Super-resolution imaging of nuclear import of adeno-associated virus in live cells

Molecular Therapy Methods and Clinical Development

Volumn 2, Issue , 2015, Pages 15047-

  Kelich, Joseph M ^a   Ma, Jiong ^a   Dong, Biao ^b   Wang, Qizhao ^b   Chin, Mario ^b   Magura, Connor M ^a   Xiao, Weidong ^b   Yang, Weidong ^a  

^a Temple University   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIGITONIN; STREPTAVIDIN;

ADENO ASSOCIATED VIRUS; ARTICLE; AUTOFLUORESCENCE; BLEACHING; BUDDING; CELL NUCLEUS MEMBRANE; ENDOSOME; FLUORESCENCE MICROSCOPY; HOST CELL; HUMAN; HUMAN CELL; ILLUMINATION; MICROSCOPY; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SINGLE POINT EDGE EXCITATION SUB DIFFRACTION MICROSCOPY; TRANSPORT KINETICS; VIRUS PARTICLE; CELL BUDDING; CELL NUCLEUS; CYTOPLASM; NONHUMAN; SPATIOTEMPORAL ANALYSIS; SUPER RESOLUTION SINGLE POINT EDGE EXCITATION SUB DIFFRACTION MICROSCOPY; VELOCITY;

EID: 84982152238     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2015.47     Document Type: Article

References (48)

1. 1 Berns, KI, Giraud, C, Biology of adeno-associated virus. Curr Top Microbiol Immunol 218 (1996), 1–23.
2. 2 Atchison, RW, Casto, BC, Hammon, WM, Electron microscopy of adenovirus-associated virus (AAV) in cell cultures. Virology 29 (1966), 353–357.
3. 3 Hoggan, MD, Blacklow, NR, Rowe, WP, Studies of small DNA viruses found in various adenovirus preparations: physical, biological, and immunological characteristics. Proc Natl Acad Sci USA 55 (1966), 1467–1474.
4. 4 Yang, GS, Schmidt, M, Yan, Z, Lindbloom, JD, Harding, TC, Donahue, BA, et al. Virus-mediated transduction of murine retina with adeno-associated virus: effects of viral capsid and genome size. J Virol 76 (2002), 7651–7660.
5. 5 Samulski, RJ, Zhu, X, Xiao, X, Brook, JD, Housman, DE, Epstein, N, et al. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J 10 (1991), 3941–3950.
6. 6 Kotin, RM, Siniscalco, M, Samulski, RJ, Zhu, XD, Hunter, L, Laughlin, CA, et al. Site-specific integration by adeno-associated virus. Proc Natl Acad Sci USA 87 (1990), 2211–2215.
7. 7 Buller, RM, Janik, JE, Sebring, ED, Rose, JA, Herpes simplex virus types 1 and 2 completely help adenovirus-associated virus replication. J Virol 40 (1981), 241–247.
8. 8 Timpe, JM, Verrill, KC, Trempe, JP, Effects of adeno-associated virus on adenovirus replication and gene expression during coinfection. J Virol 80 (2006), 7807–7815.
9. 9 Glauser, DL, Seyffert, M, Strasser, R, Franchini, M, Laimbacher, AS, Dresch, C, et al. Inhibition of herpes simplex virus type 1 replication by adeno-associated virus rep proteins depends on their combined DNA-binding and ATPase/helicase activities. J Virol 84 (2010), 3808–3824.
10. 10 Kaplitt, MG, Leone, P, Samulski, RJ, Xiao, X, Pfaff, DW, O'Malley, KL, et al. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 8 (1994), 148–154.
11. 11 Moss, RB, Milla, C, Colombo, J, Accurso, F, Zeitlin, PL, Clancy, JP, et al. Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: a randomized placebo-controlled phase 2B trial. Hum Gene Ther 18 (2007), 726–732.
12. 12 Manno, CS, Chew, AJ, Hutchison, S, Larson, PJ, Herzog, RW, Arruda, VR, et al. AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101 (2003), 2963–2972.
13. 13 Cottard, V, Mulleman, D, Bouille, P, Mezzina, M, Boissier, MC, Bessis, N, Adeno-associated virus-mediated delivery of IL-4 prevents collagen-induced arthritis. Gene Ther 7 (2000), 1930–1939.
14. 14 Fu, H, Muenzer, J, Samulski, RJ, Breese, G, Sifford, J, Zeng, X, et al. Self-complementary adeno-associated virus serotype 2 vector: global distribution and broad dispersion of AAV-mediated transgene expression in mouse brain. Mol Ther 8 (2003), 911–917.
15. 15 Zhang, H, Yang, B, Mu, X, Ahmed, SS, Su, Q, He, R, et al. Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Mol Ther 19 (2011), 1440–1448.
16. 16 Ali, RR, Reichel, MB, Thrasher, AJ, Levinsky, RJ, Kinnon, C, Kanuga, N, et al. Gene transfer into the mouse retina mediated by an adeno-associated viral vector. Hum Mol Genet 5 (1996), 591–594.
17. 17 Wang, Z, Ma, HI, Li, J, Sun, L, Zhang, J, Xiao, X, Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther 10 (2003), 2105–2111.
18. 18 Aschauer, DF, Kreuz, S, Rumpel, S, Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS ONE, 8, 2013, e76310.
19. 19 Bartlett, JS, Wilcher, R, Samulski, RJ, Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J Virol 74 (2000), 2777–2785.
20. 20 Schmidt, M, Voutetakis, A, Afione, S, Zheng, C, Mandikian, D, Chiorini, JA, Adeno-associated virus type 12 (AAV12): a novel AAV serotype with sialic acid- and heparan sulfate proteoglycan-independent transduction activity. J Virol 82 (2008), 1399–1406.
21. 21 Cohen, S, Au, S, Panté, N, How viruses access the nucleus. Biochim Biophys Acta 1813 (2011), 1634–1645.
22. 22 Whittaker, GR, Virus nuclear import. Adv Drug Deliv Rev 55 (2003), 733–747.
23. 23 Yang, W, Distinct, but not completely separate spatial transport routes in the nuclear pore complex. Nucleus 4 (2013), 166–175.
24. 24 Terry, LJ, Shows, EB, Wente, SR, Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318 (2007), 1412–1416.
25. 25 Naim, B, Brumfeld, V, Kapon, R, Kiss, V, Nevo, R, Reich, Z, Passive and facilitated transport in nuclear pore complexes is largely uncoupled. J Biol Chem 282 (2007), 3881–3888.
26. 26 Patel, SS, Belmont, BJ, Sante, JM, Rexach, MF, Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129 (2007), 83–96.
27. 27 Labokha, AA, Gradmann, S, Frey, S, Hülsmann, BB, Urlaub, H, Baldus, M, et al. Systematic analysis of barrier-forming FG hydrogels from Xenopus nuclear pore complexes. EMBO J 32 (2013), 204–218.
28. 28 Hülsmann, BB, Labokha, AA, Görlich, D, The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150 (2012), 738–751.
29. 29 Wälde, S, Kehlenbach, RH, The Part and the Whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol 20 (2010), 461–469.
30. 30 Laurence, J, Franklin, M, Translating gene therapy to the clinic: techniques and approaches. Acad Press 4 (2014), 44–48.
31. 31 Nicolson, SC, Samulski, RJ, Recombinant adeno-associated virus utilizes host cell nuclear import machinery to enter the nucleus. J Virol 88 (2014), 4132–4144.
32. 32 Sonntag, F, Schmidt, K, Kleinschmidt, JA, A viral assembly factor promotes AAV2 capsid formation in the nucleolus. Proc Natl Acad Sci USA 107 (2010), 10220–10225.
33. 33 Grieger, JC, Snowdy, S, Samulski, RJ, Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J Virol 80 (2006), 5199–5210.
34. 34 Douar, AM, Poulard, K, Danos, O, Deleterious effect of peptide insertions in a permissive site of the AAV2 capsid. Virology 309 (2003), 203–208.
35. 35 Cervelli, T, Palacios, JA, Zentilin, L, Mano, M, Schwartz, RA, Weitzman, MD, et al. Processing of recombinant AAV genomes occurs in specific nuclear structures that overlap with foci of DNA-damage-response proteins. J Cell Sci 121 (2008), 349–357.
36. 36 Seisenberger, G, Ried, MU, Endress, T, Büning, H, Hallek, M, Bräuchle, C, Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294 (2001), 1929–1932.
37. 37 Lux, K, Goerlitz, N, Schlemminger, S, Perabo, L, Goldnau, D, Endell, J, et al. Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J Virol 79 (2005), 11776–11787.
38. 38 Johnson, JS, Li, C, DiPrimio, N, Weinberg, MS, McCown, TJ, Samulski, RJ, Mutagenesis of adeno-associated virus type 2 capsid protein VP1 uncovers new roles for basic amino acids in trafficking and cell-specific transduction. J Virol 84 (2010), 8888–8902.
39. 39 Kelich, JM, Yang, W, High-resolution imaging reveals new features of nuclear export of mRNA through the nuclear pore complexes. Int J Mol Sci 15 (2014), 14492–14504.
40. 40 Daigle, N, Beaudouin, J, Hartnell, L, Imreh, G, Hallberg, E, Lippincott-Schwartz, J, et al. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J Cell Biol 154 (2001), 71–84.
41. 41 Ribbeck, K, Görlich, D, The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J 21 (2002), 2664–2671.
42. 42 Tu, LC, Fu, G, Zilman, A, Musser, SM, Large cargo transport by nuclear pores: implications for the spatial organization of FG-nucleoporins. EMBO J 32 (2013), 3220–3230.
43. 43 Mortensen, KI, Churchman, LS, Spudich, JA, Flyvbjerg, H, Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat Methods 7 (2010), 377–381.
44. 44 Quan, T, Zeng, S, Huang, ZL, Localization capability and limitation of electron-multiplying charge-coupled, scientific complementary metal-oxide semiconductor, and charge-coupled devices for superresolution imaging. J Biomed Opt, 15, 2010, 066005.
45. 45 Robbins, MS, Hadwen, BJ, The noise performance of electron multiplying charge-coupled devices. IEEE Trans Electron Devices 50 (2003), 1227–1232.
46. 46 Deschout, H, Neyts, K, Braeckmans, K, The influence of movement on the localization precision of sub-resolution particles in fluorescence microscopy. J Biophotonics 5 (2012), 97–109.
47. 47 Ma, J, Yang, W, Three-dimensional distribution of transient interactions in the nuclear pore complex obtained from single-molecule snapshots. Proc Natl Acad Sci USA 107 (2010), 7305–7310.
48. 48 Lowe, AR, Siegel, JJ, Kalab, P, Siu, M, Weis, K, Liphardt, JT, Selectivity mechanism of the nuclear pore complex characterized by single cargo tracking. Nature 467 (2010), 600–603.