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Journal of Virology, March 2003, p. 3191-3203, Vol. 77, No. 5
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.5.3191-3203.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Envelopment of Human Cytomegalovirus Occurs by Budding into Golgi-Derived Vacuole Compartments Positive for gB, Rab 3, Trans-Golgi Network 46, and Mannosidase II

M. Homman-Loudiyi,1 K. Hultenby,2 W. Britt,3 and C. Söderberg-Nauclér1*

Department of Medicine, Center for Molecular Medicine, Karolinska Institute, SE 171 76 Stockholm,1 Clinical Research Center, Karolinska Institutet, Huddinge University Hospital, SE 141 86 Huddinge, Sweden,2 Departments of Pediatrics and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama 3523323

Received 30 October 2002/ Accepted 26 November 2002

Although considerable progress has been made towards characterizing virus assembly processes, assignment of the site of tegumentation and envelopment for human cytomegalovirus (HCMV) is still not clear. In this study, we examined the envelopment of HCMV particles in human lung fibroblasts (HF) HL 411 and HL 19, human umbilical vein endothelial cells, human pulmonary arterial endothelial cells, and arterial smooth muscle cells at different time points after infection by electron microscopy (EM), immunohistochemistry, and confocal microscopy analysis. Double-immunofluorescence labeling experiments demonstrated colocalization of the HCMV glycoprotein B (gB) with the Golgi resident enzyme mannosidase II, the Golgi marker TGN (trans-Golgi network) 46, and the secretory vacuole marker Rab 3 in all cell types investigated. Final envelopment of tegumented capsids was observed at 5 days postinfection by EM, when tegumented capsids budded into subcellular compartments located in the cytoplasm, in close proximity to the Golgi apparatus. Immunogold labeling and EM analysis confirmed staining of the budding compartment with HCMV gB, Rab 3, and mannosidase II in HL 411 cells. However, the markers Rab 1, Rab 2, Rab 7, Lamp 1 (late endosomes and lysosomes), and Lamp 2 (lysosomes) neither showed specific staining of the budding compartment in the immunogold labeling experiments nor colocalized with gB in the immunofluorescent colocalization experiments in any cell type studied. Together, these results suggest that the final envelopment of HCMV particles takes place mainly into a Golgi-derived secretory vacuole destined for the plasma membrane, which may release new infectious virus particles by fusion with the plasma membrane.

* Corresponding author. Mailing address: Department of Medicine, Center for Molecular Medicine, Karolinska Institutet, SE-171 76 Stockholm, Sweden. Phone: 46-8-51779896. Fax: 46-8-313147. E-mail: cecilia.soderberg.naucler{at}cmm.ki.se.

Journal of Virology, March 2003, p. 3191-3203, Vol. 77, No. 5
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.5.3191-3203.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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