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Spermiation and sperm maturation in the marmoset.

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THE ANATOMICAL RECORD 229:315-320 (1991)
Spermiation and Sperm Maturation
in the Marmoset
R. ASOK KUMAR AND DAVID M. PHILLIPS
The Population Council, New York,New York 10021
ABSTRACT
The scanning and transmission electron microscopes were used to
examine the processes of spermiation and sperm maturation in the marmoset. We
observe that the heads of late spermatids are embedded in the apical aspect of the
large sleeve-like columnar portion of Sertoli cells. As spermiogenesis progresses,
spermatids become associated with numerous small apical Sertoli cell extensions.
These finger-like processes undergo a sequence of changes during spermiation.
Spermatozoa from the caput, corpus, and cauda epididymides were examined. In
caput epididymis of marmoset, the apical segment of the spermatozoa extends well
beyond the rostra1 edge of the nucleus and folds back on itself. In sagittal sections,
the acrosome exhibits a distinct hook shape. In the corpus, the distinctive hookshaped apical segment of the acrosome is observed in some spermatozoa, but the
apical extension is significantly smaller or projects out only slightly beyond the
nucleus. In cauda epididymis, the extension is absent. A similar acrosomal hook
has been reported in the pigtailed monkey, which is a n Old World species. We
suggest that changes in acrosome structure during sperm maturation may be
fairly widespread among primates.
The release of the sperm from the seminiferous tubule epithelium is termed spermiation. During this
process, Sertoli cells undergo a series of morphological
transformations. Although spermiation has been studied in several mammalian species (Fawcett and Phillips, 1969; Sapsford and Rae, 1968; Fawcett, 1975; Morales and Clermont, 1982; Wong and Russell, 1983;
Weber et al., 1983; Vogl et al., 1985), the release of
spermatozoa has not been examined in monkeys. We
describe here the processes of spermiation in marmosets (Callithrixjacchus).
The spermatozoa released from the seminiferous epithelium are functionally immature and have not yet
developed the capacity to fertilize. They undergo structural, biochemical, and functional changes during
epididymal transit (for reviews, see Bedford, 1975;
Orgebin-Crist, 1981). Fawcett and Hollenberg (1963)
observed remarkable change in the morphology of the
guinea pig acrosome during epididymal transit. Since
then, morphological changes have been reported in
other eutherian mammals, including rabbit (Bedford,
1963, 1965), chinchilla (Fawcett and Phillips, 19691,
monkey (Bedford and Nicander, 1971), elephant (Jones
et al., 1974), musk shrew (Cooper and Bedford, 19761,
hyrax and armadillo (Bedford and Millard, 1978), hamster (de Rosas and Burgos, 1987), and loris (Phillips
and Bedford, 1987). We describe here marked structural changes in the common marmoset, C .jacchus, a
New World monkey, which have not been previously
noted.
pH 7.2. For scanning electron microscopy (SEM), the
fixed tissue was cut into small pieces. The tissue was
postfixed in 1% osmium tetroxide buffered with 0.1 M
cacodylate buffer, dehydrated in a graded series of acetone infiltrated in Freon, and critical-point dried from
liquid CO,. The dried specimens were coated with gold
in a n Edwards 150 sputtercoater and examined with a n
ETEC Autoscan.
For transmission electron microscopy (TEM), testes
and epididymides were carefully cut into small pieces,
postfixed in 1% OsO,, and dehydrated in alcohol followed by propylene oxide. Tissues were embedded in
Epon. Sections were cut with a diamond knife on a
Reichart OmU2 microtome, stained with 3% aqueous
uranyl acetate (no lead staining was used), and examined in a Philips 300 electron microscope.
OBSERVATIONS
Sperrniation
Viewed with SEM, heads of the maturation phase
spermatids were observed to be embedded in Sertoli
cells. Some Sertoli cells displayed funnel-shaped,
sleeve-like processes. Some spermatids had presumably fallen out of these Sertoli cells during processing
(Fig. 1). We also observed finger-like extensions of the
Sertoli cells associated with late spermatids. These finger-like protuberances of the apical region of the Sertoli cells assumed different shapes and sizes (Figs. 2,3).
MATERIALS AND METHODS
Testes and epididymides of adult marmosets (C.jacchus) were fixed by perfusion in 1% glutaraldehyde, 4%
paraformaldehyde in 0.1 M sodium cacodylate buffer a t
0 1991 WILEY-LISS. INC.
Received May 29, 1990; accepted July 31, 1990.
Address reprint requests to Dr. David M. Phillips, The Population
Council, 1230 York Avenue, New York, NY 10021.
316
R. ASOK KUMAR AND D.M. PHILLIPS
Fig. 1. SEM showing the cellular association of Sertoli cells and
spermatids. Arrows indicate the sleeve-like processes of the Sertoli
cells. Spermatids presumably fell out of the sleeves during processing.
x 2,000.
Fig. 2. During spermiogenesis, the sleeve-like processes (arrows) of
Sertoli cells are in close association with spermatids. Tubular cytoplasmic specialization of the Sertoli cells (arrowhead) are observed
among the developing spermatids. x 3,300.
317
MARMOSET SPERM
Fig. 3. SEM showing Sertoli cell-spermatid association a t spermiation. Several luminal cytoplasmic
protuberances of the Sertoli cells are associated with the spermatozoa. x 6,000.
Sperm Maturation Events
The SEM revealed the caudal migration of the cytoplasmic droplet along the midpiece during epididymal
transit. Spermatozoa lying in the caput epididymis
were usually bent at their midpiece region (Fig. 4).The
bent portion of the spermatozoa was often enveloped by
the protoplasmic droplet. Spermatozoa from the corpus
epididymis were generally slightly bent at the annulus, where the protoplasmic droplet was observed (Fig.
6). In the cauda epididymis, spermatozoa were straight
and protoplasmic droplets were generally not observed
(Fig. 8). Maturational changes were not visible in the
sperm head with SEM.
With TEM, we observed maturational changes in the
sperm head that were not revealed by the SEM. In the
caput epididymis, the heads of spermatozoa were asymmetric because the apical segment of the acrosome was
extended well beyond the rostra1 edge of the nucleus
and folded under it. In sagittal sections, the acrosome
exhibited a distinct hook-shaped apical segment (Fig.
5). The occurrence of a hook-shaped apical segment of
the acroSome was evident in
the 'Perm cut sagittally.
In the 'OrPUS, the distinctive
hook-shaPed
segment of the acrOSOme was observed in Some sPermatobut not in Others.
the protuberance was
smaller than that observed in spermatozoa of the caput
epididymis (Fig. 7). In the cauda epididymis, no hooksegment Of the acrosome was Observed
(Fig. 9).
DISCUSSION
We have shown that late spermatids of the marmoset
are embedded in sleeve-like processes of Sertoli cells.
318
R. ASOK KUMAR AND D.M. PHILLIPS
Fig. 4. SEM of the spermatozoa in the caput epididymis. The bent
portion of the neck region is enveloped by a cytoplasmic droplet (D).
x 4,600.
Fig. 5. Sagittal section of the heads of two spermatozoa from the
caput epididymis. The acrosome elongates and bends back towards
the nucleus. x 11,000.
Fig. 6. SEM showing the spermatozoa in the corpus epididymis. The
cytoplasmic droplet is situated in the anterior of the midpiece region
of some spermatozoa and in the posterior of the midpiece in others.
x 4,600.
Fig. 7. Sagittal section of the head of two spermatozoa from corpus
epididymis. The rostra1 elongation is observed in only one of the two
spermatozoa. x 11,000.
MARMOSET SPERM
319
Fig. 8. SEM of the spermatozoa in the cauda epididymis. Most of the spermatozoa have straight tails.
The cytoplasmic droplet (D) has been moved to the annulus. x 4,600.
Fig. 9. TEM of spermatozoa in the cauda epididymis. x 11,000.
We have also observed that the apical end of the Sertoli World monkeys. In fact, a similar phenomenon has
cell forms numerous short processes of various shapes, been described in pigtailed monkey (Hoffer et al.,
which closely associate with the spermatids. These ob- 1981), an Old World species. Thus, although the priservations are basically similar to those of other inves- mate acrosome is not considered to undergo acrosomal
tigators working with a variety of mammalian species morphogenesis as occurs in certain other mammals,
(Fawcett and Phillips, 1969; Fawcett, 1975, 1979; Fou- further ultrastructural studies may reveal that matuquet, 1972, 1974; Phillips, 1980; Russell, 1984; Gravis, rational changes in the acrosome are more common in
1978; Sakai et al., 1988; Vogl et al., 1983,1985;Dietert, primates than was previously believed.
1966; Nicander, 1967; Sapsford and Rae, 1969; Morales
ACKNOWLEDGMENTS
and Clermont, 1982).
Although the relationship between Sertoli cells and
This research was supported in part by a research
late spermatids is similar among different species of training grant from WHO to R.A.K.
eutherian mammals, there have been various interpreLITERATURE CITED
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