Microtubule-dependent Plus- and Minus End-directed Motilities Are Competing Processes for Nuclear Targeting of Adenovirus

doi:10.1083/jcb.144.4.657

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© The Rockefeller University Press, 0021-9525/1999//657 $5.00
The Journal of Cell Biology, Volume 144, Number 4, , 1999 657-672

Regular Articles

Microtubule-dependent Plus- and Minus End–directed Motilities Are Competing Processes for Nuclear Targeting of Adenovirus

Maarit Suomalainen, Michel Y. Nakano, Stephan Keller, Karin Boucke, Robert P. Stidwill, and Urs F. Greber

Institute of Zoology, University of Zürich, CH-8057 Zürich, Switzerland

Adenovirus (Ad) enters target cells by receptor-mediated endocytosis,escapes to the cytosol, and then delivers its DNA genome intothe nucleus. Here we analyzed the trafficking of fluorophore-tagged viruses in HeLa and TC7 cells by time-lapse microscopy. Ourresults show that native or taxol-stabilized microtubules (MTs)support alternating minus- and plus end–directed movementsof 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 elementaryspeeds at frequencies up to 1 Hz was observed in the periphery and near the MT organizing center (MTOC) after recovery fromnocodazole treatment. MT-dependent motilities allowed virusaccumulation near the MTOC at population speeds of 1–10µm/min, depending on the cell type. Overexpression ofp50/dynamitin, which is known to affect dynein-dependent minusend–directed vesicular transport, significantly reducedthe extent and the frequency of minus end–directed migrationof cytosolic virus, and increased the frequency, but not theextent of plus end–directed motility. The data imply thata single cytosolic Ad particle engages with two types of MT-dependentmotor activities, the minus end– directed cytoplasmicdynein and an unknown plus end– directed activity.

Key Words: adenovirus • virus entry • microtubules • bidirectional movement • dynein/dynactin

Abbreviations used in this paper: Ad, adenovirus; Ad2, adenovirus type 2; Dyn, p50/dynamitin; ES, elementary speed; FISH, fluorescence in situ hybridization; GFP, enhanced green fluorescent protein; MAP, microtubule-associated protein; MT, microtubule; MTB, microtubule-binding domain; MTOC, microtubule organizing center; pFA, paraformaldehyde; p.i., post infection; TC7/MAP4/MTB–GFP, TC7 cells stably expressing the hybrid of MAP4/MTB–GFP; TR, Texas red; ts, temperature-sensitive; wt, wild-type.

M. Suomalainen and M.Y. Nakano contributed equally to this work.

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