[Stem Cell Studies 2011; 1:e15] [page 91]
In vitro and in vivo lineage
conversion of bone marrow
stem cells into germ cells
in experimental Azoospermia
in rat
Mohammed T. Abdel Aziz,
1
Taymour Mostafa,
2
Hazem Atta,
1
Soheir Asaad,
3
Hanan Fouad,
1
Gamal Mohsen,
1
Laila Rashed,
1
Dina Sabry,
1
Mohammed Abbas
1
1
Unit of Biochemistry and Molecular
Biology Medical Biochemistry;
2
Andrology & Sexology;
3
Histology
Departments, Faculty of Medicine, Cairo
University, Cairo, Egypt
Abstract
The present study is conducted to assess in
vitro transdifferentiation of bone marrow
derived mesenchymal stem cells (MSCs) into
germ cells and in vivo transdifferentiation into
spermatids and spermatocytes in the seminif-
erous tubules of azoospermic rats. Forty eight
male rats were included in the study and were
divided into: group 1; control rats, group 2;
experimental azoospermic rats, group 3;
azoospermic rats received undifferentiated
MSCs. Group 4; azoospermic rats received
transdifferentiated MSCs into germ cells.
Quantitative real time PCR was conducted to
assess gene expression of a primordial germ
cell marker (VASA), stem cell specific markers
(Oct4, SSEA-1 and SSEA-3), specific molecular
markers of germ cells (c-Kit, Daz1); premeiot-
ic marker (Daz1) and post-meiotic markers (c-
Kit, Stra 8). Histopathological examination of
rat testicular tissue was also conducted.
Results revealed that 12 weeks after transplan-
tation, fluorescent labeled MSCs were detected
in the seminiferous tubules of the testes of
group 3 and group 4 rats. In group 3 and 4,
stem cell specific markers; Oct4, SSEA-1 and
SSEA-3 were detected. In group 4, genes of pri-
mordial germ cell marker; VASA, premeiotic
marker; Daz1and post-meiotic markers; c-Kit,
Stra 8 were expressed. Daz1 was also
expressed in group 3 rats to a significantly
lower extent in comparison to group 4 rats.
Spermatocytes and spermatids were detected
in testicular tissue of group 4 rats. In conclu-
sion, MSCs have potentials for in vitro transd-
ifferentiation into germ cells and in vivo trans-
differentiation into spermatids and spermato-
cytes.
Introduction
Spermatogenesis is generated by male ger-
minal stem cells as evidenced by regeneration
of spermatogic cells after transplantation of
total testicular germ cells in the depleted
testis.
1,2
Several studies have assessed the
potential of reproducing germ cell differentia-
tion, or gametogenesis, in vitro.
3
Under appro-
priate conditions, bone marrow stem cells
(BMCs), embryonic stem cells (ESCs) could be
induced to transdifferentiate toward the germ
cell lineage.
4-6
Several breakthroughs discovery concerning
the in vitro derivation of male and female
germ cells from stem cells have challenged the
field of reproductive biology.
7-10
Mouse bone
marrow mesenchymal stem cells (MSCs),
grown in vitro in the presence of retinoic acid,
were found to express germ cell markers.
11,12
A
similar transdifferentiation process was
described for human bone marrow cells.
13,14
Nayernia et al.
15
stated that BMS cell-
derived germ cells expressed the known molec-
ular markers of primordial germ cells; fragilis,
stella, Rnf17, Mvh and Oct4; and molecular
markers of spermatogonial stem cells and
spermatogonia; Rbm, c-Kit, Tex18, Stra8,
Piwil2, Dazl, Hsp90alpha, beta1- and alpha6-
integrins. Another study has demonstrated
that adult bone marrow stem cells can differen-
tiate into Leydig cells in rat testes.
9
Lue et al.
12
provided evidence showing that adult bone
marrow cells injected into seminiferous
tubules or interstitial spaces of busulfan treat-
ed mice are able to differentiate into germ
cells as evidenced by the detection of VASA
marker and they are also able to differentiate
into Sertoli and Leydig cells as evidenced by
the detection of follicular stimulating hormone
receptors and cytochrome P450 (P450scc) side
chain cleavage enzyme within the seminifer-
ous tubules.
The present study was conducted to assess
transdifferentiation potentials of MSCs into
germ cells in vitro and transdifferentiation
potentials of MSCs into spermatids and sper-
matocytes in the seminiferous tubules of
azoospermic rats.
Materials and Methods
Animal studies
The in vivo study was conducted on forty
eight Cur1:HEL1 male albino rats, of an aver-
age weight 180-200 gm, age 60 days. Rats were
inbred strain in the experimental animal unit,
Faculty of Medicine, Cairo University. Animals
were maintained in an air-conditioned animal
house with specific pathogen-free conditions,
and were subjected to a 12:12-h daylight/dark-
ness and allowed unlimited access to chow and
water. They were maintained according to the
standard guidelines of Institutional Animal
Care and Use Committee and after
Institutional Review Board approval.
Rat were equally divided into the following
groups: group1 involved control rats received
phosphate buffer saline, group 2 included rats
with experimental azoospermia induced by
administration of a single intraperitoneal dose
of busulfan (GlaxoSmithKline Inc.,
Mississauga, Ontario, Canada) (35 mg/kg),
group 3 included azoospermic rats that under-
went transplantation of 1×10
8
undifferentiated
MSCs into the testis 2 weeks after induction of
azoospermia. Group 4 involved azoospermic
rats that underwent transplantation of 1×10
8
differentiated MSCs into germ cells 2 weeks
after induction of azoospermia. The injection
procedure was conducted as previously
decribed.
16
All recipient rats were kept under
anesthesia by intraperitoneal administration
of Xylazine (20 mg/kg), Ketamine (5 mg/kg),
and Athropine (0.04 mg/kg). Microinjection
needles 100 μL were used for MSCs transplan-
tation. The testes were surgically exteriorized
through a midline abdominal incision, and
MSCs suspensions (1×10
8
) were injected
using microinjection needles. Small incision
was made 5 mm from the efferent bundles’
junction with the testis. The tip of the microin-
jection needle was inserted into the bundles
and then gently pushed toward the rete testis
to enter the seminiferous tubules as described
by Ogawa et al.
16
Twelve weeks after MSCs transplantation,
animals were euthanized and testicular tis-
sues were collected from all animals and the
following parameters were assessed:
Testicular histopathological examination,
detection of the labeled bone marrow derived
stem cells by using PKH26 Red Fluorescent
Cell Linker Kit (Sigma Aldrich, St. Louis, MO,
Stem Cell Studies 2011; volume 1:e15
Correspondence: Hanan H. Fouad, Medical
Biochemistry Department, Faculty of Medicine,
Cairo University, Cairo, Egypt, POB 11562.
Tel. +20.101.418.750 - Fax: +20.223.632.297.
E-mail: hananfouadbostamy24@gmail.com
Key words: azoospermia, germs cells, MSCs,
spermatids, spermatocytes.
Received for publication: 3 September 2011.
Accepted for publication: 11 October 2011.
This work is licensed under a Creative Commons
Attribution NonCommercial 3.0 License (CC BY-
NC 3.0).
©Copyright M.T. Abdel Aziz et al., 2011
Licensee PAGEPress, Italy
Stem Cell Studies 2011; 1:e15
doi:10.4081/scs.2011.e15
Non-commercial use only