Emerging multifunctional roles of claudin tight junction proteins in bone

Endocrinology

Volumn 155, Issue 7, 2014, Pages 2363-2376

  Alshbool, Fatima Z ^a,b   Mohan, Subburaman ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN; TIGHT JUNCTION PROTEIN;

BONE; BONE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION; HOMEOSTASIS; HUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPOROSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SHORT SURVEY;

ANIMALS; BONE AND BONES; BONE REMODELING; BONE RESORPTION; CELL DIFFERENTIATION; CLAUDINS; GENE EXPRESSION; HUMANS; OSTEOCLASTS; TIGHT JUNCTION PROTEINS;

EID: 84903286833     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1173     Document Type: Short Survey

References (169)

1. Elkouby-Naor L, Ben-Yosef T. Functions of claudin tight junction proteins and their complex interactions in various physiological systems. Int Rev Cell Mol Biol. 2010;279:1-32.
2. Lecanda F, Warlow PM, Sheikh S, Furlan F, Steinberg TH, Civitelli R. Connexin43 deficiency causes delayed ossification, craniofacial abnormalities, and osteoblast dysfunction. J Cell Biol. 2000;151:931-944.
3. Cheng SL, Shin CS, Towler DA, Civitelli R. A dominant negative cadherin inhibits osteoblast differentiation. J Bone Miner Res. 2000;15:2362-2370.
4. Weinger JM, Holtrop ME. An ultrastructural study of bone cells: the occurrence of microtubules, microfilaments and tight junctions. Calcif Tissue Res. 1974;14:15-29.
5. Soares AM, Arana-Chavez VE, Reid AR, Katchburian E. Lanthanum tracer and freeze-fracture studies suggest that compartmentalisation of early bone matrix may be related to initial mineralisation. J Anat. 1992;181:345-356. (Pubitemid 23068825)
6. Prele CM, Horton MA, Caterina P, Stenbeck G. Identification of the molecular mechanisms contributing to polarized trafficking in osteoblasts. Expl Cell Res. 2003;282:24-34. (Pubitemid 36062609)
7. Saitou M, Furuse M, Sasaki H, et al. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell. 2000;11:4131-4142.
8. Wongdee K, Pandaranandaka J, Teerapornpuntakit J, et al. Osteoblasts express claudins and tight junction-associated proteins. Histochem Cell Biol. 2008;130:79-90.
9. Gunzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev. 2013;93:525-569.
10. Saitou M, Fujimoto K, Doi Y, Itoh M, Fujimoto T, Furuse M, Takano H, Noda T, Tsukita S. Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J Cell Biol. 1998;141:397-408. (Pubitemid 28237088)
11. Matter K, Aijaz S, Tsapara A, Balda MS. Mammalian tight junctions in the regulation of epithelial differentiation and proliferation. Curr Opin Cell Biol. 2005;17:453-458. (Pubitemid 41267158)
12. Angelow S, Ahlstrom R, Yu AS. Biology of claudins. Am J Physiol Renal Physiol. 2008;295:F867-F876.
13. Chiba H, Osanai M, Murata M, Kojima T, Sawada N. Transmembrane proteins of tight junctions. Biochim Biophys Acta. 2008;1778:588-600.
14. Morita K, Furuse M, Fujimoto K, Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA. 1999;96:511-516. (Pubitemid 29061239)
15. Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM. Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol. 2002;283:C142-C147. (Pubitemid 34670557)
16. Gupta IR, Ryan AK. Claudins: unlocking the code to tight junction function during embryogenesis and in disease. Clin Genet. 2010;77:314-325.
17. Fujita K, Katahira J, Horiguchi Y, Sonoda N, Furuse M, Tsukita S. Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein. FEBS Lett. 2000;476:258-261. (Pubitemid 30410828)
18. Morin PJ. Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res. 2005;65:9603-9606. (Pubitemid 41541431)
19. Findley MK, Koval M. Regulation and roles for claudin-family tight junction proteins. IUBMB Life. 2009;61:431-437.
20. Piontek J, Winkler L, Wolburg H, et al. Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J.2008;22:146-158.
21. Krause G, Winkler L, Mueller SL, Haseloff RF, Piontek J, Blasig IE. Structure and function of claudins. Biochim Biophys Acta. 2008;1778:631-645.
22. Balda MS, Matter K. Tight junctions and the regulation of gene expression. Biochim Biophys Acta. 2009;1788:761-767.
23. Gunzel D, Fromm M. Claudins and other tight junction proteins. Compr Physiol. 2012;2:1819-1852.
24. Brandner JM, Kief S, Grund C, et al. Organization and formation of the tight junction system in human epidermis and cultured keratinocytes. Eur J Cell Biol. 2002;81:253-263. (Pubitemid 34568206)
25. Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Ann Rev Physiol. 2006;68:403-429.
26. Holmes JL, Van Itallie CM, Rasmussen JE, Anderson JM. Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Exprs Patterns. 2006;6:581-588.
27. Mineta K, Yamamoto Y, Yamazaki Y, et al. Predicted expansion of the claudin multigene family. FEBS Lett. 2011;585:606-612.
28. Kwon MJ. Emerging roles of claudins in human cancer. Int J Mol Sci. 2013;14:18148-18180.
29. Wongdee K, Riengrojpitak S, Krishnamra N, Charoenphandhu N. Claudin expression in the bone-lining cells of female rats exposed to long-standing acidemia. Exp Mol Pathol. 2010;88:305-310.
30. Hatakeyama N, Kojima T, Iba K, et al. IGF-I regulates tight-junction protein claudin-1 during differentiation of osteoblast-like MC3T3-E1cells via a MAP-kinase pathway. Cell Tissue Res. 2008;334:243-254.
31. Arana-Chavez VE, Soares AM, Katchburian E. Junctions between early developing osteoblasts of rat calvaria as revealed by freeze-fracture and ultrathin section electron microscopy. Arch Histol Cytol. 1995;58:285-292.
32. Linares GR, Brommage R, Powell DR, et al. Claudin 18 is a novel negative regulator of bone resorption and osteoclast differentiation. J Bone Miner Res. 2012;27:1553-1565.
33. Fujita H, Sugimoto K, Inatomi S, et al. Tight junction proteins claudin-2 and -12 are critical for vitamin D-dependent Ca2+ absorption between enterocytes. Mol Biol Cell. 2008;19:1912-1921.
34. Ikenouchi J, Matsuda M, Furuse M, Tsukita S. Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci. 2003;116:1959-1967. (Pubitemid 36622294)
35. Ohkubo T, Ozawa M. The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J Cell Sci. 2004;117:1675-1685. (Pubitemid 38559300)
36. Kim HY, Alarcon C, Pourteymour S, Wergedal JE, Mohan S. Disruption of claudin-18 diminishes ovariectomy-induced bone loss in mice. Am J Physiol Endocrinol Metab. 2013;304:E531-E537.
37. Steed E, Balda MS, Matter K. Dynamics and functions of tight junctions. Trends Cell Biol. 2010;20:142-149.
38. Furuse M, Hata M, Furuse K, et al. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol. 2002;156:1099-1111. (Pubitemid 34839858)
39. Nitta T, Hata M, Gotoh S, et al. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol. 2003;161:653-660. (Pubitemid 36578587)
40. Tatum R, Zhang Y, Salleng K, et al. Renal salt wasting and chronic dehydration in claudin-7-deficient mice. Am J Physiol Renal Physiol. 2010;298:F24-F34.
41. Turksen K, Troy TC. Permeability barrier dysfunction in transgenic mice overexpressing claudin 6. Development. 2002;129:1775-1784. (Pubitemid 34874193)
42. Nakano Y, Kim SH, Kim HM, et al. A claudin-9-based ion permeability barrier is essential for hearing. PLoS Genet. 2009;5:e1000610.
43. Gow A, Davies C, Southwood CM, et al. Deafness in Claudin 11-null mice reveals the critical contribution of basal cell tight junctions to stria vascularis function. J Neurosci. 2004;24:7051-7062. (Pubitemid 39096371)
44. Ben-Yosef T, Belyantseva IA, Saunders TL, et al. Claudin 14 knockout mice, a model for autosomal recessive deafness DFNB29, are deaf due to cochlear hair cell degeneration. Hum Mol Genet. 2003;12:2049-2061. (Pubitemid 37038814)
45. Gow A, Southwood CM, Li JS, et al. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell. 1999;99:649-659. (Pubitemid 30004640)
46. Elkouby-Naor L, Abassi Z, Lagziel A, Gow A, Ben-Yosef T. Double gene deletion reveals lack of cooperation between claudin 11 and claudin 14 tight junction proteins. Cell Tissue Res. 2008;333:427-438.
47. Wada M, Tamura A, Takahashi N, Tsukita S. Loss of claudins 2 and 15 from mice causes defects in paracellular Na+ flow and nutrient transport in gut and leads to death from malnutrition. Gastroenterology. 2013;144:369-380.
48. Lee K, Ansar M, Andrade PB, et al. Novel CLDN14 mutations in Pakistani families with autosomal recessive non-syndromic hearing loss. Am J Genet A. 2012;158A:315-321.
49. Wilcox ER, Burton QL, Naz S, et al. Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29. Cell. 2001;104:165-172. (Pubitemid 32144981)
50. Hadj-Rabia S, Baala L, Vabres P, et al. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology. 2004;127:1386-1390. (Pubitemid 39457765)
51. Konrad M, Schaller A, Seelow D, et al. Mutations in the tightjunction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am J Hum Genet. 2006;79:949-957. (Pubitemid 44763409)
52. Simon DB, Lu Y, Choate KA, et al. Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption. Science. 1999;285:103-106. (Pubitemid 29307575)
53. Ramasamy I. Recent advances in physiological calcium homeostasis. Clin Chem Lab. 2006;44:237-273. (Pubitemid 43357683)
54. Srivastava S, Toraldo G, Weitzmann MN, Cenci S, Ross FP, Pacifici R. Estrogen decreases osteoclast formation by down-regulating receptor activator of NF-kappa B ligand (RANKL)-induced JNK activation. J Biol Chem. 2001;276:8836-8840.
55. Bord S, Ireland DC, Beavan SR, Compston JE. The effects of estrogen on osteoprotegerin, RANKL, and estrogen receptor expression in human osteoblasts. Bone. 2003;32:136-141. (Pubitemid 36299141)
56. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Spelsberg TC, Riggs BL. Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells. Endocrinology. 1999;140:4367-4370. (Pubitemid 30647136)
57. Thorleifsson G, Holm H, Edvardsson V, et al. Sequence variants in the CLDN14 gene associate with kidney stones and bone mineral density. Nature genetics. 2009;41:926-930.
58. Banan A, Zhang LJ, Shaikh M, et al. 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. 2005;313:962-982. (Pubitemid 40727000)
59. D'Souza T, Agarwal R, Morin PJ. Phosphorylation of claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells. J Biol Chem. 2005;280:26233-26240. (Pubitemid 41022220)
60. French AD, Fiori JL, Camilli TC, et al. PKC and PKA phosphorylation affect the subcellular localization of claudin-1 in melanoma cells. Int J Med Sci. 2009;6:93-101.
61. Banan A, Zhang LJ, Shaikh M, Fields JZ, Farhadi A, Keshavarzian A. Theta-isoform of PKC is required for alterations in cytoskeletal dynamics and barrier permeability in intestinal epithelium: a novel function for PKC-theta. Am J Physiol Cel Physiol. 2004;287:C218-C234. (Pubitemid 38780170)
62. Nunbhakdi-Craig V, Machleidt T, Ogris E, Bellotto D, White CL 3rd, Sontag E. Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J Cell Biol. 2002;158:967-978. (Pubitemid 35001086)
63. Tanaka M, Kamata R, Sakai R. EphA2 phosphorylates the cytoplasmic tail of Claudin-4 and mediates paracellular permeability. J Biol Chem. 2005;280:42375-42382. (Pubitemid 43023209)
64. Gonzalez-Mariscal L, Tapia R, Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim Biophys Acta. 2008;1778:729-756.
65. Bushinsky DA, Chabala JM, Levi-Setti R. Ion microprobe analysis of mouse calvariae in vitro: evidence for a "bone membrane". Am J Physiol. 1989;256:E152-E158.
66. Rubinacci A, Benelli FD, Borgo E, Villa I. Bone as an ion exchange system: evidence for a pump-leak mechanism devoted to the maintenance of high bone K(+). Am J Physiol Endocrinol Metab. 2000;278:E15-E24. (Pubitemid 30101915)
67. Marenzana M, Shipley AM, Squitiero P, Kunkel JG, Rubinacci A. Bone as an ion exchange organ: evidence for instantaneous cell-dependent calcium efflux from bone not due to resorption. Bone. 2005;37:545-554. (Pubitemid 41317327)
68. Chung JJ, Shikano S, Hanyu Y, Li M. Functional diversity of protein C-termini: more than zipcoding? Trends Cell Biol. 2002;12:146-150. (Pubitemid 34164654)
69. Sierralta J, Mendoza C. PDZ-containing proteins: alternative splicing as a source of functional diversity. Brain Res Brain Res Rev. 2004;47:105-115. (Pubitemid 39574314)
70. Matter K, Balda MS. Signalling to and from tight junctions. Nat Rev Mol Cell Biol. 2003;4:225-236. (Pubitemid 36288044)
71. Guillemot L, Paschoud S, Pulimeno P, Foglia A, Citi S. The cytoplasmic plaque of tight junctions: a scaffolding and signalling center. Biochim Biophys Acta. 2008;1778:601-613.
72. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol. 1986;103:755-766. (Pubitemid 17177325)
73. Balda MS, Garrett MD, Matter K. The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J Cell Biol. 2003;160:423-432. (Pubitemid 36182732)
74. Balda MS, Matter K. The tight junction protein ZO-1 and an interacting transcription factor regulate ErbB-2 expression. EMBO J. 2000;19:2024-2033. (Pubitemid 30237578)
75. Sourisseau T, Georgiadis A, Tsapara A, et al. Regulation of PCNA and cyclin D1 expression and epithelial morphogenesis by the ZO-1-regulated transcription factor ZONAB/DbpA. Mol Cell Biol. 2006;26:2387-2398. (Pubitemid 43346937)
76. Matter K, Balda MS. Epithelial tight junctions, gene expression and nucleo-junctional interplay. J Cell Sci. 2007;120:1505-1511. (Pubitemid 46831780)
77. Lee SK, Moon J, Park SW, Song SY, Chung JB, Kang JK. Loss of the tight junction protein claudin 4 correlates with histological growth-pattern and differentiation in advanced gastric adenocarcinoma. Oncol Rep. 2005;13:193-199.
78. Pope JL, Bhat AA, Sharma A, et al. Claudin-1 regulates intestinal epithelial homeostasis through the modulation of Notch-signalling. Gut. 2014;63:622-634.
79. Islas S, Vega J, Ponce L, Gonzalez-Mariscal L. Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Exp Cell Res. 2002;274:138-148.
80. Betanzos A, Huerta M, Lopez-Bayghen E, Azuara E, Amerena J, Gonzalez-Mariscal L. The tight junction protein ZO-2 associates with Jun, Fos and C/EBP transcription factors in epithelial cells. Exp Cell Res. 2004;292:51-66. (Pubitemid 38058263)
81. Traweger A, Lehner C, Farkas A, et al. Nuclear Zonula oc-cludens- 2 alters gene expression and junctional stability in epithelial and endothelial cells. Differentiation. 2008;76:99-106.
82. Traweger A, Fuchs R, Krizbai IA, Weiger TM, Bauer HC, Bauer H. The tight junction protein ZO-2 localizes to the nucleus and interacts with the heterogeneous nuclear ribonucleoprotein scaffold attachment factor-B. J Biol Chem. 2003;278:2692-2700. (Pubitemid 36801350)
83. Hayashi D, Tamura A, Tanaka H, et al. Deficiency of claudin-18 causes paracellular H+ leakage, up-regulation of interleukin-1beta, and atrophic gastritis in mice. Gastroenterology. 2012;142:292-304.
84. Tamura A, Yamazaki Y, Hayashi D, et al. Claudin-based paracellular proton barrier in the stomach. Ann NY Acad Sci. 2012;1258:108-114.
85. Alshbool FZ, Alarcon CM, Wergedal JE, Mohan S. A high-calcium diet failed to rescue an osteopenia phenotype in claudin-18 knockout mice. Physiol Rep. 2014;2:e00200.
86. Boyce BF. Stomaching calcium for bone health. Nat Med. 2009;15:610-612.
87. Wright MJ, Proctor DD, Insogna KL, Kerstetter JE. Proton pump-inhibiting drugs, calcium homeostasis, and bone health. Nutr Rev. 2008;66:103-108. (Pubitemid 351666656)
88. Replogle RA, Li Q, Wang L, Zhang M, Fleet JC. Gene-by-Diet Interactions Influence Calcium Absorption and Bone Density in Mice. J Bone Miner Res. 2014;29:657-665.
89. Kong J, Zhang Z, Musch MW, et al. Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier. Am J Physiol Gastrointest Liver Physiol. 2008;294:G208-G216.
90. Inai T, Kobayashi J, Shibata Y. Claudin-1 contributes to the epithelial barrier function in MDCK cells. Eur J Cell Biol. 1999;78:849-855. (Pubitemid 30021265)
91. Fujita H, Chalubinski M, Rhyner C, et al. Claudin-1 expression in airway smooth muscle exacerbates airway remodeling in asthmatic subjects. J Allergy Clin Immunol. 2011;127:1612-1621.
92. Hoshino M, Hashimoto S, Muramatsu T, Matsuki M, Ogiuchi H, Shimono M. Claudin rather than occludin is essential for differentiation in rat incisor odontoblasts. Oral Dis. 2008;14:606-612.
93. Fortier AM, Asselin E, Cadrin M. Keratin 8 and 18 loss in epithelial cancer cells increases collective cell migration and cisplatin sensitivity through claudin1 up-regulation. J Biol Chem. 2013;288:11555-11571.
94. Yoon CH, Kim MJ, Park MJ, et al. Claudin-1 acts through c-Abl-protein kinase Cdelta (PKCdelta) signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem. 2010;285:226-233.
95. Fishwick KJ, Neiderer TE, Jhingory S, Bronner ME, Taneyhill LA. The tight junction protein claudin-1 influences cranial neural crest cell emigration. Mech Dev. 2012;129:275-283.
96. Singh AB, Sharma A, Smith JJ, et al. Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology. 2011;141:2140-2153.
97. Suh Y, Yoon CH, Kim RK, et al. Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cells. Oncogene. 2013;32:4873-4882.
98. Liu Y, Wang L, Lin XY, et al. Anti-apoptotic effect of claudin-1 on TNF-alpha-induced apoptosis in human breast cancer MCF-7 cells. Tumour Biol. 2012;33:2307-2315.
99. Lee JW, Hsiao WT, Chen HY, et al. Upregulated claudin-1 expression confers resistance to cell death of nasopharyngeal carcinoma cells. Int J Cancer. 2010;126:1353-1366.
100. Meertens L, Bertaux C, Cukierman L, Cormier E, Lavillette D, Cosset FL, Dragic T. The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol. 2008;82:3555-3560. (Pubitemid 351429931)
101. Che P, Tang H, Li Q. The interaction between claudin-1 and dengue viral prM/M protein for its entry. Virology. 2013;446:303-313.
102. Amasheh S, Meiri N, Gitter AH, et al. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci. 2002;115:4969-4976. (Pubitemid 36061180)
103. Yu AS, Cheng MH, Angelow S, et al. Molecular basis for cation selectivity in claudin-2-based paracellular pores: identification of an electrostatic interaction site. J Gen Physiol. 2009;133:111-127.
104. Dhawan P, Ahmad R, Chaturvedi R, et al. Claudin-2 expression increases tumorigenicity of colon cancer cells: role of epidermal growth factor receptor activation. Oncogene. 2011;30:3234-3247.
105. Wada M, Tamura A, Takahashi N, Tsukita S. Loss of claudins 2 and 15 from mice causes defects in paracellular Na(+) flow and nutrient transport in gut and leads to death from malnutrition. Gastroenterology. 2013;144:369-380.
106. Nishida M, Yoshida M, Nishiumi S, Furuse M, Azuma T. Claudin-2 regulates colorectal inflammation via myosin light chain kinase-dependent signaling. Dig Dis Sci. 2013;58:1546-1559.
107. Milatz S, Krug SM, Rosenthal R, et al. Claudin-3 acts as a sealing component of the tight junction for ions of either charge and uncharged solutes. Biochim Biophys Acta. 2010;1798:2048-2057.
108. Okugawa T, Oshima T, Chen X, et al. Down-regulation of claudin-3 is associated with proliferative potential in early gastric cancers. Dig Dis Sci. 2012;57:1562-1567.
109. Agarwal R, D'Souza T, Morin PJ. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res. 2005;65:7378-7385. (Pubitemid 41161271)
110. Shang X, Lin X, Manorek G, Howell SB. Claudin-3 and claudin-4 regulate sensitivity to cisplatin by controlling expression of the copper and cisplatin influx transporter CTR1. Mol Pharmaol. 2013;83:85-94.
111. Sun C, Yi T, Song X, et al. Efficient inhibition of ovarian cancer by short hairpin RNA targeting claudin-3. Oncol Rep. 2011;26:193-200.
112. Veshnyakova A, Piontek J, Protze J, Waziri N, Heise I, Krause G. Mechanism of Clostridium perfringens enterotoxin interaction with claudin-3/-4 protein suggests structural modifications of the toxin to target specific claudins. J Biol Chem. 2012;287:1698-1708.
113. Van Itallie C, Rahner C, Anderson JM. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J Clin Invest. 2001;107:1319-1327. (Pubitemid 32494549)
114. Hou J, Renigunta A, Yang J, Waldegger S. Claudin-4 forms paracellular chloride channel in the kidney and requires claudin-8 for tight junction localization. Proc Natl Acad Sci U S A. 2010;107:18010-18015.
115. Webb PG, Spillman MA, Baumgartner HK. Claudins play a role in normal and tumor cell motility. BMC Cell Biol. 2013;14:19.
116. Kawai Y, Hamazaki Y, Fujita H, et al. Claudin-4 induction by E-protein activity in later stages of CD4/8 double-positive thymocytes to increase positive selection efficiency. Proc Natl Acad Sci U S A. 2011;108:4075-4080.
117. Li J, Chigurupati S, Agarwal R, et al. Possible angiogenic roles for claudin-4 in ovarian cancer. Cancer Biol Ther. 2009;8:1806-1814.
118. Rahner C, Mitic LL, Anderson JM. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut. Gastroenterology. 2001;120:411-422. (Pubitemid 32147639)
119. Wen H, Watry DD, Marcondes MC, Fox HS. Selective decrease in paracellular conductance of tight junctions: role of the first extracellular domain of claudin-5. Mol Cell Biol. 2004;24:8408-8417. (Pubitemid 39245063)
120. Fontijn RD, Rohlena J, van Marle J, Pannekoek H, Horrevoets AJ. Limited contribution of claudin-5-dependent tight junction strands to endothelial barrier function. Eur J Cell Biol. 2006;85:1131-1144. (Pubitemid 44524627)
121. Escudero-Esparza A, Jiang WG, Martin TA. Claudin-5 is involved in breast cancer cell motility through the N-WASP and ROCK signalling pathways. J Exp Clin Cancer Res. 2012;31:43.
122. Escudero-Esparza A, Jiang WG, Martin TA. Claudin-5 participates in the regulation of endothelial cell motility. Mol Cell Biochem. 2012;362:71-85.
123. Turksen K, Troy TC. Claudin-6: a novel tight junction molecule is developmentally regulated in mouse embryonic epithelium. Dev Dyn. 2001;222:292-300. (Pubitemid 32937601)
124. Abuazza G, Becker A, Williams SS, et al. Claudins 6, 9, and 13 are developmentally expressed renal tight junction proteins. Am J Physiol Renal Physiol. 2006;291:F1132-F1141. (Pubitemid 44887225)
125. Zheng A, Yuan F, Li Y, et al. Claudin-6 and claudin-9 function as additional coreceptors for hepatitis C virus. J Virol. 2007;81:12465-12471.
126. Sas D, Hu M, Moe OW, Baum M. Effect of claudins 6 and 9 on paracellular permeability in MDCK II cells. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1713-R1719.
127. Zavala-Zendejas VE, Torres-Martinez AC, Salas-Morales B, Fortoul TI, Montano LF, Rendon-Huerta EP. Claudin-6, 7, or 9 overexpression in the human gastric adenocarcinoma cell line AGS increases its invasiveness, migration, and proliferation rate. Cancer Invest. 2011;29:1-11.
128. Liu YF, Wu Q, Xu XM, et al. [Effects of 17β-estradiol on proliferation and migration of MCF-7 cell by regulating expression of claudin-6]. Zhonghua Bing Li Xue Za Zhi. 2010;39:44-47.
129. Arabzadeh A, Troy TC, Turksen K. Role of the Cldn6 cytoplasmic tail domain in membrane targeting and epidermal differentiation in vivo. Mol Cell Biol. 2006;26:5876-5887. (Pubitemid 44134341)
130. Hong YH, Hishikawa D, Miyahara H, et al. Up-regulation of the claudin-6 gene in adipogenesis. Biosci Biotechnol Biochem. 2005;69:2117-2121. (Pubitemid 41711834)
131. Guo Y, Xu X, Liu Z, et al. Apoptosis signal-regulating kinase 1 is associated with the effect of claudin-6 in breast cancer. Diagn Pathol. 2012;7:111.
132. Alexandre MD, Lu Q, Chen YH. Overexpression of claudin-7 decreases the paracellular Cl-conductance and increases the paracellular Na+ conductance in LLC-PK1 cells. J Cell Sci. 2005;118:2683-2693. (Pubitemid 40932893)
133. Alexandre MD, Jeansonne BG, Renegar RH, Tatum R, Chen YH. The first extracellular domain of claudin-7 affects paracellular Cl-permeability. Biochem Biophys Res Commun. 2007;357:87-91. (Pubitemid 46574503)
134. Hou J, Gomes AS, Paul DL, Goodenough DA. Study of claudin function by RNA interference. J Biol Chem. 2006;281:36117-36123. (Pubitemid 46041345)
135. Thuma F, Zoller M. EpCAM-associated claudin-7 supports lymphatic spread and drug resistance in rat pancreatic cancer. Int J Cancer. 2013;133:855-866.
136. Zheng JY, Yu D, Foroohar M, et al. Regulation of the expression of the prostate-specific antigen by claudin-7. J Membr Biol. 2003;194:187-197. (Pubitemid 37013811)
137. Hoggard J, Fan J, Lu Z, Lu Q, Sutton L, Chen YH. Claudin-7 increases chemosensitivity to cisplatin through the upregulation of caspase pathway in human NCI-H522 lung cancer cells. Cancer Sci. 2013;104:611-618.
138. Angelow S, Schneeberger EE, Yu AS. Claudin-8 expression in renal epithelial cells augments the paracellular barrier by replacing endogenous claudin-2. J Membr Biol. 2007;215:147-159. (Pubitemid 47282681)
139. Yu AS, Enck AH, Lencer WI, Schneeberger EE. Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem. 2003;278:17350-17359. (Pubitemid 36799620)
140. Shrestha A, McClane BA. Human claudin-8 and -14 are receptors capable of conveying the cytotoxic effects of Clostridium perfringens enterotoxin. MBio. 2013;4: e00594-12.
141. Kitajiri SI, Furuse M, Morita K, et al. Expression patterns of claudins, tight junction adhesion molecules, in the inner ear. Hear Res. 2004;187:25-34. (Pubitemid 38091559)
142. Van Itallie CM, Rogan S, Yu A, Vidal LS, Holmes J, Anderson JM. Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am J Physiol Renal Physiol. 2006;291:F1288-F1299. (Pubitemid 44887242)
143. Ip YC, Cheung ST, Lee YT, Ho JC, Fan ST. Inhibition of hepatocellular carcinoma invasion by suppression of claudin-10 in HLE cells. Mol Cancer Ther. 2007;6:2858-2867. (Pubitemid 350206764)
144. Morita K, Sasaki H, Fujimoto K, Furuse M, Tsukita S. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol. 1999;145:579-588. (Pubitemid 29215721)
145. Wolburg H, Wolburg-Buchholz K, Liebner S, Engelhardt B. Claudin-1, claudin-2 and claudin-11 are present in tight junctions of choroid plexus epithelium of the mouse. Neurosci Lett. 2001;307:77-80. (Pubitemid 32568378)
146. Van Itallie CM, Fanning AS, Anderson JM. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol. 2003;285:F1078-F1084. (Pubitemid 37421043)
147. Tiwari-Woodruff SK, Buznikov AG, Vu TQ, et al. OSP/claudin-11 forms a complex with a novel member of the tetraspanin super family and beta1 integrin and regulates proliferation and migration of oligodendrocytes. J Cell Biol. 2001;153:295-305. (Pubitemid 34280216)
148. Mazaud-Guittot S, Meugnier E, Pesenti S, et al. Claudin 11 deficiency in mice results in loss of the Sertoli cell epithelial phenotype in the testis. Biol Reprod. 2010;82:202-213.
149. Agarwal R, Mori Y, Cheng Y, et al. Silencing of claudin-11 is associated with increased invasiveness of gastric cancer cells. PloS One. 2009;4:e8002.
150. Fujita H, Chiba H, Yokozaki H, et al. Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine. J Histochem Cytochem. 2006;54:933-944. (Pubitemid 44106871)
151. Thompson PD, Tipney H, Brass A, et al. Claudin 13, a member of the claudin family regulated in mouse stress induced erythropoiesis. PloS One. 2010;5:e12667.
152. Baker M, Reynolds LE, Robinson SD, et al. Stromal Claudin14- heterozygosity, but not deletion, increases tumour blood leakage without affecting tumour growth. PloS One. 2013;8:e62516.
153. Wang F, Daugherty B, Keise LL, et al. Heterogeneity of claudin expression by alveolar epithelial cells. Am J Respir Cell Mol Biol. 2003;29:62-70. (Pubitemid 36783317)
154. Markov AG, Kruglova NM, Fomina YA, Fromm M, Amasheh S. Altered expression of tight junction proteins in mammary epithelium after discontinued suckling in mice. Pflugers Arch. 2012;463:391-398.
155. Tamura A, Kitano Y, Hata M, et al. Megaintestine in claudin-15-deficient mice. Gastroenterology. 2008;134:523-534.
156. Kausalya PJ, Amasheh S, Gunzel D, et al. Disease-associated mutations affect intracellular traffic and paracellular Mg2+ transport function of Claudin-16. J Clin Invest. 2006;116:878-891.
157. Hou J, Shan Q, Wang T, et al. Transgenic RNAi depletion of claudin-16 and the renal handling of magnesium. J Biol Chem. 2007;282:17114-17122. (Pubitemid 47093227)
158. Martin TA, Harrison GM, Watkins G, Jiang WG. Claudin-16 reduces the aggressive behavior of human breast cancer cells. J Cell Biochem. 2008;105:41-52.
159. Krug SM, Gunzel D, Conrad MP, et al. Claudin-17 forms tight junction channels with distinct anion selectivity. Cell Mol Life Sci. 2012;69:2765-2778.
160. Tureci O, Koslowski M, Helftenbein G, et al. Claudin-18 gene structure, regulation, and expression is evolutionary conserved in mammals. Gene. 2011;481:83-92.
161. Jovov B, Van Itallie CM, Shaheen NJ, et al. Claudin-18: a dominant tight junction protein in Barrett's esophagus and likely contributor to its acid resistance. Am J Physiol Gastrointest Liver Physiol. 2007;293:G1106-G1113. (Pubitemid 350255034)
162. Luk JM, Tong MK, Mok BW, Tam PC, Yeung WS, Lee KF. Sp1 site is crucial for the mouse claudin-19 gene expression in the kidney cells. FEBS Lett. 2004;578:251-256. (Pubitemid 39601790)
163. Miyamoto T, Morita K, Takemoto D, et al. Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. J Cell Biol. 2005;169:527-538. (Pubitemid 40686702)
164. Hou J, Renigunta A, Konrad M, et al. Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest. 2008;118:619-628. (Pubitemid 351206551)
165. Angelow S, El-Husseini R, Kanzawa SA, Yu AS. Renal localization and function of the tight junction protein, claudin-19. Am J Physiol Renal Physiol. 2007;293:F166-F177. (Pubitemid 47345015)
166. Ohtsuki S, Yamaguchi H, Katsukura Y, Asashima T, Terasaki T. mRNA expression levels of tight junction protein genes in mouse brain capillary endothelial cells highly purified by magnetic cell sorting. J Neurochem. 2008;104:147-154. (Pubitemid 350265064)
167. Muto S, Hata M, Taniguchi J, et al. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci USA. 2010;107:8011-8016.
168. Will C, Breiderhoff T, Thumfart J, et al. Targeted deletion of murine Cldn16 identifies extra- and intrarenal compensatory mechanisms of Ca2+ and Mg2+ wasting. Am J Physiol Renal Physiol. 2010;298:F1152-F1161.
169. Hou J, Renigunta A, Gomes AS, et al. Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci USA. 2009;106:15350-15355.