Cited by 786Viral Infectious Diseases and Gene Expression in InsectsFungal and yeast genetics researchMonoclonal and Polyclonal Antibodies Research

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The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line

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Xu, Xun, Nagarajan, Harish, Lewis, Nathan E, Pan, Shengkai, Cai, Zhiming, Liu, Xin, Chen, Wenbin, Xie, Min, Wang, Wenliang, Hammond, Stephanie, Andersen, Mikael R, Neff, Norma, Passarelli, Benedetto, Koh, Winston, Fan, H Christina, Wang, Jianbin, Gui, Yaoting, Lee, Kelvin H, Betenbaugh, Michael J, Quake, Stephen R, Famili, Iman, Palsson, Bernhard O, Wang, Jun·2011·Nature Biotechnology

DOI 10.1038/nbt.1932PMC PMC3164356

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Abstract

Since 1987, immortalized cells from the ovary of a Chinese hamster have been the workhorse for producing recombinant therapeutics, including monoclonal antibodies, blood factors, hormones, growth factors and enzymes. Xu et al. provide the genome sequence of the ancestral CHO-K1 cell line, which should aid in the optimization of current production cell lines. Chinese hamster ovary (CHO)–derived cell lines are the preferred host cells for the production of therapeutic proteins. Here we present a draft genomic sequence of the CHO-K1 ancestral cell line. The assembly comprises 2.45 Gb of genomic sequence, with 24,383 predicted genes. We associate most of the assembled scaffolds with 21 chromosomes isolated by microfluidics to identify chromosomal locations of genes. Furthermore, we investigate genes involved in glycosylation, which affect therapeutic protein quality, and viral susceptibility genes, which are relevant to cell engineering and regulatory concerns. Homologs of most human glycosylation-associated genes are present in the CHO-K1 genome, although 141 of these homologs are not expressed under exponential growth conditions. Many important viral entry genes are also present in the genome but not expressed, which may explain the unusual viral resistance property of CHO cell lines. We discuss how the availability of this genome sequence may facilitate genome-scale science for the optimization of biopharmaceutical protein production.

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De novo assembly of human genomes with massively parallel short read sequencing
Li, R., Zhu, H., Ruan, J., Qian, W., Fang, X., Shi, Z., Li, Y., Li, S., Shan, G., Kristiansen, K., et al. (2010) · Genome Research · doi:10.1101/gr.097261.109 · Cited by 2,926
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Gibbs, R. A., Weinstock, G. M., Metzker, M. L., Muzny, D. M., Sodergren, E. J., Scherer, S. E., Scott, G., Steffen, D. L., Worley, K. C., Burch, P. E., et al. (2004) · Nature · doi:10.1038/nature02426 · Cited by 2,170
Production of recombinant protein therapeutics in cultivated mammalian cells
Wurm, F. M. (2004) · Nature Biotechnology · doi:10.1038/nbt1026 · Cited by 2,032 · cited 9×
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Assembly algorithms for next-generation sequencing data
Miller, J. R., Koren, S., & Sutton, G. G. (2010) · Genomics · doi:10.1016/j.ygeno.2010.03.001 · Cited by 1,186
Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol
Yim, H. H., Haselbeck, R. J., Niu, W., Pujol-Baxley, C., Burgard, A. P., Boldt, J., Khandurina, J., Trawick, J. D., Osterhout, R. E., Stephen, R., et al. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.580 · Cited by 1,114
The role of sialic acid in determining the survival of glycoproteins in the circulation
Morell, A. G., Gregoriadis, G., Scheinberg, I. H., Hickman, J., & Ashwell, G. (1971) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)76994-4 · Cited by 1,072
A Novel Role for 3-O-Sulfated Heparan Sulfate in Herpes Simplex Virus 1 Entry
Shukla, D., Liu, J., Blaiklock, P., Shworak, N. W., Bai, X., Esko, J. D., Cohen, G. H., Eisenberg, R. J., ROSENBERG, R. D., & Spear, P. G. (1999) · Cell · doi:10.1016/s0092-8674(00)80058-6 · Cited by 1,053
Post-translational modifications in the context of therapeutic proteins
Walsh, G., & Jefferis, R. (2006) · Nature Biotechnology · doi:10.1038/nbt1252 · Cited by 1,007 · cited 1×
“For some of these proteins, differential glycosylation can substantially affect functional activity and/or in vivo circulatory half-lif”
Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor
Kohany, O., Gentles, A. J., Hankus, L., & Jurka, J. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-474 · Cited by 897

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Khan, A. H., Bayat, H., Rajabibazl, M., Sabri, S., & Rahimpour, A. (2016) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-016-2172-7 · Cited by 30
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Rajendra, Y., Balasubramanian, S., Peery, R. B., Swartling, J. R., McCracken, N. A., Norris, D. L., Frye, C. C., & Barnard, G. C. (2017) · Biotechnology Progress · doi:10.1002/btpr.2447 · Cited by 30
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Qiu, Y., Jones, N., Busch, M., Pan, P., Keegan, J., Zhou, W., Plavsic, M., Hayes, M., McPherson, J. M., Edmunds, T., et al. (2013) · Biotechnology and Bioengineering · doi:10.1002/bit.24791 · Cited by 29
CHO Glycosylation Mutants as Potential Host Cells to Produce Therapeutic Proteins with Enhanced Efficacy
Zhang, P., Chan, K. F., Haryadi, R., Bardor, M., & Song, Z. (2012) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2012_163 · Cited by 31
CHO Cell Line Development and Engineering via Site-specific Integration: Challenges and Opportunities
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Lau, S. S., Tang, T., Odeh, L., Bokenkamp, K., Wagner, E. D., Plewa, M. J., & Mitch, W. A. (2023) · Environmental Science & Technology Letters · doi:10.1021/acs.estlett.3c00655 · Cited by 29
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Authors: Xu, X., Nagarajan, H., Lewis, N. E., Pan, S., Cai, Z., Liu, X., Chen, W., Xie, M., Wang, W., Hammond, S., Andersen, M. R., Neff, N., Passarelli, B., Koh, W., Fan, H. C., Wang, J., Gui, Y., Lee, K. H., Betenbaugh, M. J., Quake, S. R., Famili, I., Palsson, B. O., & Wang, J.
Affiliations: BGI Group (China) (CN)
Peking University Shenzhen Hospital (CN)
Delaware Biotechnology Institute (US)
Technical University of Denmark (DK)
Howard Hughes Medical Institute (US)
Johns Hopkins University (US)
Corresponding author: Wang, Jianbin
Wang, Jun
ORCID: Xu, Xun
Lewis, Nathan E
Pan, Shengkai
Cai, Zhiming
Liu, Xin
Chen, Wenbin
Xie, Min
Wang, Wenliang
Andersen, Mikael R
Neff, Norma
Koh, Winston
Fan, H Christina
Wang, Jianbin
Gui, Yaoting
Lee, Kelvin H
Betenbaugh, Michael J
Quake, Stephen R
Wang, Jun
Venue: Nature Biotechnology
Publisher: Springer Science and Business Media LLC
Published: 2011-08
Volume: 29
Issue: 8
Pages: 735-741
ISSN: 0733-222X (ISSN-L)
1087-0156
1546-1696
DOI: 10.1038/nbt.1932
PMC: PMC3164356
OpenAlex: W2093343938
Cited by: 785
References: 53
Citations by year: 2026: 22 · 2025: 25 · 2024: 37 · 2023: 35 · 2022: 39 · 2021: 58 · 2020: 38 · 2019: 45 · 2018: 78 · 2017: 57 · 2016: 59 · 2015: 77 · 2014: 79 · 2013: 64 · 2012: 53
FWCI: 27.29
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/3.0/ (tdm)
creativecommons.org/licenses/by-nc-sa/3.0/ (vor)
Locations: Nature Biotechnology (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion)
Funders: Novo Nordisk Fonden (NNF10CC1016517)
National Cancer Institute (R44CA139977)
National Center for Research Resources (P20RR016472)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Viral Infectious Diseases and Gene Expression in Insects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Immunology and Microbiology › Immunology › Monoclonal and Polyclonal Antibodies Research
Keywords: CHO-K1 cells, CHO cells, draft genome sequence, therapeutic protein production, monoclonal antibodies, virus resistance, cell line engineering, genome assembly, gene expression
MeSH terms: Animals, Chromosome Mapping, Cricetulus, Glycosylation, Cricetinae, Models, Biological, Molecular Sequence Data, CHO Cells, Genome, Sequence Analysis, DNA, Genomics

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The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line

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