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Journal of Virology, September 1998, p. 7181-7190, Vol. 72, No. 9
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

The Neural Cell Adhesion Molecule Is a Receptor for Rabies Virus

Maria-Isabel Thoulouze,1 Mireille Lafage,1 Melitta Schachner,2 Ursula Hartmann,3 Harold Cremer,4 and Monique Lafon1,*

Departement de Virologie, Institut Pasteur, Paris,1 and IBDM/LGPD, CNRS/INSERM/Université de Méditerranée, Campus de Luminy, Marseille,4 France, and Zentrum für Molekulare Neurobiologie, Universität Hamburg, Hamburg,2 and Institut für Genetik, Heinrich-Heine-Universität, Düsseldorf,3 Germany

Received 29 January 1998/Accepted 27 May 1998

Previous reports strongly suggest that, in addition to the nicotinic acetylcholine receptor, rabies virus can use other, as-yet-unidentified receptors. We found that laboratory cell lines susceptible to rabies virus infection express the neural cell adhesion molecule (NCAM) (CD56) on their surface, whereas resistant cells do not, supporting the idea that NCAM could be a rabies virus receptor. We observed that (i) incubation with rabies virus decreases the surface expression of NCAM; (ii) treatment of susceptible cells with heparan sulfate, a ligand for NCAM, or with NCAM antibodies significantly reduces the rabies virus infection; and (iii) preincubation of rabies virus inoculum with soluble NCAM protein as a receptor decoy drastically neutralizes the capacity of rabies virus to infect susceptible cells. Moreover, we demonstrated that transfection of resistant L fibroblasts with the NCAM-encoding gene induces rabies virus susceptibility whereas absence of NCAM in the primary cortical cell cultures prepared from NCAM-deficient mice reduces the rabies virus infection and virus production. This provides evidence that NCAM is an in vitro receptor for the rabies virus. Moreover, the in vivo relevance for the use of NCAM as a receptor was demonstrated by the infection of NCAM-deficient mice, in which rabies mortality was delayed and brain invasion by rabies virus was drastically restricted. Our results showed that NCAM, which is expressed mainly in the adult nervous system, plays an important role in rabies infection. However, it cannot be excluded that receptors other than NCAM are utilized. Thus, the description of NCAM as a new rabies virus receptor would be another example of the use by viruses of more than one receptor to gain entry into the host.

* Corresponding author. Mailing address: Institut Pasteur, Unité de Neurovirologie et Régénération du Système Nerveux, Groupe de Neuro-Immunologie Virale, 25, rue du Dr. Roux, 75724 Paris Cedex 15, France. Phone: 33 1 45 68 87 52. Fax: 33 1 40 61 33 12. E-mail: mlafon{at}pasteur.fr.

Journal of Virology, September 1998, p. 7181-7190, Vol. 72, No. 9
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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