Cytoplasmic dynein mediates adenovirus binding to microtubules

Journal of Virology

Volumn 78, Issue 18, 2004, Pages 10122-10132

  Kelkar, Samir A ^a   Pfister, K Kevin ^b   Crystal, Ronald G ^a   Leopold, Philip L ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE SERUM ALBUMIN; CYTOPLASMIC DYNEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GLYCEROL; MICROTUBULE ASSOCIATED PROTEIN; PACLITAXEL; TAU PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ADENOVIRUS; ARTICLE; BINDING ASSAY; CELL LINE; CELL LYSATE; CONCENTRATION RESPONSE; CYTOPLASM; IMMUNOPRECIPITATION; LUNG ALVEOLUS EPITHELIUM; MICROTUBULE; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION;

ADENOSINE TRIPHOSPHATE; ADENOVIRIDAE; ANIMALS; BINDING SITES; CAPSID PROTEINS; CATTLE; CELL LINE; CYTOPLASM; DYNEIN ATPASE; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES;

EID: 4444288426     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.18.10122-10132.2004     Document Type: Article

References (83)

1. Alonso, C., J. Miskin, B. Hernaez, P. Fernandez-Zapatero, L. Soto, C. Canto, I. Rodriguez-Crespo, L. Dixon, and J. M. Escribano. 2001. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J. Virol. 75:9819-9827.
2. Acsadi, G., R. A. Anguelov, H. Yang, G. Toth, R. Thomas, A. Jani, Y. Wang, E. Ianakova, S. Mohammad, R. A. Lewis, and M. E. Shy. 2002. Increased survival and function of SOD1 mice after glial cell-derived neurotrophic factor gene therapy. Hum. Gene Ther. 13:1047-1059.
3. Bai, M., B. Harfe, and P. Freimuth. 1993. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J. Virol. 67:5198-5205.
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. Baumgartner, B. J., and H. D. Shine. 1998. Neuroprotection of spinal motoneurons following targeted transduction with an adenoviral vector carrying the gene for glial cell line-derived neurotrophic factor. Exp Neurol. 153:102-112.
6. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
7. Brady, S. T., K. K. Pfister, and G. S. Bloom. 1990. A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc. Natl. Acad. Sci. USA 87:1061-1065.
8. Brady, S. T., R. J. Lasek, and R. D. Allen. Video microscopy of fast axonal transport in extruded axoplasm: a new model for study of molecular mechanisms. Cell Motil. 5:81-101.
9. Chardonnet, Y., and S. Dales. 1972. Early events in the interaction of adenoviruses with HeLa cells. 3. Relationship between an ATPase activity in nuclear envelopes and transfer of core material: a hypothesis. Virology 48:342-359.
10. 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.
11. Dales, S. 1975. Involvement of the microtubule in replication cycles of animal viruses. Ann. N. Y. Acad. Sci. 253:440-444.
12. Davison, E., R. M. Diaz, I. R. Hart, G. Santis, and J. F. Marshall. 1997. Integrin α5β1-mediated adenovirus infection is enhanced by the integrin-activating antibody TS2/16. J. Virol. 71:6204-6207.
13. Dohner, K., A. Wolfstein, U. Prank, C. Echeverri, D. Dujardin, R. Vallee, and B. Sodeik. 2002. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13:2795-2809.
14. Everitt, E., H. Ekstrand, B. Boberg, and B. Hartley-Asp. 1990. Estramustine phosphate reversibly inhibits an early stage during adenovirus replication. Arch. Virol. 111:15-28.
15. FitzGerald, D. J., R. Padmanabhan, I. Pastan, and M. C. Willingham. 1983. Adenovirus-induced release of epidermal growth factor and pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosis. Cell 32:607-617.
16. Garcia-Mata, R., Z. Bebok, E. J. Sorscher, and E. S. Sztul. 1999. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146:1239-1254.
17. Ghadge, G. D., R. P. Roos, U. J. Kang, R. Wollmann, P. S. Fishman, A. M. Kalynych, E. Barr, and J. M. Leiden. 1995. CNS gene delivery by retrograde transport of recombinant replication-defective adenoviruses. Gene Ther. 2:132-137.
18. Gill, S. R., T. A. Schroer, I. Szilak, E. R. Steuer, M. P. Sheetz, and D. W. Cleveland. 1991. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115:1639-1650.
19. Greber, U. F., M. Suomalainen, R. P. Stidwill, 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. Greber, U. F., P. Webster, J. Weber, and A. Helenius. 1996. The role of the adenovirus protease on virus entry into cells. EMBO J. 15:1766-1777.
21. Haase, G., B. Pettmann, E. Vigne, L. Castelnau-Ptakhine, H. Schmalbruch, and A. Kahn. 1998. Adenovirus-mediated transfer of the neurotrophin-3 gene into skeletal muscle of pmn mice: therapeutic effects and mechanisms of action. J. Neurol. Sci. 160(Suppl. 1):S97-S105.
22. Hermens, W. T., and J. Verhaagen. 1997. Adenoviral vector-mediated gene expression in the nervous system of immunocompetent Wistar and T cell-deficient nude rats: preferential survival of transduced astroglial cells in nude rats. Hum. Gene Ther. 8:1049-1063.
23. Hersh, J. R. G. Crystal, and B. Bewig. 1995. Modulation of gene expression after replication-deficient, recombinant adenovirus-mediated gene transfer by the product of a second adenovirus vector. Gene Ther. 2:124-131.
24. Huang, S., T. Kamata, Y. Takada, Z. M. Ruggeri, and G. R. Nemerow. 1996. Adenovirus interaction with distinct integrins mediates separate events in cell entry and gene delivery to hematopoietic cells. J. Virol. 70:4502-4508.
25. Jacob, Y., H. Badrane, P. E. Ceccaldi, and N. Tordo. 2000. Cytoplasmic dynein LC8 interacts with lyssavirus phosphoprotein. J. Virol. 74:10217-10222.
26. Johnston, J. A., M. E. Illing, and R. R. Kopito. 2002. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskelet. 53:26-38.
27. Kalicharran, K., and S. Dales. 1995. Involvement of microtubules and the microtubule-associated protein tau in trafficking of JHM virus and components within neurons. Adv. Exp. Med. Biol. 380:57-61.
28. King, S. M., E. Barbarese, J. F. Dillman III, R. S. Patel-King, J. H. Carson, and K. K. Pfister. 1996. Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain. J. Biol. Chem. 271:19358-19366.
29. Kinoshita, N., T. Mizuno, and Y. Yoshihara. 2002. Adenovirus-mediated WGA gene delivery for transsynaptic labeling of mouse olfactory pathways. Chem. Senses 27:215-223.
30. Kuo, H., D. K. Ingram, R. G. Crystal, and A. Mastrangeli. 1995. Retrograde transfer of replication deficient recombinant adenovirus vector in the central nervous system for tracing studies. Brain Res. 705:31-38.
31. 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 adenoviral gene transfer vectors in living cells. Hum. Gene Ther. 9:367-378.
32. 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.
33. Luftig, R. B., and R. R. Weihing. 1975. Adenovirus binds to rat brain microtubules in vitro. J. Virol. 16:696-706.
34. Luftig, R. B. 1982. Does the cytoskeleton play a significant role in animal virus replication? J. Theor. Biol. 99:173-191.
35. Lukashok, S. A., L. Tarassishin, Y. Li, and M. S. Horwitz. 2000. An adenovirus inhibitor of tumor necrosis factor alpha-induced apoptosis complexes with dynein and a small GTPase. J. Virol. 74:4705-4709.
36. 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.
37. Maccioni, R. B., and V. Cambiazo. 1995. Role of microtubule-associated proteins in the control of microtubule assembly. Physiol. Rev. 75:835-864.
38. Martinez-Moreno, M., I. Navarro-Lerida, F. Roncal, J. P. Albar, C. Alonso, F. Gavilanes, and I. Rodriguez-Crespo. 2003. Recognition of novel viral sequences that associate with the dynein light chain LC8 identified through a pepscan technique. FEBS Lett. 544:262-267.
39. Martinov, V. N., I. Sefland, S. I. Walaas, T. Lomo, A. Nja, and F. Hoover. 2002. Targeting functional subtypes of spinal motoneurons and skeletal muscle fibers in vivo by intramuscular injection of adenoviral and adenoassociated viral vectors. Anat. Embryol. 205:215-221.
40. McDonald D, M. A. Vodicka, G. Lucero, T. M. Svitkina, G. G. Borisy, M. Emerman, and T. J. Hope. 2002. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159:441-452.
41. Miles, B. D., R. B. Luftig, J. A. Weatherbee, R. R. Weihing, and J. Weber. 1980. Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells. Virology 105:265-269.
42. Millecamps, S., D. Nicolle, I. Ceballos-Picot, J. Mallet, and M. Barkats. 2001. Synaptic sprouting increases the uptake capacities of motoneurons in amyotrophic lateral sclerosis mice. Proc. Natl. Acad. Sci. USA 98:7582-7587.
43. Millecamps, S., J. Mallet, and M. Barkats. 2002. Adenoviral retrograde gene transfer in motoneurons is greatly enhanced by prior intramuscular inoculation with botulinum toxin. Hum. Gene Ther. 13:225-232.
44. Mittereder, N., K. L. March, and B. C. Trapnell. 1996. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J. Virol. 70:7498-7509.
45. 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.
46. Murakami, T., I. Nagano, T. Hayashi, Y. Manabe, M. Shoji, Y. Setoguchi, and K. Abe. 2001. Impaired retrograde axonal transport of adenovirus-mediated E. coli LacZ gene in the mice carrying mutant SOD1 gene. Neurosci. Lett. 308:149-152.
47. Paschal, B. M., E. L. Holzbaur, K. K. Pfister, S. Clark, D. I. Meyer, and R. B. Vallee. 1993. Characterization of a 50-kDa polypeptide in cytoplasmic dynein preparations reveals a complex with p150GLUED and a novel actin. J. Biol. Chem. 268:15318-15323.
48. Paschal, B. M., H. S. Shpetner, and R. B. Vallee. 1987. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol. 105:1273-1282.
49. Pasick, J. M., K. Kalicharran, and S. Dales. 1994. Distribution and trafficking of JHM coronavirus structural proteins and virions in primary neurons and the OBL-21 neuronal cell line. J. Virol. 68:2915-2928.
50. Peltekian, E., Garcia, L., Danos, O. 2002. Neurotropism and retrograde axonal transport of a canine adenoviral vector: a tool for targeting key structures undergoing neurodegenerative processes. Mol. Ther. 5:25-32.
51. Petit, C., M. L. Giron, J. Tobaly-Tapiero, P, Bittoun, E. Real, Y. Jacob, N. Tordo, H. De The, and A. Saib. 2003. Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8. J. Cell Sci. 116:3433-3442.
52. Raux, H., A. Flamand, and D. Blondel. 2000. Interaction of the rabies virus P protein with the LC8 dynein light chain. J. Virol. 74:10212-10216.
53. Ridoux, V., J. J. Robert, X. Zhang, M. Perricaudet, J. Mallet, and G. Le Gal La Salle. 1994. Adenoviral vectors as functional retrograde neuronal tracers. Brain Res. 648:171-175.
54. Rosenfeld, M. A., W. Siegfried, K. Yoshimura, K. Yoneyama, M. Fukayama, L. E. Stier, P. K. Paakko, P. Gilardi, L. D. Stratford-Perricaudet, M. Perricaudet, et al. 1991. Adenovirus-mediated transfer of a recombinant alpha 1-antitrypsin gene to the lung epithelium in vivo. Science 252:431-434.
55. Schroer, T. A., and M. P. Sheetz. 1991. Two activators of microtubule-based vesicle transport. J. Cell Biol. 115:1309-1318.
56. Shpetner, H. S., B. M. Paschal, and R. B. Vallee. 1988. Characterization of the microtubule-activated ATPase of brain cytoplasmic dynein (MAP 1C). J. Cell Biol. 107:1001-1009.
57. Soudais, C., C. Laplace-Builhe, K. Kissa, and E. J. Kremer. 2001. Preferential transduction of neurons by canine adenovirus vectors and their efficient retrograde transport in vivo. FASEB J. 15:2283-2285.
58. Suikkanen, S., K. Saajarvi, J. Hirsimaki, O. Valilehto, H. Reunanen, M. Vihinen-Ranta, and M. Vuento. 2002. Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J. Virol. 76:4401-4411.
59. Suikkanen, S., T. Aaltonen, M. Nevalainen, O. Valilehto, L. Lindholm, M. Vuento, and M. Vihinen-Ranta. 2003. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 77:10270-10279.
60. Suomalainen, M., M. Y. Nakano, S. Keller, K. Boucke, R. P. Stidwill, 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.
61. Suomalainen, M., M. Y. Nakano, K. Boucke, S. Keller, and U. F. Greber. 2001. Adenovirus-activated PKA and p38/MAPK pathways boost microtubule-mediated nuclear targeting of virus. EMBO J. 20:1310-1319.
62. Svensson, U., and R. Persson. 1984. Entry of adenovirus 2 into HeLa cells. J. Virol. 51:687-694.
63. Takakuwa, H., F. Goshima, T. Koshizuka, T. Murata, T. Daikoku, and Y. Nishiyama. 2001. Herpes simplex virus encodes a virion-associated protein which promotes long cellular processes in over-expressing cells. Genes Cells 6:955-966.
64. Terashima, T., A. Miwa, Y. Kanegae, I. Saito, H. Okado. 1997. Retrograde and anterograde labeling of cerebellar afferent projection by the injection of recombinant adenoviral vectors into the mouse cerebellar cortex. Anat. Embryol. 196:363-382.
65. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94:3352-3356.
66. Trotman, L. C., N. Mosberger, M. Fornerod, R. P. Stidwill, and U. F. Greber. 2001. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3:1092-1100.
67. Turner, D. E., A. J. Noordmans, E. L. Feldman, and N. M. Boulis. 2001. Remote adenoviral gene delivery to the spinal cord: contralateral delivery and reinjection. Neurosurgery 48:1309-1316.
68. Vale, R. D., T. S. Reese, and M. P. Sheetz. 1985. Identification of a novel force-generating protein, kinesin; involved in microtubule-based motility. Cell 42:39-50.
69. Valentine, R. C., and H. G. Pereira. 1965. Antigens and structure of the adenovirus. J. Mol. Biol. 13:13-20.
70. Vallee, R. B. 1982. A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs). J. Cell Biol. 92:435-442.
71. Vasquez, E. C., R. F. Johnson, T. G. Beltz, R. E. Haskell, B. L. Davidson, and A. K. Johnson. 1998. Replication-deficient adenovirus vector transfer of gfp reporter gene into supraoptic nucleus and subfornical organ neurons. Exp Neurol. 154:353-365.
72. Vincent, T., B. G. Harvey, S. M. Hogan, C. J. Bailey, R. G. Crystal, and P. L. Leopold. 2001. Rapid assessment of adenovirus serum neutralizing antibody titer based on quantitative, morphometric evaluation of capsid binding and intracellular trafficking: population analysis of adenovirus capsid association with cells is predictive of adenovirus infectivity. J. Virol. 75:1516-1521.
73. Wagner, M. C., K. K. Pfister, G. S. Bloom, and S. T. Brady. 1989. Copurification of kinesin polypeptides with microtubule-stimulated Mg-ATPase activity and kinetic analysis of enzymatic properties. Cell Motil. Cytoskelet. 12:195-215.
74. Wang, K., S. Huang, A. Kapoor-Munshi, and G. Nemerow. 1998. Adenovirus internalization and infection require dynamin. J. Virol. 72:3455-3458.
75. Warita, H., K. Abe, Y. Setoguchi, and Y. Itoyama. 1998. Expression of adenovirus-mediated E. coli lacZ gene in skeletal muscles and spinal motor neurons of transgenic mice with a mutant superoxide dismutase gene. Neurosci. Lett. 246:153-156.
76. Weatherbee, J. A., R. B. Luftig, and R. R. Weihing. 1977. Binding of adenovirus to microtubules. II. Depletion of high-molecular-weight microtubule-associated protein content reduces specificity of in vitro binding. J. Virol. 21:732-742.
77. Wickham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
78. Wickham, T. J., E. J. Filardo, D. A. Cheresh, G. R. Nemerow. 1994. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol. 127:257-264.
79. Wisnivesky, J. P., P. L. Leopold, R. G. Crystal. 1999. Specific binding of the adenovirus capsid to the nuclear envelope. Hum. Gene Ther. 10:2187-2195.
80. Yamashita, S., S. Mita, T. Arima, Y. Maeda, E. Kimura, Y. Nishida, T. Murakami, H. Okado, and M. Uchino. 2001. Bcl-2 expression by retrograde transport of adenoviral vectors with Cre-loxP recombination system in motor neurons of mutant SOD1 transgenic mice. Gene Ther. 8:977-986.
81. Yamashita, S., S. Mita, S. Kato, H. Okado, E. Ohama, and M. Uchino. 2002. Effect on motor neuron survival in mutant SOD1 (G93A) transgenic mice by Bcl-2 expression using retrograde axonal transport of adenoviral vectors. Neurosci. Lett. 328:289-293.
82. L34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane. J. Virol. 74:1355-1363.
83. Ye, G. J., and B. Roizman. 2000. The essential protein encoded by the UL31 gene of herpes simplex virus 1 depends for its stability on the presence of UL34 protein. Proc. Natl. Acad. Sci. USA 97:11002-11007.