29–35, 1968. View at Scopus
  7. S. Bowen, M. Gill, D. A. Lee et al., “Mutations in the CYLD gene in Brooke-Spiegler syndrome, familial cylindromatosis, and multiple familial trichoepithelioma: lack of genotype-phenotype correlation,” Journal of Investigative Dermatology, vol. 124, no. 5, pp. 919–920, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. R. Massoumi, “CYLD: a deubiquitination enzyme with multiple roles in cancer,” Future Oncology, vol. 7, no. 2, pp. 285–297, 2011. View at Publisher · View at Google Scholar · View at PubMed
  9. K. Moriwaki, D. Tsuruta, K. Sugawara, H. Kobayashi, R. Massoumi, and M. Ishii, “A role of CYLD in hair cycling mouse,” Journal of Investigative Dermatology, vol. 127, p. S107, 2007.
  10. R. Massoumi, “Ubiquitin chain cleavage: CYLD at work,” Trends in Biochemical Sciences, vol. 35, no. 7, pp. 392–399, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. D. Komander, C. J. Lord, H. Scheel et al., “The structure of the CYLD USP domain explains its specificity for Lys63-linked polyubiquitin and reveals a B box module,” Molecular Cell, vol. 29, no. 4, pp. 451–464, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. T. R. Brummelkamp, S. M. B. Nijman, A. M. G. Dirac, and R. Bernards, “Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-κB,” Nature, vol. 424, no. 6950, pp. 797–801, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. E. Trompouki, E. Hatzivassillou, T. Tsichritzis, H. Farmer, A. Ashworth, and G. Mosialos, “CYLD is a deubiquitinating enzyme that negatively regulates NF-κB activation by TNFR family members,” Nature, vol. 424, no. 6950, pp. 793–796, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. A. Kovalenko, C. Chable-Bessia, G. Cantarella, A. Israël, D. Wallach, and G. Courtois, “The tumour suppressor CYLD negatively regulates NF-κB signalling by deubiquitination,” Nature, vol. 424, no. 6950, pp. 801–805, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. G. Bonizzi, M. Bebien, D. C. Otero et al., “Activation of IKKα target genes depends on recognition of specific κB binding sites by RelB:p52 dimers,” EMBO Journal, vol. 23, no. 21, pp. 4202–4210, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. S. Ghosh and M. Karin, “Missing pieces in the NF-κB puzzle,” Cell, vol. 109, no. 2, pp. S81–S96, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. R. R. Shen and W. C. Hahn, “Emerging roles for the non-canonical IKKs in cancer,” Oncogene, vol. 30, no. 6, pp. 631–641, 2011. View at Publisher · View at Google Scholar · View at PubMed
  18. M. Van Hogerlinden, B. L. Rozell, L. Ährlund-Richter, and R. Toftgård, “Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-κB signaling,” Cancer Research, vol. 59, no. 14, pp. 3299–3303, 1999. View at Scopus
  19. M. Dajee, M. Lazarov, J. Y. Zhang et al., “NF-κB blockade and oncogenic Ras trigger invasive human epidermal neoplasia,” Nature, vol. 421, no. 6923, pp. 639–643, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. T. W. McKeithan, H. Ohno, and M. O. Diaz, “Identification of a transcriptional unit adjacent to the breakpoint in the 14;19 translocation of chronic lymphocytic leukemia,” Genes Chromosomes and Cancer, vol. 1, no. 3, pp. 247–255, 1990. View at Scopus
  21. P. C. Cogswell, D. C. Guttridge, W. K. Funkhouser, and A. S. Baldwin, “Selective activation of NF-κB subunits in human breast cancer: potential roles for NF-κB2/p52 and for Bcl-3,” Oncogene, vol. 19, no. 9, pp. 1123–1131, 2000. View at Scopus
  22. R. Massoumi, S. Kuphal, C. Hellerbrand et al., “Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma,” Journal of Experimental Medicine, vol. 206, no. 1, pp. 221–232, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. S. G. Park, C. Chung, H. Kang, J. Y. Kim, and G. Jung, “Up-regulation of cyclin D1 by HBx is mediated by NF-κB2/BCL3 complex through κB site of cyclin D1 promoter,” Journal of Biological Chemistry, vol. 281, no. 42, pp. 31770–31777, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. T. R. Bürglin, “The Hedgehog protein family,” Genome biology, vol. 9, no. 11, p. 241, 2008. View at Scopus
  25. R. L. Johnson, A. L. Rothman, J. Xie et al., “Human homolog of patched, a candidate gene for the basal cell nevus syndrome,” Science, vol. 272, no. 5268, pp. 1668–1671, 1996. View at Scopus
  26. M. Van den Heuvel and P. W. Ingham, “Smoothened encodes a receptor-like serpentine protein required for hedgehog signalling,” Nature, vol. 382, no. 6591, pp. 547–551, 1996. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. M. Katoh, M. Hirai, T. Sugimura, and M. Terada, “Cloning and characterization of MST, a novel (putative) serine/threonine kinase with SH3 domain,” Oncogene, vol. 10, no. 7, pp. 1447–1451, 1995. View at Scopus
  28. M. Varjosalo, M. Björklund, F. Cheng et al., “Application of active and kinase-deficient kinome collection for identification of kinases regulating Hedgehog signaling,” Cell, vol. 133, no. 3, pp. 537–548, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. K. W. Kinzler, S. H. Bigner, and D. D. Bigner, “Identification of an amplified, highly expressed gene in a human glioma,” Science, vol. 236, no. 4797, pp. 70–73, 1987.
  30. A. Ruiz i Altaba, C. Mas, and B. Stecca, “The Gli code: an information nexus regulating cell fate, stemness and cancer,” Trends in Cell Biology, vol. 17, no. 9, pp. 438–447, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. J. Jiang, “Regulation of Hh/Gli signaling by dual ubiquitin pathways,” Cell Cycle, vol. 5, no. 21, pp. 2457–2463, 2006. View at Scopus
  32. J. E. Hooper, D. Kent, and E. W. Bush, “Roadkill attenuates Hedgehog responses through degradation of Cubitus interruptus,” Development, vol. 133, no. 10, pp. 2001–2010, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. J. Jiang, Q. Zhang, L. Zhang, B. Wang, C. Y. Ou, and C. T. Chien, “A Hedgehog-induced BTB protein modulates Hedgehog signaling by degrading Ci/Gli transcription factor,” Developmental Cell, vol. 10, no. 6, pp. 719–729, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. A. Gulino, L. Di Marcotullio, E. Ferretti et al., “Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination,” Nature Cell Biology, vol. 8, no. 12, pp. 1415–1423, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. A. Gulino, G. Canettieri, L. Di Marcotullio et al., “Histone deacetylase and Cullin3-REN KCTD11 ubiquitin ligase interplay regulates Hedgehog signalling through Gli acetylation,” Nature Cell Biology, vol. 12, no. 2, pp. 132–142, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. M. Dorsch, Z. Jagani, E. L. Mora-Blanco et al., “Loss of the tumor suppressor Snf5 leads to aberrant activation of the Hedgehog-Gli pathway,” Nature Medicine, vol. 16, no. 12, pp. 1429–1434, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. B. Cox, J. Briscoe, and F. Ulloa, “SUMOylation by pias1 regulates the activity of the hedgehog dependent gli transcription factors,” PLoS ONE, vol. 5, no. 8, Article ID e11996, 2010. View at Publisher · View at Google Scholar · View at PubMed
  38. H. Hahn, C. Wicking, P. G. Zaphiropoulos et al., “Mutations of the human homolog of drosophila patched in the nevoid basal cell carcinoma syndrome,” Cell, vol. 85, no. 6, pp. 841–851, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. M. R. Gailani, M. Stahle-Backdahl, D. J. Leffell et al., “The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas,” Nature Genetics, vol. 14, no. 1, pp. 78–81, 1996. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. C. Li, S. Chi, and J. Xie, “Hedgehog signaling in skin cancers,” Cellular Signalling, vol. 23, no. 8, pp. 1235–1243, 2011. View at Publisher · View at Google Scholar · View at PubMed
  41. S. Kuphal, G. Shaw-Hallgren, M. Eberl, et al., “GLI1-dependent transcriptional repression of CYLD in basal cell carcinoma,” Oncogene, vol. 30, no. 44, pp. 4523–4530, 2011. View at Publisher · View at Google Scholar · View at PubMed
  42. X. Li, W. Deng, C. D. Nail et al., “Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation,” Oncogene, vol. 25, no. 4, pp. 609–621, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. M. Nilsson, A. B. Undèn, D. Krause et al., “Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 7, pp. 3438–3443, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. M. R. Gailani, S. J. Bale, D. J. Leffell et al., “Developmental defects in Gorlin syndrome related to a putative tumor suppressor gene on chromosome 9,” Cell, vol. 69, no. 1, pp. 111–117, 1992. View at Publisher · View at Google Scholar · View at Scopus
  45. A. G. Quinn, S. Sikkink, and J. L. Rees, “Delineation of two distinct deleted regions on chromosome 9 in human non- melanoma skin cancers,” Genes Chromosomes and Cancer, vol. 11, no. 4, pp. 222–225, 1994. View at Publisher · View at Google Scholar · View at Scopus
  46. N. Leonard, R. Chaggar, C. Jones, M. Takahashi, A. Nikitopoulou, and S. R. Lakhani, “Loss of heterozygosity at cylindromatosis gene locus, CYLD, in sporadic skin adnexal tumours,” Journal of Clinical Pathology, vol. 54, no. 9, pp. 689–692, 2001. View at Scopus
  47. D. V. Kazakov, J. Schaller, T. Vanecek, D. Kacerovska, and M. Michal, “Brooke-Spiegler syndrome: report of a case with a novel mutation in the CYLD gene and different types of somatic mutations in benign and malignant tumors,” Journal of Cutaneous Pathology, vol. 37, no. 8, pp. 886–890, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. M. Wolter, J. Reifenberger, C. Sommer, T. Ruzicka, and G. Reifenberger, “Mutations in the human homologue of the Drosophila segment polarity gene patched (PTCH) in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system,” Cancer Research, vol. 57, no. 13, pp. 2581–2585, 1997. View at Scopus
  49. D. V. Kazakov, T. Vanecek, J. Nemcova et al., “Spectrum of tumors with follicular differentiation in a patient with the clinical phenotype of multiple familial trichoepitheliomas: a clinicopathological and molecular biological study, including analysis of the CYLD and PTCH genes,” American Journal of Dermatopathology, vol. 31, no. 8, pp. 819–827, 2009. View at Publisher · View at Google Scholar · View at PubMed
  50. G. M. Brodeur, J. E. Minturn, R. Ho et al., “Trk receptor expression and inhibition in neuroblastomas,” Clinical Cancer Research, vol. 15, no. 10, pp. 3244–3250, 2009. View at Publisher · View at Google Scholar · View at PubMed
  51. M. W. Wooten, T. Geetha, J. R. Babu et al., “Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins,” Journal of Biological Chemistry, vol. 283, no. 11, pp. 6783–6789, 2008. View at Publisher · View at Google Scholar · View at PubMed
  52. T. Geetha, J. Jiang, and M. W. Wooten, “Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling,” Molecular Cell, vol. 20, no. 2, pp. 301–312, 2005. View at Publisher · View at Google Scholar · View at PubMed
  53. N. Rajan, R. Elliott, O. Clewes et al., “Dysregulated TRK signalling is a therapeutic target in CYLD defective tumours,” Oncogene, vol. 30, no. 41, pp. 4243–4260, 2011. View at Publisher · View at Google Scholar · View at PubMed
  54. N. Vasiljević, K. Andersson, K. Bjelkenkrantz et al., “The Bcl-xL inhibitor of apoptosis is preferentially expressed in cutaneous squamous cell carcinoma compared with that in keratoacanthoma,” International Journal of Cancer, vol. 124, no. 10, pp. 2361–2366, 2009. View at Publisher · View at Google Scholar · View at PubMed
  55. R. Massoumi, K. Chmielarska, K. Hennecke, A. Pfeifer, and R. Fässler, “Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-κB signaling,” Cell, vol. 125, no. 4, pp. 665–677, 2006. View at Publisher · View at Google Scholar · View at PubMed
  56. P. M. De Marval, S. Lutfeali, J. Y. Jin, B. Leshin, M. Angelica Selim, and J. Y. Zhang, “CYLD inhibits tumorigenesis and metastasis by blocking JNK/AP1 signaling at multiple levels,” Cancer Prevention Research, vol. 4, no. 6, pp. 851–859, 2011. View at Publisher · View at Google Scholar · View at PubMed
  57. J. P. Alameda, R. Moreno-Maldonado, M. Navarro et al., “An inactivating CYLD mutation promotes skin tumor progression by conferring enhanced proliferative, survival and angiogenic properties to epidermal cancer cells,” Oncogene, vol. 29, no. 50, pp. 6522–6532, 2010. View at Publisher · View at Google Scholar · View at PubMed
  58. I. Mirones, C. J. Conti, J. Martínez, M. Garcia, and F. Larcher, “Complexity of VEGF responses in skin carcinogenesis revealed through ex vivo assays based on a VEGF-A null mouse keratinocyte cell line,” Journal of Investigative Dermatology, vol. 129, no. 3, pp. 730–741, 2009. View at Publisher · View at Google Scholar · View at PubMed
  59. M. Athar, X. Tang, J. L. Lee, L. Kopelovich, and A. L. Kim, “Hedgehog signalling in skin development and cancer,” Experimental Dermatology, vol. 15, no. 9, pp. 667–677, 2006. View at Publisher · View at Google Scholar · View at PubMed
  60. 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 PubMed
  61. J. Xie, “Molecular biology of basal and squamous cell carcinomas,” Sunlight, Vitamin D and Skin Cancer, vol. 624, pp. 241–251, 2008. View at Publisher · View at Google Scholar
  62. J. B. Sunwoo, Z. Chen, G. Dong et al., “Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-κB, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma,” Clinical Cancer Research, vol. 7, no. 5, pp. 1419–1428, 2001.
  63. A. M. Fribley, B. Evenchik, Q. Zeng et al., “Proteasome inhibitor PS-341 induces apoptosis in cisplatin-resistant squamous cell carcinoma cells by induction of Noxa,” Journal of Biological Chemistry, vol. 281, no. 42, pp. 31440–31447, 2006. View at Publisher · View at Google Scholar · View at PubMed
  64. J. Wagenblast, M. Baghi, C. Arnoldner et al., “Cetuximab enhances the efficacy of bortezomib in squamous cell carcinoma cell lines,” Journal of Cancer Research and Clinical Oncology, vol. 135, no. 3, pp. 387–393, 2009. View at Publisher · View at Google Scholar · View at PubMed
  65. A. R. Altaba, J. L. Mullor, N. Dahmane, and T. Sun, “Wnt signals are targets and mediators of Gli function,” Current Biology, vol. 11, no. 10, pp. 769–773, 2001. View at Publisher · View at Google Scholar
  66. F. Yamazaki, Y. Aragane, A. Kawada, and T. Tezuka, “Immunohistochemical detection for nuclear β-catenin in sporadic basal cell carcinoma,” British Journal of Dermatology, vol. 145, no. 5, pp. 771–777, 2001. View at Publisher · View at Google Scholar
  67. M. El-Bahrawy, N. El-Masry, M. Alison, R. Poulsom, and M. Fallowfield, “Expression of β-catenin in basal cell carcinoma,” British Journal of Dermatology, vol. 148, no. 5, pp. 964–970, 2003. View at Publisher · View at Google Scholar
  68. G. Saldanha, V. Ghura, L. Potter, and A. Fletcher, “Nuclear β-catenin in basal cell carcinoma correlates with increased proliferation,” British Journal of Dermatology, vol. 151, no. 1, pp. 157–164, 2004. View at Publisher · View at Google Scholar · View at PubMed
  69. A. A. Dlugosz, S. H. Yang, T. Andl et al., “Pathological responses to oncogenic Hedgehog signaling in skin are dependent on canonical Wnt/β-catenin signaling,” Nature Genetics, vol. 40, no. 9, pp. 1130–1135, 2008. View at Publisher · View at Google Scholar · View at PubMed