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Claudin-15 forms a water channel through the tight junction with distinct function compared to claudin-2.

Abstract

AIM

Claudin-15 is mainly expressed in the small intestine and indirectly involved in glucose absorption. Similar to claudin-2 and -10b, claudin-15 is known to form a paracellular channel for small cations. Claudin-2, but not claudin-10b, also forms water channels. Here we experimentally tested whether claudin-15 also mediates water transport and if yes, whether water transport is Na+ -coupled, as seen for claudin-2.

METHODS

MDCK C7 cells were stably transfected with claudin-15. Ion and water permeability were investigated in confluent monolayers of control and claudin-15-expressing cells. Water flux was induced by an osmotic or ionic gradient.

RESULTS

Expression of claudin-15 in MDCK cells strongly increased cation permeability. The permeability ratios for monovalent cations indicated a passage of partially hydrated ions through the claudin-15 pore. Accordingly, its pore diameter was determined to be larger than that of claudin-2 and claudin-10b. Mannitol-induced water flux was elevated in claudin-15-expressing cells compared to control cells. In contrast to the Na+ -coupled water flux of claudin-2 channels, claudin-15-mediated water flux was inhibited by Na+ flux. Consequently, water flux was increased in Na+ -free solution. Likewise, Na+ flux was decreased after induction of water flux through claudin-15.

CONCLUSION

Claudin-15, similar to claudin-2, forms a paracellular cation and water channel. In functional contrast to claudin-2, water and Na+ fluxes through claudin-15 inhibit each other. Claudin-15 allows Na+ to retain part of its hydration shell within the pore. This then reduces the simultaneous passage of additional water through the pore.

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  • Authors+Show Affiliations

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    ,

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    Department of Gastroenterology, Rheumatology and Infectious Diseases, Institute of Clinical Physiology/Nutritional Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany.

    Source

    Acta physiologica (Oxford, England) : 2019 Jun 12 pg e13334

    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31188544

    Citation

    Rosenthal, Rita, et al. "Claudin-15 Forms a Water Channel Through the Tight Junction With Distinct Function Compared to Claudin-2." Acta Physiologica (Oxford, England), 2019, pp. e13334.
    Rosenthal R, Günzel D, Piontek J, et al. Claudin-15 forms a water channel through the tight junction with distinct function compared to claudin-2. Acta Physiol (Oxf). 2019.
    Rosenthal, R., Günzel, D., Piontek, J., Krug, S. M., Ayala-Torres, C., Hempel, C., ... Fromm, M. (2019). Claudin-15 forms a water channel through the tight junction with distinct function compared to claudin-2. Acta Physiologica (Oxford, England), pp. e13334. doi:10.1111/apha.13334.
    Rosenthal R, et al. Claudin-15 Forms a Water Channel Through the Tight Junction With Distinct Function Compared to Claudin-2. Acta Physiol (Oxf). 2019 Jun 12;e13334. PubMed PMID: 31188544.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Claudin-15 forms a water channel through the tight junction with distinct function compared to claudin-2. AU - Rosenthal,Rita, AU - Günzel,Dorothee, AU - Piontek,Jörg, AU - Krug,Susanne M, AU - Ayala-Torres,Carlos, AU - Hempel,Caroline, AU - Theune,Dian, AU - Fromm,Michael, Y1 - 2019/06/12/ PY - 2018/12/04/received PY - 2019/06/06/revised PY - 2019/06/07/accepted PY - 2019/6/13/pubmed PY - 2019/6/13/medline PY - 2019/6/13/entrez KW - claudin-15 pore diameter KW - paracellular ion permeability KW - paracellular water permeability SP - e13334 EP - e13334 JF - Acta physiologica (Oxford, England) JO - Acta Physiol (Oxf) N2 - AIM: Claudin-15 is mainly expressed in the small intestine and indirectly involved in glucose absorption. Similar to claudin-2 and -10b, claudin-15 is known to form a paracellular channel for small cations. Claudin-2, but not claudin-10b, also forms water channels. Here we experimentally tested whether claudin-15 also mediates water transport and if yes, whether water transport is Na+ -coupled, as seen for claudin-2. METHODS: MDCK C7 cells were stably transfected with claudin-15. Ion and water permeability were investigated in confluent monolayers of control and claudin-15-expressing cells. Water flux was induced by an osmotic or ionic gradient. RESULTS: Expression of claudin-15 in MDCK cells strongly increased cation permeability. The permeability ratios for monovalent cations indicated a passage of partially hydrated ions through the claudin-15 pore. Accordingly, its pore diameter was determined to be larger than that of claudin-2 and claudin-10b. Mannitol-induced water flux was elevated in claudin-15-expressing cells compared to control cells. In contrast to the Na+ -coupled water flux of claudin-2 channels, claudin-15-mediated water flux was inhibited by Na+ flux. Consequently, water flux was increased in Na+ -free solution. Likewise, Na+ flux was decreased after induction of water flux through claudin-15. CONCLUSION: Claudin-15, similar to claudin-2, forms a paracellular cation and water channel. In functional contrast to claudin-2, water and Na+ fluxes through claudin-15 inhibit each other. Claudin-15 allows Na+ to retain part of its hydration shell within the pore. This then reduces the simultaneous passage of additional water through the pore. SN - 1748-1716 UR - https://www.unboundmedicine.com/medline/citation/31188544/Claudin-15_forms_a_water_channel_through_the_tight_junction_with_distinct_function_compared_to_claudin-2 L2 - https://doi.org/10.1111/apha.13334 DB - PRIME DP - Unbound Medicine ER -