Proteomic analysis of chinese hamster ovary cells

Journal of Proteome Research

Volumn 11, Issue 11, 2012, Pages 5265-5276

  Baycin Hizal, Deniz ^a   Tabb, David L ^b   Chaerkady, Raghothama ^c   Chen, Lily ^c   Lewis, Nathan E ^e   Nagarajan, Harish ^e   Sarkaria, Vishaldeep ^c   Kumar, Amit ^a   Wolozny, Daniel ^a   Colao, Joe ^a   Jacobson, Elena ^a   Tian, Yuan ^c   O'Meally, Robert N ^c   Krag, Sharon S ^d   Cole, Robert N ^c   Palsson, Bernhard O ^f   Zhang, Hui ^c   Betenbaugh, Michael ^a,f  

^a Johns Hopkins University   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f Chalmers University of Technology   (Denmark)

Author keywords

Chinese hamster ovary (CHO) cells; codon frequency; glycosylation; LC MS MS; mammalian cells; mass spectrometry; peptides; proteins; proteome; Proteomics

Indexed keywords

GLYCOPEPTIDE; GLYCOSPHINGOLIPID; MESSENGER RNA; STEROID;

ACETYLATION; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; CHO CELL; CODON; ENZYME SPECIFICITY; GEL ELECTROPHORESIS; GENE EXPRESSION; GENE SEQUENCE; GLYCOSYLATION; HORMONE METABOLISM; HUMAN; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEOMICS; REVERSED PHASE LIQUID CHROMATOGRAPHY; SOLID PHASE EXTRACTION; TANDEM MASS SPECTROMETRY;

ACETYLATION; ANIMALS; CARBOHYDRATES; CHO CELLS; CHROMATOGRAPHY, LIQUID; CODON; CRICETINAE; CRICETULUS; GLYCOSYLATION; PROTEOME; RNA, MESSENGER; TANDEM MASS SPECTROMETRY;

CRICETULUS GRISEUS; MAMMALIA;

EID: 84868324251     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300476w     Document Type: Article

References (63)

1. Walsh, G. Biopharmaceutical benchmarks 2010 Nat. Biotechnol. 2010, 28 (9) 917-24
2. Lim, Y.; Wong, N. S.; Lee, Y. Y.; Ku, S. C.; Wong, D. C.; Yap, M. G. Engineering mammalian cells in bioprocessing-current achievements and future perspectives Biotechnol. Appl. Biochem. 2010, 55 (4) 175-89
3. Mohan, C.; Kim, Y. G.; Koo, J.; Lee, G. M. Assessment of cell engineering strategies for improved therapeutic protein production in CHO cells Biotechnol. J. 2008, 3 (5) 624-30
4. Wei, Y. Y.; Naderi, S.; Meshram, M.; Budman, H.; Scharer, J. M.; Ingalls, B. P.; McConkey, B. J. Proteomics analysis of chinese hamster ovary cells undergoing apoptosis during prolonged cultivation Cytotechnology 2011, 63 (6) 663-77
5. Kim, J. Y.; Kim, Y. G.; Han, Y. K.; Choi, H. S.; Kim, Y. H.; Lee, G. M. Proteomic understanding of intracellular responses of recombinant Chinese hamster ovary cells cultivated in serum-free medium supplemented with hydrolysates Appl. Microbiol. Biotechnol. 2011, 89 (6) 1917-28
6. Gupta, P.; Lee, K. H. Genomics and proteomics in process development: opportunities and challenges Trends Biotechnol. 2007, 25 (7) 324-30
7. 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. The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line Nat. Biotechnol. 2011, 29 (8) 735-41
8. Baycin-Hizal, D.; Tian, Y.; Akan, I.; Jacobson, E.; Clark, D.; Chu, J.; Palter, K.; Zhang, H.; Betenbaugh, M. J. GlycoFly: a database of Drosophila N-linked glycoproteins identified using SPEG - MS techniques J. Proteome Res. 2011, 10 (6) 2777-84
9. Kuystermans, D.; Krampe, B.; Swiderek, H.; Al-Rubeai, M. Using cell engineering and omic tools for the improvement of cell culture processes Cytotechnology 2007, 53 (1-3) 3-22
10. Yoshida, K.; Kobayashi, K.; Miwa, Y.; Kang, C. M.; Matsunaga, M.; Yamaguchi, H.; Tojo, S.; Yamamoto, M.; Nishi, R.; Ogasawara, N.; Nakayama, T.; Fujita, Y. Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis Nucleic Acids Res. 2001, 29 (3) 683-92
11. Doolan, P.; Meleady, P.; Barron, N.; Henry, M.; Gallagher, R.; Gammell, P.; Melville, M.; Sinacore, M.; McCarthy, K.; Leonard, M.; Charlebois, T.; Clynes, M. Microarray and proteomics expression profiling identifies several candidates, including the valosin-containing protein (VCP), involved in regulating high cellular growth rate in production CHO cell lines Biotechnol. Bioeng. 2010, 106 (1) 42-56
12. Chaerkady, R.; Kelkar, D. S.; Muthusamy, B.; Kandasamy, K.; Dwivedi, S. B.; Sahasrabuddhe, N. A.; Kim, M. S.; Renuse, S.; Pinto, S. M.; Sharma, R.; Pawar, H.; Sekhar, N. R.; Mohanty, A. K.; Getnet, D.; Yang, Y.; Zhong, J.; Dash, A. P.; Maccallum, R. M.; Delanghe, B.; Mlambo, G.; Kumar, A.; Prasad, K. T.; Okulate, M.; Kumar, N.; Pandey, A. A proteogenomic analysis of Anopheles gambiae using high-resolution Fourier transform mass spectrometry Genome Res. 2011, 21, 1872-1881
13. Brunner, E.; Ahrens, C. H.; Mohanty, S.; Baetschmann, H.; Loevenich, S.; Potthast, F.; Deutsch, E. W.; Panse, C.; de Lichtenberg, U.; Rinner, O.; Lee, H.; Pedrioli, P. G.; Malmstrom, J.; Koehler, K.; Schrimpf, S.; Krijgsveld, J.; Kregenow, F.; Heck, A. J.; Hafen, E.; Schlapbach, R.; Aebersold, R. A high-quality catalog of the Drosophila melanogaster proteome Nat. Biotechnol. 2007, 25 (5) 576-83
14. Desiere, F.; Deutsch, E. W.; Nesvizhskii, A. I.; Mallick, P.; King, N. L.; Eng, J. K.; Aderem, A.; Boyle, R.; Brunner, E.; Donohoe, S.; Fausto, N.; Hafen, E.; Hood, L.; Katze, M. G.; Kennedy, K. A.; Kregenow, F.; Lee, H.; Lin, B.; Martin, D.; Ranish, J. A.; Rawlings, D. J.; Samelson, L. E.; Shiio, Y.; Watts, J. D.; Wollscheid, B.; Wright, M. E.; Yan, W.; Yang, L.; Yi, E. C.; Zhang, H.; Aebersold, R. Integration with the human genome of peptide sequences obtained by high-throughput mass spectrometry Genome Biol. 2005, 6 (1) R9
15. Yee, J. C.; de Leon Gatti, M.; Philp, R. J.; Yap, M.; Hu, W. S. Genomic and proteomic exploration of CHO and hybridoma cells under sodium butyrate treatment Biotechnol. Bioeng. 2008, 99 (5) 1186-204
16. Lee, J. S.; Park, H. J.; Kim, Y. H.; Lee, G. M. Protein reference mapping of dihydrofolate reductase-deficient CHO DG44 cell lines using 2-dimensional electrophoresis Proteomics 2010, 10 (12) 2292-302
17. Baik, J. Y.; Joo, E. J.; Kim, Y. H.; Lee, G. M. Limitations to the comparative proteomic analysis of thrombopoietin producing Chinese hamster ovary cells treated with sodium butyrate J. Biotechnol. 2008, 133 (4) 461-8
18. MyriMatch, http://forge.fenchurch.mc.vanderbilt.edu/scm/viewvc.php/ checkout/trunk/doc/index.html?root=myrimatch.
19. TagRecon, http://forge.fenchurch.mc.vanderbilt.edu/scm/viewvc.php/ checkout/trunk/doc/index.html?root=tagrecon.
20. Harsha, H. C.; Molina, H.; Pandey, A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture Nat. Protoc. 2008, 3 (3) 505-16
21. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6 (5) 359-62
22. Baycin-Hizal, D.; Tian, Y.; Akan, I.; Jacobson, E.; Clark, D.; Wu, A.; Jampol, R.; Palter, K.; Betenbaugh, M.; Zhang, H. GlycoFish: a database of zebrafish N-linked glycoproteins identified using SPEG method coupled with LC/MS Anal. Chem. 2011, 83 (13) 5296-303
23. Tian, Y.; Zhou, Y.; Elliott, S.; Aebersold, R.; Zhang, H. Solid-phase extraction of N-linked glycopeptides Nat. Protoc. 2007, 2 (2) 334-9
24. Wang, Y.; Yang, F.; Gritsenko, M. A.; Clauss, T.; Liu, T.; Shen, Y.; Monroe, M. E.; Lopez-Ferrer, D.; Reno, T.; Moore, R. J.; Klemke, R. L.; Camp, D. G., 2nd; Smith, R. D. Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells Proteomics 2011, 11 (10) 2019-26
25. Tao, D.; Qiao, X.; Sun, L.; Hou, C.; Gao, L.; Zhang, L.; Shan, Y.; Liang, Z.; Zhang, Y. Development of a highly efficient 2-D system with a serially coupled long column and its application in identification of rat brain integral membrane proteins with ionic liquids-assisted solubilization and digestion J. Proteome Res. 2011, 10 (2) 732-8
26. Tranche, https://proteomecommons.org/tranche/.
27. CHO Genome, http://www.chogenome.org/.
28. Hammond, S.; Swanberg, J. C.; Kaplarevic, M.; Lee, K. H. Genomic sequencing and analysis of a Chinese hamster ovary cell line using Illumina sequencing technology BMC Genomics 2011, 12, 67
29. Holman, J. D.; Ma, Z. Q.; Tabb, D. L., Identifying Proteomic LC-MS/MS Data Sets with Bumbershoot and IDPicker. Curr. Protoc. Bioinform. 2012, Chapter 13, Unit 13.17.
30. Dasari, S.; Chambers, M. C.; Slebos, R. J.; Zimmerman, L. J.; Ham, A. J.; Tabb, D. L. TagRecon: high-throughput mutation identification through sequence tagging J. Proteome Res. 2010, 9 (4) 1716-26
31. Tabb, D. L.; Fernando, C. G.; Chambers, M. C. MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis J. Proteome Res. 2007, 6 (2) 654-61
32. Ikemura, T. Codon usage and tRNA content in unicellular and multicellular organisms Mol. Biol. Evol. 1985, 2 (1) 13-34
33. Elf, J.; Nilsson, D.; Tenson, T.; Ehrenberg, M. Selective charging of tRNA isoacceptors explains patterns of codon usage Science 2003, 300 (5626) 1718-22
34. Plotkin, J. B.; Kudla, G. Synonymous but not the same: the causes and consequences of codon bias Nat. Rev. Genet. 2011, 12 (1) 32-42
35. Kudla, G.; Lipinski, L.; Caffin, F.; Helwak, A.; Zylicz, M. High guanine and cytosine content increases mRNA levels in mammalian cells PLoS Biol. 2006, 4 (6) e180
36. Chamary, J. V.; Hurst, L. D. Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals Genome Biol. 2005, 6 (9) R75
37. Giot, L.; Bader, J. S.; Brouwer, C.; Chaudhuri, A.; Kuang, B.; Li, Y.; Hao, Y. L.; Ooi, C. E.; Godwin, B.; Vitols, E.; Vijayadamodar, G.; Pochart, P.; Machineni, H.; Welsh, M.; Kong, Y.; Zerhusen, B.; Malcolm, R.; Varrone, Z.; Collis, A.; Minto, M.; Burgess, S.; McDaniel, L.; Stimpson, E.; Spriggs, F.; Williams, J.; Neurath, K.; Ioime, N.; Agee, M.; Voss, E.; Furtak, K.; Renzulli, R.; Aanensen, N.; Carrolla, S.; Bickelhaupt, E.; Lazovatsky, Y.; DaSilva, A.; Zhong, J.; Stanyon, C. A.; Finley, R. L., Jr.; White, K. P.; Braverman, M.; Jarvie, T.; Gold, S.; Leach, M.; Knight, J.; Shimkets, R. A.; McKenna, M. P.; Chant, J.; Rothberg, J. M. A protein interaction map of Drosophila melanogaster Science 2003, 302 (5651) 1727-36
38. Agresti, A. A Survey of Exact Inference for Contingency Tables Stat. Sci. 1992, 7, 131-53
39. Liu, H.; Sadygov, R. G.; Yates, J. R., 3rd A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 2004, 76 (14) 4193-201
40. Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.; Sato, S.; Zhu, D.; Conaway, R. C.; Conaway, J. W.; Florens, L.; Washburn, M. P. Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (50) 18928-33
41. Ross, J. mRNA stability in mammalian cells Microbiol. Rev. 1995, 59 (3) 423-50
42. Greenbaum, D.; Colangelo, C.; Williams, K.; Gerstein, M. Comparing protein abundance and mRNA expression levels on a genomic scale Genome Biol. 2003, 4 (9) 117
43. Björck, A. Numerical Methods for least squares problems; SIAM: 1996.
44. Kiemer, L.; Bendtsen, J. D.; Blom, N. NetAcet: prediction of N-terminal acetylation sites Bioinformatics 2005, 21 (7) 1269-70
45. Nolan, R. P.; Lee, K. Dynamic model of CHO cell metabolism Metab. Eng. 2011, 13 (1) 108-24
46. Meleady, P.; Doolan, P.; Henry, M.; Barron, N.; Keenan, J.; O'Sullivan, F.; Clarke, C.; Gammell, P.; Melville, M. W.; Leonard, M.; Clynes, M. Sustained productivity in recombinant Chinese Hamster Ovary (CHO) cell lines: proteome analysis of the molecular basis for a process-related phenotype BMC Biotechnol. 2011, 11, 78
47. Krawitz, D. C.; Forrest, W.; Moreno, G. T.; Kittleson, J.; Champion, K. M. Proteomic studies support the use of multi-product immunoassays to monitor host cell protein impurities Proteomics 2006, 6 (1) 94-110
48. Ahram, M.; Strittmatter, E. F.; Monroe, M. E.; Adkins, J. N.; Hunter, J. C.; Miller, J. H.; Springer, D. L. Identification of shed proteins from Chinese hamster ovary cells: application of statistical confidence using human and mouse protein databases Proteomics 2005, 5 (7) 1815-26
49. Carlage, T.; Hincapie, M.; Zang, L.; Lyubarskaya, Y.; Madden, H.; Mhatre, R.; Hancock, W. S. Proteomic profiling of a high-producing Chinese hamster ovary cell culture Anal. Chem. 2009, 81 (17) 7357-62
50. Zhang, H.; Li, X. J.; Martin, D. B.; Aebersold, R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry Nat. Biotechnol. 2003, 21 (6) 660-6
51. Levine, B. J.; Chodchoy, N.; Marzluff, W. F.; Skoultchi, A. I. Coupling of replication type histone mRNA levels to DNA synthesis requires the stem-loop sequence at the 3 end of the mRNA Proc. Natl. Acad. Sci. U.S.A. 1987, 84 (17) 6189-93
52. Casey, J. L.; Koeller, D. M.; Ramin, V. C.; Klausner, R. D.; Harford, J. B. Iron regulation of transferrin receptor mRNA levels requires iron-responsive elements and a rapid turnover determinant in the 3 untranslated region of the mRNA EMBO J. 1989, 8 (12) 3693-9
53. Scheper, W.; Meinsma, D.; Holthuizen, P. E.; Sussenbach, J. S. Long-range RNA interaction of two sequence elements required for endonucleolytic cleavage of human insulin-like growth factor II mRNAs Mol. Cell. Biol. 1995, 15 (1) 235-45
54. Bernstein, P.; Peltz, S. W.; Ross, J. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro Mol. Cell. Biol. 1989, 9 (2) 659-70
55. Caput, D.; Beutler, B.; Hartog, K.; Thayer, R.; Brown-Shimer, S.; Cerami, A. Identification of a common nucleotide sequence in the 3-untranslated region of mRNA molecules specifying inflammatory mediators Proc. Natl. Acad. Sci. U.S.A. 1986, 83 (6) 1670-4
56. Hargrove, J. L.; Schmidt, F. H. The role of mRNA and protein stability in gene expression FASEB J. 1989, 3 (12) 2360-70
57. Anderson, L.; Seilhamer, J. A comparison of selected mRNA and protein abundances in human liver Electrophoresis 1997, 18 (3-4) 533-7
58. Lichtinghagen, R.; Musholt, P. B.; Lein, M.; Romer, A.; Rudolph, B.; Kristiansen, G.; Hauptmann, S.; Schnorr, D.; Loening, S. A.; Jung, K. Different mRNA and protein expression of matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases 1 in benign and malignant prostate tissue Eur. Urol. 2002, 42 (4) 398-406
59. Lavner, Y.; Kotlar, D. Codon bias as a factor in regulating expression via translation rate in the human genome Gene 2005, 345 (1) 127-38
60. Carlini, D. B. Context-dependent codon bias and messenger RNA longevity in the yeast transcriptome Mol. Biol. Evol. 2005, 22 (6) 1403-11
61. Figueroa, B., Jr.; Sauerwald, T. M.; Mastrangelo, A. J.; Hardwick, J. M.; Betenbaugh, M. J. Comparison of Bcl-2 to a Bcl-2 deletion mutant for mammalian cells exposed to culture insults Biotechnol. Bioeng. 2001, 73 (3) 211-22
62. Figueroa, B., Jr.; Chen, S.; Oyler, G. A.; Hardwick, J. M.; Betenbaugh, M. J. Aven and Bcl-xL enhance protection against apoptosis for mammalian cells exposed to various culture conditions Biotechnol. Bioeng. 2004, 85 (6) 589-600
63. Figueroa, B., Jr.; Sauerwald, T. M.; Oyler, G. A.; Hardwick, J. M.; Betenbaugh, M. J. A comparison of the properties of a Bcl-xL variant to the wild-type anti-apoptosis inhibitor in mammalian cell cultures Metab. Eng. 2003, 5 (4) 230-45