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Journal of Virology, June 2005, p. 6655-6663, Vol. 79, No. 11
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.11.6655-6663.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Glycoprotein D Receptor-Dependent, Low-pH-Independent Endocytic Entry of Herpes Simplex Virus Type 1

Richard S. B. Milne,1,2,3* Anthony V. Nicola,4 J. Charles Whitbeck,1,2,3 Roselyn J. Eisenberg,2,3 and Gary H. Cohen1,2

Department of Microbiology,1 Center for Oral Health Research, School of Dental Medicine,2 Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104,3 Medical Virology Section, Laboratory of Clinical Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892-18884

Received 8 November 2004/ Accepted 18 January 2005

Two herpes simplex virus type 1 (HSV-1) entry pathways have been described: direct fusion between the virion envelope and the plasma membrane, as seen on Vero cells, and low-pH-dependent endocytosis, as seen on CHO nectin-1 and HeLa cells. In this paper, we studied HSV entry into C10 murine melanoma cells and identified a third entry pathway for this virus. During entry into C10 cells, virion envelope glycoproteins rapidly became protected from the membrane-impermeable chemical cross-linker BS3 and from proteinase K. Protection was gD receptor dependent, and the time taken to detect protected protein was proportional to the rate of virus entry. Ultrastructural examination revealed that virions attached to the surface of C10 cells were localized to membrane invaginations, whereas those on the surface of receptor-negative B78 cells were peripherally attached. Virus entry into C10 cells was energy dependent, and intracellular enveloped virions were seen within membrane-bound vesicles consistent with endocytic entry. Entry was not inhibited by bafilomycin A1 or ammonium chloride, showing that passage of the virion through a low-pH environment was not required for infection. Resistance to similar reagents should therefore not be taken as proof of HSV entry by a nonendosomal pathway. These data define a novel gD receptor-dependent acid-independent endocytic entry pathway for HSV.

* Corresponding author. Mailing address: Department of Microbiology, University of Pennsylvania, School of Dental Medicine, 215 Levy Building, 240 South 40th Street, Philadelphia, PA 19104-6002. Phone: (215) 898-6553. Fax: (215) 898-8385. E-mail: rmilne{at}biochem.dental.upenn.edu.

Journal of Virology, June 2005, p. 6655-6663, Vol. 79, No. 11
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.11.6655-6663.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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