Electroporation and microinjection successfully deliver single-stranded and duplex DNA into live cells as detected by FRET measurements

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Bamford, Rosemary A ^a   Zhao, Zheng Yun ^a   Hotchin, Neil A ^a   Styles, Iain B ^a   Nash, Gerard B ^a   Tucker, James H R ^a   Bicknell, Roy ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN; DOUBLE STRANDED DNA; SINGLE STRANDED DNA; CARBOCYANINE; CYANINE DYE 3; CYANINE DYE 5; DNA PROBE;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA DEGRADATION; DNA PROBE; DNA SEQUENCE; DNA SYNTHESIS; ELECTROPORATION; ENDOCYTOSIS; ENDOSOME; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; GENE EXPRESSION; MICROINJECTION; NONHUMAN; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ULTRAVIOLET SPECTROSCOPY; ANIMAL; CELL SURVIVAL; CHO CELL LINE; CRICETULUS; GENETIC TRANSFECTION; HAMSTER; METABOLISM; PROCEDURES;

ANIMALS; CARBOCYANINES; CELL SURVIVAL; CHO CELLS; CRICETINAE; CRICETULUS; DNA PROBES; DNA, SINGLE-STRANDED; ELECTROPORATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROINJECTIONS; MICROSCOPY, CONFOCAL; TRANSFECTION;

EID: 84899696466     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095097     Document Type: Article

References (49)

1. Tsuji A, Sato Y, Hirano M, Suga T, Koshimoto H, et al. (2001) Development of a time-resolved fluorometric method for observing hybridization in living cells using fluorescence resonance energy transfer. Biophys J 81: 501-515. doi:10.1016/S0006-3495(01)75717-7. (Pubitemid 32605988)
2. Zamecnik PC, Stephenson ML (1978) Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide. Proc Natl Acad Sci U S A 75: 280-284. (Pubitemid 8290783)
3. Hélène C, Toulmé JJ (1990) Specific regulation of gene expression by antisense, sense and antigene nucleic acids. Biochim Biophys Acta 1049: 99-125.
4. Dahan L, Huang L, Kedmi R, Behlke MA, Peer D (2013) SNP Detection in mRNA in Living Cells Using Allele Specific FRET Probes. PLoS One 8: e72389. doi:10.1371/journal.pone.0072389.
5. Behlke MA (2008) Chemical modification of siRNAs for in vivo use. Oligonucleotides 18: 305-319. doi:10.1089/oli.2008.0164. (Pubitemid 352791344)
6. Chen Y, Barkley MD (1998) Toward understanding tryptophan fluorescence in proteins. Biochemistry 37: 9976-9982. doi:10.1021/bi980274n. (Pubitemid 28366351)
7. Tsuji A, Koshimoto H, Sato Y, Hirano M, Sei-iida Y, et al. (2000) Direct Observation of Specific Messenger RNA in a Single Living Cell. 78: 3260-3274.
8. Fisher TL, Terhorst T, Cao X, Wagner RW (1993) Intracellular disposition and metabolism of fluorescently-labeled unmodified and modified oligonucleotides microinjected into mammalian cells. Nucleic Acids Res 21: 3857-3865. (Pubitemid 23254510)
9. Leonetti JP, Mechti N, Degols G, Gagnor C, Lebleu B (1991) Intracellular distribution of microinjected antisense oligonucleotides. Proc Natl Acad Sci U S A 88: 2702-2706. (Pubitemid 21916486)
10. Chesnoy S, Huang L (2000) Structure and function of lipid-DNA complexes for gene delivery. Annu Rev Biophys Biomol Struct 29: 27-47. doi:10.1146/annurev.biophys.29.1.27. (Pubitemid 30599587)
11. Endoh T, Ohtsuki T (2009) Cellular siRNA delivery using cell-penetrating peptides modified for endosomal escape. Adv Drug Deliv Rev 61: 704-709. doi:10.1016/j.addr.2009.04.005.
12. Nitin N, Santangelo PJ, Kim G, Nie S, Bao G (2004) Peptide-linked molecular beacons for efficient delivery and rapid mRNA detection in living cells. Nucleic Acids Res 32: e58. doi:10.1093/nar/gnh063.
13. Stein CA, Hansen JB, Lai J, Wu S, Voskresenskiy A, et al. (2010) Efficient gene silencing by delivery of locked nucleic acid antisense oligonucleotides, unassisted by transfection reagents. Nucleic Acids Res 38: e3. doi:10.1093/nar/gkp841.
14. Sixou S (1994) Intracellular oligonucleotide hybridisation detected by fluorescence resonance energy transfer (FRET). Nucleic Acids Res 22: 662-668.
15. Uchiyama H. (1996) Detection of Undegraded Oligonucleotides in Vivo by Fluorescence Resonance Energy Transfer. J Biol Chem 271: 380-384. doi:10.1074/jbc.271.1.380.
16. Neumann E (1982) Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1: 841-845.
17. Bao G, Rhee WJ, Tsourkas A (2009) Fluorescent probes for live-cell RNA detection. Annu Rev Biomed Eng 11: 25-47. doi:10.1146/annurev-bioeng-061008- 124920.
18. Forster T (1946) Energiewanderung und Fluoreszenz. Naturwissenschaften 33: 166-175. doi:10.1007/BF00585226.
19. Sapsford KE, Berti L, Medintz IL (2006) Materials for fluorescence resonance energy transfer analysis: beyond traditional donor-acceptor combinations. Angew Chem Int Ed Engl 45: 4562-4589. doi:10.1002/anie.200503873.
20. Lakowicz JR (2006) Principles of Fluorescence Spectroscopy. Lakowicz JR, editor Boston, MA: Springer US. doi:10.1007/978-0-387-46312-4.
21. Karadag A, Riminucci M, Bianco P, Cherman N, Kuznetsov SA, et al. (2004) A novel technique based on a PNA hybridization probe and FRET principle for quantification of mutant genotype in fibrous dysplasia/McCune-Albright syndrome. Nucleic Acids Res 32: e63. doi:10.1093/nar/gnh059.
22. Mergny J, Boutorine AS, Garestier T, Belloc F, Rougee M, et al. (1994) Fluorescence energy transfer structures and sequences as a probe for nucleic acid. Nucleic Acids Res 22: e6. doi: 10.1093/nar/22.6.920.
23. Masuko M, Ohuchi S, Sode K, Ohtani H, Shimadzu A (2000) Fluorescence resonance energy transfer from pyrene to perylene labels for nucleic acid hybridization assays under homogeneous solution conditions. Nucleic Acids Res 28: E34.
24. Jothikumar P, Hill V, Narayanan J (2009) Design of FRET-TaqMan probes for multiplex real-time PCR using an internal positive control. Biotechniques 46: 519-524. doi:10.2144/000113127.
25. Emig M, Saussele S, Wittor H, Weisser A, Reiter A, et al. (1999) Accurate and rapid analysis of residual disease in patients with CML using specific fluorescent hybridization probes for real time quantitative RT-PCR. Leukemia 13: 1825-1832. (Pubitemid 29535267)
26. Mhlanga MM, Malmberg L (2001) Using molecular beacons to detect single-nucleotide polymorphisms with real-time PCR. Methods 25: 463-471. doi:10.1006/meth.2001.1269. (Pubitemid 34164019)
27. Cardullo RA, Agrawal S, Flores C, Zamecnik PC, Wolf DE (1988) Detection of nucleic acid hybridization by nonradiative fluorescence resonance energy transfer. Proc Natl Acad Sci U S A 85: 8790-8794. (Pubitemid 19001794)
28. Clegg RM, Murchie AI, Zechel A, Lilley DM (1993) Observing the helical geometry of double-stranded DNA in solution by fluorescence resonance energy transfer. Proc Natl Acad Sci U S A 90: 2994-2998. (Pubitemid 23113544)
29. Morrison LE, Halder TC, Stols LM (1989) Solution-phase detection of polynucleotides using interacting fluorescent labels and competitive hybridization. Anal Biochem 183: 231-244. (Pubitemid 20016253)
30. Tyagi S, Kramer FR (1996) Molecular beacons: probes that fluoresce upon hybridisation. Nat Biotechnol 14: 303-308.
31. Okabe K, Harada Y, Zhang J, Tadakuma H, Tani T, et al. (2011) Real time monitoring of endogenous cytoplasmic mRNA using linear antisense 2′-Omethyl RNA probes in living cells. Nucleic Acids Res 39: e20. doi:10.1093/nar/gkq1196.
32. Manchester J, Bassani DM, Duprey J-LHA, Giordano L, Vyle JS, et al. (2012) Photocontrolled binding and binding-controlled photochromism within anthracene-modified DNA. J Am Chem Soc 134: 10791-10794. doi:10.1021/ja304205m.
33. Dokka S, Rojanasakul Y (2000) Novel non-endocytic delivery of antisense oligonucleotides. Adv Drug Deliv Rev 44: 35-49.
34. Pastan IH, Willingham MC (1981) Journey to the center of the cell: role of the receptosome. Science 214: 504-509. (Pubitemid 12206148)
35. Barton GM, Medzhitov R (2002) Retroviral delivery of small interfering RNA into primary cells. Proc Natl Acad Sci U S A 99: 14943-14945. doi:10.1073/pnas.242594499. (Pubitemid 35334589)
36. Dominska M, Dykxhoorn DM (2010) Breaking down the barriers: siRNA delivery and endosome escape. J Cell Sci 123: 1183-1189. doi:10.1242/jcs.066399.
37. Price NC, Stevens L (1999) Fundamentals of Enzymology: The cell and molecular biology of catalytic proteins. New York: Oxford University Press.
38. Alwan HAJ, van Zoelen EJJ, van Leeuwen JEM (2003) Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J Biol Chem 278: 35781-35790. doi:10.1074/jbc.M301326200. (Pubitemid 37102355)
39. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, et al. (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23: 33-42. (Pubitemid 28223394)
40. Diacumakos EG (1973) Microsurgically fused human somatic cell hybrids: analysis and cloning. Proc Natl Acad Sci U S A 70: 3382-3386.
41. Capecchi MR (1980) High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell 22: 479-488.
42. Zhang Y, Yu L-C (2008) Single-cell microinjection technology in cell biology. Bioessays 30: 606-610. doi:10.1002/bies.20759. (Pubitemid 351859417)
43. Saleh M-C, van Rij RP, Hekele A, Gillis A, Foley E, et al. (2006) The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol 8: 793-802. doi:10.1038/ncb1439. (Pubitemid 44151582)
44. Gupta B, Levchenko TS, Torchilin VP (2005) Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev 57: 637-651. doi:10.1016/j.addr.2004.10.007. (Pubitemid 40255564)
45. Torchilin VP (2006) Recent approaches to intracellular delivery of drugs and DNA and organelle targeting. Annu Rev Biomed Eng 8: 343-375. doi:10.1146/annurev.bioeng.8.061505.095735.
46. Jepsen JS, Sørensen MD, Wengel J (2004) Locked nucleic acid: a potent nucleic acid analog in therapeutics and biotechnology. Oligonucleotides 14: 130-146. doi:10.1089/1545457041526317. (Pubitemid 38987382)
47. Sokol DL, Zhang X, Lu P, Gewirtz AM (1998) Real time detection of DNA.RNA hybridization in living cells. Proc Natl Acad Sci U S A 95: 11538-11543. (Pubitemid 28460450)
48. Politz JC, Browne ES, Wolf DE, Pederson T (1998) Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells. Proc Natl Acad Sci U S A 95: 6043-6048. (Pubitemid 28248961)
49. Paillasson S, Van De Corput M, Dirks RW, Tanke HJ, Robert-Nicoud M, et al. (1997) In Situ Hybridization in Living Cells: Detection of RNA Molecules. 233: 226-233.