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The evolution of chicken stem cell culture methods
Article in British Poultry Science · August 2017
DOI: 10.1080/00071668.2017.1365354
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British Poultry Science
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The evolution of chicken stem cell culture
methods
M. Farzaneh, F. Attari, P. E. Mozdziak & S. E. Khoshnam
To cite this article: M. Farzaneh, F. Attari, P. E. Mozdziak & S. E. Khoshnam (2017):
The evolution of chicken stem cell culture methods, British Poultry Science, DOI:
10.1080/00071668.2017.1365354
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Date: 29 September 2017, At: 00:57
BRITISH POULTRY SCIENCE, 2017
https://doi.org/10.1080/00071668.2017.1365354
SHORT REVIEW
The evolution of chicken stem cell culture methods
M. Farzaneha, F. Attarib, P. E. Mozdziakc and S. E. Khoshnamd,e
Downloaded by [5.56.129.55] at 00:57 29 September 2017
a
Department of Stem Cells and Developmental Biology, Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology,
ACECR, Tehran, Iran; bDepartment of Animal Biology, School of Biology, College of Science, University of Tehran, Tehran, Iran; cPhysiology
Graduate Program, North Carolina State University, Raleigh, NC, USA; dDepartment of Physiology, Faculty of Medicine, Physiology Research
Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran; eStudent Research Committee, Ahvaz Jundishapur University of Medical
Sciences, Ahvaz, Iran
ABSTRACT
ARTICLE HISTORY
1. The avian embryo is an excellent model for studying embryology and the production of pharmaceutical proteins in transgenic chickens. Furthermore, chicken stem cells have the potential for
proliferation and differentiation and emerged as an attractive tool for various cell-based technologies.
2. The objective of these studies is the derivation and culture of these stem cells is the production of
transgenic birds for recombinant biomaterials and vaccine manufacture, drug and cytotoxicity
testing, as well as to gain insight into basic science, including cell tracking.
3. Despite similarities among the established chicken stem cell lines, fundamental differences have
been reported between their culture conditions and applications. Recent conventional protocols
used for expansion and culture of chicken stem cells mostly depend on feeder cells, serum-containing media and static culture.
4. Utilising chicken stem cells for generation of cell-based transgenic birds and a variety of vaccines
requires large-scale cell production. However, scaling up the conventional adherent chicken stem
cells is challenging and labour intensive. Development of a suspension cell culture process for
chicken embryonic stem cells (cESCs), chicken primordial germ cells (PGCs) and chicken induced
pluripotent stem cells (ciPSCs) will be an important advance for increasing the growth kinetics of
these cells.
6. This review describes various approaches and suggestions to achieve optimal cell growth for
defined chicken stem cells cultures and use in future manufacturing applications.
Received 17 February 2017
Accepted 29 June 2017
Introduction
The avian embryo provides an excellent model for studying
embryology, developmental biology and production of
pharmaceutical proteins in transgenic chickens (Naito
2003; Farzaneh et al. 2016; Farzaneh et al. 2017b). The
first chicken stem cells were derived from blastodermal
cells (BCs) of fertilised eggs at embryonic stage X and
were designated as chicken embryonic stem cells (cESCs)
(Pain et al. 1996; van de Lavoir and Mather-Love 2006;
Intarapat and Stern 2013). Since the establishment of the
first cESCs, rapid progress has been made and several
groups have described the derivation and culture of chicken
stem cells from various developmental stages (Petitte et al.
2004; ; Jung et al. 2007; Motono et al. 2008; Trefil et al.
2012; Bednarczyk 2014; Farzaneh et al. 2017a) . The second
population of in vitro chicken stem cells, named embryonic
germ cells (EGCs), were derived from primordial germ cells
(PGCs) (Park and Han 2000; Guan et al. 2010). The third
population are known as chicken-induced pluripotent stem
cells (ciPSCs) and have been generated by in vitro reprogramming of chicken fibroblast cells (from 8–12dold
embryos) on a feeder layer (Lu et al. 2011; Yu et al. 2013).
Chicken stem cells with self-renewal capacity can be propagated in culture indefinitely and have the ability to differentiate into multiple cell types representing all primitive
embryonic germ layers (Lavial and Pain 2010; Intarapat
KEYWORDS
Chicken embryo; defined
culture medium; stem cells;
suspension culture; vaccine
manufacture
and Stern 2013). Chicken stem cells have provided an
ideal opportunity for generating cell-based transgenic
birds (Han et al. 2015; Farzaneh et al. 2017a) and a powerful
source of cells for vaccine production for poultry and
human viral diseases. Moreover, they provide insight into
basic science including cell tracking, as well as drug and
cytotoxicity testing (Aubrit et al. 2015; Gallo–Ramírez et al.
2015; Genzel 2015). For reliable use of chicken stem cells in
basic and applied sciences, it is necessary to eliminate the
variations in culture conditions required for their establishment. Standardised cell culture protocols are important not
only for gene manipulation, but also for biological research
carried out using these cells. Hence, this mini review
describes different culture conditions required for chicken
stem cell culture and development of serum/feeder-containing media to defined conditions for the purpose of largescale and suspension culture of chicken stem cells for drug
discovery and recombinant protein production.
Derivation of chicken stem cells
The chicken embryo spends approximately its first 20 h in
the hen’s body and as the embryo traverses the oviduct cell
division occurs in a meroblastic pattern to generate BCs
(Jacobson 1989). By the time the egg is laid, there are
approximately 40 000–50 000 BCs, which arise from the
cleavage of a single fertilised ovum surrounded by islands of
CONTACT M. Farzaneh
maryamfarzaneh2013@yahoo.com
Department of Stem Cells and Developmental Biology, Cell Science Research Center, Royan
khoshnam.e@ajums.ac.ir
Department of Physiology, Faculty of Medicine,
Institute for Stem Cell Biology and Technology, Tehran, Iran; S. E. Khoshnam
Physiology Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
© 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.0/),
which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
Downloaded by [5.56.129.55] at 00:57 29 September 2017
2
M. FARZANEH ET AL.
yolk cells (Lavial and Pain 2010). The entire embryo develops from the centre of the epiblast, and it has a remarkable
regenerative capacity (Alev et al. 2013). cESCs were isolated
from BCs at embryonic stage X; these have a relatively small
amount of cytoplasm with a large translucent nucleus containing a single nucleolus (Wei et al. 2000; van de Lavoir
and Mather-Love 2006). In culture, cESCs grow on feeder
cells and attach to each other with visible borders (Aubel
and Pain 2013). Moreover, it was shown that cESCs are able
to contribute to different cell lineages including somatic and
germ cell lines (Etches et al. 1996; Pain et al. 1996). cESCs
have been derived from chicken eggs of meat strains more
efficiently compared with egg-laying strains (Aubel and
Pain 2013). These cells are of interest for transgenic technology and vaccine manufacturing (Brown and Mehtali
2010; Olivier et al. 2010). However, some reports mentioned
that cESCs lost their pluripotency after long-term culture
(Yu et al. 2013). Therefore, it seems that their potential for
germ line transmission into offspring was low (van de
Lavoir et al. 2006; Intarapat and Stern 2013) and only a
few laboratories have taken the risk of establishing cESCs
for developmental studies (Jean et al. 2015).
Scientists have established long-term culture of chicken
PGCs harvested from the circulatory system of 2.5–3 d old
embryos (van de Lavoir et al. 2006) and embryonic gonads
(5.5–6 d old) (Park and Han 2000). Approximately 30–130
PGCs are present in the extraembryonic region of the
chicken embryo and unlike mammals, they use blood circulation as the migratory route and stop active migration as
soon as they reach the genital ridges (Eyal-Giladi et al. 1981;
Kuwana 1993; Petitte et al. 1997; Bernardo et al. 2012).
PGCs are identified by their remarkably large size, large
spherical nuclei and refractive cytoplasmic lipids with high
glycogen content (Li et al. 2010; Pinkert 2014). These cells
are a suitable vehicle for developing cell-based transgenic
birds (Han et al. 2015; Taylor et al. 2017) and a cell-free
culture system has been described (Whyte et al. 2015).
Research on iPSCs paved the way to identify the molecular mechanisms underlying pluripotency of all kinds of
chicken stem cells (Lu et al. 2011) as well as providing a
better tool for vaccine manufacturing (Shittu et al. 2016).
Although feeder cell, serum and growth factor employment
in culture conditions leads to the successful derivation and
culture of chicken stem cells, it presents a risk of propagating contaminating virus particles making these supplements
unsuitable for vaccine manufacturing and cell-based transgenic technology (Halme and Kessler 2006; Eaker et al.
2017; Gupta et al. 2017).
Culture medium for chicken stem cells
Knockout Dulbecco’s modified Eagle’s medium
(Knockout DMEM or KO/DMEM) is a basic culture
medium which can support the growth of chicken stem
cells in vitro. The composition of KO/DMEM is suitable
for all kinds of mammalian and non-mammalian stem
cells and can increase their growth rate to produce an
adequate population (van de Lavoir and Mather-Love
2006; Amit and Itskovitz-Eldor 2016). Although
Dulbecco’s modified Eagle’s medium (DMEM) can support the growth of chicken stem cells, its high osmolarity
(320–350 mOsm) may have an adverse effect on proliferation of these cells in vitro (van de Lavoir and Mather-
Love 2006). Traditionally, KO/DMEM has been enriched
with foetal bovine serum (FBS) to stimulate cell proliferation due to the presence of growth factors. The routine
FBS used for mouse ESC (mESC) culture may not be
suitable for chicken stem cell growth; however, FBS cannot be completely replaced by chicken serum since the
foetal environment from which the FBS is derived is rich
in growth factors (Horiuchi et al. 2006). Normally, it is
preferred to keep both FBS and chicken serum at −70°C
rather than 4°C (Pinkert 2014). One of the fundamental
problems related to FBS or chicken serum is that both of
them are highly complex containing unknown compounds
including self-renewal and differentiation-inducing factors
(Skottman and Hovatta 2006). All serums often have
batch to batch and lot to lot variation that could affect
in vitro chicken stem cell propagation (Stein 2007).
Hence, the optimisation of a serum-free culture medium
would be a suitable solution for these problems (Amit
et al. 2004; Brunner et al. 2010). The commercial protein
supplements such as knockout serum replacement (KSR)
are often used in mammalian culture systems to replace
FBS (Lin and Talbot 2011; Desai et al. 2015). KSR is also
useful for proliferation and maintaining the undifferentiated state of long-term cultured chicken PGCs (Naito
et al. 2015).
Feeder cells in chicken stem cell culture
The feeder layer is an important factor for derivation and
maintenance of chicken stem cells. The establishment of
cESCs was first described by using a Sandos inbred mouse
(SIM)-derived 6-thioguanine- and ouabain-resistant (STO)
cell line (mouse fibroblast cell line) feeder cells in a FBScontaining culture medium (Pain et al. 1996). Moreover, the
first cEGCs were derived in the presence of chicken
embryonic fibroblast (CEF) cells as the feeder layer (Park
and Han 2000). Previous studies suggested that embryonic
fibroblasts are capable of secreting paracrine factors including chicken leukaemia inhibitory factor (LIF) and basic
fibroblast growth factor (bFGF); both factors inhibit differentiation of germ cells and increase their proliferation (De
Felici et al. 2005; Tang et al. 2007). Mouse embryonic
fibroblast cells (MEF) play a central role for derivation of
ciPSCs (Lu et al. 2011). It seems that mitotically inactivated
MEF cells are able to secret LIF as a factor that supports the
self-renewal property of mouse stem cells (Lin and Talbot
2011), but its use was not beneficial for the culture of cESCs
(van de Lavoir and Mather-Love 2006). Utilisation of mitotically inactivated STO cells as feeder cells leads to the
augmentation of alkaline phosphatase positive cESCs colonies and can also increase the proliferation rate of PGCs,
but cEGCs are unable to proliferate on STO cells in culture
(Park and Han 2000). Although, CEF has been successfully
used for cEGC expansion and was one of the best substrates
for proliferation of PGCs (Tang et al. 2007), it cannot
support the growth of cESCs and ciPSCs (van de Lavoir
and Mather-Love 2006). cESCs can be grown on Buffalo rat
liver (BRL) cells as well (van de Lavoir et al. 2006), but they
attach more firmly to BRL layer compared to STO cells.
However, it should be noticed that high concentrations of
STO cells can impede the growth of cESCs and it is essential
to seed these feeder cells at low concentrations (van de
Lavoir et al. 2006).
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BRITISH POULTRY SCIENCE
3
Figure 1. Derivation and culture of chicken stem cells from various developmental stages. Chicken ESCs derived from the blastodermal cells at embryonic stage
X. In the culture, cESCs grow on the STO feeder layer and attach to each other with visible borders. PGCs have the ability to be reprogrammed into EGC colonies
(from 5.5–6 d old embryo) on the CEF feeder layer. Chicken iPSCs have been generated by in vitro reprogramming of chicken fibroblast cells (from 8–12 d old
embryo) on MEF feeder layer.
ESCs: embryonic stem cells; STO: mouse fibroblast cell line; CEF: chicken embryonic fibroblast cells; MEF: mouse embryonic fibroblast cells; EGCs: embryonic germ cells; iPSCs: induced
pluripotent stem cells.
The presence of conditioned medium for chicken stem
cell culture is also important. Conditioned medium derived
from STO cells and BRL cells can maintain the self-renewal
property of cESCs and cPGCs but not cEGCs or ciPSCs
(Petitte et al. 2004). Taken together, the employment of
feeder cells in chicken stem cells cultures can provide an
appropriate attachment substrate and they also release the
necessary growth factors to the culture media (Lavial and
Pain 2010). However, some released factors may have unfavourable effects on chicken stem cell self-renewal or on the
undifferentiated state. Moreover, derivation and maintenance of chicken stem cells in the presence of a feeder
layer results in variation and ambiguity of culture composition which can affect the final characteristics of these cells
(Intarapat and Stern 2013). It has been suggested that a
feeder-free condition eliminates the influence of unknown
factors and animal pathogens on optimisation procedures
required for highly efficient and large-scale generation of
functional stem cells (Kraus et al. 2011). Feeder-free culture
of human stem cells is feasible on matrigel that contains
laminin, collagen type IV and other substances that are each
part of the extracellular matrix (ECM) including synthetic
laminin or fibronectin (Desai et al. 2015). To date, longterm feeder-free culture of cESCs and ciPSCs has been
conducted successfully (Reiter et al. 2014). For this purpose,
chicken stem cells were cultured on matrigel or gelatincoated dishes, the step-wise reduction of serum and growth
factors was done and the cells were transferred to the
suspension culture dish on a shaker in optimum culture
conditions (Madeline et al. 2015; Shittu et al. 2016).
However, the functional roles of natural or synthetic ECM
in controlling stem cell behaviour are not clear and they
cannot be a permanent substitute for feeder cells in the
culture system (Hayashi and Furue 2016). Derivation and
culture of chicken stem cells from various developmental
stages are shown in Figure 1 (Park and Han 2000; Lavial
and Pain 2010; Yu et al. 2014).
Culture medium supplements
The distinct role of growth factors in derivation and maintenance of chicken stem cells is undisputed. For instance,
the presence of several growth factors such as chicken stem
cell factor (SCF), bFGF, mouse IL-6, human IL-11, human
insulin-like growth factor-1 (hIGF-1) and mouse LIF
(mLIF) has been shown to be necessary for chicken stem
cell proliferation (Pain et al. 1996). Several research groups
have reported successful use of SCF, bFGF and mLIF in
chicken PGC and EGC cultures (Park and Han 2000). LIF is
a member of the cytokine family that by activation of the
JAK/STAT pathway can result in long-term propagation of
chicken stem cells (Petitte et al. 2004). Mammalian cytokines including human and mouse LIF (Petitte et al. 2004)
4
M. FARZANEH ET AL.
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and also avian cytokine such as chicken LIF (Nakano et al.
2011) are able to maintain chicken stem cells in an undifferentiated state. The role of other signalling pathways in
maintenance of an undifferentiated state of these cells is not
fully understood. bFGF is a key growth factor that turns the
MEK/ERK signalling pathway on and is required to maintain proliferation-associated factors in chicken PGCs
(Whyte et al. 2015). SCF also has an important role as a
cofactor together with bFGF, since its presence in culture is
critical for propagation of PGCs and its effect without bFGF
is not significant (Miyahara et al. 2016). It seems that the
effect of chicken SCF, specifically in its soluble form, which
was extracted from the BRL cell line, can enhance proliferation rate more than the membrane-bound SCF (Miyahara
et al. 2016). Insulin-like growth factor (IGF) is another
growth factor which activates the insulin pathway and
along with FGF increases self-renewal of chicken stem
cells (Jean et al. 2013). Most probably, a central network
of pluripotency is conserved between animals and the role
of one or two pathways might be highlighted in one but
reduced in the others (Jean et al. 2013).
Suspension culture of chicken stem cells for largescale production
Chicken stem cells are master cells having the potential to
develop cell-based transgenic birds and vaccines requiring
large-scale cell technologies (Kraus et al. 2011; Genzel 2015;
Farzaneh et al. 2017b). However, scaling up the conventional adherent chicken stem cell cultures is challenging and
labour intensive (Sart et al. 2014). Therefore, development
of a suspension cell culture process for these stem cells can
be a very important step for increasing their dynamic culture (Kirouac and Zandstra 2008). Although current
chicken stem cell culture dependency on feeder cells and
serum has created major problems with suspension culture
systems, this issue was recently addressed by the Vivalis
Company (Bushell-Embling 2012). These authors demonstrated that suspension culture of chicken and duck ESCs
(named as EBx and EB66, respectively) has a considerable
potential for production of a variety of viral vaccines and
therapeutic proteins in high yield (Olivier et al. 2010;
Mehtali et al. 2015). EB66 cells can be maintained in a
serum-free medium named EX-CELL EBx-GRO-I that is
animal-component-free (Olivier et al. 2010). Hence, an efficient cell-based system has been provided and it can be
applied as a safe, cheap and fast method for vaccine production (Merten et al. 2014). The optimum cell culture to
maintain chicken stem cells involved the use of defined
medium and dynamic culture in feeder and serum-free
conditions is shown in Figure 2 (Olivier et al. 2010;
Mehtali et al. 2015). Replacement of feeder and serum
culture conditions with defined constituents that are free
of animal-derived components has advanced the research
on large-scale chicken stem cell culture for production of
transgenic birds and vaccines (Mehtali et al. 2015).
Figure 2. Optimisation of culture conditions for suspension culture of chicken
stem cells. Strategies for generating large-scale cultures using feeder-free and
serum-free suspension culture.
conditions for establishment of long-term culture of chicken
stem cells and different methods have been used to create
defined culture conditions. However, serum-free and feederfree culture methods for these cells are preferable for reducing
or eliminating undefined factors. The establishment of chicken
stem cell culture systems offers an important advance for
genetic, developmental and vaccine manufacture studies.
Acknowledgement
The authors would like to thank staff at the Royan Institute for Stem
Cell Biology and Technology, Department of Stem Cells and
Developmental Biology. The authors declare that there is no conflict
of interest.
Disclosure statement
No potential conflict of interest was reported by the authors.
Conclusion
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