Table of Contents Author Guidelines Submit a Manuscript
Gastroenterology Research and Practice
Volume 2016, Article ID 6089658, 11 pages
http://dx.doi.org/10.1155/2016/6089658
Research Article

The Role of Chromosomal Instability and Epigenetics in Colorectal Cancers Lacking β-Catenin/TCF Regulated Transcription

1Department of Medical Laboratory Sciences, College of Health Sciences and Sharjah Institute for Medical Research (SIMR), University of Sharjah, P.O. Box 27272, Sharjah, UAE
2Department of Medical and Clinical Genetics, University of Helsinki, 00290 Helsinki, Finland
3Department of Pathology, Haartman Institute and HUSLAB, University of Helsinki and Helsinki University Central Hospital, Helsinki, 00029 HUS, Finland
4Second Department of Surgery, Helsinki University Central Hospital, Helsinki, 00029 HUS, Finland
5Department of Surgery, Jyväskylä Central Hospital, 40620 Jyväskylä, Finland
6Institute of Clinical Medicine, University of Eastern Finland, Kuopio, Finland

Received 3 December 2015; Revised 1 February 2016; Accepted 2 February 2016

Academic Editor: Antoni Castells

Copyright © 2016 Wael M. Abdel-Rahman 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. P. J. Morin, A. B. Sparks, V. Korinek et al., “Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC,” Science, vol. 275, no. 5307, pp. 1787–1790, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. A. B. Sparks, P. J. Morin, B. Vogelstein, and K. W. Kinzler, “Mutational analysis of the APC/β-catenin/Tcf pathway in colorectal cancer,” Cancer Research, vol. 58, no. 6, pp. 1130–1134, 1998. View at Google Scholar · View at Scopus
  3. M. Miyaki, T. Iijima, J. Kimura et al., “Frequent mutation of β-catenin and APC genes in primary colorectal tumors from patients with hereditary nonpolyposis colorectal cancer,” Cancer Research, vol. 59, no. 18, pp. 4506–4509, 1999. View at Google Scholar · View at Scopus
  4. The Cancer Genome Atlas Network, “Comprehensive molecular characterization of human colon and rectal cancer,” Nature, vol. 487, no. 7407, pp. 330–337, 2012. View at Publisher · View at Google Scholar
  5. L. T. da Costa, T.-C. He, J. Yu et al., “CDX2 is mutated in a colorectal cancer with normal APC/β-catenin signaling,” Oncogene, vol. 18, no. 35, pp. 5010–5014, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. W. M. Abdel-Rahman, M. Ollikainen, R. Kariola et al., “Comprehensive characterization of HNPCC-related colorectal cancers reveals striking molecular features in families with no germline mismatch repair gene mutations,” Oncogene, vol. 24, no. 9, pp. 1542–1551, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. C. V. Raoand and H. Y. Yamada, “Genomic instability and colon carcinogenesis: from the perspective of genes,” Frontiers in Oncology, vol. 3, article 130, 2013. View at Google Scholar
  8. W. M. Abdel-Rahman, K. Katsura, W. Rens et al., “Spectral karyotyping suggests additional subsets of colorectal cancers characterized by pattern of chromosome rearrangement,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 5, pp. 2538–2543, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. S. L. Donahue, Q. Lin, S. Cao, and H. E. Ruley, “Carcinogens induce genome-wide loss of heterozygosity in normal stem cells without persistent chromosomal instability,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 31, pp. 11642–11646, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. T. T. Nieminen, S. Shoman, S. Eissa, P. Peltomäki, and W. M. Abdel-Rahman, “Distinct genetic and epigenetic signatures of colorectal cancers according to ethnic origin,” Cancer Epidemiology Biomarkers and Prevention, vol. 21, no. 1, pp. 202–211, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Mouradov, E. Domingo, P. Gibbs et al., “Survival in stage II/III colorectal cancer is independently predicted by chromosomal and microsatellite instability, but not by specific driver mutations,” The American Journal of Gastroenterology, vol. 108, no. 11, pp. 1785–1793, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Coppedè, A. Lopomo, R. Spisni, and L. Migliore, “Genetic and epigenetic biomarkers for diagnosis, prognosis and treatment of colorectal cancer,” World Journal of Gastroenterology, vol. 20, no. 4, pp. 943–956, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. E. I. Joensuu, W. M. Abdel-Rahman, M. Ollikainen, S. Ruosaari, S. Knuutila, and P. Peltomäki, “Epigenetic signatures of familial cancer are characteristic of tumor type and family category,” Cancer Research, vol. 68, no. 12, pp. 4597–4605, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. S. A. Kuismanen, M. T. Holmberg, R. Salovaara, A. De la Chapell, and P. Peltomaki, “Genetic and epigenetic modification of MLH1 accounts for a major share of microsatellite-unstable colorectal cancers,” The American Journal of Pathology, vol. 156, no. 5, pp. 1773–1779, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. A.-L. Moisio, H. Järvinen, and P. Peltomäki, “Genetic and clinical characterisation of familial adenomatous polyposis: a population based study,” Gut, vol. 50, no. 6, pp. 845–850, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Niskakoski, S. Kaur, L. Renkonen-Sinisalo et al., “Distinct molecular profiles in Lynch syndrome-associated and sporadic ovarian carcinomas,” International Journal of Cancer, vol. 133, no. 11, pp. 2596–2608, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. J. R. Eshleman, G. Casey, M. E. Kochera et al., “Chromosome number and structure both are markedly stable in RER colorectal cancers and are not destabilized by mutation of p53,” Oncogene, vol. 17, no. 6, pp. 719–725, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Kleivi, M. R. Teixeira, M. Eknæs et al., “Genome signatures of colon carcinoma cell lines,” Cancer Genetics and Cytogenetics, vol. 155, no. 2, pp. 119–131, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Nymark, P. M. Lindholm, M. V. Korpela et al., “Gene expression profiles in asbestos-exposed epithelial and mesothelial lung cell lines,” BMC Genomics, vol. 8, article 62, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. C. R. Boland, S. N. Thibodeau, S. R. Hamilton et al., “A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer,” Cancer Research, vol. 58, no. 22, pp. 5248–5257, 1998. View at Google Scholar · View at Scopus
  21. W. M. Abdel-Rahman, S. Ruosaari, S. Knuutila, and P. Peltomaki, “Differential roles of EPS8 in carcinogenesis: loss of protein expression in a subset of colorectal carcinoma and adenoma,” World Journal of Gastroenterology, vol. 18, no. 29, pp. 3896–3903, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. J. S. W. Low, Q. Tao, K. M. Ng et al., “A novel isoform of the 8p22 tumor suppressor gene DLC1 suppresses tumor growth and is frequently silenced in multiple common tumors,” Oncogene, vol. 30, no. 16, pp. 1923–1935, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. A. H. S. Gylling, T. T. Nieminen, W. M. Abdel-Rahman et al., “Differential cancer predisposition in Lynch syndrome: insights from molecular analysis of brain and urinary tract tumors,” Carcinogenesis, vol. 29, no. 7, pp. 1351–1359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. W. M. Abdel-Rahman, J. Kalinina, S. Shoman et al., “Somatic FGF9 mutations in colorectal and endometrial carcinomas associated with membranous β-catenin,” Human Mutation, vol. 29, no. 3, pp. 390–397, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. A. V. Roschke, G. Tonon, K. S. Gehlhaus et al., “Karyotypic complexity of the NCI-60 drug-screening panel,” Cancer Research, vol. 63, no. 24, pp. 8634–8647, 2003. View at Google Scholar · View at Scopus
  26. T. Knutsen, H. M. Padilla-Nash, D. Wangsa et al., “Definitive molecular cytogenetic characterization of 15 colorectal cancer cell lines,” Genes Chromosomes and Cancer, vol. 49, no. 3, pp. 204–223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Herbst, V. Jurinovic, S. Krebs et al., “Comprehensive analysis of β-catenin target genes in colorectal carcinoma cell lines with deregulated Wnt/β-catenin signaling,” BMC Genomics, vol. 15, article 74, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. Z. Dai and Y. Jin, “Promoter methylation of the DLC-1 gene and its inhibitory effect on human colon cancer,” Oncology Reports, vol. 30, no. 3, pp. 1511–1517, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. X. Qian, M. E. Durkin, D. Wang et al., “Inactivation of the Dlc1 gene cooperates with downregulation of p15INK4b and p16Ink4a, leading to neoplastic transformation and poor prognosis in human cancer,” Cancer Research, vol. 72, no. 22, pp. 5900–5911, 2012. View at Publisher · View at Google Scholar
  30. W. M. Abdel-Rahman, H. Lohi, S. Knuutila, and P. Peltomäki, “Restoring mismatch repair does not stop the formation of reciprocal translocations in the colon cancer cell line HCA7 but further destabilizes chromosome number,” Oncogene, vol. 24, no. 4, pp. 706–713, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Camps, C. Morales, E. Prat et al., “Genetic evolution in colon cancer KM12 cells and metastatic derivates,” International Journal of Cancer, vol. 110, no. 6, pp. 869–874, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Mur, M. Pineda, A. Romero et al., “Identification of a founder EPCAM deletion in Spanish Lynch syndrome families,” Clinical Genetics, vol. 85, no. 3, pp. 260–266, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Spaepen, E. Neven, X. Sagaert et al., “EPCAM germline and somatic rearrangements in lynch syndrome: identification of a novel 3ΩEPCAM deletion,” Genes Chromosomes and Cancer, vol. 52, no. 9, pp. 845–854, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Huth, M. Kloor, A. Y. Voigt et al., “The molecular basis of EPCAM expression loss in Lynch syndrome-associated tumors,” Modern Pathology, vol. 25, no. 6, pp. 911–916, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Domingo, P. Laiho, M. Ollikainen et al., “BRAF screening as a low-cost effective strategy for simplifying HNPCC genetic testing,” Journal of Medical Genetics, vol. 41, no. 9, pp. 664–668, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Ogino, K. Nosho, G. J. Kirkner et al., “CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer,” Gut, vol. 58, no. 1, pp. 90–96, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. T. T. Seppälä, J. P. Böhm, M. Friman et al., “Combination of microsatellite instability and BRAF mutation status for subtyping colorectal cancer,” British Journal of Cancer, vol. 112, no. 12, pp. 1966–1975, 2015. View at Publisher · View at Google Scholar
  38. R. Melcher, E. Hartmann, W. Zopf et al., “LOH and copy neutral LOH (cnLOH) act as alternative mechanism in sporadic colorectal cancers with chromosomal and microsatellite instability,” Carcinogenesis, vol. 32, no. 4, pp. 636–642, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. E. J. Douglas, H. Fiegler, A. Rowan et al., “Array comparative genomic hybridization analysis of colorectal cancer cell lines and primary carcinomas,” Cancer Research, vol. 64, no. 14, pp. 4817–4825, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. S. J. Williams, M. A. McGuckin, D. C. Gotley, H. J. Eyre, G. R. Sutherland, and T. M. Antalis, “Two novel mucin genes down-regulated in colorectal cancer identified by differential display,” Cancer Research, vol. 59, no. 16, pp. 4083–4089, 1999. View at Google Scholar · View at Scopus
  41. F. Sangar, A.-S. Schreurs, C. Umaña-Diaz et al., “Involvement of small ArfGAP1 (SMAP1), a novel Arf6-specific GTPase-activating protein, in microsatellite instability oncogenesis,” Oncogene, vol. 33, no. 21, pp. 2758–2767, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Pages, A. Berger, S. Lebel-Binay et al., “Proinflammatory and antitumor properties of interleukin-18 in the gastrointestinal tract,” Immunology Letters, vol. 75, no. 1, pp. 9–14, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Cui, Y. Ying, A. van Hasselt et al., “OPCML is a broad tumor suppressor for multiple carcinomas and lymphomas with frequently epigenetic inactivation,” PLoS ONE, vol. 3, no. 8, Article ID e2990, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Li, E. A. Fattah, G. Cao et al., “Glioma pathogenesis-related protein 1 exerts tumor suppressor activities through proapoptotic reactive oxygen species-c-Jun-NH2 kinase signaling,” Cancer Research, vol. 68, no. 2, pp. 434–443, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Bier, N. Giladi, N. Kronfeld et al., “MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1,” Oncotarget, vol. 4, no. 5, pp. 665–676, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Fujita, T. Satoh, T. L. Timme et al., “Combined therapeutic effects of adenoviral vector-mediated GLIPR1 gene therapy and radiotherapy in prostate and bladder cancer models,” Urologic Oncology: Seminars and Original Investigations, vol. 32, no. 2, pp. 92–100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Xia, P. Jia, K. E. Hutchinson et al., “A meta-analysis of somatic mutations from next generation sequencing of 241 melanomas: a road map for the study of genes with potential clinical relevance,” Molecular Cancer Therapeutics, vol. 13, no. 7, pp. 1918–1928, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Etcheverry, M. Aubry, M. de Tayrac et al., “DNA methylation in glioblastoma: impact on gene expression and clinical outcome,” BMC Genomics, vol. 11, article 701, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Wöhrle, B. Wallmen, and A. Hecht, “Differential control of Wnt target genes involves epigenetic mechanisms and selective promoter occupancy by T-cell factors,” Molecular and Cellular Biology, vol. 27, no. 23, pp. 8164–8177, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Ying and Q. Tao, “Epigenetic disruption of the WNT/β-catenin signaling pathway in human cancers,” Epigenetics, vol. 4, no. 5, pp. 307–312, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. P. M. Campbell and M. Szyf, “Human DNA methyltransferase gene DNMT1 is regulated by the APC pathway,” Carcinogenesis, vol. 24, no. 1, pp. 17–24, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Wang, J. Li, Y. Cui et al., “CMTM3, located at the critical tumor suppressor locus 16q22.1, is silenced by CpG methylation in carcinomas and inhibits tumor cell growth through inducing apoptosis,” Cancer Research, vol. 69, no. 12, pp. 5194–5201, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Xie, Y. Yuan, Z. Liu et al., “CMTM3 is frequently reduced in clear cell renal cell carcinoma and exhibits tumor suppressor activities,” Clinical and Translational Oncology, vol. 16, no. 4, pp. 402–409, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Su, Y. Lin, L. Zhang et al., “CMTM3 inhibits cell migration and invasion and correlates with favorable prognosis in gastric cancer,” Cancer Science, vol. 105, no. 1, pp. 26–34, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. Z. Li, J. Xie, J. Wu et al., “CMTM3 inhibits human testicular cancer cell growth through inducing cell-cycle arrest and apoptosis,” PLoS ONE, vol. 9, no. 2, Article ID e88965, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. F. Zhou, G. Tao, X. Chen, W. Xie, M. Liu, and X. Cao, “Methylation of OPCML promoter in ovarian cancer tissues predicts poor patient survival,” Clinical Chemistry and Laboratory Medicine, vol. 52, no. 5, pp. 735–742, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. W. Chen, J. Xiang, D.-F. Chen et al., “Screening for differentially methylated genes among human colorectal cancer tissues and normal mucosa by microarray chip,” Molecular Biology Reports, vol. 40, no. 5, pp. 3457–3464, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. D. K. Alexopoulou, I. N. Papadopoulos, and A. Scorilas, “Clinical significance of kallikrein-related peptidase (KLK10) mRNA expression in colorectal cancer,” Clinical Biochemistry, vol. 46, no. 15, pp. 1453–1461, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Olkhov-Mitsel, T. Van der Kwast, K. J. Kron et al., “Quantitative DNA methylation analysis of genes coding for kallikrein-related peptidases 6 and 10 as biomarkers for prostate cancer,” Epigenetics, vol. 7, no. 9, pp. 1037–1045, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Talieri, D. K. Alexopoulou, A. Scorilas et al., “Expression analysis and clinical evaluation of kallikrein-related peptidase 10 (KLK10) in colorectal cancer,” Tumor Biology, vol. 32, no. 4, pp. 737–744, 2011. View at Publisher · View at Google Scholar · View at Scopus