Introduction
Spermatogenesis is a complex, highly organized process
that originates from stem cell spermatogonia. In non-
primate mammals, the A
s
(A single) spermatogonia are
considered to be the stem cells of spermatogenesis
(Huckins, 1971; Oakberg, 1971; de Rooij, 1973). Upon
division of the A
s
spermatogonia, the daughter cells either
migrate away from each other and become two new stem
cells, or stay together through an intercellular bridge
and become A-paired (A
pr
) spermatogonia. The A
pr
sper-
matogonia develop further into chains of four, eight or 16
A-aligned (A
al
) spermatogonia. The A
al
spermatogonia
differentiate into A1 spermatogonia and after six mitotic
divisions result in A2, A3, A4 and, finally, B spermatogonia,
which give rise to spermatocytes at the last mitotic division.
Irrespective of species-specific differences, in the bovine
testis, a comparable classification with another terminology
has been reported (Wrobel et al., 1995a). In this species,
spermatogonial precursor cells have been divided into basal
stem cells (BSC), aggregated spermatogonial precursor cells
(ASPC) and committed spermatogonial precursor cells
(CSPC), which, according to this classification, represent
A
s
–A
pr
spermatogonia, A
al
spermatogonia and A
1
–A
4
differ-
entiating spermatogonia, respectively. Hence, in bulls, A
pr
spermatogonia are also thought to have stem cell properties
(Wrobel, et al., 1995a).
As there are relatively few stem cells that can be defined
only by their function, the identification and isolation of these
cells has been very difficult. To date, the most effective way
to enrich germ cell populations for stem cells is to purify all
forms of type A spermatogonia. In the adult mammalian
testis, owing to the presence of multiple generations of
germinal cells, purification of spermatogonia is more diffi-
cult than it is before puberty. Bellve et al. (1977) obtained a
90% pure fraction of type A spermatogonia from immature
mice. Similarly, highly purified spermatogonia have been
obtained from immature rat (Morena et al., 1996) and pig
(Dirami et al., 1999) testes. In addition, vitamin A-deficient
animals can be used as a source of spermatogonia as, in
these animals, spermatogenesis stops at a spermatogonial
Isolation and purification of type A spermatogonia
from the bovine testis
F. Izadyar
1,2
, G. T. Spierenberg
3
, L. B. Creemers
1,2
,
K. den Ouden
1,2
and D. G. de Rooij
1,2
1
Department of Endocrinology, Faculty of Biology, University Medical Center Utrecht,
Utrecht, The Netherlands; and Departments of
2
Cell Biology and
3
Immunology, University
Medical Center Utrecht, Utrecht, The Netherlands
Reproduction (2002) 124, 85–94
Research
The aim of this study was to isolate and purify bovine type
A spermatogonia. Testes from 5–7-month-old calves were
used to isolate germ cells using a two-step enzymatic
digestion. During the isolation and purification steps,
the viability of cells was determined using live/dead
staining. The identity of type A spermatogonia during isola-
tion and purification was determined under a light micro-
scope equipped with a Nomarski lens. Isolated cells were
characterized further by using specific markers for type A
spermatogonia, including Dolichos biflorus agglutinin
(DBA) and c-kit. The cell suspension was transplanted into
immunodeficient recipient mouse testes and the colon-
ization was assessed 1–3 months after transplantation, to
assess the stem cell population among the isolated cells.
After isolation, a cell suspension was obtained containing
about 25% type A spermatogonia, which was enriched
further by differential plating and separation on a discon-
tinuous Percoll gradient. Finally, fractions containing
65–87% pure type A spermatogonia were obtained. Large
and small type A spermatogonia with different numbers
and sizes of nucleoli were found. DBA stained both large
and small type A spermatogonia and its application in
fluorescence-activated cell sorting (FACS) resulted in
comparable percentages of type A spermatogonia to those
determined by morphological examination under a light
microscope equipped with a Nomarski lens. Nearly all
of the large type A spermatogonia showed strong c-kit
immunoreactivity, indicating that these cells had under-
gone at least an initial differentiation step. In contrast,
approximately half of the small type A spermatogonia were
negative for c-kit, indicating the presence of the sper-
matogonial stem cells in this population. At 3 months after
transplantation, groups of bovine type A spermatogonia
were found in most tubule cross-sections of the recipient
mouse testes, showing the presence of spermatogonial
stem cells among the isolated cells.
© 2002 Society for Reproduction and Fertility
1470-1626/2002
Email: fizadyar@lab.azu.nl
Downloaded from Bioscientifica.com at 02/17/2023 02:44:42PM
via free access