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Contents
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[1]T. W. Cooper: Epididymis. In: Encyclopedia of reproduction. Ed N. J. Knobil E. Academic Press, San Diego (1998)
[2]J. M. Bedford: The status and the state of the human epididymis. Hum Reprod, 9(11), 2187-99 (1994)
[3]R. Sullivan and F. Saez: Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction, 146(1), R21-35 (2013)
[4]R. Sullivan, F. Saez, J. Girouard and G. Frenette: Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis, 35(1), 1-10 (2005)
[5]R. C. Jones: Evolution of the epididymis. In: The epididymis From molecules to clinical practice. A comprehensive survey of the efferent ducts, the epididymis and the vas deferens. Ed H. B. Robaire B. Kluwer Academic/Plenum Publishers, New York (2002)
[6]T. T. Turner: De Graaf’s thread: the human epididymis. J Androl, 29(3), 237-50 (2008)
[7]G. A. Cornwall, Lareyre, J.J., Matusik, R.J., Hinton, B.T., Orgebin-Crist, M.C.: Gene expression and epididymal function. In: The epididymis: from molecules to clinical practice. Ed B. Robaire, Hinton BT. Klumer academic/Plenum Publishers, New York (2002)
[8]D. S. Johnston, S. A. Jelinsky, H. J. Bang, P. Dicandeloro, E. Wilson, G. S. Kopf and T. T. Turner: The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod, 73(3), 404-13 (2005)
[9]R. C. Jones: Evolution of the vertebrate epididymis. J Reprod Fertil Suppl, 53, 163-81 (1998)
[10]J. Girouard, G. Frenette and R. Sullivan: Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int J Androl, 34(5 Pt 2), e475-86 (2011)
[11]T. G. Cooper: Interactions between epididymal secretions and spermatozoa. J Reprod Fertil Suppl, 53, 119-36 (1998)
[12]C. Belleannee, V. Thimon and R. Sullivan: Region-specific gene expression in the epididymis. Cell Tissue Res, 349(3), 717-31 (2012)
[13]D. G. Cyr: Connexins and pannexins: Coordinating cellular communication in the testis and epididymis. Spermatogenesis, 1(4), 325-338 (2011)
[14]G. J. Dacheux JL, Castella S, Metayer S, Fouchecourt S, Dacheux F.: The epididymal proteome. In: The third international conference on the epididymis. Ed T. T. Hinton B. The Van Doren Co., Charlottesveill, Virginia, USA (2003)
[15]J. L. Dacheux, M. Belghazi, Y. Lanson and F. Dacheux: Human epididymal secretome and proteome. Mol Cell Endocrinol, 250(1-2), 36-42 (2006)
[16]J. L. Dacheux, C. Belleannee, R. Jones, V. Labas, M. Belghazi, B. Guyonnet, X. Druart, J. L. Gatti and F. Dacheux: Mammalian epididymal proteome. Mol Cell Endocrinol, 306(1-2), 45-50 (2009)
[17]E. Dube, P. T. Chan, L. Hermo and D. G. Cyr: Gene expression profiling and its relevance to the blood-epididymal barrier in the human epididymis. Biol Reprod, 76(6), 1034-44 (2007)
[18]V. Thimon, O. Koukoui, E. Calvo and R. Sullivan: Region-specific gene expression profiling along the human epididymis. Mol Hum Reprod, 13(10), 691-704 (2007)
[19]R. Sullivan: Interaction between sperm and epididymal secretory proteins. In: The male gamete: from basic to clinical applications. Ed C. Gagnon. Cache River Press., Vienna (IL, USA) (1999)
[20]Z. Arsov, M. Schara, M. Zorko and J. Strancar: The membrane lateral domain approach in the studies of lipid-protein interaction of GPI-anchored bovine erythrocyte acetylcholinesterase. Eur Biophys J, 33(8), 715-725 (2004)
[21]R. Sullivan, G. Frenette and J. Girouard: Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl, 9(4), 483-91 (2007)
[22]R. Yanagimachi, Y. Kamiguchi, K. Mikamo, F. Suzuki and H. Yanagimachi: Maturation of spermatozoa in the epididymis of the Chinese hamster. Am J Anat, 172(4), 317-30 (1985)
[23]C. Legare, B. Berube, F. Boue, L. Lefievre, C. R. Morales, M. El-Alfy and R. Sullivan: Hamster sperm antigen P26h is a phosphatidylinositol-anchored protein. Mol Reprod Dev, 52(2), 225-33 (1999)
[24]G. S. Griffiths, D. S. Galileo, K. Reese and P. A. Martin-Deleon: Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Mol Reprod Dev, 75(11), 1627-36 (2008)
[25]H. Rejraji, B. Sion, G. Prensier, M. Carreras, C. Motta, J. M. Frenoux, E. Vericel, G. Grizard, P. Vernet and J. R. Drevet: Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod, 74(6), 1104-13 (2006)
[26]P. Grimalt, F. Bertini and M. W. Fornes: High-affinity sites for beta-D-galactosidase on membrane-bound vesicles isolated from rat epididymal fluid. Arch Androl, 44(2), 85-91 (2000)
[27]G. Frenette and R. Sullivan: Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev, 59(1), 115-21 (2001)
[28]G. Frenette, C. Lessard and R. Sullivan: Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod, 67(1), 308-13 (2002)
[29]J. L. Gatti, S. Castella, F. Dacheux, H. Ecroyd, S. Metayer, V. Thimon and J. L. Dacheux: Post-testicular sperm environment and fertility. Anim Reprod Sci, 82-83, 321-39 (2004)
[30]H. Ecroyd, P. Sarradin, J. L. Dacheux and J. L. Gatti: Compartmentalization of prion isoforms within the reproductive tract of the ram. Biol Reprod, 71(3), 993-1001. Epub 2004 May 26. (2004)
[31]V. Thimon, Frenette, G, Saez, S, Thabet, M, Sullivan, R: Protein composition of human epididymosomes: a proteomic and genomic approach. Hum. Reprod., Under revision (2008)
[32]J. N. Caballero, G. Frenette, C. Belleannee and R. Sullivan: CD9-positive microvesicles mediate the transfer of molecules to Bovine Spermatozoa during epididymal maturation. PLoS One, 8(6), e65364 (2013)
[33]T. G. Paunescu, W. W. Shum, C. Huynh, L. Lechner, B. Goetze, D. Brown and S. Breton: High-resolution helium ion microscopy of epididymal epithelial cells and their interaction with spermatozoa. Mol Hum Reprod (2014)
[34]A. Schwarz, G. Wennemuth, H. Post, T. Brandenburger, G. Aumuller and B. Wilhelm: Vesicular transfer of membrane components to bovine epididymal spermatozoa. Cell Tissue Res, 353(3), 549-61 (2013)
[35]J. L. Gatti, S. Metayer, M. Belghazi, F. Dacheux and J. L. Dacheux: Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol Reprod, 72(6), 1452-65 (2005)
[36]G. Aumuller, B. Wilhelm and J. Seitz: Apocrine secretion--fact or artifact? Anat Anz, 181(5), 437-46 (1999)
[37]G. Aumuller, H. Renneberg, P. J. Schiemann, B. Wilhelm, J. Seitz, L. Konrad and G. Wennemuth: The role of apocrine released proteins in the post-testicular regulation of human sperm function. Adv Exp Med Biol, 424, 193-219 (1997)
[38]L. Hermo and D. Jacks: Nature’s ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev, 63(3), 394-410 (2002)
[39]C. Thery, L. Zitvogel and S. Amigorena: Exosomes: composition, biogenesis and function. Nat Rev Immunol, 2(8), 569-79 (2002)
[40]D. S. Friend: Cytochemical staining of multivesicular body and golgi vesicles. J Cell Biol, 41(1), 269-79 (1969)
[41]C. C. Beu, A. M. Orsi and R. F. Domeniconi: Structure of the lining epithelium of the cauda epididymis of the golden hamster. Anat Histol Embryol, 38(1), 49-57 (2009)
[42]G. Frenette, J. Girouard and R. Sullivan: Comparison between epididymosomes collected in the intraluminal compartment of the bovine caput and cauda epididymidis. Biol Reprod, 75(6), 885-90 (2006)
[43]C. A. Mawson and M. I. Fischer: Zinc content of the genital organs of the rat. Nature, 167(4256), 859 (1951)
[44]P. A. Martin-Deleon: Epididymal SPAM1 and its impact on sperm function. Mol Cell Endocrinol (2006)
[45]J. Caballero, G. Frenette, O. D’Amours, C. Belleannee, N. Lacroix-Pepin, C. Robert and R. Sullivan: Bovine sperm raft membrane associated Glioma Pathogenesis-Related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. J Cell Physiol, 227(12), 3876-86 (2012)
[46]J. S. Oh, C. Han and C. Cho: ADAM7 is associated with epididymosomes and integrated into sperm plasma membrane. Mol Cells, 28(5), 441-6 (2009)
[47]E. Chabory, C. Damon, A. Lenoir, G. Kauselmann, H. Kern, B. Zevnik, C. Garrel, F. Saez, R. Cadet, J. Henry-Berger, M. Schoor, U. Gottwald, U. Habenicht, J. R. Drevet and P. Vernet: Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Invest, 119(7), 2074-85 (2009)
[48]P. Sutovsky, R. Moreno, J. Ramalho-Santos, T. Dominko, W. E. Thompson and G. Schatten: A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci, 114(Pt 9), 1665-75 (2001)
[49]C. Kirchhoff and G. Hale: Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Mol Hum Reprod, 2(3), 177-84 (1996)
[50]O. D’Amours, L. J. Bordeleau, G. Frenette, P. Blondin, P. Leclerc and R. Sullivan: Binder of sperm 1 and epididymal sperm binding protein 1 are associated with different bull sperm subpopulations. Reproduction, 143(6), 759-71 (2012)
[51]O. D’Amours, G. Frenette, L. J. Bordeleau, N. Allard, P. Leclerc, P. Blondin and R. Sullivan: Epididymosomes transfer epididymal sperm binding protein 1 (ELSPBP1) to dead spermatozoa during epididymal transit in bovine. Biol Reprod, 87(4), 94 (2012)
[52]D. Krapf, Y. C. Ruan, E. V. Wertheimer, M. A. Battistone, J. B. Pawlak, A. Sanjay, S. H. Pilder, P. Cuasnicu, S. Breton and P. E. Visconti: cSrc is necessary for epididymal development and is incorporated into sperm during epididymal transit. Dev Biol, 369(1), 43-53 (2012)
[53]R. Eickhoff, C. Baldauf, H. W. Koyro, G. Wennemuth, Y. Suga, J. Seitz, R. Henkel and A. Meinhardt: Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: indications for a new role of MIF in sperm maturation. Mol Hum Reprod, 10(8), 605-11 (2004)
[54]R. Eickhoff, G. Jennemann, G. Hoffbauer, M. P. Schuring, H. Kaltner, F. Sinowatz, H. J. Gabius and J. Seitz: Immunohistochemical detection of macrophage migration inhibitory factor in fetal and adult bovine epididymis: release by the apocrine secretion mode? Cells Tissues Organs, 182(1), 22-31 (2006)
[55]G. Frenette, C. Lessard, E. Madore, M. A. Fortier and R. Sullivan: Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol Reprod, 69(5), 1586-92 (2003)
[56]A. R. Suryawanshi, S. A. Khan, C. S. Joshi and V. V. Khole: Epididymosome-mediated acquisition of MMSDH, an androgen-dependent and developmentally regulated epididymal sperm protein. J Androl, 33(5), 963-74 (2012)
[57]S. Asuvapongpatana, A. Saewu, C. Chotwiwatthanakun, R. Vanichviriyakit and W. Weerachatyanukul: Localization of cathepsin D in mouse reproductive tissues and its acquisition onto sperm surface during epididymal sperm maturation. Acta Histochem, 115(5), 425-33 (2013)
[58]J. Girouard, G. Frenette and R. Sullivan: Compartmentalization of proteins in epididymosomes coordinates the association of epididymal proteins with the different functional structures of bovine spermatozoa. Biol Reprod, 80(5), 965-72 (2009)
[59]R. Jones: Plasma membrane structure and remodelling during sperm maturation in the epididymis. J Reprod Fertil Suppl, 53, 73-84 (1998)
[60]R. Eickhoff, B. Wilhelm, H. Renneberg, G. Wennemuth, M. Bacher, D. Linder, R. Bucala, J. Seitz and A. Meinhardt: Purification and characterization of macrophage migration inhibitory factor as a secretory protein from rat epididymis: evidences for alternative release and transfer to spermatozoa. Mol Med, 7(1), 27-35 (2001)
[61]G. Frenette, J. Girouard, O. D’Amours, N. Allard, L. Tessier and R. Sullivan: Characterization of two distinct populations of epididymosomes collected in the intraluminal compartment of the bovine cauda epididymis. Biol Reprod, 83(3), 473-80 (2010)
[62]M. W. Fornes, A. Barbieri and J. C. Cavicchia: Morphological and enzymatic study of membrane-bound vesicles from the lumen of the rat epididymis. Andrologia, 27(1), 1-5 (1995)
[63]M. W. Fornes, A. Barbieri, M. A. Sosa and F. Bertini: First observations on enzymatic activity and protein content of vesicles separated from rat epididymal fluid. Andrologia, 23(5), 347-51 (1991)
[64]C. Belleannee, E. Calvo, J. Caballero and R. Sullivan: Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol Reprod, 89(2), 30 (2013)
[65]C. Belleannee, E. Calvo, V. Thimon, D. G. Cyr, C. Legare, L. Garneau and R. Sullivan: Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoS One, 7(4), e34996 (2012)
[66]C. Belleannee, C. Legare, E. Calvo, V. Thimon and R. Sullivan: microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum Reprod, 28(6), 1455-67 (2013)
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Frontiers in Bioscience-Scholar (FBS) is published by IMR Press from Volume 13 Issue 1 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Epididymosomes: Role of extracellular microvesicles in sperm maturation
1 Department of Obstetrics, Gynecology and Reproduction, Faculty of Medicine, Universite Laval, and, Reproduction, Mother and Youth Health Division, Centre de Recherche du CHU de Quebec
*Author to whom correspondence should be addressed.
Abstract
The spermatozoa of vertebrate species that practice internal fertilization have to transit along the epididymis after leaving the testis. This epididymis is a single, long convoluted tubule that links the testis to the vas deferens (1). During this transit, the male gametes acquire their fertilizing ability and their forward motility properties. Collectively, these modifications known as sperm maturation depend on a series of well-orchestrated biochemical modifications imposed upon the transiting male gamete (2). These modifications are in part regulated by extracellular microvesicles called epididymosomes that are found in the intraluminal epididymal compartment (3, 4). In this review, the biochemical composition of epididymosomes, their mode of secretion, the mechanisms underlying their interactions with the male gamete, and how they are involved in sperm maturation will be described.
Keywords
- Epididymis
- Spermatozoa
- Andrology
- Sperm Maturation
- Exosomes
- Epididymosomes
- Extracellular Microvesicles
- Male Reproductive Tract
- Review
References
- [1] T. W. Cooper: Epididymis. In: Encyclopedia of reproduction. Ed N. J. Knobil E. Academic Press, San Diego (1998)
- [2] J. M. Bedford: The status and the state of the human epididymis. Hum Reprod, 9(11), 2187-99 (1994)
- [3] R. Sullivan and F. Saez: Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction, 146(1), R21-35 (2013)
- [4] R. Sullivan, F. Saez, J. Girouard and G. Frenette: Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis, 35(1), 1-10 (2005)
- [5] R. C. Jones: Evolution of the epididymis. In: The epididymis From molecules to clinical practice. A comprehensive survey of the efferent ducts, the epididymis and the vas deferens. Ed H. B. Robaire B. Kluwer Academic/Plenum Publishers, New York (2002)
- [6] T. T. Turner: De Graaf’s thread: the human epididymis. J Androl, 29(3), 237-50 (2008)
- [7] G. A. Cornwall, Lareyre, J.J., Matusik, R.J., Hinton, B.T., Orgebin-Crist, M.C.: Gene expression and epididymal function. In: The epididymis: from molecules to clinical practice. Ed B. Robaire, Hinton BT. Klumer academic/Plenum Publishers, New York (2002)
- [8] D. S. Johnston, S. A. Jelinsky, H. J. Bang, P. Dicandeloro, E. Wilson, G. S. Kopf and T. T. Turner: The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod, 73(3), 404-13 (2005)
- [9] R. C. Jones: Evolution of the vertebrate epididymis. J Reprod Fertil Suppl, 53, 163-81 (1998)
- [10] J. Girouard, G. Frenette and R. Sullivan: Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int J Androl, 34(5 Pt 2), e475-86 (2011)
- [11] T. G. Cooper: Interactions between epididymal secretions and spermatozoa. J Reprod Fertil Suppl, 53, 119-36 (1998)
- [12] C. Belleannee, V. Thimon and R. Sullivan: Region-specific gene expression in the epididymis. Cell Tissue Res, 349(3), 717-31 (2012)
- [13] D. G. Cyr: Connexins and pannexins: Coordinating cellular communication in the testis and epididymis. Spermatogenesis, 1(4), 325-338 (2011)
- [14] G. J. Dacheux JL, Castella S, Metayer S, Fouchecourt S, Dacheux F.: The epididymal proteome. In: The third international conference on the epididymis. Ed T. T. Hinton B. The Van Doren Co., Charlottesveill, Virginia, USA (2003)
- [15] J. L. Dacheux, M. Belghazi, Y. Lanson and F. Dacheux: Human epididymal secretome and proteome. Mol Cell Endocrinol, 250(1-2), 36-42 (2006)
- [16] J. L. Dacheux, C. Belleannee, R. Jones, V. Labas, M. Belghazi, B. Guyonnet, X. Druart, J. L. Gatti and F. Dacheux: Mammalian epididymal proteome. Mol Cell Endocrinol, 306(1-2), 45-50 (2009)
- [17] E. Dube, P. T. Chan, L. Hermo and D. G. Cyr: Gene expression profiling and its relevance to the blood-epididymal barrier in the human epididymis. Biol Reprod, 76(6), 1034-44 (2007)
- [18] V. Thimon, O. Koukoui, E. Calvo and R. Sullivan: Region-specific gene expression profiling along the human epididymis. Mol Hum Reprod, 13(10), 691-704 (2007)
- [19] R. Sullivan: Interaction between sperm and epididymal secretory proteins. In: The male gamete: from basic to clinical applications. Ed C. Gagnon. Cache River Press., Vienna (IL, USA) (1999)
- [20] Z. Arsov, M. Schara, M. Zorko and J. Strancar: The membrane lateral domain approach in the studies of lipid-protein interaction of GPI-anchored bovine erythrocyte acetylcholinesterase. Eur Biophys J, 33(8), 715-725 (2004)
- [21] R. Sullivan, G. Frenette and J. Girouard: Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl, 9(4), 483-91 (2007)
- [22] R. Yanagimachi, Y. Kamiguchi, K. Mikamo, F. Suzuki and H. Yanagimachi: Maturation of spermatozoa in the epididymis of the Chinese hamster. Am J Anat, 172(4), 317-30 (1985)
- [23] C. Legare, B. Berube, F. Boue, L. Lefievre, C. R. Morales, M. El-Alfy and R. Sullivan: Hamster sperm antigen P26h is a phosphatidylinositol-anchored protein. Mol Reprod Dev, 52(2), 225-33 (1999)
- [24] G. S. Griffiths, D. S. Galileo, K. Reese and P. A. Martin-Deleon: Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Mol Reprod Dev, 75(11), 1627-36 (2008)
- [25] H. Rejraji, B. Sion, G. Prensier, M. Carreras, C. Motta, J. M. Frenoux, E. Vericel, G. Grizard, P. Vernet and J. R. Drevet: Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod, 74(6), 1104-13 (2006)
- [26] P. Grimalt, F. Bertini and M. W. Fornes: High-affinity sites for beta-D-galactosidase on membrane-bound vesicles isolated from rat epididymal fluid. Arch Androl, 44(2), 85-91 (2000)
- [27] G. Frenette and R. Sullivan: Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev, 59(1), 115-21 (2001)
- [28] G. Frenette, C. Lessard and R. Sullivan: Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod, 67(1), 308-13 (2002)
- [29] J. L. Gatti, S. Castella, F. Dacheux, H. Ecroyd, S. Metayer, V. Thimon and J. L. Dacheux: Post-testicular sperm environment and fertility. Anim Reprod Sci, 82-83, 321-39 (2004)
- [30] H. Ecroyd, P. Sarradin, J. L. Dacheux and J. L. Gatti: Compartmentalization of prion isoforms within the reproductive tract of the ram. Biol Reprod, 71(3), 993-1001. Epub 2004 May 26. (2004)
- [31] V. Thimon, Frenette, G, Saez, S, Thabet, M, Sullivan, R: Protein composition of human epididymosomes: a proteomic and genomic approach. Hum. Reprod., Under revision (2008)
- [32] J. N. Caballero, G. Frenette, C. Belleannee and R. Sullivan: CD9-positive microvesicles mediate the transfer of molecules to Bovine Spermatozoa during epididymal maturation. PLoS One, 8(6), e65364 (2013)
- [33] T. G. Paunescu, W. W. Shum, C. Huynh, L. Lechner, B. Goetze, D. Brown and S. Breton: High-resolution helium ion microscopy of epididymal epithelial cells and their interaction with spermatozoa. Mol Hum Reprod (2014)
- [34] A. Schwarz, G. Wennemuth, H. Post, T. Brandenburger, G. Aumuller and B. Wilhelm: Vesicular transfer of membrane components to bovine epididymal spermatozoa. Cell Tissue Res, 353(3), 549-61 (2013)
- [35] J. L. Gatti, S. Metayer, M. Belghazi, F. Dacheux and J. L. Dacheux: Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol Reprod, 72(6), 1452-65 (2005)
- [36] G. Aumuller, B. Wilhelm and J. Seitz: Apocrine secretion--fact or artifact? Anat Anz, 181(5), 437-46 (1999)
- [37] G. Aumuller, H. Renneberg, P. J. Schiemann, B. Wilhelm, J. Seitz, L. Konrad and G. Wennemuth: The role of apocrine released proteins in the post-testicular regulation of human sperm function. Adv Exp Med Biol, 424, 193-219 (1997)
- [38] L. Hermo and D. Jacks: Nature’s ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev, 63(3), 394-410 (2002)
- [39] C. Thery, L. Zitvogel and S. Amigorena: Exosomes: composition, biogenesis and function. Nat Rev Immunol, 2(8), 569-79 (2002)
- [40] D. S. Friend: Cytochemical staining of multivesicular body and golgi vesicles. J Cell Biol, 41(1), 269-79 (1969)
- [41] C. C. Beu, A. M. Orsi and R. F. Domeniconi: Structure of the lining epithelium of the cauda epididymis of the golden hamster. Anat Histol Embryol, 38(1), 49-57 (2009)
- [42] G. Frenette, J. Girouard and R. Sullivan: Comparison between epididymosomes collected in the intraluminal compartment of the bovine caput and cauda epididymidis. Biol Reprod, 75(6), 885-90 (2006)
- [43] C. A. Mawson and M. I. Fischer: Zinc content of the genital organs of the rat. Nature, 167(4256), 859 (1951)
- [44] P. A. Martin-Deleon: Epididymal SPAM1 and its impact on sperm function. Mol Cell Endocrinol (2006)
- [45] J. Caballero, G. Frenette, O. D’Amours, C. Belleannee, N. Lacroix-Pepin, C. Robert and R. Sullivan: Bovine sperm raft membrane associated Glioma Pathogenesis-Related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. J Cell Physiol, 227(12), 3876-86 (2012)
- [46] J. S. Oh, C. Han and C. Cho: ADAM7 is associated with epididymosomes and integrated into sperm plasma membrane. Mol Cells, 28(5), 441-6 (2009)
- [47] E. Chabory, C. Damon, A. Lenoir, G. Kauselmann, H. Kern, B. Zevnik, C. Garrel, F. Saez, R. Cadet, J. Henry-Berger, M. Schoor, U. Gottwald, U. Habenicht, J. R. Drevet and P. Vernet: Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Invest, 119(7), 2074-85 (2009)
- [48] P. Sutovsky, R. Moreno, J. Ramalho-Santos, T. Dominko, W. E. Thompson and G. Schatten: A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci, 114(Pt 9), 1665-75 (2001)
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