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A TCR β-Chain Motif Biases toward Recognition of Human CD1 Proteins

Peter Reinink, Adam Shahine, Stephanie Gras, Tan-Yun Cheng, Rachel Farquhar, Kattya Lopez, Sara A. Suliman, Josephine F. Reijneveld, Jérôme Le Nours, Li Lynn Tan, Segundo R. León, Judith Jimenez, Roger Calderon, Leonid Lecca, Megan B. Murray, Jamie Rossjohn, D. Branch Moody and Ildiko Van Rhijn
J Immunol November 6, 2019, ji1900872; DOI: https://doi.org/10.4049/jimmunol.1900872
Peter Reinink
*Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, the Netherlands;
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
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Adam Shahine
‡Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia;
§Australian Research Council Centre of Excellence in Advanced Molecular Imaging, Monash University, Clayton, Victoria 3800, Australia;
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Stephanie Gras
‡Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia;
§Australian Research Council Centre of Excellence in Advanced Molecular Imaging, Monash University, Clayton, Victoria 3800, Australia;
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Tan-Yun Cheng
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
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Rachel Farquhar
‡Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia;
§Australian Research Council Centre of Excellence in Advanced Molecular Imaging, Monash University, Clayton, Victoria 3800, Australia;
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Kattya Lopez
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
¶Socios en Salud Sucursal Peru, 15001 Lima, Peru;
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Sara A. Suliman
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
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Josephine F. Reijneveld
*Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, the Netherlands;
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
‖Stratingh Institute for Chemistry, University of Groningen, 9747AG Groningen, the Netherlands;
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Jérôme Le Nours
‡Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia;
§Australian Research Council Centre of Excellence in Advanced Molecular Imaging, Monash University, Clayton, Victoria 3800, Australia;
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Li Lynn Tan
‡Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia;
§Australian Research Council Centre of Excellence in Advanced Molecular Imaging, Monash University, Clayton, Victoria 3800, Australia;
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Segundo R. León
¶Socios en Salud Sucursal Peru, 15001 Lima, Peru;
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Judith Jimenez
¶Socios en Salud Sucursal Peru, 15001 Lima, Peru;
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Roger Calderon
¶Socios en Salud Sucursal Peru, 15001 Lima, Peru;
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Leonid Lecca
¶Socios en Salud Sucursal Peru, 15001 Lima, Peru;
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Megan B. Murray
#Department of Global Health and Social Medicine, Harvard Medical School, Boston, MA 02115;
**Division of Global Health Equity, Brigham and Women’s Hospital, Boston, MA 02115;
††Department of Epidemiology, Harvard School of Public Health, Boston, MA 02115; and
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Jamie Rossjohn
‡Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia;
§Australian Research Council Centre of Excellence in Advanced Molecular Imaging, Monash University, Clayton, Victoria 3800, Australia;
‡‡Institute of Infection and Immunity, School of Medicine, Cardiff University, CF14 4XN Cardiff, United Kingdom
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D. Branch Moody
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
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Ildiko Van Rhijn
*Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, the Netherlands;
†Division of Rheumatology, Inflammation, and Immunity, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115;
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Key Points

  • TCR β variable gene 4-1 (TRBV4-1) is overrepresented among CD1b-specific T cells.

  • The association between TRBV4-1 usage and CD1b is independent of lipid Ag.

  • CD1b residue E80 is essential for binding of TRBV4-1–utilizing TCRs.

Abstract

High-throughput TCR sequencing allows interrogation of the human TCR repertoire, potentially connecting TCR sequences to antigenic targets. Unlike the highly polymorphic MHC proteins, monomorphic Ag-presenting molecules such as MR1, CD1d, and CD1b present Ags to T cells with species-wide TCR motifs. CD1b tetramer studies and a survey of the 27 published CD1b-restricted TCRs demonstrated a TCR motif in humans defined by the TCR β-chain variable gene 4-1 (TRBV4-1) region. Unexpectedly, TRBV4-1 was involved in recognition of CD1b regardless of the chemical class of the carried lipid. Crystal structures of two CD1b-specific TRBV4-1+ TCRs show that germline-encoded residues in CDR1 and CDR3 regions of TRBV4-1–encoded sequences interact with each other and consolidate the surface of the TCR. Mutational studies identified a key positively charged residue in TRBV4-1 and a key negatively charged residue in CD1b that is shared with CD1c, which is also recognized by TRBV4-1 TCRs. These data show that one TCR V region can mediate a mechanism of recognition of two related monomorphic Ag-presenting molecules that does not rely on a defined lipid Ag.

Footnotes

  • This work was supported by the Australian Research Council (ARC) and National Health and Medical Research Council (NHMRC), the National Institutes of Health (Grants AI049313, AR048632, and AI111224), and the Netherlands Organization for Scientific Research. S.G. is an NHMRC Senior Research Fellow. J.R. is supported by an ARC Laureate Fellowship.

  • The online version of this article contains supplemental material.

  • Received July 29, 2019.
  • Accepted October 9, 2019.
  • Copyright © 2019 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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A TCR β-Chain Motif Biases toward Recognition of Human CD1 Proteins
Peter Reinink, Adam Shahine, Stephanie Gras, Tan-Yun Cheng, Rachel Farquhar, Kattya Lopez, Sara A. Suliman, Josephine F. Reijneveld, Jérôme Le Nours, Li Lynn Tan, Segundo R. León, Judith Jimenez, Roger Calderon, Leonid Lecca, Megan B. Murray, Jamie Rossjohn, D. Branch Moody, Ildiko Van Rhijn
The Journal of Immunology November 6, 2019, ji1900872; DOI: 10.4049/jimmunol.1900872

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A TCR β-Chain Motif Biases toward Recognition of Human CD1 Proteins
Peter Reinink, Adam Shahine, Stephanie Gras, Tan-Yun Cheng, Rachel Farquhar, Kattya Lopez, Sara A. Suliman, Josephine F. Reijneveld, Jérôme Le Nours, Li Lynn Tan, Segundo R. León, Judith Jimenez, Roger Calderon, Leonid Lecca, Megan B. Murray, Jamie Rossjohn, D. Branch Moody, Ildiko Van Rhijn
The Journal of Immunology November 6, 2019, ji1900872; DOI: 10.4049/jimmunol.1900872
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Print ISSN 0022-1767        Online ISSN 1550-6606