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BioMed Research International
Volume 2015, Article ID 504831, 11 pages
http://dx.doi.org/10.1155/2015/504831
Review Article

Current and Emerging Cell Culture Manufacturing Technologies for Influenza Vaccines

Department of Bioengineeringt, McGill University, Macdonald Engineering Building, 817 Sherbrooke Street W, Montreal, QC, Canada H3A 0C3

Received 3 December 2014; Revised 5 February 2015; Accepted 16 February 2015

Academic Editor: Gregory Tannock

Copyright © 2015 Ernest Milián and Amine A. Kamen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Citations to this Article [55 citations]

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  • Aziza P. Manceur, and Amine A. Kamen, “Critical review of current and emerging quantification methods for the development of influenza vaccine candidates,” Vaccine, 2015. View at Publisher · View at Google Scholar
  • Irina Isakova-Sivak, and Larisa Rudenko, “Safety, immunogenicity and infectivity of new live attenuated influenza vaccines,” Expert Review of Vaccines, vol. 14, no. 10, pp. 1313–1329, 2015. View at Publisher · View at Google Scholar
  • Scott A. Leddon, Katherine A. Richards, John J. Treanor, and Andrea J. Sant, “Abundance and specificity of influenza reactive circulating memory follicular helper and non-follicular helper CD4 T cells in healthy adults,” Immunology, 2015. View at Publisher · View at Google Scholar
  • Lise Besnard, Virginie Fabre, Michael Fettig, Elina Gousseinov, Yasuhiro Kawakami, Nicolas Laroudie, Claire Scanlan, and Priyabrata Pattnaik, “Clarification of vaccines: An overview of membrane based technology trends and best practices,” Biotechnology Advances, 2015. View at Publisher · View at Google Scholar
  • Ming Chu, Lan Xu, Ming-bo Zhang, Zheng-yun Chu, and Yue-dan Wang, “Role of Baicalin in Anti-Influenza Virus A as a Potent Inducer of IFN-Gamma,” BioMed Research International, vol. 2015, pp. 1–11, 2015. View at Publisher · View at Google Scholar
  • Takato Odagiri, Eri Nobusawa, Yasushi Suzuki, and Masato Tashiro, “Development of an influenza A master virus for generating high-growth reassortants for A/Anhui/1/2013(H7N9) vaccine production in qualified MDCK cells,” PLoS ONE, vol. 11, no. 7, 2016. View at Publisher · View at Google Scholar
  • Lisa M. Dunkle, and Ruvim Izikson, “Recombinant hemagglutinin influenza vaccine provides broader spectrum protection,” Expert Review of Vaccines, pp. 1–10, 2016. View at Publisher · View at Google Scholar
  • Alina Venereo-Sanchez, Amine Kamen, Melanie Simoneau, Antoine Caron, Wangxue Chen, Renald Gilbert, Parminder Chahal, Sven Ansorge, Xuguang Li, and Olivier Henry, “Hemagglutinin and neuraminidase containing virus-like particles produced in HEK-293 suspension culture: An effective influenza vaccine candidate,” Vaccine, vol. 34, no. 29, pp. 3371–3380, 2016. View at Publisher · View at Google Scholar
  • Muhammad Asif Zahoor, Mohsin Khurshid, Rabia Qureshi, Aneeqa Naz, and Muhammad Shahid, “Cell culture-based viral vaccines: current status and future prospects,” Future Virology, 2016. View at Publisher · View at Google Scholar
  • Priyadharshini Devarajan, Bianca Bautista, Allen M. Vong, Karl Kai McKinstry, Tara M. Strutt, and Susan L. Swain, “New Insights into the Generation of CD4 Memory May Shape Future Vaccine Strategies for Influenza,” Frontiers in Immunology, vol. 7, 2016. View at Publisher · View at Google Scholar
  • Kripa Ram, Diane Hatton, Sanjeev Ahuja, Jean Bender, Alan Hunter, and Richard Turner, “Protein Production in Eukaryotic Cells,” Protein Therapeutics, vol. 21, pp. 1–39, 2016. View at Publisher · View at Google Scholar
  • Aitor Nogales, and Luis Martínez-Sobrido, “Reverse Genetics Approaches for the Development of Influenza Vaccines,” International Journal of Molecular Sciences, vol. 18, no. 1, pp. 20, 2016. View at Publisher · View at Google Scholar
  • Ralf Pörtner, Uwe Jandt, and An-Ping Zeng, “Cell Culture Technology,” Industrial Biotechnology, pp. 129–158, 2016. View at Publisher · View at Google Scholar
  • Kristin G-I Mohn, Ingrid Smith, Haakon Sjursen, and Rebecca Cox, “Immune responses after live attenuated influenza vaccination,” Human Vaccines & Immunotherapeutics, pp. 00–00, 2017. View at Publisher · View at Google Scholar
  • Peggy Riese, and Carlos A. Guzmán, “Roads to advanced vaccines: influenza case study,” Microbial Biotechnology, 2017. View at Publisher · View at Google Scholar
  • Sofia B. Carvalho, Mafalda G. Moleirinho, David Wheatley, John Welsh, René Gantier, Paula M. Alves, Cristina Peixoto, and Manuel J. T. Carrondo, “Universal label-free in-process quantification of influenza virus-like particles,” Biotechnology Journal, pp. 1700031, 2017. View at Publisher · View at Google Scholar
  • Johannes Khinast, Jukka Rantanen, Alois Jungbauer, and Nikolaus Hammerschmidt, “Integrated Continuous Manufacturing of Biopharmaceuticals,” Continuous Manufacturing of Pharmaceuticals, pp. 247–281, 2017. View at Publisher · View at Google Scholar
  • Eunbi Yi, Jinsoo Oh, Ngoc Q. Giao, Soohwan Oh, and Se-Ho Park, “Enhanced production of enveloped viruses in BST-2-deficient cell lines,” Biotechnology and Bioengineering, 2017. View at Publisher · View at Google Scholar
  • Lisa M. Dunkle, Ruvim Izikson, Peter Patriarca, Karen L. Goldenthal, Derek Muse, Janice Callahan, and Manon M.J. Cox, “Efficacy of Recombinant Influenza Vaccine in Adults 50 Years of Age or Older,” New England Journal of Medicine, vol. 376, no. 25, pp. 2427–2436, 2017. View at Publisher · View at Google Scholar
  • Aziza P. Manceur, Wei Zou, Anne Marcil, Eric Paquet, Christine Gadoury, Bozena Jaentschke, Xuguang Li, Emma Petiot, Yves Durocher, Jason Baardsnes, Manuel Rosa-Calatrava, Sven Ansorge, and Amine A. Kamen, “Generation of monoclonal pan-hemagglutinin antibodies for the quantification of multiple strains of influenza,” Plos One, vol. 12, no. 6, pp. e0180314, 2017. View at Publisher · View at Google Scholar
  • Ernest Milián, Thomas Julien, Rafael Biaggio, Alina Venereo-Sanchez, Johnny Montes, Aziza P. Manceur, Sven Ansorge, Emma Petiot, Manuel Rosa-Calatrava, and Amine Kamen, “Accelerated mass production of influenza virus seed stocks in HEK-293 suspension cell cultures by reverse genetics,” Vaccine, 2017. View at Publisher · View at Google Scholar
  • Sofia B Carvalho, A Raquel Fortuna, Michael W Wolff, Cristina Peixoto, Paula M Alves, Udo Reichl, and Manuel JT Carrondo, “Purification of influenza virus-like particles using sulfated cellulose membrane adsorbers,” Journal of Chemical Technology & Biotechnology, 2017. View at Publisher · View at Google Scholar
  • Bonnie C Wintle, Christian R Boehm, Catherine Rhodes, Jennifer C Molloy, Piers Millett, Laura Adam, Rainer Breitling, Rob Carlson, Rocco Casagrande, Malcolm Dando, Robert Doubleday, Eric Drexler, Brett Edwards, Tom Ellis, Nicholas G Evans, Richard Hammond, Jim Haseloff, Linda Kahl, Todd Kuiken, Benjamin R Lichman, Colette A Matthewman, Johnathan A Napier, Seán S ÓhÉigeartaigh, Nicola J Patron, Edward Perello, Philip Shapira, Joyce Tait, Eriko Takano, and William J Sutherland, “A transatlantic perspective on 20 emerging issues in biological engineering,” eLife, vol. 6, 2017. View at Publisher · View at Google Scholar
  • Nicholas C. Wu, Seth J. Zost, Andrew J. Thompson, David Oyen, Corwin M. Nycholat, Ryan McBride, James C. Paulson, Scott E. Hensley, and Ian A. Wilson, “A structural explanation for the low effectiveness of the seasonal influenza H3N2 vaccine,” PLOS Pathogens, vol. 13, no. 10, pp. e1006682, 2017. View at Publisher · View at Google Scholar
  • M. Butler, and Ing. U. Reichl, “Animal Cell Expression Systems,” 2017. View at Publisher · View at Google Scholar
  • Yan-Jun Liu, Shiaw-Lin Wu, Kerry R. Love, and William S. Hancock, “ Characterization of Site-Specific Glycosylation in Influenza A Virus Hemagglutinin Produced by Spodoptera frugiperda Insect Cell Line ,” Analytical Chemistry, 2017. View at Publisher · View at Google Scholar
  • Ilseob Lee, Jin Il Kim, Sehee Park, Joon-Yong Bae, Kirim Yoo, Soo-Hyeon Yun, Joo-Yeon Lee, Kisoon Kim, Chun Kang, and Man-Seong Park, “Single PA mutation as a high yield determinant of avian influenza vaccines,” Scientific Reports, vol. 7, pp. 40675, 2017. View at Publisher · View at Google Scholar
  • Soyoung Kim, Jonggul Lee, and Eunok Jung, “Mathematical model of transmission dynamics and optimal control strategies for 2009 A/H1N1 influenza in the Republic of Korea,” Journal of Theoretical Biology, vol. 412, pp. 74–85, 2017. View at Publisher · View at Google Scholar
  • Xiaofeng Kevin Han, Ulrike Becken, and Ma Sha, “Vero Perfusion, Packed-Bed Vessels Intensify Vaccine Production,” Genetic Engineering and Biotechnology News, vol. 38, no. 15, pp. S16–S18, 2018. View at Publisher · View at Google Scholar
  • Chi Eun Oh, Ui-Yoon Choi, Byung Wook Eun, Taek Jin Lee, Ki Hwan Kim, Dong Ho Kim, Nam Hee Kim, Dae Sun Jo, Sun Hee Shin, Kyung-Ho Kim, Hun Kim, and Yun-Kyung Kim, “A Randomized, Double-blind, Active-controlled Clinical Trial of a Cell Culture-derived Inactivated Trivalent Influenza Vaccine (NBP607) in Healthy Children 6 Months Through 18 Years of Age,” The Pediatric Infectious Disease Journal, vol. 37, no. 6, pp. 605–611, 2018. View at Publisher · View at Google Scholar
  • Alberto Pérez Rubio, and Jose María Eiros, “Cell culture-derived flu vaccine: Present and future,” Human Vaccines & Immunotherapeutics, pp. 1–9, 2018. View at Publisher · View at Google Scholar
  • Julie A Fogarty, and James R Swartz, “The exciting potential of modular nanoparticles for rapid development of highly effective vaccines,” Current Opinion in Chemical Engineering, vol. 19, pp. 1–8, 2018. View at Publisher · View at Google Scholar
  • Daniela S. Rajão, and Daniel R. Pérez, “Universal Vaccines and Vaccine Platforms to Protect against Influenza Viruses in Humans and Agriculture,” Frontiers in Microbiology, vol. 9, 2018. View at Publisher · View at Google Scholar
  • Zoltán Kis, Robin Shattock, Nilay Shah, and Cleo Kontoravdi, “Emerging Technologies for Low‐Cost, Rapid Vaccine Manufacture,” Biotechnology Journal, pp. 1800376, 2018. View at Publisher · View at Google Scholar
  • Omar Khan, Chandra Mouli R. Madhuranthakam, Patrick Farrell, Peter Douglas, Heron Lau, and Jacob Sun, “Optimized PID controller for an industrial biological fermentation process,” Journal of Process Control, vol. 71, pp. 75–89, 2018. View at Publisher · View at Google Scholar
  • Lei Deng, and Bao-Zhong Wang, “A Perspective on Nanoparticle Universal Influenza Vaccines,” ACS Infectious Diseases, 2018. View at Publisher · View at Google Scholar
  • Nicole Darricarrère, Svetlana Pougatcheva, Xiaochu Duan, Rebecca S. Rudicell, Te-Hui Chou, Joshua DiNapoli, Ted M. Ross, Tim Alefantis, Thorsten U. Vogel, Harry Kleanthous, Chih-Jen Wei, and Gary J. Nabel, “Development of a Pan-H1 Influenza Vaccine,” Journal of Virology, vol. 92, no. 22, 2018. View at Publisher · View at Google Scholar
  • Feng Wen, Lei Li, Nan Zhao, Meng-Jung Chiang, Hang Xie, Jim Cooley, Richard Webby, Peng George Wang, and Xiu-Feng Wan, “A Y161F Hemagglutinin Substitution Increases Thermostability and Improves Yields of 2009 H1N1 Influenza A Virus in Cells,” Journal of Virology, vol. 92, no. 2, pp. e01621-17, 2018. View at Publisher · View at Google Scholar
  • Emma Rey-Jurado, Felipe Tapia, Natalia Muñoz-Durango, Margarita K. Lay, Leandro J. Carreño, Claudia A. Riedel, Susan M. Bueno, Yvonne Genzel, and Alexis M. Kalergis, “Assessing the Importance of Domestic Vaccine Manufacturing Centers: An Overview of Immunization Programs, Vaccine Manufacture, and Distribution,” Frontiers in Immunology, vol. 9, 2018. View at Publisher · View at Google Scholar
  • Nita Madhav, Ben Oppenheim, Mark Gallivan, Prime Mulembakani, Edward Rubin, and Nathan Wolfe, “Pandemics: Risks, Impacts, and Mitigation,” Disease Control Priorities, Third Edition (Volume 9): Improving Health and Reducing Poverty, pp. 315–345, 2018. View at Publisher · View at Google Scholar
  • V. Zadorozhna, and N. Vynnyk, “Questions of bioethics and biosafety in the problem of biotechnology and use of vaccine for prevention of human infectious diseases,” Bulletin "Veterinary biotechnology", vol. 32, no. 1, pp. 459–465, 2018. View at Publisher · View at Google Scholar
  • Hari Pujar, and Mats Lundgren, “Modern Production Strategies in the Vaccine Industry,” Biopharmaceutical Processing, pp. 877–898, 2018. View at Publisher · View at Google Scholar
  • Shinya Yamada, Atsuhiro Yasuhara, and Yoshihiro Kawaoka, “Soluble Recombinant Hemagglutinin Protein of H1N1pdm09 Influenza Virus Elicits Cross-Protection Against a Lethal H5N1 Challenge in Mice,” Frontiers in Microbiology, vol. 10, 2019. View at Publisher · View at Google Scholar
  • Chia-Chun Lai, Tsai-Chuan Weng, Yu-Fen Tseng, Jen-Ron Chiang, Min-Shi Lee, and Alan Yung-Chih Hu, “Evaluation of novel disposable bioreactors on pandemic influenza virus production,” Plos One, vol. 14, no. 8, pp. e0220803, 2019. View at Publisher · View at Google Scholar
  • Mandy Gebauer, Hans C. Hürlimann, Martina Behrens, Thorsten Wolff, and Sven-Erik Behrens, “Subunit vaccines based on recombinant yeast protect against influenza A virus in a one-shot vaccination scheme,” Vaccine, 2019. View at Publisher · View at Google Scholar
  • Claudia Maria Trombetta, Serena Marchi, Ilaria Manini, Giacomo Lazzeri, and Emanuele Montomoli, “Challenges in the development of egg-independent vaccines for influenza,” Expert Review of Vaccines, pp. 1–14, 2019. View at Publisher · View at Google Scholar
  • Soyoung Kim, and Eunok Jung, “Prioritization of vaccine strategy using an age-dependent mathematical model for 2009 A/H1N1 influenza in the Republic of Korea,” Journal of Theoretical Biology, 2019. View at Publisher · View at Google Scholar
  • Alberto Perez-Rubio, and José María Eiros, “Quadrivalent cell culture influenza virus vaccine. Towards improving the efficacy of the influenza vaccine,” Medicina Clínica (English Edition), 2019. View at Publisher · View at Google Scholar
  • A. Raquel Fortuna, Sebastian van Teeffelen, Adrian Ley, Laura M. Fischer, Florian Taft, Yvonne Genzel, Louis Villain, Michael M. Wolff, and Udo Reichl, “Use of sulfated cellulose membrane adsorbers for chromatographic purification of cell cultured-derived influenza A and B viruses,” Separation and Purification Technology, 2019. View at Publisher · View at Google Scholar
  • Yugo Miyata, Shoko Tokumoto, Yoichiro Sogame, Ruslan Deviatiiarov, Jun Okada, Richard Cornette, Oleg Gusev, Elena Shagimardanova, Minoru Sakurai, and Takahiro Kikawada, “Identification of a novel strong promoter from the anhydrobiotic midge, Polypedilum vanderplanki, with conserved function in various insect cell lines,” Scientific Reports, vol. 9, no. 1, 2019. View at Publisher · View at Google Scholar
  • Alberto Perez-Rubio, and José María Eiros, “La vacuna tetravalente de cultivo celular: hacia la mejora de la eficacia de la vacuna de la gripe,” Medicina Clínica, 2019. View at Publisher · View at Google Scholar
  • Gwendal Gränicher, Juliana Coronel, Alexander Pralow, Pavel Marichal-Gallardo, Michael Wolff, Erdmann Rapp, Alexander Karlas, Volker Sandig, Yvonne Genzel, and Udo Reichl, “Efficient influenza A virus production in high cell density using the novel porcine suspension cell line PBG.PK2.1,” Vaccine, 2019. View at Publisher · View at Google Scholar
  • Sofia B. Carvalho, Ricardo Silva, Ana Sofia Moreira, Bárbara Cunha, João J. Clemente, Paula M. Alves, Manuel J.T. Carrondo, Alex Xenopoulos, and Cristina Peixoto, “Efficient filtration strategies for the clarification of influenza virus-like particles derived from insect cells,” Separation and Purification Technology, 2019. View at Publisher · View at Google Scholar
  • Natalia V. Menshutina, Elena V. Guseva, Ruslan R. Safarov, and Joseph Boudrant, “Modelling of hollow fiber membrane bioreactor for mammalian cell cultivation using computational hydrodynamics,” Bioprocess and Biosystems Engineering, 2019. View at Publisher · View at Google Scholar
  • Omar Khan, and Chandra Mouli R. Madhuranthakam, “Optimization of Robust Model Predictive Controllers for Second-Order Biological Processes Using Markov Chain Monte Carlo Techniques,” Industrial & Engineering Chemistry Research, 2019. View at Publisher · View at Google Scholar