Temperature-sensitive miR-483 is a conserved regulator of recombinant protein and viral vector production in mammalian cells

Biotechnology and Bioengineering

Volumn 113, Issue 4, 2016, Pages 830-841

  Emmerling, Verena V ^a,b   Fischer, Simon ^c   Stiefel, Fabian ^c   Holzmann, Karlheinz ^a   Handrick, René ^c   Hesse, Friedemann ^c   Hörer, Markus ^b,d   Kochanek, Stefan ^a   Otte, Kerstin ^c  

^a UNIVERSITY OF ULM   (Germany)

^b Rentschler Biotechnologie GmbH   (Germany)

^c BIBERACH UNIVERSITY OF APPLIED SCIENCES   (Germany)

^d VBBio Consultant   (Germany)

Author keywords

Adeno associated virus; HeLa packaging cells; Hypothermia; MicroRNA; MiR 483; Viral vector

Indexed keywords

ANTIBODIES; CYTOLOGY; GENE EXPRESSION; GENES; HYPOTHERMIA; LOW TEMPERATURE PRODUCTION; MAMMALS; MONOCLONAL ANTIBODIES; PROTEINS; RECOMBINANT PROTEINS; RNA; TEMPERATURE; VIRUSES;

ADENO-ASSOCIATED VIRUS; BIOPROCESS OPTIMIZATION; CHINESE HAMSTER OVARY CELLS; MICRORNAS; MIR-483; MONOCLONAL ANTIBODIES (MABS); RECOMBINANT ADENO-ASSOCIATED VIRUS; VIRAL VECTORS;

CELL ENGINEERING;

MICRORNA; MICRORNA 483; MONOCLONAL ANTIBODY; RECOMBINANT PROTEIN; SMALL UNTRANSLATED RNA; SOMATOMEDIN B; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL CELL; ANTIBODY PRODUCTION; ARTICLE; BINDING SITE; CELL CULTURE; CELL ENGINEERING; CELL SURVIVAL; CELLS BY BODY ANATOMY; CHO CELL LINE; CONTROLLED STUDY; FEMALE; GENE IDENTIFICATION; HELA CELL LINE; HUMAN; HUMAN CELL; LOW TEMPERATURE; LOW TEMPERATURE PROCEDURES; MAMMAL CELL; MILD HYPOTHERMIA; NONHUMAN; PROTEIN EXPRESSION; RNA SEQUENCE; TEMPERATURE SENSITIVITY; UPREGULATION; VIRUS RECOMBINANT; ANIMAL; BIOSYNTHESIS; CRICETULUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; RADIATION RESPONSE; TEMPERATURE;

ANIMALS; CELL SURVIVAL; CHO CELLS; CRICETULUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICRORNAS; RECOMBINANT PROTEINS; TEMPERATURE;

EID: 84959473263     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25853     Document Type: Article

References (65)

1. Al-Fageeh MB, Marchant RJ, Carden MJ, Smales CM. 2006. The cold-shock response in cultured mammalian cells: Harnessing the response for the improvement of recombinant protein production. Biotechnol Bioeng 93(5):829-835.
2. Avraham R, Yarden Y. 2012. Regulation of signalling by microRNAs. Biochem Soc Trans 40(1):26-30.
3. Baik JY, Lee MS, An SR, Yoon SK, Joo EJ, Kim YH, Park HW, Lee GM. 2006. Initial transcriptome and proteome analyses of low culture temperature-induced expression in CHO cells producing erythropoietin. Biotechnol Bioeng 93(2):361-371.
4. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136(2):215-233.
5. Beer C, Buhr P, Hahn H, Laubner D, Wirth M. 2003. Gene expression analysis of murine cells producing amphotropic mouse leukaemia virus at a cultivation temperature of 32 and 37 degrees C. J Gen Virol 84(Pt 7):1677-1686.
6. Bertero T, Gastaldi C, Bourget-Ponzio I, Imbert V, Loubat A, Selva E, Busca R, Mari B, Hofman P, Barbry P, Meneguzzi G, Ponzio G, Rezzonico R. 2011. MiR-483-3p controls proliferation in wounded epithelial cells. FASEB J 25(9):3092-3105.
7. Bertero T, Gastaldi C, Bourget-Ponzio I, Mari B, Meneguzzi G, Barbry P, Ponzio G, Rezzonico R. 2013. CDC25A targeting by miR-483-3p decreases CCND-CDK4/6 assembly and contributes to cell cycle arrest. Cell Death Differ 20(6):800-811.
8. Buggele WA, Johnson KE, Horvath CM. 2012. Influenza A virus infection of human respiratory cells induces primary microRNA expression. J Biol Chem 287(37):31027-31040.
9. Chadeuf G, Favre D, Tessier J, Provost N, Nony P, Kleinschmidt J, Moullier P, Salvetti A. 2000. Efficient recombinant adeno-associated virus production by a stable rep-cap HeLa cell line correlates with adenovirus-induced amplification of the integrated rep-cap genome. J Gene Med 2(4):260-268.
10. Chen Y, Jacamo R, Konopleva M, Garzon R, Croce C, Andreeff M. 2013. CXCR4 downregulation of let-7a drives chemoresistance in acute myeloid leukemia. J Clin Invest 123(6):2395-2407.
11. Clark KR, Voulgaropoulou F, Fraley DM, Johnson PR. 1995. Cell lines for the production of recombinant adeno-associated virus. Hum Gene Ther 6(10):1329-1341.
12. Da Sacco L, Masotti A. 2012. Recent Insights and Novel Bioinformatics Tools to Understand the Role of MicroRNAs Binding to 5′ Untranslated Region. Int J Mol Sci 14(1):480-495.
13. Emmerling VV, Pegel A, Milian EG, Venereo-Sanchez A, Kunz M, Wegele J, Kamen AA, Kochanek S, Hoerer M. 2015. Rational plasmid design and bioprocess optimization to enhance recombinant adeno-associated virus (AAV) productivity in mammalian cells. Biotechnol J. doi: 10.1002/biot.201500176.
14. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9(2):102-114.
15. Fischer S, Buck T, Wagner A, Ehrhart C, Giancaterino J, Mang S, Schad M, Mathias S, Aschrafi A, Handrick R, Otte K. 2014. A functional high-content miRNA screen identifies miR-30 family to boost recombinant protein production in CHO cells. Biotechnol J 9(10):1279-1292.
16. Fischer S, Paul AJ, Wagner A, Mathias S, Geiss M, Schandock F, Domnowski M, Zimmermann J, Handrick R, Hesse F, Otte K. 2015. miR-2861 as novel HDAC5 inhibitor in CHO cells enhances productivity while maintaining product quality. Biotechnol Bioeng 112:2142-2153. doi: 10.1002/bit.25626.
17. Fu H, Tie Y, Xu C, Zhang Z, Zhu J, Shi Y, Jiang H, Sun Z, Zheng X. 2005. Identification of human fetal liver miRNAs by a novel method. FEBS Lett 579(17):3849-3854.
18. Gammell P, Barron N, Kumar N, Clynes M. 2007. Initial identification of low temperature and culture stage induction of miRNA expression in suspension CHO-K1 cells. J Biotechnol 130(3):213-218.
19. Gao GP, Qu G, Faust LZ, Engdahl RK, Xiao W, Hughes JV, Zoltick PW, Wilson JM. 1998. High-titer adeno-associated viral vectors from a Rep/Cap cell line and hybrid shuttle virus. Hum Gene Ther 9(16):2353-2362.
20. Hao J, Zhang S, Zhou Y, Hu X, Shao C. 2011. MicroRNA 483-3p suppresses the expression of DPC4/Smad4 in pancreatic cancer. FEBS Lett 585(1):207-213.
21. Henikoff S, Henikoff JG. 1992. Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89(22):10915-10919.
22. Inoue N, Russell DW. 1998. Packaging cells based on inducible gene amplification for the production of adeno-associated virus vectors. J Virol 72(9):7024-7031.
23. Jadhav V, Hackl M, Klanert G, Hernandez Bort JA, Kunert R, Grillari J, Borth N. 2014. Stable overexpression of miR-17 enhances recombinant protein production of CHO cells. J Biotechnol 175:38-44.
24. Jardon M, Garnier A. 2003. PH, pCO2, and temperature effect on R-adenovirus production. Biotechnol Prog 19(1):202-208.
25. Kakinuma N, Zhu Y, Wang Y, Roy BC, Kiyama R. 2009. Kank proteins: Structure, functions and diseases. Cell Mol Life Sci 66(16):2651-2659.
26. Kaptein LC, Greijer AE, Valerio D, van Beusechem VW. 1997. Optimized conditions for the production of recombinant amphotropic retroviral vector preparations. Gene Ther 4(2):172-176.
27. Kaufmann H, Mazur X, Fussenegger M, Bailey JE. 1999. Influence of low temperature on productivity, proteome and protein phosphorylation of CHO cells. Biotechnol Bioeng 63(5):573-582.
28. Kozomara A, Griffiths-Jones S. 2014. MiRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42(Database issue):D68-D73.
29. Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11(9):597-610.
30. Kumar N, Gammell P, Meleady P, Henry M, Clynes M. 2008. Differential protein expression following low temperature culture of suspension CHO-K1 cells. BMC Biotechnol 8:42.
31. Lee S, Vasudevan S. 2013. Post-transcriptional stimulation of gene expression by microRNAs. Adv Exp Med Biol 768:97-126.
32. Liang T, Yang C, Li P, Liu C, Guo L. 2014. Genetic analysis of loop sequences in the let-7 gene family reveal a relationship between loop evolution and multiple isomiRs. PLoS ONE 9(11):e113042.
33. Liu G, Min H, Yue S, Chen CZ. 2008. Pre-miRNA loop nucleotides control the distinct activities of mir-181a-1 and mir-181c in early T cell development. PLoS ONE 3(10):e3592.
34. Liu M, Roth A, Yu M, Morris R, Bersani F, Rivera MN, Lu J, Shioda T, Vasudevan S, Ramaswamy S, Maheswaran S, Diederichs S, Haber DA. 2013. The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev 27(23):2543-2548.
35. Liu X, Voulgaropoulou F, Chen R, Johnson PR, Clark KR. 2000. Selective Rep-Cap gene amplification as a mechanism for high-titer recombinant AAV production from stable cell lines. Mol Ther 2(4):394-403.
36. Loh WP, Loo B, Zhou L, Zhang P, Lee DY, Yang Y, Lam KP. 2014. Overexpression of microRNAs enhances recombinant protein production in Chinese hamster ovary cells. Biotechnol J 9(9):1140-1151.
37. MacLaren RE, Groppe M, Barnard AR, Cottriall CL, Tolmachova T, Seymour L, Clark KR, During MJ, Cremers FP, Black GC, Lotery AJ, Downes SM, Webster AR, Seabra MC. 2014. Retinal gene therapy in patients with choroideremia: Initial findings from a phase 1/2 clinical trial. Lancet 383(9923):1129-1137.
38. Maguire AM, High KA, Auricchio A, Wright JF, Pierce EA, Testa F, Mingozzi F, Bennicelli JL, Ying GS, Rossi S, Fulton A, Marshall KA, Banfi S, Chung DC, Morgan JI, Hauck B, Zelenaia O, Zhu X, Raffini L, Coppieters F, De Baere E, Shindler KS, Volpe NJ, Surace EM, Acerra C, Lyubarsky A, Redmond TM, Stone E, Sun J, McDonnell JW, Leroy BP, Simonelli F, Bennett J. 2009. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: A phase 1 dose-escalation trial. Lancet 374(9701):1597-1605.
39. Martin J, Frederick A, Luo Y, Jackson R, Joubert M, Sol B, Poulin F, Pastor E, Armentano D, Wadsworth S, Vincent K. 2013. Generation and characterization of adeno-associated virus producer cell lines for research and preclinical vector production. Hum Gene Ther Methods 24(4):253-269.
40. Moore A, Mercer J, Dutina G, Donahue CJ, Bauer KD, Mather JP, Etcheverry T, Ryll T. 1997. Effects of temperature shift on cell cycle, apoptosis and nucleotide pools in CHO cell batch cultues. Cytotechnology 23(1-3):47-54.
41. Nathwani AC, Tuddenham EG, Rangarajan S, Rosales C, McIntosh J, Linch DC, Chowdary P, Riddell A, Pie AJ, Harrington C, O'Beirne J, Smith K, Pasi J, Glader B, Rustagi P, Ng CY, Kay MA, Zhou J, Spence Y, Morton CL, Allay J, Coleman J, Sleep S, Cunningham JM, Srivastava D, Basner-Tschakarjan E, Mingozzi F, High KA, Gray JT, Reiss UM, Nienhuis AW, Davidoff AM. 2011. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365(25):2357-2365.
42. Orom UA, Nielsen FC, Lund AH. 2008. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30(4):460-471.
43. Otte K, Choudhury D, Charalambous M, Engstrom W, Rozell B. 1998. A conserved structural element in horse and mouse IGF2 genes binds a methylation sensitive factor. Nucleic Acids Res 26(7):1605-1612.
44. Pasquinelli AE. 2012. MicroRNAs and their targets: Recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13(4):271-282.
45. Qiao Y, Ma N, Wang X, Hui Y, Li F, Xiang Y, Zhou J, Zou C, Jin J, Lv G, and Others. 2011. MiR-483-5p controls angiogenesis in vitro and targets serum response factor. FEBS Lett 585(19):3095-3100.
46. Randle PJ. 1986. Fuel selection in animals. Biochem Soc Trans 14(5):799-806.
47. Rieder CL, Cole RW. 2002. Cold-shock and the Mammalian cell cycle. Cell Cycle 1(3):169-175.
48. Salvetti A, Oreve S, Chadeuf G, Favre D, Cherel Y, Champion-Arnaud P, David-Ameline J, Moullier P. 1998. Factors influencing recombinant adeno-associated virus production. Hum Gene Ther 9(5):695-706.
49. Sarkar S, Roy BC, Hatano N, Aoyagi T, Gohji K, Kiyama R. 2002. A novel ankyrin repeat-containing gene (Kank) located at 9p24 is a growth suppressor of renal cell carcinoma. J Biol Chem 277(39):36585-36591.
50. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101-1108.
51. Scott S, Marchant R, Al-Fageeh M, Underhill M, Smales C. 2007. The molecular response(s) during cellular adaptation to, and recovery from, sub-physiological temperatures. In: Al-Rubeai M, Fussenegger M, editors. Systems biology. Netherlands: Springer. p 185-212.
52. Shi Y, Seto E, Chang LS, Shenk T. 1991. Transcriptional repression by YY1, a human GLI-Kruppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67(2):377-388.
53. Song Q, Xu Y, Yang C, Chen Z, Jia C, Chen J, Zhang Y, Lai P, Fan X, Zhou X, Lin J, Li M, Ma W, Luo S, Bai X. 2014. MiR-483-5p promotes invasion and metastasis of lung adenocarcinoma by targeting RhoGDI1 and ALCAM. Cancer Res 74(11):3031-3042.
54. Strotbek M, Florin L, Koenitzer J, Tolstrup A, Kaufmann H, Hausser A, Olayioye MA. 2013. Stable microRNA expression enhances therapeutic antibody productivity of Chinese hamster ovary cells. Metab Eng 20:157-166.
55. Tamayose K, Hirai Y, Shimada T. 1996. A new strategy for large-scale preparation of high-titer recombinant adeno-associated virus vectors by using packaging cell lines and sulfonated cellulose column chromatography. Hum Gene Ther 7(4):507-513.
56. Teicher BA, Fricker SP. 2010. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 16(11):2927-2931.
57. uniQure. 2012. uniQure's Glybera® First Gene Therapy Approved by European Commission. http://www.uniqure.com/news/167/182/. p First Gene Therapy Approved by European Commission.
58. Veronese A, Lupini L, Consiglio J, Visone R, Ferracin M, Fornari F, Zanesi N, Alder H, D'Elia G, Gramantieri L, Bolondi L, Lanza G, Querzoli P, Angioni A, Croce CM, Negrini M. 2010. Oncogenic role of miR-483-3p at the IGF2/483 locus. Cancer Res 70(8):3140-3149.
59. Wang L, Shi M, Hou S, Ding B, Liu L, Ji X, Zhang J, Deng Y. 2012. MiR-483-5p suppresses the proliferation of glioma cells via directly targeting E RK1. FEBS Lett 586(9):1312-1317.
60. Wechuck JB, Ozuer A, Goins WF, Wolfe D, Oligino T, Glorioso JC, Ataai MM. 2002. Effect of temperature, medium composition, and cell passage on production of herpes-based viral vectors. Biotechnol Bioeng 79(1):112-119.
61. Wulhfard S, Tissot S, Bouchet S, Cevey J, De Jesus M, Hacker DL, Wurm FM. 2008. Mild hypothermia improves transient gene expression yields several fold in Chinese hamster ovary cells. Biotechnol Prog 24(2):458-465.
62. Xiao S, Chen Y-C, Betenbaugh MJ, Martin SE, Shiloach J. 2015. MiRNA mimic screen for improved expression of functional neurotensin receptor from HEK 293 cells. Biotechnol Bioeng 112:1632-1643. doi: 10.1002/bit.25567.
63. Yoon SK, Song JY, Lee GM. 2003. Effect of low culture temperature on specific productivity, transcription level, and heterogeneity of erythropoietin in Chinese hamster ovary cells. Biotechnol Bioeng 82(3):289-298.
64. Yue SB, Trujillo RD, Tang Y, O'Gorman WE, Chen CZ. 2011. Loop nucleotides control primary and mature miRNA function in target recognition and repression. RNA Biol 8(6):1115-1123.
65. Zhou M, Crawford Y, Ng D, Tung J, Pynn AF, Meier A, Yuk IH, Vijayasankaran N, Leach K, Joly J, Snedecor B, Shen A. 2011. Decreasing lactate level and increasing antibody production in Chinese Hamster Ovary cells (CHO) by reducing the expression of lactate dehydrogenase and pyruvate dehydrogenase kinases. J Biotechnol 153(1-2):27-34.