A mechanistic dissection of polyethylenimine mediated transfection of CHO cells: To enhance the efficiency of recombinant DNA utilization

Biotechnology Progress

Volumn 30, Issue 5, 2014, Pages 1161-1170

  Mozley, Olivia L ^a   Thompson, Ben C ^a   Fernandez Martell, Alejandro ^a   James, David C ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Biopharmaceutical; Chinese hamster ovary cell; Gene delivery; Heparan sulphate proteoglycan; Nonviral vectors; Polyethylenimine; Transfection; Transient gene expression

Indexed keywords

ALKALINITY; CELL MEMBRANES; CLONING; CYTOLOGY; DESIGN OF EXPERIMENTS; DNA; EFFICIENCY; GENE EXPRESSION; GENE TRANSFER; HYDROPHOBICITY; NONIONIC SURFACTANTS; PHOSPHATASES; RECOMBINANT PROTEINS; SULFUR COMPOUNDS; SURFACE CHARGE; ZETA POTENTIAL;

BIOPHARMACEUTICAL; CHINESE HAMSTER OVARY CELLS; GENE DELIVERY; NONVIRAL VECTORS; POLYETHYLENIMINES; PROTEOGLYCANS; TRANSFECTION; TRANSIENT GENE EXPRESSIONS;

MOLECULAR BIOLOGY;

CRICETULUS GRISEUS;

POLYETHYLENEIMINE; PROTEOHEPARAN SULFATE; RECOMBINANT DNA;

ALKYLATION; ANIMAL; CELL MEMBRANE; CHEMICAL PHENOMENA; CHEMISTRY; CHO CELL LINE; CRICETULUS; GENETIC TRANSFECTION; HAMSTER; MEMBRANE FLUIDITY; METABOLISM; STATIC ELECTRICITY;

ALKYLATION; ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; DNA, RECOMBINANT; HEPARAN SULFATE PROTEOGLYCANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE FLUIDITY; POLYETHYLENEIMINE; STATIC ELECTRICITY; TRANSFECTION;

EID: 84914169668     PISSN: 87567938     EISSN: 15206033     Source Type: Journal    
DOI: 10.1002/btpr.1932     Document Type: Article

References (58)

1. Boussif O, Lezoualch F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP. A versatile vector for gene and oligonucleotide transfer into cells in culture and in-vivo - polyethylenimine. Proc Natl Acad Sci USA. 1995;92:7297-7301.
2. Eberhardy SR, Radzniak L, Liu Z, Iron III. citrate inhibits polyethylenimine-mediated transient transfection of Chinese hamster ovary cells in serum-free medium. Cytotechnology. 2009;60:1-9.
3. Wong AW, Baginsky TK, Reilly DE. Enhancement of DNA uptake in FUT8-deleted CHO cells for transient production of afucosylated antibodies. Biotechnol Bioeng. 2010;106:751-763.
4. Daramola O, Stevenson J, Dean G, Hatton D, Pettman G, Holmes W, Field R. A high-yielding CHO transient system: coexpression of genes encoding EBNA-1 and GS enhances transient protein expression. Biotechnol Prog. 2014;30:132-141.
5. Backliwal G, Hildinger M, Chenuet S, Wulhfard S, De Jesus M, Wurm FM. Rational vector design and multi-pathway modulation of HEK 293E cells yield recombinant antibody titers exceeding 1 g/l by transient transfection under serum-free conditions. Nucleic Acids Res. 2008;36:e96.
6. Kichler A, Leborgne C, Danos O. Dilution of reporter gene with stuffer DNA does not alter the transfection efficiency of polyethylenimines. J Gene Med. 2005;7:1459-1467.
7. Rajendra Y, Kiseljak D, Manoli S, Baldi L, Hacker DL, Wurm FM. Role of non-specific DNA in reducing coding DNA requirement for transient gene expression with CHO and HEK-293E cells. Biotechnol Bioeng. 2012;109:2271-2278.
8. Mizuguchi H, Hosono T, Hayakawa T. Long-term replication of Epstein-Barr virus-derived episomal vectors in the rodent cells. Febs Lett. 2000;472:173-178.
9. Payne CK, Jones SA, Chen C, Zhuang XW. Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands. Traffic. 2007;8:389-401.
10. Paris S, Burlacu A, Durocher Y. Opposing roles of syndecan-1 and syndecan-2 in polyethyleneimine-mediated gene delivery. J Biol Chem. 2008;283:7697-7704.
11. Thomas M, Klibanov AM. Enhancing polyethylenimine's delivery of plasmid DNA into mammalian cells. Proc Natl Acad Sci USA. 2002;99:14640-14645.
12. Walker GF, Fella C, Pelisek J, Fahrmeir J, Boeckle S, Ogris M, Wagner E. Toward synthetic viruses: endosomal pH-Triggered deshielding of targeted polyplexes greatly enhances gene transfer in vitro and in vivo. Mol Ther. 2005;11:418-425.
13. Fortune JA, Novobrantseva TI, Klibanov AM. Highly effective gene transfection in vivo by alkylated polyethylenimine. J Drug Deliv. 2011; doi:10.1155/2011/204058.
14. Aravindan L, Bicknell KA, Brooks G, Khutoryanskiy VV, Williams AC. Effect of acyl chain length on transfection efficiency and toxicity of polyethylenimine. Int J Pharm. 2009;378:201-210.
15. Lee CH, Ni YH, Chen CC, Chou CK, Chang FH. Synergistic effect of polyethylenimine and cationic liposomes in nucleic acid delivery to human cancer cells. Biochim Biophys Acta. 2003;1611:55-62.
16. Garcia L, Bunuales M, Duzgunes N, Tros deIlarduya C. Serum-resistant lipopolyplexes for gene delivery to liver tumour cells. Eur J Pharm Biopharm. 2007;67:58-66.
17. Song H, Wang G, He B, Li L, Li C, Lai Y, Xu X, Gu Z. Cationic lipid-coated PEI/DNA polyplexes with improved efficiency and reduced cytotoxicity for gene delivery into mesenchymal stem cells. Int J Nanomed. 2012;7:4637-4648.
18. Incani V, Lavasanifar A, Uludag H. Lipid and hydrophobic modification of cationic carriers on route to superior gene vectors. Soft Matter. 2010;6:2124-2138.
19. Liu Z, Zhang Z, Zhou C, Jiao Y. Hydrophobic modifications of cationic polymers for gene delivery. Prog Polym Sci. 2010;35:1144-1162.
20. Thompson BC, Segarra CRJ, Mozley OL, Daramola O, Field R, Levison PR, James DC. Cell line specific control of polyethylenimine-mediated transient transfection optimized with "Design of experiments" methodology. Biotechnol Prog. 2012;28:179-187.
21. Ye JX, Kober V, Tellers M, Naji Z, Salmon P, Markusen JF. High-level protein expression in scalable CHO transient transfection. Biotechnol Bioeng. 2009;103:542-551.
22. Galbraith DJ, Tait AS, Racher AJ, Birch JR, James DC. Control of culture environment for improved polyethylenimine-mediated transient production of recombinant monoclonal antibodies by CHO cells. Biotechnol Prog. 2006;22(3):753-762.
23. Wulhfard S, Baldi L, Hacker DL, Wurm F. Valproic acid enhances recombinant mRNA and protein levels in transiently transfected Chinese hamster ovary cells. J Biotechnol. 2010;148:128-132.
24. Luo D, Saltzman WM. Enhancement of transfection by physical concentration of DNA at the cell surface. Nat Biotechnol. 2000;18:893-895.
25. Davies SL, Lovelady CS, Grainger RK, Racher AJ, Young RJ, James DC. Functional heterogeneity and heritability in CHO cell populations. Biotechnol Bioeng. 2013;110:260-274.
26. Hunter RJ. Zeta Potential in Colloid Science. New York: Academic Press; 1981.
27. Derouazi M, Girard P, Tilbogh F, Iglesias K, Muller N, Bertschinger M, Wurm F. Serum-free large scale transient transfection of CHO cells. Biotechnol Bioeng. 2004;87:537-545.
28. Christianson HC, Svensson KJ, van Kuppevelt TH, Li J-P, Belting M. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci. 2013;110:17380-17385.
29. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000;1:31-39.
30. Sharma VK, Thomas M, Klibanov AM. Mechanistic studies on aggregation of polyethylenimine-DNA complexes and its prevention. Biotechnol Bioeng. 2005;90:614-620.
31. Elouahabi A, Ruysschaert JM. Formation and intracellular trafficking of lipoplexes and polyplexes. Mol Ther. 2005;11:336-347.
32. Tros de Ilarduya C, Sun Y, Duezguenes N. Gene delivery by lipoplexes and polyplexes. Eur J Pharm Sci. 2010;40:159-170.
33. Shaw DJ. Charged interfaces. In Colloid and Surface Chemistry, 4th ed. Oxford: Butterworth Heinemann; 1992:174-210.
34. Petri-Fink A, Steitz B, Finka A, Salaklang J, Hofmann H. Effect of cell media on polymer coated superparamagnetic iron oxide nanoparticles (SPIONs): colloidal stability, cytotoxicity, and cellular uptake studies. Eur J Pharm Biopharm. 2008;68:129-137.
35. Boeckle S, von Gersdorff K, van der Piepen S, Culmsee C, Wagner E, Ogris M. Purification of polyethylenimine polyplexes highlights the role of free polycations in gene transfer. J Gene Med. 2004;6:1102-1111.
36. Frohlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomed. 2012;7:5577-5591.
37. Kopatz I, Remy JS, Behr JP. A model for non-viral gene delivery: through syndecan adhesion molecules and powered by actin. J Gene Med. 2004;6:769-776.
38. Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010;11:688-699.
39. Crook K, Stevenson BJ, Dubouchet M, Porteous DJ. Inclusion of cholesterol in DOTAP transfection complexes increases the delivery of DNA to cells in vitro in the presence of serum. Gene Ther. 1998;5:137-143.
40. Simons K, Ehehalt R. Cholesterol, lipid rafts, and disease. J Clin Invest. 2002;110:597-603.
41. Chu CL, Buczek-Thomas JA, Nugent MA. Heparan sulphate proteoglycans modulate fibroblast growth factor-2 binding through a lipid raft-mediated mechanism. Biochem J. 2004;379:331-341.
42. von Gersdorff K, Sanders NN, Vandenbroucke R, De Smedt SC, Wagner E, Ogris M. The internalization route resulting in successful gene expression depends on both cell line and polyethylenimine polyplex type. Mol Ther. 2006;14:745-753.
43. Mercer J, Helenius A. Virus entry by macropinocytosis. Nat Cell Biol. 2009;11:510-520.
44. Sandgren S, Cheng F, Belting M. Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide - Role for cell-surface proteoglycans. J Biol Chem. 2002;277:38877-38883.
45. Ruponen M, Honkakoski P, Tammi M, Urtti A. Cell-surface glycosaminoglycans inhibit cation-mediated gene transfer. J Gene Med. 2004;6:405-414.
46. Imamura J, Suzuki Y, Gonda K, Roy CN, Gatanaga H, Ohuchi N, Higuchi H. Single particle tracking confirms that multivalent tat protein transduction domain-induced heparan sulfate proteoglycan cross-linkage activates Rac1 for internalization. J Biol Chem. 2011;286:10581-10592.
47. Chen K, Williams KJ, Molecular mediators for raft-dependent endocytosis of syndecan-1, a highly conserved, multifunctional receptor. J Biol Chem. 2013;288:13988-13999.
48. Christianson HC, Belting M. Heparan sulphate proteoglycan as a cell-surface endocytosis receptor. Matrix Biol. 2014;35:51-55.
49. Akinc A, Thomas M, Klibanov AM, Langer R. Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis. J Gene Med. 2005;7:657-663.
50. O'Callaghan PM, McLeod J, Pybus LP, Lovelady CS, Wilkinson SJ, Racher AJ, Porter A, James DC. Cell line-specific control of recombinant monoclonal antibody production by CHO cells. Biotechnol Bioeng. 2010;106:938-951.
51. Raymond C, Tom R, Perret S, Moussouami P, L'Abbe D, St-Laurent G, Durocher Y. A simplified polyethylenimine-mediated transfection process for large-scale and high-throughput applications. Methods. 2011;55:44-51.
52. Macaraeg NF, Reilly DE, Wong AW. Use of an anti-apoptotic CHO cell line for transient gene expression. Biotechnol Prog. 2013;29:1050-1058.
53. Grandinetti G, Ingle NP, Reineke TM. Interaction of poly(ethylenimine)-DNA polyplexes with mitochondria: implications for a mechanism of cytotoxicity. Mol Pharm. 2011;8:1709-1719.
54. Moghimi SM, Symonds P, Murray JC, Hunter AC, Debska G, Szewczyk A. A two-stage poly(ethylenimine)-mediated cytotoxicity: implications for gene transfer/therapy. Mol Ther. 2005;11:990-995.
55. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009;417:1-13.
56. Lee MS, Kim NW, Lee K, Kim H, Jeong JH. Enhanced transfection by antioxidative polymeric gene carrier that reduces polyplex-mediated cellular oxidative stress. Pharm Res. 2013;30:1642-1651.
57. Majors BS, Betenbaugh MJ, Pederson NF, Chiang GG. Enhancement of transient gene expression and culture viability using Chinese hamster ovary cells overexpressing Bcl-x(L). Biotechnol Bioeng. 2008;101:567-578.
58. Cataldi A. Cell responses to oxidative stressors. Curr Pharm Des. 2010;16:1387-1395.