High-Level Expression of Recombinant IgG in the Human Cell Line
PER.C6
David Jones, Nathalie Kroos, Regina Anema, Bart van Montfort, Andre Vooys,
Sven van der Kraats, Esmeralda van der Helm, Shirley Smits, Jan Schouten,
Kirsten Brouwer, Fija Lagerwerf, Patrick van Berkel, Dirk-Jan Opstelten,
Ton Logtenberg, and Abraham Bout*
Crucell, Archimedesweg 4, P.O. Box 2048, 2301 CA Leiden, The Netherlands
The number of therapeutic monoclonal antibodies in production is expected to rise
rapidly in the next few years. As a result, there is much focus on the optimization of
antibody expression platforms. Several issues are important including the speed of
transition from bench to manufacturing, yield of IgG, and quality (particularly of the
glycan structures present on immunoglobulins). We have characterized the human
cell line PER.C6 for its ability to produce recombinant IgG. Production yields are still
being optimized, but in nonfed batch culture, PER.C6 is able to grow to a cell density
of 5 × 10
6
cells/mL and produce 300-500 mg/L IgG; this is likely to increase
significantly in fed batch cultures. The generation of antibody-producing cell lines is
fast, as rounds of amplification of inserted genes are not required for high production
yields. The gene copy number of inserted genes is in the region of 1-10 copies per
genome. In addition, PER.C6 is a human cell line, and so does not add glycans, which
are immunogenic in humans. A core fucose molecule is essentially always present,
and galactose residues are present at a physiological level (0, 1, and 2 galactose residues
per glycan are present at a ratio of 1:2:1). No hybrid or high-mannose structures are
seen.
Introduction
Over the past few years, great progress has been made
in monoclonal antibody technology (1). There are cur-
rently around 10 monoclonal antibodies approved as
therapeutics, and a great deal more are in various stages
of clinical testing. One reason for this sudden explosion
is the development of new technologies which allow the
generation of fully human antibodies, including antibody
phage display and transgenic mice (which contain in their
chromosome key sequences of human antibody genes (2-
4)). Thus, fully human antibodies lacking mouse se-
quences can now be made.
Antibodies are also glycoproteins, and IgG1 contains
a conserved N-glycosylation site at asparagine 297 in the
constant region of the molecule. The most complete
glycan structure found on an IgG is shown in Figure 1;
however, glycans are heterogeneous. In human serum,
almost all IgGs contain a biantennary structure with a
core fucose. A minor portion (about 10-20%) of these
glycans contain a bisecting N-acetylglucosamine, and
levels of sialylation have been estimated at 5-20%. In
addition, approximately 25% of the structures contain no
galactose, 50% contain one galactose residue, and 25%
contain two galactose residues (5). The role these glycans
play is not fully understood, but the presence of bisecting
N-acetylglucosamine appears to increase binding to Fcγ
receptors, and galactosylation appears to facilitate in-
teraction with complement (6-10).
There are also differences in the nature of the glycan
structures present on IgGs in different mammalian
species (5). This becomes important when antibodies for
human therapy are produced in nonhuman cell lines, for
reasons of optimal biological activity and potential im-
munogenicity (11). It is known that, in some instances,
NS0 cells (a mouse myeloma cell line) add a Gal R(1-3)
Gal structure to IgG glycans (12); this structure does not
exist in humans, and it has been estimated that up to
1% of circulating antibody in humans is directed against
this moiety (13). In addition, some cell lines add high-
mannose or hybrid structures (14).
Production systems for full-length antibodies include
expression in mammalian cell lines grown in bioreactors
as well as transgenic systems such as plants and larger
animals. Important parameters that drive selection of the
most optimal expression system for a particular antibody
are product quality and quantity, safety issues, time to
clinic and market, and economic considerations such as
cost of goods and regulatory issues. There is an urgency
for further development and optimization of existing
technology but also for novel expression technology,
* To whom correspondence should be addressed. Phone: +31
(0)71 524 8701. Fax: +31 (0)71 524 8702. E-mail: a.bout@crucell.com.
Figure 1. Structure of the most complete glycan found at the
conserved N-linked glycosylation site of IgG1. GlcNAc ) N-
acetylglucosamine, Man ) mannose, Fuc ) fucose, Gal )
galactose, and Sia ) sialic acid.
163 Biotechnol. Prog. 2003, 19, 163-168
10.1021/bp025574h CCC: $25.00 © 2003 American Chemical Society and American Institute of Chemical Engineers
Published on Web 01/14/2003