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Sperm
quiescence in cauda epididymis: a mini-review
Ramtej
Jayram Verma
Department
of Zoology, University
School of Sciences, Gujarat University,
Ahmedabad-380 009, INDIA
Asian J Androl 2001 Sep; 3: 181-183
Keywords:
sperm
quiescence; sperm motility; epididymis
Abstract
The concentration of sodium chloride is of prime importance in the initiation and reversal of sperm quiescence in the cauda epididymis. Other factors such as inorganic and organic constituents of the luminal fluid are of secondary importance and might assist in inducing sperm quiescence.1 Introduction
The
mammalian testicular spermatozoa present in the seminiferous tubules of
testis are either immotile or display very restricted vibratory motions;
theyare non-viable with no fertilizing capacity. As the spermatozoa traverse
through the tubules
of the epididymis, they attain progressive motility and fertilizing ability[1-4].
The
mammalian epididymis is an elongated coiled duct suspended within the
mesorchium and is firmly or loosely bound to the tunica albuginea. The
epididymal tubular lumen is continuous with the lumina of vasa efferentes
in the testis and ends in the vas deferens. The gross division of epididymis
comprises of the caput, corpus and cauda epididymis.
The
epididymal luminal epithelium consists of the principal, the pale or clear
cells and the basal cells[5,6]. Ultrastructural studies on
cauda epididymis revealed occurrence of two separate and functionally
distinct compartments which are sealed off from the epididymal lumen by
occluding tight junctions joining the
adluminal ends of epithelial cells. These junctional complexes form the
blood-epididymal barrier[7]. The epididymal tubular epithelium
is surrounded by smooth musculature along its whole length, which helps
in sperm transport.
The
principal cells secrete products of Golgi origin into each of the epididymal
compartments. The principal cells also absorb substances from the luminal and
intraepithelial compartments. The pale cells or clear cells are known
to be the source of
glycerylphosphoryl-choline. The basal cells absorb substances and possibly
provide mechanical function of lending stability to the epithelium by
virtue of possessing tonofilaments[6,8,9]. The secretory and
reabsorptive function of the epididymal epithelium provides the congenial
microenvironment for proper sperm maturation.
Once
fully mature, spermatozoa then could be stored in the terminal region of
the cauda epididymis for a long period of time, till ejaculation occurs.
Although, cauda epididymal spermatozoa have the capacity of progressive
motility, but they are immotile while suspended in the native fluid. This
physiological phenomenon is known as sperm quiescence, the exact mechanism
of which is not clearly understood.
Speculations
on the physiological mechanisms inducing sperm quiescence in cauda epididymis
are hotly debated. Studies are mainly done in two directions:
(1)
Analyzing the microenvironment of cauda epididymis, and
(2)
Studying the influence exerted by different organic and inorganic
constituents of the microenvironment on sperm motility.
2 Analyzing the microenvironment of cauda epididymis
Spermatozoa
as well as their surrounding fluid microenvironment initially elaborated
by the seminiferous tubules undergo numerous changes during their passage
through the entire length of the epididymal tubules. The following changes
were observed when samples collected from different sections of the duct
were analyzed:
(1)
The sperm density increases as the testicular fluid passes through the
epididymis, which is attributable to water reabsorption by the epididymal
tubular epithelium[4].
(2) While passage
through the epididymal tubules, a decline in the sodium and a rise in
the potassium ion concentrations occurred in the luminal fluid[10].
(3) The pH
optima of the epididymal millieu shifted from the acidic range at the
caput to the alkaline at the cauda[11].
(4) Osmolality of
the epididymal fluid increases from the caput to the cauda
epididymis[12].
(5) The epididymal
plasma contains high concentrations of glycerylphosphoryl-choline (GPC)[5],
total lipid, phospholipids[13], sialic acid and total protein[7,12,14].
(6) In rats,
the concentration of carnitine in the epididymis is 500 fold higher than
that in the blood plasma[7,12].
(7) Utilizable
substrates such as glucose and fructose are almost absent
in the cauda epididymal luminal fluid[14].
3 Influence exerted by different organic and inorganic constituents of microenvironment on sperm motility in vitro
3.1
Organic constituents and sperm motility
Hamilton
and Olson[15] observed a reduction in the uptake of oxygen
when bovine ejaculated spermatozoa were incubated with higher concentrations
of carnitine, suggesting that the occurrence of sperm quiescence in cauda
epididymis might be due to a high concentration of carnitine present in
cauda epididymis.
Later
studies of Turner and Giles[16] indicated that there was no
initiation of sperm motility when the quiescence state spermatozoa collected
from caudaepididymis of rat were incubated with high concentrations of
carnitine and GPC. The sperm motility was inhibited when motile spermatozoa
were incubated with high concentrations of carnitine and GPC. Thus increased
carnitine and GPC concentrations in the microenvironment of cauda epididymis
could not be possible factors for the initiation of sperm motility, but
may help in maintaining spermatozoa in the quiescence state.
3.2 Ionic constituents and sperm motility
Vigorous
motility was initiated when sperm samples from cauda epididymis were diluted
with any ionic solutions in which the pH and osmolality were reasonably
close to the physiological conditions[12]. Morton and his colleagues[17,18]
have observed that spermatozoa collected from the cauda epididymis of
hamsters were immotile when present in the native fluid. Initiation of
sperm motility did not occur when samples were diluted with calcium free
medium. Upon the addition of calcium into the diluting medium, spermatozoa
immediately became motile. It is thus suggested that the calcium ions
are involved in the initiation of mammalian sperm motility.
Our
studies with the micropuncture samples obtained from the cauda epididymis
of rat indicated that sperm motility could be initiated in a calcium-free
medium[19]. The influence of various cations on cauda epididymal
sperm motility in vitro was
studied in a time-dependent fashion. Results revealed that sodium chloride
(NaCl) was essential for sperm motility, since sperm motility was completely
absent with the addition of a NaCl-free Krebs ringer bicarbonate (KRB)
buffer(pH 7.4) or a low-NaCl medium to the sperm samples. Sperm motility
was only detectable
upon the addition of 100 mmol/L NaCl and was augmented to the maximum
level with the addition of 150 mmol/L NaCl in KRB buffer. Sperm motility
was low, yet still present if KCl and/or CaCl2 were excluded
from the buffer, indicating their secondary importance. The maximum sperm
motility was obtained when 150 mmol/L NaCl was
mixed with 50 mmol/L KCl and 10 mmol/L CaCl2 in the KRB buffer[19,20].
The
micropuncture samples obtained from different sections of epididymis were
analysed for cationic concentration by Turner et al[21]
and Jenkins et al[22]. The results indicate that the
Na+ concentration decreased in succession from the
seminiferous tubules (135.44 mmol/L) to the caput epididymis (104.02 mmol/L)
and the distal cauda epididymis (37.17 mmol/L), whereas the K+
concentration was higher in the seminiferous tubules (39.77 mmol/L) and
the distal cauda epididymis (39.98
mmol/L), and lower in the caput epididymis (20.53 mmol/L). Chloride concentration
remained stable (27.04 mmol/L) throughout the epididymis.
Microperfusion
studies of Wong et al[10] have indicated that the
caput, the corpus and the cauda epididymis absorb Na+, Cl-
and water, and secrete K+. The rate
of these transport processes has been found to vary with the regions of
the duct. The caudaepididymis has the highest rate of Na+ and
water reabsorption and K+ secretion. Approximately 76.1 % of
the luminal fluid sodium was lost from the caput to the cauda epididymis[10].
Thus
the mature spermatozoa after attaining progressive motility and fertilizing
ability in the corpus and proximal cauda epididymis encounter a drastic
change in ionic concentrations in the distal cauda epididymis and they
remain in the quiescence state.
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Correspondence
to:
Dr.
R.J.Verma, Department of Zoology,
University School of Sciences,
Gujarat University, Ahmedabad-380 009, INDIA
E-mail: zooldeptgu@satyam.net.in
Received 2001-08-20 Accepted 2001-08-29
