Abstract
The epididymis is a long convoluted tubule through which spermatozoa must pass to acquire the functions of progressive motility and fertility. Since spermatozoa entering the epididymis are, for the most part, synthetically inactive, the process of sperm maturation is thought to involve the interaction of spermatozoa with proteins that are synthesized and secreted by the epididymal epithelium. The epididymal epithelial cells secrete proteins in a highly regulated and regionalized manner such that spermatozoa encounter luminal fluid proteins in a specific sequence. Indeed, each region within the epididymis is its own microenvironment uniquely controlled by the cells’ differential response to extracellular signals and mediated by specific signaling molecules and DNA binding proteins ultimately resulting in region-specific gene expression and secretion of proteins. To understand the complex process of sperm maturation, therefore, not only requires the identification of secretory proteins which interact with spermatozoa but also knowledge of specific signal transduction pathways and regulatory proteins involved in this highly orchestrated series of events. Recently, significant progress has been made towards our understanding of epididymal function by the application of transgenic and gene inactivation approaches to examine gene regulation and function in the epididymis. The objectives of this review are to discuss region-specific expression of genes expressed exclusively or predominantly in the epididymis, the mechanisms regulating this tissue- and region-specific gene expression, and the value of transgenic technology for understanding epididymal function.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abe, T., Tominaga, Y., Kickuchi, T., Watanabe, A., Satoh, K., Watanabe, Y., and Nukiwa, T., 1997, Bacterial pneumonia causes augmented expression of the secretory leukoprotease inhibitor gene in the murine lung, Am. J. Respir. Crit. Care Med156:1235.
Adamali, H., Somani, I.H., Huang, J.Q., Mahuran, D., Gravel, R.A., Trasler, J.M., and Hermo, L., 1999a, Abnormalities in cells of the testis, efferent ducts, and epididymis in juvenile and adult mice with beta- hexosaminidase A and B deficiency, J. Androl 20:779.
Adamali, H.I., Somani, I.H., Huang, J.Q., Gravel, R.A., Tralser, J.M., and Hermo, L., 1999b, Characterization and development of the regional- and cellular-specific abnormalities in the epididymis of mice with beta-hexosaminidase A deficiency, J. Androl 20:803.
Akmal, K.M., Dufour, J.M., and Kim, K.H., 1996, Region-specific localization of retinoic acid receptor-alpha expression in the rat epididymis, Biol Reprod54:111.
Alarid, E.T., Cunha, G.R., Young, P., and Nicoll, C.S., 1991, Evidence for an organ- and sex-specific role of basic fibroblast growth factor in the development of the fetal mammalian reproductive tract, Endocrinology 129:2148.
Anonymous, 1994, Control of gene expression (chapter 9): combinatorial gene control is the norm in eucaryotes, in: Molecular Biology of the Cell, B. Alberts, D. Bray, J. Lewis, M. Raff, K. Roberts, and J. D. Watson, eds., Garland Publishing Inc., New York & London.
Araki, Y., Suzuki, K., Matusik, R.J., Obinata, M., and Orgebin-Crist, M.-C. 2001, Immortalized epididymal cell lines from transgenic mice harboring temperature-sensitive simian virus 40 large T-antigen gene, submitted.
Arnone, M.I., and Davidson, E.H., 1997, The hardwiring of development: organization and function of genomic regulatory systems, Development 124:1851.
Ayer-LeLievre, C., Olson, L., Ebendal, T., Hallbook, F., and Persson, H., 1988, Nerve growth factor mRNA and protein in the testis and epididymis of mouse and rat, Proc. Natl Acad. Sci85:2628.
Bartolomei, M.S., and Tilghman, S.M., 1997, Genomic imprinting in mammals, Annu. Rev. Genet. 31:493.
Bauer-Dantoin, A.C., McDonald, J.K., and Levine, J.E., 1992, Neuropeptide Y potentiates luteinizing hormone (LH)-releasing hormone-induced LH secretion only under conditions leading to preovulatory LH surges, Endocrinology 131:2946.
Beato, M., and Eisfeld, K., 1997, Transcription factor access to chromatin, Nucleic Acids Res25:3559.
Benson, G.V., Lim, H., Paria, B.C., Satokata, I., Dey, S.K., and Maas, R.L., 1996, Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression, Development 122:2687.
Bentvelsen, F.M., Brinkmann, A.O., van der Schoot, P., van der Linden, J.E., van der Kwast, T.H.,
Boersma, W.J., Schroder, F.H., and Nijman, J.M., 1995, Developmental pattern and regulation by androgens of androgen receptor expression in the urogenital tract of the rat, Mol Cell Endocrinol. 113:245.
Berman, D.M., and Russell, D.W., 1993, Cell-type-specific expression of rat steroid 5 alpha-reductase isozymes, Proc. Natl. Acad. Sci. USA 90:9359.
Bérubé, B., and Sullivan, R., 1994, Inhibition of in vivo fertilization by active immunization of male hamsters against a 26-kDa sperm glycoprotein, Biol. Reprod51:1255.
Bhandari, V., Giaid, A., and Bateman, A., 1993, The complementary deoxyribonucleic acid sequence, tissue distribution, and cellular localization of the rat granulin precursor, Endocrinology 133:2682.
Birchmeier, C., and Birchmeier, W., 1993, Molecular aspects of mesenchymal-epithelial interactions, Annu. Rev. Cell Biol 9:511.
Bitgood, M.J., and McMahon, A.P., 1995, Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo, Dev. Biol172:126.
Blobel, C.P., Myles, D.G., Primakoff, P., and White, J.M., 1990, Proteolytic processing of a protein involved in sperm-egg fusion correlates with acquisition of fertilization competence, J. Cell Biol111:69.
Bodnar, J.W., and Bradley, M.K., 1996, A chromatin switch, J. Theor. Biol183:1.
Borsook, D., Rosen, H., Collard, M., Dressier, H., Herrup, K., Comb, M.J., and Hyman, S.E., 1992, Expression and regulation of a proenkephalin beta-galactosidase fusion gene in the reproductive system of transgenic mice, Mol. Endocrinol6:1502.
Bouchard, L., Lamarre, L., Tremblay, P.J., and Jolicoeur, P., 1989, Stochastic appearance of mammary tumors in transgenic mice carrying the MMTV/c-neu oncogene, Cell 57:931.
Boué, F., Blais, J., and Sullivan, R., 1996, Surface localization of P34H, an epididymal protein, during maturation, capacitation, and acrosome reaction of human spermatozoa, Biol. Reprod. 54:1009.
Brooks, D.E., 1983, Effect of androgens on protein synthesis and secretion in various regions of the rat epididymis, as analysed by two-dimensional gel electrophoresis, Mol. Cell Endocrinol29:255.
Brooks, D.E., Means, A.R., Wright, E.J., Singh, S.P., and Tiver, K.K., 1986a, Molecular cloning of the cDNA for two major androgen-dependent secretory proteins of 18.5 kilodaltons synthesized by the rat epididymis, J. Biol Chem26:4956.
Brooks, D.E., Means, A.R., Wright, E.J., Singh, S.P., and Tiver, K.K., 1986b, Molecular cloning of the cDNA for androgen-dependent sperm-coating glycoproteins secreted by the rat epididymis, Eur. J. Biochem161:13.
Brooks, D.E., 1987, Developmental expression and androgenic regulation of the mRNA for major secretory proteins of the rat epididymis, Mol. Cell. Endocrinol 53:59.
Byskov, A.G., and Hoyer, P.E., 1988, Embryology of mammalian gonads and ducts, in: The Physiology of ReproductionE. Knobil, and J. Neill, eds., Raven Press, New York.
Carballada, R., and Saling, P.M., 1997, Regulation of mouse epididymal epithelium in vitro by androgens, temperature and fibroblasts, J. Reprod. Fertil 110:171.
Chen, M.Y., Carpenter, D., and Zhao, G.Q., 1999, Expression of bone morphogenetic protein 7 in murine epididymis is developmentally regulated, Biol Reprod60:1503.
Civitareale, D., Lonigro, R., Sinclair, A.J., and Di Lauro, R., 1989, A thyroid-specific nuclear protein essential for tissue-specific expression of the thyroglobulin promoter, EMBO J. 8:2537.
Cohen, D.J., Rochwerger, L., Ellerman, D.A., Morgenfeld, M.M., Busso, D., and Cuasnicú, 2000, Relationship between the association of rat epididymal protein “DE” with spermatozoa and the behavior and function of the protein, Mol Reprod. Dev56:180.
Collard, M.W., Sylvester, S.R., Tsuruta, J.K., and Griswold, M.D., 1988, Biosynthesis and molecular cloning of sulfated glycoprotein 1 secreted by rat Sertoli cells: sequence similarity with the 70-kilodalton precursor to sulfatide/Gml activator, Biochemistry 27:4557.
Cooke, P.S., Young, P., and Cunha, G.R., 1991, Androgen receptor expression in developing male reproductive organs, Endocrinology 128:2867.
Cornwall, G.A., Orgebin-Crist, M.-C, and Hann, S.R., 1992, The CRES gene: a unique testis-regulated gene related to the cystatin family is highly restricted in its expression to the proximal region of the mouse epididymis, Mol. Endocrinol6:1653.
Cornwall, G.A., and Hann, S.R., 1995a, Specialized gene expression in the epididymis, J. Androl 16:379.
Cornwall, G.A., and Hann, S.R., 1995b, Transient appearance of CRES protein during spermatogenesis and caput epididymal sperm maturation, Mol. Reprod. Develop41:37.
Cornwall, G.A., and Hsia, N., 1997, ADAM7, a member of the ADAM (A Disintegrin And Metalloprotease) gene family is specifically expressed in the mouse anterior pituitary and epididymis, Endocrinology 138:4262.
Cornwall, G.A., Hsia, N., and Sutton, H.G., 1999, Structure, alternative splicing, and chromosomal localization of the cystatin-related epididymal spermatogenic gene, Biochem. J340:85.
Cornwall, G.A., Collis, R., Xiao, Q., Hsia, N., and Hann, S.R., 2001, B-Myc, a proximal caput epididymal protein is dependent on androgens and testicular factors for expression, Biol. Reprodin press.
Costa, S.L., Boekelheide, K., Vanderhyden, B.C., Seth, R., and McBurney, M.W., 1997, Male infertility caused by epididymal dysfunction in transgenic mice expressing a dominant negative mutation of retinoic acid receptor alpha, Biol. Reprod56:985.
Cunha, G.R., Alarid, E.T., Turner, T., Donjacour, A.A., Boutin, E.L., and Foster, B.A., 1992, Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors, J. Androl13:465.
Cunha, G.R., 1994, Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate, Cancer 74:1030.
Danzo, B.J., Cooper, T.G., and Orgebin-Crist, M.-C., 1977, Androgen binding protein (ABP) in fluids collected from the rete testis and cauda epididymis of sexually mature and immature rabbits and observations on morphological changes in the epididymis following ligation of the ductuli efferentes, Biol. Reprod17:64.
Davis, A.P., Witte, D.P., hsieh-Li, H.M., Potter, S.S., and Capecchi, M.R., 1995, Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11, Nature 375:791.
Delagebeaudeuf, C., Gassama-Diagne, A., Nauze, M., Ragab, A., Li, R.Y., Capdevielle, J., Ferrara, P., Fauvel, J., and Chap, H., 1998, Ectopic epididymal expression of guinea pig intestinal phospholipase B. Possible role in sperm maturation and activation by limited proteolytic digestion, J. Biol. Chem273:13407.
Desai, K.V., Flanders, K.C., and Kondaiah, P., 1998, Expression of transforming growth factor-beta isoforms in the rat male accessory sex organs and epididymis, Cell Tissue Res294:27l.
DiMattia, G.E., Rhodes, S.J., Krones, A., Carriere, C, O’Connell, S., Kalla, K., Arias, C., Sawchenko, P., and Rosenfeld, M.G., 1997, The Pit-1 gene is regulated by distinct early and late pituitary-specific enhancers, Dev. Biol 182:180.
Ding, Y., Davisson, R.L., Hardy, D.O., Zhu, L.J., Merrill, D.C., Catterall, J.F., and Sigmund, CD., 1997, The kidney androgen-regulated protein promoter confers renal proximal tubule cell-specific and highly androgen-responsive expression on the human angiotensinogen gene in transgenic mice, J. Biol. Chem. 272:28142.
Dixon, A.K., Tait, T.M., Campbell, E.A., Bobrow, M., Roberts, R.G., and Freeman, T.C., 1997, Expression of the dystrophin-related protein 2 (Drp2) transcript in mouse, J. Mol. Biol270:551.
Domino, S.E., Hiraiwa, N., and Lowe, J.B., 1997, Molecular cloning, chromosomal assignment and tissuespecific expression of murine alpha (1,2) fucosyltransferase expressed in thymic and epididymal epithelial cells, Biochem. J327:105.
Drevet, J.R., Lareyre, J.-J., Schwaab, V., Vernet, P., and Dufaure, J.-P., 1998, The PEA3 protein of the Ets oncogene family is a putative transcriptional modulator of the mouse epididymis-specific glutathione peroxidase gene gpx5, Mol. Reprod. Develop49:131.
Drevet, J.R., 2000, Glutathione peroxidases expression in the mammalian epididymis and vas deferens, in: Andrology 2000, Proceedings of the 1 st European Congress of AndrologyF. Francavilla, S. Francavilla, and G. Forti, eds., Collana Di Studi Abruzzesi Press, L’Aquila, Italy, pp 427.
Eberspaecher, U., Roosterman, D., Kratzschmar, J., Haendler, B., Habenicht, U.-F., Becker, A., Quensel, C., Petri, T., Schleunig, W.-D., and Donner, P., 1995, Mouse androgen-dependent epididymal glycoprotein CRISP-1 (DE/AEG): Isolation, biochemical characterization, and expression in recombinant form, Mol Reprod. Dev42:157.
Eddy, E.M., Washburn, T.F., Bunch, D.O., Goulding, E.H., Gladeb, B.C., Labahn, D.B., and Korach, K.S., 1996, Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility, Endocrinology 137:4796.
Ellerman, D.A., Brantua, V.S., Martinez, S.P., Cohen, D.J., Conesa, D., Cuasnicu, P.S., 1998, Potential contraceptive use of epididymal proteins: immunization of male rats with epididymal protein DE inhibits sperm fusion ability, Biol Reprod. 59:1029.
Fawcett, D.W., and Hoffer, A.P., 1979, Failture of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy, Biol. Reprod20:162.
Garrett, J.E., Garrett, S.H., and Douglass J.A., 1990, Spermatozoa-associated factor regulates proenkephalin gene expression in the rat epididymis, Mol. Endocrinol4:108.
Garrett, S.H., Garrett, J.E., and Douglass, J. A., 1991, In situ histochemical analysis of region-specific gene expression in the adult rat epididymis, Mol. Reprod. Develop30:1.
Gaudreault, C., Le gare C., Berube, B., and Sullivan, R., 1999, Hamster sperm protein, p26h: a member of the short-chain dehydrogenase/reductase superfamily, Biol Reprod61:264.
Gebhardt, K., Ellerbrock, K., Pera, I., Ivell, R., and Kirchhoff, C., 1999, Differential expression of novel abundant and highly regionalized mRNAs of the canine epididymis, J. Reprod. Fertil 116:391.
Ghyselinck, N.B., Jimenez, C, Lefrancois, A.M., and Dufaure, J.-P., 1990, Molecular cloning of a cDNA for androgen-regulated proteins secreted by the mouse epididymis, Mol. Endocrinol 4:5.
Gierer, A., 1974, Molecular models and combinatorial principles in cell differentiation and morphogenesis, in: Cold Spring Harbor Symposia on Quantitative Biologyp. 951.
Gilbert, E., Morel, A., Tulliez, M., Maunoury, R., Terzi, F., Miquerol, L., and Kahn, A., 1997, In vivo effects of activated H-ras oncogene expressed in the liver and in the urogenital tissues, Int. J. Cancer73:749.
Gizang-Ginsberg, E., and Wolgemuth, D.J., 1987, Expression of the proopiomelanocortin gene is developmentally regulated and affected by germ cells in the male mouse reproductive system, Proc. Natl Acad. Sci. USA 84:1600.
Graessmann, M., and Graessmann, A., 1993, DNA methylation, chromatin structure and the regulation of gene expression, EXS 64:404.
Gregory, M.A., Xiao, Q., Cornwall, G.A., Lutterbach, B., and Hann, S.R., 2000, B-Myc is preferentially expressed in hormonally-controlled tissues and inhibits cellular proliferation, Oncogene 42:4886.
Griffin, J.K. and Blecher, S.R., 1994, Extracellular matrix abnormalities in testis and epididymis of XXSxr (“sex-reversed”) mice, Mol. Reprod. Dev38:1.
Gupta, C., 1997, Cellular localization of immunoreactive epidermal growth factor during Wolffian duct differentiation of the fetal mouse, Urol. Res25:277.
Guy, C.T., Cardiff, R.C., and Mueller, W.J., 1996, Activated neu induces rapid tumor progression, J. Biol Chem27:7673.
Hagaman, J.R., Moyer, J.S., Bachman, E.S., Sibony, M., Magyar, P.L., Welch, J.E., Smithies, O., Krege, J.H., and O’Brien, D.A., 1998, Angiotensin-converting enzyme and male fertility, Proc. Natl Acad. Sci. USA 95:2552.
Hall, J.C., Perez, F.M., Kochins, J.G., Pettersen, C.A., Li, Y., Tubbs, C.E., and LaMarche, M.D., 1996, Quantification and localization of N-acetyl-Ăź-D-hexosaminidase in the adult rat testis and epididymis, Biol Reprod 54:914.
Hamil, K.G., Sivashanmugam, P., Richardson, R.T., Grossman, G., Ruben, S.M., Mohler, J.L., Petrusz, P., O’Rand, M.G., French, F.S., and Hall, S.H., 2000, HE2ß and HE2???, new members of an epididymis-specific family of androgen-regulated proteins in the human, Endocrinology 141:1245.
Hermo, L., Adamali, H.I., Mahuran, D., Gravel, R.A., and Trasler, J.M., 1997, Beta-hexosaminidase immunolocalization and alpha- and beta-subunit gene expression in the rat testis and epididymis, Mol. Reprod. Develop46:227.
Hermo, L., Lustig, M., Lefrancois, S., Argraves, W.S., and Morales, C.R., 1999, Expression and regulation of LRP-2/megalin in epithelial cells lining the efferent ducts and epididymis during postnatal development, Mol Reprod. Dev53:282.
Hermo, L., Wright, J., Oko, R., and Morales CR., 1991, Role of epithelial cells of the male excurrent duct system of the rat in the endocytosis or secretion of sulfated glycoprotein-2 (clusterin). Biol. Reprod44:1113.
Hess, R.A., Bunick, D., Lee, K.H., Bahr, J., Taylor, J.A., Korach, K.S., and Lubahn, D.B., 1997a, A role for oestrogens in the male reproductive system, Nature 390:447.
Hess, R.A., Gist, D.H., Bunick, D., Lubahn, D.B., Farrell, A., Bahr, J., Cooke, P.S., and Greene, G.L., 1997b, Estrogen receptor (alpha and beta) expression in the excurrent ducts of the adult male rat reproductive tract, J. Androl18:602.
Hess, R.A., Bunick, D., Lubahn, D.B., Zhou, Q., and Bouma, J., 2000, Morphologic changes in efferent ductules and epididymis in estrogen receptor alpha knockout mice, J. Androl 21:107.
Hinton, B.T., Palladino, M.A., Rudolph, D., and Labus, J.C., 1995, The epididymis as protector of maturing spermatozoa, Reprod. Fertil. Dev7:731.
Hinton, B.T., Lan, Z.J., Rudolph, D.B., Labus, J.C., and Lye, R.J., 1998, Testicular regulation of epididymal gene expression, J. Reprod. Fertil. Suppl53:47.
Holland, M.K., and Orgebin-Crist, M.-C, 1988a, Characterization and hormonal regulation of protein synthesis by the murine epididymis, Biol. Reprod38:487.
Holland, M.K., and Orgebin-Crist, M.-C., 1988b, Epididymal protein synthesis and secretion in strains of mice bearing single gene mutations which affect fertility, Biol. Reprod38:497.
Howard, L., Maciewicz, R.A., and Blobel, C.P., 2000, Cloning and characterization of ADAM28: evidence for autocatalytic pro-domain removal and for cell surface localization of mature ADAM28, Biochem. J. 348:21.
Hsia, N. and Cornwall, G.A., 2001, CCAAT/Enhancer-binding protein beta regulates expression of the cystatin-related epididymal spermatogenic (CRES) gene, submitted.
Hsieh-Li, H.M., Witte, D.P., Weinstein, M., Branford, W., Li, H., Small, K., and Potter, S.S., 1995, Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility, Development 121:1373.
Huang, L.S., Voyiaziakis, E., Chen, H.L., Rubin, E.M., and Gordon, J.W., 1996, A novel role for apolipoprotein B in male infertility in heterozygous apolipoprotein B knock-out mice, Proc. Natl. Acad. Sci. USA93:10903.
Hunnicutt, G.R., Koppel, D.E., and Myles, D.G., 1997, Analysis of the process of localization of fertilin to the sperm posterior head plasma membrane domain during sperm maturation in the epididymis, Dev. Biol191:146.
Ingvarsson, S., Asker, C, Acelson, H., Klein, G., and Sumegi, J., 1988a, Structure and expression of B-myc, a new member of the myc gene family, Mol. Cell. Biol8:3168.
Ingvarsson, S., Sundaresan, S., Jin, P., Francke, U., Asker, C, Sumegi, J., Klein, G., and Sejersen, T., 1988b, Chromosomal localization and expression pattern of Lmyc and Bmyc in murine embryonal carcinoma cells, Oncogene 3:679.
Jeannotte, L., Burbach, J.P.H., and Drouin, J., 1987, Unusual proopiomelanocortin ribonucleic acids in extrapituitary tissues: intronless transcripts in testes and long poly (A) tails in hypothalamus, Mol. Endocrinol1:749.
Jhappan, C, Gallahan, D., Stahle, C, Chu, E., Smith, G.H., Merlino, G., and Callahan, R, 1992, Expression of an activated Notch-related int-3 transgene interferes with cell differentiation and induces neoplastic transformation in mammary and salivary glands, Genes Develop6:345.
Johnson, P.F., and Williams, S.C.C., 1994, CCAAT/Enhancer binding (C/EBP) proteins, in: Liver Gene ExpressionF. Tronch and M. Yaniv, eds., Landes CO, Austin, TX.
Jones, R., Brown, C.R., Von Gos, K.I., and Parker, M.G., 1980, Hormonal regulation of protein synthesis in the rat epididymis. Characterization of androgen-dependent and testicular fluid-dependent proteins, Biochem. J188:667.
Jornvall, H., Persson, B., Krook, M., Atrian, S., Gonzalez-Duarte, R., Jeffery, J., and Ghosh, D., 1995, Short-chain dehydrogenases/reductases (SDR), Biochemistry 34:6003.
Joseph, D.R., O’Brien, D.A., Sullivan, P.M., Becchis, M., Tsuruta, J.K., and Petrusz, P., 1997, Overexpression of androgen-binding protein/sex hormone-binding globulin in male transgenic mice: tissue distribution and phenotypic disorders, Biol. Reprod56:21.
Kanwar, Y.S., Liu, Z.Z., Kumar, A., Wada, J., and Carone, F.A., 1995, Cloning of mouse c-ros renal cDNA, its role in development and relationship to extracellular matrix glycoproteins, Kidney Int. 48:1646.
Kanzaki, M., Fujisawa, M., Okuda, Y., Okada, H., Arakawa, S., and Kamidono, S., 1996, Expression and regulation of neuropeptide Y messenger ribonucleic acid in cultured immature rat Leydig and Sertoli cells, Endocrinology 137:1249.
Kaunisto, K., Fleming, R.E., Kneer, J., Sly, W.S., and Rajaniemi, H., 1999, Regional expression and androgen regulation of carbonic anhydrase IV and II in the adult rat epididymis, Biol. Reprod61:1521.
Keilhack, H., Muller, M., Bohmer, S.A., Frank, C, Weidner, K.M., Birchmeier, W., Ligensa, T., Berndt, A., Kosmehl, H., Gunther, B., Muller, T., Birchmeier, C., Bohmer, F.D., 2001, Negative regulation of Ros receptor tyrosine kinase signaling. An epithelial function of the SH2 domain protein tyrosine phosphatase SHP-1. J. Cell Biol152: 325.
Kirchhoff, C, 1994, A major messenger ribonucleic acid of the rodent epididymis encodes a small glycosylphosphatidylinositol-anchored surface antigen, Biol. Reprod50:896.
Kirchhoff, C, and Hale, G., 1996, Cell-to-cell transfer of glycosylphosphatidyl-inositol-anchored membrane proteins during sperm maturation, Mol. Hum. Reprod2:177.
Klinefelter, G.R., and Amann, R.P., 1980, Metabolism of testosterone by principal cells and basal cells isolated from the rat epididymal epithelium, Biol. Reprod22:1149.
Korpelainen, E.I., Karkkainen, M.J., Tenhunen, A., Lasko, M., Rauvala, H., Vierula, M., Parvinen, M., and Alitalo, K., 1998, Overexpression of VEGF in testis and epididymis causes infertility in transgenic mice: evidence for nonendothelial targets for VEGF, J. Cell Biol143:1705.
Lan, Z.-J., Palladino, M.A., Rudolph, D.B., Labus, J.C., and Hinton, B.T., 1997, Identification, expression and regulation of the transcriptional factor polyomavirus enhancer activator 3 (PEA3) and its putative role in regulating the expression of gamma glutamyl transpeptidase mRNA-IV in the rat epididymis, Biol. Reprod57: 186.
Lan, Z.-J., Labus, J.C., and Hinton, B.T., 1998, Regulation of gamma-glutamyl transpeptidase catalytic activity and protein level in the initial segment of the rat epididymis by testicular factors: role of basic fibroblast growth factor, Biol. Reprod58:197.
Lan, Z.J., Lye, R.J., Holic, N., Labus, J.C., and Hinton, B.T., 1999, Involvement of polyomavirus enhancer activator 3 in the regulation of expression of gamma-glutamyl transpeptidase messenger ribonucleic acid-IV in the rat epididymis, Biol. Reprod60:664.
Lareyre, J.-J., Mattel, M.-G., Kasper, S., Ong, D.E., Matusik, R.J., and Orgebin-Crist, M.-C., 1998a, Genomic organization and chromosomal localization of the murine epididymal retinoic acid-binding protein (mE-RABP) gene, Mol. Reprod. Dev50:387.
Lareyre, J.-J., Zheng, W.-L., Zhao, G.-Q., Kasper, S., Newcomer, M.E., Matusik, R.J., Ong, D.E., and Orgebin-Crist, M.-C., 1998b, Molecular cloning and hormonal regulation of a murine epididymal retinoic acid-binding protein, Endocrinology 139:2971.
Lareyre, J.-J., Thomas, T.Z., Zheng, W.L., Kasper, S., Ong, D.E., Orgebin-Crist, M.-C., and Matusik, R.J., 1999, A 5-kilobase pair promoter fragment of the murine epididymal retinoic acid-binding protein gene drives the tissue-specific, cell-specific, and androgen-regulated expression of a foreign gene in the epididymis of transgenic mice, J. Biol. Chem. 274:8282.
Lareyre, J.-J., Reid, K., Nelson, C., Kasper, S., Rennie, P.S., Orgebin-Crist, M.-C., and Matusik, R.J., 2000, Characterization of an androgen-specific response region within the 5’ flanking region of the murine epididymal retinoic acid binding protein gene (mE-RABP), Biol. Reprod63: 1881.
Lareyre, J.-J., Winfrey, V.P., Kasper, S., Ong, D.E., Matusik, R.J., Olson, G.E., Orgebin-Crist, M.-C., 2001, Gene duplication gives rise to a new 17-kilodalton lipocalin that shows epididymal region-specific expression and testicular factor(s) regulation, Endocrinology 142: 1296.
Le Barr, D.K., and Blecher, S., 1986, Epididymides of sex-reversed XX mice lack the initial segment, Develop. Genetics 7:109.
Le Barr, D.K., Blecher, S., and Moger, W.H., 1986, Androgen levels and androgenization in six-reversed (XXSxr pseudomale) mouse: absence of initial segment of epididymis is independent of androgens, ArckAndrol17:195.
Le Barr, D.K., and Blecher, S.R., 1987, Decreased arterial vasculature of the epididymal head in XXSxr pseudomale (sex-reversed) mice, Arch. Androl.20:11.
Le Barr, D.K., Blecher, S.R., and Moger, W.H., 1991, Development of the normal XY male and sex-reversed XXSxr pseudomale mouse epididymis, Mol. Reprod. Dev28:9.
Legaré, C., Gaudreault, C., St-Jacques, S., and Sullivan, R., 1999, P34H sperm protein is preferentially expressed by the human corpus epididymidis, 1999, Endocrinology 140:3318.
Leung, A.Y., Wong, P.Y., Yankaskas, J.R., and Boucher, R.C., 1996, cAMP-but not Ca(2+)-regulated CI conductance is lacking in cystic fibrosis mice epididymides and seminal vesicles, Am. J. Physiol271:C188.
Leung, P.S., Wong, T.P., and Sernia, C., 1999, Angiotensinogen expression by rat epididymis: evidence for an intrinsic, angiotensin-generating system, Mol. Cell. Endocr155:115.
Li, C., and Gudas, L.J., 1997, Sequences 5’ of the basement membrane laminin beta 1 chain gene (LAMB1) direct the expression of beta-galactosidase during development of the mouse testis and ovary, Differentiation62:129.
Lieberman, M.W., Wiseman, A.L., Shi, Z.-Z., Carter, B.Z., Barrios, R., Ou, C.-N., Chevrez-Barrios, P., Wang, Y., Habib, G.M., Goodman, J.C., Huang, S.L., Lebovitz, R.M., and Matzuk, M.M., 1996, Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-deficient mice, Proc. Natl. Adad. Sci. USA 93:7923.
Lie-Venema, H., de Boer, P. A., Moorman, A.F., and Lamers, W.H., 1997a, Organ-specific activity of the regulatory region of the glutamine synthetase gene in developing mice, Eur. J. Biochem248:644.
Lie-Venema, H., de Boer, P. A., Moorman, A.F., and Lamers, W.H., 1997b, Role of the 5’ enhancer of the glutamine synthetase gene in its organ-specific expression, BiochemJ. 323:611.
Lindsey, J.S., and Wilkinson, M.F., 1996a, An androgen-regulated homeobox gene expressed in rat testis and epididymis, Biol. Reprod55:975.
Lindsey, J.S., and Wilkinson, M.F., 1996b, Pern:A testosterone- and LH-regulated homeobox gene expressed in mouse Sertoli cells and epididymis, Dev. Biol179:471.
Liu, Z.Z., Wada, J., Kumar, A., Carone, F.A., Takahashi, M., and Kanwar, Y.S., 1996, Comparative role of phosphotyrosine kinase domains of c-ros and c-ret protooncogenes in metanephric development with respect to growth factors and matrix morphogens, Dev. Biol178:133.
Lucchini, F., Sacco, M.G., Hu, N., Villa, A., Brown, J., Cesano, L., Mangiarini, L., Rindi, G., Kindl, S., Sessa, F. et al., 1992, Early and multifocal tumors in breast, salivary, harderian and epididymal tissues developed in MMTY-Neu transgenic mice, Cancer Letters64:203.
Mangues, R., Seidman, I., Pellicer, A., and Gordon, J.W., 1990, Tumorigenesis and male sterility in transgenic mice expressing a MMTV/N-ras oncogene, Oncogene 5:1491.
Mansouri, A., Goudreau, G., and Gruss, P., 1999, Pax genes and their role in organogenesis, Cancer Res. Suppl59:1707s.
Maruyama, K., Tsudada, T., Dandoh, S., Sasaki, K., Ohkura, N., and Yamaguchi, K., 1995, Expression of NOR-1 and its closely related members of the steroid/thyroid hormone receptor superfamily in human neuroblastoma cell lines, Cancer Lett 96:117.
Maruyama, K., Tsukada, T., Bandoh, S., Sasaki, K., Ohkura, N., and Yamaguchi, K., 1997, Expression of the putative transcription factor NOR-1 in the nervous, endocrine and the immune systems and the developing brain of the rat, Neuroendocrinology 65:2.
Mastrangelo, P., Zwingman, T., Erickson, R.P., and Blecher, S.R., 1994, Zfy is transcribed in the normal mouse epididymis and in the XXSxr (“sex reversed”) testis, Develop. Genet15:129.
Matsuda, J., Suzuki, O., Oshima, A., Ogura, A., Noguchi, Y., Yamamoto, Y., Asano, T., Takimoto, K., Sukegawa, K., Suzuki, Y., and Naiki, M., 1997, Ăź-Galactosidase-deficient mouse as an animal model for GM1-gangliosidosis, Glycoconjugate J. 14:729.
Mattmueller, D.R., and Hinton, B.T., 1991, In vivo secretion and association of clusterin (SGP-2) in luminal fluid with spermatozoa in the rat testis and epididymis, Mol. Reprod. Dev30:62.
McGinnis, W., and Krumlauf, R., 1992, Homeobox genes and axial patterning, Cell 68:283.
Mendelsohn, C, Lohnes, D., Decimo, D., Lufkin, T., LeMeur, M., Chambon, P., and Mark, M., 1994, Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants, Development 120:2749.
Miranda, P.V., Brandelli, A., and TezĂłn, J.G., 1995, Characterization of p-N-acetylglucosaminidase from human epididymis, Intl. J. Androl 18:263.
Miyamoto, N., Yoshida, M., Kuratani, S., Matsuo, I., and Aizawa, S., 1997, Defects of urogenital development in mice lacking Emx2, Development 124:1653.
Morales, C.R., Igdoura, S.A., Wosu, U.A., Boman, J., and Argraves, W.S., 1996, Low density lipoprotein receptor-related protein 2 expression in efferent duct and epididymal epithelia: Evidence in rats for its in vivo role in endocytosis of apolipoprotein J/clusterin, Biol. Reprod55:676.
Muller, W.J., Sinn, E., Pattengale, P.K., Wallace, R., and Leder, P., 1988, Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene, Cell 54:105.
Mulryan, K., Gitterman, D.P., Lewis, C.J., Vial, C., Leckie, B.J., Cobb, A.L., Brown, J.E., Conley, E.C., Buell, G., Pritchard, C.A., and Evans, R.J., 2000, Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors, Nature 403:86.
Neckameyer, W.S., and Wang, L.H., 1985, Nucleotide sequence of avian sarcoma virus UR2 and comparison of its transforming gene with other members of the tyrosine protein kinase oncogene family, J. Virol. 53:879.
Oefelein, M., Grapey, D., Schaeffer, T., Chin-Chance, C, and Bushman, W., 1996, Pax-2: a developmental gene constitutively expressed in the mouse epididymis and ductus deferens, J. Urology156:1204.
Okamura, N., Dacheux, F., Venien, A., Onoe, S., Huet, J.-C., and Dacheux, J.-L., 1992, Localization of a maturation-dependent epididymal sperm surface antigen recognized by a monoclonal antibody raised against a 135-kilodalton protein in porcine epididymal fluid, Biol. Reprod47:1040.
Okamura, N., Tamba, M., Liao, H.-J., Onoe, S., Sugita, Y., Dacheux, F., and Dacheux, J.-L., 1995a, Cloning of complementary DNA encoding a 135-kilodalton protein secreted from porcine corpus epididymis and its identification as an epididymis-specific a-mannosidase, Mol. Reprod. Dev42:141.
Okamura, N., Tamba, M., Uchiyama, Y., Sugita, Y., Dacheux, F., Syntin, P., and Dacheux, J.L., 1995b, Direct evidence for the elevated synthesis and secretion of procathepsin L in the distal caput epididymis of boar, Biochim. Biophys Acta 1245:221.
Orgebin-Crist, M.-C, 1996, Androgens and epididymal function, in: Pharmacology, Biology, and Clinical Applications of Androgens, D. Bhasin, H.L. Gabelnick, J. M. Spieler, R.S. Swerdloff, and C. Wang, eds., Wiley-Liss, New York.
Pachnis, V., Mankoo, B., and Costantini, F., 1993, Expression of the c-ret proto-oncogene during mouse embryogenesis, Development 119:1005.
Palladino, M.A., and Hinton, B.T., 1994, Expression of multiple gamma glutamyl transpeptidase messenger ribonucleic acid transcripts in the adult rat epididymis is differentially regulated by androgens and testicular factors in a region-specific manner, Endocrinology 135:1146.
Parkkila, S., Parkkila, A.K., Kaunisto, K., Waheed, A., Sly, W.S., Rajaniemi, H., 1993, Location of a membrane-bound carbonic anhydrase isoenzyme (CA IV) in the human male reproductive tract, J. Histochem. Cytochem. 41:751.
Pera, I., Ivell, R., and Kirchhoff, C, 1994, Regional variation of specific gene expression in the dog epididymis as revealed by in situ transcript hybridization, Intl. J. Androl17:324.
Perry, A.C.F., Jones, R., Barker, P.J., and Hall, L., 1992, A mammalian epididymal protein with remarkable sequence similarity to snake venom haemorrhagic peptides, Biochem. J286:671.
Perry, A.C.F., Jones, R., and Hall, L., 1993, Isolation and characterization of a rat cDNA clone encoding a secreted superoxide dismutase reveals the epididymis to be a major site of its expression, Biochem. J293:21.
Petruszak, J.A.M., Nehme, C.L., and Bartles, J.R., 1991, Endoproteolytic cleavage in the extracellular domain of the integral plasma membrane protein CE9 precedes its redistribution from the posterior to the anterior tail of the rat spermatozoa during epididymal maturation, J. Cell Biol114:917.
Phelps, B.M., Koppel, D.E., Primakoff, P., and Myles, D.G., 1990, Evidence that proteolysis of the surface is an initial step in the mechanism of formation of sperm cell surface domains, J. Cell Biol111:1839.
Pitman, J.L., Lin, T.-P., Kleeman, J.E., Erickson, G.F., and MacLeod, C.L., 1998, Normal reproductive and macrophage function in Pern homeobox gene-deficient mice, Dev. Biol202: 196.
Pollard, J.W., Dominguez, M.G., Mocci, S., Cohen, P.E., and Stanley, E.R., 1997, Effect of the colony-stimulating factor-1 null mutation, osteopetrotic (csfm(op)), on the distribution of macrophages in the male mouse reproductive tract, Biol. Reprod56:1290.
Rajan, N., Sung, W.K., and Goodman, D.S., 1990, Localization of cellular retinol-binding protein mRNA in rat testis and epididymis and its stage-dependent expression during the cycle of the seminiferous epithelium, Biol. Reprod. 43:835.
Ram, P.A., Cardullo, R.A., and Millette, C.F., 1989, Expression and topographical localization of cell surface fucosyltransferase activity during epididymal sperm maturation in the mouse, Gamete Res22:321.
Rankin, T.L., Tsuruta, K.J., Holland, M.K., Griswold, M.D., and Orgebin-Crist, M.-C., 1992, Isolation, immunolocalization, and sperm-association of three proteins of 18,25, and 29 kilodaltons secreted by the mouse epididymis, Biol. Reprod46:141.
Reventos, J., Sullivan, P.M., Joseph, D.R., and Gordon, J.W., 1993, Tissue-specific expression of the rat androgen-binding protein/sex hormone-binding globulin gene in transgenic mice, Mol. Cell. Endocr96:69.
Robaire, B., 1979, Effects of unilateral orchidectomy on rat epididymal Δ4-5α-reductase and 3α- hydroxysteroid dehydrogenase. Can. J. Physiol. Pharmacol57:998.
Robaire, B., Ewing, L.L., Zirkin, B.R., and Irby, D.C., 1977, Steroid delta4–5alpha-reductase and 3alpha-hydroxysteroid dehydrogenase in the rat epididymis, Endocrinology 101:1379.
Robitaille, G., Sullivan, R., and Bleau, G., 1991, Identification of epididymal proteins associated with hamster sperm, J. Exp. Zool258:69.
Roselli, C.E., West, N.B., and Brenner, R.M., 1991, Androgen receptor and 5 alpha-reductase activity in the ductuli efferentes and epididymis of adult rhesus macaques, Biol. Reprod44:739.
Sandmoller, A., Voss, A.K., Hahn, J., Redemann-Fibi, B., Suske, G., and Beato, M., 1991, Cell-specific developmentally and hormonally regulated expression of the rabbit uteroglobin transgene and the endogenous mouse uteroglobin gene in transgenic mice, Mech. Dev34:57.
Sato, M., and Tada, N., 1995, Preferential expression of osteocalcin-related protein mRNA in gonadal tisues of male mice, Biochem. Biophys. Res. Comm215:412.
Satokata, I., Benson, G., and Mass, R., 1995, Sexually dimorphic sterility phenotypes in Hoxa1O-deficient mice, Nature 30:460.
Schwaab, V., Faure, J., Dufaure, J.-P., and Drevet, J.R., 1998, GPx3: The plasma-type glutathione peroxidase is expressed under androgenic control in the mouse epididymis and vas deferens, Mol. Reprod. Dev51: 362.
Scieglinska, D., Widlak, W., Rusin, M., Markkula, M., and Krawczyk, Z., 1997, Expression of the testis- specific HSP70-related gene (hst 70 gene) in somatic non-testicular rat tissues revealed by RT-PCR and transgenic mice analysis, Cell Biol. Intl21:813.
Seaton, G.J., Hall, L., and Jones, R., 2000, Ram sperm 2B1 glycoprotein (PH20) contains a C-terminal sequence motif for attachment of a glycosyl phosphatidylinositol anchor. Effects of endoproteolytic cleavage on hyaluronidase activity, Biol. Reprod62:1667.
Shu-Dong, T., Phillips, D.M., Halmi, N., Krieger, D., and Bardin, C.W., 1982, Ăź-Endorphin is present in the male reproductive tract of five species, Biol. Reprod27:755.
Skudlarek, M.D., Tulsiani, D.R.P., and Orgebin-Crist, M.-C., 1992, Rat epididymal luminal fluid acid Ăź-D-galactosidase optimally hydrolyses glycoprotein substrate at neutral pH, Biochem. J286:907.
Sonnenberg, E., Godecke, A., Walter, B., Bladt, F., and Birchmeier, C., 1991, Transient and locally restricted expression of the rosl protooncogene during mouse development, Embo J10:3693.
Sonnenberg-Riethmacher, E., Walter, B., Riethmacher, D., Godecke, S., and Birchmeier, C, 1996, The c-ros kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis, Gene. Develop. 10:1184.
Sornson, M.W., Wu, W., Dasen, J.S., Flynn, S.E., Norman, D.J., O’Connell, S.M., Gukovsky, I., Carriere, C., Ryan, A.K., Miller, A.P., Zuo, L., Gleiberman, A.S., Andersen, B., Beamer, W.G., and Rosenfeld, M.G., 1996, Pituitary lineage determination by the Prophet of Pit-1 homeodomain factor defective in Ames dwarfism, Nature 384:327.
Steinmayr, M., Andre, E., Conquet, F., Rondi-Reig, L., Delhaye-Bouchaud, N., Auclair, N., Daniel, H., Crepel, F., Mariani, J., Sotelo, C, and Becker-Andre, M., 1998, Staggerer phenotype in retinoid-related orphan receptor alpha-deficient mice, Proc. Natl. Acad. Sci95:3960.
Stocklin, E., Botterie, F., and Groner, B., 1993, An activated allele of the c-erbB-2 oncogene impairs kidney and lung function and causes early death of transgenic mice, J. Cell Biol122:199.
Stoykova, A., Fritsch, R., Walther, C., and Gruss, P., 1996, Forebrain patterning defects in small eye mutant mice, Development 122:3453.
Sun, E.L., and Flickinger, C.J., 1979, Development of cell types and of regional differences in the postnatal rat epididymis, Am. J. Anat154:27.
Sutton, H.G., Fusco, A., and Cornwall, G.A., 1999, Cystatin-related epididymal spermatogenic protein colocalizes with luteinizing hormone-beta protein in mouse anterior pituitary gonadotropes, Endocrinology 140:2721.
Sylvester, S.R., Morales, C., Oko, R., and Griswold, M.D., 1991, Localization of sulfated glycoprotein-1 (saponin precursor) in the reproductive tract of the male rat, Biol. Reprod41:941.
Syntin, P., Dacheux, F., Druart, X., Gatti, J.L., Okamura, N., and Dacheux, J.-J., 1996, Characterization and identification of proteins secreted in the various regions of the adult boar epididymis, Biol. Reprod. 55:956.
Syntin, P. and Cornwall, G.A., 1999, Immunolocalization of CRES (cystatin-related epididymal spermatogenic) protein in the acrosomes of mouse spermatozoa, Biol. Reprod60:1542.
Tanaka, T., Urade, Y., Kimura, H., Eguchi, N., Nishikawa, A., and Hayaishi, O., 1997, Lipocalin-type prostaglandin D synthase (beta-trace) is a newly recognized type of retinoid transporter, J. Biol. Chem272:15789.
Tate, P.H., and Bird, A.P., 1993, Effects of DNA methylation on DNA-binding proteins and gene expression, Curr. Opin. Genet. Dev3:226.
Tehranian, A., Morris, D.W., Min, B.H., Bird, D.J., Cardiff, R.D., and Barry, P.A., 1996, Neoplastic transformation of prostatic and urogenital epithelium by the polyoma virus middle T gene, Am. J. Path149:1177.
Torres, M., Gomez-Pardo, E., Dressier, G.R., and Gruss, P., 1995, Pax-2 controls multiple steps of urogenital development, Development121:4057.
Toshimori, K., Kuwajima, M., Yoshinaga, K., Wakayama, T., and Shima, K., 1999, Dysfunction of the epididymis as a result of primary carnitine deficiency in juvenile visceral steatosis mice, FEBS Letters 446:323.
Treier, M., and Rosenfeld, M.G., 1996, The hypothalamic-pituitary axis: co-development of two organs, Curr. Opin. Cell Biol. 8:833.
Troen, G., Esklid, W., Fromm, S.H., Reppe, S., Nilsson, A., Norum, K.R., and Blomhoff, R., 1996, Retinyl ester storage is normal in transgenic mice with enhanced expression of cellular retinol-binding protein type 1, J. Nutr126:2709.
Tulsiani, D.R.P., Skudlarek, M.D., Holland, M.K., and Orgebin-Crist, M.-C., 1993, Glycosylation of rat sperm plasma membrane during epididymal maturation, 1993, Biol. Reprod48:417.
Tulsiani, D.R.P., Skudlarek, M.D., Araki, Y., and Orgebin-Crist, M.-C., 1995, Purification and characterization of two forms of Ăź-D-galactosidase from rat epididymal luminal fluid: evidence for their role in the modification of sperm plasma membrane glycoprotein(s), Biochem. J305:41.
Ungefroren, H., lvell, R., and Ergun, S., 1997, Region-specific expression of the androgen receptor in the human epididymis, Mol. Hum. Reprod. 3:933.
Viger, R.S., and Robaire, B., 1991, Differential regulation of steady state 4-ene steroid 5 alpha-reductase messenger ribonucleic acid levels along the rat epididymis, Endocrinology 128:2407.
Viger, R.S., and Robaire, B., 1994, Immunocytochemical localization of 4-ene steroid 5 alpha-reductase type 1 along the rat epididymis during postnatal development, Endocrinology 134:2298.
Viger, R.S., and Robaire, B., 1995, Gene expression in the aging Brown Norway rat epididymis, J. Androl 16:2.
Viger, R.S., and Robaire, B., 1996, The mRNAs for the steroid 5α-reductase isozymes, type 1 and type 2, are differentially regulated in the rat epididymis, J. Androl17:27.
Wagenfeld, A., Yeung, C.-H., and Cooper, T.G., 2000, Altered epididymal protein and RNA expression in infertile c-ros tyrosine kinase receptor knockout mice, 11 th European Workshop in Molecular and Cellular Endocrinology of the TestisH4 (abstract).
Wan, Y.J.Y., Wang, L., and Wu, T.C.J., 1992, Detection of retinoic acid receptor mRNA in rat tissues by reverse transcriptase-polymerase chain reaction, J. Mol. Endocr9:291.
Wasylyk, C, Flores, P., Gutman, A., Wasylyk, B., 1989, PEA3 is a nuclear target for transcription activation by non-nuclear oncogenes, EMBO J8:3371.
Wilkinson, L., Sweeny, P.R., and Blecher, S.R., 1988, Ultrastructural abnormalities of epididymal tissues in XXSxr pseudomale (sex-reversed) mice, Arch. Androl.20:11.
Willnow, T.E., Nykjaer, A., and Herz, J., 1999, Lipoprotein receptors: new roles for ancient proteins, Nature Cell Biol1:E157.
Wilson, C.L., Heppner, K.J., Rudolph, L.A., and Matrisian, L.M., 1995, The metalloproteinase matrilysin is preferentially expressed by epithelial cells in a tissue-restricted pattern in the mouse, Mol Biol. Cell6:851.
Winer, M.A., Wadewitz, A.G., and Wolgemuth, D.J., 1993, Members of the raf gene family exhibit segment-specific patterns of expression in mouse epididymis, Mol. Reprod. Develop35:16.
Wolfsberg, T.G., and White, J.M., 1996, ADAMs in fertilization and development, Dev. Biol. 180:389. Wong, P.Y., and Uchendu, C.N., 1990, The role of angiotensin-converting enzyme in the rat epididymis, J. Endocrin125:457.
Xie, W., Paterson, A. J., Chin, E., Nabell, L.M., and Kudlow, J.E., 1997, Targeted expression of a dominant negative epidermal growth factor receptor in the mammary gland of transgenic mice inhibits pubertal mammary duct development, Mol. Endocrinol11:1766.
Xin, J.-H., Cowie, A., Lachance, P., Hassell, J.A., 1992, Molecular cloning and characterization of PEA3, a new member of the Ets oncogene family that is differentially expressed in mouse embryonic cells, Genes and Develop. 6:481.
Yeung, C.H., Sonnenberg-Riethmacher, E., and Cooper, T.G., 1999, Infertile spermatozoa of c-ros tyrosine kinase receptor knockout mice show flagellar angulation and maturational defects in cell volume regulatory mechanisms, Biol. Reprod61:1062
Zhao, W., Leung, P.Y., Cheng Chew, S.B., Chan, H.C., and Wong, P.Y.D., 1996, Localization and distribution of angiotensin II in the rat epididymis, J. Endocrin149:217.
Zhao, G.Q., Liaw, L., and Hogan, B.L., 1998, Bone morphogenetic protein 8A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis, Development 125:1103.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer Science+Business Media New York
About this chapter
Cite this chapter
Cornwall, G.A., Lareyre, JJ., Matusik, R.J., Hinton, B.T., Orgebin-Crist, MC. (2002). Gene Expression and Epididymal Function. In: Robaire, B., Hinton, B.T. (eds) The Epididymis: From Molecules to Clinical Practice. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0679-9_10
Download citation
DOI: https://doi.org/10.1007/978-1-4615-0679-9_10
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5191-7
Online ISBN: 978-1-4615-0679-9
eBook Packages: Springer Book Archive