Review Article
Somatic Cell Cloning for Livestock and Endangered Species
Rangsun Parnpai* Kanokwan Srirattana Sumeth Imsoonthornruksa
Mariena Ketudat-Cairns
Abstract
It has now been 15 years since the first cloned sheep was born using somatic cell nuclear transfer (SCNT).
This technique provides a unique tool for preservation of valuable individuals, livestock propagation, genetically
modified animals, production research of biomedicine and conservation of endangered species. In this review,
research of the SCNT in livestock and endangered species, including our current work, will be discussed.
Keywords: cloning, endangered species, somatic cell nuclear transfer
Embryo Technology and Stem Cell Research Center, School of Biotechnology, Suranaree University of Technology, Nakhon
Ratchasima 30000, Thailand.
Corresponding author E-mail: [email protected]
Thai J Vet Med Suppl. 2011. 41: 77-85.
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Parnpai et al. / Thai J Vet Med Suppl. 2011. 41: 77-85.
Introduction
Assisted reproductive techniques (ART) such
as artificial insemination, embryos transfer, in vitro
fertilization, gamete/embryo micromanipulation and
somatic cell nuclear transfer (SCNT) or cloning have
been developed to obtain offspring from genetically
individuals or infertile animals (reviewed by Andrabi
and Maxwell, 2007). SCNT is the transplantation of a
nucleus from donor cell into an enucleated oocyte.
After Dolly, the first cloned sheep produced by SCNT
was born in July, 1996 (Wilmut et al., 1997). SCNT has
been successfully applied to many mammalian
species for the production of offspring. Examples of
these are mouse (Wakayama et al., 1998), bovine
(Cibelli et al., 1998; Kato et al., 1998), goat (Baguisi et
al., 1999), pig (Onishi et al., 2000; Polejaeva et al.,
2000), rat (Zhou et al., 2003), cat (Shin et al., 2002),
rabbit (Chesné et al., 2002), horse (Galli et al., 2003),
mule (Woods et al., 2003), dog (Lee et al., 2005), water
buffalo (Shi et al., 2007), ferret (Li Z. et al., 2006) and
camel (Wani et al., 2009). However, SCNT technique
is almost impossible for the endangered species
production because of the lack of oocytes and
recipients. Interspecies somatic cell nuclear transfer
(iSCNT) is an alternative technique to solve this
problem by transferring a donor cell from one species
into an enucleated oocyte of another species. This
technique is useful for studying nucleus-cytoplasm
interaction and conservation of the endangered
species (reviewed by Beyhan et al., 2007). The
offspring productions from iSCNT have been
reported in several endangered species such as
mouflon (Loi et al., 2001), gaur (Lanza et al., 2000;
Vogel, 2001), Afican wild cat (Gómez et al., 2003),
gray wolf (Kim et al., 2007), bucardo (Folch et al.,
2009) and sand cat (Gomez et al., 2008). Although
successful production of cloned animals from SCNT
and iSCNT has been achieved, the overall efficiency is
still very low, only 2-10% of reconstructed embryos
developed to term (Pandey et al., 2009). In this review,
we will concentrate on the cloning of livestock and
endangered species.
Success in livestock species
1. Sheep
An improvement in farm animal cloning was
achieved in 1996 with the birth of the sheep Dolly
through the SCNT technique (Wilmut et al., 1997).
However, Dolly had shorter telomere region than age
matched control (Shiels, et al., 1999). In 2003, Dolly
suffered from a progressive lung disease and died at
the age of 6 years, about half the lifespan of a normal
sheep (Wilmut, 2003). The second breakthrough in
farm animal cloning was the birth of Polly, a
genetically modified sheep (Schnieke et al., 1997).
Genetically modified animals, also known as
transgenic animals, carry one or several genes from
other organisms in their genome. Since then, cloned
transgenic farm animals using SCNT were reported in
bovine (Cibelli et al., 1998; Brink et al., 2000; Brophy et
al., 2003), goat (Keefer et al., 2001) and pig (Park et al.,
2002; Lai et al., 2002; 2003).
2. Bovine
Two years following the birth of Dolly,
SCNT had successfully produced live offspring
bovines from fetal fibroblasts (Cibelli et al., 1998) and
adult cells (Kato et al., 1998). The first cloned calf in
Thailand was born in 2000 using ear fibroblasts of
female Brangus (Parnpai et al., 2000a,b). We also
produced 7 live cloned calves from ear fibroblasts of
Brahman bull and 3 live cloned calves from ear
fibroblasts of Holstein-Friesian cow (Parnpai et al.,
2004). Subsequently, we produced 1 cloned calf using
ear fibroblasts from Khaw Lamphun cattle, the native
breed of the Northern part of Thailand
(Keawmungkun et al., 2008). SCNT process is known
to be affected by many factors, including suitable
donor cells and recipient cytoplasts, compatibility
between the karyoplasts and cytoplasts, technical
efficiency and optimal culture conditions. From our
previous studies, fetal fibroblasts (FFs), ear fibroblasts
(EFs), granulosa cells (GCs) and cumulus cells (CCs)
have similar potentials to support the development of
cloned bovine and buffalo embryos to blastocyst stage
with the same quality (Table 1). Moreover, the SCNT
blastocyst rates in bovine were significantly higher
than those in swamp buffalo (Srirattana et al., 2010).
The proportions of SCNT blastocysts were not
different when either cycling or quiescent ear
fibroblasts were used as donor cells (Parnpai et al.,
2000a). Several studies indicated that trichostatin A
(TSA), a histone deacetylase inhibitor treatment of
cloned bovine embryos, improved the in vitro embryo
development (Ding et al., 2008; Srirattana et al., 2009;
Akagi et al., 2011; Lee et al., 2011). In vitrified
embryos, the SCNT bovine blastocysts, regardless of
their hatching stage, were relatively resistant to
cryopreservation by vitrification (Laowtammathron et
al., 2005). Laowtammathron et al. (2009) reported that
after transferring fresh and vitrified/thawed cloned
bovine embryo to recipients, the pregnancy rate of the
vitrified group was lower (25.0%) than the fresh
group (42.5%). In the vitrified group and fresh group
12.5% and 21.4% pregnancy to term, respectively.
Finally, we obtained 3 cloned calves from the fresh
group and twin cloned calves from the vitrified
group.
3. Goat
Goat is an important source of milk, meat,
and manure throughout the world. It also helps in
sustaining the economy of the farmers. Goats have
also been reported as an ideal species for production
of recombinant proteins due to its unique advantages
over cattle and sheep (Baguisi et al., 1999; Reggio et
al., 2001; Baldassarre et al., 2004; Behboodi et al., 2004;
Melican et al., 2005; Lan et al., 2006). Several attempts
have been made to produce cloned goats (Baguisi et
al., 1999; Keefer et al., 2001; Lan et al., 2006; Shen et
al., 2006). The first successful report of goat cloning
turns back to 1999 as there were prefixes in the field of
goat in vitro cloning and embryo culture, for example
the majority of goat SCNT studies have used ovulated
or laporoscopic OPU-derived oocytes, which make
goat cloning expensive and demanding (Baldassarre
and Karatzas, 2004; Baldassarre et al., 2004); and in
most reports, reconstructed goat embryos have been
Parnpai et al. / Thai J Vet Med Suppl. 2011. 41: 77-85.
either cultured in vitro as short as possible (up to the
eight-cell stage) (Baguisi et al., 1999; Keefer et al.,
2001; Reggio et al., 2001; Ohkoshi et al., 2003;
Behboodi et al., 2004; Melican et al., 2005; Lan et al.,
2006; Chen et al., 2007) or temporarily incubated in an
intermediate oviduct (Zou et al., 2001; Behboodi et al.,
2004) to avoid the abnormal/poor embryo
development that has been reported to be associated
with the in vitro culture of goat embryos. Our
previous study found that the rates of cleavage,
development to 2- and 4-cell stages embryo had no
significant difference when using male and female ear
fibroblasts as donor cells but the development to 8cell stage of embryos derived from male ear
fibroblasts was significantly higher than that of female
ear fibroblasts. After transferring 2-8 cell stage
embryos to the oviducts of recipients, only the
recipients received the male cloned goat embryos
were pregnant (2/15, 13.3%). Both pregnant recipients
delivered two healthy male kids by Caesarean section.
Both kids were phenotypically and genotypically
identical to the donor. Unfortunately, one kid died 32
h after birth (Sangmalee et al., 2007).
4. Pig
The main applications of SCNT in pig are for
biomodels of research and are for creating genetically
modified animals as potential tissues and organ
donors for xenotransplantation (Gil et al., 2010). The
first piglets produced by SCNT were achieved with
both in vivo–matured (Onishi et al., 2000; Polajaeva et
al., 2000) and in vitro–matured oocytes (Betthauser et
al., 2000). Zona-free nuclear transfer with mechanical
aspiration of the metaphase plate (Lagutina et al.
2007) or micromanipulator-free handmade cloning
(Vajta et al., 2005) have resulted in high in vitro
developmental rates to good quality blastocyst stage
embryos. In pig SCNT, TSA treatments have been
shown to have beneficial effects on the development
of cloned embryos (Zhang et al., 2007; Li et al., 2008,
Beebe et al., 2009; Matinez-Diaz et al., 2010; Kimaki et
al., 2010; Kim et al., 2011). Interestingly, successful
cloned piglet production after co-transfer with
parthenogenetic embryos (Kawarasaki et al. 2009) or
hormonal injection after the transfer (Lee et al., 2008)
to enhance and maintain the signal of pregnancy have
been reported.
5. Buffalo
Buffalo is a multi-purpose animal in
agriculture which can provide work draft power, milk
and meat. Fertility in water buffalo is generally low
owing to the late onset of puberty, seasonal anoestrus,
long post-partum anoestrus period, silent estrus and
long calving interval (Drost, 2007). Although
researches on SCNT in buffalo started rather late and
developed slowly, there have been a number of
reports on SCNT in buffalo (Parnpai et al., 1999;
79
Parnpai et al., 2002; Saikhun et al., 2004; Meena and
Das, 2006; Simon et al., 2006; Shi et al., 2007; Shah et
al., 2009; Srirattana et al., 2010; Yang et al., 2010). Only
two live cloned buffalos have been reported (Shi et al.,
2007; Yang et al., 2010). From our report, the
activation of reconstructed swamp buffalo embryos
with 7% ethanol followed by cultured in the
combination of 6-DMAP, cycloheximide (CHX) and
cytochalasin D (CD) gave higher morulae and
blastocysts yields than cultured in 6-DMAP+CD or
CHX+CD (Parnpai and Tasripoo, 2003). Moreover, the
parthenogenetic development to blastocyst stage of
buffalo oocytes activated by ethanol or calcium
ionophore combined with 6-DMAP was higher than
that activated by electrical pulses (Kitiyanant et al.,
2003). As described herein, FFs, EFs, GCs and CCs
had similar potentials to support the development of
cloned buffalo embryos (Table 1, Srirattana et al.,
2010) while Shah et al. (2009) reported that cumulus
cells were better than ear fibroblasts. In some species,
telomere length becomes abnormally shortened
following SCNT and the embryo failed to develop.
The telomerase activities in SCNT buffalo embryos
were up-regulated as early as the morula stage and
reached the highest levels at the blastocyst stage,
which was similar to the IVF embryos (Saikhun et al.,
2004). In cryopreservation of cloned buffalo embryos,
our studies demonstrated that cloned buffalo embryos
at the morula stage could be vitrified by solid surface
vitrification. After thawing, vitrified cloned morulae
could develop to hatching blastocysts with no
difference from fresh morula (79.6% and 84.0%,
respectively) (Parnpai et al., 2001). Laowtammathron
et al. (2005) studied the effect of the hatching stage of
cloned swamp buffalo blastocysts on the cryosurvival
ability of embryos after vitrification and found that
cryosurvival of early hatching blastocysts were not
different from those of middle - and late-hatching
blastocysts (hatching blastocyst rates: 87-89%).
Epigenetic modification involves altering gene
expression without changing the DNA sequence.
DNA methylation and histone acetylation
are the key mechanisms of this process. Abnormal
epigenetic mechanisms are suspected to be the cause
of developmental failure particularly in SCNT
experiment. The SCNT swamp buffalo embryos are
not only hypermethylated and hyperacetylated but
are also more heterogenous in DNA methylation and
histone acetylation among different cells of the same
embryos than those of IVF embryos (Suteevun et al.,
2006a). The expression levels of DNA modifying genes
(DNMT1, DNMT3A, DNMT3B, HAT1 and HDAC1)
were higher in the SCNT embryos than in the IVF
embryos at 8-cell and blastocyst stages. The HDAC1
and HAT1 genes were also expressed significantly
higher at the blastocyst stage in SCNT embryos
(Suteevun et al., 2006b).
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Parnpai et al. / Thai J Vet Med Suppl. 2011. 41: 77-85.
Table 1 Effect of donor cell type on developmental potential of cloned cattle and buffalo embryos*
Species
Cattle
Buffalo
No. (%) embryos developed to
Donor cell
type
No. of
couplets
fused (%)
No. of
embryos
cultured
No. of
embryos
cleaved
(%)
8-Cell
Morula
Blastocyst
FF
113/132
(85.6)b
110
108 (98.2)a
88 (80.0)a
60 (54.5)a
45 (40.9)a
EF
111/121
(91.7)a
111
100 (90.1)ab
78 (70.3)abc
60 (54.1)a
43 (38.7)a
GC
111/124
(89.5)ab
111
101 (91.0)ab
76 (68.5)ab
51 (45.9)ab
46 (41.4)a
CC
118/145
(81.4)c
108
100 (92.6)ab
65 (60.2)abc
46 (42.6)ab
40 (37.0)ab
PA
-
105
86 (81.9)bc
48 (45.7)c
43 (41.0)ab
27 (25.7)cd
FF
120/136
(88.2)ab
119
100 (84.0)bc
76 (63.9)abc
38 (31.9)b
26 (21.8)cd
EF
112/130
(86.2)b
112
96 (85.7)bc
71 (63.4)abc
37 (33.0)b
30 (26.8)cd
GC
108/122
(88.5)ab
102
88 (86.3)bc
69 (67.6)ab
35 (34.3)b
25 (24.5)cd
CC
117/143
(81.8)c
104
86 (82.7)bc
63 (60.6)abc
35 (33.7)b
29 (27.9)bc
PA
-
104
82 (78.8)c
58 (55.8)bc
36 (34.6)b
20 (19.2)d
*Five replicates were performed. Different superscripts within a column indicate significant differences (p<0.05).
FF: fetal fibroblasts, EF: ear fibroblasts, GC: granulosa cells, CC: cumulus cells, PA: parthenogenetic activation.
Cited from Srirattana et al. (2010)
Success in endangered species
Shortly after the birth of cloned lamb, the
first iSCNT experiment showed that bovine oocytes
could support the in vitro development of sheep, pig,
monkey and rat cells (Dominko et al., 1999). Since
then, the feasibility of iSCNT has been addressed by
several researchers employing various model systems.
Endangered species offspring have also been
produced by nuclear transfer techniques. Lanza et al.
(2000) performed iSCNT by using gaur skin
fibroblasts fused with enucleated bovine oocytes. The
blastocyst rate of gaur-bovine iSCNT was 12% and the
pregnancy rate was 25%. Only one recipient carried to
term. Noah, the cloned gaur was born with a 36 kg
birth weight. The cloned gaur was healthy at birth but
died 2 days later (Vogel, 2001). From our studies in
gaur iSCNT, the rates of fusion, cleavage and
development to the blastocyst stage were not
significantly different between male and female
fibroblasts-derived embryos (Sangngam et al., 2005).
Surprisingly, TSA, a histone deacetylase inhibitor,
could not improve the development to the blastocyst
stage of gaur iSCNT (Srirattana et al., 2008). As with
the other endangered species, mouflon has been
successfully produced by mouflon-sheep iSCNT (Loi
et al., 2001). Surprisingly, successful production of
African wild cat iSCNT using domestic cat oocytes as
recipient cytoplasts resulted in a total of 17 cloned
kittens born, 7 were stillborn, 8 died within hours of
delivery or up to 6 weeks of age, and 2 were alive and
healthy (Gómez et al., 2004). Gómez et al. (2008)
successfully produced sand cat kittens using domestic
cat oocytes. In our work, aberrant gene expression of
Oct4, DNMT1, DNMT3a, DNMT3b, HAT1 and
HDAC1 in leopard cat and marbled cat iSCNT
embryos, which was related to the lower in vitro
development to the blastocyst stage, was reported
(Imsoonthornruksa et al., 2010). Moreover, early fetal
losses of sand cat iSCNT embryos were shown to be
associated with the abnormal expression of the Oct-4
gene (Gómez et al., 2008). Subsequently, two cloned
gray wolves were obtained by iSCNT of wolf cell and
domestic dog oocyte (Kim et al., 2007). Moreover, an
extinct mountain goat, bucardo (Capra pyrenaica
pyrenaica), were produced by fusing the bucardo
fibroblasts with enucleated domestic goat oocytes.
One cloned bucardo offspring was obtained but died
a few minutes after birth due to physical defects in the
lungs (Folch et al., 2009). To date, live river buffalo
offspring has been obtained by subspecies SCNT
using swamp buffalo oocytes. The cloned calf has
been growing well with no abnormalities observed
(Yang et al., 2010).
Additionally, iSCNT allows examination of
nucleo–cytoplasmic interactions, shedding light on
limiting embryo development affecting the host of
assisted reproductive technologies (Beyhan et al.,
2007; Mastromonaco and King, 2007). The
Parnpai et al. / Thai J Vet Med Suppl. 2011. 41: 77-85.
incompatibility of nuclear and mitochondrial encoded
components from different species and subspecies is
likely to hinder the normal development of
reconstructed embryos which affect the efficiency of
cloning. In buffalo-bovine iSCNT embryos, buffalo
mtDNA copy numbers in iSCNT embryos were
constant throughout the iSCNT process until an arrest
at the 8- to 16-cell stage (Srirattana et al., 2011).
Constant copy numbers of donor cell mtDNA from
the 1-cell to the 8-cell stage embryos were also found
in sheep–bovine (Hua et al. 2008), cat–bovine
(Thongphakdee et al. 2008), goat–sheep (Ma et al.
2008) and macaque–rabbit (Yang et al. 2004) arrested
embryos. In contrast, the copy numbers of donor cell
and recipient cytoplast mtDNAs in gaur–bovine
embryos remained constant during the early cleavage
until the morula stage but then increased at the
blastocyst stage (Mastromonaco et al. 2007).
Moreover, homoplasmy of recipient oocyte mtDNA
was found in some iSCNT offspring (Lanza et al. 2000;
Loi et al. 2001; Meirelles et al. 2001; Steinborn et al.
2002; Kim et al. 2007). In addition, Gómez et al. (2009)
reported that coexistence of mtDNA in African wild
cat cloned offspring produced from iSCNT did not
impart negative effects on the health of offspring.
However, the success of producing cloned embryos,
even offspring by iSCNT, indicated that the technique
of iSCNT can be adopted to increase the population
size of endangered mammals or even to restore
extinct species.
Conclusion
Although
blastocyst
and
offspring
productions from both SCNT and iSCNT have been
reported in several mammalian species, the overall
success rates are still low. There are too many
unknown factors and sub-optimal conditions to
efficiently produce live healthy animals. Therefore,
better understanding of cell function, embryo
development and fetal-maternal interaction are
needed to improve these SCNT and iSCNT
procedures.
Acknowledgments
The research in our laboratory is supported
by Thailand Research Fund, National Research
Council of Thailand, National Center for Genetic
Engineering and Biotechnology and Suranaree
University of Technology.
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