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Science 29 August 1997:
Vol. 277. no. 5330, pp. 1306 - 1309
DOI: 10.1126/science.277.5330.1306
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Reports

A Critical Role for Tapasin in the Assembly and Function of Multimeric MHC Class I-TAP Complexes

Bodo Ortmann, *dagger James Copeman, *ddagger Paul J. Lehner, * Bhanu Sadasivan, § Jethro A. Herberg, Andeas G. Grandea, Stanley R. Riddell, Robert Tampé, Thomas Spies, John Trowsdale, | Peter Cresswell

Newly assembled major histocompatibility complex (MHC) class I molecules, together with the endoplasmic reticulum chaperone calreticulin, interact with the transporter associated with antigen processing (TAP) through a molecule called tapasin. The molecular cloning of tapasin revealed it to be a transmembrane glycoprotein encoded by an MHC-linked gene. It is a member of the immunoglobulin superfamily with a probable cytoplasmic endoplasmic reticulum retention signal. Up to four MHC class I-tapasin complexes were found to bind to each TAP molecule. Expression of tapasin in a negative mutant human cell line (220) restored class I-TAP association and normal class I cell surface expression. Tapasin expression also corrected the defective recognition of virus-infected 220 cells by class I-restricted cytotoxic T cells, establishing a critical functional role for tapasin in MHC class I-restricted antigen processing.

B. Ortmann, J. Copeman, P. J. Lehner, B. Sadasivan, P. Cresswell, Howard Hughes Medical Institute, Section of Immunobiology, Yale University School of Medicine, 310 Cedar Street, New Haven, CT 06510, USA.
J. A. Herberg and J. Trowsdale, Human Immunogenetics Laboratory, Imperial Cancer Research Fund, 44 Lincoln's Inn Fields, London WC2A 3PX, UK.
A. G. Grandea, S. R. Riddell, T. Spies, Clinical Research Division, Fred Hutchinson Cancer Research Center, 1124 Columbia Street, Seattle, WA 98104, USA.
R. Tampé, Max-Planck-Institute for Biochemistry, D-82152 Martinsried, Germany.
*   These authors contributed equally to this work.

dagger    Present address: Institute of Genetics, University of Cologne, Zuelpicher Strasse 47, D-50674 Köeln, Germany.

ddagger    Present address: Samuel Lunenfeld Research Institute, Mt. Sinai Hospital, 600 University Avenue, Toronto, Ontario, Canada M5G1X5.

§   Present address: Department of Immunology, Brigham and Women's Hospital, 250 Longwood Avenue, Boston, MA 02115, USA.

|   Present address: Division of Immunology, Department of Pathology, Tennis Court Road, Cambridge CB2 1QP, UK.

   To whom correspondence should be addressed.

Volume 277, Number 5330, Issue of 29 August 1997, pp. 1306-1309
©1997 by The American Association for the Advancement of Science.

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J. Biol. Chem. 275, 1581-1586
   Abstract »    Full Text »    PDF »
Distinct Functions of Tapasin Revealed by Polymorphism in MHC Class I Peptide Loading.
C. A. Peh, N. Laham, S. R. Burrows, Y. Zhu, and J. McCluskey (2000)
J. Immunol. 164, 292-299
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Membrane Topology and Dimerization of the Two Subunits of the Transporter Associated with Antigen Processing Reveal a Three-Domain Structure.
J. C. Vos, P. Spee, F. Momburg, and J. Neefjes (1999)
J. Immunol. 163, 6679-6685
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Setting the Standards: Quality Control in the Secretory Pathway.
L. Ellgaard, M. Molinari, and A. Helenius (1999)
Science 286, 1882-1888
   Abstract »    Full Text »
Definition and transfer of a serological epitope specific for peptide-empty forms of MHC class I.
Y. Y. L. Yu, N. B. Myers, C. M. Hilbert, M. R. Harris, G. K. Balendiran, and T. H. Hansen (1999)
Int. Immunol. 11, 1897-1906
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Human Transporters Associated with Antigen Processing (Taps) Select Epitope Precursor Peptides for Processing in the Endoplasmic Reticulum and Presentation to T Cells.
G. Lauvau, K. Kakimi, G. Niedermann, M. Ostankovitch, P. Yotnda, H. Firat, F. V. Chisari, and P. M. van Endert (1999)
J. Exp. Med. 190, 1227-1240
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Tapasin Enhances Assembly of Transporters Associated with Antigen Processing-dependent and -independent Peptides with HLA-A2 and HLA-B27 Expressed in Insect Cells.
G. Lauvau, B. Gubler, H. Cohen, S. Daniel, S. Caillat-Zucman, and P. M. van Endert (1999)
J. Biol. Chem. 274, 31349-31358
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An Extensive Region of an MHC Class I {alpha}2 Domain Loop Influences Interaction with the Assembly Complex.
Y. Y. L. Yu, H. R. Turnquist, N. B. Myers, G. K. Balendiran, T. H. Hansen, and J. C. Solheim (1999)
J. Immunol. 163, 4427-4433
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The Majority of H2-M3 Is Retained Intracellularly in a Peptide-Receptive State and Traffics to the Cell Surface in the Presence of N-Formylated Peptides.
N. M. Chiu, T. Chun, M. Fay, M. Mandal, and C.-R. Wang (1999)
J. Exp. Med. 190, 423-434
   Abstract »    Full Text »    PDF »
Calreticulin Is Expressed on the Cell Surface of Activated Human Peripheral Blood T Lymphocytes in Association with Major Histocompatibility Complex Class I Molecules.
F. A. Arosa, O. de Jesus, G. Porto, A. M. Carmo, and M. de Sousa (1999)
J. Biol. Chem. 274, 16917-16922
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Calreticulin Displays In Vivo Peptide-Binding Activity and Can Elicit CTL Responses Against Bound Peptides.
S. Nair, P. A. Wearsch, D. A. Mitchell, J. J. Wassenberg, E. Gilboa, and C. V. Nicchitta (1999)
J. Immunol. 162, 6426-6432
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Cutting Edge: Adenovirus E19 Has Two Mechanisms for Affecting Class I MHC Expression1.
E. M. Bennett, J. R. Bennink, J. W. Yewdell, and F. M. Brodsky (1999)
J. Immunol. 162, 5049-5052
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TAP Association Influences the Conformation of Nascent MHC Class I Molecules.
B. A. L. Owen and L. R. Pease (1999)
J. Immunol. 162, 4677-4684
   Abstract »    Full Text »    PDF »
Specific Proteolytic Cleavages Limit the Diversity of the Pool of Peptides Available to MHC Class I Molecules in Living Cells.
T. Serwold and N. Shastri (1999)
J. Immunol. 162, 4712-4719
   Abstract »    Full Text »    PDF »
Peptide-bound Major Histocompatibility Complex Class I Molecules Associate with Tapasin before Dissociation from Transporter Associated with Antigen Processing.
S. Li, K. M. Paulsson, H.-O. Sjogren, and P. Wang (1999)
J. Biol. Chem. 274, 8649-8654
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Interaction of Murine MHC Class I Molecules with Tapasin and TAP Enhances Peptide Loading and Involves the Heavy Chain {alpha}3 Domain.
W.-K. Suh, M. A. Derby, M. F. Cohen-Doyle, G. J. Schoenhals, K. Fruh, J. A. Berzofsky, and D. B. Williams (1999)
J. Immunol. 162, 1530-1540
   Abstract »    Full Text »    PDF »
In vitro reconstitution of calreticulin-substrate interactions.
J. Peterson and A Helenius (1999)
J. Cell Sci. 112, 2775-2784
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MHC Class I Molecules Compete in the Endoplasmic Reticulum for Access to Transporter Associated with Antigen Processing.
M. R. Knittler, K. Gulow, A. Seelig, and J. C. Howard (1998)
J. Immunol. 161, 5967-5977
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Assembly of MHC Class I Molecules with Biosynthesized Endoplasmic Reticulum-Targeted Peptides Is Inefficient in Insect Cells and Can Be Enhanced by Protease Inhibitors.
Y. Deng, J. Gibbs, I. Bacik, A. Porgador, J. Copeman, P. Lehner, B. Ortmann, P. Cresswell, J. R. Bennink, and J. W. Yewdell (1998)
J. Immunol. 161, 1677-1685
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Herpes Simplex Virus Inhibitor ICP47 Destabilizes the Transporter Associated with Antigen Processing (TAP) Heterodimer.
V. G. Lacaille and M. J. Androlewicz (1998)
J. Biol. Chem. 273, 17386-17390
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Calreticulin and Calnexin Interact with Different Protein and Glycan Determinants During the Assembly of MHC Class I.
M. R. Harris, Y. Y. L. Yu, C. S. Kindle, T. H. Hansen, and J. C. Solheim (1998)
J. Immunol. 160, 5404-5409
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Maturation of Qa-1b Class I Molecules Requires {beta}2-Microglobulin But Is TAP Independent.
P. J. Robinson, P. J. Travers, A. Stackpoole, L. Flaherty, and H. Djaballah (1998)
J. Immunol. 160, 3217-3224
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Physical and Functional Association of the Major Histocompatibility Complex Class I Heavy Chain {alpha}3 Domain with the Transporter Associated with Antigen Processing.
K. Kulig, D. Nandi, I. Bacik, J. J. Monaco, and S. Vukmanovic (1998)
J. Exp. Med. 187, 865-874
   Abstract »    Full Text »    PDF »
Evolving Views of the Major Histocompatibility Complex.
J. R. Gruen and S. M. Weissman (1997)
Blood 90, 4252-4265
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