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J. Biol. Chem., Vol. 281, Issue 9, 5623-5633, March 3, 2006

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Sodium and Epithelial Sodium Channels Participate in the Regulation of the Capacitation-associated Hyperpolarization in Mouse Sperm^*

Enrique O. Hernández-González, Julian Sosnik, Jennifer Edwards^¶, Juan José Acevedo^||**, Irene Mendoza-Lujambio^**, Ignacio López-González^**, Ignacio Demarco^¶, Eva Wertheimer, Alberto Darszon^**1, and Pablo E. Visconti

From the Department of Veterinary and Animal Science, Paige Laboratories, University of Massachusetts, Amherst, Massachusetts 01003, the Department of Cell Biology, Center for Research and Advanced Studies, Instituto Politécnico Nacional, 07300 México City, México, the ^¶Department of Cell Biology, University of Virginia, CITY, Charlottesville, Virginia 22908, the ^||Department of Physiology and Pathophysiology, School of Medicine, Universidad Autónoma de Morelos, 62210 Cuernavaca, México, the ^**Department of Developmental Genetics and Molecular Physiology, Institute of Biotechnology, Universidad Nacional Autónoma de México, 62210 Cuernavaca, México, and the Molecular Biomedicine Postgraduate Program, National Medicine and Homeopathy School, Instituto Politécnico Nacional, 07320 México City, México

In a process called capacitation, mammalian sperm gain the ability to fertilize after residing in the female tract. During capacitation the mouse sperm plasma membrane potential (E_m) hyperpolarizes. However, the mechanisms that regulate sperm E_m are not well understood. Here we show that sperm hyperpolarize when external Na⁺ is replaced by N-methyl-glucamine. Readdition of external Na⁺ restores a more depolarized E_m by a process that is inhibited by amiloride or by its more potent derivative 5-(N-ethyl-N-isopropyl)-amiloride hydrochloride. These findings indicate that under resting conditions an electrogenic Na⁺ transporter, possibly involving an amiloride sensitive Na⁺ channel, may contribute to the sperm resting E_m. Consistent with this proposal, patch clamp recordings from spermatogenic cells reveal an amiloride-sensitive inward Na⁺ current whose characteristics match those of the epithelial Na⁺ channel (ENaC) family of epithelial Na⁺ channels. Indeed, ENaC- and - mRNAs were detected by reverse transcription-PCR in extracts of isolated elongated spermatids, and ENaC- and - proteins were found on immunoblots of sperm membrane preparations. Immunostaining indicated localization of ENaC- to the flagellar midpiece and of ENaC- to the acrosome. Incubations known to produce capacitation in vitro or induction of capacitation by cell-permeant cAMP analogs decreased the depolarizing response to the addition of external Na⁺. These results suggest that increases in cAMP content occurring during capacitation may inhibit ENaCs to produce a required hyperpolarization of the sperm membrane.

Received for publication, July 26, 2005 , and in revised form, December 30, 2005.

^* This work was supported by National Institutes of Health Grants HD38082 and HD44044 (to P. E. V.), by a Fogarty International Research Collaboration Award Grant RO3 TW 006121 (to P. E. V. and A. D.), and by funds from Consejo Nacional de Ciencia y Tecnologiá and Dirección General de Asuntos del Personal Académico (to A. D.). 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 To whom correspondence should be addressed: Dept. of Developmental Genetics and Molecular Physiology, Institute of Biotechnology, Universidad Nacional Autónoma de México, Avenida Universidad #2001 Col. Chamilpa, CP 62210, Cuernavaca, Mor., Mexico. Tel.: 525-622-7611; Fax: 5273-17-23-88; E-mail: darszon{at}ibt.unam.mx.

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