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J. Biol. Chem., Vol. 280, Issue 41, 34718-34722, October 14, 2005

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Characterization of Single Channel Currents from Primary Cilia of Renal Epithelial Cells^*

Malay K. Raychowdhury12, Margaret McLaughlin1, Arnolt J. Ramos, Nicolás Montalbetti¶, Richard Bouley3, Dennis A. Ausiello3, and Horacio F. Cantiello¶4

From the Renal Unit, Massachusetts General Hospital East, Charlestown, Massachusetts 02129 and Harvard Medical School, Boston, Massachusetts 02115, and the ^¶Laboratorio de Canales Iónicos, Departamento de Fisicoquiímica y Quiímica Analiítica, Facultad de Farmacia y Bioquímica, Buenos Aires 1113, Argentina

The primary cilium is a ubiquitous, non-motile microtubular organelle lacking the central pair of microtubules found in motile cilia. Primary cilia are surrounded by a membrane, which has a unique complement of membrane proteins, and may thus be functionally different from the plasma membrane. The function of the primary cilium remains largely unknown. However, primary cilia have important sensory transducer properties, including the response of renal epithelial cells to fluid flow or mechanical stimulation. Recently, renal cystic diseases have been associated with dysfunctional ciliary proteins. Although the sensory properties of renal epithelial primary cilia may be associated with functional channel activity in the organelle, information in this regard is still lacking. This may be related to the inherent difficulties in assessing electrical activity in this rather small and narrow organelle. In the present study, we provide the first direct electrophysiological evidence for the presence of single channel currents from isolated primary cilia of LLC-PK1 renal epithelial cells. Several channel phenotypes were observed, and addition of vasopressin increased cation channel activity, which suggests the regulation, by the cAMP pathway of ciliary conductance. Ion channel reconstitution of ciliary versus plasma membranes indicated a much higher channel density in cilia. At least three channel proteins, polycystin-2, TRPC1, and interestingly, the -epithelial sodium channel, were immunodetected in this organelle. Ion channel activity in the primary cilium of renal cells may be an important component of its role as a sensory transducer.

Received for publication, July 18, 2005

^* This work was funded in part by the PKD Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Both authors contributed equally to this work.

² Supported by a NIDDK, National Institutes of Health Training grant.

³ Supported by R01 grants from the NIDDK, National Institutes of Health.

⁴ To whom correspondence should be addressed: Renal Unit, MA General Hospital East, 149 13th St., Charlestown, MA 02129. Tel.: 617-726-5640; Fax: 617-726-5669; E-mail: cantiello{at}helix.mgh.harvard.edu.

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