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J. Biol. Chem., Vol. 276, Issue 10, 7630-7636, March 9, 2001
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From the Center for Research on Reproduction and Women's Health,
Biomedical Research Building II/III, University of Pennsylvania Medical
Center, Philadelphia, Pennsylvania 19104-6142
Spermatozoa are highly polarized cells with
specific metabolic pathways compartmentalized in different regions.
Previously, we hypothesized that glycolysis is organized in the fibrous
sheath of the flagellum to provide ATP to dynein ATPases that generate motility and to protein kinases that regulate motility. Although a
recent report suggested that glucose is not essential for murine sperm
capacitation, we demonstrated that glucose (but not lactate or
pyruvate) was necessary and sufficient to support the protein tyrosine
phosphorylation events associated with capacitation. The effect of
glucose on this signaling pathway was downstream of cAMP, and appeared
to arise indirectly as a consequence of metabolism as opposed to a
direct signaling effect. Moreover, the phosphorylation events were not
affected by uncouplers of oxidative respiration, inhibitors of electron
transfer, or by a lack of substrates for oxidative respiration in the
medium. Further experiments aimed at identifying potential regulators of sperm glycolysis focused on a germ cell-specific isoform of hexokinase, HK1-SC, which localizes to the fibrous sheath. HK1-SC activity and biochemical localization did not change during sperm capacitation, suggesting that glycolysis in sperm is regulated either
at the level of substrate availability or by downstream enzymes. These
data support the hypothesis that ATP specifically produced by a
compartmentalized glycolytic pathway in the principal piece of the
flagellum, as opposed to ATP generated by mitochondria in the
mid-piece, is strictly required for protein tyrosine phosphorylation events that take place during sperm capacitation. The relationship between these pathways suggests that spermatozoa offer a model system
for the study of integration of compartmentalized metabolic and
signaling pathways.
Functional Relationships between
Capacitation-dependent Cell Signaling and
Compartmentalized Metabolic Pathways in Murine Spermatozoa*
*
This work was supported in part by National Institutes of
Health Grants HD-33052 (to A. J. T., T. M., G. S. K., and S. B. M.),
T32-HD-07305-15 (to A. J. T.), 1RO1-RR00188-01 (to A. J. T.),
PO1-HD-06274 (to B. H. J., B. T. S., G. S. K., and S. B. M.), and
RR-07065 (to D. M. D.), and by the Bourat Foundation (C. J. J.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The 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. Tel.: 215-573-4782;
Fax: 215-573-7627; E-mail: smoss@mail.med.upenn.edu.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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