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Cited by 70Viral Infectious Diseases and Gene Expression in InsectsGlycosylation and Glycoproteins ResearchTransgenic Plants and Applications

Glycoengineering in CHO cells: advances in systems biology

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Tejwani, Vijay, Andersen, Mikael R., Nam, Jong Hyun, Sharfstein, Susan T.·2018·Biotechnology Journal
DOI 10.1002/biot.201700234
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Abstract

For several decades, glycoprotein biologics have been successfully produced from Chinese hamster ovary (CHO) cells. The therapeutic efficacy and potency of glycoprotein biologics are often dictated by their post-translational modifications, particularly glycosylation, which unlike protein synthesis, is a non-templated process. Consequently, both native and recombinant glycoprotein production generate heterogeneous mixtures containing variable amounts of different glycoforms. Stability, potency, plasma half-life, and immunogenicity of the glycoprotein biologic are directly influenced by the glycoforms. Recently, CHO cells have also been explored for production of therapeutic glycosaminoglycans (e.g., heparin), which presents similar challenges as producing glycoproteins biologics. Approaches to controlling heterogeneity in CHO cells and directing the biosynthetic process toward desired glycoforms are not well understood. A systems biology approach combining different technologies is needed for complete understanding of the molecular processes accounting for this variability and to open up new venues in cell line development. In this review, we describe several advances in genetic manipulation, modeling, and glycan and glycoprotein analysis that together will provide new strategies for glycoengineering of CHO cells with desired or enhanced glycosylation capabilities.

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  • Combining glycomics and glycoproteomics methodologies with genomic, transcriptomic, proteomic and metabolomic data has proven to be an effective systems biology strategy for the optimisation of glycosylated biotherapeutics.

    “Combining these methodologies with genomic, transcriptomic, proteomic and metabolomic data has proven to be an effective systems biology strategy for the optimisation of glycosylated biotherapeutics [74].”

    From Glycoengineering Chinese hamster ovary cells: a short history (2021) · cites this paper as [74]

    Section 5 (page unavailable) discusses glycomic and glycoproteomic methods alongside genomic, transcriptomic and proteomic studies. But the Conclusions (page unavailable) say these advances will *hopefully* guide glycoengineering, not that combining them has proven effective for optimizing biotherapeutics; the cited passages also do not establish a role for metabolomic data. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • In CHO cells, knock down, knock out and overexpression of glycosylation enzymes and NSD transporters have been used in biotherapeutic functional studies and for development of biobetters.

    “In CHO cells, the knock down (KD), knock out (KO) and overexpression (OE) of glycosylation enzymes and NSD transporters have been used in biotherapeutic functional studies and for the development of biobetters, as summarised in Figure 2 [73,74].”

    From Glycoengineering Chinese hamster ovary cells: a short history (2021) · cites this paper as [74]

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  1. J. Y. Kim, Y. G. Kim, and G. M. Lee, Appl Microbiol Biotechnol. 2012, 93, 917.
  2. G. Walsh, Nat Biotechnol. 2014, 32, 992.
  3. B. Kelley, MAbs. 2009, 1, 443.
  4. G. Walsh, Nat Biotechnol. 2010, 28, 917.
  5. R. J. Kaufman, L. C. Wasley, A. J. Spiliotes, S. D. Gossels, S. A. Latt, G. R. Larsen, and R. M. Kay, Mol Cell Biol. 1985, 5, 1750.
  6. M. Butler and A. Meneses-Acosta, Appl Microbiol Biotechnol. 2012, 96, 885.
  7. G. Walsh, Drug Discov Today. 2010, 15, 773.
  8. B. A. Macher and U. Galili, Biochim Biophys Acta. 2008, 1780, 75.
  9. A. Noguchi, C. J. Mukuria, E. Suzuki, and M. Naiki, J Biochem. 1995, 117, 59.
  10. C. J. Bosques, B. E. Collins, J. W. Meador, 3rd, H. Sarvaiya, J. L. Murphy, G. Dellorusso, D. A. Bulik, I. H. Hsu, N. Washburn, S. F. Sipsey, J. R. Myette, R. Raman, Z. Shriver, R. Sasisekharan, and G. Venkataraman, Nat Biotechnol. 2010, 28, 1153.
  11. E. U. Lee, J. Roth, and J. C. Paulson, J Biol Chem. 1989, 264, 13848.
  12. Y. Li and X. Chen, Appl Microbiol Biotechnol. 2012, 94, 887.
  13. C. Ferrara, P. Brunker, T. Suter, S. Moser, U. Puntener, and P. Umana, Biotechnol Bioeng. 2006, 93, 851.
  14. M. Kurogochi, M. Mori, K. Osumi, M. Tojino, S. Sugawara, S. Takashima, Y. Hirose, W. Tsukimura, M. Mizuno, J. Amano, A. Matsuda, M. Tomita, A. Takayanagi, S. Shoda, and T. Shirai, PLoS One. 2015, 10, e0132848.
  15. C. W. Lin, M. H. Tsai, S. T. Li, T. I. Tsai, K. C. Chu, Y. C. Liu, M. Y. Lai, C. Y. Wu, Y. C. Tseng, S. S. Shivatare, C. H. Wang, P. Chao, S. Y. Wang, H. W. Shih, Y. F. Zeng, T. H. You, J. Y. Liao, Y. C. Tu, Y. S. Lin, H. Y. Chuang, C. L. Chen, C. S. Tsai, C. C. Huang, N. H. Lin, C. Ma, C. Y. Wu, and C. H. Wong, Proc Natl Acad Sci U S A. 2015, 112, 10611.
  16. R. Jefferis, Adv Exp Med Biol. 2005, 564, 143.
  17. P. Umana, J. Jean-Mairet, R. Moudry, H. Amstutz, and J. E. Bailey, Nat Biotechnol. 1999, 17, 176.
  18. G. Ashwell and J. Harford, Annu Rev Biochem. 1982, 51, 531.
  19. D. Ghaderi, M. Zhang, N. Hurtado-Ziola, and A. Varki, Biotechnol Genet Eng Rev. 2012, 28, 147.
  20. D. Ghaderi, R. E. Taylor, V. Padler-Karavani, S. Diaz, and A. Varki, Nat Biotechnol. 2010, 28, 863.
  21. R. Jefferis, J Immunol Res. 2016, 2016, 5358272.
  22. A. Kuriakose, N. Chirmule, and P. Nair, J Immunol Res. 2016, 2016, 1298473.
  23. R. Jefferis, Curr Pharm Biotechnol. 2016, 17, 1333.
  24. S. Dietmair, L. K. Nielsen, and N. E. Timmins, Biotechnol J. 2012, 7, 75.
  25. P. Datta, R. J. Linhardt, and S. T. Sharfstein, Biotechnol Bioeng. 2013, 110, 1255.
  26. X. Xu, H. Nagarajan, N. E. Lewis, S. Pan, Z. Cai, X. Liu, W. Chen, M. Xie, W. Wang, S. Hammond, M. R. Andersen, N. Neff, B. Passarelli, W. Koh, H. C. Fan, J. Wang, Y. Gui, K. H. Lee, M. J. Betenbaugh, S. R. Quake, I. Famili, B. O. Palsson, and J. Wang, Nat Biotechnol. 2011, 29, 735.
  27. K. Brinkrolf, O. Rupp, H. Laux, F. Kollin, W. Ernst, B. Linke, R. Kofler, S. Romand, F. Hesse, W. E. Budach, S. Galosy, D. Muller, T. Noll, J. Wienberg, T. Jostock, M. Leonard, J. Grillari, A. Tauch, A. Goesmann, B. Helk, J. E. Mott, A. Puhler, and N. Borth, Nat Biotechnol. 2013, 31, 694.
  28. N. E. Lewis, X. Liu, Y. Li, H. Nagarajan, G. Yerganian, E. O'Brien, A. Bordbar, A. M. Roth, J. Rosenbloom, C. Bian, M. Xie, W. Chen, N. Li, D. Baycin-Hizal, H. Latif, J. Forster, M. J. Betenbaugh, I. Famili, X. Xu, J. Wang, and B. O. Palsson, Nat Biotechnol. 2013, 31, 759.
  29. E. J. Blondeel, R. Ho, S. Schulze, S. Sokolenko, S. R. Guillemette, I. Slivac, Y. Durocher, J. G. Guillemette, B. J. McConkey, D. Chang, and M. G. Aucoin, J Biotechnol. 2016, 234, 127.
  30. D. Ley, A. K. Seresht, M. Engmark, O. Magdenoska, K. F. Nielsen, H. F. Kildegaard, and M. R. Andersen, Biotechnol Bioeng. 2015, 112, 2373.
  31. A. Farrell, N. McLoughlin, J. J. Milne, I. W. Marison, and J. Bones, J Proteome Res. 2014, 13, 3144.
  32. H. F. Kildegaard, D. Baycin-Hizal, N. E. Lewis, and M. J. Betenbaugh, Curr Opin Biotechnol. 2013, 24, 1102.
  33. A. M. Lewis, N. R. Abu-Absi, M. C. Borys, and Z. J. Li, Biotechnol Bioeng. 2016, 113, 26.
  34. P. M. Rudd, R. J. Woods, M. R. Wormald, G. Opdenakker, A. K. Downing, I. D. Campbell, and R. A. Dwek, Biochim Biophys Acta. 1995, 1248, 1.
  35. R. B. Parekh, A. G. Tse, R. A. Dwek, A. F. Williams, and T. W. Rademacher, Embo J 1987, 6, 1233.
  36. A. F. Williams, R. B. Parekh, D. R. Wing, A. C. Willis, A. N. Barclay, R. Dalchau, J. W. Fabre, R. A. Dwek, and T. W. Rademacher, Glycobiology. 1993, 3, 339.
  37. G. Reuter and H. J. Gabius, Cell Mol Life Sci. 1999, 55, 398.
  38. F. J. Olson, M. Bäckström, H. Karlsson, J. Burchell, and G. C. Hansson, Glycobiology. 2005, 15, 177.
  39. C. Ravanat, C. Gachet, J. M. Herbert, S. Schuhler, J. C. Guillemot, F. Uzabiaga, C. Picard, P. Ferrara, M. Freund, and J. P. Cazenave, Eur J Biochem. 1994, 223, 203.
  40. Z. Yang, S. Wang, A. Halim, M. A. Schulz, M. Frodin, S. H. Rahman, M. B. Vester- Christensen, C. Behrens, C. Kristensen, S. Y. Vakhrushev, E. P. Bennett, H. H. Wandall, and H. Clausen, Nat Biotechnol. 2015, 33, 842.
  41. R. L. Shields, J. Lai, R. Keck, L. Y. O'Connell, K. Hong, Y. G. Meng, S. H. Weikert, and L. G. Presta, J Biol Chem. 2002, 277, 26733.
  42. S. Matsumiya, Y. Yamaguchi, J. Saito, M. Nagano, H. Sasakawa, S. Otaki, M. Satoh, K. Shitara, and K. Kato, J Mol Biol. 2007, 368, 767.
  43. A. M. Goetze, Y. D. Liu, Z. Zhang, B. Shah, E. Lee, P. V. Bondarenko, and G. C. Flynn, Glycobiology. 2011, 21, 949.
  44. T. Angata and A. Varki, Chem Rev. 2002, 102, 439.
  45. L. Santell, T. Ryll, T. Etcheverry, M. Santoris, G. Dutina, A. Wang, J. Gunson, and T. G. Warner, Biochem Biophys Res Commun. 1999, 258, 132.
  46. M. Takeuchi, S. Takasaki, H. Miyazaki, T. Kato, S. Hoshi, N. Kochibe, and A. Kobata, J Biol Chem. 1988, 263, 3657.
  47. M. Zhang, K. Koskie, J. S. Ross, K. J. Kayser, and M. V. Caple, Biotechnol Bioeng. 2010, 105, 1094.
  48. O. M. Pearce, H. Laubli, A. Verhagen, P. Secrest, J. Zhang, N. M. Varki, P. R. Crocker, J. D. Bui, and A. Varki, Proc Natl Acad Sci U S A. 2014, 111, 5998.
  49. V. Padler-Karavani, H. Yu, H. Cao, H. Chokhawala, F. Karp, N. Varki, X. Chen, and A. Varki, Glycobiology. 2008, 18, 818.
  50. M. Hedlund, V. Padler-Karavani, N. M. Varki, and A. Varki, Proc Natl Acad Sci U S A. 2008, 105, 18936.
  51. C. Yu, K. Gao, L. Zhu, W. Wang, L. Wang, F. Zhang, C. Liu, M. Li, M. R. Wormald, P. M. Rudd, and J. Wang, Sci Rep. 2016, 7, 20029.
  52. R. M. Anthony, F. Nimmerjahn, D. J. Ashline, V. N. Reinhold, J. C. Paulson, and J. V. Ravetch, Science. 2008, 320, 373.
  53. Y. Kaneko, F. Nimmerjahn, and J. V. Ravetch, Science. 2006, 313, 670.
  54. C. Y. Chung, Q. Wang, S. Yang, B. Yin, H. Zhang, and M. Betenbaugh, Biotechnol J. 2017, 12, 1600502.
  55. X. Yu, K. Baruah, D. J. Harvey, S. Vasiljevic, D. S. Alonzi, B. D. Song, M. K. Higgins, T. A. Bowden, C. N. Scanlan, and M. Crispin, J Am Chem Soc. 2013, 135, 9723.
  56. Y. Mimura, R. M. Kelly, L. Unwin, S. Albrecht, R. Jefferis, M. Goodall, Y. Mizukami, Y. Mimura-Kimura, T. Matsumoto, H. Ueoka, and P. M. Rudd, J Immunol Methods. 2016, 428, 30.
  57. C. Raymond, A. Robotham, M. Spearman, M. Butler, J. Kelly, and Y. Durocher, MAbs. 2015, 7, 571.
  58. Y. T. Jeong, O. Choi, H. R. Lim, Y. D. Son, H. J. Kim, and J. H. Kim, J Microbiol Biotechnol. 2008, 18, 1945.
  59. J. H. Lee, Y. G. Kim, and G. M. Lee, Biotechnol Prog. 2015, 31, 1133.
  60. Z. Wang, J. H. Park, H. H. Park, W. Tan, and T. H. Park, Biotechnol Bioeng. 2011, 108, 1634.
  61. A. Varki and R. Schauer, in Essentials of Glycobiology, (Eds: A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etzler), Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY) 2009, Ch. 14.
  62. N. S. Wong, M. G. Yap, and D. I. Wang, Biotechnol Bioeng. 2006, 93, 1005.
  63. X. Gu and D. I. Wang, Biotechnol Bioeng. 1998, 58, 642.
  64. B. Yin, Q. Wang, C. Y. Chung, R. Bhattacharya, X. Ren, J. Tang, K. J. Yarema, and M. J. Betenbaugh, Biotechnol Bioeng. 2017, 114, 1899.
  65. Y. T. Jeong, O. Choi, Y. D. Son, S. Y. Park, and J. H. Kim, Biotechnol Appl Biochem. 2009, 52, 283.
  66. Y. D. Son, Y. T. Jeong, S. Y. Park, and J. H. Kim, Glycobiology. 2011, 21, 1019.
  67. E. Monti, A. Preti, B. Venerando, and G. Borsani, Neurochem Res. 2002, 27, 649.
  68. V. Seyrantepe, K. Landry, S. Trudel, J. A. Hassan, C. R. Morales, and A. V. Pshezhetsky, J Biol Chem. 2004, 279, 37021.
  69. Y. Kakugawa, T. Wada, K. Yamaguchi, H. Yamanami, K. Ouchi, I. Sato, and T. Miyagi, Proc Natl Acad Sci U S A. 2002, 99, 10718.
  70. A. Hinek, A. V. Pshezhetsky, M. von Itzstein, and B. Starcher, J Biol Chem. 2006, 281, 3698.
  71. N. de Geest, E. Bonten, L. Mann, J. de Sousa-Hitzler, C. Hahn, and A. d'Azzo, Hum Mol Genet. 2002, 11, 1455.
  72. M. J. Gramer, Adv Biochem Eng Biotechnol. 2014, 139, 123.
  73. J. Ferrari, J. Gunson, J. Lofgren, L. Krummen, and T. G. Warner, Biotechnol Bioeng. 1998, 60, 589.
  74. T. Shinkawa, K. Nakamura, N. Yamane, E. Shoji-Hosaka, Y. Kanda, M. Sakurada, K. Uchida, H. Anazawa, M. Satoh, M. Yamasaki, N. Hanai, and K. Shitara, J Biol Chem. 2003, 278, 3466.
  75. S. Krapp, Y. Mimura, R. Jefferis, R. Huber, and P. Sondermann, J Mol Biol. 2003, 325, 979.
  76. E. Suzuki, R. Niwa, S. Saji, M. Muta, M. Hirose, S. Iida, Y. Shiotsu, M. Satoh, K. Shitara, M. Kondo, and M. Toi, Clin Cancer Res. 2007, 13, 1875.
  77. T. T. Junttila, K. Parsons, C. Olsson, Y. Lu, Y. Xin, J. Theriault, L. Crocker, O. Pabonan, T. Baginski, G. Meng, K. Totpal, R. F. Kelley, and M. X. Sliwkowski, Cancer Res. 2010, 70, 4481.
  78. Q. Wang, M. Stuczynski, Y. Gao, and M. J. Betenbaugh, Methods Mol Biol. 2015, 1321, 287.
  79. L. Malphettes, Y. Freyvert, J. Chang, P. Q. Liu, E. Chan, J. C. Miller, Z. Zhou, T. Nguyen, C. Tsai, A. W. Snowden, T. N. Collingwood, P. D. Gregory, and G. J. Cost, Biotechnol Bioeng. 2010, 106, 774.
  80. N. Yamane-Ohnuki, S. Kinoshita, M. Inoue-Urakubo, M. Kusunoki, S. Iida, R. Nakano, M. Wakitani, R. Niwa, M. Sakurada, K. Uchida, K. Shitara, and M. Satoh, Biotechnol Bioeng. 2004, 87, 614.
  81. K. F. Chan, W. Shahreel, C. Wan, G. Teo, N. Hayati, S. J. Tay, W. H. Tong, Y. Yang, P. M. Rudd, P. Zhang, and Z. Song, Biotechnol J. 2016, 11, 399.
  82. H. Schachter, Biochem Cell Biol. 1986, 64, 163.
  83. M. Schuster, P. Umana, C. Ferrara, P. Brunker, C. Gerdes, G. Waxenecker, S. Wiederkum, C. Schwager, H. Loibner, G. Himmler, and G. C. Mudde, Cancer Res. 2005, 65, 7934.
  84. A. M. Abdel Rahman, M. Ryczko, M. Nakano, J. Pawling, T. Rodrigues, A. Johswich, N. Taniguchi, and J. W. Dennis, Glycobiology. 2015, 25, 225.
  85. Y. Zhao, Y. Sato, T. Isaji, T. Fukuda, A. Matsumoto, E. Miyoshi, J. Gu, and N. Taniguchi, FEBS J 2008, 275, 1939.
  86. K. S. Lau, E. A. Partridge, A. Grigorian, C. I. Silvescu, V. N. Reinhold, M. Demetriou, and J. W. Dennis, Cell. 2007, 129, 123.
  87. J. W. Dennis, S. Laferte, C. Waghorne, M. L. Breitman, and R. S. Kerbel, Science. 1987, 236, 582.
  88. K. Shirato, K. Nakajima, H. Korekane, S. Takamatsu, C. Gao, T. Angata, K. Ohtsubo, and N. Taniguchi, J Clin Biochem Nutr. 2011, 48, 20.
  89. K. Fukuta, R. Abe, T. Yokomatsu, N. Kono, M. Asanagi, F. Omae, M. T. Minowa, M. Takeuchi, and T. Makino, Glycobiology. 2000, 10, 421.
  90. B. Yin, Y. Gao, C. Y. Chung, S. Yang, E. Blake, M. C. Stuczynski, J. Tang, H. F. Kildegaard, M. R. Andersen, H. Zhang, and M. J. Betenbaugh, Biotechnol Bioeng. 2015, 112, 2343.
  91. Y. Gavel and G. von Heijne, Protein Eng. 1990, 3, 433.
  92. H. A. Kaplan, J. K. Welply, and W. J. Lennarz, Biochim Biophys Acta. 1987, 906, 161.
  93. N. Ceaglio, M. Etcheverrigaray, R. Kratje, and M. Oggero, Biochimie. 2008, 90, 437.
  94. J. Jones, S. S. Krag, and M. J. Betenbaugh, Biochim Biophys Acta. 2005, 1726, 121.
  95. S. H. Shakin-Eshleman, S. L. Spitalnik, and L. Kasturi, J Biol Chem. 1996, 271, 6363.
  96. L. Kasturi, J. R. Eshleman, W. H. Wunner, and S. H. Shakin-Eshleman, J Biol Chem. 1995, 270, 14756.
  97. V. Picard, E. Ersdal-Badju, and S. C. Bock, Biochemistry. 1995, 34, 8433.
  98. E. Bause, H. Hettkamp, and G. Legler, Biochem J. 1982, 203, 761.
  99. J. L. Mellquist, L. Kasturi, S. L. Spitalnik, and S. H. Shakin-Eshleman, Biochemistry. 1998, 37, 6833.
  100. E. Bause, Biochem Soc Trans. 1984, 12, 514.
  101. E. Bause, Biochem J. 1983, 209, 331.
  102. S. Perlman, B. van den Hazel, J. Christiansen, S. Gram-Nielsen, C. B. Jeppesen, K. V. Andersen, T. Halkier, S. Okkels, and H. T. Schambye, J Clin Endocrinol Metab. 2003, 88, 3227.
  103. J. C. Egrie, E. Dwyer, J. K. Browne, A. Hitz, and M. A. Lykos, Exp Hematol. 2003, 31, 290.
  104. T. Chitlaru, C. Kronman, B. Velan, and A. Shafferman, Biochem J. 2001, 354, 613.
  105. T. Chitlaru, C. Kronman, B. Velan, and A. Shafferman, Biochem J. 2002, 363, 619.
  106. C. Kronman, T. Chitlaru, E. Elhanany, B. Velan, and A. Shafferman, J Biol Chem. 2000, 275, 29488.
  107. J. Powell and C. Gurk-Turner, Proceedings (Baylor University. Medical Center). 2002, 15, 332.
  108. A. Gervais, Y. A. Hammel, S. Pelloux, P. Lepage, G. Baer, N. Carte, O. Sorokine, J. M. Strub, R. Koerner, E. Leize, and A. Van Dorsselaer, Glycobiology. 2003, 13, 179.
  109. E. Böhm, B. K. Seyfried, M. Dockal, M. Graninger, M. Hasslacher, M. Neurath, C. Konetschny, P. Matthiessen, A. Mitterer, and F. Scheiflinger, BMC Biotechnology. 2015, 15, 87.
  110. Y. Seo, G. M. Park, M. J. Oh, and H. J. An, Bioanalysis. 2017, 9, 1361.
  111. S. Houel, M. Hilliard, Y. Q. Yu, N. McLoughlin, S. M. Martin, P. M. Rudd, J. P. Williams, and W. Chen, Anal Chem. 2014, 86, 576.
  112. L. Zhu, Q. Guo, H. Guo, T. Liu, Y. Zheng, P. Gu, X. Chen, H. Wang, S. Hou, and Y. Guo, MAbs. 2014, 6, 1474.
  113. A. Seyhan and B. Ata, International Journal of Women's Health. 2011, 3, 243.
  114. C. Spahr, J. J. Kim, S. Deng, P. Kodama, Z. Xia, J. Tang, R. Zhang, S. Siu, N. Nuanmanee, B. Estes, J. Stevens, M. Zhou, and H. S. Lu, Protein Science : A Publication of the Protein Society. 2013, 22, 1739.
  115. J. Zaia, Molecular & Cellular Proteomics. 2013, 12, 885.
  116. P. L. DeAngelis, Appl Microbiol Biotechnol. 2012, 94, 295.
  117. U. Bhaskar, E. Sterner, A. M. Hickey, A. Onishi, F. Zhang, J. S. Dordick, and R. J. Linhardt, Applied Microbiology and Biotechnology. 2012, 93, 1.
  118. R. J. Linhardt, Journal of Medicinal Chemistry. 2003, 46, 2551.
  119. H. Liu, Z. Zhang, and R. J. Linhardt, Natural Product Reports. 2009, 26, 313.
  120. B. Casu, A. Naggi, and G. Torri, Matrix Biology. 2010, 29, 442.
  121. A. Maraveyas, M. J. Johnson, Y. P. Xiao, and S. Noble, Cancer and Metastasis Reviews. 2010, 29, 777.
  122. F. Robert, Journal of Hematology & Oncology. 2010, 3, 3.
  123. L. Y. Yu, H. G. Garg, B. Li, R. J. Linhardt, and C. A. Hales, Current Cancer Drug Targets. 2010, 10, 229.
  124. P. L. Li, J. Z. Sheng, Y. H. Liu, J. Li, J. Liu, and F. S. Wang, Medicinal Research Reviews. 2013, 33, 665.
  125. N. Potdar, T. A. Gelbaya, J. C. Konje, and L. G. Nardo, Human Reproduction Update. 2013, 19, 674.
  126. S. Seshadri, S. K. Sunkara, Y. Khalaf, T. El-Toukhy, and H. Hamoda, Reproductive Biomedicine Online. 2012, 25, 572.
  127. M. D. Shastri, G. M. Peterson, N. Stewart, S. S. Sohal, and R. P. Patel, Expert Opinion on Investigational Drugs. 2014, 23, 357.
  128. V. K. Yadav, M. Saraswat, N. Chhikara, S. Singh, and S. Yadav, Current Protein & Peptide Science. 2013, 14, 61.
  129. J. Y. Baik, L. Gasimli, B. Yang, P. Datta, F. Zhang, C. A. Glass, J. D. Esko, R. J. Linhardt, and S. T. Sharfstein, Metabolic Engineering. 2012, 14, 81.
  130. P. Datta, G. Y. Li, B. Yang, X. Zhao, J. Y. Baik, T. R. Gemmill, S. T. Sharfstein, and R. J. Linhardt, Journal of Biological Chemistry. 2013, 288, 37308.
  131. G. Li, B. Yang, L. Li, F. Zhang, C. Xue, and R. J. Linhardt, Analytical Biochemistry. 2014, 455, 3.
  132. P. Hossler, B. C. Mulukutla, and W. S. Hu, PLoS One. 2007, 2, e713.
  133. F. J. Krambeck, S. V. Bennun, M. R. Andersen, and M. J. Betenbaugh, PLoS One. 2017, 12, e0175376.
  134. P. Umana and J. E. Bailey, Biotechnol Bioeng. 1997, 55, 890.
  135. H. Hefzi, K. S. Ang, M. Hanscho, A. Bordbar, D. Ruckerbauer, M. Lakshmanan, C. A. Orellana, D. Baycin-Hizal, Y. Huang, D. Ley, V. S. Martinez, S. Kyriakopoulos, N. E. Jimenez, D. C. Zielinski, L. E. Quek, T. Wulff, J. Arnsdorf, S. Li, J. S. Lee, G. Paglia, N. Loira, P. N. Spahn, L. E. Pedersen, J. M. Gutierrez, Z. A. King, A. M. Lund, H. Nagarajan, A. Thomas, A. M. Abdel-Haleem, J. Zanghellini, H. F. Kildegaard, B. G. Voldborg, Z. P. Gerdtzen, M. J. Betenbaugh, B. O. Palsson, M. R. Andersen, L. K. Nielsen, N. Borth, D. Y. Lee, and N. E. Lewis, Cell Syst. 2016, 3, 434.
  136. P. N. Spahn, A. H. Hansen, S. Kol, B. G. Voldborg, and N. E. Lewis, Biotechnol J. 2017, 12, 1600489.
  137. P. N. Spahn, A. H. Hansen, H. G. Hansen, J. Arnsdorf, H. F. Kildegaard, and N. E. Lewis, Metab Eng. 2016, 33, 52.
  138. I. Jimenez del Val, J. M. Nagy, and C. Kontoravdi, Biotechnol Prog. 2011, 27, 1730.
  139. F. J. Krambeck, S. V. Bennun, S. Narang, S. Choi, K. J. Yarema, and M. J. Betenbaugh, Glycobiology. 2009, 19, 1163.
  140. F. J. Krambeck and M. J. Betenbaugh, Biotechnol Bioeng. 2005, 92, 711.
  141. A. G. McDonald, J. M. Hayes, T. Bezak, S. A. Gluchowska, E. F. Cosgrave, W. B. Struwe, C. J. Stroop, H. Kok, T. van de Laar, P. M. Rudd, K. F. Tipton, and G. P. Davey, J Cell Sci. 2014, 127, 5014.
  142. S. R. Hamilton, P. Bobrowicz, B. Bobrowicz, R. C. Davidson, H. Li, T. Mitchell, J. H. Nett, S. Rausch, T. A. Stadheim, H. Wischnewski, S. Wildt, and T. U. Gerngross, Science. 2003, 301, 1244.
  143. S. J. North, H. H. Huang, S. Sundaram, J. Jang-Lee, A. T. Etienne, A. Trollope, S. Chalabi, A. Dell, P. Stanley, and S. M. Haslam, J Biol Chem. 2010, 285, 5759.
  144. K. N. Baker, M. H. Rendall, A. E. Hills, M. Hoare, R. B. Freedman, and D. C. James, Biotechnol Bioeng. 2001, 73, 188.
  145. D. Chee Furng Wong, K. Tin Kam Wong, L. Tang Goh, C. Kiat Heng, and M. Gek Sim Yap, Biotechnol Bioeng. 2005, 89, 164.
  146. M. Yang and M. Butler, Cytotechnology. 2000, 34, 83.
  147. N. Kochanowski, F. Blanchard, R. Cacan, F. Chirat, E. Guedon, A. Marc, and J. L. Goergen, Biotechnol Bioeng. 2008, 100, 721.
  148. N. S. Wong, L. Wati, P. M. Nissom, H. T. Feng, M. M. Lee, and M. G. Yap, Biotechnol Bioeng. 2010, 107, 321.
  149. P. M. Jedrzejewski, I. J. del Val, A. Constantinou, A. Dell, S. M. Haslam, K. M. Polizzi, and C. Kontoravdi, Int J Mol Sci. 2014, 15, 4492.
  150. J. Becker, M. Hackl, O. Rupp, T. Jakobi, J. Schneider, R. Szczepanowski, T. Bekel, N. Borth, A. Goesmann, and J. Grillari, J Biotechnol. 2011, 156, 227.
  151. D. Baycin-Hizal, D. L. Tabb, R. Chaerkady, L. Chen, N. E. Lewis, H. Nagarajan, V. Sarkaria, A. Kumar, D. Wolozny, J. Colao, E. Jacobson, Y. Tian, R. N. O'Meally, S. S. Krag, R. N. Cole, B. O. Palsson, H. Zhang, and M. Betenbaugh, J Proteome Res. 2012, 11, 5265.
  152. D. C. Frost and L. Li, in Adv. Protein Chem. Struct. Biol, Vol. 95 (Ed: R. Donev), Academic Press 2014,
  153. S. B. Levery, C. Steentoft, A. Halim, Y. Narimatsu, H. Clausen, and S. Y. Vakhrushev, Biochimica et Biophysica Acta (BBA) -General Subjects. 2015, 1850, 33.
  154. H. Lu, Y. Zhang, and P. Yang, National Science Review. 2016, 3, 345.
  155. K. K. Palaniappan and C. R. Bertozzi, Chem Rev. 2016, 116, 14277.
  156. M. Thaysen-Andersen and N. H. Packer, … et Biophysica Acta (BBA)-Proteins and …. 2014, 1844, 1437.
  157. L. Veillon, S. Zhou, and Y. Mechref, Methods in Enzymology. 2017, 585, 431.
  158. Y. Yang, V. Franc, and A. Heck, Trends in Biotechnology. 2017, 35, 598.
  159. J. N. Liu, C. S. Jin, R. M. Cherian, N. G. Karlsson, and J. Holgersson, J Biotechnol. 2015, 199, 77.
  160. Z. Yang, A. Halim, Y. Narimatsu, H. J. Joshi, C. Steentoft, K. Schjoldager, M. A. Schulz, N. R. Sealover, K. J. Kayser, E. P. Bennett, S. B. Levery, S. Y. Vakhrushev, and H. Clausen, Molecular & Cellular Proteomics. 2014, 13, 3224.
  161. P. G. Slade, M. Hajivandi, C. M. Bartel, and S. F. Gorfien, J Proteome Res. 2012, 11, 6175.

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Authors
Tejwani, V., Andersen, M. R., Nam, J. H., & Sharfstein, S. T.
Affiliations
  • SUNY Polytechnic Institute (US)
  • Technical University of Denmark (DK)
  • Export–Import Bank of Korea (KR)
Corresponding author
Sharfstein, Susan T.
ORCID
Venue
Biotechnology Journal
Publisher
Wiley
Published
2018-02-12
Volume
13
Issue
3
Pages
e1700234-e1700234
ISSN
  • 1860-6768 (ISSN-L)
  • 1860-7314
DOI
10.1002/biot.201700234
OpenAlex
W2784292626
Cited by
70
References
169
Citations by year
2026: 6 · 2025: 4 · 2024: 8 · 2023: 7 · 2022: 8 · 2021: 14 · 2020: 10 · 2019: 10 · 2018: 3
FWCI
0.91
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Biotechnology Journal (publishedVersion)
  • PubMed (publishedVersion)
  • Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion, other-oa)
Funders
National Science Foundation (1622959)
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 › Glycosylation and Glycoproteins Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Transgenic Plants and Applications
Keywords
glycoengineering, CHO cells, glycosylation, glycoforms, glycan heterogeneity, glycosaminoglycans, heparin, cell line development, systems biology, glycan analysis, genetic engineering
MeSH terms
Animals, Cricetulus, Glycoproteins, Glycosylation, Cricetinae, Humans, Protein Processing, Post-Translational, Recombinant Proteins, CHO Cells, Systems Biology

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