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Journal of Virology, November 2003, p. 11332-11346, Vol. 77, No. 21
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.21.11332-11346.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Measles Virus (MV) Nucleoprotein Binds to a Novel Cell Surface Receptor Distinct from Fc{gamma}RII via Its C-Terminal Domain: Role in MV-Induced Immunosuppression

David Laine,1 Marie-Claude Trescol-Biémont,1 Sonia Longhi,2 Geneviève Libeau,3 Julien C. Marie,1,{dagger} Pierre-Olivier Vidalain,1 Olga Azocar,1 Adama Diallo,4 Bruno Canard,2 Chantal Rabourdin-Combe,1 and Hélène Valentin1*

Laboratoire d'Immunobiologie Fondamentale et Clinique, INSERM U503, IFR128 BioSciences Lyon-Gerland, 69365 Lyon Cedex 07,1 Architecture et Fonction des Macromolécules Biologiques, UMR 6098,CNRS et Universités d'Aix-Marseille, 13288 Marseille,2 Programme Santé Animale, CIRAD/EMVT, 34398 Montpellier Cedex 5, France,3 Animal Production Unit, Agriculture and Biotechnology Laboratory, IAEA Laboratories, A-2444 Seibersdorf, Austria4

Received 19 February 2003/ Accepted 22 July 2003

During acute measles virus (MV) infection, an efficient immune response occurs, followed by a transient but profound immunosuppression. MV nucleoprotein (MV-N) has been reported to induce both cellular and humoral immune responses and paradoxically to account for immunosuppression. Thus far, this latter activity has been attributed to MV-N binding to human and murine Fc{gamma}RII. Here, we show that apoptosis of MV-infected human thymic epithelial cells (TEC) allows the release of MV-N in the extracellular compartment. This extracellular N is then able to bind either to MV-infected or uninfected TEC. We show that recombinant MV-N specifically binds to a membrane protein receptor, different from Fc{gamma}RII, highly expressed on the cell surface of TEC. This new receptor is referred to as nucleoprotein receptor (NR). In addition, different Ns from other MV-related morbilliviruses can also bind to Fc{gamma}RII and/or NR. We show that the region of MV-N responsible for binding to NR maps to the C-terminal fragment (NTAIL). Binding of MV-N to NR on TEC triggers sustained calcium influx and inhibits spontaneous cell proliferation by arresting cells in the G0 and G1 phases of the cell cycle. Finally, MV-N binds to both constitutively expressed NR on a large spectrum of cells from different species and to human activated T cells, leading to suppression of their proliferation. These results provide evidence that MV-N, after release in the extracellular compartment, binds to NR and thereby plays a role in MV-induced immunosuppression.

* Corresponding author. Mailing address: Laboratoire d'Immunobiologie Fondamentale et Clinique, INSERM U503, 21 Avenue Tony Garnier, 69365 Lyon Cedex 07, France. Phone: (33) 4-37-28-23-77. Fax: (33) 4-37-28-23-41. E-mail: valentin{at}cervi-lyon.inserm.fr.

{dagger} Present address: Department of Immunology, University of Washington, Seattle, WA 98195-7370.

Journal of Virology, November 2003, p. 11332-11346, Vol. 77, No. 21
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.21.11332-11346.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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