Crossref journal-article
Rockefeller University Press
The Journal of Cell Biology (291)
Abstract

Adenovirus (Ad) enters target cells by receptor-mediated endocytosis, escapes to the cytosol, and then delivers its DNA genome into the nucleus. Here we analyzed the trafficking of fluorophore-tagged viruses in HeLa and TC7 cells by time-lapse microscopy. Our results show that native or taxol-stabilized microtubules (MTs) support alternating minus- and plus end–directed movements of cytosolic virus with elementary speeds up to 2.6 μm/s. No directed movement was observed in nocodazole-treated cells. Switching between plus- and minus end–directed elementary speeds at frequencies up to 1 Hz was observed in the periphery and near the MT organizing center (MTOC) after recovery from nocodazole treatment. MT-dependent motilities allowed virus accumulation near the MTOC at population speeds of 1–10 μm/min, depending on the cell type. Overexpression of p50/dynamitin, which is known to affect dynein-dependent minus end–directed vesicular transport, significantly reduced the extent and the frequency of minus end–directed migration of cytosolic virus, and increased the frequency, but not the extent of plus end–directed motility. The data imply that a single cytosolic Ad particle engages with two types of MT-dependent motor activities, the minus end– directed cytoplasmic dynein and an unknown plus end– directed activity.

Bibliography

Suomalainen, M., Nakano, M. Y., Keller, S., Boucke, K., Stidwill, R. P., & Greber, U. F. (1999). Microtubule-dependent Plus- and Minus End–directed Motilities Are Competing Processes for Nuclear Targeting of Adenovirus. The Journal of Cell Biology, 144(4), 657–672.

Authors 6
  1. Maarit Suomalainen (first)
  2. Michel Y. Nakano (additional)
  3. Stephan Keller (additional)
  4. Karin Boucke (additional)
  5. Robert P. Stidwill (additional)
  6. Urs F. Greber (additional)
References 76 Referenced 371
  1. 10.1083/jcb.140.2.391 / J Cell Biol / Cytoplasmic dynein and dynactin are required for the transport Of microtubules into the axon by Ahmad (1998)
  2. 10.1083/jcb.123.6.1373 / J Cell Biol / Cytoplasmic dynein-dependent vesicular transport from early to late endosomes by Aniento (1993)
  3. 10.1247/csf.22.139 / Cell Struct Funct / Molecular mechanisms of myofibril assembly in heart by Auerbach (1997)
  4. 10.1016/S0955-0674(97)80159-7 / Curr Opin Cell Biol / mRNA and cytoskeletal filaments by Bassell (1997)
  5. 10.1038/295701a0 / Nature / Inhibitors of dynein activity block intracellular transport in erythrophores by Beckerle (1982)
  6. 10.1126/science.275.5304.1320 / Science / Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5 by Bergelson (1997)
  7. 10.1074/jbc.272.31.19418 / J Biol Chem / Phosphorylation by p34cdc2 protein kinase regulates binding of the kinesin-related motor HsEg5 to the dynactin subunit p150 by Blangy (1997)
  8. 10.1083/jcb.137.1.113 / J Cell Biol / Molecular requirements for bi-directional movement of phagosomes along microtubules by Blocker (1997)
  9. 10.1242/jcs.110.24.3055 / J Cell Sci / Overexpression of Map4 inhibits organelle motility and trafficking in vivo by Bulinski (1997)
  10. 10.1083/jcb.139.2.469 / J Cell Biol / Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution by Burkhardt (1997)
  11. {'key': '2023072900081569800_B11'}
  12. 10.1016/S0092-8674(00)80360-8 / Cell / The directional preference of kinesin motors is specified by an element outside of the motor catalytic domain by Case (1997)
  13. 10.1083/jcb.141.4.993 / J Cell Biol / Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis eleganssensory neurons by Cole (1998)
  14. 10.1016/S0966-842X(97)01011-1 / Trends Microbiol / Viral manipulations of the actin cytoskeleton by Cudmore (1997)
  15. 10.1016/0042-6822(73)90050-0 / Virology / 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 by Dales (1973)
  16. 10.1073/pnas.93.18.9559 / Proc Natl Acad Sci USA / Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling by Daro (1996)
  17. 10.1146/annurev.cellbio.13.1.83 / Ann Rev Cell Dev Biol / Microtubule polymerization dynamics by Desai (1997)
  18. 10.1083/jcb.101.1.19 / J Cell Biol / An efficient method for introducing macromolecules into living cells by Doxsey (1985)
  19. 10.1083/jcb.132.4.617 / J Cell Biol / Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis by Echeverri (1996)
  20. 10.1083/jcb.139.5.1169 / J Cell Biol / Molecular motors and a spectrin matrix associate with Golgi membranes in vitro by Fath (1997)
  21. 10.1038/37663 / Nature / An extended microtubule-binding structure within the dynein motor domain by Gee (1997)
  22. 10.1073/pnas.87.17.6579 / Proc Natl Acad Sci USA / Detection of individual fluorescently labeled reovirions in living cells by Georgi (1990)
  23. {'key': '2023072900081569800_B23', 'first-page': '132', 'article-title': 'CNS gene delivery by retrograde transport of recombinant replication-defective adenoviruses', 'volume': '2', 'author': 'Ghadge', 'year': '1995', 'journal-title': 'Gene Ther'} / Gene Ther / CNS gene delivery by retrograde transport of recombinant replication-defective adenoviruses by Ghadge (1995)
  24. 10.1016/S0955-0674(97)80147-0 / Curr Opin Cell Biol / Motors and membrane traffick by Goodson (1997)
  25. {'key': '2023072900081569800_B25'}
  26. 10.1002/(SICI)1099-1654(1998100)8:4<213::AID-RMV225>3.0.CO;2-W / Rev Med Virol / Virus assembly and disassembly: the adenovirus cysteine protease as a trigger factor by Greber (1998)
  27. 10.1016/0092-8674(93)90382-Z / Cell / Stepwise dismantling of adenovirus 2 during entry into cells by Greber (1993)
  28. 10.1002/j.1460-2075.1996.tb00525.x / EMBO (Eur Mol Biol Organ) J / The role of the adenovirus protease in virus entry into cells by Greber (1996)
  29. 10.1093/emboj/16.19.5998 / EMBO (Eur Mol Biol Organ) J / The role of the nuclear pore complex in adenovirus DNA entry by Greber (1997)
  30. {'key': '2023072900081569800_B30'}
  31. 10.1083/jcb.108.4.1301 / J Cell Biol / Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro by Gruenberg (1989)
  32. 10.1016/S0959-437X(96)80059-1 / Curr Opin Gen Dev / RNA localization and the development of asymmetry during Drosophilaoogenesis by Grünert (1996)
  33. 10.1073/pnas.82.23.7952 / Proc Natl Acad Sci USA / Complexes of polyoma virus medium T antigen and cellular proteins by Grussenmeyer (1985)
  34. 10.1038/38022 / Nature / Reversal in the direction of movement of a molecular motor by Henningsen (1997)
  35. 10.1126/science.279.5350.519 / Science / Kinesin and dynein superfamily proteins and the mechanism of organelle transport by Hirokawa (1998)
  36. 10.1016/S0955-0674(98)80087-2 / Curr Opin Cell Biol / Kinesin and dynein superfamily proteins in organelle transport and cell division by Hirokawa (1998)
  37. 10.1016/S0074-7696(08)62168-3 / Int Rev Cytol / The role of the dynactin complex in intracellular motility by Holleran (1998)
  38. {'key': '2023072900081569800_B38'}
  39. 10.1038/39247 / Nature / Molecular motors: structural adaptations to cellular functions by Howard (1997)
  40. 10.1073/pnas.94.24.12747 / Proc Natl Acad Sci USA / Motor proteins of the eukaryotic cytoskeleton by Hoyt (1997)
  41. 10.1146/annurev.genet.31.1.113 / Annu Rev Genet / Host-pathogen interactions during entry and actin-based movement of Listeriamonocytogenes by Ireton (1997)
  42. 10.1073/pnas.94.10.5078 / Proc Natl Acad Sci USA / Microtubule release from the centrosome by Keating (1997)
  43. 10.1242/jcs.109.8.2089 / J Cell Sci / The intracompartmental sorting of myosin alkali light chain isoproteins reflects the sequence of developmental expression as determined by double epitope-tagging competition by Komiyama (1996)
  44. 10.1002/j.1460-2075.1987.tb02550.x / EMBO (Eur Mol Biol Organ) J / Microtubules containing detyrosinated tubulin are less dynamic by Kreis (1987)
  45. 10.1089/hum.1998.9.3-367 / Hum Gene Ther / Fluorescent virions—dynamic tracking of the pathway of adenoviral gene transfer vectors in living cells by Leopold (1998)
  46. 10.1242/jcs.108.11.3473 / J Cell Sci / Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion by Liao (1995)
  47. 10.1016/S0955-0674(98)80086-0 / Curr Opin Cell Biol / Cytoskeletal proteins and Golgi dynamics by Lippincott-Schwartz (1998)
  48. 10.1016/0955-0674(94)90109-0 / Curr Opin Cell Biol / Physical properties of the cytoplasm by Luby-Phelps (1994)
  49. 10.1128/jvi.16.3.696-706.1975 / J Virol / Adenovirus binds to rat brain microtubules in vitro by Luftig (1975)
  50. 10.1016/0955-0674(95)80047-6 / Curr Opin Cell Biol / Microtubules and microtubule-associated proteins by Mandelkow (1995)
  51. 10.1126/science.279.5350.527 / Science / Unconventional myosins in cell movement, membrane traffic, and signal transduction by Mermall (1998)
  52. 10.1016/0042-6822(80)90177-4 / Virol / Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells by Miles (1980)
  53. 10.1242/jcs.109.4.875 / J Cell Sci / γ-Tubulin in mammalian cells: the centrosomal and the cytosolic forms by Moudjou (1996)
  54. 10.1242/jcs.110.2.281 / J Cell Sci / Overexpression of full- or partial length Map4 stabilizes microtubules and alters cell growth by Nguyen (1997)
  55. 10.1002/(SICI)1097-0169(1996)33:1<38::AID-CM5>3.0.CO;2-E / Cell Motil Cytoskel / γ Tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies by Novakova (1996)
  56. 10.1083/jcb.130.3.639 / J Cell Biol / Analysis of MAP 4 function in living cells using green fluorescent protein (GFP) chimeras by Olson (1995)
  57. 10.1083/jcb.141.4.979 / J Cell Biol / A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT) by Pazour (1998)
  58. 10.1083/jcb.131.1.111 / J Cell Biol / Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2 by Prchla (1995)
  59. 10.1038/38001 / Nature / ER-to-Golgi transport visualized in living cells by Presley (1997)
  60. 10.1091/mbc.9.7.1617 / Mol Biol Cell / Golgi membrane dynamics by Presley (1998)
  61. 10.1016/0962-8924(96)10017-9 / Trends Cell Biol / Clips for organelle–microtubule interactions by Rickard (1996)
  62. 10.1016/0006-8993(94)91919-4 / Brain Res / Adenoviral vectors as functional retrograde neuronal tracers by Ridoux (1994)
  63. 10.1006/scdb.1996.0041 / Semin Cell Dev Biol / Structure and function of dynactin by Schroer (1996)
  64. 10.1083/jcb.138.1.131 / J Cell Biol / Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus by Seksek (1997)
  65. {'key': '2023072900081569800_B65'}
  66. 10.1083/jcb.136.5.1007 / J Cell Biol / Microtubule-mediated transport of incoming Herpes Simplex Virus 1 capsids to the nucleus by Sodeik (1997)
  67. 10.1083/jcb.133.4.831 / J Cell Biol / Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles by Vaisberg (1996)
  68. 10.1146/annurev.cellbio.13.1.745 / Annu Rev Cell Dev Biol / The design plan of kinesin motors by Vale (1997)
  69. 10.1126/science.271.5255.1539 / Science / Targeting of motor proteins by Vallee (1996)
  70. 10.1083/jcb.139.2.417 / J Cell Biol / Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling by Waterman-Storer (1997)
  71. 10.1016/S0960-9822(02)00495-5 / Curr Biol / Cytoskeleton: a catastrophic kinesin by Waters (1996)
  72. 10.1128/jvi.21.2.732-742.1977 / J Virol / Binding of adenovirus to microtubules. II. Depletion of high-molecular-weight microtubule-associated protein content reduces specificity of in vitro binding by Weatherbee (1977)
  73. {'key': '2023072900081569800_B73'}
  74. 10.1016/S0955-0674(97)80152-4 / Curr Opin Cell Biol / Actin dynamics in vivo by Welch (1997)
  75. 10.1006/viro.1998.9165 / Virology / Nuclear import and export of viruses and virus genomes by Whittaker (1998)
  76. 10.1016/S0092-8674(00)80329-3 / Cell / Microtubule interaction site of the kinesin motor by Woehlke (1997)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited 2 years, 1 month ago (July 28, 2023, 8:10 p.m.)
Indexed 1 month ago (Aug. 5, 2025, 8:26 a.m.)
Issued 26 years, 6 months ago (Feb. 22, 1999)
Published 26 years, 6 months ago (Feb. 22, 1999)
Published Online 26 years, 6 months ago (Feb. 22, 1999)
Published Print 26 years, 6 months ago (Feb. 22, 1999)
Funders 0

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@article{Suomalainen_1999, title={Microtubule-dependent Plus- and Minus End–directed Motilities Are Competing Processes for Nuclear Targeting of Adenovirus}, volume={144}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.144.4.657}, DOI={10.1083/jcb.144.4.657}, number={4}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Suomalainen, Maarit and Nakano, Michel Y. and Keller, Stephan and Boucke, Karin and Stidwill, Robert P. and Greber, Urs F.}, year={1999}, month=feb, pages={657–672} }