X-linked Lymphoproliferative Disease: 2B4 Molecules Displaying Inhibitory Rather Than Activating Function Are Responsible for the Inability of Natural Killer Cells to Kill Epstein-Barr Virus-infected Cells

doi:10.1084/jem.192.3.337

Published online 31 July 2000.

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© The Rockefeller University Press, 0022-1007/2000/8/337/ $5.00
The Journal of Experimental Medicine, Volume 192, Number 3, August 7, 2000 337-346

Original Article

X-linked Lymphoproliferative Disease: 2B4 Molecules Displaying Inhibitory Rather Than Activating Function Are Responsible for the Inability of Natural Killer Cells to Kill Epstein-Barr Virus–infected Cells

Silvia Parolini^a, Cristina Bottino^b, Michela Falco^c, Raffaella Augugliaro^b, Silvia Giliani^d, Roberta Franceschini^d, Hans D. Ochs^e, Hermann Wolf^f, Jean-Yves Bonnefoy^g, Roberto Biassoni^b, Lorenzo Moretta^b,c, Luigi D. Notarangelo^d, and Alessandro Moretta^c
^a Dipartimento di Scienze Biomediche e Biotecnologie, Università di Brescia, 25123 Brescia, Italy
^b Istituto Nazionale per la Ricerca sul Cancro, 16132 Genova, Italy
^c Dipartimento di Medicina Sperimentale, Università di Genova, 16132 Genova, Italy
^d Istituto di Medicina Molecolare Angelo Nocivelli, Clinica Pediatrica, Università di Brescia, 25123 Brescia, Italy
^e Department of Pediatrics, University of Washington, Seattle, Washington 98195-6320
^f Department of Immunology, University of Vienna, A-1090 Vienna, Austria
^g Centre d'Immunologie Pierre Fabre, F74164 St. Julien-en-Genevois, France

Correspondence to: Alessandro Moretta, Dipartimento di Medicina Sperimentale, Sezione di Istologia, Via G.B. Marsano 10, 16132 Genova, Italy. Tel:39-10-3537868 Fax:39-10-512747 E-mail:alemoret{at}unige.it.

2B4 is a surface molecule involved in activation of the naturalkiller (NK) cell–mediated cytotoxicity. It binds a proteintermed Src homology 2 domain–containing protein (SH2D1A)or signaling lymphocyte activation molecule (SLAM)-associatedprotein (SAP), which in turn has been proposed to function asa regulator of the 2B4-associated signal transduction pathway.In this study, we analyzed patients with X-linked lymphoproliferativedisease (XLP), a severe inherited immunodeficiency characterizedby critical mutations in the SH2D1A gene and by the inabilityto control Epstein-Barr virus (EBV) infections. We show that,in these patients, 2B4 not only fails to transduce triggeringsignals, but also mediates a sharp inhibition of the NK-mediatedcytolysis. Other receptors involved in NK cell triggering, includingCD16, NKp46, NKp44, and NKp30, displayed a normal functionalcapability. However, their activating function was inhibitedupon engagement of 2B4 molecules. CD48, the natural ligand of2B4, is highly expressed on the surface of EBV⁺ B cell lines.Remarkably, NK cells from XLP patients could not kill EBV⁺ Bcell lines. This failure was found to be the consequence ofinhibitory signals generated by the interaction between 2B4and CD48, as the antibody-mediated disruption of the 2B4–CD48interaction restored lysis of EBV⁺ target cells lacking humanhistocompatibility leukocyte antigen (HLA) class I molecules.In the case of autologous or allogeneic (HLA class I⁺) EBV⁺lymphoblastoid cell lines, restoration of lysis was achievedonly by the simultaneous disruption of 2B4–CD48 and NKreceptor–HLA class I interactions. Molecular analysisrevealed that 2B4 molecules isolated from either XLP or normalNK cells were identical. As expected, in XLP-NK cells, 2B4 didnot associate with SH2D1A, whereas similar to 2B4 moleculesisolated from normal NK cells, it did associate with Src homology2 domain–containing phosphatase 1.

Key Words: X-linked lymphoproliferative disease, Epstein-Barr virus infection,natural killer cell, natural cytotoxicity receptor, 2B4 molecule

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