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An Economical, Quantitative, and Robust Protocol for High-Throughput T Cell Receptor Sequencing from Tumor or Blood

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Cancer Immunosurveillance

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1884))

Abstract

The T cell receptor repertoire provides a window to the cellular adaptive immune response within a tumor, and has the potential to identify specific and personalized biomarkers for tracking host responses during cancer therapy, including immunotherapy. We describe a protocol for amplifying, sequencing, and analyzing T cell receptors which is economical, robust, sensitive, and versatile. The key experimental step is the ligation of a single-stranded oligonucleotide to the 3′ end of the T cell receptor cDNA, which allows easy amplification of all possible rearrangements using only a single set of primers per locus, while simultaneously introducing a unique molecular identifier to label each starting cDNA molecule. After sequencing, this molecular identifier can be used to correct both sequence errors and the effects of differential PCR amplification efficiency, thus producing a more accurate measure of the true T cell receptor frequency within the sample. This method has been applied to the analysis of unfractionated human tumor lysates, subpopulations of tumor-infiltrating lymphocytes, and peripheral blood samples from patients with a variety of solid tumors.

TRAcking Cancer Evolution through therapy (Rx). Full list of members in Appendix.

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Acknowledgments

This research was funded by grants from CancerResearchUK, the UK MRC, the Rosetrees Trust, the Stoneygate Foundation, a grant to BC from Unilever PLC, and supported by the National Institute for Health Research UCL Hospitals Biomedical Research. JH was supported by an MRC studentship. K.J. is funded by the Sam Keen Foundation and UCL/Royal Marsden Hospital NIHR Biomedical Research Centres. We are grateful to the TRACERx consortium, funded by Cancer Research UK (http://www.cruklungcentre.org/Research/TRACERx) for giving us access to the tumor samples which the amplified TCR libraries illustrated in Figs. 5 and 6 were prepared.

Author information

Author notes

  1. Imran Uddin and Kroopa Joshi have contributed equally to this work.

Authors and Affiliations

  1. Division of Infection and Immunity, UCL, London, UK

    Imran Uddin, Theres Oakes, James M. Heather & Benny Chain

  2. Cancer Immunology Unit, UCL Cancer Institute, UCL, London, UK

    Kroopa Joshi

  3. Cancer Research UK Lung Cancer Centre of Excellence, UCL Cancer Institute, UCL, London, UK

    Charles Swanton

  4. Translational Cancer Therapeutics Laboratory, The Francis Crick Institute, London, UK

    Charles Swanton

Authors
  1. Imran Uddin
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  2. Kroopa Joshi
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  3. Theres Oakes
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  4. James M. Heather
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  5. Charles Swanton
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  6. Benny Chain
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Consortia

on behalf of the TRACERx consortium

Corresponding author

Correspondence to Benny Chain .

Editor information

Editors and Affiliations

  1. Departamento de Biología Funcional, Inmunología, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Oviedo, Spain

    Alejandro López-Soto

  2. Departamento de Bioquímica y Biología Molecular, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Oviedo, Asturias, Spain

    Alicia R. Folgueras

Appendix: The TRACERx Consortium

Appendix: The TRACERx Consortium

Name

Site/Institution

Jason Lester

Velindre Cancer Centre, Cardiff, Wales

Fiona Morgan

Cardiff & Vale University Health Board, Cardiff, Wales

Malgorzata Kornaszewska

Cardiff & Vale University Health Board, Cardiff, Wales

Richard Attanoos

Cardiff & Vale University Health Board, Cardiff, Wales

Haydn Adams

Cardiff & Vale University Health Board, Cardiff, Wales

Helen Davies

Cardiff & Vale University Health Board, Cardiff, Wales

Dean Fennell

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK & Leicester University Hospitals, Leicester, UK

John Le Quesne

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK

Apostolos Nakas

Leicester University Hospitals, Leicester, UK

Sridhar Rathinam

Leicester University Hospitals, Leicester, UK

William Monteiro

National Institute for Health Research Leicester Respiratory Biomedical Research Unit, Leicester, UK

Hilary Marshall

National Institute for Health Research Leicester Respiratory Biomedical Research Unit, Leicester, UK

Louise Nelson

Leicester University Hospitals, Leicester, UK

Kim Ryanna

Leicester University Hospitals, Leicester, UK

Alan Dawson

Leicester University Hospitals, Leicester, UK

Mohamad Tuffail

Leicester University Hospitals, Leicester, UK

Amrita Bajaj

Leicester University Hospitals, Leicester, UK

Jan Brozik

Leicester University Hospitals, Leicester, UK

Harriet Walter

Leicester University Hospitals, Leicester, UK

Jacqui Shaw

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK

Joan Riley

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK

Lindsay Primrose

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK

Luke Martinson

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK

Nicolas Carey

Cancer Studies and Molecular Medicine, University of Leicester, Leicester, UK

Girija Anand

Barnet Hospital, Barnet, UK

Sajid Khan

Barnet Hospital, Barnet, UK

Gillian Price

Aberdeen Royal Infirmary, Aberdeen, UK

Marianne Nicolson

Aberdeen Royal Infirmary, Aberdeen, UK

Keith Kerr

Aberdeen Royal Infirmary, Aberdeen, UK

Shirley Palmer

Aberdeen Royal Infirmary, Aberdeen, UK

Hardy Remmen

Aberdeen Royal Infirmary, Aberdeen, UK

Joy Miller

Aberdeen Royal Infirmary, Aberdeen, UK

Keith Buchan

Aberdeen Royal Infirmary, Aberdeen, UK

Mahendran Chetty

Aberdeen Royal Infirmary, Aberdeen, UK

Lesley Gomersall

Aberdeen Royal Infirmary, Aberdeen, UK

Sara Lock

The Whittington Hospital NHS Trust, London, UK

Kayleigh Gilbert

The Whittington Hospital NHS Trust, London, UK

Babu Naidu

Heart of England NHS Foundation Trust, Birmingham, UK

Gerald Langman

Heart of England NHS Foundation Trust, Birmingham, UK

Simon Trotter

Heart of England NHS Foundation Trust, Birmingham, UK

Hollie Bancroft

Heart of England NHS Foundation Trust, Birmingham, UK

Amy Kerr

Heart of England NHS Foundation Trust, Birmingham, UK

Salma Kadiri

Heart of England NHS Foundation Trust, Birmingham, UK

Joanne Webb

Heart of England NHS Foundation Trust, Birmingham, UK

Gary Middleton

Heart of England NHS Foundation Trust, Birmingham, UK

Madava Djearaman

Heart of England NHS Foundation Trust, Birmingham, UK

Akshay Patel

Heart of England NHS Foundation Trust, Birmingham, UK

Yvonne Summers

University Hospital of South Manchester, Manchester, UK

Raffaele Califano

University Hospital of South Manchester, Manchester, UK

Paul Taylor

University Hospital of South Manchester, Manchester, UK

Rajesh Shah

University Hospital of South Manchester, Manchester, UK

Piotr Krysiak

University Hospital of South Manchester, Manchester, UK

Kendadai Rammohan

University Hospital of South Manchester, Manchester, UK

Eustace Fontaine

University Hospital of South Manchester, Manchester, UK

Richard Booton

University Hospital of South Manchester, Manchester, UK

Matthew Evison

University Hospital of South Manchester, Manchester, UK

Phil Crosbie

University Hospital of South Manchester, Manchester, UK

Stuart Moss

University Hospital of South Manchester, Manchester, UK

Juliette Novasio

University Hospital of South Manchester, Manchester, UK

Leena Joseph

University Hospital of South Manchester, Manchester, UK

Paul Bishop

University Hospital of South Manchester, Manchester, UK

Anshuman Chaturvedi

University Hospital of South Manchester, Manchester, UK

Anne Marie Quinn

University Hospital of South Manchester, Manchester, UK

Helen Doran

University Hospital of South Manchester, Manchester, UK

Felice Granato

University Hospital of South Manchester, Manchester, UK

Angela leek

Manchester Cancer Research Centre Biobank, Manchester, UK

Phil Harrison

Manchester Cancer Research Centre Biobank, Manchester, UK

Katrina Moore

Manchester Cancer Research Centre Biobank, Manchester, UK

Rachael Waddington

Manchester Cancer Research Centre Biobank, Manchester, UK

Fiona Blackhall

Christie NHS Foundation Trust, Manchester, UK

Jane Rogan

Manchester Cancer Research Centre Biobank, Manchester, UK

Elaine Smith

University Hospital of South Manchester, Manchester, UK

Katie Baker

Christie NHS Foundation Trust, Manchester, UK

Mathew Carter

Christie NHS Foundation Trust, Manchester, UK

Lynsey Priest

Christie NHS Foundation Trust, Manchester, UK

Matthew G Krebs

Christie NHS Foundation Trust, Manchester, UK

Colin Lindsay

Christie NHS Foundation Trust, Manchester, UK

Fabio Gomes

Christie NHS Foundation Trust, Manchester, UK

Caroline Dive

Manchester labs

Ged Brady

Manchester labs

Dominic Rothwell

Manchester labs

Sakshi Gulati

Manchester labs

Francesca Chemie

Manchester labs

Jonathan Tugwood

Manchester labs

Jackie Pierce

Manchester labs

David Lawrence

University College London Hospitals, London, UK

Martin Hayward

University College London Hospitals, London, UK

Nikolaos Panagiotopoulos

University College London Hospitals, London, UK

Robert George

University College London Hospitals, London, UK

Davide Patrini

University College London Hospitals, London, UK

Mary Falzon

University College London Hospitals, London, UK

Elaine Borg

University College London Hospitals, London, UK

Reena Khiroya

University College London Hospitals, London, UK

Charles Swanton

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK; Department of Medical Oncology, University College London Hospitals, London, UK; Translational Cancer Therapeutics Laboratory, London Research Institute, London, UK

Mariam Jamal-Hanjani

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK; Department of Medical Oncology, University College London Hospitals, London, UK

Gareth Wilson

The Francis Crick Institute, London, UK

Nicolai Juul Birkbak

The Francis Crick Institute, London, UK

Thomas Watkins

The Francis Crick Institute, London, UK

Nicholas McGranahan

The Francis Crick Institute, London, UK

Christopher Abbosh

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK

Rachel Rosenthal

The Francis Crick Institute, London, UK

Mickael Escudero

The Francis Crick Institute, London, UK

Aengus Stewart

The Francis Crick Institute, London, UK

Andrew Rowan

The Francis Crick Institute, London, UK

Crispin Hiley

The Francis Crick Institute, London, UK; Cancer Research UK Lung Cancer Centre of Excellence, UCL Cancer Institute, London, UK

Jacki Goldman

The Francis Crick Institute, London, UK

Asia Ahmed

University College London Hospitals, London, UK

Magali Taylor

University College London Hospitals, London, UK

Junaid Choudhary

University College London Hospitals, London, UK

Penny Shaw

 

Raju Veeriah

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK

Justyna Czyzewska-Khan

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK

Diana Johnson

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK

Joanne Laycock

Translational Cancer Therapeutics Laboratory, University College London Cancer Institute, London, UK

Marcin Skrzypski

 

Robert Hynds

 

Kroopa Joshi

 

Assma Ben Aissa

 

Yien Ning Sophia Wong

Andy Georgiou

 

Mariana Werner Sunderland

James Reading

 

Sergio Quezada

 

Carmella Beastall

University College London Cancer Institute, London, UK

Nagina Mangal

University College London Cancer Institute, London, UK

Karl Peggs

 

Teresa Marafioti

 

Sam Janes

University College London Hospitals, London, UK

Martin Forster

University College London Hospitals, London, UK

Tanya Ahmad

University College London Hospitals, London, UK

Siow Ming Lee

University College London Hospitals, London, UK

Peter van Loo

 

Javier Herrero

The Francis Crick Institute, London, UK

John Hartley

 

Richard Kevin Stone

The Francis Crick Institute, London, UK

Tamara Denner

The Francis Crick Institute, London, UK

Emma Nye

The Francis Crick Institute, London, UK

Sophia Ward

The Francis Crick Institute, London, UK

Emilia Lim

The Francis Crick Institute, London, UK

Maise Al-Bakir

 

Dawn Carnell

University College London Hospitals, London, UK

Ruheena Mendes

University College London Hospitals, London, UK

Jeremy George

University College London Hospitals, London, UK

Neal Navani

University College London Hospitals, London, UK

Dionysis Papadatos-Pastos

University College London Hospitals, London, UK

Marco Scarci

University College London Hospitals, London, UK

Pat Gorman

 

Helen Lowe

 

Leah Ensell

 

David Moore

 

Dhruva Biswas

University College London Cancer Institute, London, UK

Roberto Salgado

Department of Pathology, GZA-ZNA Antwerp, Belgium

Maryam Razaq

 

Jerome Nicod

 

Stephan Beck

 

Saioa Lopez

Nickys lab

Ariana Huebner

Nickys lab

Michelle Dietzen

Nickys lab

Thanos Mourikis

Nickys lab

Mairead MacKenzie

Independent Cancer Patients Voice

Maggie Wilcox

Independent Cancer Patients Voice

Harriet Bell

Cancer Research UK & UCL Cancer Trials Centre, London, UK

Allan Hackshaw

Cancer Research UK & UCL Cancer Trials Centre, London, UK

Yenting Ngai

Cancer Research UK & UCL Cancer Trials Centre, London, UK

Sean Smith

Cancer Research UK & UCL Cancer Trials Centre, London, UK

Nicole Gower

Cancer Research UK & UCL Cancer Trials Centre, London, UK

Christian Ottensmeier

University Hospital Southampton NHS Foundation Trust

Serena Chee

University Hospital Southampton NHS Foundation Trust

Benjamin Johnson

University Hospital Southampton NHS Foundation Trust

Aiman Alzetani

University Hospital Southampton NHS Foundation Trust

Emily Shaw

University Hospital Southampton NHS Foundation Trust

Eric Lim

Royal Brompton and Harefield NHS Foundation Trust

Paulo De Sousa

Royal Brompton and Harefield NHS Foundation Trust

Monica Tavares Barbosa

Royal Brompton and Harefield NHS Foundation Trust

Andrew Nicholson

Royal Brompton and Harefield NHS Foundation Trust

Alex Bowman

Royal Brompton and Harefield NHS Foundation Trust

Simon Jordan

Royal Brompton and Harefield NHS Foundation Trust

Alexandra Rice

Royal Brompton and Harefield NHS Foundation Trust

Hilgardt Raubenheimer

Royal Brompton and Harefield NHS Foundation Trust

Harshil Bhayani

Royal Brompton and Harefield NHS Foundation Trust

Morag Hamilton

Royal Brompton and Harefield NHS Foundation Trust

Natalie Mensah

Royal Brompton and Harefield NHS Foundation Trust

Lyn Ambrose

Royal Brompton and Harefield NHS Foundation Trust

Anand Devaraj

Royal Brompton and Harefield NHS Foundation Trust

Hemangi Chavan

Royal Brompton and Harefield NHS Foundation Trust

Toyin Adefila-Ideozu

Royal Brompton and Harefield NHS Foundation Trust

Sofina Begum

Royal Brompton and Harefield NHS Foundation Trust

Henriette Klein

Royal Brompton and Harefield NHS Foundation Trust

Aleksander Mani

Royal Brompton and Harefield NHS Foundation Trust

Soraia Carvalho

Royal Brompton and Harefield NHS Foundation Trust

Daniel Kaniu

Royal Brompton and Harefield NHS Foundation Trust

Cristina Realingo

Royal Brompton and Harefield NHS Foundation Trust

Mpho Malima

Royal Brompton and Harefield NHS Foundation Trust

Sarah Booth

Royal Brompton and Harefield NHS Foundation Trust

Kelvin Lau

Barts Health NHS Trust

Michael Sheaff

Barts Health NHS Trust

Peter Schmid

Barts Health NHS Trust

Louise Lim

Barts Health NHS Trust

John Conibear

Barts Health NHS Trust

Veni Ezhil

Ashford and St. Peter's Hospitals NHS Foundation Trust

Vineet Prakash

Ashford and St. Peter's Hospitals NHS Foundation Trust

Sarah Danson

Sheffield Teaching Hospitals NHS Foundation Trust

Jonathan Bury

Sheffield Teaching Hospitals NHS Foundation Trust

John Edwards

Sheffield Teaching Hospitals NHS Foundation Trust

Jennifer Hill

Sheffield Teaching Hospitals NHS Foundation Trust

Sue Matthews

Sheffield Teaching Hospitals NHS Foundation Trust

Yota Kitsanta

Sheffield Teaching Hospitals NHS Foundation Trust

Jagan Rao

Sheffield Teaching Hospitals NHS Foundation Trust

Sara Tenconi

Sheffield Teaching Hospitals NHS Foundation Trust

Laura Socci

Sheffield Teaching Hospitals NHS Foundation Trust

Kim Suvarna

Sheffield Teaching Hospitals NHS Foundation Trust

Faith Kibutu

Sheffield Teaching Hospitals NHS Foundation Trust

Michael Agyemang

Sheffield Teaching Hospitals NHS Foundation Trust

Patricia Fisher

Sheffield Teaching Hospitals NHS Foundation Trust

Robin Young

Sheffield Teaching Hospitals NHS Foundation Trust

Michael Shackcloth

Liverpool Heart and Chest Hospital NHS Foundation Trust

John Gosney

Liverpool Heart and Chest Hospital NHS Foundation Trust

Sarah Feeney

Liverpool Heart and Chest Hospital NHS Foundation Trust

Julius Asante-Siaw

Liverpool Heart and Chest Hospital NHS Foundation Trust

Teresa Light

The Princess Alexandra Hospital NHS Trust

Tracey Horey

The Princess Alexandra Hospital NHS Trust

Dr. Dionysis Papadatos-Pastos

The Princess Alexandra Hospital NHS Trust

Dr. Peter Russell

The Princess Alexandra Hospital NHS Trust

Kevin G. Blyth

NHS Greater Glasgow and Clyde

Craig Dick

NHS Greater Glasgow and Clyde

Alan Kirk

Golden Jubilee National Hospital

Andrew Kidd

NHS Greater Glasgow and Clyde

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Uddin, I. et al. (2019). An Economical, Quantitative, and Robust Protocol for High-Throughput T Cell Receptor Sequencing from Tumor or Blood. In: López-Soto, A., Folgueras, A. (eds) Cancer Immunosurveillance. Methods in Molecular Biology, vol 1884. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-8885-3_2

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  • DOI: https://doi.org/10.1007/978-1-4939-8885-3_2

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  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-8884-6

  • Online ISBN: 978-1-4939-8885-3

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