Rat sperm AS-A: subcellular localization in testis and epididymis and surface distribution in epididymal sperm
Tóm tắt
In this study, we investigated the subcellular compartmentalization of arylsulfatase-A (AS-A) in the testis and epididymis as well as the surface distribution in rat epididymal sperm. Testicular AS-A was compartmentalized specifically to the area underneath the outer acrosomal membrane of the acrosomal granule and to the dorsal aspect of the sperm acrosome. Epididymal AS-A was synthesized in the endoplasmic reticular (ER) network of principal cells and secreted into epididymal lumen as evident by its reactivity in the apical cytoplasm and vesicles therein underneath stereocilia. In clear cells, AS-A reactivity was found throughout the cytoplasmic machineries involved in endocytosis. Surface distribution of AS-A was initially detectable at the concave ridge as early as in sperm of the initial segment (IS). AS-A was additionally localized to the post-acrosomal region in caput (CP), corpus (CO) and cauda (CD) epididymal sperm. The expression levels of surface AS-A gradually increased during sperm transit from IS to CD epididymidis. These results favored the adsorption of AS-A from epididymal fluid onto the sperm surface, rather than shunting from the acrosome as a consequence of capacitation-associated membrane priming.
Tài liệu tham khảo
Andonian S, Hermo L (1999) Cell- and region-specific localization of lysosomal and secretory proteins and endocytic receptors in epithelial cells of the cauda epididymidis and vas deferens of the adult rat. J Androl 20:415–429
Barbieri AM, Sosa MA, Grimalt P, Mayorga LS, Bertini F (1995) Phosphomannosyl receptors on the surface of spermatozoa from the cauda epididymis of the rat. Int J Androl 18:113–119
Brandon CI, Srivastava PN, Heusner GL, Fayrer-Hosken RA (1997) Extraction and quantification of acrosin, β-N-acetylglucosaminidase, and arylsulfatase-A from equine ejaculated spermatozoa. J Exp Zool 279:301–308
Carmona E, Weerachatyanukul W, Soboloff T, Fluhary AL, White D, Promdee L, Ekker M, Berger T, Buhr M, Tanphaichitr N (2002a) Arylsulfatase A is present on the pig sperm surface and is involved in sperm-zona pellucida binding. Dev Biol 247:182a–196a
Carmona E, Weerachatyanukul W, Xu H, Fluharty AL, Anupriwan A, Shoushtarian A, Chakrabandhu K, Tanphaichitr N (2002b) Binding of arylsulfatase A to mouse sperm inhibits gamete interaction and induces the acrosome reaction. Biol Reprod 66:1820b–1827b
Cooper TG (1998) Interactions between epididymal secretions and spermatozoa. J Reprod Fertil Suppl 53:119–136
Cooper TG, Yeung CH, Bergmann M (1987) Protein transport to the epididymal lumen. Cell Tissue Res 248:527–530
Dahms NM, Lobel P, Kornfeld S (1989) Mannose 6-phosphate receptors and lysosomal enzyme targeting. J Biol Chem 264:12115–12118
Dudkiewicz AB (1984) Purification of boar acrosomal arylsulfatase A and possible role in the penetration of cumulus cells. Biol Reprod 30:1005–1014
Foster JA, Friday BB, Maulit MT, Blobel C, Winfrey VP, Olson GE, Kim KS, Gerton GL (1997) AM67, a secretory component of the guinea pig sperm acrosomal matrix, is related to mouse sperm protein sp56 and the complement component 4-binding proteins. J Biol Chem 272:12714–12722
Frenette G, Sullivan R (2001) Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev 59:115–121
Fujii T, Kobayashi T, Honke K, Gasa S, Ishikawa M, Shimizu T, Makita A (1992) Proteolytic processing of human lysosomal arylsulfatase A. Biochim Biophys Acta 1122:93–98
Gadella BM, Colenbrander B, van Golde LMG, Lopes-Cardozo M (1992) Characterization of three arylsulfatases in semen: seminolipid sulfohydrolase activity is present in seminal plasma. Biochim Biophys Acta 1128:155–162
Grima J, Wong CCS, Zhu L, Zong S, Cheng CY (1998) Testin secreted by Sertoli cells is associated with the cell surface, and its expression correlates with the disruption of Sertoli-germ cell junctions but not the inter-Sertoli tight junction. J Biol Chem 273:21040–21053
Grimalt P, Barbieri MA, Sosa MA, Bertini F (1995) Organ-specific binding system for beta-galactosidase in the male reproductive tract. Int J Androl 18:243–247
Hermo L, Robaire B (2002) Epididymal cell types and functions. In: Robaire B, Hinton BT (eds) The epididymis: from molecule to clinical practice. Kluwer/Plenum, New York, pp 81–102
Hermo L, Oko R, Morales CR (1994) Secretion and endocytosis in the male reproductive tract: a role in sperm maturation. Int Rev Cytol 154:106–189
Hinton BT, Howards SS (1982) Rat testis and epididymis can transport [3H] 3-O-methyl-d-glucose, [3H] inositol and [3H] alpha-aminoisobutyric acid across its epithelia in vivo. Biol Reprod 27:1181–1189
Kelly BM, Yu CZ, Chang PL (1989) Presence of a lysosomal enzyme, arylsulfatase-A, in the prelysosome–endosome compartments of human cultured fibroblasts. Eur J Cell Biol 48:71–78
Kreysing J, Polten A, Hess B, von Figura K, Menz K, Steiner F, Gieselmann V (1994a) Structure of the mouse arylsulfatase A gene and cDNA. Genomics 19:249b–256b
Kreysing J, Polten A, Lukatela G, Matzner U, van Figura K, Gieselmann V (1994b) Translational control of arylsulfatase A expression in mouse testis. J Biol Chem 269:23255a–23261a
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Legare C, Berube B, Boue F, Lefievre L, Morales CR, El-Alfy M, Sullivan R (1999) Hamster sperm antigen P26h is a phosphatidylinositol-anchored protein. Mol Reprod Dev 52:225–233
Mehl E, Jatzkewitz H (1968) Cerebroside 3-sulfate as a physiological substrate of arylsulfatase A. Biochim Biophys Acta 151:619–627
Oko RJ, Jando V, Wagner CL, Kistler WS, Hermo LS (1996) Chromatin reorganization in rat spermatids during the disappearance of testis-specific histone, H1t, and the appearance of transition proteins TP1 and TP2. Biol Reprod 54:1141–1157
Olson GE, Winfrey VP, NagDas SK (2003) Structural modifications of the hamster sperm acrosome during post-testicular development in the epididymis. Microsc Res Tech 61:46–55
Robaire B, Hermo L (1988) Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven, New York, pp 999–1080
Tantibhedhyangkul J, Weerachatyanukul W, Carmona E, Xu H, Anupriwan A, Michaud D, Tanphaichitr N (2002) Role of sperm surface arylsulfatase A in mouse sperm-zona pellucida binding. Biol Reprod 67:212–219
Toshimori K (1998) Maturation of spermatozoa: modifications of the acrosome and plasma membrane leading to fertilization. Cell Tissue Res 293:177–187
Towbin H, Staehelin T, Gordon J (1979) Electrophoresis transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc Natl Acad Sci USA 76:4350
Tulsiani DRP, Abou-Haila A (2004) Is sperm capacitation analogous to early phases of Ca2+-triggered membrane fusion in somatic cells and viruses? Bioessays 26:281–290
Vreeburg JT, Holland MK, Cornwall GA, Rankin TL, Orgebin-Crist MC (1991) Secretion of epididymal proteins and their interactions with spermatozoa. Bull Assoc Anat (Nancy) 75:171–173
Weerachatyanukul W, Xu H, Anupriwan A, Carmona E, Wade M, Hermo L, da Silva SM, Rippstein P, Sobhon P, Sretarugsa P, Tanphaichitr N (2003) Acquisition of arylsulfatase A onto the mouse sperm surface during epididymal transit. Biol Reprod 69:1183–1192
Yanagimachi R (1994) Mammalian fertilization. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven, New York, pp 189–317
Yoshinaka K, Toshimori K (2003) Organization and modifications of sperm acrosome molecules during spermatogenesis and epididymal maturation. Microsc Res Tech 61:39–45