Regulation and roles for claudin-family tight junction proteins

IUBMB Life

Volumn 61, Issue 4, 2009, Pages 431-437

  Findley, Mary K ^a   Koval, Michael ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Claudin; Epithelium; Occluding; Tetraspanin; Tight junction; Zonula occludens

Indexed keywords

CLAUDIN; OCCLUDIN; SCAFFOLD PROTEIN; CLDND1 PROTEIN, HUMAN; MEMBRANE PROTEIN; NERVE PROTEIN;

CELL MEMBRANE PERMEABILITY; CELL TRANSFORMATION; ENDOCYTOSIS; EPITHELIUM CELL; INFLAMMATION; MESENCHYME CELL; PALMITOYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; TIGHT JUNCTION; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIPOYLATION; METABOLISM; MULTIGENE FAMILY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING;

CELL DIFFERENTIATION; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LIPOYLATION; MEMBRANE PROTEINS; MULTIGENE FAMILY; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TIGHT JUNCTIONS;

EID: 67650348496     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.175     Document Type: Review

References (79)

1. Schneeberger, E. E., and Lynch, R. D. (2004) The tight junction: A multifunctional complex. Am. J. Physiol. Cell Physiol. 286, C1213-C1228.
2. Angelow, S., Ahlstrom, R., and Yu, A. S. (2008) Biology of Claudins. Am. J. Physiol. Renal. Physiol. 295, F867-F876.
3. Turksen, K., and Troy, T. C. (2004) Permeability barrier dysfuntion in transgenic mice overexpressing claudin 6. Development 129, 1775-1784. (Pubitemid 34874193)
4. Koval, M. (2006) Claudins--key pieces in the tight junction puzzle. Cell Commun. Adhes. 13, 127-138.
5. Morita, K., Furuse, M., Fujimoto, K., and Tsukita, S. (1999) Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA 96, 511-516.
6. Van Itallie, C. M., Rogan, S., Yu, A., Vidal, L. S., Holmes, J., and Anderson, J. M. (2006) Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am. J. Physiol. Renal. Physiol. 291, F1288-F1299.
7. Niimi, T., Nagashima, K., Ward, J. M., Minoo, P., Zimonjic, D. B., Popescu, N. C., and Kimura, S. (2001) Claudin-18, a novel downstream target gene for the T/EBP/NKX2.1 homeodomain transcription factor, encodes lung- and stomach-specific isoforms through alternative splicing. Mol. Cell Biol. 21, 7380-7390.
8. Umeda, K., Ikenouchi, J., Katahira-Tayama, S., Furuse, K., Sasaki, H., Nakayama, M., Matsui, T., Tsukita, S., and Furuse, M. (2006) ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126, 741-754. (Pubitemid 44233624)
9. Van Itallie, C. M., and Anderson, J. M. (2006) Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68, 403-429.
10. Piontek, J., Winkler, L., Wolburg, H., Muller, S. L., Zuleger, N., Piehl, C., Wiesner, B., Krause, G., and Blasig, I. E. (2008) Formation of tight junction: Determinants of homophilic interaction between classic claudins. FASEB J. 22, 146-158.
11. Tsukita, S., and Furuse, M. (2002) Claudin-based barrier in simple and stratified cellular sheets. Curr. Opin. Cell Biol. 14, 531-536.
12. Coyne, C. B., Gambling, T. M., Boucher, R. C., Carson, J. L., and Johnson, L. G. (2003) Role of claudin interactions in airway tight junctional permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L1166-L1178.
13. Mitic, L. L., Unger, V. M., and Anderson, J. M. (2003) Expression, solubilization, and biochemical characterization of the tight junction transmembrane protein claudin-4. Protein Sci. 12, 218-227.
14. Van Itallie, C. M., Gambling, T. M., Carson, J. L., and Anderson, J. M. (2005) Palmitoylation of claudins is required for efficient tight-junction localization. J. Cell Sci. 118, 1427-1436. (Pubitemid 40585123)
15. Nusrat, A., Parkos, C. A., Verkade, P., Foley, C. S., Liang, T. W., Innis-Whitehouse, W., Eastburn, K. K., and Madara, J. L. (2000) Tight junctions are membrane microdomains. J. Cell Sci. 113, (Part 10), 1771-1781. (Pubitemid 30333126)
16. Hemler, M. E. (2005) Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6, 801-811.
17. Kovalenko, O. V., Yang, X. H., and Hemler, M. E. (2007) A novel cysteine cross-linking method reveals a direct association between claudin-1 and tetraspanin CD9. Mol. Cell Proteomics 6, 1855-1867.
18. Evans, M. J., von Hahn, T., Tscherne, D. M., Syder, A. J., Panis, M., Wolk, B., Hatziioannou, T., McKeating, J. A., Bieniasz, P. D., and Rice, C. M. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446, 801-805. (Pubitemid 46582027)
19. Furuse, M., Sasaki, H., and Tsukita, S. (1999) Manner of interaction of heterogeneous claudin species within and between tight junction strands. J. Cell Biol. 147, 891-903.
20. Blasig, I. E., Winkler, L., Lassowski, B., Mueller, S. L., Zuleger, N., Krause, E., Krause, G., Gast, K., Kolbe, M., and Piontek, J. (2006) On the self-association potential of transmembrane tight junction proteins. Cell. Mol. Life Sci. 63, 505-514.
21. Daugherty, B. L., Ward, C., Smith, T., Ritzenthaler, J. D., and Koval, M. (2007) Regulation of heterotypic claudin compatibility. J. Biol. Chem. 282, 30005-30013.
22. Tsukita, S., and Furuse, M. (1999) Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol. 9, 268-273.
23. Saitou, M., Furuse, M., Sasaki, H., Schulzke, J. D., Fromm, M., Takano, H., Noda, T., and Tsukita, S. (2000) Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol. Biol. Cell 11, 4131-4142.
24. Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K., and Tsukita, S. (1998) Claudin-1 and -2: Novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141, 1539-1550.
25. Nusrat, A., Brown, G. T., Tom, J., Drake, A., Bui, T. T., Quan, C., and Mrsny, R.J. (2005) Multiple protein interactions involving proposed extracellular loop domains of the tight junction protein occludin. Mol. Biol. Cell 16, 1725-1734.
26. Balda, M. S., Whitney, J. A., Flores, C., Gonzalez, S., Cereijido, M., and Matter, K. (1996) Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apicalbasolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell Biol. 134, 1031-1049.
27. Mrsny, R. J., Brown, G. T., Gerner-Smidt, K., Buret, A. G., Meddings, J. B., Quan, C., Koval, M., and Nusrat, A. (2008) A key claudin extracellular loop domain is critical for epithelial barrier integrity. Am. J. Pathol. 172, 905-915.
28. Itoh, M., Furuse, M., Morita, K., Kubota, K., Saitou, M., and Tsukita, S. (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J. Cell Biol. 147, 1351-1363.
29. Poliak, S., Matlis, S., Ullmer, C., Scherer, S. S., and Peles, E. (2002) Distinct claudins and associated PDZ proteins form different autotypic tight junctions in myelinating Schwann cells. J. Cell Biol. 159, 361-372.
30. Roh, M. H., Makarova, O., Liu, C. J., Shin, K., Lee, S., Laurinec, S., Goyal, M., Wiggins, R., and Margolis, B. (2002) The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell Biol. 157, 161-172.
31. Van Itallie, C. M., Colegio, O. R., and Anderson, J. M. (2004) The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability. J. Membr. Biol. 199, 29-38.
32. D'Souza, T., Agarwal, R., and Morin, P. J. (2005) Phosphorylation of claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells. J. Biol. Chem. 280, 26233-26240.
33. Ikari, A., Matsumoto, S., Harada, H., Takagi, K., Hayashi, H., Suzuki, Y., Degawa, M., and Miwa, M. (2006) Phosphorylation of paracellin-1 at Ser217 by protein kinase A is essential for localization in tight junctions. J. Cell. Sci. 119, 1781-1789.
34. Banan, A., Zhang, L. J., Shaikh, M., Fields, J. Z., Choudhary, S., Forsyth, C. B., Farhadi, A., and Keshavarzian, A. (2005) Theta Isoform of protein kinase C alters barrier function in intestinal epithelium through modulation of distinct claudin isotypes: A novel mechanism for regulation of permeability. J. Pharmacol. Exp. Ther. 313, 962-982.
35. Nunbhakdi-Craig, V., Machleidt, T., Ogris, E., Bellotto, D., White, C. L., III, and Sontag, E. (2002) Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J. Cell Biol. 158, 967-978.
36. Fernandez, A. L., Koval, M., Fan, X., and Guidot, D. M. (2007) Chronic alcohol ingestion alters claudin expression in the alveolar epithelium of rats. Alcohol 41, 371-379.
37. Haorah, J., Heilman, D., Knipe, B., Chrastil, J., Leibhart, J., Ghorpade, A., Miller, D. W., and Persidsky, Y. (2005) Ethanol-induced activation of myosin light chain kinase leads to dysfunction of tight junctions and blood-brain barrier compromise. Alcohol Clin. Exp. Res. 29, 999-1009.
38. Turner, J. R., Angle, J. M., Black, E. D., Joyal, J. L., Sacks, D. B., and Madara, J. L. (1999) PKC-dependent regulation of transepithelial resistance: roles of MLC and MLC kinase. Am. J. Physiol. 277, C554-C562.
39. Prasad, S., Mingrino, R., Kaukinen, K., Hayes, K. L., Powell, R. M., MacDonald, T. T., and Collins, J. E. (2005) Inflammatory processes have differential effects on claudins 2, 3, and 4 in colonic epithelial cells. Lab. Invest. 85, 1139-1162.
40. Tanaka, M., Kamata, R., and Sakai, R. (2005) EphA2 phosphorylates the cytoplasmic tail of Claudin-4 and mediates paracellular permeability. J. Biol. Chem. 280, 42375-42382.
41. Pasquale, E. B. (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6, 462-475.
42. Carrozzino, F., Soulie, P., Huber, D., Mensi, N., Orci, L., Cano, A., Feraille, E., and Montesano, R. (2005) Inducible expression of Snail selectively increases paracellular ion permeability and differentially modulates tight junction proteins. Am. J. Physiol. Cell Physiol. 289, C1002-C1014.
43. Ikenouchi, J., Matsuda, M., Furuse, M., and Tsukita, S. (2003) Regulation of tight junctions during the epithelium-mesenchyme transition: Direct repression of the gene expression of claudins/occludin by Snail. J. Cell. Sci. 116, 1959-1967.
44. Sasaki, H., Matsui, C., Furuse, K., Mimori-Kiyosue, Y., Furuse, M., and Tsukita, S. (2003) Dynamic behavior of paired claudin strands within apposing plasma membranes. Proc. Natl. Acad. Sci. USA 100, 3971-3976.
45. Shen, L., Weber, C. R., and Turner, J. R. (2008) The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J. Cell Biol. 181, 683-695.
46. Ivanov, A. I., Nusrat, A., and Parkos, C. A. (2004) Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell 15, 176-188.
47. Daugherty, B. L., Mateescu, M., Patel, A. S., Wade, K., Kimura, S., Gonzales, L. W., Guttentag, S., Ballard, P. L., and Koval, M. (2004) Developmental regulation of claudin localization by fetal alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L1266-L1273.
48. Jordan, K., Chodock, R., Hand, A. R., and Laird, D. W. (2001) The origin of annular junctions: a mechanism of gap junction internalization. J. Cell Sci. 114, 763-773.
49. Fedwick, J. P., Lapointe, T. K., Meddings, J. B., Sherman, P. M., and Buret, A. G. (2005) Helicobacter pylori activates myosin light-chain kinase to disrupt claudin-4 and claudin-5 and increase epithelial permeability. Infect. Immun. 73, 7844-7852.
50. Hopkins, A. M., Walsh, S. V., Verkade, P., Boquet, P., and Nusrat, A. (2003) Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J. Cell Sci. 116, 725-742.
51. Fujita, K., Katahira, J., Horiguchi, Y., Sonoda, N., Furuse, M., and Tsukita, S. (2000) Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein. FEBS Lett. 476, 258-261.
52. Walsh, S. V., Hopkins, A. M., and Nusrat, A. (2000) Modulation of tight junction structure and function by cytokines. Adv. Drug Deliv. Rev. 41, 303-313.
53. Bruewer, M., Utech, M., Ivanov, A. I., Hopkins, A. M., Parkos, C. A., and Nusrat, A. (2005) Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J 19, 923-933.
54. Tedelind, S., Ericson, L. E., Karlsson, J. O., and Nilsson, M. (2003) Interferon-gamma down-regulates claudin-1 and impairs the epithelial barrier function in primary cultured human thyrocytes. Eur. J. Endocrinol. 149, 215-221.
55. Heller, F., Florian, P., Bojarski, C., Richter, J., Christ, M., Hillenbrand, B., Mankertz, J., Gitter, A. H., Burgel, N., Fromm, M., Zeitz, M., Fuss, I., Strober, W., and Schulzke, J. D. (2005) Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129, 550-564.
56. Laukoetter, M. G., Nava, P., Lee, W. Y., Severson, E. A., Capaldo, C. T., Babbin, B. A., Williams, I. R., Koval, M., Peatman, E., Campbell, J. A., Dermody, T. S., Nusrat, A., and Parkos C. A. (2007). JAMA regulates permeability and inflammation in the intestine in vivo. J. Exp. Med. 204, 3067-3076.
57. Wang, F., Daugherty, B., Keise, L. L., Wei, Z., Foley, J. P., Savani, R. C., and Koval, M. (2003) Heterogeneity of claudin expression by alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 29, 62-70.
58. Hadj-Rabia, S., Baala, L., Vabres, P., Hamel-Teillac, D., Jacquemin, E., Fabre, M., Lyonnet, S., De Prost, Y., Munnich, A., Hadchouel, M., and Smahi, A. (2004) Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology 127, 1386-1390.
59. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A., and Tsukita, S. (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J. Cell Biol. 156, 1099-1111.
60. Wattenhofer, M., Reymond, A., Falciola, V., Charollais, A., Caille, D., Borel, C., Lyle, R., Estivill, X., Petersen, M. B., Meda, P., and Antonarakis, S. E. (2005) Different mechanisms preclude mutant CLDN14 proteins from forming tight junctions in vitro. Hum. Mutat. 25, 543-549.
61. Ben-Yosef, T., Belyantseva, I. A., Saunders, T. L., Hughes, E. D., Kawamoto, K., Van Itallie, C. M., Beyer, L. A., Halsey, K., Gardner, D. J., Wilcox, E. R., Rasmussen, J., Anderson, J. M., Dolan, D. F., Forge, A., Raphael, Y., Camper, S. A., and Friedman, T. B. (2003) Claudin 14 knockout mice, a model for autosomal recessive deafness DFNB29, are deaf due to cochlear hair cell degeneration. Hum. Mol. Genet. 12, 2049-2061.
62. Konrad, M., Schaller, A., Seelow, D., Pandey, A. V., Waldegger, S., Lesslauer, A., Vitzthum, H., Suzuki, Y., Luk, J. M., Becker, C., Schlingmann, K. P., Schmid, M., Rodriguez-Soriano, J., Ariceta, G., Cano, F., Enriquez, R., Juppner, H., Bakkaloglu, S. A., Hediger, M. A., Gallati, S., Neuhauss, S. C., Nurnberg, P., and Weber, S. (2006) Mutations in the tight-junction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am. J. Hum. Genet. 79, 949-957.
63. Weber, S., Schneider, L., Peters,M.,Misselwitz, J., Ronnefarth, G., Boswald, M., Bonzel, K. E., Seeman, T., Sulakova, T., Kuwertz-Broking, E., Gregoric, A., Palcoux, J. B., Tasic, V., Manz, F., Scharer, K., Seyberth, H. W., and Konrad, M. (2001) Novel paracellin-1 mutations in 25 families with familial hypomagnesemia with hypercalciuria and nephrocalcinosis. J. Am. Soc. Nephrol. 12, 1872-1881.
64. Hou, J., Renigunta, A., Konrad, M., Gomes, A. S., Schneeberger, E. E., Paul, D. L., Waldegger, S., and Goodenough, D. A. (2008) Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J. Clin. Invest. 118, 619-628.
65. Angelow, S., and Yu, A. S. (2007) Claudins and paracellular transport: An update. Curr. Opin. Nephrol. Hypertens. 16, 459-464.
66. Yang, J., and Weinberg, R. A. (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829.
67. Radisky, D. C., Kenny, P. A., and Bissell, M. J. (2007) Fibrosis and cancer: Do myofibroblasts come also from epithelial cells via EMT? J. Cell. Biochem. 101, 830-839.
68. Martinez-Estrada, O. M., Culleres, A., Soriano, F. X., Peinado, H., Bolos, V., Martinez, F. O., Reina, M., Cano, A., Fabre, M., and Vilaro, S. (2006) The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 394, 449-457.
69. Ohkubo, T., and Ozawa, M. (2004) The transcription factor Snail down-regulates the tight junction components independently of E-cadherin downregulation. J. Cell. Sci. 117, 1675-1685.
70. Oliveira, S. S., and Morgado-Diaz, J. A. (2007) Claudins: Multifunctional players in epithelial tight junctions and their role in cancer. Cell. Mol. Life Sci. 64, 17-28.
71. Sauer, T., Pedersen, M. K., Ebeltoft, K., and Naess, O. (2005) Reduced expression of Claudin-7 in fine needle aspirates from breast carcinomas correlate with grading and metastatic disease. Cytopathology 16, 193-198.
72. Montogomery, E., Mamelak, A. J., Gibson, M., Maitra, A., Sheikh, S., Amr, S. S., Yang, S., Brock, M., Forastiere, A., Zhang, S., Murphy, K. M., and Berg, K. D. (2006). Overexpression of claudin proteins in esophageal adenocarcinoma and its precursor lesions. Appl. Immunohistochem. Mol. Morphol. 14, 24-30.
73. Tokes, A. M., Kulka, J., Paku, S., Szik, A., Paska, C., Novak, P. K., Szilak, L., Kiss, A., Bogi, K., and Schaff, Z. (2005) Claudin-1, -3 and - 4 proteins and mRNA expression in benign and malignant breast lesions: A research study. Breast Cancer Res. 7, R296-R305.
74. Dhawan, P., Singh, A. B., Deane, N. G., No, Y., Shiou, S. R., Schmidt, C., Neff, J., Washington, M. K., and Beauchamp, R. D. (2005) Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J. Clin. Invest. 115, 1765-1776.
75. Cunningham, S. C., Kamangar, F., Kim, M. P., Hammoud, S., Haque, R., lacobuzio-Donahue, C. A., Maitra, A., Ashfaq, R., Hustinx, S., Heitmiller, R. E., Choti, M. A., Lillemoe, K. D., Cameron, J. L., Yao, C. J., Schulick, R. D., and Montgormery, E. (2006) Claudin-4, mitogen-activated protein kinase 4, and stratifin are markers of gastric adenocarcinoma precursor lesions. Cancer Epidemiol. Biomarkers. Prev 15, 281-287.
76. Kominsky, S. L. (2006) Claudins: Emerging targets for cancer therapy. Expert Rev. Mol. Med. 8, 1-11.
77. Kominsky, S. L., Vali, M., Korz, D., Gabig, T. G., Weitzman, S. A., Argani, P., and Sukumar, S. (2004) Clostridium perfringens enterotoxin elicits rapid and specific cytolysis of breast carcinoma cells mediated through tight junction proteins claudin 3 and 4. Am. J. Pathol. 164, 1627-1633.
78. Michl, P., Buchholz, M., Rolke, M., Kunsch, S., Lohr, M., McClane, B., Tsukita, S., Leder, G., Adler, G., and Gress, T. M. (2001) Claudin-4: A new target for pancreatic cancer treatment using Clostridium perfringens enterotoxin. Gastroenterology 121, 678-684.
79. Van Itallie, C. M., Betts, L., Smedley, J. G., III, McClane, B. A., and Anderson, J. M. (2008) Structure of the claudin-binding domain of Clostridium perfringens enterotoxin. J. Biol. Chem. 283, 268-274.