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Steve Pascolo^*, Nathalie Bervas^*, Jan M. Ure, Austin G. Smith, François A. Lemonnier^*, and Béatrice Pérarnau^*

From the ^* Institut Pasteur, Département SIDA-Rétrovirus, Unité d'Immunité Cellulaire Antivirale, 75724 Paris Cedex 15, France; and Gene Targeting Laboratory, Centre for Genome Research, University of Edinburgh, Edinburgh EH9 3JQ, United Kingdom

Three different HLA-A2.1 monochains were engineered in which either the human or mouse β2-microglobulin (β2m) is covalently linked to the NH₂ terminus of the heavy chain by a 15– amino acid long peptide: HHH, entirely human, HHD, with the mouse H-2D^b 3, transmembrane, and cytoplasmic domains, and MHD, homologous to HHD but linked to the mouse β2m^b. The cell surface expression and immunological capacities of the three monochains were compared with transfected cells, and the selected HHD construct was introduced by transgenesis in H-2D^b–/– β2m^–/– double knockout mice. Expression of this monochain restores a sizable peripheral CD8⁺ T cell repertoire essentially educated on the transgenic human molecule. Consequently, infected HHD, H-2D^b–/– β2m^–/– mice generate only HLA-A2.1–restricted CD8⁺ CTL responses against influenza A and vaccinia viruses. Interestingly, the CTL response to influenza A virus is mostly, if not exclusively, directed to the 58-66 matrix peptide which is the HLA-A2.1–restricted immunodominant epitope in humans. Such mice might constitute a versatile animal model for the study of HLA-A2.1–restricted CTL responses of vaccine interest.

During her postdoctoral stay at the Centre for Genome Research (Edinburgh, U.K.), B. Pérarnau was a recipient of a fellowship from the Human Frontier Science Program Organisation. The Centre for Genome Research is supported by the Biotechnology and Biological Sciences Research Council of the United Kingdom. This work was funded by the Institut Pasteur and by grants from the Association pour la Recherche contre le Cancer, the Ligue contre le Cancer, and the Pasteur-Weizmann committees.

¹Abbreviations used in this paper: β2m, β-2 microglobulin; HA, hemagglutinin; TAP, transporter associated with antigen presentation.

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• Cheuk, E., D'Souza, C., Hu, N., Liu, Y., Lang, H., Chamberlain, J. W. (2002). Human MHC Class I Transgenic Mice Deficient for H2 Class I Expression Facilitate Identification and Characterization of New HLA Class I-Restricted Viral T Cell Epitopes. J. Immunol. 169: 5571-5580 [Abstract] [Full Text]  
• Himoudi, N., Abraham, J.-D., Fournillier, A., Lone, Y. C., Joubert, A., De Beeck, A. O., Freida, D., Lemonnier, F., Kieny, M. P., Inchauspe, G. (2002). Comparative Vaccine Studies in HLA-A2.1-Transgenic Mice Reveal a Clustered Organization of Epitopes Presented in Hepatitis C Virus Natural Infection. J. Virol. 76: 12735-12746 [Abstract] [Full Text]  
• Francini, G., Scardino, A., Kosmatopoulos, K., Lemonnier, F. A., Campoccia, G., Sabatino, M., Pozzessere, D., Petrioli, R., Lozzi, L., Neri, P., Fanetti, G., Cusi, M. G., Correale, P. (2002). High-Affinity HLA-A(*)02.01 Peptides from Parathyroid Hormone-Related Protein Generate In Vitro and In Vivo Antitumor CTL Response Without Autoimmune Side Effects. J. Immunol. 169: 4840-4849 [Abstract] [Full Text]  
• Ito, Y., Arai, S., van Oers, N. S. C., Aifantis, I., von Boehmer, H., Miyazaki, T. (2002). Positive Selection by the Pre-TCR Yields Mature CD8+ T Cells. J. Immunol. 169: 4913-4919 [Abstract] [Full Text]  
• Cohen, C. J., Hoffmann, N., Farago, M., Hoogenboom, H. R., Eisenbach, L., Reiter, Y. (2002). Direct Detection and Quantitation of a Distinct T-Cell Epitope Derived from Tumor-specific Epithelial Cell-associated Mucin Using Human Recombinant Antibodies Endowed with the Antigen-specific, Major Histocompatibility Complex-restricted Specificity of T Cells. Cancer Res. 62: 5835-5844 [Abstract] [Full Text]  
• Denkberg, G., Klechevsky, E., Reiter, Y. (2002). Modification of a Tumor-Derived Peptide at an HLA-A2 Anchor Residue Can Alter the Conformation of the MHC-Peptide Complex: Probing with TCR-Like Recombinant Antibodies. J. Immunol. 169: 4399-4407 [Abstract] [Full Text]  
• Boissonnas, A., Bonduelle, O., Antzack, A., Lone, Y.-C., Gache, C., Debre, P., Autran, B., Combadiere, B. (2002). In Vivo Priming Of HIV-Specific CTLs Determines Selective Cross-Reactive Immune Responses Against Poorly Immunogenic HIV-Natural Variants. J. Immunol. 169: 3694-3699 [Abstract] [Full Text]  
• Hernandez, J., Garcia-Pons, F., Lone, Y. C., Firat, H., Schmidt, J. D., Langlade-Demoyen, P., Zanetti, M. (2002). Identification of a human telomerase reverse transcriptase peptide of low affinity for HLA A2.1 that induces cytotoxic T lymphocytes and mediates lysis of tumor cells. Proc. Natl. Acad. Sci. USA 99: 12275-12280 [Abstract] [Full Text]  
• Firat, H., Cochet, M., Rohrlich, P.-S., Garcia-Pons, F., Darche, S., Danos, O., Lemonnier, F. A., Langlade-Demoyen, P. (2002). Comparative analysis of the CD8+ T cell repertoires of H-2 class I wild-type/HLA-A2.1 and H-2 class I knockout/HLA-A2.1 transgenic mice. Int Immunol 14: 925-934 [Abstract] [Full Text]  
• Graff-Dubois, S., Faure, O., Gross, D.-A., Alves, P., Scardino, A., Chouaib, S., Lemonnier, F. A., Kosmatopoulos, K. (2002). Generation of CTL Recognizing an HLA-A*0201-Restricted Epitope Shared by MAGE-A1, -A2, -A3, -A4, -A6, -A10, and -A12 Tumor Antigens: Implication in a Broad-Spectrum Tumor Immunotherapy. J. Immunol. 169: 575-580 [Abstract] [Full Text]  
• Lev, A., Denkberg, G., Cohen, C. J., Tzukerman, M., Skorecki, K. L., Chames, P., Hoogenboom, H. R., Reiter, Y. (2002). Isolation and Characterization of Human Recombinant Antibodies Endowed with the Antigen-specific, Major Histocompatibility Complex-restricted Specificity of T Cells Directed toward the Widely Expressed Tumor T-cell Epitopes of the Telomerase Catalytic Subunit. Cancer Res. 62: 3184-3194 [Abstract] [Full Text]  
• Scardino, A., Gross, D.-A., Alves, P., Schultze, J. L., Graff-Dubois, S., Faure, O., Tourdot, S., Chouaib, S., Nadler, L. M., Lemonnier, F. A., Vonderheide, R. H., Cardoso, A. A., Kosmatopoulos, K. (2002). HER-2/neu and hTERT Cryptic Epitopes as Novel Targets for Broad Spectrum Tumor Immunotherapy. J. Immunol. 168: 5900-5906 [Abstract] [Full Text]  
• Passoni, L., Scardino, A., Bertazzoli, C., Gallo, B., Coluccia, A. M. L., Lemonnier, F. A., Kosmatopoulos, K., Gambacorti-Passerini, C. (2002). ALK as a novel lymphoma-associated tumor antigen: identification of 2 HLA-A2.1-restricted CD8+ T-cell epitopes. Blood 99: 2100-2106 [Abstract] [Full Text]  
• Brinster, C., Chen, M., Boucreux, D., Paranhos-Baccala, G., Liljestrom, P., Lemmonier, F., Inchauspe, G. (2002). Hepatitis C virus non-structural protein 3-specific cellular immune responses following single or combined immunization with DNA or recombinant Semliki Forest virus particles. J. Gen. Virol. 83: 369-381 [Abstract] [Full Text]  
• Miconnet, I., Koenig, S., Speiser, D., Krieg, A., Guillaume, P., Cerottini, J.-C., Romero, P. (2002). CpG Are Efficient Adjuvants for Specific CTL Induction Against Tumor Antigen-Derived Peptide. J. Immunol. 168: 1212-1218 [Abstract] [Full Text]  
• Pascolo, S., Schirle, M., Gückel, B., Dumrese, T., Stumm, S., Kayser, S., Moris, A., Wallwiener, D., Rammensee, H.-G., Stevanovic, S. (2001). A MAGE-A1 HLA-A*0201 Epitope Identified by Mass Spectrometry. Cancer Res. 61: 4072-4077 [Abstract] [Full Text]  
• Karadimitris, A., Gadola, S., Altamirano, M., Brown, D., Woolfson, A., Klenerman, P., Chen, J.-L., Koezuka, Y., Roberts, I. A. G., Price, D. A., Dusheiko, G., Milstein, C., Fersht, A., Luzzatto, L., Cerundolo, V. (2001). From the Cover: Human CD1d-glycolipid tetramers generated by in vitro oxidative refolding chromatography. Proc. Natl. Acad. Sci. USA 98: 3294-3298 [Abstract] [Full Text]  
• Loirat, D., Lemonnier, F. A., Michel, M.-L. (2000). Multiepitopic HLA-A*0201-Restricted Immune Response Against Hepatitis B Surface Antigen After DNA-Based Immunization. J. Immunol. 165: 4748-4755 [Abstract] [Full Text]  
• Borenstein, S. H., Graham, J., Zhang, X.-L., Chamberlain, J. W. (2000). CD8+ T Cells Are Necessary for Recognition of Allelic, But Not Locus-Mismatched or Xeno-, HLA Class I Transplantation Antigens. J. Immunol. 165: 2341-2353 [Abstract] [Full Text]  
• Azoulay-Cayla, A., Dethlefs, S., Pérarnau, B., Larsson-Sciard, E.-L., Lemonnier, F. A., Brahic, M., Bureau, J.-F. (2000). H-2Db-/- Mice Are Susceptible to Persistent Infection by Theiler's Virus. J. Virol. 74: 5470-5476 [Abstract] [Full Text]  
• Bullock, T. N. J., Colella, T. A., Engelhard, V. H. (2000). The Density of Peptides Displayed by Dendritic Cells Affects Immune Responses to Human Tyrosinase and gp100 in HLA-A2 Transgenic Mice. J. Immunol. 164: 2354-2361 [Abstract] [Full Text]  
• Su, R.-C., Kung, S. K.-P., Silver, E. T., Lemieux, S., Kane, K. P., Miller, R. G. (1999). Ly-49CB6 NK Inhibitory Receptor Recognizes Peptide-Receptive H-2Kb 1. J. Immunol. 163: 5319-5330 [Abstract] [Full Text]  
• Murali-Krishna, K., Lau, L. L., Sambhara, S., Lemonnier, F., Altman, J., Ahmed, R. (1999). Persistence of Memory CD8 T Cells in MHC Class I-Deficient Mice. Science 286: 1377-1381 [Abstract] [Full Text]  
• Lauvau, G., Kakimi, K., Niedermann, G., Ostankovitch, M., Yotnda, P., Firat, H., Chisari, F. V., van Endert, P. M. (1999). Human Transporters Associated with Antigen Processing (Taps) Select Epitope Precursor Peptides for Processing in the Endoplasmic Reticulum and Presentation to T Cells. JEM 190: 1227-1240 [Abstract] [Full Text]  
• Chung, D. H., Dorfman, J., Plaksin, D., Natarajan, K., Belyakov, I. M., Hunziker, R., Berzofsky, J. A., Yokoyama, W. M., Mage, M. G., Margulies, D. H. (1999). NK and CTL Recognition of a Single Chain H-2Dd Molecule: Distinct Sites of H-2Dd Interact with NK and TCR. J. Immunol. 163: 3699-3708 [Abstract] [Full Text]  
• Mateo, L., Gardner, J., Chen, Q., Schmidt, C., Down, M., Elliott, S. L., Pye, S. J., Firat, H., Lemonnier, F. A., Cebon, J., Suhrbier, A. (1999). An HLA-A2 Polyepitope Vaccine for Melanoma Immunotherapy. J. Immunol. 163: 4058-4063 [Abstract] [Full Text]  
• Ureta-Vidal, A., Firat, H., Perarnau, B., Lemonnier, F. A. (1999). Phenotypical and Functional Characterization of the CD8+ T Cell Repertoire of HLA-A2.1 Transgenic, H-2Kb{degrees}Db{degrees} Double Knockout Mice. J. Immunol. 163: 2555-2560 [Abstract] [Full Text]  
• Woodberry, T., Gardner, J., Mateo, L., Eisen, D., Medveczky, J., Ramshaw, I. A., Thomson, S. A., Ffrench, R. A., Elliott, S. L., Firat, H., Lemonnier, F. A., Suhrbier, A. (1999). Immunogenicity of a Human Immunodeficiency Virus (HIV) Polytope Vaccine Containing Multiple HLA A2 HIV CD8+ Cytotoxic T-Cell Epitopes. J. Virol. 73: 5320-5325 [Abstract] [Full Text]  
• Men, Y., Miconnet, I., Valmori, D., Rimoldi, D., Cerottini, J.-C., Romero, P. (1999). Assessment of Immunogenicity of Human Melan-A Peptide Analogues in HLA-A*0201/Kb Transgenic Mice. J. Immunol. 162: 3566-3573 [Abstract] [Full Text]  
• Vugmeyster, Y., Glas, R., Perarnau, B., Lemonnier, F. A., Eisen, H., Ploegh, H. (1998). Major histocompatibility complex (MHC) class I KbDb -/- deficient mice possess functional CD8+ T cells and natural killer cells. Proc. Natl. Acad. Sci. USA 95: 12492-12497 [Abstract] [Full Text]  
• Miyazaki, T., Lemonnier, F. A. (1998). Modulation of Thymic Selection by Expression of an Immediate-early Gene, Early Growth Response 1 (Egr-1). JEM 188: 715-723 [Abstract] [Full Text]  
• Tanchot, C., Lemonnier, F. A., Pérarnau, B., Freitas, A. A., Rocha, B. (1997). Differential Requirements for Survival and Proliferation of CD8 Naïve or Memory T Cells. Science 276: 2057-2062 [Abstract] [Full Text]  

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