A simple, highly efficient method for heterologous expression in mammalian primary neurons using cationic lipid-mediated mRNA transfection

Frontiers in Neuroscience

Volumn 4, Issue NOV, 2010, Pages

  Williams, Damian J ^a   Puhl III, Henry L ^a   Ikeda, Stephen R ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Alfalfa mosaic virus; Globin; Peripheral neurons; Tobacco mosaic virus; Untranslated regions; Voltage clamp

Indexed keywords

EID: 84859803428     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2010.00181     Document Type: Article

References (62)

1. Babendure, J. R., Babendure, J. L., Ding, J. H., and Tsien, R. Y. (2006). Control of mammalian translation by mRNA structure near caps. RNA 12, 851-861.
2. Barreau, C., Dutertre, S., Paillard, L., and Osborne, H. B. (2006). Liposome-mediated RNA transfection should be used with caution. RNA 12, 1790-1793.
3. Bettinger, T., Carlisle, R. C., Read, M. L., Ogris, M., and Seymour, L. W. (2001). Peptide-mediated RNA delivery: a novel approach for enhanced transfection of primary and post-mitotic cells. Nucleic Acids Res. 29, 3882-3891.
4. Bettinger, T., and Read, M. L. (2001). Recent developments in RNA-based strategies for cancer gene therapy. Curr. Opin. Mol. Ther. 3, 116-124.
5. Brunner, S., Sauer, T., Carotta, S., Cotten, M., Saltik, M., and Wagner, E. (2000). Cell cycle dependence of gene transfer by lipoplex, polyplex and recombinant adenovirus. Gene Ther. 7, 401-407.
6. Chen, C. Y., Gherzi, R., Andersen, J. S., Gaietta, G., Jurchott, K., Royer, H. D., Mann, M., and Karin, M. (2000). Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14, 1236-1248.
7. Denizot, F., and Lang, R. (1986). Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89, 271-277.
8. Ehrengruber, M. U., Hennou, S., Bueler, H., Naim, H. Y., Deglon, N., and Lundstrom, K. (2001). Gene transfer into neurons from hippocampal slices: comparison of recombinant semliki forest virus, adenovirus, adeno-associated virus, lentivirus, and measles virus. Mol. Cell. Neurosci. 17, 855-871.
9. Elango, N., Elango, S., Shivshankar, P., and Katz, M. S. (2005). Optimized transfection of mRNA transcribed from a d(A/T)100 tail-containing vector. Biochem. Biophys. Res. Commun. 330, 958-966.
10. Elmslie, K. S., Zhou, W., and Jones, S. W. (1990). LHRH and GTP-gamma-S modify calcium current activation in bullfrog sympathetic neurons. Neuron 5, 75-80.
11. Farhood, H., Bottega, R., Epand, R. M., and Huang, L. (1992). Effect of cationic cholesterol derivatives on gene transfer and protein kinase C activity. Biochim. Biophys. Acta 1111, 239-246.
12. Gallie, D. R. (2002). The 5'-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res. 30, 3401-3411.
13. Gallie, D. R., Feder, J. N., Schimke, R. T., and Walbot, V. (1991). Post-transcriptional regulation in higher eukaryotes: the role of the reporter gene in controlling expression. Mol. Gen. Genet. 228, 258-264.
14. Gallie, D. R., Sleat, D. E., Watts, J. W., Turner, P. C., and Wilson, T. M. (1987a). The 5'-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res. 15, 3257-3273.
15. Gallie, D. R., Sleat, D. E., Watts, J. W., Turner, P. C., and Wilson, T. M. (1987b). A comparison of eukaryotic viral 5'-leader sequences as enhancers of mRNA expression in vivo. Nucleic Acids Res. 15, 8693-8711.
16. Gallie, D. R., and Walbot, V. (1990). RNA pseudoknot domain of tobacco mosaic virus can functionally substitute for a poly(A) tail in plant and animal cells. Genes Dev. 4, 1149-1157.
17. Gehrke, L., Auron, P. E., Quigley, G. J., Rich, A., and Sonenberg, N. (1983). 5'-Conformation of capped alfalfa mosaic virus ribonucleic acid 4 may reflect its independence of the cap structure or of cap-binding protein for efficient translation. Biochemistry 22, 5157-5164.
18. Geiser, M., Cebe, R., Drewello, D., and Schmitz, R. (2001). Integration of PCR fragments at any specific site within cloning vectors without the use of restriction enzymes and DNA ligase. BioTechniques 31, 88-92.
19. Guo, J., and Ikeda, S. R. (2004). Endocannabinoids modulate N-type calcium channels and G-protein-coupled inwardly rectifying potassium channels via CB1 cannabinoid receptors heterologously expressed in mammalian neurons. Mol. Pharmacol. 65, 665-674.
20. 2+ channels by G-protein βγ subunits. Nature 380, 258-262.
21. Herskowitz, I. (1987). Functional inactivation of genes by dominant negative mutations. Nature 329, 219-222.
22. Holtkamp, S., Kreiter, S., Selmi, A., Simon, P., Koslowski, M., Huber, C., Tureci, O., and Sahin, U. (2006). Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood 108, 4009-4017.
23. Ikeda, S. R. (1991). Double-pulse calcium channel current facilitation in adult rat sympathetic neurones. J. Physiol. (Lond.) 439, 181-214.
24. Ikeda, S. R. (1996). Voltage-dependent modulation of N-type calcium channels by G-protein βγ subunits. Nature 380, 255-258.
25. Ikeda, S. R. (2004). Expression of G-protein signaling components in adult mammalian neurons by microinjection. Methods Mol. Biol. 259, 167-181.
26. Jacobsen, L., Calvin, S., and Lobenhofer, E. (2009). Transcriptional effects of transfection: the potential for misinterpretation of gene expression data generated from transiently transfected cells. BioTechniques 47, 617-624.
27. Jiang, Y., Xu, X. S., and Russell, J. E. (2006). A nucleolin-binding 3' untranslated region element stabilizes ß-globin mRNA in vivo. Mol. Cell. Biol. 26, 2419-2429.
28. Jobling, S. A., and Gehrke, L. (1987). Enhanced translation of chimaeric messenger RNAs containing a plant viral untranslated leader sequence. Nature 325, 622-625.
29. Johanning, F. W., Conry, R. M., LoBuglio, A. F., Wright, M., Sumerel, L. A., Pike, M. J., and Curiel, D. T. (1995). A sindbis virus mRNA polynucleotide vector achieves prolonged and high level heterologous gene expression in vivo. Nucleic Acids Res. 23, 1495-1501.
30. Kariko, K., Kuo, A., Barnathan, E. S., and Langer, D. J. (1998). Phosphate-enhanced transfection of cationic lipid-complexed mRNA and plasmid DNA. Biochim. Biophys. Acta 1369, 320-334.
31. Kozak, M. (1986). Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc. Natl. Acad. Sci. U.S.A. 83, 2850-2854.
32. Kozak, M. (1991a). A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr. 1, 111-115.
33. Kozak, M. (1991b). Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266, 19867-19870.
34. Kozak, M. (1994). Features in the 5' non-coding sequences of rabbit a and ß-globin mRNAs that affect translational efficiency. J. Mol. Biol. 235, 95-110.
35. Lappalainen, K., Jaaskelainen, I., Syrjanen, K., Urtti, A., and Syrjanen, S. (1994). Comparison of cell proliferation and toxicity assays using two cationic liposomes. Pharm. Res. 11, 1127-1131.
36. Lei, Q., Jones, M. B., Talley, E. M., Schrier, A. D., McIntire, W. E., Garrison, J. C., and Bayliss, D. A. (2000). Activation and inhibition of G protein-coupled inwardly rectifying potassium (Kir3) channels by G protein beta gamma subunits. Proc. Natl. Acad. Sci. USA. 97, 9771-9776.
37. Lu, V. B., Williams, D. J., Won, Y., and Ikeda, S. R. (2009). Intranuclear microinjection of DNA into dissociated adult mammalian neurons. J. Vis. Exp. 34, 1614.
38. Malone, R. W., Felgner, P. L., and Verma, I. M. (1989). Cationic liposome-mediated RNA transfection. Proc. Natl. Acad. Sci. U.S.A. 86, 6077-6081.
39. Marbaix, G., Huez, G., Burny, A., Cleuter, Y., Hubert, E., Leclercq, M., Chantrenne, H., Soreq, H., Nudel, U., and Littauer, U. Z. (1975). Absence of polyadenylate segment in globin messenger RNA accelerates its degradation in Xenopus oocytes. Proc. Natl. Acad. Sci. U.S.A. 72, 3065-3067.
40. Mortimer, I., Tam, P., MacLachlan, I., Graham, R. W., Saravolac, E. G., and Joshi, P. B. (1999). Cationic lipid-mediated transfection of cells in culture requires mitotic activity. Gene Ther. 6, 403-411.
41. Pain, V. M. (1996). Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236, 747-771.
42. Pesole, G., Mignone, F., Gissi, C., Grillo, G., Licciulli, F., and Liuni, S. (2001). Structural and functional features of eukaryotic mRNA untranslated regions. Gene 276, 73-81.
43. Ross, J. (1995). mRNA stability in mammalian cells. Microbiol. Rev. 59, 423-450.
44. Ruiz-Velasco, V., and Ikeda, S. R. (1998). Heterologous expression and coupling of G protein-gated inwardly rectifying K+ channels in adult rat sympathetic neurons. J. Physiol. (Lond.) 513, 761-773.
45. Sachs, A. B., Sarnow, P., and Hentze, M. W. (1997). Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89, 831-838.
46. Slepak, V. Z., Wilkie, T. M., and Simon, M. I. (1993). Mutational analysis of G protein alpha subunit G(o) alpha expressed in Escherichia coli. J. Biol. Chem. 268, 1414-1423.
47. Tebo, J. M., Datta, S., Kishore, R., Kolosov, M., Major, J. A., Ohmori, Y., and Hamilton, T. A. (2000). Interleukin-1-mediated stabilization of mouse KC mRNA depends on sequences in both 5'- and 3'-untranslated regions. J. Biol. Chem. 275, 12987-12993.
48. Teruel, M. N., Blanpied, T. A., Shen, K., Augustine, G. J., and Meyer, T. (1999). A versatile microporation technique for the transfection of cultured CNS neurons. J. Neurosci. Methods 93, 37-48.
49. Thaler, C., Koushik, S. V., Puhl, H. L. 3rd, Blank, P. S., and Vogel, S. S. (2009). Structural rearrangement of CaMKIIa catalytic domains encodes activation. Proc. Natl. Acad. Sci. U.S.A. 106, 6369-6374.
50. Van Tendeloo, V. F., Ponsaerts, P., and Berneman, Z. N. (2007). mRNA-based gene transfer as a tool for gene and cell therapy. Curr. Opin. Mol. Ther. 9, 423-431.
51. Vivaudou, M., Chan, K. W., Sui, J. L., Jan, L. Y., Reuveny, E., and Logothetis, D. E. (1997). Probing the G-protein regulation of GIRK1 and GIRK4, the two subunits of the KACh channel, using functional homomeric mutants. J. Biol. Chem. 272, 31553-31560.
52. Wang, Z., and Kiledjian, M. (2000). The poly(A)-binding protein and an mRNA stability protein jointly regulate an endoribonuclease activity. Mol. Cell. Biol. 20, 6334-6341.
53. Washbourne, P., and McAllister, A. K. (2002). Techniques for gene transfer into neurons. Curr. Opin. Neurobiol. 12, 566-573.
54. Wellmann, H., Kaltschmidt, B., and Kaltschmidt, C. (1999). Optimized protocol for biolistic transfection of brain slices and dissociated cultured neurons with a hand-held gene gun. J. Neurosci. Methods 92, 55-64.
55. Wells, D. R., Tanguay, R. L., Le, H., and Gallie, D. R. (1998). HSP101 functions as a specific translational regulatory protein whose activity is regulated by nutrient status. Genes Dev. 12, 3236-3251.
56. Wilkie, G. S., Dickson, K. S., and Gray, N. K. (2003). Regulation of mRNA translation by 5'- and 3'-UTR-binding factors. Trends Biochem. Sci. 28, 182-188.
57. Williams, D. J., Puhl, H. L. 3rd, and Ikeda, S. R. (2009). Rapid modification of proteins using a rapamycin-inducible tobacco etch virus protease system. PLoS ONE 4, e7474. doi: 10.1371/journal.pone.0007474.
58. Wolff, J. A., Malone, R. W., Williams, P., Chong, W., Acsadi, G., Jani, A., and Felgner, P. L. (1990). Direct gene transfer into mouse muscle in vivo. Science 247, 1465-1468.
59. Yu, J., and Russell, J. E. (2001). Structural and functional analysis of an mRNP complex that mediates the high stability of human beta-globin mRNA. Mol. Cell. Biol. 21, 5879-5888.
60. Zabner, J., Fasbender, A. J., Moninger, T., Poellinger, K. A., and Welsh, M. J. (1995). Cellular and molecular barrieirs to gene-transfer by a cationic lipid. J. Biol. Chem. 270, 18997-19007.
61. Zou, S., Scarfo, K., Nantz, M. H., and Hecker, J. G. (2010). Lipid-mediated delivery of RNA is more efficient than delivery of DNA in non-dividing cells. Int. J. Pharm. 389, 232-243.
62. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415.