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New saliva secretion model based on the expression of Na+-K+ pump and K+ channels in the apical membrane of parotid acinar cells

  • Ion channels, receptors and transporters
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Abstract

The plasma membrane of parotid acinar cells is functionally divided into apical and basolateral regions. According to the current model, fluid secretion is driven by transepithelial ion gradient, which facilitates water movement by osmosis into the acinar lumen from the interstitium. The osmotic gradient is created by the apical Cl− efflux and the subsequent paracellular Na+ transport. In this model, the Na+-K+ pump is located exclusively in the basolateral membrane and has essential role in salivary secretion, since the driving force for Cl− transport via basolateral Na+–K+–2Cl− cotransport is generated by the Na+-K+ pump. In addition, the continuous electrochemical gradient for Cl− flow during acinar cell stimulation is maintained by the basolateral K+ efflux. However, using a combination of single-cell electrophysiology and Ca2+-imaging, we demonstrate that photolysis of Ca2+ close to the apical membrane of parotid acinar cells triggered significant K+ current, indicating that a substantial amount of K+ is secreted into the lumen during stimulation. Nevertheless, the K+ content of the primary saliva is relatively low, suggesting that K+ might be reabsorbed through the apical membrane. Therefore, we investigated the localization of Na+-K+ pumps in acinar cells. We show that the pumps appear evenly distributed throughout the whole plasma membrane, including the apical pole of the cell. Based on these results, a new mathematical model of salivary fluid secretion is presented, where the pump reabsorbs K+ from and secretes Na+ to the lumen, which can partially supplement the paracellular Na+ pathway.

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Acknowledgements

The authors thank Timea Horváth and Alexandra Nagy for their excellent technical assistance. This work was supported by the Hungarian National Research Development and Innovation Office (PD112199 to JA and K115307 to PPN) and by the National Institutes of Health grant DE014756. JA is supported by the Janos Bolyai Research Scholarship of the Hungarian Academy of Sciences and the Lajos Szodoray Scholarship of the University of Debrecen. The publication was supported also by the GINOP-2.3.2-15-2016-00040 and EFOP-3.6.2-16-2017-00006 projects (to PPN and JA), which are co-financed by the European Union and the European Regional Development Fund. KM is supported by the Faculty of Dentistry, University of Debrecen.

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Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, University of Debrecen, PO Box: 400, Debrecen, 4002, Hungary

    János Almássy, Marianna Skaliczki & Péter P. Nánási

  2. Department of Mathematics, University of Auckland, Auckland, New Zealand

    Elias Siguenza & James Sneyd

  3. Department of Dentistry, University of Debrecen, Debrecen, Hungary

    Marianna Skaliczki

  4. Department of Anatomy, Histology and Embryology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

    Klara Matesz

  5. Department of Pharmacology and Physiology and the Centre for Oral Biology, University of Rochester Medical Center, Rochester, NY, 14642, USA

    David I. Yule

  6. Department of Dental Physiology and Pharmacology, Faculty of Dentistry, University of Debrecen, Debrecen, Hungary

    Péter P. Nánási

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  1. János Almássy
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Correspondence to János Almássy.

Electronic supplementary material

Supplementary figure 1

3D reconstruction of confocal optical sections of an isolated parotid acinus show the localization of the Na+-K+ pump (PDF 609 kb)

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Almássy, J., Siguenza, E., Skaliczki, M. et al. New saliva secretion model based on the expression of Na+-K+ pump and K+ channels in the apical membrane of parotid acinar cells. Pflugers Arch - Eur J Physiol 470, 613–621 (2018). https://doi.org/10.1007/s00424-018-2109-0

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