Animal Reproduction (AR)
Animal Reproduction (AR)

The epididymis and its role on sperm quality and male fertility

Ana Paula Binato de Souza, Ângela Maria Schorr-Lenz, Franciele Lucca, Ivan Cunha Bustamante-Filho

Downloads: 11
Views: 3044


The epididymis is a complex organ where spermatozoa acquire motility and ability to fertilize the egg. Epididymal maturation lasts 1 or 2 weeks and exposes the immature spermatozoa to a sequentially modified milieu, promoting intense interactions with secretions by the epididymal epithelium. Sperm surface modifications in response to interactions with epididymal secretions are key steps to achieve fertility ability. However, the precise molecular mechanisms that convert an immotile and infertile gamete into a highly motile cell capable of fusion with an oocyte are still unknown. Recent data on proteomics and transcriptomics of epididymal fluid and epididymosomes brought new ideas of the physiological roles of proteins and miRNAs in epididymal maturation in spermatozoa. This review focuses on the recent discoveries on epididymal fluid composition and its role on sperm maturation and preservation, linking to their survival and fertility potential.


epididymis, epididymosomes, spermatozoa, proteomics, sperm maturation.


Abe K, Takano H. 1989. Cytological response of the principal cells in the initial segment of the epididymal duct to efferent duct cutting in mice. Arch Histol Cytol, 52:321-326.

Amaral A, Castillo J, Estanyol JM, Ballesca JL, Ramalho-Santos J, Oliva R. 2013. Human sperm tail proteome suggests new endogenous metabolic pathways. Mol Cell Proteomics, 12:330-342.

Amaral A, Castillo J, Ramalho-Santos J, Oliva R. 2014. The combined human sperm proteome: cellular pathways and implications for basic and clinical science. Hum Reprod Update, 20:40-62.

Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell, 136:215-233.

Beaulieu V, Da Silva N, Pastor-Soler N, Brown CR, Smith PJ, Brown D, Breton S. 2005. Modulation of the actin cytoskeleton via gelsolin regulates vacuolar H+-ATPase recycling. J Biol Chem, 280:8452-8463.

Belleannee C, Belghazi M, Labas V, Teixeira-Gomes AP, Gatti JL, Dacheux JL, Dacheux F. 2011a. Purification and identification of sperm surface proteins and changes during epididymal maturation. Proteomics, 11:1952-1964.

Belleannee C, Calvo E, Caballero J, Sullivan R. 2013. Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol Reprod, 89:30.

Belleannee C, Calvo E, Thimon V, Cyr DG, Legare C, Garneau L, Sullivan R. 2012a. Role of microRNAs in controlling gene expression in different segments of the human epididymis. PloS one, 7:e34996.

Belleannee C, Labas V, Teixeira-Gomes AP, Gatti JL, Dacheux JL, Dacheux F. 2011b. Identification of luminal and secreted proteins in bull epididymis. J Proteomics, 74:59-78.

Belleannee C, Thimon V, Sullivan R. 2012b. Regionspecific gene expression in the epididymis. Cell Tissue Res, 349:717-731.

Bilinska B, Wiszniewska B, Kosiniak-Kamysz K, Kotula-Balak M, Gancarczyk M, Hejmej A, Sadowska J, Marchlewicz M, Kolasa A, WendaRozewicka L. 2006. Hormonal status of male reproductive system: androgens and estrogens in the testis and epididymis. In vivo and in vitro approaches. Reprod Biol, 6(Suppl. 1):43-58.

Bjorkgren I, Saastamoinen L, Krutskikh A, Huhtaniemi I, Poutanen M, Sipila P. 2012. Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling. PloS one, 7:e38457.

Blomqvist SR, Vidarsson H, Soder O, Enerback S. 2006. Epididymal expression of the forkhead transcription factor Foxi1 is required for male fertility. EMBO J, 25:4131-4141.

Bork K, Chevrier C, Paquignon M, Jouannet P, Dacheux JL. 1988. [Flagellar motility amd movement of boar spermatozoa during epididymal transit]. Reprod Nutr Dev, 28:1307-1315.

Breton S, Ruan YC, Park YJ, Kim B. 2016. Regulation of epithelial function, differentiation, and remodeling in the epididymis. Asian J Androl, 18:3-9.

Brooks DE. 1976. Changes in the composition of the excurrent duct system of the rat testis during postnatal development. J Reprod Fertil, 46:31-38.

Cancel AM, Chapman DA, Killian GJ. 1997. Osteopontin Is the 55-Kilodalton Fertility-Associated Protein in Holstein Bull Seminal Plasma. Biol Reprod, 57:1293-1301.

Carlson AE, Hille B, Babcock DF. 2007. External Ca2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. Dev Biol, 312:183-192.

Carlson AE, Westenbroek RE, Quill T, Ren D, Clapham DE, Hille B, Garbers DL, Babcock DF. 2003. CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci U S A, 100:14864-14868.

Castella S, Benedetti H, de Llorens R, Dacheux JL, Dacheux F. 2004. Train A, an RNase A-like protein without RNase activity, is secreted and reabsorbed by the same epididymal cells under testicular control. Biol Reprod, 71:1677-1687.

Chevrier C, Dacheux JL. 1992. Evolution of the flagellar waveform of ram spermatozoa in relation to the degree of epididymal maturation. Cell Motil Cytoskeleton, 23:8-18.

Clulow J, Jones RC, Hansen LA. 1994. Micropuncture and cannulation studies of fluid composition and transport in the ductuli efferentes testis of the rat: comparisons with the homologous metanephric proximal tubule. Exp Physiol, 79:915-928.

Cooper TG. 1998. Interactions between epididymal secretions and spermatozoa. J Reprod Fertil Suppl, 53:119-136.

Cooper TG, Barfield JP. 2006. Utility of infertile male models for contraception and conservation. Mol Cell Endocrinol, 250:206-211.

Cornwall GA. 2009. New insights into epididymal biology and function. Hum Reprod Update, 15:213-227.

Cornwall GA, 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- 4272.

D'Amours O, Frenette G, Bordeleau L-J, Allard N, Leclerc P, Blondin P, Sullivan R. 2012. Epididymosomes Transfer Epididymal Sperm Binding Protein 1 (ELSPBP1) to Dead Spermatozoa During Epididymal Transit in Bovine. Biol Reprod, 87:94, 91- 11.

Da Silva N, Barton CR. 2016. Macrophages and dendritic cells in the post-testicular environment. Cell Tissue Res, 363:97-104.

Da Silva N, Shum WW, Breton S. 2007a. Regulation of vacuolar proton pumping ATPase-dependent luminal acidification in the epididymis. Asian J Androl, 9:476- 482.

Da Silva N, Shum WW, El-Annan J, Paunescu TG, McKee M, Smith PJ, Brown D, Breton S. 2007b. Relocalization of the V-ATPase B2 subunit to the apical membrane of epididymal clear cells of mice deficient in the B1 subunit. American journal of physiology Cell physiology, 293:C199-210.

Dacheux JL, Belghazi M, Lanson Y, Dacheux F. 2006. Human epididymal secretome and proteome. Mol Cell Endocrinol, 250:36-42.

Dacheux JL, Belleannee C, Guyonnet B, Labas V, Teixeira-Gomes AP, Ecroyd H, Druart X, Gatti JL, Dacheux F. 2012. The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa. Syst Biol Reprod Med, 58:197-210.

Dacheux JL, Belleannee C, Jones R, Labas V, Belghazi M, Guyonnet B, Druart X, Gatti JL, Dacheux F. 2009. Mammalian epididymal proteome. Mol Cell Endocrinol, 306:45-50.

Dacheux JL, Castella S, Gatti JL, Dacheux F. 2005. Epididymal cell secretory activities and the role of proteins in boar sperm maturation. Theriogenology, 63:319-341.

Dacheux JL, Dacheux F. 2014. New insights into epididymal function in relation to sperm maturation. Reproduction, 147:R27-42.

Dacheux JL, Dacheux F, Paquignon M. 1989. Changes in sperm surface membrane and luminal protein fluid content during epididymal transit in the boar. Biol Reprod, 40:635-651.

Dacheux JL, Gatti JL, Dacheux F. 2003. Contribution of epididymal secretory proteins for spermatozoa maturation. Microsc Res Tech, 61:7-17.

Dacheux JL, Paquignon M. 1980. Relations between the fertilizing ability, motility and metabolism of epididymal spermatozoa. Reprod Nutr Dev, 20:1085- 1099.

Damm OS, Cooper TG. 2010. Maturation of sperm volume regulation in the rat epididymis. Asian J Androl, 12:578-590.

Danzo BJ, Cooper TG, Orgebin-Crist MC. 1977. Androgen binding protein (ABP) in fluids collected from the rete testis and cauda epididymidis of sexually mature and immature rabbits and observations on morphological changes in the epididymis following ligation of the ductuli efferentes. Biol Reprod, 17:64-77.

Domeniconi RF, Souza AC, Xu B, Washington AM, Hinton BT. 2016. Is the Epididymis a Series of Organs Placed Side By Side? Biol Reprod, 95:10.

Ecroyd H, Asquith KL, Jones RC, Aitken RJ. 2004. The development of signal transduction pathways during epididymal maturation is calcium dependent. Dev Biol, 268:53-63.

Eickhoff R, Baldauf C, Koyro HW, Wennemuth G, Suga Y, Seitz J, Henkel R, Meinhardt A. 2004. Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of proteinbound sulphydryl groups in rat sperm: indications for a new role of MIF in sperm maturation. Mol Hum Reprod, 10:605-611.

Eickhoff R, Jennemann G, Hoffbauer G, Schuring MP, Kaltner H, Sinowatz F, Gabius HJ, Seitz J. 2006. Immunohistochemical detection of macrophage migration inhibitory factor in fetal and adult bovine epididymis: release by the apocrine secretion mode? Cells Tissues Organs, 182:22-31.

Eickhoff R, Wilhelm B, Renneberg H, Wennemuth G, Bacher M, Linder D, Bucala R, Seitz J, Meinhardt A. 2001. 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, 7:27-35.

Ekhlasi-Hundrieser M, Schafer B, Philipp U, Kuiper H, Leeb T, Mehta M, Kirchhoff C, Topfer-Petersen E. 2007. Sperm-binding fibronectin type II-module proteins are genetically linked and functionally related. Gene, 392:253-265.

Esseltine JL, Scott JD. 2013. AKAP signaling complexes: pointing towards the next generation of therapeutic targets? Trends Pharmacol Sci, 34:648-655.

Ezer N, Robaire B. 2003. Gene expression is differentially regulated in the epididymis after orchidectomy. Endocrinology, 144:975-988.

Fan X, Robaire B. 1998. Orchidectomy induces a wave of apoptotic cell death in the epididymis. Endocrinology, 139:2128-2136.

Fawcett DW, Hoffer AP. 1979. Failure of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy. Biol Reprod, 20:162-181.

Fornes WM, Sosa MA, Bertini F, Burgos MH. 1995. Vesicles in rat epididymal fluid. Existence of two populations differing in ultrastructure and enzymatic composition. Andrologia, 27:233-237.

Fouchécourt S, Métayer S, Locatelli A, Dacheux F, Dacheux J-L. 2000. Stallion Epididymal Fluid Proteome: Qualitative and Quantitative Characterization; Secretion and Dynamic Changes of Major Proteins. Biol Reprod, 62:1790-1803.

Fouchecourt S, Metayer S, Locatelli A, Dacheux F, Dacheux JL. 2000. Stallion epididymal fluid proteome: qualitative and quantitative characterization; secretion and dynamic changes of major proteins. Biol Reprod, 62:1790-1803.

Fraile B, Martin R, De Miguel MP, Arenas MI, Bethencourt FR, Peinado F, Paniagua R, Santamaria L. 1996. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol Reprod, 55:291-297.

Frenette G, Lessard C, Madore E, Fortier MA, Sullivan R. 2003. Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol Reprod, 69:1586-1592.

Frenette G, Lessard C, Sullivan R. 2002. Selected proteins of "prostasome-like particles" from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod, 67:308-313.

Gatti JL, Castella S, Dacheux F, Ecroyd H, Metayer S, Thimon V, Dacheux JL. 2004. Post-testicular sperm environment and fertility. Anim Reprod Sci, 82-83:321- 339.

Gatti JL, Metayer S, Belghazi M, Dacheux F, Dacheux JL. 2005. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol Reprod, 72:1452-1465.

Girouard J, Frenette G, Sullivan R. 2011. Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int J Androl, 34:e475-486.

Guduric-Fuchs J, O'Connor A, Camp B, O'Neill CL, Medina RJ, Simpson DA. 2012. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics, 13:357.

Guyonnet B, Dacheux F, Dacheux JL, Gatti JL. 2011. The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J Androl, 32:651-664.

Hamzeh M, Robaire B. 2011. Androgens activate mitogen-activated protein kinase via epidermal growth factor receptor/insulin-like growth factor 1 receptor in the mouse PC-1 cell line. J Endocrinol, 209:55-64.

Hawkins SM, Buchold GM, Matzuk MM. 2011. Minireview: The roles of small RNA pathways in reproductive medicine. Mol Endocrinol, 25:1257-1279.

Heinlein CA, Chang C. 2002a. Androgen receptor (AR) coregulators: an overview. Endocr Rev, 23:175- 200.

Heinlein CA, Chang C. 2002b. The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Mol Endocrinol, 16:2181-2187.

Herak-Kramberger CM, Breton S, Brown D, Kraus O, Sabolic I. 2001. Distribution of the vacuolar H+ atpase along the rat and human male reproductive tract. Biol Reprod, 64:1699-1707.

Hermo L, Jacks D. 2002. Nature's ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev, 63:394-410.

Hermo L, Xiaohong S, Morales CR. 2000. Circulating and luminal testicular factors affect LRP-2 and Apo J expression in the epididymis following efferent duct ligation. J Androl, 21:122-144.

Hess RA. 2002. The Efferent Ductules: Structure and Functions. In: Robaire B, Hinton BT (Eds.). The Epididymis: from Molecules to Clinical Practice. New York: Kluwer Academic/Plenum Publishers. pp.49-80.

Hess RA, Bunick D, Bahr J. 2001a. Oestrogen, its receptors and function in the male reproductive tract - a review. Mol Cell Endocrinol, 178:29-38.

Hess RA, Bunick D, Bahr JM. 1995. Sperm, a source of estrogen. Environ Health Perspect, 103(Suppl 7):59- 62.

Hess RA, Zhou Q, Nie R, Oliveira C, Cho H, Nakaia M, Carnes K. 2001b. Estrogens and epididymal function. Reprod Fertil Dev, 13:273-283.

Hinton BT, Galdamez MM, Sutherland A, Bomgardner D, Xu B, Abdel-Fattah R, Yang L. 2011. How do you get six meters of epididymis inside a human scrotum? J Androl, 32:558-564.

Hinton BT, Lan ZJ, Rudolph DB, Labus JC, Lye RJ. 1998. Testicular regulation of epididymal gene expression. J Reprod Fertil Suppl, 53:47-57.

Holland MK, Vreeburg JT, Orgebin-Crist MC. 1992. Testicular regulation of epididymal protein secretion. J Androl, 13:266-273.

Hoskins DD, Stephens DT, Hall ML. 1974. Cyclic adenosine 3':5'-monophosphate and protein kinase levels in developing bovine spermatozoa. J Reprod Fertil, 37:131-133.

Inskeep PB, Hammerstedt RH. 1982. Changes in metabolism of ram sperm associated with epididymal transit or induced by exogenous carnitine. Biol Reprod, 27:735-743.

Janne OA, Moilanen AM, Poukka H, Rouleau N, Karvonen U, Kotaja N, Hakli M, Palvimo JJ. 2000. Androgen-receptor-interacting nuclear proteins. Biochem Soc Trans, 28:401-405.

Jones RC, Dacheux JL, Nixon B, Ecroyd HW. 2007. Role of the epididymis in sperm competition. Asian J Androl, 9:493-499.

Joseph A, Shur BD, Hess RA. 2011. Estrogen, efferent ductules, and the epididymis. Biol Reprod, 84:207-217.

Kempinas WG, Klinefelter GR. 2014. Interpreting histopathology in the epididymis. Spermatogenesis, 4:e979114.

Kirchhoff C, Osterhoff C, Young L. 1996. Molecular cloning and characterization of HE1, a major secretory protein of the human epididymis. Biol Reprod, 54:847- 856.

Krege JH, John SW, Langenbach LL, Hodgin JB, Hagaman JR, Bachman ES, Jennette JC, O'Brien DA, Smithies O. 1995. Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature, 375:146-148.

Lan ZJ, Labus JC, Hinton BT. 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 Reprod, 58:197-206.

Legare C, Gaudreault C, St-Jacques S, Sullivan R. 1999. P34H sperm protein is preferentially expressed by the human corpus epididymidis. Endocrinology, 140:3318-3327.

Lindemann CB, Gardner TK, Westbrook E, Kanous KS. 1991. The calcium-induced curvature reversal of rat sperm is potentiated by cAMP and inhibited by anticalmodulin. Cell Motil Cytoskeleton, 20:316-324.

Manjunath P, Bergeron A, Lefebvre J, Fan J. 2007. Seminal plasma proteins: functions and interaction with protective agents during semen preservation. Society of Reproduction and Fertility Supplement, 65:217-228.

Manjunath P, Thérien I. 2002. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation J Reprod Immunol, 53:109-119

Mittelbrunn M, Gutierrez-Vazquez C, VillarroyaBeltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. 2011. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nature communications, 2:282.

Moura AA, Souza CE, Stanley BA, Chapman DA, Killian GJ. 2010. Proteomics of cauda epididymal fluid from mature Holstein bulls. Journal of proteomics, 73:2006-2020.

Nicander L, Osman DI, Ploen L, Bugge HP, Kvisgaard KN. 1983. Early effects of efferent ductule ligation on the proximal segment of the rat epididymis. Int J Androl, 6:91-102.

Nixon B, Ecroyd HW, Dacheux JL, Jones RC. 2011. Monotremes provide a key to understanding the evolutionary significance of epididymal sperm maturation. J Androl, 32:665-671.

Palladino MA, Hinton BT. 1994a. Developmental regulation of expression of multiple gamma-glutamyl transpeptidase mRNAs in the postnatal rat epididymis. Biochem Biophys Res Commun, 198:554-559.

Palladino MA, Hinton BT. 1994b. 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, 135:1146-1156.

Papaioannou MD, Nef S. 2010. microRNAs in the testis: building up male fertility. J Androl, 31:26-33.

Pariset CC, Feinberg JM, Dacheux JL, Weinman SJ. 1985. Changes in calmodulin level and cAMPdependent protein kinase activity during epididymal maturation of ram spermatozoa. J Reprod Fertil, 74:105-112.

Pastor-Soler N, Beaulieu V, Litvin TN, Da Silva N, Chen Y, Brown D, Buck J, Levin LR, Breton S. 2003. Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem, 278:49523-49529.

Pastor-Soler NM, Hallows KR, Smolak C, Gong F, Brown D, Breton S. 2008. Alkaline pH- and cAMP- induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. American journal of physiology Cell physiology, 294:C488-494.

Payan-Carreira R, Borges P, Mir F, Fontbonne A.2013. Molecular Markers in Sperm Analysis. In: Lemma A (Eds.). Success in Artificial Insemination - Quality of Semen and Diagnostics Employed: InTech.

Perino A, Ghigo A, Scott JD, Hirsch E. 2012. Anchoring proteins as regulators of signaling pathways. Circ Res, 111:482-492.

Rejraji H, Sion B, Prensier G, Carreras M, Motta C, Frenoux JM, Vericel E, Grizard G, Vernet P, Drevet JR. 2006. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod,74:1104-1113.

Rejraji H, Vernet P, Drevet JR. 2002. GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Mol Reprod Dev, 63:96-103.

Rigaudiere N, Ghyselinck NB, Faure J, Dufaure JP. 1992. Regulation of the epididymal glutathione peroxidase-like protein in the mouse: dependence upon androgens and testicular factors. Mol Cell Endocrinol, 89:67-77.

Robaire B, Hamzeh M. 2011. Androgen action in the epididymis. J Androl, 32:592-599.

Robaire B, Hinton BT, Orgebin-Crist M-C, Jimmy DN, Ph.D, Tony MP, Ph.D, Donald WP, Ph.D, John RGC, D.Sc, F.R.S.C, David MdK, M.D, A.O, JoAnne SR, Ph.D, Paul MW, Ph.D.2006. The EpididymisKnobil and Neill's Physiology of Reproduction (Third Edition). St Louis: Academic Press. pp.1071-1148.

Saez F, Ouvrier A, Drevet JR. 2011. Epididymis cholesterol homeostasis and sperm fertilizing ability. Asian J Androl, 13:11-17.

Schorr-Lenz AM, Alves J, Henckes NA, Seibel PM, Benham AM, Bustamante-Filho IC. 2016. GnRH immunization alters the expression and distribution of protein disulfide isomerases in the epididymis. Andrology, 4(5):957-963.

Schwarz A, Wennemuth G, Post H, Brandenburger T, Aumuller G, Wilhelm B. 2013. Vesicular transfer of membrane components to bovine epididymal spermatozoa. Cell Tissue Res, 353:549-561.

Shum WW, Da Silva N, McKee M, Smith PJ, Brown D, Breton S. 2008. Transepithelial projections from basal cells are luminal sensors in pseudostratified epithelia. Cell, 135:1108-1117.

Shum WW, Ruan YC, Da Silva N, Breton S. 2011. Establishment of cell-cell cross talk in the epididymis: control of luminal acidification. J Androl, 32:576-586.

Shum WW, Smith TB, Cortez-Retamozo V, Grigoryeva LS, Roy JW, Hill E, Pittet MJ, Breton S, Da Silva N. 2014. Epithelial basal cells are distinct from dendritic cells and macrophages in the mouse epididymis. Biol Reprod, 90:90.

Sostaric E, Aalberts M, Gadella BM, Stout TA. 2008. The roles of the epididymis and prostasomes in the attainment of fertilizing capacity by stallion sperm. Anim Reprod Sci, 107:237-248.

Souza CE, Rego JP, Lobo CH, Oliveira JT, Nogueira FC, Domont GB, Fioramonte M, Gozzo FC, Moreno FB, Monteiro-Moreira AC, Figueiredo JR, Moura AA. 2012. Proteomic analysis of the reproductive tract fluids from tropically-adapted Santa Ines rams. Journal of proteomics, 75:4436-4456.

Sullivan R, Frenette G, Girouard J. 2007. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl, 9:483-491.

Sullivan R, Saez F. 2013. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction, 146:R21- 35.

Sullivan R, Saez F, Girouard J, Frenette G. 2005. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis, 35:1-10.

Sutovsky P. 2015. New Approaches to Boar Semen Evaluation, Processing and Improvement. Reprod Domest Anim, 50(Suppl.2):11-19.

Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G. 2001. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci, 114:1665-1675.

Syntin P, Dacheux F, Druart X, Gatti JL, Okamura N, Dacheux JL. 1996. Characterization and identification of proteins secreted in the various regions of the adult boar epididymis. Biol Reprod, 55:956-974.

Syntin P, Dacheux J-L, Dacheux F. 1999. Postnatal Development and Regulation of Proteins Secreted in the Boar Epididymis. Biol Reprod, 61:1622-1635.

Thimon V, Calvo E, Koukoui O, Legare C, Sullivan R. 2008a. Effects of vasectomy on gene expression profiling along the human epididymis. Biol Reprod, 79:262-273.

Thimon V, Frenette G, Saez F, Thabet M, Sullivan R. 2008b. Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum Reprod, 23:1698-1707.

Turner RM. 2006. Moving to the beat: a review of mammalian sperm motility regulation. Reprod Fertil Dev, 18:25-38.

Turner TT, Bomgardner D, Jacobs JP, Nguyen QA. 2003. Association of segmentation of the epididymal interstitium with segmented tubule function in rats and mice. Reproduction, 125:871-878.

Turner TT, Johnston DS, Finger JN, Jelinsky SA. 2007a. Differential gene expression among the proximal segments of the rat epididymis is lost after efferent duct ligation. Biol Reprod, 77:165-171.

Turner TT, Johnston DS, Jelinsky SA, Tomsig JL, Finger JN. 2007b. Segment boundaries of the adult rat epididymis limit interstitial signaling by potential paracrine factors and segments lose differential gene expression after efferent duct ligation. Asian J Androl, 9:565-573.

Veeramachaneni DN, Amann RP. 1991. Endocytosis of androgen-binding protein, clusterin, and transferrin in the efferent ducts and epididymis of the ram. J Androl, 12:288-294.

Vernet P, Faure J, Dufaure JP, Drevet JR. 1997. Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPX5, a murine epididymis-specific glutathione peroxidase. Mol Reprod Dev, 47:87-98.

Vidarsson H, Westergren R, Heglind M, Blomqvist SR, Breton S, Enerback S. 2009. The forkhead transcription factor Foxi1 is a master regulator of vacuolar H-ATPase proton pump subunits in the inner ear, kidney and epididymis. PloS one, 4:e4471.

Viger RS, Robaire B. 1996. The mRNAs for the steroid 5 alpha-reductase isozymes, types 1 and 2, are differentially regulated in the rat epididymis. J Androl, 17:27-34.

Voglmayr JK, Sawyer RF, Jr., Dacheux JL. 1985. Glycoproteins: a variable factor in surface transformation of ram spermatozoa during epididymal transit. Biol Reprod, 33:165-176.

Wang G, Guo Y, Zhou T, Shi X, Yu J, Yang Y, et al. 2013. In-depth proteomic analysis of the human sperm reveals complex protein compositions. Journal of proteomics, 79:114-122.

Xia J, Reigada D, Mitchell CH, Ren D. 2007. CATSPER channel-mediated Ca2+ entry into mouse sperm triggers a tail-to-head propagation. Biol Reprod, 77:551-559.

Yeung CH, Breton S, Setiawan I, Xu Y, Lang F, jCooper TG. 2004. Increased luminal pH in the epididymis of infertile c-ros knockout mice and the expression of sodium-hydrogen exchangers and vacuolar proton pump H+-ATPase. Mol Reprod Dev, 68:159-168.

5b7335230e8825113d8068a8 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections