Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 936401, 12 pages
http://dx.doi.org/10.1155/2014/936401
Research Article

The K–Cl Cotransporter KCC3 as an Independent Prognostic Factor in Human Esophageal Squamous Cell Carcinoma

1Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, Kyoto 602-8566, Japan
2Department of Pathology, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan
3Departments of Molecular Cell Physiology and Bio-Ionomics, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan
4Japan Institute for Food Education and Health, St. Agnes’ University, Kyoto 602-8013, Japan

Received 22 May 2014; Accepted 16 June 2014; Published 9 July 2014

Academic Editor: Akio Tomoda

Copyright © 2014 Atsushi Shiozaki 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. K. Lauf and N. C. Adragna, “K-Cl cotransport: properties and molecular mechanism,” Cellular Physiology and Biochemistry, vol. 10, no. 5-6, pp. 341–354, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. P. B. Dunham, G. W. Stewart, and J. C. Ellory, “Chloride-activated passive potassium transport in human erythrocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 3, pp. 1711–1715, 1980. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. F. Chen, C. Y. Chou, J. C. Ellory, and M. R. Shen, “The emerging role of KCl cotransport in tumor biology,” The American Journal of Translational Research, vol. 2, no. 4, pp. 345–355, 2010. View at Google Scholar · View at Scopus
  4. D. B. Mount, A. Mercado, L. Song et al., “Cloning and characterization of KCC3 and KCC4, new members of the cation-chloride cotransporter gene family,” The Journal of Biological Chemistry, vol. 274, no. 23, pp. 16355–16362, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. C. M. Gillen, S. Brill, J. A. Payne, and B. Forbush III, “Molecular cloning and functional expression of the K-Cl cotransporter from rabbit, rat, and human: A new member of the cation-chloride cotransporter family,” Journal of Biological Chemistry, vol. 271, no. 27, pp. 16237–16244, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. J. A. Payne, T. J. Stevenson, and L. F. Donaldson, “Molecular characterization of a putative K-Cl cotransporter in rat brain: a neuronal-specific isoform,” Journal of Biological Chemistry, vol. 271, no. 27, pp. 16245–16252, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. J. E. Race, F. N. Makhlouf, P. J. Logue, F. H. Wilson, P. B. Dunham, and E. J. Holtzman, “Molecular cloning and functional characterization of KCC3, a new K-Cl cotransporter,” The American Journal of Physiology, vol. 277, no. 6, part 1, pp. C1210–C1219, 1999. View at Google Scholar · View at Scopus
  8. Y. M. Hsu, Y. F. Chen, C. Y. Chou et al., “KCl cotransporter-3 down-regulates E-cadherin/β-catenin complex to promote epithelial-mesenchymal transition,” Cancer Research, vol. 67, no. 22, pp. 11064–11073, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. M. Hsu, C. Y. Chou, H. H. Chen et al., “IGF-1 upregulates electroneutral K-Cl cotransporter KCC3 and KCC4 which are differentially required for breast cancer cell proliferation and invasiveness,” Journal of Cellular Physiology, vol. 210, no. 3, pp. 626–636, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. F. Chen, C. Y. Chou, R. J. Wilkins, J. C. Ellory, D. B. Mount, and M. Shen, “Motor protein-dependent membrane trafficking of KCl cotransporter-4 is important for cancer cell invasion,” Cancer Research, vol. 69, no. 22, pp. 8585–8593, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Kitagawa, N. Niisato, A. Shiozaki et al., “A regulatory role of K+-Cl- cotransporter in the cell cycle progression of breast cancer MDA-MB-231 cells,” Archives of Biochemistry and Biophysics, vol. 539, no. 1, pp. 92–98, 2013. View at Google Scholar
  12. K. B. Gagnon, “High-grade glioma motility reduced by genetic knockdown of KCC3,” Cellular Physiology and Biochemistry, vol. 30, no. 2, pp. 466–476, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. M. R. Shen, C. Y. Chou, K. F. Hsu et al., “The KCI cotransporter isoform KCC3 can play an important role in cell growth regulation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 25, pp. 14714–14719, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Sobin, M. Gospodarowicz, and C. Wittekind, Eds., TNM Classification of Malignant Tumors, John Wiley & Sons, Hoboken, NJ, USA, 7th edition, 2009.
  15. W. Remmele and H. E. Stegner, “Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue,” Pathologe, vol. 8, no. 3, pp. 138–140, 1987. View at Google Scholar · View at Scopus
  16. T. Nishihira, Y. Hashimoto, M. Katayama, S. Mori, and T. Kuroki, “Molecular and cellular features of esophageal cancer cells,” Journal of Cancer Research and Clinical Oncology, vol. 119, no. 8, pp. 441–449, 1993. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Kunzelmann, “Ion channels and cancer,” Journal of Membrane Biology, vol. 205, no. 3, pp. 159–173, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Schönherr, “Clinical relevance of ion channels for diagnosis and therapy of cancer,” The Journal of Membrane Biology, vol. 205, no. 3, pp. 175–184, 2005. View at Google Scholar
  19. C. J. Kim, Y. G. Cho, S. W. Jeong et al., “Altered expression of KCNK9 in colorectal cancers,” APMIS, vol. 112, no. 9, pp. 588–594, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. X. D. Shao, K. C. Wu, Z. M. Hao, L. Hong, J. Zhang, and D. Fan, “The potent inhibitory effects of cisapride, a specific blocker for human ether-a-go-go-related gene (HERG) channel, on gastric cancer cells,” Cancer Biology and Therapy, vol. 4, no. 3, pp. 295–301, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. X. Wang, Y. Nagaba, H. S. Cross, F. Wrba, L. Zhang, and S. E. Guggino, “The mRNA of L-type calcium channel elevated in colon cancer: protein distribution in normal and cancerous colon,” The American Journal of Pathology, vol. 157, no. 5, pp. 1549–1562, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Cai, X. Ding, K. Zhou et al., “Blockade of TRPC6 channels induced G2/M phase arrest and suppressed growth in human gastric cancer cells,” International Journal of Cancer, vol. 125, no. 10, pp. 2281–2287, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Wu, Y.-C. Zhang, W.-H. Suo et al., “Induction of anion exchanger-1 translation and its opposite roles in the carcinogenesis of gastric cancer cells and differentiation of K562 cells,” Oncogene, vol. 29, no. 13, pp. 1987–1996, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Nagata, X. Che, K. Miyazawa et al., “Rapid decrease of intracellular pH associated with inhibition of Na +/H+ exchanger precedes apoptotic events in the MNK45 and MNK74 gastric cancer cell lines treated with 2-aminophenoxazine-3-one,” Oncology Reports, vol. 25, no. 2, pp. 341–346, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Chen, C. Röcken, J. Hoffmann et al., “Expression of carbonic anhydrase 9 at the invasion front of gastric cancers,” Gut, vol. 54, no. 7, pp. 920–927, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. C. D. Chen, C. S. Wang, Y. H. Huang et al., “Overexpression of CLIC1 in human gastric carcinoma and its clinicopathological significance,” Proteomics, vol. 7, no. 1, pp. 155–167, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Shiozaki, E. Otsuji, and Y. Marunaka, “Intracellular chloride regulates the G1/S cell cycle progression in gastric cancer cells,” World Journal of Gastrointestinal Oncology, vol. 3, no. 8, pp. 119–122, 2011. View at Google Scholar
  28. H. Miyazaki, A. Shiozaki, N. Niisato et al., “Chloride ions control the G1/S cell-cycle checkpoint by regulating the expression of p21 through a p53-independent pathway in human gastric cancer cells,” Biochemical and Biophysical Research Communications, vol. 366, no. 2, pp. 506–512, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Ohsawa, H. Miyazaki, N. Niisato et al., “Intracellular chloride regulates cell proliferation through the activation of stress-activated protein kinases in MKN28 human gastric cancer cells,” Journal of Cellular Physiology, vol. 223, no. 3, pp. 764–770, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Sasagawa, A. Shiozaki, D. Iitaka et al., “Ki-67 labeling index as an independent prognostic factor in human esophageal squamous cell carcinoma,” Esophagus, vol. 9, no. 4, pp. 195–202, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Nakashima, A. Shiozaki, D. Ichikawa et al., “Anti-phosphohistone H3 as an independent prognostic factor in human esophageal squamous cell carcinoma,” Anticancer Research, vol. 33, no. 2, pp. 461–467, 2013. View at Google Scholar · View at Scopus
  32. A. Shiozaki, S. Nakashima, D. Ichikawa et al., “Prognostic significance of p21 expression in patients with esophageal squamous cell carcinoma,” Anticancer Research, vol. 33, no. 10, pp. 4329–4335, 2013. View at Google Scholar
  33. T. Ishimoto, A. Shiozaki, D. Ichikawa et al., “E2F5 as an independent prognostic factor in esophageal squamous cell carcinoma,” Anticancer Research, vol. 33, no. 12, pp. 5415–5420, 2013. View at Google Scholar
  34. B. Jiang, N. Hattori, B. Liu et al., “Expression and roles of Cl-channel ClC-5 in cell cycles of myeloid cells,” Biochemical and Biophysical Research Communications, vol. 317, no. 1, pp. 192–197, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Menegazzi, S. Busetto, P. Dri, R. Cramer, and P. Patriarca, “Chloride ion efflux regulates adherence, spreading, and respiratory burst of neutrophils stimulated by tumor necrosis factor-α (TNF) on biologic surfaces,” Journal of Cell Biology, vol. 135, no. 2, pp. 511–522, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. N. Niisato, D. C. Eaton, and Y. Marunaka, “Involvement of cytosolic Cl in osmoregulation of α-ENaC gene expression,” The American Journal of Physiology: Renal Physiology, vol. 287, no. 5, pp. F932–F939, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Shiozaki, H. Miyazaki, N. Niisato et al., “Furosemide, a blocker of Na+/K+/2Cl- cotransporter, diminishes proliferation of poorly differentiated human gastric cancer cells by affecting G0/G1 state,” Journal of Physiological Sciences, vol. 56, no. 6, pp. 401–406, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Hiraoka, H. Miyazaki, N. Niisato et al., “Chloride ion modulates cell proliferation of human androgen-independent prostatic cancer cell,” Cellular Physiology and Biochemistry, vol. 25, no. 4-5, pp. 379–388, 2010. View at Publisher · View at Google Scholar · View at Scopus