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J. Biol. Chem., Vol. 279, Issue 38, 40194-40203, September 17, 2004

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Particulate Adenylate Cyclase Plays a Key Role in Human Sperm Olfactory Receptor-mediated Chemotaxis^*

Marc Spehr, Katlen Schwane¶, Jeffrey A. Riffell||, Jon Barbour¶, Richard K. Zimmer||**, Eva M. Neuhaus¶, and Hanns Hatt¶

From the Department of Anatomy and Neurobiology, University of Maryland, Baltimore, Maryland 21201, the ^¶Lst. Zellphysiologie, Ruhr-Universität Bochum, Universitätsstrasse 150, 44780 Bochum, Germany, the ^||Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095-1606, and the ^**Department of Neurosciences, Brain Research Institute, University of California, Los Angeles, California 90095-1606

Human sperm chemotaxis is a critical component of the fertilization process, but the molecular basis for this behavior remains unclear. Recent evidence shows that chemotactic responses depend on activation of the sperm olfactory receptor, hOR17-4. Certain floral scents, including bourgeonal, activate hOR17-4, trigger pronounced Ca²⁺ fluxes, and evoke chemotaxis. Here, we provide evidence that hOR17-4 activation is coupled to a cAMP-mediated signaling cascade. Multidimensional protein identification technology was used to identify potential components of a G-protein-coupled cAMP transduction pathway in human sperm. These products included various membrane-associated adenylate cyclase (mAC) isoforms and the G_olf-subunit. Using immunocytochemistry, specific mAC isoforms were localized to particular cell regions. Whereas mAC III occurred in the sperm head and midpiece, mAC VIII was distributed predominantly in the flagellum. In contrast, G_olf was found mostly in the flagellum and midpiece. The observed spatial distribution patterns largely correspond to the spatiotemporal character of hOR17-4-induced Ca²⁺ changes. Behavioral and Ca²⁺ signaling responses of human sperm to bourgeonal were bioassayed in the presence, or absence, of the adenylate cyclase antagonist SQ22536. This specific agent inhibits particulate AC, but not soluble AC, activation. Upon incubation with SQ22536, cells ceased to exhibit Ca²⁺ signaling, chemotaxis, and hyperactivation (faster swim speed and flagellar beat rate) in response to bourgeonal. Particulate AC is therefore required for induction of hOR17-4-mediated human sperm behavior and represents a promising target for future design of contraceptive drugs.

Received for publication, April 8, 2004 , and in revised form, July 6, 2004.

^* This work was supported by the Alma und Heinrich Vogelsang Stiftung. 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.

To whom correspondence should be addressed: Dept. Anatomy and Neurobiology, School of Medicine, University of Maryland, 685 West Baltimore St., Baltimore, MD 21201. Tel.: 410-706-8921; Fax: 410-706-2512; E-mail: mspeh001{at}umaryland.edu.

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