Development of a Strategy of Influenza Virus
Separation Based on Pseudoaffinity
Chromatography on Short Monolithic Columns
I. Kalashnikova, N. Ivanova, and T. Tennikova*
Institute of Macromolecular Compounds, Russian Academy of Sciences, St. Petersburg, Russia
This research is devoted to the development and optimi-
zation of fine purification processes realized on short
monolithic columns (CIM disks), using influenza vaccine
and viruslike synthetic particles as model objects. The
pseudoaffinity mode of liquid chromatography has been
used as a tool for dynamic adsorption experiments.
Viruslike particles, close to the dimensions of influenza
viruses, were developed by means of main antigen of
influenza viruses (hemeagglutinin) covalent binding to the
outer aminated surface of synthetic latex particles. The
natural receptor analogues of sialic acid were used as
affinity ligands immobilized on the surface of the CIM disk
by different ways to achieve a high adsorption capacity.
Also, some other ligands were tested as possible candi-
dates for virus capturing. The affinity binding parameters
for influenza A virus were obtained by frontal elution
method at optimized chromatographic conditions and
immobilization schemes. The experimental data pointed
out the possibility of selective isolation of hemeagglutinin
from a mixture of vaccine proteins. The results obtained
by fast affinity chromatography have shown functional and
sterical correspondence viruslike synthetic models to
influenza viruses. Additionally, the optimization of chro-
matographic conditions allowed isolation of influenza
virus A while maintaining its virulence. The maximum
value of adsorption capacity was registered for a mono-
lithic disk, modified subsequently by chitosan and 2,6-
sialyllactose and found to be equal to 6.9 × 10
12
virions/
mL support.
Influenza remains, due to its annual death rate and potential
to cause pandemics, a major public health concern. The efforts
to control the annual spread of influenza have focused on
prophylactic vaccinations. Human influenza vaccines are tradition-
ally produced in embryonated hen’s eggs and specific cell cultures.
The latter crude material containing virus requires thorough
purification from cell components (the components of nonviral
origin) without lost of biological activity of antigenic determinates
during vaccine manufacturing.
Different modes of liquid chromatography, namely, ion ex-
change, size exclusion, and others, as well as their combination,
are widely used at influenza virus purification.
1-3
The most delicate
and highly selective virus isolation can be realized using affinity
chromatography. Recently obtained data illustrated that monolithic
material on the base of a copolymer of glycidyl methacrylate
(GMA) and ethylene glycol dimethacrylate (EDMA) seemed to
be suitable for construction of biorecognizing systems in two
formats,
4,5
both for isolation of viruslike particles by fast affinity
chromatography and for their sensitive detection (diagnostics)
using miccroarray technique. Besides that, the chromatography
on short methacrylate-based monolithic columns (Convective
Interaction Media, CIM, disks), demonstrating unique hydrody-
namic and separation properties,
6-8
seems to be preferable to
overcome many critical disadvantages of conventional separation
techniques concerning large bioobjects’ separation.
9-14
Because
of superior mass transfer and open porous structure (totally
permeable for a flowing liquid large pores), the monoliths will be
able to provide very fast biospecific pair formation involving viruses
that reduces the risk of product degradation.
It is known that the distinct terminal sialic acid species (N-
acetylneuraminic acid) on the cell membrane surface serves as a
hemeagglutinin-binding receptor to induce the penetration of the
interior of influenza viruses by membrane fusion.
15,16
In this
* To whom correspondence should be addressed. E-mail: tennikova@mail.ru.
(1) Kalbfuss, B.; Wolff, M.; Morenweiser, R.; Reichl, U. Biotechnol. Bioeng.
2007, 96, 932-944.
(2) Opitz, L.; Salaklang, J.; Bu ¨ttner, H.; Reichl, U.; Wolff, M. Vaccine 2007, 25,
939-947.
(3) Zhao, R.; Fang, C.; Yu, X.; Liu, Y.; Luo, J.; Shangguan, D.; Xiong, S.; Su, T.;
Liu, G. J. Chromatogr., A 2005, 1064, 59-66.
(4) Kalashnikova, I.; Ivanova, N.; Evseeva, T.; Menshikova, A.; Vlakh, E.;
Tennikova, T. J. Chromatogr. A 2007, 1144, 40-47.
(5) Kalashnikova, I.; Ivanova, N.; Tennikova, T. Anal. Chem. 2007, 9, 5173-
5181.
(6) Josic, Dj.; Buchacher, A. J. Biochem. Biophys. Methods 2001, 49, 153-174.
(7) Branovic, K.; Lattner, G.; Barut, M.; Strancar, A.; Josic, Dj.; Buchacher, A.
J. Immunol. Methods 2002, 271, 47-58.
(8) Jungbauer, A. J. Chromatogr. A 2005, 1065,3-12.
(9) Kramberger, P.; Glover, D.; Strancar, A. Am. Biotechnol. Lab. 2003, 21,
27-38.
(10) Branovic, K.; Forcic, D.; Ivancic, J.; Strancar, A.; Barut, M.; Kosutic-Gulija,
T.; Zgorelec, R.; Mazuran, R. J. Virol. Methods 2003, 110, 163-171.
(11) Kramberger, P.; Petrovic, N.; Strancar,, A.; Ravnikar, M. J. Virol. Methods
2004, 120, 51-57.
(12) Barut, M.; Podgornik, A.; Brne, P.; Strancar, A. J. Sep. Sci. 2005, 28, 1876-
1892.
(13) Williams, S.; Eccleston, M.; Slater, N. Biotechnol. Bioeng. 2005, 89, 783-
787.
(14) Kramberger, P.; Peterka, M.; Boben, J.; Ravnikar, M.; Strancar, A. J.
Chromatogr. A 2007, 1144, 143-149.
(15) Ito, T. Microbiol. Immunol. 2000, 44, 423-430.
(16) Gambaryan, A.; Piskarev, V.; Yamskov, I.; Sakharov, A.; Tuzikov, A.; Bovin,
N.; Nifant’ev, N.; Matrosovich, M. FEBS Lett. 1995, 366, 57-60.
Anal. Chem. 2008, 80, 2188-2198
2188 Analytical Chemistry, Vol. 80, No. 6, March 15, 2008 10.1021/ac702258t CCC: $40.75 © 2008 American Chemical Society
Published on Web 02/14/2008