Table of Contents Author Guidelines Submit a Manuscript
Disease Markers
Volume 2017, Article ID 9253495, 10 pages
https://doi.org/10.1155/2017/9253495
Research Article

Expression Levels and Localizations of DVL3 and sFRP3 in Glioblastoma

1Laboratory of Neuro-oncology, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Salata 12, Zagreb, Croatia
2Department of Biology, School of Medicine, University of Zagreb, Salata 3, Zagreb, Croatia
3Department of Pathology, School of Medicine, University of Zagreb, Salata 10, 10000 Zagreb, Croatia
4University Hospital “Sisters of Charity”, Vinogradska 29, 10000 Zagreb, Croatia
5Department of Pathology & Laboratory Medicine, University of California, Davis Medical Center, 4400 V Street, Sacramento, CA 95817, USA

Correspondence should be addressed to Nives Pećina-Šlaus; rh.fem@anin

Received 20 April 2017; Accepted 14 September 2017; Published 19 October 2017

Academic Editor: Alex J. Rai

Copyright © 2017 Anja Kafka 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. D. N. Louis, H. Ohgaki, O. D. Wiestler et al., “The 2007 WHO classification of tumours of the central nervous system,” Acta Neuropathologica, vol. 114, no. 2, pp. 97–109, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. D. N. Louis, A. Perry, P. Burger et al., “International Society Of Neuropathology-Haarlem consensus guidelines for nervous system tumor classification and grading,” Brain Pathology, vol. 24, no. 5, pp. 429–435, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. D. N. Louis, A. Perry, G. Reifenberger et al., “The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary,” Acta Neuropathologica, vol. 131, no. 6, pp. 803–820, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. S. P. Ferris, J. W. Hofmann, D. A. Solomon, and A. Perry, “Characterization of gliomas: from morphology to molecules,” Virchows Archiv, vol. 471, no. 2, pp. 257–269, 2017. View at Publisher · View at Google Scholar
  5. S. Agnihotri, K. D. Aldape, and G. Zadeh, “Isocitrate dehydrogenase status and molecular subclasses of glioma and glioblastoma,” Neurosurgical Focus, vol. 37, no. 6, article E13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. J. L. Izquerido-Garcia, P. Viswanath, P. Eriksson et al., “IDH1 mutation induces reprogramming of pyruvate metabolism,” Cancer Research, vol. 75, no. 15, pp. 2999–3009, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Reya and H. Clevers, “Wnt signaling in stem cells and cancer,” Nature, vol. 434, no. 7035, pp. 843–850, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. S. J. Harrison-Uy and S. J. Pleasure, “Wnt signaling and forebrain development,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 7, article a008094, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Polakis, “Wnt signaling in cancer,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 5, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Kahn, “Can we safely target the WNT pathway?” Nature Reviews Drug Discovery, vol. 13, no. 7, pp. 513–532, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Roth, C. Wild-Bode, M. Platten et al., “Secreted Frizzled-related proteins inhibit motility and promote growth of human malignant glioma cells,” Oncogene, vol. 19, no. 37, pp. 4210–4220, 2000. View at Publisher · View at Google Scholar
  12. S. Götze, M. Wolter, G. Reifenberger, O. Müller, and S. Sievers, “Frequent promoter hypermethylation of Wnt pathway inhibitor genes in malignant astrocytic gliomas,” International Journal of Cancer, vol. 126, no. 11, pp. 2584–2593, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Zhang, P. Wei, A. Gong et al., “FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis,” Cancer Cell, vol. 20, no. 4, pp. 427–442, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. U. D. Kahlert, D. Maciaczyk, S. Doostkam et al., “Activation of canonical WNT/β-catenin signaling enhances in vitro motility of glioblastoma cells by activation of ZEB1 and other activators of epithelial-to-mesenchymal transition,” Cancer Letters, vol. 325, no. 1, pp. 42–53, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Rheinbay, M. L. Suva, S. M. Gillespie et al., “An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma,” Cell Reports, vol. 3, no. 5, pp. 1567–1579, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Delic, N. Lottmann, A. Stelzl et al., “MiR-328 promotes glioma cell invasion via SFRP1-dependent Wnt-signaling activation,” Neuro-Oncology, vol. 16, no. 2, pp. 179–190, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Schiefer, M. Visweswaran, V. Perumal et al., “Epigenetic regulation of the secreted frizzled-related protein family in human glioblastoma multiforme,” Cancer Gene Therapy, vol. 21, no. 7, pp. 297–303, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Pećina-Šlaus, T. Nikuševa Martić, T. Kokotović, V. Kusec, D. Tomas, and R. Hrasćan, “AXIN-1 protein expression and localization in glioblastoma,” Collegium Antropologicum, vol. 35, no. 1, pp. 101–106, 2011. View at Google Scholar
  19. N. Pećina-Šlaus, A. Kafka, D. Tomas et al., “Wnt signaling transcription factors TCF-1 and LEF-1 are upregulated in malignant astrocytic brain tumors,” Histology and Histopathology, vol. 29, no. 12, pp. 1557–1564, 2014. View at Publisher · View at Google Scholar
  20. T. Nikuševa Martić, V. Beroš, N. Pećina-Šlaus, H. I. Pećina, and F. Bulić-Jakus, “Genetic changes of CDH1, APC and CTNNB1 found in human brain tumors,” Pathology Research and Practice, vol. 203, no. 11, pp. 779–787, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Nikuševa Martić, N. Pećina-Šlaus, V. Kušec et al., “Changes of AXIN-1 and beta-catenin in neuroepithelial brain tumors,” Patholology Oncology Research, vol. 16, no. 1, pp. 75–79, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. X. Zhao, H. Huang, Y. Chen et al., “Dynamic expression of secreted Frizzled-related protein 3 (sFRP3) in the developing mouse spinal cord and dorsal root ganglia,” Neuroscience, vol. 248, pp. 594–601, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Lin, S. Wang, M. A. Julius, J. Kitajewski, M. Moos Jr, and F. P. Luyten, “The cysteine-rich frizzled domain of Frzb-1 is required and sufficient for modulation of Wnt signaling,” Proceedings of the National Academy of Sciences, vol. 94, no. 21, pp. 11196–11200, 1997. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Bafico, A. Gazit, T. Pramila, P. W. Finch, A. Yaniv, and S. A. Aaronson, “Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling,” The Journal of Biological Chemistry, vol. 274, no. 23, pp. 16180–16187, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Bovolenta, P. Esteve, J. M. Ruiz, E. Cisneros, and J. Lopez-Rios, “Beyond Wnt Inhibition: new functions of secreted Frizzled-related proteins in development and disease,” Journal of Cell Science, vol. 121, no. 6, pp. 737–746, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. F. Fagotto, “Looking beyond the Wnt pathway for the deep nature of β-catenin,” EMBO Reports, vol. 14, no. 5, pp. 422–433, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Gao and Y. G. Chen, “Dishevelled: the hub of wnt signaling,” Cellular Signalling, vol. 22, no. 5, pp. 717–727, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Kafka, S. Bašić-Kinda, and N. Pećina-Šlaus, “The cellular story of dishevelleds,” Croatian Medical Journal, vol. 55, no. 5, pp. 459–467, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Habas and I. B. Dawid, “Dishevelled and Wnt signaling: is the nucleus the final frontier?” Journal of Biology, vol. 4, no. 1, p. 2, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Itoh, B. K. Brott, G. Bae, M. J. Ratcliffe, and S. Y. Sokol, “Nuclear localization is required for Dishevelled function inWnt/β-catenin signaling,” Journal of Biology, vol. 4, no. 1, p. 2, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. J. B. Weitzman, “Dishevelled nuclear shuttling,” Journal of Biology, vol. 4, no. 1, p. 1, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Surana, S. Sikka, W. Cai et al., “Secreted frizzled related proteins: implications in cancer,” Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, vol. 1845, no. 1, pp. 53–65, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Kawano and R. Kypta, “Secreted antagonists of the Wnt signalling pathway,” Journal of Cell Science, vol. 116, Part 13, pp. 2627–2634, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Mii and M. Taira, “Secreted Wnt “inhibitors” are not just inhibitors: regulation of extracellular Wnt by secreted Frizzled-related proteins,” Development, Growth & Differentiation, vol. 53, no. 8, pp. 911–923, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Leyns, T. Bouwmeester, S. H. Kim, S. Piccolo, and E. M. De Robertis, “Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer,” Cell, vol. 88, no. 6, pp. 747–756, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. S. E. Jones and C. Jomary, “Secreted Frizzled-related proteins: searching for relationships and patterns,” BioEssays, vol. 24, no. 9, pp. 811–820, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Z. Partl, D. Fabijanovic, A. Skrtic, S. Vranic, T. N. Martic, and L. Serman, “Immunohistochemical expression of SFRP1 and SFRP3 proteins in normal and malignant reproductive tissues of rats and humans,” Applied Immunohistochemistry & Molecular Morphology, vol. 22, no. 9, pp. 681–687, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Wang, T. Xu, Y. Jiang et al., “The challenges and the promise of molecular targeted therapy in malignant gliomas,” Neoplasia, vol. 17, no. 3, pp. 239–255, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. Cancer Genome Atlas Research Network, “Comprehensive genomic characterization defines human glioblastoma genes and core pathways,” Nature, vol. 455, no. 7216, pp. 1061–1068, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. M. V. Sofroniew and H. V. Vinters, “Astrocytes: biology and pathology,” Acta Neuropathologica, vol. 119, no. 1, pp. 7–35, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. L. Wang, C. B. Zhang, J. Q. Cai, Q. B. Li, Z. Wang, and T. Jiang, “Integrated analysis of genome-wide DNA methylation, gene expression and protein expression profiles in molecular subtypes of WHO II-IV gliomas,” Journal of Experimental & Clinical Cancer Research, vol. 34, p. 127, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Rossi, L. Magnoni, C. Miracco et al., “β-Catenin and GLI1 are prognostic markers in glioblastoma,” Cancer Biology & Therapy, vol. 11, no. 8, pp. 753–761, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. Z. Shi, X. Qian, L. Li et al., “Nuclear translocation of β-catenin is essential for glioma cell survival,” Journal of Neuroimmune Pharmacology, vol. 7, no. 4, pp. 892–903, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Schule, C. Dictus, B. Campos et al., “Potential canonical WNT pathway activation in high-grade astrocytomas,” The Scientific World Journal, vol. 2012, Article ID 697313, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Yang, R. R. Iyer, A. C. Yu et al., “β-Catenin signaling initiates the activation of astrocytes and its dysregulation contributes to the pathogenesis of astrocytomas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 18, pp. 6963–6968, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Rampazzo, L. Persano, F. Pistollato et al., “Wnt activation promotes neuronal differentiation of glioblastoma,” Cell Death and Disease, vol. 4, no. 2, article e500, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Coluccia, C. Figuereido, S. Isik, C. Smith, and J. T. Rutka, “Medulloblastoma: tumor biology and relevance to treatment and prognosis paradigm,” Current Neurology and Neuroscience Reports, vol. 16, no. 5, p. 43, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Hirano, H. Yonezawa, S. Yunoue et al., “Immunoreactivity of Wnt5a, Fzd2, Fzd6, and Ryk in glioblastoma: evaluative methodology for DAB chromogenic immunostaining,” Brain Tumor Pathology, vol. 31, no. 2, pp. 85–93, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Gabud, Ekspresija proteina sFRP3 i DVL3, ključnih molekula signalnog puta Wnt u glioblastomu, [M.S. thesis], University of Zagreb, Zagreb, Croatia, 2015, http://digre.pmf.unizg.hr/4600/1/gabud%20diplomski.pdf.
  50. J. Li, G. Guo, J. Li et al., “The expression and significance of dishevelled in human glioma,” Journal of Surgical Research, vol. 192, no. 2, pp. 509–514, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. X. Q. Gan, J. Y. Wang, Y. Xi, Z. L. Wu, Y. P. Li, and L. Li, “Nuclear Dvl, c-Jun, β-catenin, and TCF form a complex leading to stabilization of β-catenin-TCF interaction,” The Journal of Cell Biology, vol. 180, no. 6, pp. 1087–1100, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Liu, Y. Tu, X. Sun et al., “WNT/β-catenin pathway in human glioma: expression pattern and clinical/prognostic correlations,” Clinical and Experimental Medicine, vol. 11, no. 2, pp. 105–112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Nagahata, T. Shimada, A. Harada et al., “Amplification, up-regulation and over-expression of DVL-1, the human counterpart of the Drosophila disheveled gene, in primary breast cancers,” Cancer Science, vol. 94, no. 6, pp. 515–518, 2003. View at Publisher · View at Google Scholar
  54. K. Uematsu, B. He, L. You, Z. Xu, F. McCormick, and D. M. Jablons, “Activation of the Wnt pathway in non small cell lung cancer: evidence of disheveled overexpression,” Oncogene, vol. 22, no. 46, pp. 7218–7221, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Uematsu, S. Kanazawa, L. You et al., “Wnt pathway activation in mesothelioma: evidence of Dishevelled overexpression and transcriptional activity of β-catenin,” Cancer Research, vol. 63, no. 15, pp. 4547–4551, 2003. View at Google Scholar
  56. Y. Zhao, Z.-Q. Yang, Y. Wang et al., “Dishevelled-1 and Dishevelled-3 affect cell invasion mainly through canonical and noncanonical Wnt pathway, respectively, and associate with poor prognosis in nonsmall cell lung cancer,” Molecular Carcinogenesis, vol. 49, no. 8, pp. 760–770, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. X. Y. Li, S. L. Liu, N. Cha et al., “Transcription expression and clinical significance of Dishevelled-3 mRNA and δ-catenin mRNA in pleural effusions from patients with lung cancer,” Clinical and Developmental Immunology, vol. 2012, Article ID 904946, 6 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Kafka, D. Tomas, V. Beroš, H. I. Pećina, M. Zeljko, and N. Pećina-Šlaus, “Brain metastases from lung cancer show increased expression of DVL1, DVL3 and beta-catenin and down-regulation of E-cadherin,” International Journal of Molecular Sciences, vol. 15, no. 6, pp. 10635–10651, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. V. Barbashina, P. Salazar, E. C. Holland, M. K. Rosenblum, and M. Ladanyi, “Allelic losses at 1p36 and 19q13 in gliomas: correlation with histologic classification, definition of a 150-kb minimal deleted region on 1p36, and evaluation of CAMTA1 as a candidate tumor suppresor gene,” Clinical Cancer Research, vol. 11, no. 3, pp. 1119–1128, 2005. View at Google Scholar
  60. K. Tsukamoto, N. Ito, M. Yoshimoto et al., “Allelic loss on chromosome 1p is associated with progression and lymph node metastasis of primary breast carcinoma,” Cancer, vol. 82, no. 2, pp. 317–322, 1998. View at Publisher · View at Google Scholar
  61. I. Paw, R. C. Carpenter, K. Watabe, W. Debinski, and H. W. Lo, “Mechanisms regulating glioma invasion,” Cancer Letters, vol. 362, no. 1, pp. 1–7, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. Shi, B. He, L. You, and D. M. Jablons, “Roles of secreted frizzled-related proteins in cancer,” Acta Pharmacologica Sinica, vol. 28, no. 9, pp. 1499–1504, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. J. L. Lee, C. J. Chang, S. Y. Wu, D. R. Sargan, and C. T. Lin, “Secreted frizzled-related protein 2 (SFRP2) is highly expressed in canine mammary gland tumors but not in normal mammary glands,” Breast Cancer Research and Treatment, vol. 84, no. 2, pp. 139–149, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. J. Drake, A. M. Shearwood, J. White et al., “Expression of secreted frizzled-related protein 4 (SFRP4) in primary serous ovarian tumours,” European Journal of Gynaecological Oncology, vol. 30, no. 2, pp. 133–141, 2009. View at Google Scholar
  65. H. Hirata, Y. Hinoda, K. Ueno, S. Majid, S. Saini, and R. Dahiya, “Role of secreted Frizzled-related protein 3 in human renal cell carcinoma,” Cancer Research, vol. 70, no. 5, pp. 1896–1905, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Huang, B. Yu, Y. Deng et al., “SFRP4 was overexpressed in colorectal carcinoma,” Journal of Cancer Research and Clinical Oncology, vol. 136, pp. 395–401, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. C. P. Xavier, M. Melikovaa, Y. Chumana, A. Üren, B. Baljinnyam, and J. S. Rubin, “Secreted Frizzled-related protein potentiation versus inhibition of Wnt3a/β-catenin signaling,” Cellular Signalling, vol. 26, no. 1, pp. 94–101, 2014. View at Publisher · View at Google Scholar · View at Scopus
  68. R. Da Silva, S. K. N. Marie, M. Uno et al., “CTNNB1, AXIN1 and APC expression analysis of different medulloblastoma variants,” Clinics, vol. 68, no. 2, pp. 167–172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. E. J. Ekström, V. Sherwood, and T. Andersson, “Methylation and loss of secreted Frizzled-related protein 3 enhances melanoma cell migration and invasion,” PLoS One, vol. 6, no. 4, article e18674, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Uren, F. Reichsman, V. Anest et al., “Secreted frizzled-related protein-1 binds directly to Wingless and is a biphasic modulator of Wnt signaling,” The Journal of Biological Chemistry, vol. 275, no. 6, pp. 4374–4382, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Sun, M. A. Bonaguidi, H. Jun et al., “A septo-remporal molecular gradient of sfrp3 in the dentate gyrus differentially regulates quiescent adult hippocampal neural stem activation,” Molecular Brain, vol. 8, p. 52, 2015. View at Publisher · View at Google Scholar · View at Scopus