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Journal of Virology, April 2000, p. 3321-3329, Vol. 74, No. 7
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

An Envelope Glycoprotein of the Human Endogenous Retrovirus HERV-W Is Expressed in the Human Placenta and Fuses Cells Expressing the Type D Mammalian Retrovirus Receptor

Jean-Luc Blond,1 Dimitri Lavillette,2 Valérie Cheynet,1 Olivier Bouton,1 Guy Oriol,1 Sylvie Chapel-Fernandes,2 Bernard Mandrand,1 François Mallet,1,* and François-Loïc Cosset2

Unité Mixte 103 CNRS-bioMérieux1 and Laboratoire de Vectorologie Rétrovirale et Thérapie Génique, INSERM U412,2 Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 07, France

Received 10 November 1999/Accepted 3 January 2000

A new human endogenous retrovirus (HERV) family, termed HERV-W, was recently described (J.-L. Blond, F. Besème, L. Duret, O. Bouton, F. Bedin, H. Perron, B. Mandrand, and F. Mallet, J. Virol. 73:1175-1185, 1999). HERV-W mRNAs were found to be specifically expressed in placenta cells, and an env cDNA containing a complete open reading frame was recovered. In cell-cell fusion assays, we demonstrate here that the product of the HERV-W env gene is a highly fusogenic membrane glycoprotein. Transfection of an HERV-W Env expression vector in a panel of cell lines derived from different species resulted in formation of syncytia in primate and pig cells upon interaction with the type D mammalian retrovirus receptor. Moreover, envelope glycoproteins encoded by HERV-W were specifically detected in placenta cells, suggesting that they may play a physiological role during pregnancy and placenta formation.


* Corresponding author. Mailing address: Unité Mixte 103 CNRS-bioMérieux, Ecole Normale Supérieure de Lyon, 46 allée d'Italie, 69364 Lyon Cedex 07, France. Phone: 33472 72 83 58. Fax: 33472 72 85 33. E-mail: fmallet{at}ens-bma.cnrs.fr.


Journal of Virology, April 2000, p. 3321-3329, Vol. 74, No. 7
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



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  • Pavlicek, A., Paces, J., Elleder, D., Hejnar, J. (2002). Processed Pseudogenes of Human Endogenous Retroviruses Generated by LINEs: Their Integration, Stability, and Distribution. Genome Res 12: 391-399 [Abstract] [Full Text]