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BOR - Papers in Press, published online ahead of print June 2, 2004.
Biol Reprod 2004, 10.1095/biolreprod.104.029975
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BIOLOGY OF REPRODUCTION 71, 1128–1134 (2004)
DOI: 10.1095/biolreprod.104.029975
© 2004 by the Society for the Study of Reproduction, Inc.

Gamete Biology

Zonadhesin Assembly into the Hamster Sperm Acrosomal Matrix Occurs by Distinct Targeting Strategies During Spermiogenesis and Maturation in the Epididymis1

Gary E. Olson2,3, Virginia P. Winfrey3, Ming Bi4, Daniel M. Hardy4, and Subir K. NagDas3

Department of Cell and Developmental Biology,3 Vanderbilt University School of Medicine, Nashville, Tennessee 37232 Department of Cell Biology and Biochemistry,4 Texas Tech University Health Sciences Center, Lubbock, Texas 79430

Zonadhesin is the only sperm protein known to bind in a species-specific manner to the zona pellucida. The zonadhesin precursor is a mosaic protein with a predicted transmembrane segment and large extracellular region composed of cell adhesion, mucin, and tandem von Willebrand D domains. Because the precursor possesses a predicted transmembrane segment and localizes to the anterior head, the mature protein was presumed to be a sperm surface zona pellucida-binding protein. In this study of hamster spermatozoa, we demonstrate that zonadhesin does not localize to the sperm surface but is instead a constituent of the acrosomal matrix. Immunoelectron microscopy revealed that distinct targeting pathways during spermiogenesis and sperm maturation in the epididymis result in trafficking of zonadhesin to the acrosomal matrix. In round spermatids, zonadhesin localized specifically to the acrosomal membrane, where it appeared to be evenly distributed between the outer and inner membrane domains. Subsequent redistribution of zonadhesin resulted in its elimination from the inner acrosomal membrane and restriction to the outer acrosomal membrane of the apical and principal segments and the contents of the posterior acrosome. During sperm maturation in the epididymis, zonadhesin dissociated from the outer acrosomal membrane and became incorporated into the forming acrosomal matrix. These data suggest an important structural role for zonadhesin in assembly of the acrosomal matrix and further support the view that the species specificity of zona pellucida adhesion is mediated by egg-binding proteins contained within the acrosome rather than on the periacrosomal plasma membrane.

1 Supported by HD-35166 (D.M.H.) and HD-20419 (G.E.O.).

2 Correspondence: Gary E. Olson, Department of Cell and Developmental Biology, 1161 21st Ave. S, Room T-2208 MCN, Vanderbilt University, Nashville, TN 37232. FAX: 615 343 4539; gary.olson{at}vanderbilt.edu






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Copyright © 2004 by the Society for the Study of Reproduction.