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Mitochondrial sheath movement and detachment in mammalian, but not nonmammalian, sperm induced by disulfide bond reduction
Author(s) -
Sutovsky Peter,
Tengowski Mark W.,
Navara Christopher S.,
Zoran Sara S.,
Schatten Gerald
Publication year - 1997
Publication title -
molecular reproduction and development
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 0.745
H-Index - 105
eISSN - 1098-2795
pISSN - 1040-452X
DOI - 10.1002/(sici)1098-2795(199705)47:1<79::aid-mrd11>3.0.co;2-v
Subject(s) - sperm , biology , mitochondrion , human fertilization , microbiology and biotechnology , dithiothreitol , cytoplasm , biophysics , anatomy , biochemistry , genetics , enzyme
The successful completion of the fertilization process requires the properly choreographed unsheathing of the tightly packaged sperm once it has been fully incorporated into the egg's cytoplasm. The nuclear and accessory structures of mammalian sperm become stabilized by disulfide bonds (S‐S) during epididymal maturation. This stabilization is reversed during fertilization by the reduction of S‐S cross‐linking, but little is known about the effect of S‐S reduction on individual disulfide‐hardened structures such as the sperm's connecting piece, fibrous sheath, and mitochondria. Here, we demonstrate the action of the S‐S‐reducing environment on the mitochondrial sheath of mammalian sperm, visualized by the vital fluorescent probe Mito Tracker and by electron microscopy. In both human and bull sperm, mitochondria form a compact helix (mitochondrial sheath) wrapped around the midpiece and connecting piece that can be fluorescently labelled by a short incubation with 100 mM Mito‐Tracker. Exposure of bull sperm to 0.1–10 mM dithiothreitol (DTT; a disulfide bond‐reducing agent) induced a time and dose‐dependent sliding of the mitochondrial sheath down the axoneme, accompanied by the excision of the sperm tail and decondensation of the sperm nucleus. Increasing the concentration of DTT to 100 mM accelerated mitochondrial movement, causing a completed stripping of sperm mitochondria and partial disassembly of the connecting piece. Likewise, human sperm responded to DTT treatment by the sliding or removal of the mitochondrial sheath and decondensation of the sperm chromatin. These events were not observed in the sperm of lower vertebrates and invertebrates ( Xenopus laevis and Lytechinus pictus , respectively) exposed to an excess of DTT. Thus the sensitivity of sperm mitochondria to the S‐S reducing environment seems to be an exclusive feature of mammalian sperm. The movement of sperm mitochondria induced by S‐S reduction may be an initial critical step in the disassembly of the mammalian sperm tail during fertilization. Mol. Reprod. Dev. 47:79–86, 1997. © 1997 Wiley‐Liss, Inc.