Microtubule-mediated and microtubule-independent transport of adenovirus type 5 in HEK293 cells

Journal of Virology

Volumn 81, Issue 13, 2007, Pages 6899-6908

  Yea, Carmen ^a,b   Dembowy, Joanna ^a,c   Pacione, Laura ^a   Brown, Martha ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYFLUORESCEIN; COLCHICINE; GREEN FLUORESCENT PROTEIN; NOCODAZOLE;

ADENOVIRUS 2; ADENOVIRUS 5; ARTICLE; CELL STRAIN HEK293; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE; GOLGI COMPLEX; HEP 2 CELL; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; MITOSIS; NONHUMAN; NUCLEAR PORE; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION;

ADENOVIRIDAE; ANTINEOPLASTIC AGENTS; BIOLOGICAL TRANSPORT; COLCHICINE; GENOME, VIRAL; GOLGI APPARATUS; HELA CELLS; HUMANS; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; NOCODAZOLE; NUCLEAR PORE; TIME FACTORS; TUBULIN MODULATORS; VIRION; VIRUS REPLICATION;

ADENOVIRIDAE; HUMAN ADENOVIRUS TYPE 5;

EID: 34250900288     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02330-05     Document Type: Article

References (45)

1. Arnberg, N., K. Edlund, A. H. Kidd, and G. Wadell. 2000. Adenovirus type 37 uses sialic acid as a cellular receptor. J. Virol. 74:42-48.
2. v integrins. J. Virol. 74:7691-7693.
3. Arnberg, N., P. Pring-Akerblom, and G. Wadell. 2002. Adenovirus type 37 uses sialic acid as a cellular receptor on Chang C cells. J. Virol. 76:8834-8841.
4. Bailey, C. J., R. G. Crystal, and P. L. Leopold. 2003. Association of adenovirus with the microtubule organizing center. J. Virol. 77:13275-13287.
5. Birukova, A. A., K. Smurova, K. G. Birukov, P. Usatyuk, F. Liu, K. Kaibuchi, A. Ricks-Cord, V. Natarajan, I. Alieva, J. G. Garcia, and A. D. Verin. 2004. Microtubule disassembly induces cytoskeletal remodeling and lung vascular barrier dysfunction: role of Rho-dependent mechanisms. J. Cell Physiol. 201:55-70.
6. Brown, C. R., S. J. Doxsey, E. White, and W. J. Welch. 1994. Both viral (adenovirus E1B) and cellular (hsp70, p53) components interact with centrosomes. J. Cell Physiol. 160:47-60.
7. Brown, M. 1985. Selection of nonfastidious adenovirus species in 293 cells inoculated with stool specimens containing adenovirus type 40. J. Clin. Microbiol. 22:205-209.
8. Brown, M., H. L. Wilson-Friesen, and F. Doane. 1992. A block in release of progeny virus and a high particle-to-infectious ratio contribute to poor growth of enteric adenovirus types 40 and 41 in cell culture. J. Virol. 66: 3198-3205.
9. Cashman, S. M., D. J. Morris, and R. Kumar-Singh. 2004. Adenovirus type 5 pseudotyped with adenovirus type 37 fiber uses sialic acid as a receptor. Virology 324:129-139.
10. Chang, L., and R. D. Goldman. 2004. Intermediate filaments mediate cytoskeletal crosstalk. Nat. Rev. Mol. Cell Biol. 5:601-613.
11. Dales, S., and Y. Chardonnet. 1973. Early events in the interaction of adenoviruses with HeLa cells. IV. Association with microtubules and the nuclear pore complex during vectorial movement of the inoculum. Virology 56:465-483.
12. Davis, B. D., R. Dulbecco, H. N. Eisen, H. S. Ginsberg, and W. B. Wood, Jr. 1973. Microbiology, 2nd ed., p. 1042-1044. Harper and Row Publishers, Inc., Hagerstown, MD.
13. Fujimuro, M., H. Sawada, and H. Yokosawa. 1994. Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349:173-180.
14. Gaggar, A., D. M. Shayakhmetov, and A. Lieber. 2003. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9:1408-1412.
15. Garcia-Mata, R., Z. Bebok, E. J. Sorscher, and E. Sztul. 1999. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146:1239-1254.
16. Giannakakou, P., M. Nakano, K. C. Nicolaou, A. O'Brate, J. Yu, M. V. Blagoslonny, U. F. Greber, and T. Fojo. 2002. Enhanced microtubule-dependent trafficking and p53 nuclear accumulation by suppression of microtubule dynamics. Proc. Natl. Acad. Sci. USA 99:10855-10860.
17. Glotzer, J. B., A. I. Michou, A. Baker, M. Saltik, and M. Cotten. 2001. Microtubule-independent motility and nuclear targeting of adenoviruses with fluorescently labeled genomes. J. Virol. 75:2421-2434.
18. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59-72.
19. Greber, U. F., M. Suomalainen, R. P. Stidwell, K. Boucke, M. W. Ebersold, and A. Helenius. 1997. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16:5998-6007.
20. Horwitz, M. S. 2001. Adenoviruses, p. 2301-2326. In D. M. Knipe and P. M. Howley (ed.), Field's virology, vol. 2, 4th ed. Lippincott Williams and Wilkins, Philadelphia, PA.
21. Johnston, J. A., C. L. Ward, and R. R. Kopito. 1998. Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143:1883-1898.
22. Kolodziejska, K., E., A. R. Burns, R. H. Moore, D. L. Stenoien, and N. T. Eissa. 2005. Regulation of inducible nitric oxide synthase by aggresome formation. Proc. Natl. Acad. Sci. USA 102:4854-4859.
23. Leopold, P. L., B. Ferris, I. Grinberg, S. Worgall, N. R. Hackett, and R. G. Crystal. 1998. Fluorescent virions: dynamic tracking of the pathway of adenovirus gene transfer vectors in living cells. Hum. Gene Ther. 9:367-378.
24. Leopold, P. L., G. Kreitzer, N. Miyazawa, S. Rempel, K. K. Pfister, E. Rodriguez-Boulan, and R. G. Crystal. 2000. Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Hum. Gene Ther. 11:151-165.
25. Liu, Y., A. Shevchenko, A. Shevchenko, and A. J. Berk. 2005. Adenovirus exploits the cellular aggresome response to accelerate inactivation of the MRN complex. J. Virol. 79:14004-14016.
26. Mabit, H., M. Y. Nakano, U. Prank, B. Saam, K. Dohner, B. Sodeik, and U. F. Greber. 2002. Intact microtubules support adenovirus and herpes simplex virus infections. J. Virol. 76:9962-9971.
27. Maizel, J. V., Jr., D. O. White, and M. D. Scharff. 1968. The polypeptides of adenovirus. II. Soluble proteins, cores, top components and the structure of the virion. Virology 36:126-136.
28. Marceiller, J., A. Drechou, G. Durand, F. Perez, and C. Poüs. 2005. Kinesin is involved in protecting nascent microtubules from disassembly after recovery from nocodazole treatment. Exp. Cell Res. 304:483-492.
29. Meier, O., and U. F. Greber. 2004. Adenovirus endocytosis. J. Gene Med. 6:S152-S163.
30. Mittereder, N., K. L. March, and B. C. Trapnell. 1996. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J. Virol. 70:7489-7509.
31. Miyazawa, N., P. L. Leopold, N. R. Hackett, B. Ferris, S. Worgall, E. Falck-Pedersen, and R. G. Crystal. 1999. Fiber swap between adenovirus subgroups B and C alters intracellular trafficking of adenovirus gene transfer vectors. J. Virol. 73:6056-6065.
32. Miyazawa, N., C. G. Ronald, and P. Leopold. 2001. Adenovirus serotype 7 retention in a late endosomal compartment prior to cytosol escape is modulated by fiber protein. J. Virol. 75:1387-1400.
33. Segerman, A., N. Arnberg, A. Erikson, K. Lindman, and G. Wadell. 2003. There are two different species B adenovirus receptors: sBAR, common to species B1 and B2 adenoviruses, and sB2AR, exclusively used by species B2 adenoviruses. J. Virol. 77:1157-1162.
34. Segerman, A., J. P. Atkinson, M. Marttila, V. Dennerquist, G. Wadell, and N. Arnberg. 2003. Adenovirus type 11 uses CD46 as a cellular receptor. J. Virol. 77:9183-9191.
35. Shaw, G., S. Morse, M. Ararat, and F. L. Graham. 2002. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK293 cells. FASEB J. 16:869-871.
36. Shayakhmetov, D. M., Z.-Y. Li, V. Ternovoi, A. Gaggar, H. Gharwan, and A. Lieber. 2003. The interaction between the fiber knob domain and the cellular attachment receptor determines the intracellular trafficking route of adenoviruses. J. Virol. 77:3712-3723.
37. Shayakhmetov, D. M., Z.-Y. Li, A. Gaggar, H. Gharwan, V. Ternovoi, V. Sandig, and A. Lieber. 2004. Genome size and structure determine efficiency of postinternalization steps and gene transfer of capsid-modified adenovirus vectors in a cell-type specific manner. J. Virol. 78:10009-10022.
38. Shortt, J. J., A. V. Pereboev, Y. Kawakami, C. Vasu, M. J. Holterman, and D. T. Curiel. 2004. Adenovirus serotype 3 utilizes CD80 (B7.1) and CD86 (B7.2) as cellular attachment receptors. Virology 322:349-359.
39. Sirena, D., B. Lilienfeld, M. Eisenhut, S. Kalin, K. Boucke, R. R. Beerli, L. Vogt, C. Ruedl, M. F. Bachmann, U. F. Greber, and S. Hemmi. 2004. The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3. J. Virol. 78:4454-4462.
40. Strunze, S., L. C. Trotman, K. Boucke, and U. F. Greber. 2005. Nuclear targeting of adenovirus type 2 requires CRM1-mediated nuclear export. Mol. Biol. Cell 16:2999-3009.
41. Suomalainen, M., M. Y. Nakano, K. Boucke, S. Keller, and U. F. Greber. 1999. Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144: 657-672.
42. van Regenmortel, M. H. V., C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch. C. R. Pringle, and R. B. Wickner (ed.). 2000. Virus taxonomy. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
43. Wadell, G. 1999. In A. Granoff and R. G. Webster (ed.), Encyclopedia of virology, 2nd ed.. Academic Press, San Diego, CA.
44. Wojcik, C., and G. N. DeMartino. 2003. Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35:579-589.
45. Wu, E., S. A. Trauger, L. Pache, T. M. Mulle, D. J. von Seggern, G. Siuzdak, and G. R. Nemerow. 2004. Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. J. Virol. 78:3897-3905.