High-throughput identification of antigen-specific TCRs by TCR gene capture

The lack of robust and high-throughput technologies to analyze the human TCR repertoire has been a bottleneck in the analysis of human T cell responses. Linnemann and colleagues have addressed this issue by using a TCR gene capture technology that, because of its quantitative nature, allows the rapi...

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Vydané v:	Nature medicine Ročník 19; číslo 11; s. 1534 - 1541
Hlavní autori:	Linnemann, Carsten, Heemskerk, Bianca, Kvistborg, Pia, Kluin, Roelof J C, Bolotin, Dmitriy A, Chen, Xiaojing, Bresser, Kaspar, Nieuwland, Marja, Schotte, Remko, Michels, Samira, Gomez-Eerland, Raquel, Jahn, Lorenz, Hombrink, Pleun, Legrand, Nicolas, Shu, Chengyi Jenny, Mamedov, Ilgar Z, Velds, Arno, Blank, Christian U, Haanen, John B A G, Turchaninova, Maria A, Kerkhoven, Ron M, Spits, Hergen, Hadrup, Sine Reker, Heemskerk, Mirjam H M, Blankenstein, Thomas, Chudakov, Dmitriy M, Bendle, Gavin M, Schumacher, Ton N M
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	New York Nature Publishing Group US 01.11.2013 Nature Publishing Group
Predmet:	631/250/251 631/61/201 631/61/24 Animals Antibodies Antigen receptors, T cell Antigens Antigens, Neoplasm - metabolism Biomedicine Cancer Cancer Research Care and treatment Deoxyribonucleic acid DNA DNA sequencing Gene Library Gene therapy Genes, T-Cell Receptor Genetic Therapy Genomics High-Throughput Nucleotide Sequencing - methods Humans Identification and classification Infectious Diseases Metabolic Diseases Methods Mice Molecular Medicine Neoplasms - genetics Neoplasms - immunology Neoplasms - therapy Neurosciences Nucleotide sequencing Receptors Receptors, Antigen, T-Cell - genetics Receptors, Antigen, T-Cell - metabolism T cell receptors T cells T-Lymphocytes - immunology technical-report Tumors Viral antibodies United States
ISSN:	1078-8956, 1546-170X, 1546-170X
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Abstract	The lack of robust and high-throughput technologies to analyze the human TCR repertoire has been a bottleneck in the analysis of human T cell responses. Linnemann and colleagues have addressed this issue by using a TCR gene capture technology that, because of its quantitative nature, allows the rapid identification of TCRab pairs from bulk populations of cells without the need for single-cell cloning. Such an approach should be useful in obtaining defined antigen-reactive TCRs for therapeutic purposes. The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although efficient methods exist to identify antibodies for the treatment of these diseases, comparable strategies to identify TCRs have been lacking. We have developed a high-throughput DNA-based strategy to identify TCR sequences by the capture and sequencing of genomic DNA fragments encoding the TCR genes. We establish the value of this approach by assembling a large library of cancer germline tumor antigen–reactive TCRs. Furthermore, by exploiting the quantitative nature of TCR gene capture, we show the feasibility of identifying antigen-specific TCRs in oligoclonal T cell populations from either human material or TCR-humanized mice. Finally, we demonstrate the ability to identify tumor-reactive TCRs within intratumoral T cell subsets without knowledge of antigen specificities, which may be the first step toward the development of autologous TCR gene therapy to target patient-specific neoantigens in human cancer.
AbstractList	The lack of robust and high-throughput technologies to analyze the human TCR repertoire has been a bottleneck in the analysis of human T cell responses. Linnemann and colleagues have addressed this issue by using a TCR gene capture technology that, because of its quantitative nature, allows the rapid identification of TCRab pairs from bulk populations of cells without the need for single-cell cloning. Such an approach should be useful in obtaining defined antigen-reactive TCRs for therapeutic purposes. The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although efficient methods exist to identify antibodies for the treatment of these diseases, comparable strategies to identify TCRs have been lacking. We have developed a high-throughput DNA-based strategy to identify TCR sequences by the capture and sequencing of genomic DNA fragments encoding the TCR genes. We establish the value of this approach by assembling a large library of cancer germline tumor antigen–reactive TCRs. Furthermore, by exploiting the quantitative nature of TCR gene capture, we show the feasibility of identifying antigen-specific TCRs in oligoclonal T cell populations from either human material or TCR-humanized mice. Finally, we demonstrate the ability to identify tumor-reactive TCRs within intratumoral T cell subsets without knowledge of antigen specificities, which may be the first step toward the development of autologous TCR gene therapy to target patient-specific neoantigens in human cancer. The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although efficient methods exist to identify antibodies for the treatment of these diseases, comparable strategies to identify TCRs have been lacking. We have developed a high-throughput DNA-based strategy to identify TCR sequences by the capture and sequencing of genomic DNA fragments encoding the TCR genes. We establish the value of this approach by assembling a large library of cancer germline tumor antigen-reactive TCRs. Furthermore, by exploiting the quantitative nature of TCR gene capture, we show the feasibility of identifying antigen-specific TCRs in oligoclonal T cell populations from either human material or TCR-humanized mice. Finally, we demonstrate the ability to identify tumor-reactive TCRs within intratumoral T cell subsets without knowledge of antigen specificities, which may be the first step toward the development of autologous TCR gene therapy to target patient-specific neoantigens in human cancer. The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although efficient methods exist to identify antibodies for the treatment of these diseases, comparable strategies to identify TCRs have been lacking. We have developed a high-throughput DNA-based strategy to identify TCR sequences by the capture and sequencing of genomic DNA fragments encoding the TCR genes. We establish the value of this approach by assembling a large library of cancer germline tumor antigen-reactive TCRs. Furthermore, by exploiting the quantitative nature of TCR gene capture, we show the feasibility of identifying antigen-specific TCRs in oligoclonal T cell populations from either human material or TCR-humanized mice. Finally, we demonstrate the ability to identify tumor-reactive TCRs within intratumoral T cell subsets without knowledge of antigen specificities, which may be the first step toward the development of autologous TCR gene therapy to target patient-specific neoantigens in human cancer. [PUBLICATION ABSTRACT] The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although efficient methods exist to identify antibodies for the treatment of these diseases, comparable strategies to identify TCRs have been lacking. We have developed a high-throughput DNA-based strategy to identify TCR sequences by the capture and sequencing of genomic DNA fragments encoding the TCR genes. We establish the value of this approach by assembling a large library of cancer germline tumor antigen-reactive TCRs. Furthermore, by exploiting the quantitative nature of TCR gene capture, we show the feasibility of identifying antigen-specific TCRs in oligoclonal T cell populations from either human material or TCR-humanized mice. Finally, we demonstrate the ability to identify tumor-reactive TCRs within intratumoral T cell subsets without knowledge of antigen specificities, which may be the first step toward the development of autologous TCR gene therapy to target patient-specific neoantigens in human cancer.The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although efficient methods exist to identify antibodies for the treatment of these diseases, comparable strategies to identify TCRs have been lacking. We have developed a high-throughput DNA-based strategy to identify TCR sequences by the capture and sequencing of genomic DNA fragments encoding the TCR genes. We establish the value of this approach by assembling a large library of cancer germline tumor antigen-reactive TCRs. Furthermore, by exploiting the quantitative nature of TCR gene capture, we show the feasibility of identifying antigen-specific TCRs in oligoclonal T cell populations from either human material or TCR-humanized mice. Finally, we demonstrate the ability to identify tumor-reactive TCRs within intratumoral T cell subsets without knowledge of antigen specificities, which may be the first step toward the development of autologous TCR gene therapy to target patient-specific neoantigens in human cancer.
Audience	Academic
Author	Haanen, John B A G Heemskerk, Mirjam H M Nieuwland, Marja Hadrup, Sine Reker Linnemann, Carsten Legrand, Nicolas Kerkhoven, Ron M Heemskerk, Bianca Jahn, Lorenz Hombrink, Pleun Velds, Arno Bolotin, Dmitriy A Spits, Hergen Schumacher, Ton N M Chen, Xiaojing Turchaninova, Maria A Mamedov, Ilgar Z Gomez-Eerland, Raquel Chudakov, Dmitriy M Kvistborg, Pia Kluin, Roelof J C Michels, Samira Blankenstein, Thomas Schotte, Remko Shu, Chengyi Jenny Bendle, Gavin M Bresser, Kaspar Blank, Christian U
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Liver and Intestinal Research, Academic Medical Center of the University of Amsterdam – sequence: 23 givenname: Sine Reker surname: Hadrup fullname: Hadrup, Sine Reker organization: Center for Cancer Immune Therapy, Herlev Hospital – sequence: 24 givenname: Mirjam H M surname: Heemskerk fullname: Heemskerk, Mirjam H M organization: Department of Hematology, Laboratory of Experimental Hematology, Leiden University Medical Center – sequence: 25 givenname: Thomas surname: Blankenstein fullname: Blankenstein, Thomas organization: Max Delbrück Center for Molecular Medicine, Institute of Immunology, Charité Campus Benjamin Franklin – sequence: 26 givenname: Dmitriy M orcidid: 0000-0003-0430-790X surname: Chudakov fullname: Chudakov, Dmitriy M organization: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences – sequence: 27 givenname: Gavin M surname: Bendle fullname: Bendle, Gavin M email: g.bendle@bham.ac.uk organization: Division of Immunology, The 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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24121928$$D View this record in MEDLINE/PubMed
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Copyright	Springer Nature America, Inc. 2013 COPYRIGHT 2013 Nature Publishing Group Copyright Nature Publishing Group Nov 2013
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Snippet	The lack of robust and high-throughput technologies to analyze the human TCR repertoire has been a bottleneck in the analysis of human T cell responses.... The transfer of T cell receptor (TCR) genes into patient T cells is a promising approach for the treatment of both viral infections and cancer. Although...
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SubjectTerms	631/250/251 631/61/201 631/61/24 Animals Antibodies Antigen receptors, T cell Antigens Antigens, Neoplasm - metabolism Biomedicine Cancer Cancer Research Care and treatment Deoxyribonucleic acid DNA DNA sequencing Gene Library Gene therapy Genes, T-Cell Receptor Genetic Therapy Genomics High-Throughput Nucleotide Sequencing - methods Humans Identification and classification Infectious Diseases Metabolic Diseases Methods Mice Molecular Medicine Neoplasms - genetics Neoplasms - immunology Neoplasms - therapy Neurosciences Nucleotide sequencing Receptors Receptors, Antigen, T-Cell - genetics Receptors, Antigen, T-Cell - metabolism T cell receptors T cells T-Lymphocytes - immunology technical-report Tumors Viral antibodies
Title	High-throughput identification of antigen-specific TCRs by TCR gene capture
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