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Journal of Oncology
Volume 2010, Article ID 541957, 11 pages
http://dx.doi.org/10.1155/2010/541957
Review Article

Claudin Family of Proteins and Cancer: An Overview

1Department of Surgery, Vanderbilt University Medical Center, Nashville, TN 37232, USA
2Cancer Biology, Vanderbilt University Medical Center, Nashville, TN 37232, USA

Received 16 March 2010; Accepted 9 May 2010

Academic Editor: Ala-Eddin Al Moustafa

Copyright © 2010 Amar B. Singh 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. F. Zeng, A. B. Singh, and R. C. Harris, “The role of the EGF family of ligands and receptors in renal development, physiology and pathophysiology,” Experimental Cell Research, vol. 315, no. 4, pp. 602–610, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. J. D. Huber, K. A. Witt, S. Hom, R. D. Egleton, K. S. Mark, and T. P. Davis, “Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression,” American Journal of Physiology, vol. 280, no. 3, pp. H1241–H1248, 2001. View at Google Scholar · View at Scopus
  3. N. Sawada, M. Murata, K. Kikuchi et al., “Tight junctions and human diseases,” Medical Electron Microscopy, vol. 36, no. 3, pp. 147–156, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Wolburg, K. Wolburg-Buchholz, S. Liebner, and B. Engelhardt, “Claudin-1, claudin-2 and claudin-11 are present in tight junctions of choroid plexus epithelium of the mouse,” Neuroscience Letters, vol. 307, no. 2, pp. 77–80, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. J. M. Bronstein, S. Tiwari-Woodruff, A. G. Buznikov, and D. B. Stevens, “Involvement of OSP/claudin-11 in oligodendrocyte membrane interactions: role in biology and disease,” Journal of Neuroscience Research, vol. 59, no. 6, pp. 706–711, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Coraux, J. Roux, T. Jolly, and P. Birembaut, “Epithelial cell-extracellular matrix interactions and stem cells in airway epithelial regeneration,” Proceedings of the American Thoracic Society, vol. 5, no. 6, pp. 689–694, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. W. R. Lima, K. S. Parreira, O. Devuyst et al., “ZONAB promotes proliferation and represses differentiation of proximal tubule epithelial cells,” Journal of the American Society of Nephrology, vol. 21, no. 3, pp. 478–488, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Buchert, M. Papin, C. Bonnans et al., “Symplekin promotes tumorigenicity by up-regulating claudin-2 expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 6, pp. 2628–2633, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. M. S. Balda, M. D. Garrett, and K. Matter, “The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density,” Journal of Cell Biology, vol. 160, no. 3, pp. 423–432, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. M. E. Feigin and S. K. Muthuswamy, “Polarity proteins regulate mammalian cell-cell junctions and cancer pathogenesis,” Current Opinion in Cell Biology, vol. 21, no. 5, pp. 694–700, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Krause, L. Winkler, S. L. Mueller, R. F. Haseloff, J. Piontek, and I. E. Blasig, “Structure and function of claudins,” Biochimica et Biophysica Acta, vol. 1778, no. 3, pp. 631–645, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. T. A. Martin and W. G. Jiang, “Loss of tight junction barrier function and its role in cancer metastasis,” Biochimica et Biophysica Acta, vol. 1788, no. 4, pp. 872–891, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Miyoshi and Y. Takai, “Molecular perspective on tight-junction assembly and epithelial polarity,” Advanced Drug Delivery Reviews, vol. 57, no. 6, pp. 815–855, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. B. L. Daugherty, M. Mateescu, A. S. Patel et al., “Developmental regulation of claudin localization by fetal alveolar epithelial cells,” American Journal of Physiology, vol. 287, no. 6, pp. L1266–L1273, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. C. Gye, “Changes in the expression of claudins and transepithelial electrical resistance of mouse Sertoli cells by Leydig cell coculture,” International Journal of Andrology, vol. 26, no. 5, pp. 271–278, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. A. P. Soler, J. M. Mullin, K. A. Knudsen, and C. W. Marano, “Tissue remodeling during tumor necrosis factor-induced apoptosis in LLC-PK1 renal epithelial cells,” American Journal of Physiology, vol. 270, no. 5, pp. F869–F879, 1996. View at Google Scholar · View at Scopus
  17. M. D. McCartney and D. Cantu-Crouch, “Rabbit corneal epithelial wound repair: tight junction reformation,” Current Eye Research, vol. 11, no. 1, pp. 15–24, 1992. View at Google Scholar · View at Scopus
  18. T. E. Riehl and W. F. Stenson, “Mechanisms of transit of lipid mediators of inflammation and bacterial peptides across intestinal epithelia,” American Journal of Physiology, vol. 267, no. 4, pp. G687–G695, 1994. View at Google Scholar · View at Scopus
  19. J. L. Madara, C. Parkos, S. Colgan, A. Nusrat, K. Atisook, and P. Kaoutzani, “The movement of solutes and cells across tight junctions,” Annals of the New York Academy of Sciences, vol. 664, pp. 47–60, 1992. View at Publisher · View at Google Scholar · View at Scopus
  20. J. G. Swift, T. M. Mukherjee, and R. Rowland, “Intercellular junctions in hepatocellular carcinoma,” Journal of Submicroscopic Cytology, vol. 15, no. 3, pp. 799–810, 1983. View at Google Scholar · View at Scopus
  21. C.-A. Schoenenberger, A. Zuk, D. Kendall, and K. S. Matlin, “Multilayering and loss of apical polarity in MDCK cells transformed with viral K-ras,” Journal of Cell Biology, vol. 112, no. 5, pp. 873–889, 1991. View at Google Scholar · View at Scopus
  22. J. M. Mullin, K. V. Snock, R. D. Shurina et al., “Effects of acute vs. chronic phorbol ester exposure on transepithelial permeability and epithelial morphology,” Journal of Cellular Physiology, vol. 152, no. 1, pp. 35–47, 1992. View at Publisher · View at Google Scholar · View at Scopus
  23. J. M. Mullin, A. P. Soler, K. V. Laughlin et al., “Chronic exposure of LLC-PK1 epithelia to the phorbol ester TPA produces polyp-like foci with leaky tight junctions and altered protein kinase C-α expression and localization,” Experimental Cell Research, vol. 227, no. 1, pp. 12–22, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. J. M. Mullin, J. A. Kampherstein, K. V. Laughlin, D. T. Saladik, and A. P. Soler, “Transepithelial paracellular leakiness induced by chronic phorbol ester exposure correlates with polyp-like foci and redistribution of protein kinase C-α,” Carcinogenesis, vol. 18, no. 12, pp. 2339–2345, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. C. B. Collares-Buzato, M. A. Jepson, N. L. Simmons, and B. H. Hirst, “Increased tyrosine phosphorylation causes redistribution of adherens junction and tight junction proteins and perturbs paracellular barrier function in MDCK epithelia,” European Journal of Cell Biology, vol. 76, no. 2, pp. 85–92, 1998. View at Google Scholar · View at Scopus
  26. B. R. Stevenson, J. D. Siliciano, and M. S. Mooseker, “Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (Zonula Occludens) in a variety of epithelia,” Journal of Cell Biology, vol. 103, no. 3, pp. 755–766, 1986. View at Google Scholar · View at Scopus
  27. B. Gumbiner, T. Lowenkopf, and D. Apatira, “Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 8, pp. 3460–3464, 1991. View at Google Scholar · View at Scopus
  28. L. A. Jesaitis and D. A. Goodenough, “Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppressor protein,” Journal of Cell Biology, vol. 124, no. 6, pp. 949–961, 1994. View at Google Scholar · View at Scopus
  29. M. Itoh, A. Nagafuchi, S. Yonemura, T. Kitani-Yasuda, S. Tsukita, and S. Tsukita, “The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy,” Journal of Cell Biology, vol. 121, no. 3, pp. 491–502, 1993. View at Google Scholar · View at Scopus
  30. M. Furuse, T. Hirase, M. Itoh et al., “Occludin: a novel integral membrane protein localizing at tight junctions,” Journal of Cell Biology, vol. 123, no. 6, pp. 1777–1788, 1993. View at Publisher · View at Google Scholar · View at Scopus
  31. L. A. Williams, I. Martin-Padura, E. Dejana, N. Hogg, and D. L. Simmons, “Identification and characterization of human junctional adhesion molecule (JAM),” Molecular Immunology, vol. 36, no. 17, pp. 1175–1188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Furuse, K. Fujita, T. Hiiragi, K. Fujimoto, and S. Tsukita, “Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin,” Journal of Cell Biology, vol. 141, no. 7, pp. 1539–1550, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Bazzoni, “The JAM family of junctional adhesion molecules,” Current Opinion in Cell Biology, vol. 15, no. 5, pp. 525–530, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Sasaki, C. Matsui, K. Furuse, Y. Mimori-Kiyosue, M. Furuse, and S. Tsukita, “Dynamic behavior of paired claudin strands within apposing plasma membranes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 3971–3976, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Kanatsu-Shinohara, M. Ikawa, M. Takehashi et al., “Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 21, pp. 8018–8023, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Tsukita and M. Furuse, “Pores in the wall: claudins constitute tight junction strands containing aqueous pores,” Journal of Cell Biology, vol. 149, no. 1, pp. 13–16, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Tsukita, M. Furuse, and M. Itoh, “Multifunctional strands in tight junctions,” Nature Reviews Molecular Cell Biology, vol. 2, no. 4, pp. 285–293, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Rahner, L. L. Mitic, and J. M. Anderson, “Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut,” Gastroenterology, vol. 120, no. 2, pp. 411–422, 2001. View at Google Scholar · View at Scopus
  39. A. Nusrat, G. T. Brown, J. Tom et al., “Multiple protein interactions involving proposed extracellular loop domains of the tight junction protein occludin,” Molecular Biology of the Cell, vol. 16, no. 4, pp. 1725–1734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Itoh, M. Furuse, K. Morita, K. Kubota, M. Saitou, and S. Tsukita, “Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins,” Journal of Cell Biology, vol. 147, no. 6, pp. 1351–1363, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. M. H. Roh, C.-J. Liu, S. Laurinec, and B. Margolis, “The carboxyl terminus of zona occludens-3 binds and recruits a mammalian homologue of discs lost to tight junctions,” Journal of Biological Chemistry, vol. 277, no. 30, pp. 27501–27509, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Hamazaki, M. Itoh, H. Sasaki, M. Furuse, and S. Tsukita, “Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule,” Journal of Biological Chemistry, vol. 277, no. 1, pp. 455–461, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Yamamoto, N. Nishimura, S. Morimoto et al., “Distinct roles of Rab3B and Rab13 in the polarized transport of apical, basolateral, and tight junctional membrane proteins to the plasma membrane,” Biochemical and Biophysical Research Communications, vol. 308, no. 2, pp. 270–275, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. X. Wu, K. Hepner, S. Castelino-Prabhu et al., “Evidence for regulation of the PTEN tumor suppressor by a membrane-localized multi-PDZ domain containing scaffold protein MAGI-2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 8, pp. 4233–4238, 2000. View at Google Scholar · View at Scopus
  45. T. Nakamura, J. Blechman, S. Tada et al., “huASH1 protein, a putative transcription factor encoded by a human homologue of the Drosophila ash1 gene, localizes to both nuclei and cell-cell tight junctions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 13, pp. 7284–7289, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. E. R. Wilcox, Q. L. Burton, S. Naz et al., “Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29,” Cell, vol. 104, no. 1, pp. 165–172, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. J. H. Kang, H. J. Choi, H. Y. Cho et al., “Familial hypomagnesemia with hypercalciuria and nephrocalcinosis associated with CLDN16 mutations,” Pediatric Nephrology, vol. 20, no. 10, pp. 1490–1493, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Morita, H. Sasaki, K. Fujimoto, M. Furuse, and S. Tsukita, “Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis,” Journal of Cell Biology, vol. 145, no. 3, pp. 579–588, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Tan, S. Cruet-Hennequart, A. Troussard et al., “Regulation of tumor angiogenesis by integrin-linked kinase (ILK),” Cancer Cell, vol. 5, no. 1, pp. 79–90, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. S. L. Kominsky, P. Argani, D. Korz et al., “Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast,” Oncogene, vol. 22, no. 13, pp. 2021–2033, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Usami, H. Chiba, F. Nakayama et al., “Reduced expression of claudin-7 correlates with invasion and metastasis in squamous cell carcinoma of the esophagus,” Human Pathology, vol. 37, no. 5, pp. 569–577, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Sauer, M. K. Pedersen, K. Ebeltoft, and O. Næss, “Reduced expression of Claudin-7 in fine needle aspirates from breast carcinomas correlate with grading and metastatic disease,” Cytopathology, vol. 16, no. 4, pp. 193–198, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Michl, C. Barth, M. Buchholz et al., “Claudin-4 expression decreases invasiveness and metastatic potential of pancreatic cancer,” Cancer Research, vol. 63, no. 19, pp. 6265–6271, 2003. View at Google Scholar · View at Scopus
  54. L. B. A. Rangel, R. Agarwal, T. D'Souza et al., “Tight junction proteins claudin-3 and claudin-4 are frequently overexpressed in ovarian cancer but not in ovarian cystadenomas,” Clinical Cancer Research, vol. 9, no. 7, pp. 2567–2575, 2003. View at Google Scholar · View at Scopus
  55. Y. Soini, “Expression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours,” Histopathology, vol. 46, no. 5, pp. 551–560, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. J.-W. Lee, S.-J. Lee, J. Seo et al., “Increased expressions of claudin-1 and claudin-7 during the progression of cervical neoplasia,” Gynecologic Oncology, vol. 97, no. 1, pp. 53–59, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Agarwal, T. D'Souza, and P. J. Morin, “Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity,” Cancer Research, vol. 65, no. 16, pp. 7378–7385, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. Y.-C. Chao, S.-H. Pan, S.-C. Yang et al., “Claudin-1 is a metastasis suppressor and correlates with clinical outcome in lung adenocarcinoma,” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 2, pp. 123–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. P. Dhawan, A. B. Singh, N. G. Deane et al., “Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer,” Journal of Clinical Investigation, vol. 115, no. 7, pp. 1765–1776, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Jin, I. George Fantus, and J. Sun, “Wnt and beyond Wnt: multiple mechanisms control the transcriptional property of β-catenin,” Cellular Signalling, vol. 20, no. 10, pp. 1697–1704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. C. J. Gottardi, M. Arpin, A. S. Fanning, and D. Louvard, “The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 20, pp. 10779–10784, 1996. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Islas, J. Vega, L. Ponce, and L. González-Mariscal, “Nuclear localization of the tight junction protein ZO-2 in epithelial cells,” Experimental Cell Research, vol. 274, no. 1, pp. 138–148, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Reichert, T. Müller, and W. Hunziker, “The PDZ domains of zonula occludens-1 induce an epithelial to mesenchymal transition of Madin-Darby canine kidney I cells. Evidence for a role of β-catenin/Tcf/Lef signaling,” Journal of Biological Chemistry, vol. 275, no. 13, pp. 9492–9500, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. L. González-Mariscal, S. Lechuga, and E. Garay, “Role of tight junctions in cell proliferation and cancer,” Progress in Histochemistry and Cytochemistry, vol. 42, no. 1, pp. 1–57, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. O. Huber, R. Korn, J. McLaughlin, M. Ohsugi, B. G. Herrmann, and R. Kemler, “Nuclear localization of β-catenin by interaction with transcription factor LEF-1,” Mechanisms of Development, vol. 59, no. 1, pp. 3–10, 1996. View at Publisher · View at Google Scholar · View at Scopus
  66. J. C. Croce and D. R. McClay, “The canonical Wnt pathway in embryonic axis polarity,” Seminars in Cell and Developmental Biology, vol. 17, no. 2, pp. 168–174, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Wehrle, H. Lickert, R. Kemler, and A. D. Edward, “Wnt signaling in development,” in Handbook of Cell Signaling, pp. 789–792, Academic Press, Burlington, Vt, USA, 2003. View at Google Scholar
  68. R. Fodde, “The APC gene in colorectal cancer,” European Journal of Cancer, vol. 38, no. 7, pp. 867–871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Miwa, M. Furuse, S. Tsukita, N. Niikawa, Y. Nakamura, and Y. Furukawa, “Involvement of claudin-1 in the β-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers,” Oncology Research, vol. 12, no. 11-12, pp. 469–476, 2000. View at Google Scholar · View at Scopus
  70. J. Mankertz, B. Hillenbrand, S. Tavalali, O. Huber, M. Fromm, and J.-D. Schulzke, “Functional crosstalk between Wnt signaling and Cdx-related transcriptional activation in the regulation of the claudin-2 promoter activity,” Biochemical and Biophysical Research Communications, vol. 314, no. 4, pp. 1001–1007, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. K. W. Kinzler and B. Vogelstein, “Lessons from hereditary colorectal cancer,” Cell, vol. 87, no. 2, pp. 159–170, 1996. View at Publisher · View at Google Scholar · View at Scopus
  72. T. Flohr, J.-C. Dai, J. Büttner, O. Popanda, E. Hagmüller, and H. W. Thielmann, “Detection of mutations in the DNA polymerase δ gene of human sporadic colorectal cancers and colon cancer cell lines,” International Journal of Cancer, vol. 80, no. 6, pp. 919–929, 1999. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Bogenrieder and M. Herlyn, “Axis of evil: molecular mechanisms of cancer metastasis,” Oncogene, vol. 22, no. 43, pp. 6524–6536, 2003. View at Google Scholar · View at Scopus
  74. M. Takehara, T. Nishimura, S. Mima, T. Hoshino, and T. Mizushima, “Effect of claudin expression on paracellular permeability, migration and invasion of colonic cancer cells,” Biological and Pharmaceutical Bulletin, vol. 32, no. 5, pp. 825–831, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. H. Miyamori, T. Takino, Y. Kobayashi et al., “Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases,” Journal of Biological Chemistry, vol. 276, no. 30, pp. 28204–28211, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. M. K. Findley and M. Koval, “Regulation and roles for claudin-family tight junction proteins,” IUBMB Life, vol. 61, no. 4, pp. 431–437, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. K. Zhang, H.-P. Yao, and M.-H. Wang, “Activation of RON differentially regulates claudin expression and localization: role of claudin-1 in RON-mediated epithelial cell motility,” Carcinogenesis, vol. 29, no. 3, pp. 552–559, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. R. Macek, K. Swisshelm, and M. Kubbies, “Expression and function of tight junction associated molecules in human breast tumor cells is not affected by the Ras-MEK1 pathway,” Cellular and Molecular Biology, vol. 49, no. 1, pp. 1–11, 2003. View at Google Scholar · View at Scopus
  79. J. Pinkas and P. Leder, “MEK1 signaling mediates transformation and metastasis of EpH4 mammary epithelial cells independent of an epithelial to mesenchymal transition,” Cancer Research, vol. 62, no. 16, pp. 4781–4790, 2002. View at Google Scholar · View at Scopus
  80. H. Clarke, C. W. Marano, A. Peralta Soler, and J. M. Mullin, “Modification of tight junction function by protein kinase C isoforms,” Advanced Drug Delivery Reviews, vol. 41, no. 3, pp. 283–301, 2000. View at Publisher · View at Google Scholar · View at Scopus
  81. T. D'Souza, R. Agarwal, and P. J. Morin, “Phosphorylation of Claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells,” Journal of Biological Chemistry, vol. 280, no. 28, pp. 26233–26240, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. T. D'Souza, F. E. Indig, and P. J. Morin, “Phosphorylation of claudin-4 by PKCε regulates tight junction barrier function in ovarian cancer cells,” Experimental Cell Research, vol. 313, no. 15, pp. 3364–3375, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. L. González-Mariscal, R. Tapia, and D. Chamorro, “Crosstalk of tight junction components with signaling pathways,” Biochimica et Biophysica Acta, vol. 1778, no. 3, pp. 729–756, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Yamauchi, T. Rai, K. Kobayashi et al., “Disease-causing mutant WNK4 increases paracellular chloride permeability and phosphorylates claudins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 13, pp. 4690–4694, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. D. F. Balkovetz, E. R. Gerrard Jr., S. Li et al., “Gene expression alterations during HGF-induced dedifferentiation of a renal tubular epithelial cell line (MDCK) using a novel canine DNA microarray,” American Journal of Physiology, vol. 286, no. 4, pp. F702–F710, 2004. View at Google Scholar · View at Scopus
  86. Y. Peter, A. Comellas, E. Levantini, E. P. Ingenito, and S. D. Shapiro, “Epidermal growth factor receptor and claudin-2 participate in A549 permeability and remodeling: implications for non-small cell lung cancer tumor colonization,” Molecular Carcinogenesis, vol. 48, no. 6, pp. 488–497, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. A. B. Singh and R. C. Harris, “Epidermal growth factor receptor activation differentially regulates claudin expression and enhances transepithelial resistance in Madin-Darby canine kidney cells,” Journal of Biological Chemistry, vol. 279, no. 5, pp. 3543–3552, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. T. A. Martin, G. Watkins, R. E. Mansel, and W. G. Jiang, “Hepatocyte growth factor disrupts tight junctions in human breast cancer cells,” Cell Biology International, vol. 28, no. 5, pp. 361–371, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Kinugasa, T. Sakaguchi, X. Gu, and H. Reinecker, “Claudins regulate the intestinal barrier in response to immune mediators,” Gastroenterology, vol. 118, no. 6, pp. 1001–1011, 2000. View at Google Scholar · View at Scopus
  90. M. Matsuda, A. Kubo, M. Furuse, and S. Tsukita, “A peculiar internalization of claudins, tight junction-specific adhesion molecules, during the intercellular movement of epithelial cells,” Journal of Cell Science, vol. 117, no. 7, pp. 1247–1257, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. C. M. Van Itallie, T. M. Gambling, J. L. Carson, and J. M. Anderson, “Palmitoylation of claudins is required for efficient tight-junction localization,” Journal of Cell Science, vol. 118, no. 7, pp. 1427–1436, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. J. Ikenouchi, M. Matsuda, M. Furuse, and S. Tsukita, “Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail,” Journal of Cell Science, vol. 116, no. 10, pp. 1959–1967, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. F. Escaffit, F. Boudreau, and J.-F. Beaulieu, “Differential expression of claudin-2 along the human intestine: implication of GATA-4 in the maintenance of claudin-2 in differentiating cells,” Journal of Cellular Physiology, vol. 203, no. 1, pp. 15–26, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. T. Sakaguchi, X. Gu, H. M. Golden, E. Suh, D. B. Rhoads, and H.-C. Reinecker, “Cloning of the human claudin-2 5′-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1α,” Journal of Biological Chemistry, vol. 277, no. 24, pp. 21361–21370, 2002. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Krishnan, A. B. Singh, J. J. Smith et al., “HDAC inhibitors regulate claudin-1 expression in colon cancer cells through modulation of mRNA stability,” Oncogene, vol. 29, pp. 305–312, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. S.-R. Shiou, A. B. Singh, K. Moorthy et al., “Smad4 regulates claudin-1 expression in a transforming growth factor-β-independent manner in colon cancer cells,” Cancer Research, vol. 67, no. 4, pp. 1571–1579, 2007. View at Publisher · View at Google Scholar · View at Scopus