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Molecular and Cellular Biology, February 2007, p. 1486-1494, Vol. 27, No. 4
0270-7306/07/$08.00+0     doi:10.1128/MCB.01468-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Extracellular pH Dynamically Controls Cell Surface Delivery of Functional TRPV5 Channels{triangledown}

Tim T. Lambers,1 Elena Oancea,2 Theun de Groot,1 Catalin N. Topala,1 Joost G. Hoenderop,1 and René J. Bindels1*

Department of Physiology, Nijmegen Centre for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands,1 Department of Cardiology, Howard Hughes Medical Institute, Children's Hospital Boston, Harvard Medical School, Boston, Massachusetts2

Received 8 August 2006/ Returned for modification 18 September 2006/ Accepted 2 December 2006

Extracellular pH has long been known to affect the rate and magnitude of ion transport processes among others via regulation of ion channel activity. The Ca2+-selective transient receptor potential vanilloid 5 (TRPV5) channel constitutes the apical entry gate in Ca2+-transporting cells, contributing significantly to the overall Ca2+ balance. Here, we demonstrate that extracellular pH determines the cell surface expression of TRPV5 via a unique mechanism. By a comprehensive approach using total internal reflection fluorescence microscopy, cell surface protein labeling, electrophysiology, 45Ca2+ uptake assays, and functional channel recovery after chemobleaching, this study shows that upon extracellular alkalinization, a pool of TRPV5-containing vesicles is rapidly recruited to the cell surface without collapsing into the plasma membrane. These vesicles contain functional TRPV5 channels since extracellular alkalinization is accompanied by increased TRPV5 activity. Conversely, upon subsequent extracellular acidification, vesicles are retrieved from the plasma membrane, simultaneously resulting in decreased TRPV5 activity. Thus, TRPV5 accesses the extracellular compartment via transient openings of vesicles, suggesting that rapid responses of constitutive active TRP channels to physiological stimuli rely on vesicular "kiss and linger" interactions with the plasma membrane.

* Corresponding author. Mailing address: 286 Physiology, Nijmegen Centre for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands. Phone: 31 24 3614211. Fax: 31 24 3616413. E-mail: R.Bindels{at}ncmls.ru.nl.

{triangledown} Published ahead of print on 18 December 2006.

Molecular and Cellular Biology, February 2007, p. 1486-1494, Vol. 27, No. 4
0270-7306/07/$08.00+0     doi:10.1128/MCB.01468-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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