Overexpression of microRNAs enhances recombinant protein production in Chinese hamster ovary cells

Biotechnology Journal

Volumn 9, Issue 9, 2014, Pages 1140-1151

  Loh, Wan Ping ^a   Loo, Bernard ^a   Zhou, Lihan ^b   Zhang, Peiqing ^a   Lee, Dong Yup ^a,c   Yang, Yuansheng ^a   Lam, Kong Peng ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell engineering; CHO cells; MicroRNA profiling; MiR 17 92 cluster; Recombinant protein production

Indexed keywords

CELLS; CYTOLOGY; GENE EXPRESSION; LAKES; MONOCLONAL ANTIBODIES; POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; RNA;

CHINESE HAMSTER OVARY CELLS; CHO CELL; MICRORNA PROFILING; MIR-17-92 CLUSTER; NEXT-GENERATION SEQUENCING; QUANTITATIVE REAL TIME PCR; RECOMBINANT PROTEIN PRODUCTIONS; SPECIFIC PRODUCTIVITY;

CELL ENGINEERING;

MICRORNA; MONOCLONAL ANTIBODY; RECOMBINANT PROTEIN;

ANIMAL; CELL ENGINEERING; CELL LINE; CELL PROLIFERATION; CHO CELL LINE; CRICETULUS; GENETICS; PROCEDURES;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL ENGINEERING; CELL LINE; CELL PROLIFERATION; CHO CELLS; CRICETULUS; MICRORNAS; RECOMBINANT PROTEINS;

EID: 84906950855     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400050     Document Type: Article

References (54)

1. Butler, M., Meneses-Acosta, A., Recent advances in technology supporting biopharmaceutical production from mammalian cells. Appl. Microbiol. Biotechnol. 2012, 96, 885-894.
2. Matasci, M., Hacker, D. L., Baldi, L., Wurm, F. M., Recombinant therapeutic protein production in cultivated mammalian cells: Current status and future prospects. Drug Discov. Today Technol. 2008, 5, e37-e42.
3. Zhu, J., Mammalian cell protein expression for biopharmaceutical production. Biotechnol. Adv. 2012, 30, 1158-1170.
4. Jayapal, 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.
5. Davis, R., Schooley, K., Rasmussen, B., Thomas, J. et al., Effect of PDI overexpression on recombinant protein secretion in CHO cells. Biotechnol. Prog. 2000, 16, 736-743.
6. Lakkaraju, A. K., Mary, C., Scherrer, A., Johnson, A. E. et al., SRP keeps polypeptides translocation-competent by slowing translation to match limiting ER-target sites. Cell 2008, 133, 440-451.
7. Ku, S. C. Y., Ng, D. T. W., Yap, M. G. S., Chao, S. H., Effects of overexpression of X-box binding protein 1 on recombinant protein production in Chinese hamster ovary and NS0 myeloma cells. Biotechnol. Bioeng. 2008, 99, 155-164.
8. Dinnis, D. M., James, D. C., Engineering mammalian cell factories for improved recombinant monoclonal antibody production: Lessons from nature? Biotechnol. Bioeng. 2005, 91, 180-189.
9. Olsen, P., Ambros, V., The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 1999, 216, 671-680.
10. Guo, H., Ingolia, N. T., Weissman, J. S., Bartel, D. P., Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466, 835-840.
11. Bommer, G. T., Gerin, I., Feng, Y., Kaczorowski, A. J. et al., p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 2007, 17, 1298-1307.
12. Fish, J. E., Santoro, M. M., Morton, S. U., Yu, S. et al., miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 2008, 15, 272-284.
13. Harris, T. A., Yamakuchi, M., Ferlito, M., Mendell, J. T. et al., MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc. Natl. Acad. Sci. USA 2008, 105, 1516-1521.
14. Wang, S., Aurora, A. B., Johnson, B. A., Qi, X. et al., The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev. Cell 2008, 15, 261-271.
15. Barron, N., Sanchez, N., Kelly, P., Clynes, M., MicroRNAs: Tiny targets for engineering CHO cell phenotypes? Biotechnol. Lett. 2011, 33, 11-21.
16. Müller, D., Katinger, H., Grillari, J., MicroRNAs as targets for engineering of CHO cell factories. Trends Biotechnol. 2008, 26, 359-365.
17. Jadhav, V., Hackl, M., Druz, A., Shridhar, S. et al., CHO microRNA engineering is growing up: Recent successes and future challenges. Biotechnol. Adv. 2013, 31, 1501-1513.
18. Klanert, G., Jadhav, V., Chanoumidou, K., Grillari, J. et al., Endogenous microRNA clusters outperform chimeric sequence clusters in Chinese hamster ovary cells. Biotechnol. J. 2014, 9, 538-544.
19. 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.
20. 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.
21. Hammond, S., Swanberg, J. C., Polson, S. W., Lee, K. H., Profiling conserved microRNA expression in recombinant CHO cell lines using Illumina sequencing. Biotechnol. Bioeng. 2012, 109, 1371-1375.
22. Bort, J. A. H., Hackl, M., Höflmayer, H., Jadhav, V. et al., Dynamic mRNA and miRNA profiling of CHO-K1 suspension cell cultures. Biotechnol. J. 2012, 7, 500-515.
23. Clarke, C., Henry, M., Doolan, P., Kelly, S. et al., Integrated miRNA, mRNA and protein expression analysis reveals the role of post-transcriptional regulation in controlling CHO cell growth rate. BMC Genomics 2012, 13, 656.
24. Druz, A., Chu, C., Majors, B., Santuary, R. et al., A novel microRNA mmu-miR-466h affects apoptosis regulation in mammalian cells. Biotechnol. Bioeng. 2011, 108, 1651-1661.
25. 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.
26. 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.
27. 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. 2011, 27, 1163-1171.
28. Druz, A., Son, Y. J., Betenbaugh, M., Shiloach, J., Stable inhition of mmu-miR-466h-5p improves apoptosis resistance and protein production in CHO cells. Metab. Eng. 2013, 16, 87-94.
29. Meleady, P., Gallagher, M., Clarke, C., Henry, M. et al., Impact of miR-7 over-expression on the proteome of Chinese hamster ovary cells. J. Biotechnol. 2012, 160, 251-262.
30. Jadhav, V., Hackl, M., Bort, J. A. H., Wieser, M. et al., A screening method to assess biological effects of microRNA overexpression in Chinese hamster ovary cells. Biotechnol. Bioeng. 2012, 109, 1376-1385.
31. Jadhav, V., Hackl, M., Klanert, G., Bort, J. A. H. et al., Stable overexpression of miR-17 enhances recombinant protein production of CHO cells. J. Biotechnol. 2014, 175, 38-44.
32. Ho, S. C. L., Bardor, M., Feng, H., Mariati, et al., IRES-mediated tricistronic vectors for enhancing generation of high monoclonal antibody expressing CHO cell lines. J. Biotechnol. 2012, 157, 130-139.
33. Wan, G., Lim, Q., Too, H., High-performance quantification of mature microRNAs by real-time RT-PCR using deoxyuridine-incorporated oligonucleotides and hemi-nested primers. RNA 2010, 16, 1436-1445.
34. 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.
35. Melmer, M., Stangler, T., Schiefermeier, M., Brunner, W. et al., HILIC analysis of fluorescence-labeled N-glycans from recombinant biopharmaceuticals. Anal. Bioanal. Chem. 2010, 398, 905-914.
36. Royle, L., Campbell, M. P., Radcliffe, C. M., White, D. M. et al., HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Anal. Biochem. 2008, 376, 1-12.
37. Chusainow, J., Yang, Y. S., Yeo, J. H., Toh, P. C. et al., A study of monoclonal antibody-producing CHO cell lines: What makes a stable high producer? Biotechnol. Bioeng. 2009, 102, 1182-1196.
38. Peng, G., Yuan, Y., He, Q., Wu, W. et al., MicroRNA let-7e regulates the expression of caspase-3 during apoptosis of PC12 cells following anoxia/reoxygenation injury. Brain Res. Bull. 2011, 86, 272-276.
39. Qu, S., Yao, Y., Shang, C., Xue, Y. et al., MicroRNA-330 is an oncogenic factor in glioblastoma cells by regulating SH3GL2 gene. PLos One 2012, 7, e46010.
40. Conkrite, K., Sundby, M., Mukai, S., Thomson, J. M. et al., Mir-17∼92 cooperates with rb pathway mutations to promote retinoblastoma. Genes Dev. 2011, 25, 1734-1745.
41. Connolly, E., Melegari, M., Landgraf, P., Tchaikovskaya, T. et al., Elevated expression of the mir-17-92 polycistron and mir-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype. Am. J. Pathol. 2008, 173, 856-864.
42. Tsitsiou, E., Lindsay, M. A., Micrornas and the immune response. Curr. Opin. Pharmacol. 2009, 9, 514-520.
43. Keck, R., Nayak, N., Lerner, L., Raju, S. et al., Characterization of a complex glycoprotein whose variable metabolic clearance in humans is dependent on terminal N-acetylglucossamine content. Biologicals 2008, 36, 49-60.
44. Shields, R. L., Lai, J., Keck, R., O'Connell, L. Y. et al., Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 2002, 277, 26733-26740.
45. Fontana, L., Fiori, M. E., Albini, S., Cifaldi, L. et al., Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 2008, 3, e2236.
46. Olive, V., Bennett, M. J., Walker, J. C., Ma, C. et al., miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009, 23, 2839-2849.
47. Mu, P., Han, Y. C., Betel, D., Yao, E. et al., Genetic dissection of the miR-17∼92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 2009, 23, 2806-2811.
48. Ventura, A., Young, A. G., Winslow, M. M., Lintault, L. et al., Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008, 132, 875-886.
49. Bonauer, A., Carmona, G., Iwasaki, M., Mione, M. et al., MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 2009, 324, 1710-1713.
50. 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.
51. Kumar, P., Luo, Y., Tudela, C., Alexander, J. M. et al., The c-Myc-regulated microRNA-17∼92 (miR-17∼92) and miR-106a∼363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol. Cell Biol. 2013, 33, 1782-1796.
52. He, M., Wang, Q. Y., Yin, Q. Q., Tang, J. et al., HIF-1α downregulates miR-17/20a directly targeting p21 and STAT3: A role in myeloid leukemic cell differentiation. Cell Death Differ. 2013, 20, 408-418.
53. Mitra, D., Das, P. M., Huynh, F. C., Jones, F. E., Jumonji/ARID1 B (JARID1B) protein promotes breast tumor cell cycle progression through epigenetic repression of microRNA let-7e. J. Biol. Chem. 2011, 286, 40531-40535.
54. Sun, M. M., Li, J. F., Guo, L. L., Xiao, H. T. et al., TGF-β1 suppression of microRNA-450b-5p expression: A novel mechanism for blocking myogenic differentiation of rhabdomyosarcoma. Oncogene 2014, 33, 2075-2086.