Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals

Department of Biological Sciences, University of Newcastle, NSW, Australia.
Reproduction Fertility and Development (Impact Factor: 2.4). 02/1996; 8(4):553-68. DOI: 10.1071/RD9960553
Source: PubMed


The present review examines the mechanisms involved in sperm storage in the epididymis of therian mammals in terms of the supply of energy substrate and the regulation of motility and metabolism. Lipids, glucose, lactate and glycerol are possible metabolic substrates for sperm in the epididymis, but the role of these is uncertain and it may differ between marsupials and eutherians. Sperm are normally immotile in the epididymis, but ram and rabbit sperm may have an uncoordinated motility. Sperm metabolism is suppressed but is probably not strongly coupled to motility. Work on diluted sperm indicates that cyclic adenosine monophosphate, Ca2+, and pH play roles as intracellular messengers controlling the motility and metabolism of sperm, but no first messenger has been identified. A number of mechanisms of suppressing sperm motility and metabolism in the epididymis are considered, including a collective autoregulation, oxygen tension, osmotic pressure, viscosity and the extracellular concentration of H+, Ca2+, Na+, HCO3- and carnitine. However, there is no conclusive evidence for any of the mechanisms and there is clearly some variation between species in the mechanism of suppressing sperm activity. Sperm activation stimulates motility and a 4-5-fold increase in respiration rate that has not been reversed without compromising viability. Following activation, respiration supported by endogenous and/or exogenous substrates is much higher in marsupial than eutherian sperm, and marsupial sperm do not show a large stimulation of respiration on the addition of exogenous substrate, as is characteristic of most eutherian sperm.


Available from: Russell C Jones
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    • "It has been known for more than sixty years that the luminal fluid of the female reproductive tract has a HCO 3 À content two to four times higher than that of the plasma (Vishwakarma, 1962; Murdoch and White, 1968; Maas et al., 1977). It is also known that HCO 3 À is essential to a number of reproductive events occurring in the female reproductive tract (Chan et al., 2006, 2009, 2012; Liu et al., 2012), including sperm motility (Mann and Lutwak-Mann, 1982; Tajima et al., 1987; Jones and Murdoch, 1996; Abaigar et al., 1999; Holt and Harrison, 2002; Wennemuth et al., 2003; Wennemuth, 2004; Mannowetz et al., 2011), capacitation (Boatman and Robbins, 1991; Shi and Roldan, 1995; Zhou et al., 2005), a sperm activation process by which sperm acquire their ability to fertilise the egg, and early embryo development (Chen et al., 2010; Lu et al., 2012). The questions as to how HCO 3 À is secreted into the lumen of the female reproductive tract and how HCO 3 À is transported into sperm and embryo have not been fully addressed. "
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    ABSTRACT: The solute carrier 26 (SLC26) family emerges as a distinct class of anion transporters with its members SLC26A3 (Slc26a3) and SLC26A6 (Slc26a6) reported to be electrogenic Cl(-) /HCO3 (-) exchangers. While it is known that uterine fluid has high HCO3 (-) content and that HCO3 (-) is essential for sperm capacitation, the molecular mechanisms underlying the transport of HCO3 (-) across uterine epithelial cells and sperm have not been fully investigated. The present review re-examines the results from early reports studying anion transport, finding clues for the involvement of Cl(-) /HCO3 (-) anion exchanges in electrogenic HCO3 (-) transport across endometrial epithelium. We also summarize recent work on Slc26a3 and Slc26a6 in uterine epithelial cells and sperm, revealing their functional role in working closely with the cystic fibrosis transmembrane conductance regulator (CFTR) for HCO3 (-) transport in these cells. The possible involvement of these anion exchangers in other HCO3 (-) dependent reproductive processes and their implications for infertility are also discussed.
    Cell Biology International 01/2014; 38(1). DOI:10.1002/cbin.10183 · 1.93 Impact Factor
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    • "Although it is well established that mammalian sperm must undergo maturation in the epididymis to gain the potential to fertilize an ovum (Bedford 1967, Orgebin-Crist 1967, Sonnenberg-Riethmacher et al. 1996), and then spend time in the female tract in order to capacitate before they can actually fertilize an ovum (Austin 1951, Chang 1951), the need for extra-testicular sperm maturation in birds is contentious. In mammals, sperm maturation involves structural modifications, changes in the lipid and protein composition of the plasmalemma (Jones 1989, 1998), and development of a characteristic pattern of motility (Morton et al. 1978, Jones & Murdoch 1996). "
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    ABSTRACT: The role of the avian epididymis in post-testicular development and capacitation was examined in order to assess whether avian spermatozoa undergo any processes similar to those characteristic of mammalian sperm development. We found no evidence of a need for quail sperm to undergo capacitation and 90% of testicular sperm could bind to a perivitelline membrane and acrosome react. However, CASA analysis showed that only 20% of testicular sperm from the quail were capable of movement and only about 12% of the motile sperm would have a curvilinear velocity greater than the mean for sperm from the distal epididymis. Nevertheless, epididymal transit was associated with mean increases in sperm velocity and the proportion of motile sperm. Together these findings explain why earlier workers have achieved some fertilizations following inseminations of testicular spermatozoa, but also demonstrate the need for some epididymal maturation of avian spermatozoa. Analysis of the electrophoretic profile of quail epididymal luminal proteins revealed that only one major protein (~16 kDa) is secreted by the epididymis and it was virtually the only protein secreted by the ipsilateral epididymis following unilateral orchidectomy. Mass spectrometry showed that this protein is hemoglobin; this finding was confirmed using anti-hemoglobin antibodies. It is suggested that hemoglobin may support sperm metabolism in the quail epididymis, aid in motility, and/or serve as an antioxidant.
    Reproduction 12/2013; 147(3). DOI:10.1530/REP-13-0566 · 3.17 Impact Factor
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    • "In addition, the extracellur pH decreases through the epididymal tract and the acidification of the tract is caused by H+ pumped into the epididymis tract via H+-ATPase distributed at the apical membrane of epididymal clear cells [10]. Moreover, the concentration of HCO3− in epididymal tract is far lower than that in blood [25]. Morphological evidences show that the epididymis epithelium express various bicarbonate transporters, such as NBC [19] and anion exchanger(AE) [26], indicating that the epididymal epithelium obtains a powerful capability of HCO3− reabsorption, but the function of HCO3− transportation is still unknown. "
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    ABSTRACT: Background The epithelium lining the epididymis provides an optimal acidic fluid microenvironment in the epididymal tract that enable spermatozoa to complete the maturation process. The present study aims to investigate the functional role of Na+/HCO3− cotransporter in the pH regulation in rat epididymis. Method/Principal Findings Immunofluorescence staining of pan cytokeratin in the primary culture of rat caput epididymal epithelium showed that the system was a suitable model for investigating the function of epididymal epithelium. Intracellular and apical pH were measured using the fluorescent pH sensitive probe carboxy-seminaphthorhodafluor-4F acetoxymethyl ester (SNARF-4F) and sparklet pH electrode respectively to explore the functional role of rat epididymal epithelium. In the HEPES buffered Krebs-Henseleit(KH) solution, the intracellular pH (pHi) recovery from NH4Cl induced acidification in the cultured caput epididymal epithelium was completely inhibited by amiloride, the inhibitor of Na+/H+ exchanger (NHE). Immediately changing of the KH solution from HEPES buffered to HCO3− buffered would cause another pHi recovery. The pHi recovery in HCO3− buffered KH solution was inhibited by 4, 4diisothiocyanatostilbene-2, 2-disulfonic acid (DIDS), the inhibitor of HCO3− transporter or by removal of extracellular Na+. The extracellular pH measurement showed that the apical pH would increase when adding DIDS to the apical side of epididymal epithelial monolayer, however adding DIDS to the basolateral side had no effect on apical pH. Conclusions The present study shows that sodium coupled bicarbonate influx regulates intracellular and apical pH in cultured caput epididymal epithelium.
    PLoS ONE 08/2011; 6(8):e22283. DOI:10.1371/journal.pone.0022283 · 3.23 Impact Factor
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