- About this Journal ·
- Abstracting and Indexing ·
- Aims and Scope ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Volume 2011 (2011), Article ID 598218, 11 pages
Human Chondrosarcoma Cells Acquire an Epithelial-Like Gene Expression Pattern via an Epigenetic Switch: Evidence for Mesenchymal-Epithelial Transition during Sarcomagenesis
1Free Radical and Radiation Biology Program, Department of Radiation Oncology, University of Iowa, Iowa City, IA 52242, USA
2Department of Orthopaedics and Rehabilitation, University of Iowa, Iowa City, IA 52242, USA
3Department of Otolaryngology-Head and Neck Surgery, University of Iowa, Iowa City, IA 52242, USA
Received 15 September 2010; Accepted 20 January 2011
Academic Editor: Stephen Lessnick
Copyright © 2011 Matthew P. Fitzgerald 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.
- H. D. Dorfman and B. Czerniak, “Bone cancers,” Cancer, vol. 75, no. 1, pp. 203–210, 1995.
- S. Gitelis, F. Bertoni, P. Picci, and M. Campanacci, “Chondrosarcoma of bone. The experience at the Istituto Ortopedico Rizzoli,” Journal of Bone and Joint Surgery—Series A, vol. 63, no. 8, pp. 1248–1257, 1981.
- R. M. Terek, G. K. Schwartz, K. Devaney et al., “Chemotherapy and P-glycoprotein expression in chondrosarcoma,” Journal of Orthopaedic Research, vol. 16, no. 5, pp. 585–590, 1998.
- F. Moussavi-Harami, A. Mollano, J. A. Martin et al., “Intrinsic radiation resistance in human chondrosarcoma cells,” Biochemical and Biophysical Research Communications, vol. 346, no. 2, pp. 379–385, 2006.
- A. M. Cleton-Jansen, H. M. van Beerendonk, H. J. Baelde, J. V. G. M. Bovée, M. Karperien, and P. C. W. Hogendoorn, “Estrogen signaling is active in cartilaginous tumors: implications for antiestrogen therapy as treatment option of metastasized or irresectable chondrosarcoma,” Clinical Cancer Research, vol. 11, no. 22, pp. 8028–8035, 2005.
- H. M. van Beerendonk, L. B. Rozeman, A. H. M. Taminiau et al., “Molecular analysis of the INK4A/INK4A-ARF gene locus in conventional (central) chondrosarcomas and enchondromas: indication of an important gene for tumour progression,” Journal of Pathology, vol. 202, no. 3, pp. 359–366, 2004.
- M. Röpke, C. Boltze, H. W. Neumann, A. Roessner, and R. Schneider-Stock, “Genetic and epigenetic alterations in tumor progression in a dedifferentiated chondrosarcoma,” Pathology Research and Practice, vol. 199, no. 6, pp. 437–444, 2003.
- T. Tsuchiya, T. Osanai, A. Ogose et al., “Methylation status of EXT1 and EXT2 promoters and two mutations of EXT2 in chondrosarcoma,” Cancer Genetics and Cytogenetics, vol. 158, no. 2, pp. 148–155, 2005.
- P. Ouyang, “An in vitro model to study mesenchymal-epithelial transformation,” Biochemical and Biophysical Research Communications, vol. 246, no. 3, pp. 771–776, 1998.
- H. Hugo, M. L. Ackland, T. Blick et al., “Epithelial—mesenchymal and mesenchymal—epithelial transitions in carcinoma progression,” Journal of Cellular Physiology, vol. 213, no. 2, pp. 374–383, 2007.
- C. L. Chaffer, E. W. Thompson, and E. D. Williams, “Mesenchymal to epithelial transition in development and disease,” Cells Tissues Organs, vol. 185, no. 1–3, pp. 7–19, 2007.
- T. Naka, Y. Iwamoto, N. Shinohara, M. Ushijima, H. Chuman, and M. Tsuneyoshi, “Expression of c-met proto-oncogene product (c-MET) in benign and malignant bone tumors,” Modern Pathology, vol. 10, no. 8, pp. 832–838, 1997.
- K. Scotlandi, N. Baldini, M. Oliviero et al., “Expression of met/hepatocyte growth factor receptor gene and malignant behavior of musculoskeletal tumors,” American Journal of Pathology, vol. 149, no. 4, pp. 1209–1219, 1996.
- M. Jeffers, S. Rong, and G. F. Woude, “Hepatocyte growth factor/scatter factor-met signaling in tumorigenicity and invasion/metastasis,” Journal of Molecular Medicine, vol. 74, no. 9, pp. 505–513, 1996.
- I. Tsarfaty, S. Rong, J. H. Resau, S. Rulong, P. P. Da Silva, and G. F. Vande Woude, “The Met proto-oncogene mesenchymal to epithelial cell conversion,” Science, vol. 263, no. 5143, pp. 98–101, 1994.
- M. Darmon, J. F. Nicolas, and D. Lamblin, “5-Azacytidine is able to induce the conversion of teratocarcinoma-derived mesenchymal cells into epithelia cells,” EMBO Journal, vol. 3, no. 5, pp. 961–967, 1984.
- C. S. Bathula, S. H. Garrett, X. D. Zhou, M. A. Sens, D. A. Sens, and S. Somji, “Cadmium, vectorial active transport, and MT-3-Dependent regulation of cadherin expression in human proximal tubular cells,” Toxicological Sciences, vol. 102, no. 2, pp. 310–318, 2008.
- M. Jorda, A. Vinyals, A. Marazuela et al., “Id-1 is induced in MDCK epithelial cells by activated Erk/MAPK pathway in response to expression of the Snail and E47 transcription factors,” Experimental Cell Research, vol. 313, no. 11, pp. 2389–2403, 2007.
- M. A. Horswill, M. Narayan, D. J. Warejcka, L. A. Cirillo, and S. S. Twining, “Epigenetic silencing of maspin expression occurs early in the conversion of keratocytes to fibroblasts,” Experimental Eye Research, vol. 86, no. 4, pp. 586–600, 2008.
- C. Boltze, R. Schneider-Stock, C. Quednow et al., “Silencing of the maspin gene by promoter hypermethylation in thyroid cancer,” International Journal of Molecular Medicine, vol. 12, no. 4, pp. 479–484, 2003.
- M. Fitzgerald, M. Oshiro, N. Holtan et al., “Human pancreatic carcinoma cells activate maspin expression through loss of epigenetic control,” Neoplasia, vol. 5, no. 5, pp. 427–436, 2003.
- Y. Yatabe, T. Mitsudomi, and T. Takahashi, “Maspin expression in normal lung and non-small-cell lung cancers: cellular property-associated expression under the control of promoter DNA methylation,” Oncogene, vol. 23, no. 23, pp. 4041–4049, 2004.
- R. Henrique, C. Jerónimo, M. O. Hoque et al., “Frequent 14-3-3σ promoter methylation in benign and malignant prostate lesions,” DNA and Cell Biology, vol. 24, no. 4, pp. 264–269, 2005.
- A. Benzinger, N. Muster, H. B. Koch, J. R. Yates, and H. Hermeking, “Targeted proteomic analysis of 14-3-3σ, a p53 effector commonly silenced in cancer,” Molecular and Cellular Proteomics, vol. 4, no. 6, pp. 785–795, 2005.
- A. Cano, M. A. Pérez-Moreno, I. Rodrigo et al., “The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression,” Nature Cell Biology, vol. 2, no. 2, pp. 76–83, 2000.
- Z. Zou, A. Anisowicz, M. J. C. Hendrix et al., “Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells,” Science, vol. 263, no. 5146, pp. 526–529, 1994.
- R. Sager, S. Sheng, P. Pemberton, and M. J. C. Hendrix, “Maspin: a tumor suppressing serpin,” Advances in Experimental Medicine and Biology, vol. 425, pp. 77–88, 1997.
- M. Zhang, O. Volpert, Y. H. Shi, and N. Bouck, “Maspin is an angiogenesis inhibitor,” Nature Medicine, vol. 6, no. 2, pp. 196–199, 2000.
- B. W. Futscher, M. M. Oshiro, R. J. Wozniak et al., “Role for DNA methylation in the control of cell type-specific maspin expression,” Nature Genetics, vol. 31, no. 2, pp. 175–179, 2002.
- J. S. Schaefer and M. Zhang, “Role of maspin in tumor metastasis and angiogenesis,” Current Molecular Medicine, vol. 3, no. 7, pp. 653–658, 2003.
- M. Zhang, “Multiple functions of maspin in tumor progression and mouse development,” Frontiers in Bioscience, vol. 9, pp. 2218–2226, 2004.
- F. E. Domann, J. C. Rice, M. J. C. Hendrix, and B. W. Futscher, “Epigenetic silencing of maspin gene expression in human breast cancers,” International Journal of Cancer, vol. 85, no. 6, pp. 805–810, 2000.
- K. Wada, C. Maesawa, T. Akasaka, and T. Masuda, “Aberrant expression of the maspin gene associated with epigenetic modification in melanoma cells,” Journal of Investigative Dermatology, vol. 122, no. 3, pp. 805–811, 2004.
- S. L. Rose, M. P. Fitzgerald, N. O. White et al., “Epigenetic regulation of maspin expression in human ovarian carcinoma cells,” Gynecologic Oncology, vol. 102, no. 2, pp. 319–324, 2006.
- A. K. Sood, M. S. Fletcher, L. M. Gruman et al., “The paradoxical expression of Maspin in ovarian carcinoma,” Clinical Cancer Research, vol. 8, no. 9, pp. 2924–2932, 2002.
- H. J. Son, T. S. Sohn, S. Y. Song, J. H. Lee, and J. C. Rhee, “Maspin expression in human gastric adenocarcinoma,” Pathology International, vol. 52, no. 8, pp. 508–513, 2002.
- G. L. Prasad, E. M. Valverius, E. McDuffie, and H. L. Cooper, “Complementary DNA cloning of a novel epithelial cell marker protein, HME1, that may be down-regulated in neoplastic mammary cells,” Cell growth & Differentiation, vol. 3, no. 8, pp. 507–513, 1992.
- H. Hermeking, C. Lengauer, K. Polyak et al., “14-3-3σ is a p53-regulated inhibitor of G2/M progression,” Molecular Cell, vol. 1, no. 1, pp. 3–11, 1997.
- W. R. Taylor and G. R. Stark, “Regulation of the G2/M transition by p53,” Oncogene, vol. 20, no. 15, pp. 1803–1815, 2001.
- A. T. Ferguson, E. Evron, C. B. Umbricht et al., “High frequency of hypermethylation at the 14-3-3 σ locus leads to gene silencing in breast cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 11, pp. 6049–6054, 2000.
- N. Iwata, H. Yamamoto, S. Sasaki et al., “Frequent hypermethylation of CpG islands and loss of expression of the 14-3-3 σ gene in human hepatocellular carcinoma,” Oncogene, vol. 19, no. 46, pp. 5298–5302, 2000.
- A. Guweidhi, J. Kleeff, N. Giese et al., “Enhanced expression of 14-3-3sigma in pancreatic cancer and its role in cell cycle regulation and apoptosis,” Carcinogenesis, vol. 25, no. 9, pp. 1575–1585, 2004.
- T. Sano, H. Shimooka, P. Weixa et al., “Immunohistochemical expression of 14-3-3 sigma protein in various histological subtypes of uterine cervical cancers,” Pathology International, vol. 54, no. 10, pp. 743–750, 2004.
- M. M. Oshiro, C. J. Kim, R. J. Wozniak et al., “Epigenetic silencing of DSC3 is a common event in human breast cancer,” Breast Cancer Research, vol. 7, no. 5, pp. R669–R680, 2005.
- M. T. Debies and D. R. Welch, “Genetic basis of human breast cancer metastasis,” Journal of Mammary Gland Biology and Neoplasia, vol. 6, no. 4, pp. 441–451, 2001.
- S. O. Lim, J. M. Gu, M. S. Kim et al., “Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter,” Gastroenterology, vol. 135, no. 6, pp. 2128–2140, 2008.
- J. A. Martin, E. Forest, J. A. Block et al., “Malignant transformation in human chondrosarcoma cells supported by telomerase activation and tumor suppressor inactivation,” Cell Growth and Differentiation, vol. 13, no. 9, pp. 397–407, 2002.
- M. M. Oshiro, B. W. Futscher, A. Lisberg et al., “Epigenetic regulation of the cell type-specific gene 14-3-3σ,” Neoplasia, vol. 7, no. 9, pp. 799–808, 2005.
- S. Murai, C. Maesawa, T. Masuda, and T. Sugiyama, “Aberrant maspin expression in human endometrial cancer,” Cancer Science, vol. 97, no. 9, pp. 883–888, 2006.
- Y. Akiyama, C. Maesawa, S. Ogasawara, M. Terashima, and T. Masuda, “Cell-type-specific repression of the maspin gene is disrupted frequently by demethylation at the promoter region in gastric intestinal metaplasia and cancer cells,” American Journal of Pathology, vol. 163, no. 5, pp. 1911–1919, 2003.
- M. Gasco, A. K. Bell, V. Heath et al., “Epigenetic inactivation of 14-3-3 σ in oral carcinoma: association with p16 silencing and human papillomavirus negativity,” Cancer Research, vol. 62, no. 7, pp. 2072–2076, 2002.
- J. M. A. Moreira, G. Ohlsson, F. E. Rank, and J. E. Celis, “Down-regulation of the tumor suppressor protein 14-3-3σ is a sporadic event in cancer of the breast,” Molecular and Cellular Proteomics, vol. 4, no. 4, pp. 555–569, 2005.
- T. Saito, M. Nagai, and M. Ladanyi, “SYT-SSX1 and SYT-SSX2 interfere with repression of E-cadherin by snail and slug: a potential mechanism for aberrant mesenchymal to epithelial transition in human synovial sarcoma,” Cancer Research, vol. 66, no. 14, pp. 6919–6927, 2006.
- D. Olmeda, M. Jordá, H. Peinado, A. Fabra, and A. Cano, “Snail silencing effectively suppresses tumour growth and invasiveness,” Oncogene, vol. 26, no. 13, pp. 1862–1874, 2007.
- F. E. Domann and B. W. Futschert, “Flipping the epigenetic switch,” American Journal of Pathology, vol. 164, no. 6, pp. 1883–1886, 2004.
- N. Auersperg, J. Pan, B. D. Grove et al., “E-cadherin induces mesenchymal-to-epithelial transition in human ovarian surface epithelium,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 11, pp. 6249–6254, 1999.
- Y. Kang and J. Massagué, “Epithelial-mesenchymal transitions: twist in development and metastasis,” Cell, vol. 118, no. 3, pp. 277–279, 2004.
- N. K. Kurrey, K. Amit, and S. A. Bapat, “Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level,” Gynecologic Oncology, vol. 97, no. 1, pp. 155–165, 2005.
- D. Olmeda, G. Moreno-Bueno, J. M. Flores, A. Fabra, F. Portillo, and A. Cano, “SNAI1 is required for tumor growth and lymph node metastasis of human breast carcinoma MDA-MB-231 cells,” Cancer Research, vol. 67, no. 24, pp. 11721–11731, 2007.
- Y. Liu, H. Liu, B. Han, and J. T. Zhang, “Identification of 14-3-3σ as a contributor to drug resistance in human breast cancer cells using functional proteomic analysis,” Cancer Research, vol. 66, no. 6, pp. 3248–3255, 2006.
- P. Sinha, G. Hütter, E. Köttgen, M. Dletel, D. Schadendorf, and H. Lage, “Increased expression of epidermal fatty acid binding protein, cofilin, and 14-3-3-σ (stratifin) detected by two-dimensional gel electrophoresis, mass spectrometry and microsequencing of drug-resistant human adenocarcinoma of the pancreas,” Electrophoresis, vol. 20, no. 14, pp. 2952–2960, 1999.