Dynamic mRNA and miRNA profiling of CHO-K1 suspension cell cultures

Biotechnology Journal

Volumn 7, Issue 4, 2012, Pages 500-515

  Bort, Juan A Hernández ^a   Hackl, Matthias ^a   Höflmayer, Helga ^a   Jadhav, Vaibhav ^a   Harreither, Eva ^a   Kumar, Niraj ^a   Ernst, Wolfgang ^a,b   Grillari, Johannes ^a   Borth, Nicole ^a,b  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

Author keywords

CHO cells; Microarray; MicroRNA; MRNA; Transcriptomics

Indexed keywords

BATCH CULTURE; CELLULAR PHENOTYPES; CELLULAR STATE; CHANGING ENVIRONMENT; CHINESE HAMSTER OVARY CELLS; CHO CELL; ENHANCED GROWTH; EXPONENTIAL GROWTH PHASE; EXPRESSION PATTERNS; FED-BATCH CULTIVATION; FUNCTIONAL CAPACITY; HIGH PRODUCTIVITY; MICROARRAY ANALYSIS; MICRORNA; MICRORNAS; MRNA; PATHWAY ANALYSIS; POST-TRANSCRIPTIONAL; RECOMBINANT PROTEIN PRODUCTIONS; REGULATORY MECHANISM; SERUM-FREE CONDITIONS; STATIONARY PHASIS; SUSPENSION CELL CULTURE; TRANSCRIPTOMES; TRANSCRIPTOMICS;

BATCH CELL CULTURE; GENES; MICROARRAYS; PRODUCTIVITY; RECOMBINANT PROTEINS;

TRANSCRIPTION;

MESSENGER RNA; MICRORNA;

ANIMAL CELL; ARTICLE; BACTERIUM CULTURE; CELL CULTURE; CHO CELL; DATA PROCESSING; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; HYBRIDIZATION; MICROARRAY ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CHO CELLS; CRICETINAE; GENE EXPRESSION PROFILING; MICRORNAS; RNA, MESSENGER; TRANSCRIPTOME;

CRICETULUS GRISEUS;

EID: 84859221633     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201100143     Document Type: Article

References (76)

1. Wurm, F. M., Production of recombinant protein therapeutics in cultivated mammalian cells. Nat. Biotechnol. 2004, 22, 1393-1398.
2. Hacker, D. L., De Jesus, M., Wurm, F. M., 25 years of recombinant proteins from reactor-grown cells - where do we go from here? Biotechnol. Adv. 2009, 27, 1023-1027.
3. Javapal, K. P., Wlaschin, K. F., Hu, W. S., Yap, M. G. S., Recombinant protein therapeutics from CHO Cells - 20 Years and counting. Chem. Eng. Prog. 2007, 103, 40-47.
4. Wlaschin, K. F., Nissom, P. M., Gatti, M. e. L., Ong, P. F. et al., EST sequencing for gene discovery in Chinese hamster ovary cells. Biotechnol. Bioeng. 2005, 91, 592-606.
5. Baik, J. Y., Lee, M. S., An, S. R., Yoon, S. K. et al., Initial transcriptome and proteome analyses of low culture temperature-induced expression in CHO cells producing erythropoietin. Biotechnol. Bioeng. 2006, 93, 361-371.
6. Nissom, P. M., Sanny, A., Kok, Y. J., Hiang, Y. T. et al., Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Mol. Biotechnol. 2006, 34, 125-140.
7. Kantardjieff, A., Nissom, P. M., Chuah, S. H., Yusufi, F. et al., Developing genomic platforms for Chinese hamster ovary cells. Biotechnol. Adv. 2009, 27, 1028-1035.
8. Kantardjieff, A., Jacob, N. M., Yee, J. C., Epstein, E. et al., Transcriptome and proteome analysis of Chinese hamster ovary cells under low temperature and butyrate treatment. J. Biotechnol. 2010, 145, 143-159.
9. Doolan, P., Meleady, P., Barron, N., Henry, M. et al., 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, 42-56.
10. Baik, J. Y., Lee, G. M., A DIGE approach for the assessment of differential expression of the CHO proteome under sodium butyrate addition: Effect of Bcl-x(L) overexpression. Biotechnol. Bioeng. 2010, 105, 358-367.
11. Carlage, T., Hincapie, M., Zang, L., Lyubarskaya, Y. et al., Proteomic profiling of a high-producing Chinese hamster ovary cell culture. Anal. Chem. 2009, 81, 7357-7362.
12. Chong, W. P., Reddy, S. G., Yusufi, F. N., Lee, D. Y. et al., Metabolomics-driven approach for the improvement of Chinese hamster ovary cell growth: Overexpression of malate dehydrogenase II. J. Biotechnol. 2010, 147, 116-121.
13. Nolan, R. P., Lee, K., Dynamic model of CHO cell metabolism. Metab. Eng. 2011, 13, 108-124.
14. Chong, W. P., Yusufi, F. N., Lee, D. Y., Reddy, S. G. et al., Metabolomics-based identification of apoptosis-inducing metabolites in recombinant fed-batch CHO culture media. J. Biotechnol. 2011, 151, 218-224.
15. Kim, K., Zakharkin, S. O., Allison, D. B., Expectations, validity, and reality in gene expression profiling. J. Clin. Epidemiol. 2010, 63, 950-959.
16. Clarke, C., Doolan, P., Barron, N., Meleady, P. et al., Predicting cell-specific productivity from CHO gene expression. J. Biotechnol. 2011, 151, 159-165.
17. Ernst, W., Trummer, E., Mead, J., Bessant, C. et al., Evaluation of a genomics platform for cross-species transcriptome analysis of recombinant CHO cells. Biotechnol. J. 2006, 1, 639-650.
18. Trummer, E., Ernst, W., Hesse, F., Schriebl, K. et al., Transcriptional profiling of phenotypically different Epo-Fc expressing CHO clones by cross-species microarray analysis. Biotechnol. J. 2008, 3, 924-937.
19. De Leon Gatti, M., Wlaschin, K. F., Nissom, P. M., Yap, M., Hu, W. S., Comparative transcriptional analysis of mouse hybridoma and recombinant Chinese hamster ovary cells undergoing butyrate treatment. J. Biosci. Bioeng. 2007, 103, 82-91.
20. Wong, D. C., Wong, K. T., Lee, Y. Y., Morin, P. N. et al., Transcriptional profiling of apoptotic pathways in batch and fed-batch CHO cell cultures. Biotechnol. Bioeng. 2006, 94, 373-382.
21. Storey, J., Xiao, W., Leek, J., Tompkins, R., Davis, R., Significance analysis of time course microarray experiments. Proc. Natl. Acad. Sci. USA 2005, 102, 12837-12842.
22. Lee, Y. Y., Wong, K. T., Nissom, P. M., Wong, D. C., Yap, M. G., Transcriptional profiling of batch and fed-batch protein-free 293-HEK cultures. Metab. Eng. 2007, 9, 52-67.
23. Huntzinger, E., Izaurralde, E., Gene silencing by microRNAs: Contributions of translational repression and mRNA decay. Nat. Rev. Genet. 2011, 12, 99-110.
24. Lee, Y., Ahn, C., Han, J., Choi, H. et al., The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425, 415-419.
25. Hutvágner, G., McLachlan, J., Pasquinelli, A. E., Bálint, E. et al., A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293, 834-838.
26. Khvorova, A., Reynolds, A., Jayasena, S. D., Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115, 209-216.
27. Guo, H., Ingolia, N., Weissman, J., Bartel, D., Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466, 835-840.
28. Lewis, B. P., Burge, C. B., Bartel, D. P., Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120, 15-20.
29. Friedman, R. C., Farh, K. K., Burge, C. B., Bartel, D. P., Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19, 92-105.
30. Hackl, M., Jakobi, T., Blom, J., Doppmeier, D. et al., Next-generation sequencing of the Chinese hamster ovary microRNA transcriptome: Identification, annotation and profiling of microRNAs as targets for cellular engineering. J. Biotechnol. 2011, 153, 62-75.
31. Johnson, K. C., Jacob, N. M., Nissom, P. M., Hackl, M. et al., Conserved microRNAs in Chinese hamster ovary cell lines. Biotechnol. Bioeng. 2011, 108, 475-480.
32. Barron, N., Kumar, N., Sanchez, N., Doolan, P. et al., Engineering CHO cell growth and recombinant protein productivity by overexpression of miR-7. J. Biotechnol. 2011, 151, 204-211.
33. Lin, N., Davis, A., Bahr, S., Borgschulte, T. et al., Profiling highly conserved MicroRNA expression in recombinant IgG-producing and parental chinese hamster ovary cells. Biotechnol. Prog. 2010, in press. DOI: 10.1002/btpr.556.
34. Khraiwesh, B., Arif, M. A., Seumel, G. I., Ossowski, S. et al., Transcriptional control of gene expression by microRNAs. Cell 2010, 140, 111-122.
35. Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A. et al., Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433, 769-773.
36. Park, H., An, S., Choe, T., Change of insulin-like growth factor gene expression in Chinese hamster ovary cells cultured in serum-free media. Biotechnol. Bioprocess Eng. 2006, 11, 319-324.
37. Birzele, F., Schaub, J., Rust, W., Clemens, C. et al., Into the unknown: Expression profiling without genome sequence information in CHO by next generation sequencing. Nucleic Acids Res. 2010, 38, 3999-4010.
38. Gammell, P., Barron, N., Kumar, N., Clynes, M., Initial identification of low temperature and culture stage induction of miRNA expression in suspension CHO-K1 cells. J. Biotechnol. 2007, 130, 213-218.
39. Koh, T. C., Lee, Y. Y., Chang, S. Q., Nissom, P. M., Identification and expression analysis of miRNAs during batch culture of HEK-293 cells. J. Biotechnol. 2009, 140, 149-155.
40. Tzur, G., Israel, A., Levy, A., Benjamin, H. et al., Comprehensive gene and microRNA expression profiling reveals a role for microRNAs in human liver development. PLoS One 2009, 4, e7511-e7513.
41. Lanza, G., Ferracin, M., Gafà, R., Veronese, A. et al., mRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer. Mol. Cancer 2007, 6, 54.
42. Hackl, M., Brunner, S., Fortschegger, K., Schreiner, C. et al., miR-17, miR-19b, miR-20a, and miR-106a are down-regulated in human aging. Aging Cell 2010, 9, 291-296.
43. Bort, J. A., Stern, B., Borth, N., CHO-K1 host cells adapted to growth in glutamine-free medium by FACS-assisted evolution. Biotechnol. J. 2010, 5, 1090-1097.
44. Jung, M., Schaefer, A., Steiner, I., Kempkensteffen, C. et al., Robust microRNA stability in degraded RNA preparations from human tissue and cell samples. Clin. Chem. 2010, 56, 998-1006.
45. Yee, J. C., Wlaschin, K. F., Chuah, S. H., Nissom, P. M., Hu, W. S., Quality assessment of cross-species hybridization of CHO transcriptome on a mouse DNA oligo microarray. Biotechnol. Bioeng. 2008, 101, 1359-1365.
46. Cleveland, W., Devlin, S., Locally weighted regression: An approach to regression analysis by local fitting. J. Am. Stat. Assoc. 1988, 83, 596-610.
47. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B (Methodological) 1995, 57, 289-300.
48. Rozen, S., Skaletsky, H., Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132, 365-386.
49. Smyth, G. K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3, Article 3.
50. Smyth, G. K., Michaud, J., Scott, H. S., Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 2005, 21, 2067-2075.
51. Livak, K. J., Schmittgen, T. D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402-408.
52. Sturn, A., Quackenbush, J., Trajanoski, Z., Genesis: Cluster analysis of microarray data. Bioinformatics 2002, 18, 207-208.
53. Huang, d. W., Sherman, B., Lempicki, R., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4, 44-57.
54. Dennis, G. J., Sherman, B., Hosack, D., Yang, J. et al., DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol. 2003, 4, P3.
55. Antonov, A., Dietmann, S., Wong, P., Lutter, D., Mewes, H., GeneSet2miRNA: Finding the signature of cooperative miRNA activities in the gene lists. Nucl. Acids Res. 2009, 37, W323-328.
56. Xiao, F., Zuo, Z., Cai, G., Kang, S. et al., miRecords: An integrated resource for microRNA-target interactions. Nucleic Acids Res. 2009, 37, D105-110.
57. Bahr, S. M., Borgschulte, T., Kayser, K. J., Lin, N., Using microarray technology to select housekeeping genes in Chinese hamster ovary cells. Biotechnol. Bioeng. 2009, 104, 1041-1046.
58. Lu, M., Shi, B., Wang, J., Cao, Q., Cui, Q., TAM: A method for enrichment and depletion analysis of a microRNA category in a list of microRNAs. BMC Bioinformatics 2010, 11, 419.
59. Cloonan, N., Brown, M. K., Steptoe, A. L., Wani, S. et al., The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol. 2008, 9, R127.
60. Chun-Zhi, Z., Lei, H., An-Ling, Z., Yan-Chao, F. et al., MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer 2010, 10, 367.
61. Moskwa, P., Buffa, F. M., Pan, Y., Panchakshari, R. et al., miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol. Cell. 2011, 41, 210-220.
62. Wyman, C., Ristic, D., Kanaar, R., Homologous recombination-mediated double-strand break repair. DNA Repair (Amst) 2004, 3, 827-833.
63. Li, X., Heyer, W.-D., Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 2008, 18, 99-113.
64. Serrano, L., Liang, L., Chang, Y., Deng, L. et al., Homologous recombination conserves DNA sequence integrity throughout the cell cycle in embryonic stem cells. Stem Cells Dev. 2011, 20, 363-374.
65. Abraham, J., Lemmers, B., Hande, M. P., Moynahan, M. E. et al., Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J. 2003, 22, 6137-6147.
66. Rawlings, J. S., Rosler, K. M., Harrison, D. A., The JAK/STAT signaling pathway. J. Cell Sci. 2004, 117, 1281-1283.
67. Saltiel, A. R., Kahn, C. R., Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001, 414, 799-806.
68. Shimomura, I., Bashmakov, Y., Ikemoto, S., Horton, J. D. et al., Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. USA 1999, 96, 13656-13661.
69. Ogawa, W., Matozaki, T., Kasuga, M., Role of binding proteins to IRS-1 in insulin signalling. Mol. Cell. Biochem. 1998, 182, 13-22.
70. Guan, K. L., Jenkins, C. W., Li, Y., Nichols, M. A. et al., Growth suppression by p18, a p16INK4/MTS1- and p14INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev. 1994, 8, 2939-2952.
71. Ivanovska, I., Ball, A. S., Diaz, R. L., Magnus, J. F. et al., MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol. Cell. Biol. 2008, 28, 2167-2174.
72. Sengupta, S., Nie, J., Wagner, R. J., Yang, C. et al., MicroRNA 92b controls the G1/S checkpoint gene p57 in human embryonic stem cells. Stem Cells 2009, 27, 1524-1528.
73. Volinia, S., Calin, G. A., Liu, C.-G., Ambs, S. et al., A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 2006, 103, 2257-2261.
74. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P., Burge, C. B., Prediction of mammalian microRNA targets. Cell 2003, 115, 787-798.
75. He, L., Thomson, J. M., Hemann, M. T., Hernando-Monge, E. et al., A microRNA polycistron as a potential human oncogene. Nature 2005, 435, 828-833.
76. Breslauer, K. J., Frank, R., Blöcker, H., Marky, L. A., Predicting DNA duplex stability from the base sequence. Proc. Natl. Acad. Sci. USA 1986, 83, 3746-3750.