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

• Published in: Biology of reproduction Vol. 71; no. 4; pp. 1128 - 1134
• Main Authors: OLSON, Gary E, WINFREY, Virginia P, MING BI, HARDY, Daniel M, NAGDAS, Subir K
• Format: Journal Article
• Language: English
• Published: Madison, WI Society for the Study of Reproduction 01-10-2004
• Subjects: Acrosome - metabolism; Acrosome - ultrastructure; Animals; Biological and medical sciences; Cricetinae; Epididymis - metabolism; Fertilization - physiology; Fundamental and applied biological sciences. Psychology; Intracellular Membranes - metabolism; Intracellular Membranes - ultrastructure; Male; Mammalian male genital system; Membrane Proteins - metabolism; Mesocricetus; Morphology. Physiology; Protein Transport - physiology; Sperm Maturation - physiology; Spermatogenesis - physiology; Vertebrates: reproduction; Spermatozoa; Targeting; Spermiogenesis; Rodentia; Male genital duct; Germinal cell; Male genital system; Vertebrata; Epididymis; Reproduction; Mammalia; Animal; Hamster
• ISSN: 0006-3363; 1529-7268
• DOI: 10.1095/biolreprod.104.029975

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.