Cell Reports (May 2020)
Representative Sequencing: Unbiased Sampling of Solid Tumor Tissue
- Kevin Litchfield,
- Stacey Stanislaw,
- Lavinia Spain,
- Lisa L. Gallegos,
- Andrew Rowan,
- Desiree Schnidrig,
- Heidi Rosenbaum,
- Alexandre Harle,
- Lewis Au,
- Samantha M. Hill,
- Zayd Tippu,
- Jennifer Thomas,
- Lisa Thompson,
- Hang Xu,
- Stuart Horswell,
- Aoune Barhoumi,
- Carol Jones,
- Katherine F. Leith,
- Daniel L. Burgess,
- Thomas B.K. Watkins,
- Emilia Lim,
- Nicolai J. Birkbak,
- Philippe Lamy,
- Iver Nordentoft,
- Lars Dyrskjøt,
- Lisa Pickering,
- Stephen Hazell,
- Mariam Jamal-Hanjani,
- James Larkin,
- Charles Swanton,
- Nelson R. Alexander,
- Samra Turajlic,
- Chris Abbosh,
- Kai-Keen Shiu,
- John Bridgewater,
- Daniel Hochhauser,
- Martin Forster,
- Siow-Ming Lee,
- Tanya Ahmad,
- Dionysis Papadatos-Pastos,
- Sam Janes,
- Peter Van Loo,
- Katey Enfield,
- Nicholas McGranahan,
- Ariana Huebner,
- Sergio Quezada,
- Stephan Beck,
- Peter Parker,
- Henning Walczak,
- Tariq Enver,
- Rob Hynds,
- Mary Falzon,
- Ian Proctor,
- Ron Sinclair,
- Chi-wah Lok,
- Zoe Rhodes,
- David Moore,
- Teresa Marafioti,
- Elaine Borg,
- Miriam Mitchison,
- Reena Khiroya,
- Giorgia Trevisan,
- Peter Ellery,
- Mark Linch,
- Sebastian Brandner,
- Crispin Hiley,
- Selvaraju Veeriah,
- Maryam Razaq,
- Heather Shaw,
- Gert Attard,
- Mita Afroza Akther,
- Cristina Naceur-Lombardelli,
- Lizi Manzano,
- Maise Al-Bakir,
- Simranpreet Summan,
- Nnenna Kanu,
- Sophie Ward,
- Uzma Asghar,
- Emilia Lim,
- Faye Gishen,
- Adrian Tookman,
- Paddy Stone,
- Caroline Stirling,
- Andrew Furness,
- Kim Edmonds,
- Nikki Hunter,
- Sarah Sarker,
- Sarah Vaughan,
- Mary Mangwende,
- Karla Pearce,
- Lavinia Spain,
- Scott Shepherd,
- Haixi Yan,
- Ben Shum,
- Eleanor Carlyle,
- Steve Hazell,
- Annika Fendler,
- Fiona Byrne,
- Nadia Yousaf,
- Sanjay Popat,
- Olivia Curtis,
- Gordon Stamp,
- Antonia Toncheva,
- Emma Nye,
- Aida Murra,
- Justine Korteweg,
- Nahid Sheikh,
- Debra Josephs,
- Ashish Chandra,
- James Spicer,
- Ula Mahadeva,
- Anna Green,
- Ruby Stewart,
- Lara-Rose Iredale,
- Tina Mackay,
- Ben Deakin,
- Debra Enting,
- Sarah Rudman,
- Sharmistha Ghosh,
- Lena Karapagniotou,
- Elias Pintus,
- Andrew Tutt,
- Sarah Howlett,
- Vasiliki Michalarea,
- James Brenton,
- Carlos Caldas,
- Rebecca Fitzgerald,
- Merche Jimenez-Linan,
- Elena Provenzano,
- Alison Cluroe,
- Grant Stewart,
- Colin Watts,
- Richard Gilbertson,
- Ultan McDermott,
- Simon Tavare,
- Emma Beddowes,
- Patricia Roxburgh,
- Andrew Biankin,
- Anthony Chalmers,
- Sioban Fraser,
- Karin Oien,
- Andrew Kidd,
- Kevin Blyth,
- Matt Krebs,
- Fiona Blackhall,
- Yvonne Summers,
- Caroline Dive,
- Richard Marais,
- Fabio Gomes,
- Mat Carter,
- Jo Dransfield,
- John Le Quesne,
- Dean Fennell,
- Jacqui Shaw,
- Babu Naidu,
- Shobhit Baijal,
- Bruce Tanchel,
- Gerald Langman,
- Andrew Robinson,
- Martin Collard,
- Peter Cockcroft,
- Charlotte Ferris,
- Hollie Bancroft,
- Amy Kerr,
- Gary Middleton,
- Joanne Webb,
- Salma Kadiri,
- Peter Colloby,
- Bernard Olisemeke,
- Rodelaine Wilson,
- Ian Tomlinson,
- Sanjay Jogai,
- Christian Ottensmeier,
- David Harrison,
- Massimo Loda,
- Adrienne Flanagan,
- Mairead McKenzie,
- Allan Hackshaw,
- Jonathan Ledermann,
- Abby Sharp,
- Laura Farrelly,
- Hayley Bridger
Affiliations
- Kevin Litchfield
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
- Stacey Stanislaw
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA
- Lavinia Spain
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK; Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK
- Lisa L. Gallegos
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA
- Andrew Rowan
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
- Desiree Schnidrig
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
- Heidi Rosenbaum
- Roche Sequencing Solutions, Madison, 500 S. Rosa Road, Madison, WI 53719, USA
- Alexandre Harle
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK; Université de Lorraine, CNRS UMR 7039 CRAN, Institut de Cancérologie de Lorraine, Service de Biopathologie, 54000 Nancy, France
- Lewis Au
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK; Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK
- Samantha M. Hill
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA; Department of Cancer Biology, University of Arizona Cancer Center, Tucson, AZ 85724, USA
- Zayd Tippu
- Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK
- Jennifer Thomas
- Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK
- Lisa Thompson
- The Centre for Molecular Pathology, The Royal Marsden Hospital, London SW3 6JJ, UK
- Hang Xu
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
- Stuart Horswell
- Department of Bioinformatics and Biostatistics, The Francis Crick Institute, London NW1 1AT, UK
- Aoune Barhoumi
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA
- Carol Jones
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA
- Katherine F. Leith
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA
- Daniel L. Burgess
- Roche Sequencing Solutions, Madison, 500 S. Rosa Road, Madison, WI 53719, USA
- Thomas B.K. Watkins
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
- Emilia Lim
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
- Nicolai J. Birkbak
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK; Department of Molecular Medicine, Aarhus University Hospital, Aarhus, Denmark
- Philippe Lamy
- Department of Molecular Medicine, Aarhus University Hospital, Aarhus, Denmark
- Iver Nordentoft
- Department of Molecular Medicine, Aarhus University Hospital, Aarhus, Denmark
- Lars Dyrskjøt
- Department of Molecular Medicine, Aarhus University Hospital, Aarhus, Denmark
- Lisa Pickering
- Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK
- Stephen Hazell
- Histopathology Department, Royal Marsden NHS Foundation Trust, London and Sutton, UK
- Mariam Jamal-Hanjani
- Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK; Department of Medical Oncology, University College London Hospitals, London, UK
- James Larkin
- Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK
- Charles Swanton
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK; Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, London, UK; Department of Medical Oncology, University College London Hospitals, London, UK; Corresponding author
- Nelson R. Alexander
- Roche Tissue Diagnostics, 1910 E. Innovation Park Drive, Tucson, AZ 85755, USA; Corresponding author
- Samra Turajlic
- Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK; Renal and Skin Units, The Royal Marsden Hospital, London SW3 6JJ, UK; Corresponding author
- Chris Abbosh
- Kai-Keen Shiu
- John Bridgewater
- Daniel Hochhauser
- Martin Forster
- Siow-Ming Lee
- Tanya Ahmad
- Dionysis Papadatos-Pastos
- Sam Janes
- Peter Van Loo
- Katey Enfield
- Nicholas McGranahan
- Ariana Huebner
- Sergio Quezada
- Stephan Beck
- Peter Parker
- Henning Walczak
- Tariq Enver
- Rob Hynds
- Mary Falzon
- Ian Proctor
- Ron Sinclair
- Chi-wah Lok
- Zoe Rhodes
- David Moore
- Teresa Marafioti
- Elaine Borg
- Miriam Mitchison
- Reena Khiroya
- Giorgia Trevisan
- Peter Ellery
- Mark Linch
- Sebastian Brandner
- Crispin Hiley
- Selvaraju Veeriah
- Maryam Razaq
- Heather Shaw
- Gert Attard
- Mita Afroza Akther
- Cristina Naceur-Lombardelli
- Lizi Manzano
- Maise Al-Bakir
- Simranpreet Summan
- Nnenna Kanu
- Sophie Ward
- Uzma Asghar
- Emilia Lim
- Faye Gishen
- Adrian Tookman
- Paddy Stone
- Caroline Stirling
- Andrew Furness
- Kim Edmonds
- Nikki Hunter
- Sarah Sarker
- Sarah Vaughan
- Mary Mangwende
- Karla Pearce
- Lavinia Spain
- Scott Shepherd
- Haixi Yan
- Ben Shum
- Eleanor Carlyle
- Steve Hazell
- Annika Fendler
- Fiona Byrne
- Nadia Yousaf
- Sanjay Popat
- Olivia Curtis
- Gordon Stamp
- Antonia Toncheva
- Emma Nye
- Aida Murra
- Justine Korteweg
- Nahid Sheikh
- Debra Josephs
- Ashish Chandra
- James Spicer
- Ula Mahadeva
- Anna Green
- Ruby Stewart
- Lara-Rose Iredale
- Tina Mackay
- Ben Deakin
- Debra Enting
- Sarah Rudman
- Sharmistha Ghosh
- Lena Karapagniotou
- Elias Pintus
- Andrew Tutt
- Sarah Howlett
- Vasiliki Michalarea
- James Brenton
- Carlos Caldas
- Rebecca Fitzgerald
- Merche Jimenez-Linan
- Elena Provenzano
- Alison Cluroe
- Grant Stewart
- Colin Watts
- Richard Gilbertson
- Ultan McDermott
- Simon Tavare
- Emma Beddowes
- Patricia Roxburgh
- Andrew Biankin
- Anthony Chalmers
- Sioban Fraser
- Karin Oien
- Andrew Kidd
- Kevin Blyth
- Matt Krebs
- Fiona Blackhall
- Yvonne Summers
- Caroline Dive
- Richard Marais
- Fabio Gomes
- Mat Carter
- Jo Dransfield
- John Le Quesne
- Dean Fennell
- Jacqui Shaw
- Babu Naidu
- Shobhit Baijal
- Bruce Tanchel
- Gerald Langman
- Andrew Robinson
- Martin Collard
- Peter Cockcroft
- Charlotte Ferris
- Hollie Bancroft
- Amy Kerr
- Gary Middleton
- Joanne Webb
- Salma Kadiri
- Peter Colloby
- Bernard Olisemeke
- Rodelaine Wilson
- Ian Tomlinson
- Sanjay Jogai
- Christian Ottensmeier
- David Harrison
- Massimo Loda
- Adrienne Flanagan
- Mairead McKenzie
- Allan Hackshaw
- Jonathan Ledermann
- Abby Sharp
- Laura Farrelly
- Hayley Bridger
- Journal volume & issue
-
Vol. 31,
no. 5
Abstract
Summary: Although thousands of solid tumors have been sequenced to date, a fundamental under-sampling bias is inherent in current methodologies. This is caused by a tissue sample input of fixed dimensions (e.g., 6 mm biopsy), which becomes grossly under-powered as tumor volume scales. Here, we demonstrate representative sequencing (Rep-Seq) as a new method to achieve unbiased tumor tissue sampling. Rep-Seq uses fixed residual tumor material, which is homogenized and subjected to next-generation sequencing. Analysis of intratumor tumor mutation burden (TMB) variability shows a high level of misclassification using current single-biopsy methods, with 20% of lung and 52% of bladder tumors having at least one biopsy with high TMB but low clonal TMB overall. Misclassification rates by contrast are reduced to 2% (lung) and 4% (bladder) when a more representative sampling methodology is used. Rep-Seq offers an improved sampling protocol for tumor profiling, with significant potential for improved clinical utility and more accurate deconvolution of clonal structure.