The impact of viral mutations on recognition by SARS-CoV-2 specific T cells

COVID-19 Genomics UK (COG-UK) Consortium; ISARIC4C Investigators; Thushan I. de Silva; Guihai Liu; Benjamin B. Lindsey; Danning Dong; Shona C. Moore; Nienyun Sharon Hsu; Dhruv Shah; Dannielle Wellington; Alexander J. Mentzer; Adrienn Angyal; Rebecca Brown; Matthew D. Parker; Zixi Ying; Xuan Yao; Lance Turtle; Susanna Dunachie; Mala K. Maini; Graham Ogg; Julian C. Knight; Yanchun Peng; Sarah L. Rowland-Jones; Tao Dong

doi:10.1016/j.isci.2021.103353

The impact of viral mutations on recognition by SARS-CoV-2 specific T cells

COVID-19 Genomics UK (COG-UK) Consortium, ISARIC4C Investigators, Thushan I. de Silva^*, Guihai Liu, Benjamin B. Lindsey, Danning Dong, Shona C. Moore, Nienyun Sharon Hsu, Dhruv Shah, Dannielle Wellington, Alexander J. Mentzer, Adrienn Angyal, Rebecca Brown, Matthew D. Parker, Zixi Ying, Xuan Yao, Lance Turtle, Susanna Dunachie, Mala K. Maini, Graham OggJulian C. Knight, Yanchun Peng, Sarah L. Rowland-Jones, Tao Dong^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract / Description of output

We identify amino acid variants within dominant SARS-CoV-2 T cell epitopes by interrogating global sequence data. Several variants within nucleocapsid and ORF3a epitopes have arisen independently in multiple lineages and result in loss of recognition by epitope-specific T cells assessed by IFN-γ and cytotoxic killing assays. Complete loss of T cell responsiveness was seen due to Q213K in the A∗01:01-restricted CD8+ ORF3a epitope FTSDYYQLY_207-215; due to P13L, P13S, and P13T in the B∗27:05-restricted CD8+ nucleocapsid epitope QRNAPRITF_9-17; and due to T362I and P365S in the A∗03:01/A∗11:01-restricted CD8+ nucleocapsid epitope KTFPPTEPK_361-369. CD8+ T cell lines unable to recognize variant epitopes have diverse T cell receptor repertoires. These data demonstrate the potential for T cell evasion and highlight the need for ongoing surveillance for variants capable of escaping T cell as well as humoral immunity.

Original language	English
Article number	103353
Journal	iScience
Volume	24
Issue number	11
DOIs	https://doi.org/10.1016/j.isci.2021.103353
Publication status	Published - 19 Nov 2021

Keywords / Materials (for Non-textual outputs)

Immune response
Immunology
Molecular biology
Phylogenetics
Virology

Access to Document

10.1016/j.isci.2021.103353

PIIS2589004221013225Final published version, 2.03 MBLicence: Creative Commons: Attribution (CC-BY)

Cite this

COVID-19 Genomics UK (COG-UK) Consortium, ISARIC4C Investigators, de Silva, T. I., Liu, G., Lindsey, B. B., Dong, D., Moore, S. C., Hsu, N. S., Shah, D., Wellington, D., Mentzer, A. J., Angyal, A., Brown, R., Parker, M. D., Ying, Z., Yao, X., Turtle, L., Dunachie, S., Maini, M. K., ... Dong, T. (2021). The impact of viral mutations on recognition by SARS-CoV-2 specific T cells. iScience, 24(11), Article 103353. https://doi.org/10.1016/j.isci.2021.103353

@article{4eb7c9777bc44bcba698c3e84ae431c4,

title = "The impact of viral mutations on recognition by SARS-CoV-2 specific T cells",

abstract = "We identify amino acid variants within dominant SARS-CoV-2 T cell epitopes by interrogating global sequence data. Several variants within nucleocapsid and ORF3a epitopes have arisen independently in multiple lineages and result in loss of recognition by epitope-specific T cells assessed by IFN-γ and cytotoxic killing assays. Complete loss of T cell responsiveness was seen due to Q213K in the A∗01:01-restricted CD8+ ORF3a epitope FTSDYYQLY207-215; due to P13L, P13S, and P13T in the B∗27:05-restricted CD8+ nucleocapsid epitope QRNAPRITF9-17; and due to T362I and P365S in the A∗03:01/A∗11:01-restricted CD8+ nucleocapsid epitope KTFPPTEPK361-369. CD8+ T cell lines unable to recognize variant epitopes have diverse T cell receptor repertoires. These data demonstrate the potential for T cell evasion and highlight the need for ongoing surveillance for variants capable of escaping T cell as well as humoral immunity.",

keywords = "Immune response, Immunology, Molecular biology, Phylogenetics, Virology",

author = "{COVID-19 Genomics UK (COG-UK) Consortium} and {ISARIC4C Investigators} and {de Silva}, {Thushan I.} and Guihai Liu and Lindsey, {Benjamin B.} and Danning Dong and Moore, {Shona C.} and Hsu, {Nienyun Sharon} and Dhruv Shah and Dannielle Wellington and Mentzer, {Alexander J.} and Adrienn Angyal and Rebecca Brown and Parker, {Matthew D.} and Zixi Ying and Xuan Yao and Lance Turtle and Susanna Dunachie and Aanensen, {David M.} and Khalil Abudahab and Helen Adams and Alexander Adams and Safiah Afifi and Dinesh Aggarwal and Ahmad, {Shazaad S.Y.} and Louise Aigrain and Adela Alcolea-Medina and Alikhan, {Nabil Fareed} and Elias Allara and Roberto Amato and Tara Annett and Stephen Aplin and Ariani, {Cristina V.} and Hibo Asad and Amy Ash and Paula Ashfield and Fiona Ashford and Laura Atkinson and Attwood, {Stephen W.} and Cressida Auckland and Alp Aydin and Baker, {David J.} and Paul Baker and Balcazar, {Carlos E.} and Jonathan Ball and Barrett, {Jeffrey C.} and Magdalena Barrow and Edward Barton and Matthew Bashton and Bassett, {Andrew R.} and Rahul Batra and Chris Baxter and Nadua Bayzid and Charlotte Beaver and Beckett, {Angela H.} and Beckwith, {Shaun M.} and Luke Bedford and Robert Beer and Andrew Beggs and Bellis, {Katherine L.} and Louise Berry and Beatrice Bertolusso and Angus Best and Emma Betteridge and David Bibby and Kelly Bicknell and Debbie Binns and Alec Birchley and Bird, {Paul W.} and Chloe Bishop and Rachel Blacow and Victoria Blakey and Beth Blane and Frances Bolt and James Bonfield and Stephen Bonner and David Bonsall and Tim Boswell and Andrew Bosworth and Yann Bourgeois and Olivia Boyd and Bradley, {Declan T.} and Cassie Breen and Catherine Bresner and Judith Breuer and Stephen Bridgett and Bronner, {Iraad F.} and Ellena Brooks and Alice Broos and Brown, {Julianne R.} and Giselda Bucca and Buchan, {Sarah L.} and David Buck and Matthew Bull and Burns, {Phillipa J.} and Shirelle Burton-Fanning and Timothy Byaruhanga and Matthew Byott and Sharon Campbell and Carabelli, {Alessandro M.} and Cargill, {James S.} and Matthew Carlile and Carvalho, {Silvia F.} and Anna Casey and Anibolina Castigador and Jana Catalan and Vicki Chalker and Chaloner, {Nicola J.} and Meera Chand and Chappell, {Joseph G.} and Themoula Charalampous and Wendy Chatterton and Yasmin Chaudhry and Churcher, {Carol M.} and Gemma Clark and Phillip Clarke and Cogger, {Benjamin J.} and Kevin Cole and Jennifer Collins and Rachel Colquhoun and Connor, {Thomas R.} and Cook, {Kate F.} and Jason Coombes and Sally Corden and Claire Cormie and Nicholas Cortes and Marius Cotic and Seb Cotton and Simon Cottrell and Lindsay Coupland and MacGregor Cox and Alison Cox and Noel Craine and Liam Crawford and Aidan Cross and Crown, {Matthew R.} and Dorian Crudgington and Nicola Cumley and Tanya Curran and Curran, {Martin D.} and {da Silva Filipe}, Ana and Gavin Dabrera and Darby, {Alistair C.} and Davidson, {Rose K.} and Alisha Davies and Davies, {Robert M.} and Thomas Davis and {de Angelis}, Daniela and {De Lacy}, Elen and {de Oliveira Martins}, Leonardo and Johnny Debebe and Rebecca Denton-Smith and Samir Dervisevic and Rebecca Dewar and Jayasree Dey and Joana Dias and Donald Dobie and Dorman, {Matthew J.} and Fatima Downing and Megan Driscoll and {du Plessis}, Louis and Nichola Duckworth and Jillian Durham and Kirstine Eastick and Easton, {Lisa J.} and Richard Eccles and Jonathan Edgeworth and Sue Edwards and {El Bouzidi}, Kate and Sahar Eldirdiri and Nicholas Ellaby and Scott Elliott and Gary Eltringham and Leah Ensell and Erkiert, {Michelle J.} and Zamudio, {Marina Escalera} and Sarah Essex and Evans, {Johnathan M.} and Cariad Evans and William Everson and Fairley, {Derek J.} and Karlie Fallon and Arezou Fanaie and Farr, {Ben W.} and Christopher Fearn and Theresa Feltwell and Lynne Ferguson and Laia Fina and Flavia Flaviani and Fleming, {Vicki M.} and Sally Forrest and Ebenezer Foster-Nyarko and Foulkes, {Benjamin H.} and Luke Foulser and Mireille Fragakis and Dan Frampton and Sarah Francois and Christophe Fraser and Freeman, {Timothy M.} and Helen Fryer and Marc Fuchs and William Fuller and Kavitha Gajee and Katerina Galai and Abbie Gallagher and Eileen Gallagher and Gallagher, {Michael D.} and Marta Gallis and Amy Gaskin and Bree Gatica-Wilcox and Lily Geidelberg and Matthew Gemmell and Iliana Georgana and George, {Ryan P.} and Laura Gifford and Lauren Gilbert and Girgis, {Sophia T.} and Sharon Glaysher and Goldstein, {Emily J.} and Tanya Golubchik and Gomes, {Andrea N.} and S{\'o}nia Gon{\c c}alves and Goodfellow, {Ian G.} and Scott Goodwin and Salman Goudarzi and Marina Gourtovaia and Clive Graham and Lee Graham and Grant, {Paul R.} and Green, {Luke R.} and Angie Green and Jane Greenaway and Richard Gregory and Martyn Guest and Gunson, {Rory N.} and Gupta, {Ravi K.} and Bernardo Gutierrez and Haldenby, {Sam T.} and Hamilton, {William L.} and Hansford, {Samantha E.} and Tanzina Haque and Harris, {Kathryn A.} and Ian Harrison and Harrison, {Ewan M.} and Jennifer Hart and Hartley, {John A.} and Harvey, {William T.} and Matthew Harvey and Hassan-Ibrahim, {Mohammed O.} and Judith Heaney and Thomas Helmer and Henderson, {John H.} and Hesketh, {Andrew R.} and Jessica Hey and David Heyburn and Higginson, {Ellen E.} and Verity Hill and Hill, {Jack D.} and Hilson, {Rachel A.} and Ember Hilvers and Holden, {Matthew T.G.} and Amy Hollis and Holmes, {Christopher W.} and Nadine Holmes and Holmes, {Alison H.} and Richard Hopes and Hornsby, {Hailey R.} and Myra Hosmillo and Catherine Houlihan and Howson-Wells, {Hannah C.} and Jonathan Hubb and Hannah Huckson and Warwick Hughes and Joseph Hughes and Margaret Hughes and Stephanie Hutchings and Giles Idle and Illingworth, {Chris J.} and Robert Impey and Dianne Irish-Tavares and Miren Iturriza-Gomara and Rhys Izuagbe and Chris Jackson and Ben Jackson and Jackson, {Leigh M.} and Jackson, {Kathryn A.} and Jackson, {David K.} and Jahun, {Aminu S.} and Victoria James and Keith James and Christopher Jeanes and Jeffries, {Aaron R.} and Sarah Jeremiah and Andrew Jermy and Michaela John and Rob Johnson and Kate Johnson and Ian Johnston and Owen Jones and Sophie Jones and Hannah Jones and Jones, {Christopher R.} and Neil Jones and Amelia Joseph and Sarah Judges and Kay, {Gemma L.} and Sally Kay and Keatley, {Jon Paul} and Keeley, {Alexander J.} and Anita Kenyon and Kermack, {Leanne M.} and Manjinder Khakh and Kidd, {Stephen P.} and Maimuna Kimuli and Stuart Kirk and Christine Kitchen and Katie Kitchman and Knight, {Bridget A.} and Cherian Koshy and Kraemer, {Moritz U.G.} and Sara Kumziene-Summerhayes and Dominic Kwiatkowski and Angie Lackenby and Laing, {Kenneth G.} and Temi Lampejo and Langford, {Cordelia F.} and Deborah Lavin and Lawton, {Andrew I.} and Jack Lee and David Lee and Lensing, {Stefanie V.} and Steven Leonard and Levett, {Lisa J.} and Thanh Le-Viet and Jonathan Lewis and Kevin Lewis and Jennifier Liddle and Steven Liggett and Lillie, {Patrick J.} and Lister, {Michelle M.} and Rich Livett and Stephanie Lo and Loman, {Nicholas J.} and Loose, {Matthew W.} and Louka, {Stavroula F.} and Loveson, {Katie F.} and Sarah Lowdon and Hannah Lowe and Lowe, {Helen L.} and Lucaci, {Anita O.} and Catherine Ludden and Jessica Lynch and Lyons, {Ronan A.} and Katrina Lythgoe and Machin, {Nicholas W.} and George MacIntyre-Cockett and Andrew Mack and Ben Macklin and Alasdair Maclean and Emily Macnaughton and Pinglawathee Madona and Mailis Maes and Laurentiu Maftei and Mahanama, {Adhyana I.K.} and Mahungu, {Tabitha W.} and Daniel Mair and Joshua Maksimovic and Malone, {Cassandra S.} and Daniel Maloney and Nikos Manesis and Robin Manley and Anna Mantzouratou and Angela Marchbank and Arun Mariappan and Inigo Martincorena and {Martinez Nunez}, {Rocio T.} and Mather, {Alison E.} and Patrick Maxwell and Megan Mayhew and Tamyo Mbisa and McCann, {Clare M.} and McCarthy, {Shane A.} and Kathryn McCluggage and McClure, {Patrick C.} and McCrone, {J. T.} and McHugh, {Martin P.} and McKenna, {James P.} and Caoimhe McKerr and McManus, {Georgina M.} and McMurray, {Claire L.} and Claire McMurray and Alan McNally and Lizzie Meadows and Nathan Medd and Oliver Megram and Mirko Menegazzo and Ian Merrick and Michell, {Stephen L.} and Michelsen, {Michelle L.} and Mariyam Mirfenderesky and Jeremy Mirza and Julia Miskelly and Emma Moles-Garcia and Moll, {Robin J.} and Zoltan Molnar and Monahan, {Irene M.} and Matteo Mondani and Siddharth Mookerjee and Christopher Moore and Jonathan Moore and Nathan Moore and Catherine Moore and Helen Morcrette and Sian Morgan and Mari Morgan and Matilde Mori and Arthur Morriss and Samuel Moses and Craig Mower and Peter Muir and Afrida Mukaddas and Florence Munemo and Robert Munn and Abigail Murray and Murray, {Leanne J.} and Murray, {Darren R.} and Manasa Mutingwende and Richard Myers and Eleni Nastouli and Gaia Nebbia and Andrew Nelson and Charlotte Nelson and Sam Nicholls and Jenna Nichols and Roberto Nicodemi and Kyriaki Nomikou and Justin O'Grady and Sarah O'Brien and Mina Odedra and Natasha Ohemeng-Kumi and Karen Oliver and Orton, {Richard J.} and Husam Osman and {xeine O'Toole}, O'Toole and Nicole Pacchiarini and Debra Padgett and Page, {Andrew J.} and Park, {Emily J.} and Park, {Naomi R.} and Surendra Parmar and Partridge, {David G.} and David Pascall and Amita Patel and Bindi Patel and Steve Paterson and Payne, {Brendan A.I.} and Peacock, {Sharon J.} and Clare Pearson and Emanuela Pelosi and Benita Percival and Jon Perkins and Malorie Perry and Pinckert, {Malte L.} and Steven Platt and Olga Podplomyk and Manoj Pohare and Marcus Pond and Pope, {Cassie F.} and Radoslaw Poplawski and Jessica Powell and Jennifer Poyner and Liam Prestwood and Anna Price and Price, {James R.} and Prieto, {Jacqui A.} and Pritchard, {David T.} and Prosolek, {Sophie J.} and Georgia Pugh and Monika Pusok and Pybus, {Oliver G.} and Pymont, {Hannah M.} and Quail, {Michael A.} and Joshua Quick and Clara Radulescu and Jayna Raghwani and Manon Ragonnet-Cronin and Lucille Rainbow and Diana Rajan and Shavanthi Rajatileka and Ramadan, {Newara A.} and Andrew Rambaut and John Ramble and Randell, {Paul A.} and Paul Randell and Liz Ratcliffe and Veena Raviprakash and Mohammad Raza and Redshaw, {Nicholas M.} and Sara Rey and Nicola Reynolds and Alex Richter and Robertson, {David L.} and Esther Robinson and Robson, {Samuel C.} and Fiona Rogan and Stefan Rooke and Will Rowe and Sunando Roy and Steven Rudder and Chris Ruis and Steven Rushton and Felicity Ryan and Kordo Saeed and Buddhini Samaraweera and Sambles, {Christine M.} and Roy Sanderson and Theo Sanderson and Fei Sang and Thea Sass and Emily Scher and Garren Scott and Carol Scott and Jasveen Sehmi and Sharif Shaaban and Divya Shah and Jessica Shaw and Ekaterina Shelest and Shepherd, {James G.} and Sheridan, {Liz A.} and Nicola Sheriff and Lesley Shirley and John Sillitoe and Siona Silviera and Simpson, {David A.} and Aditi Singh and Dawn Singleton and Timofey Skvortsov and Sloan, {Tim J.} and Graciela Sluga and Ken Smith and Smith, {Kim S.} and Perminder Smith and Smith, {Darren L.} and Louise Smith and Smith, {Colin P.} and Nikki Smith and Smollett, {Katherine L.} and Snell, {Luke B.} and Thomas Somassa and Joel Southgate and Karla Spellman and {Spencer Chapman}, {Michael H.} and Spurgin, {Lewis G.} and Spyer, {Moira J.} and Rachael Stanley and William Stanley and Stanton, {Thomas D.} and Igor Starinskij and Joanne Stockton and Susanne Stonehouse and Nathaniel Storey and Studholme, {David J.} and Malur Sudhanva and Emma Swindells and Yusri Taha and Tan, {Ngee Keong} and Tang, {Julian W.} and Miao Tang and Taylor, {Ben E.W.} and Taylor, {Joshua F.} and Sarah Taylor and Ben Temperton and Templeton, {Kate E.} and Claire Thomas and Laura Thomson and Thomson, {Emma C.} and Alicia Thornton and Thurston, {Scott A.J.} and Todd, {John A.} and Rachael Tomb and Lily Tong and Gerry Tonkin-Hill and Torok, {M. Estee} and Tovar-Corona, {Jaime M.} and Amy Trebes and Trotter, {Alexander J.} and Ioulia Tsatsani and Robyn Turnbull and Twohig, {Katherine A.} and Helen Umpleby and Underwood, {Anthony P.} and Vamos, {Edith E.} and Vasylyeva, {Tetyana I.} and Sreenu Vattipally and Gabrielle Vernet and Vipond, {Barry B.} and Volz, {Erik M.} and Sarah Walsh and Dennis Wang and Ben Warne and Joanna Warwick-Dugdale and Elizabeth Wastnedge and Joanne Watkins and Watson, {Louisa K.} and Sheila Waugh and Webster, {Hermione J.} and Danni Weldon and Elaine Westwick and Thomas Whalley and Helen Wheeler and Mark Whitehead and Max Whiteley and Andrew Whitwham and Claudia Wierzbicki and Willford, {Nicholas J.} and Williams, {Lesley Anne} and Rebecca Williams and Cheryl Williams and Chris Williams and Williams, {Charlotte A.} and Williams, {Rachel J.} and Thomas Williams and Catryn Williams and Williamson, {Kathleen A.} and Eleri Wilson-Davies and Eric Witele and Withell, {Karen T.} and Witney, {Adam A.} and Paige Wolverson and Nick Wong and Trudy Workman and Victoria Wright and Wright, {Derek W.} and Tim Wyatt and Sarah Wyllie and Li Xu-McCrae and Mehmet Yavus and Geraldine Yaze and Yeats, {Corin A.} and Gonzalo Yebra and Yew, {Wen C.} and Young, {Gregory R.} and Jamie Young and Zarebski, {Alex E.} and Peijun Zhang and Maini, {Mala K.} and Graham Ogg and Knight, {Julian C.} and Baillie, {J. Kenneth} and Semple, {Malcolm G.} and Openshaw, {Peter J.M.} and Gail Carson and Beatrice Alex and Petros Andrikopoulos and Benjamin Bach and Barclay, {Wendy S.} and Debby Bogaert and Kanta Chechi and Cooke, {Graham S.} and Docherty, {Annemarie B.} and Correia, {Gon{\c c}alo dos Santos} and Dumas, {Marc Emmanuel} and Jake Dunning and Tom Fletcher and Green, {Christopher A.} and William Greenhalf and Griffin, {Julian L.} and Gupta, {Rishi K.} and Harrison, {Ewen M.} and Hiscox, {Julian A.} and {Wai Ho}, {Antonia Ying} and Horby, {Peter W.} and Samreen Ijaz and Saye Khoo and Paul Klenerman and Andrew Law and Lewis, {Matthew R.} and Sonia Liggi and Lim, {Wei Shen} and Lynn Maslen and Laura Merson and Meynert, {Alison M.} and Mahdad Noursadeghi and Michael Olanipekun and Anthonia Osagie and Massimo Palmarini and Carlo Palmieri and Paxton, {William A.} and Georgios Pollakis and Nicholas Price and Russell, {Clark D.} and Vanessa Sancho-Shimizu and Sands, {Caroline J.} and Scott, {Janet T.} and Louise Sigfrid and Tom Solomon and Shiranee Sriskandan and David Stuart and Charlotte Summers and Swann, {Olivia V.} and Zoltan Takats and Panteleimon Takis and Tedder, {Richard S.} and Thompson, {A. A.Roger} and Thwaites, {Ryan S.} and Maria Zambon and Hayley Hardwick and Chloe Donohue and Fiona Griffiths and Wilna Oosthuyzen and Cara Donegan and Spencer, {Rebecca G.} and Jo Dalton and Michelle Girvan and Egle Saviciute and Stephanie Roberts and Janet Harrison and Laura Marsh and Marie Connor and Sophie Halpin and Clare Jackson and Carrol Gamble and Daniel Plotkin and James Lee and Gary Leeming and Murray Wham and Sara Clohisey and Ross Hendry and James Scott-Brown and Victoria Shaw and Sarah McDonald and Se{\'a}n Keating and Ahmed, {Katie A.} and Armstrong, {Jane A.} and Milton Ashworth and Asiimwe, {Innocent G.} and Siddharth Bakshi and Barlow, {Samantha L.} and Laura Booth and Benjamin Brennan and Katie Bullock and Catterall, {Benjamin W.A.} and Clark, {Jordan J.} and Clarke, {Emily A.} and Sarah Cole and Louise Cooper and Helen Cox and Christopher Davis and Oslem Dincarslan and Chris Dunn and Philip Dyer and Angela Elliott and Anthony Evans and Lorna Finch and Fisher, {Lewis W.S.} and Terry Foster and Isabel Garcia-Dorival and Philip Gunning and Catherine Hartley and Jensen, {Rebecca L.} and Jones, {Christopher B.} and Jones, {Trevor R.} and Shadia Khandaker and Katharine King and Kiy, {Robyn T.} and Chrysa Koukorava and Annette Lake and Suzannah Lant and Diane Latawiec and Lara Lavelle-Langham and Daniella Lefteri and Lauren Lett and Livoti, {Lucia A.} and Maria Mancini and Sarah McDonald and Laurence McEvoy and John McLauchlan and Soeren Metelmann and Miah, {Nahida S.} and Joanna Middleton and Joyce Mitchell and Murphy, {Ellen G.} and Rebekah Penrice-Randal and Jack Pilgrim and Tessa Prince and Will Reynolds and Ridley, {P. Matthew} and Debby Sales and Shaw, {Victoria E.} and Shears, {Rebecca K.} and Benjamin Small and Subramaniam, {Krishanthi S.} and Agnieska Szemiel and Aislynn Taggart and Jolanta Tanianis-Hughes and Jordan Thomas and Erwan Trochu and {van Tonder}, Libby and Eve Wilcock and Zhang, {J. Eunice} and Lisa Flaherty and Nicole Maziere and Emily Cass and Carracedo, {Alejandra Doce} and Nicola Carlucci and Anthony Holmes and Hannah Massey and Lee Murphy and Nicola Wrobel and Sarah McCafferty and Kirstie Morrice and Alan MacLean and Kayode Adeniji and Daniel Agranoff and Ken Agwuh and Dhiraj Ail and Aldera, {Erin L.} and Ana Alegria and Sam Allen and Brian Angus and Abdul Ashish and Dougal Atkinson and Shahedal Bari and Gavin Barlow and Stella Barnass and Nicholas Barrett and Christopher Bassford and Sneha Basude and David Baxter and Michael Beadsworth and Jolanta Bernatoniene and John Berridge and Colin Berry and Nicola Best and Pieter Bothma and David Chadwick and Robin Brittain-Long and Naomi Bulteel and Tom Burden and Andrew Burtenshaw and Vikki Caruth and Duncan Chambler and Nigel Chee and Jenny Child and Srikanth Chukkambotla and Tom Clark and Paul Collini and Catherine Cosgrove and Jason Cupitt and Cutino-Moguel, {Maria Teresa} and Paul Dark and Chris Dawson and Phil Donnison and Sam Douthwaite and Andrew Drummond and Ingrid DuRand and Ahilanadan Dushianthan and Tristan Dyer and Chi Eziefula and Chrisopher Fegan and Adam Finn and Duncan Fullerton and Sanjeev Garg and Atul Garg and Effrossyni Gkrania-Klotsas and Jo Godden and Arthur Goldsmith and Elaine Hardy and Stuart Hartshorn and Daniel Harvey and Peter Havalda and Hawcutt, {Daniel B.} and Maria Hobrok and Luke Hodgson and Anil Hormis and Michael Jacobs and Susan Jain and Paul Jennings and Agilan Kaliappan and Vidya Kasipandian and Stephen Kegg and Michael Kelsey and Jason Kendall and Caroline Kerrison and Ian Kerslake and Oliver Koch and Gouri Koduri and George Koshy and Shondipon Laha and Steven Laird and Susan Larkin and Tamas Leiner and Patrick Lillie and James Limb and Vanessa Linnett and Jeff Little and Mark Lyttle and Michael MacMahon and Ravish Mankregod and Huw Masson and Elijah Matovu and Katherine McCullough and Ruth McEwen and Manjula Meda and Gary Mills and Jane Minton and Kavya Mohandas and Quen Mok and James Moon and Elinoor Moore and Patrick Morgan and Craig Morris and Katherine Mortimore and Mbiye Mpenge and Rohinton Mulla and Michael Murphy and Megan Nagel and Thapas Nagarajan and Mark Nelson and Lillian Norris and O'Shea, {Matthew K.} and Igor Otahal and Marlies Ostermann and Mark Pais and Selva Panchatsharam and Danai Papakonstantinou and Hassan Paraiso and Brij Patel and Natalie Pattison and Justin Pepperell and Mark Peters and Mandeep Phull and Stefania Pintus and Pooni, {Jagtur Singh} and Tim Planche and Frank Post and David Price and Rachel Prout and Nikolas Rae and Henrik Reschreiter and Tim Reynolds and Neil Richardson and Mark Roberts and Devender Roberts and Alistair Rose and Guy Rousseau and Bobby Ruge and Brendan Ryan and Taranprit Saluja and Schmid, {Matthias L.} and Aarti Shah and Prad Shanmuga and Anil Sharma and Anna Shawcross and Jeremy Sizer and Manu Shankar-Hari and Richard Smith and Catherine Snelson and Nick Spittle and Nikki Staines and Tom Stambach and Richard Stewart and Pradeep Subudhi and Tamas Szakmany and Kate Tatham and Jo Thomas and Chris Thompson and Robert Thompson and Ascanio Tridente and Darell Tupper-Carey and Mary Twagira and Nick Vallotton and Rama Vancheeswaran and Lisa Vincent-Smith and Shico Visuvanathan and Alan Vuylsteke and Sam Waddy and Rachel Wake and Andrew Walden and Ingeborg Welters and Tony Whitehouse and Paul Whittaker and Ashley Whittington and Padmasayee Papineni and Meme Wijesinghe and Martin Williams and Lawrence Wilson and Stephen Winchester and Martin Wiselka and Adam Wolverson and Wootton, {Daniel G.} and Andrew Workman and Bryan Yates and Peter Young and Yanchun Peng and Rowland-Jones, {Sarah L.} and Tao Dong",

note = "Funding Information: This work is supported by the UK Medical Research Council (MRC); Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (CIFMS), China; National Institute for Health Research (NIHR) Oxford Biomedical Research Centre , and UK Research and Innovation (UKRI)/NIHR through the UK Coronavirus Immunology Consortium (UK-CIC). Sequencing of SARS-CoV-2 samples and collation of data was undertaken by the COG-UK CONSORTIUM. COG-UK is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR), and Genome Research Limited , operating as the Wellcome Sanger Institute. T.I.d.S. is supported by a Wellcome Trust Intermediate Clinical Fellowship ( 110058/Z/15/Z ). L.T. is supported by the Wellcome Trust (grant number 205228/Z/16/Z ) and by the University of Liverpool Centre for Excellence in Infectious Disease Research (CEIDR). S.D. is funded by an NIHR Global Research Professorship ( NIHR300791 ). L.T. and S.C.M. are also supported by the U.S. Food and Drug Administration Medical Countermeasures Initiative contract 75F40120C00085 and the National Institute for Health Research Health Protection Research Unit (HPRU) in Emerging and Zoonotic Infections ( NIHR200907 ) at University of Liverpool in partnership with Public Health England (PHE), in collaboration with Liverpool School of Tropical Medicine and the University of Oxford. L.T. is based at the University of Liverpool. M.D.P. is funded by the NIHR Sheffield Biomedical Research Centre (BRC – IS-BRC-1215-20017). ISARIC4C is supported by the MRC (grant no MC_PC_19059 ). J.C.K. is a Wellcome Investigator ( WT204969/Z/16/Z ) and supported by NIHR Oxford Biomedical Research Centre and CIFMS . The views expressed are those of the authors and not necessarily those of the NIHR or MRC. Funding Information: This work is supported by the UK Medical Research Council (MRC); Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (CIFMS), China; National Institute for Health Research (NIHR) Oxford Biomedical Research Centre, and UK Research and Innovation (UKRI)/NIHR through the UK Coronavirus Immunology Consortium (UK-CIC). Sequencing of SARS-CoV-2 samples and collation of data was undertaken by the COG-UK CONSORTIUM. COG-UK is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR), and Genome Research Limited, operating as the Wellcome Sanger Institute. T.I.d.S. is supported by a Wellcome Trust Intermediate Clinical Fellowship (110058/Z/15/Z). L.T. is supported by the Wellcome Trust (grant number 205228/Z/16/Z) and by the University of Liverpool Centre for Excellence in Infectious Disease Research (CEIDR). S.D. is funded by an NIHR Global Research Professorship (NIHR300791). L.T. and S.C.M. are also supported by the U.S. Food and Drug Administration Medical Countermeasures Initiative contract 75F40120C00085 and the National Institute for Health Research Health Protection Research Unit (HPRU) in Emerging and Zoonotic Infections (NIHR200907) at University of Liverpool in partnership with Public Health England (PHE), in collaboration with Liverpool School of Tropical Medicine and the University of Oxford. L.T. is based at the University of Liverpool. M.D.P. is funded by the NIHR Sheffield Biomedical Research Centre (BRC – IS-BRC-1215-20017). ISARIC4C is supported by the MRC (grant no MC_PC_19059). J.C.K. is a Wellcome Investigator (WT204969/Z/16/Z) and supported by NIHR Oxford Biomedical Research Centre and CIFMS. The views expressed are those of the authors and not necessarily those of the NIHR or MRC. T.I.d.S. and T.D. conceptualized the project; T.D. T.I.d.S. L.T. and Y.P. designed and supervised T cell experiments; B.B.L. N.S.H. and M.D.P. conducted the viral sequence analyses; D.S. conducted the literature review and collated T cell epitope information; G.L. D.D. and S.C.M. performed experiments and analyzed the data; X.Y. Z.Y. A.A. and R.B. provided critical reagents and technical assistance; J.C.K. and A.J.M. established clinical cohorts; T.I.d.S. and T.D. wrote and edited the original draft; all co-authors reviewed and edited the manuscript. The authors have no competing interests to declare. Publisher Copyright: {\textcopyright} 2021 The Author(s)",

year = "2021",

month = nov,

day = "19",

doi = "10.1016/j.isci.2021.103353",

language = "English",

volume = "24",

journal = "iScience",

issn = "2589-0042",

publisher = "Cell Press",

number = "11",

}

COVID-19 Genomics UK (COG-UK) Consortium, ISARIC4C Investigators, de Silva, TI, Liu, G, Lindsey, BB, Dong, D, Moore, SC, Hsu, NS, Shah, D, Wellington, D, Mentzer, AJ, Angyal, A, Brown, R, Parker, MD, Ying, Z, Yao, X, Turtle, L, Dunachie, S, Maini, MK, Ogg, G, Knight, JC, Peng, Y, Rowland-Jones, SL & Dong, T 2021, 'The impact of viral mutations on recognition by SARS-CoV-2 specific T cells', iScience, vol. 24, no. 11, 103353. https://doi.org/10.1016/j.isci.2021.103353

TY - JOUR

T1 - The impact of viral mutations on recognition by SARS-CoV-2 specific T cells

AU - COVID-19 Genomics UK (COG-UK) Consortium

AU - ISARIC4C Investigators

AU - de Silva, Thushan I.

AU - Liu, Guihai

AU - Lindsey, Benjamin B.

AU - Dong, Danning

AU - Moore, Shona C.

AU - Hsu, Nienyun Sharon

AU - Shah, Dhruv

AU - Wellington, Dannielle

AU - Mentzer, Alexander J.

AU - Angyal, Adrienn

AU - Brown, Rebecca

AU - Parker, Matthew D.

AU - Ying, Zixi

AU - Yao, Xuan

AU - Turtle, Lance

AU - Dunachie, Susanna

AU - Aanensen, David M.

AU - Abudahab, Khalil

AU - Adams, Helen

AU - Adams, Alexander

AU - Afifi, Safiah

AU - Aggarwal, Dinesh

AU - Ahmad, Shazaad S.Y.

AU - Aigrain, Louise

AU - Alcolea-Medina, Adela

AU - Alikhan, Nabil Fareed

AU - Allara, Elias

AU - Amato, Roberto

AU - Annett, Tara

AU - Aplin, Stephen

AU - Ariani, Cristina V.

AU - Asad, Hibo

AU - Ash, Amy

AU - Ashfield, Paula

AU - Ashford, Fiona

AU - Atkinson, Laura

AU - Attwood, Stephen W.

AU - Auckland, Cressida

AU - Aydin, Alp

AU - Baker, David J.

AU - Baker, Paul

AU - Balcazar, Carlos E.

AU - Ball, Jonathan

AU - Barrett, Jeffrey C.

AU - Barrow, Magdalena

AU - Barton, Edward

AU - Bashton, Matthew

AU - Bassett, Andrew R.

AU - Batra, Rahul

AU - Baxter, Chris

AU - Bayzid, Nadua

AU - Beaver, Charlotte

AU - Beckett, Angela H.

AU - Beckwith, Shaun M.

AU - Bedford, Luke

AU - Beer, Robert

AU - Beggs, Andrew

AU - Bellis, Katherine L.

AU - Berry, Louise

AU - Bertolusso, Beatrice

AU - Best, Angus

AU - Betteridge, Emma

AU - Bibby, David

AU - Bicknell, Kelly

AU - Binns, Debbie

AU - Birchley, Alec

AU - Bird, Paul W.

AU - Bishop, Chloe

AU - Blacow, Rachel

AU - Blakey, Victoria

AU - Blane, Beth

AU - Bolt, Frances

AU - Bonfield, James

AU - Bonner, Stephen

AU - Bonsall, David

AU - Boswell, Tim

AU - Bosworth, Andrew

AU - Bourgeois, Yann

AU - Boyd, Olivia

AU - Bradley, Declan T.

AU - Breen, Cassie

AU - Bresner, Catherine

AU - Breuer, Judith

AU - Bridgett, Stephen

AU - Bronner, Iraad F.

AU - Brooks, Ellena

AU - Broos, Alice

AU - Brown, Julianne R.

AU - Bucca, Giselda

AU - Buchan, Sarah L.

AU - Buck, David

AU - Bull, Matthew

AU - Burns, Phillipa J.

AU - Burton-Fanning, Shirelle

AU - Byaruhanga, Timothy

AU - Byott, Matthew

AU - Campbell, Sharon

AU - Carabelli, Alessandro M.

AU - Cargill, James S.

AU - Carlile, Matthew

AU - Carvalho, Silvia F.

AU - Casey, Anna

AU - Castigador, Anibolina

AU - Catalan, Jana

AU - Chalker, Vicki

AU - Chaloner, Nicola J.

AU - Chand, Meera

AU - Chappell, Joseph G.

AU - Charalampous, Themoula

AU - Chatterton, Wendy

AU - Chaudhry, Yasmin

AU - Churcher, Carol M.

AU - Clark, Gemma

AU - Clarke, Phillip

AU - Cogger, Benjamin J.

AU - Cole, Kevin

AU - Collins, Jennifer

AU - Colquhoun, Rachel

AU - Connor, Thomas R.

AU - Cook, Kate F.

AU - Coombes, Jason

AU - Corden, Sally

AU - Cormie, Claire

AU - Cortes, Nicholas

AU - Cotic, Marius

AU - Cotton, Seb

AU - Cottrell, Simon

AU - Coupland, Lindsay

AU - Cox, MacGregor

AU - Cox, Alison

AU - Craine, Noel

AU - Crawford, Liam

AU - Cross, Aidan

AU - Crown, Matthew R.

AU - Crudgington, Dorian

AU - Cumley, Nicola

AU - Curran, Tanya

AU - Curran, Martin D.

AU - da Silva Filipe, Ana

AU - Dabrera, Gavin

AU - Darby, Alistair C.

AU - Davidson, Rose K.

AU - Davies, Alisha

AU - Davies, Robert M.

AU - Davis, Thomas

AU - de Angelis, Daniela

AU - De Lacy, Elen

AU - de Oliveira Martins, Leonardo

AU - Debebe, Johnny

AU - Denton-Smith, Rebecca

AU - Dervisevic, Samir

AU - Dewar, Rebecca

AU - Dey, Jayasree

AU - Dias, Joana

AU - Dobie, Donald

AU - Dorman, Matthew J.

AU - Downing, Fatima

AU - Driscoll, Megan

AU - du Plessis, Louis

AU - Duckworth, Nichola

AU - Durham, Jillian

AU - Eastick, Kirstine

AU - Easton, Lisa J.

AU - Eccles, Richard

AU - Edgeworth, Jonathan

AU - Edwards, Sue

AU - El Bouzidi, Kate

AU - Eldirdiri, Sahar

AU - Ellaby, Nicholas

AU - Elliott, Scott

AU - Eltringham, Gary

AU - Ensell, Leah

AU - Erkiert, Michelle J.

AU - Zamudio, Marina Escalera

AU - Essex, Sarah

AU - Evans, Johnathan M.

AU - Evans, Cariad

AU - Everson, William

AU - Fairley, Derek J.

AU - Fallon, Karlie

AU - Fanaie, Arezou

AU - Farr, Ben W.

AU - Fearn, Christopher

AU - Feltwell, Theresa

AU - Ferguson, Lynne

AU - Fina, Laia

AU - Flaviani, Flavia

AU - Fleming, Vicki M.

AU - Forrest, Sally

AU - Foster-Nyarko, Ebenezer

AU - Foulkes, Benjamin H.

AU - Foulser, Luke

AU - Fragakis, Mireille

AU - Frampton, Dan

AU - Francois, Sarah

AU - Fraser, Christophe

AU - Freeman, Timothy M.

AU - Fryer, Helen

AU - Fuchs, Marc

AU - Fuller, William

AU - Gajee, Kavitha

AU - Galai, Katerina

AU - Gallagher, Abbie

AU - Gallagher, Eileen

AU - Gallagher, Michael D.

AU - Gallis, Marta

AU - Gaskin, Amy

AU - Gatica-Wilcox, Bree

AU - Geidelberg, Lily

AU - Gemmell, Matthew

AU - Georgana, Iliana

AU - George, Ryan P.

AU - Gifford, Laura

AU - Gilbert, Lauren

AU - Girgis, Sophia T.

AU - Glaysher, Sharon

AU - Goldstein, Emily J.

AU - Golubchik, Tanya

AU - Gomes, Andrea N.

AU - Gonçalves, Sónia

AU - Goodfellow, Ian G.

AU - Goodwin, Scott

AU - Goudarzi, Salman

AU - Gourtovaia, Marina

AU - Graham, Clive

AU - Graham, Lee

AU - Grant, Paul R.

AU - Green, Luke R.

AU - Green, Angie

AU - Greenaway, Jane

AU - Gregory, Richard

AU - Guest, Martyn

AU - Gunson, Rory N.

AU - Gupta, Ravi K.

AU - Gutierrez, Bernardo

AU - Haldenby, Sam T.

AU - Hamilton, William L.

AU - Hansford, Samantha E.

AU - Haque, Tanzina

AU - Harris, Kathryn A.

AU - Harrison, Ian

AU - Harrison, Ewan M.

AU - Hart, Jennifer

AU - Hartley, John A.

AU - Harvey, William T.

AU - Harvey, Matthew

AU - Hassan-Ibrahim, Mohammed O.

AU - Heaney, Judith

AU - Helmer, Thomas

AU - Henderson, John H.

AU - Hesketh, Andrew R.

AU - Hey, Jessica

AU - Heyburn, David

AU - Higginson, Ellen E.

AU - Hill, Verity

AU - Hill, Jack D.

AU - Hilson, Rachel A.

AU - Hilvers, Ember

AU - Holden, Matthew T.G.

AU - Hollis, Amy

AU - Holmes, Christopher W.

AU - Holmes, Nadine

AU - Holmes, Alison H.

AU - Hopes, Richard

AU - Hornsby, Hailey R.

AU - Hosmillo, Myra

AU - Houlihan, Catherine

AU - Howson-Wells, Hannah C.

AU - Hubb, Jonathan

AU - Huckson, Hannah

AU - Hughes, Warwick

AU - Hughes, Joseph

AU - Hughes, Margaret

AU - Hutchings, Stephanie

AU - Idle, Giles

AU - Illingworth, Chris J.

AU - Impey, Robert

AU - Irish-Tavares, Dianne

AU - Iturriza-Gomara, Miren

AU - Izuagbe, Rhys

AU - Jackson, Chris

AU - Jackson, Ben

AU - Jackson, Leigh M.

AU - Jackson, Kathryn A.

AU - Jackson, David K.

AU - Jahun, Aminu S.

AU - James, Victoria

AU - James, Keith

AU - Jeanes, Christopher

AU - Jeffries, Aaron R.

AU - Jeremiah, Sarah

AU - Jermy, Andrew

AU - John, Michaela

AU - Johnson, Rob

AU - Johnson, Kate

AU - Johnston, Ian

AU - Jones, Owen

AU - Jones, Sophie

AU - Jones, Hannah

AU - Jones, Christopher R.

AU - Jones, Neil

AU - Joseph, Amelia

AU - Judges, Sarah

AU - Kay, Gemma L.

AU - Kay, Sally

AU - Keatley, Jon Paul

AU - Keeley, Alexander J.

AU - Kenyon, Anita

AU - Kermack, Leanne M.

AU - Khakh, Manjinder

AU - Kidd, Stephen P.

AU - Kimuli, Maimuna

AU - Kirk, Stuart

AU - Kitchen, Christine

AU - Kitchman, Katie

AU - Knight, Bridget A.

AU - Koshy, Cherian

AU - Kraemer, Moritz U.G.

AU - Kumziene-Summerhayes, Sara

AU - Kwiatkowski, Dominic

AU - Lackenby, Angie

AU - Laing, Kenneth G.

AU - Lampejo, Temi

AU - Langford, Cordelia F.

AU - Lavin, Deborah

AU - Lawton, Andrew I.

AU - Lee, Jack

AU - Lee, David

AU - Lensing, Stefanie V.

AU - Leonard, Steven

AU - Levett, Lisa J.

AU - Le-Viet, Thanh

AU - Lewis, Jonathan

AU - Lewis, Kevin

AU - Liddle, Jennifier

AU - Liggett, Steven

AU - Lillie, Patrick J.

AU - Lister, Michelle M.

AU - Livett, Rich

AU - Lo, Stephanie

AU - Loman, Nicholas J.

AU - Loose, Matthew W.

AU - Louka, Stavroula F.

AU - Loveson, Katie F.

AU - Lowdon, Sarah

AU - Lowe, Hannah

AU - Lowe, Helen L.

AU - Lucaci, Anita O.

AU - Ludden, Catherine

AU - Lynch, Jessica

AU - Lyons, Ronan A.

AU - Lythgoe, Katrina

AU - Machin, Nicholas W.

AU - MacIntyre-Cockett, George

AU - Mack, Andrew

AU - Macklin, Ben

AU - Maclean, Alasdair

AU - Macnaughton, Emily

AU - Madona, Pinglawathee

AU - Maes, Mailis

AU - Maftei, Laurentiu

AU - Mahanama, Adhyana I.K.

AU - Mahungu, Tabitha W.

AU - Mair, Daniel

AU - Maksimovic, Joshua

AU - Malone, Cassandra S.

AU - Maloney, Daniel

AU - Manesis, Nikos

AU - Manley, Robin

AU - Mantzouratou, Anna

AU - Marchbank, Angela

AU - Mariappan, Arun

AU - Martincorena, Inigo

AU - Martinez Nunez, Rocio T.

AU - Mather, Alison E.

AU - Maxwell, Patrick

AU - Mayhew, Megan

AU - Mbisa, Tamyo

AU - McCann, Clare M.

AU - McCarthy, Shane A.

AU - McCluggage, Kathryn

AU - McClure, Patrick C.

AU - McCrone, J. T.

AU - McHugh, Martin P.

AU - McKenna, James P.

AU - McKerr, Caoimhe

AU - McManus, Georgina M.

AU - McMurray, Claire L.

AU - McMurray, Claire

AU - McNally, Alan

AU - Meadows, Lizzie

AU - Medd, Nathan

AU - Megram, Oliver

AU - Menegazzo, Mirko

AU - Merrick, Ian

AU - Michell, Stephen L.

AU - Michelsen, Michelle L.

AU - Mirfenderesky, Mariyam

AU - Mirza, Jeremy

AU - Miskelly, Julia

AU - Moles-Garcia, Emma

AU - Moll, Robin J.

AU - Molnar, Zoltan

AU - Monahan, Irene M.

AU - Mondani, Matteo

AU - Mookerjee, Siddharth

AU - Moore, Christopher

AU - Moore, Jonathan

AU - Moore, Nathan

AU - Moore, Catherine

AU - Morcrette, Helen

AU - Morgan, Sian

AU - Morgan, Mari

AU - Mori, Matilde

AU - Morriss, Arthur

AU - Moses, Samuel

AU - Mower, Craig

AU - Muir, Peter

AU - Mukaddas, Afrida

AU - Munemo, Florence

AU - Munn, Robert

AU - Murray, Abigail

AU - Murray, Leanne J.

AU - Murray, Darren R.

AU - Mutingwende, Manasa

AU - Myers, Richard

AU - Nastouli, Eleni

AU - Nebbia, Gaia

AU - Nelson, Andrew

AU - Nelson, Charlotte

AU - Nicholls, Sam

AU - Nichols, Jenna

AU - Nicodemi, Roberto

AU - Nomikou, Kyriaki

AU - O'Grady, Justin

AU - O'Brien, Sarah

AU - Odedra, Mina

AU - Ohemeng-Kumi, Natasha

AU - Oliver, Karen

AU - Orton, Richard J.

AU - Osman, Husam

AU - xeine O'Toole, O'Toole

AU - Pacchiarini, Nicole

AU - Padgett, Debra

AU - Page, Andrew J.

AU - Park, Emily J.

AU - Park, Naomi R.

AU - Parmar, Surendra

AU - Partridge, David G.

AU - Pascall, David

AU - Patel, Amita

AU - Patel, Bindi

AU - Paterson, Steve

AU - Payne, Brendan A.I.

AU - Peacock, Sharon J.

AU - Pearson, Clare

AU - Pelosi, Emanuela

AU - Percival, Benita

AU - Perkins, Jon

AU - Perry, Malorie

AU - Pinckert, Malte L.

AU - Platt, Steven

AU - Podplomyk, Olga

AU - Pohare, Manoj

AU - Pond, Marcus

AU - Pope, Cassie F.

AU - Poplawski, Radoslaw

AU - Powell, Jessica

AU - Poyner, Jennifer

AU - Prestwood, Liam

AU - Price, Anna

AU - Price, James R.

AU - Prieto, Jacqui A.

AU - Pritchard, David T.

AU - Prosolek, Sophie J.

AU - Pugh, Georgia

AU - Pusok, Monika

AU - Pybus, Oliver G.

AU - Pymont, Hannah M.

AU - Quail, Michael A.

AU - Quick, Joshua

AU - Radulescu, Clara

AU - Raghwani, Jayna

AU - Ragonnet-Cronin, Manon

AU - Rainbow, Lucille

AU - Rajan, Diana

AU - Rajatileka, Shavanthi

AU - Ramadan, Newara A.

AU - Rambaut, Andrew

AU - Ramble, John

AU - Randell, Paul A.

AU - Randell, Paul

AU - Ratcliffe, Liz

AU - Raviprakash, Veena

AU - Raza, Mohammad

AU - Redshaw, Nicholas M.

AU - Rey, Sara

AU - Reynolds, Nicola

AU - Richter, Alex

AU - Robertson, David L.

AU - Robinson, Esther

AU - Robson, Samuel C.

AU - Rogan, Fiona

AU - Rooke, Stefan

AU - Rowe, Will

AU - Roy, Sunando

AU - Rudder, Steven

AU - Ruis, Chris

AU - Rushton, Steven

AU - Ryan, Felicity

AU - Saeed, Kordo

AU - Samaraweera, Buddhini

AU - Sambles, Christine M.

AU - Sanderson, Roy

AU - Sanderson, Theo

AU - Sang, Fei

AU - Sass, Thea

AU - Scher, Emily

AU - Scott, Garren

AU - Scott, Carol

AU - Sehmi, Jasveen

AU - Shaaban, Sharif

AU - Shah, Divya

AU - Shaw, Jessica

AU - Shelest, Ekaterina

AU - Shepherd, James G.

AU - Sheridan, Liz A.

AU - Sheriff, Nicola

AU - Shirley, Lesley

AU - Sillitoe, John

AU - Silviera, Siona

AU - Simpson, David A.

AU - Singh, Aditi

AU - Singleton, Dawn

AU - Skvortsov, Timofey

AU - Sloan, Tim J.

AU - Sluga, Graciela

AU - Smith, Ken

AU - Smith, Kim S.

AU - Smith, Perminder

AU - Smith, Darren L.

AU - Smith, Louise

AU - Smith, Colin P.

AU - Smith, Nikki

AU - Smollett, Katherine L.

AU - Snell, Luke B.

AU - Somassa, Thomas

AU - Southgate, Joel

AU - Spellman, Karla

AU - Spencer Chapman, Michael H.

AU - Spurgin, Lewis G.

AU - Spyer, Moira J.

AU - Stanley, Rachael

AU - Stanley, William

AU - Stanton, Thomas D.

AU - Starinskij, Igor

AU - Stockton, Joanne

AU - Stonehouse, Susanne

AU - Storey, Nathaniel

AU - Studholme, David J.

AU - Sudhanva, Malur

AU - Swindells, Emma

AU - Taha, Yusri

AU - Tan, Ngee Keong

AU - Tang, Julian W.

AU - Tang, Miao

AU - Taylor, Ben E.W.

AU - Taylor, Joshua F.

AU - Taylor, Sarah

AU - Temperton, Ben

AU - Templeton, Kate E.

AU - Thomas, Claire

AU - Thomson, Laura

AU - Thomson, Emma C.

AU - Thornton, Alicia

AU - Thurston, Scott A.J.

AU - Todd, John A.

AU - Tomb, Rachael

AU - Tong, Lily

AU - Tonkin-Hill, Gerry

AU - Torok, M. Estee

AU - Tovar-Corona, Jaime M.

AU - Trebes, Amy

AU - Trotter, Alexander J.

AU - Tsatsani, Ioulia

AU - Turnbull, Robyn

AU - Twohig, Katherine A.

AU - Umpleby, Helen

AU - Underwood, Anthony P.

AU - Vamos, Edith E.

AU - Vasylyeva, Tetyana I.

AU - Vattipally, Sreenu

AU - Vernet, Gabrielle

AU - Vipond, Barry B.

AU - Volz, Erik M.

AU - Walsh, Sarah

AU - Wang, Dennis

AU - Warne, Ben

AU - Warwick-Dugdale, Joanna

AU - Wastnedge, Elizabeth

AU - Watkins, Joanne

AU - Watson, Louisa K.

AU - Waugh, Sheila

AU - Webster, Hermione J.

AU - Weldon, Danni

AU - Westwick, Elaine

AU - Whalley, Thomas

AU - Wheeler, Helen

AU - Whitehead, Mark

AU - Whiteley, Max

AU - Whitwham, Andrew

AU - Wierzbicki, Claudia

AU - Willford, Nicholas J.

AU - Williams, Lesley Anne

AU - Williams, Rebecca

AU - Williams, Cheryl

AU - Williams, Chris

AU - Williams, Charlotte A.

AU - Williams, Rachel J.

AU - Williams, Thomas

AU - Williams, Catryn

AU - Williamson, Kathleen A.

AU - Wilson-Davies, Eleri

AU - Witele, Eric

AU - Withell, Karen T.

AU - Witney, Adam A.

AU - Wolverson, Paige

AU - Wong, Nick

AU - Workman, Trudy

AU - Wright, Victoria

AU - Wright, Derek W.

AU - Wyatt, Tim

AU - Wyllie, Sarah

AU - Xu-McCrae, Li

AU - Yavus, Mehmet

AU - Yaze, Geraldine

AU - Yeats, Corin A.

AU - Yebra, Gonzalo

AU - Yew, Wen C.

AU - Young, Gregory R.

AU - Young, Jamie

AU - Zarebski, Alex E.

AU - Zhang, Peijun

AU - Maini, Mala K.

AU - Ogg, Graham

AU - Knight, Julian C.

AU - Baillie, J. Kenneth

AU - Semple, Malcolm G.

AU - Openshaw, Peter J.M.

AU - Carson, Gail

AU - Alex, Beatrice

AU - Andrikopoulos, Petros

AU - Bach, Benjamin

AU - Barclay, Wendy S.

AU - Bogaert, Debby

AU - Chechi, Kanta

AU - Cooke, Graham S.

AU - Docherty, Annemarie B.

AU - Correia, Gonçalo dos Santos

AU - Dumas, Marc Emmanuel

AU - Dunning, Jake

AU - Fletcher, Tom

AU - Green, Christopher A.

AU - Greenhalf, William

AU - Griffin, Julian L.

AU - Gupta, Rishi K.

AU - Harrison, Ewen M.

AU - Hiscox, Julian A.

AU - Wai Ho, Antonia Ying

AU - Horby, Peter W.

AU - Ijaz, Samreen

AU - Khoo, Saye

AU - Klenerman, Paul

AU - Law, Andrew

AU - Lewis, Matthew R.

AU - Liggi, Sonia

AU - Lim, Wei Shen

AU - Maslen, Lynn

AU - Merson, Laura

AU - Meynert, Alison M.

AU - Noursadeghi, Mahdad

AU - Olanipekun, Michael

AU - Osagie, Anthonia

AU - Palmarini, Massimo

AU - Palmieri, Carlo

AU - Paxton, William A.

AU - Pollakis, Georgios

AU - Price, Nicholas

AU - Russell, Clark D.

AU - Sancho-Shimizu, Vanessa

AU - Sands, Caroline J.

AU - Scott, Janet T.

AU - Sigfrid, Louise

AU - Solomon, Tom

AU - Sriskandan, Shiranee

AU - Stuart, David

AU - Summers, Charlotte

AU - Swann, Olivia V.

AU - Takats, Zoltan

AU - Takis, Panteleimon

AU - Tedder, Richard S.

AU - Thompson, A. A.Roger

AU - Thwaites, Ryan S.

AU - Zambon, Maria

AU - Hardwick, Hayley

AU - Donohue, Chloe

AU - Griffiths, Fiona

AU - Oosthuyzen, Wilna

AU - Donegan, Cara

AU - Spencer, Rebecca G.

AU - Dalton, Jo

AU - Girvan, Michelle

AU - Saviciute, Egle

AU - Roberts, Stephanie

AU - Harrison, Janet

AU - Marsh, Laura

AU - Connor, Marie

AU - Halpin, Sophie

AU - Jackson, Clare

AU - Gamble, Carrol

AU - Plotkin, Daniel

AU - Lee, James

AU - Leeming, Gary

AU - Wham, Murray

AU - Clohisey, Sara

AU - Hendry, Ross

AU - Scott-Brown, James

AU - Shaw, Victoria

AU - McDonald, Sarah

AU - Keating, Seán

AU - Ahmed, Katie A.

AU - Armstrong, Jane A.

AU - Ashworth, Milton

AU - Asiimwe, Innocent G.

AU - Bakshi, Siddharth

AU - Barlow, Samantha L.

AU - Booth, Laura

AU - Brennan, Benjamin

AU - Bullock, Katie

AU - Catterall, Benjamin W.A.

AU - Clark, Jordan J.

AU - Clarke, Emily A.

AU - Cole, Sarah

AU - Cooper, Louise

AU - Cox, Helen

AU - Davis, Christopher

AU - Dincarslan, Oslem

AU - Dunn, Chris

AU - Dyer, Philip

AU - Elliott, Angela

AU - Evans, Anthony

AU - Finch, Lorna

AU - Fisher, Lewis W.S.

AU - Foster, Terry

AU - Garcia-Dorival, Isabel

AU - Gunning, Philip

AU - Hartley, Catherine

AU - Jensen, Rebecca L.

AU - Jones, Christopher B.

AU - Jones, Trevor R.

AU - Khandaker, Shadia

AU - King, Katharine

AU - Kiy, Robyn T.

AU - Koukorava, Chrysa

AU - Lake, Annette

AU - Lant, Suzannah

AU - Latawiec, Diane

AU - Lavelle-Langham, Lara

AU - Lefteri, Daniella

AU - Lett, Lauren

AU - Livoti, Lucia A.

AU - Mancini, Maria

AU - McDonald, Sarah

AU - McEvoy, Laurence

AU - McLauchlan, John

AU - Metelmann, Soeren

AU - Miah, Nahida S.

AU - Middleton, Joanna

AU - Mitchell, Joyce

AU - Murphy, Ellen G.

AU - Penrice-Randal, Rebekah

AU - Pilgrim, Jack

AU - Prince, Tessa

AU - Reynolds, Will

AU - Ridley, P. Matthew

AU - Sales, Debby

AU - Shaw, Victoria E.

AU - Shears, Rebecca K.

AU - Small, Benjamin

AU - Subramaniam, Krishanthi S.

AU - Szemiel, Agnieska

AU - Taggart, Aislynn

AU - Tanianis-Hughes, Jolanta

AU - Thomas, Jordan

AU - Trochu, Erwan

AU - van Tonder, Libby

AU - Wilcock, Eve

AU - Zhang, J. Eunice

AU - Flaherty, Lisa

AU - Maziere, Nicole

AU - Cass, Emily

AU - Carracedo, Alejandra Doce

AU - Carlucci, Nicola

AU - Holmes, Anthony

AU - Massey, Hannah

AU - Murphy, Lee

AU - Wrobel, Nicola

AU - McCafferty, Sarah

AU - Morrice, Kirstie

AU - MacLean, Alan

AU - Adeniji, Kayode

AU - Agranoff, Daniel

AU - Agwuh, Ken

AU - Ail, Dhiraj

AU - Aldera, Erin L.

AU - Alegria, Ana

AU - Allen, Sam

AU - Angus, Brian

AU - Ashish, Abdul

AU - Atkinson, Dougal

AU - Bari, Shahedal

AU - Barlow, Gavin

AU - Barnass, Stella

AU - Barrett, Nicholas

AU - Bassford, Christopher

AU - Basude, Sneha

AU - Baxter, David

AU - Beadsworth, Michael

AU - Bernatoniene, Jolanta

AU - Berridge, John

AU - Berry, Colin

AU - Best, Nicola

AU - Bothma, Pieter

AU - Chadwick, David

AU - Brittain-Long, Robin

AU - Bulteel, Naomi

AU - Burden, Tom

AU - Burtenshaw, Andrew

AU - Caruth, Vikki

AU - Chambler, Duncan

AU - Chee, Nigel

AU - Child, Jenny

AU - Chukkambotla, Srikanth

AU - Clark, Tom

AU - Collini, Paul

AU - Cosgrove, Catherine

AU - Cupitt, Jason

AU - Cutino-Moguel, Maria Teresa

AU - Dark, Paul

AU - Dawson, Chris

AU - Donnison, Phil

AU - Douthwaite, Sam

AU - Drummond, Andrew

AU - DuRand, Ingrid

AU - Dushianthan, Ahilanadan

AU - Dyer, Tristan

AU - Eziefula, Chi

AU - Fegan, Chrisopher

AU - Finn, Adam

AU - Fullerton, Duncan

AU - Garg, Sanjeev

AU - Garg, Atul

AU - Gkrania-Klotsas, Effrossyni

AU - Godden, Jo

AU - Goldsmith, Arthur

AU - Hardy, Elaine

AU - Hartshorn, Stuart

AU - Harvey, Daniel

AU - Havalda, Peter

AU - Hawcutt, Daniel B.

AU - Hobrok, Maria

AU - Hodgson, Luke

AU - Hormis, Anil

AU - Jacobs, Michael

AU - Jain, Susan

AU - Jennings, Paul

AU - Kaliappan, Agilan

AU - Kasipandian, Vidya

AU - Kegg, Stephen

AU - Kelsey, Michael

AU - Kendall, Jason

AU - Kerrison, Caroline

AU - Kerslake, Ian

AU - Koch, Oliver

AU - Koduri, Gouri

AU - Koshy, George

AU - Laha, Shondipon

AU - Laird, Steven

AU - Larkin, Susan

AU - Leiner, Tamas

AU - Lillie, Patrick

AU - Limb, James

AU - Linnett, Vanessa

AU - Little, Jeff

AU - Lyttle, Mark

AU - MacMahon, Michael

AU - Mankregod, Ravish

AU - Masson, Huw

AU - Matovu, Elijah

AU - McCullough, Katherine

AU - McEwen, Ruth

AU - Meda, Manjula

AU - Mills, Gary

AU - Minton, Jane

AU - Mohandas, Kavya

AU - Mok, Quen

AU - Moon, James

AU - Moore, Elinoor

AU - Morgan, Patrick

AU - Morris, Craig

AU - Mortimore, Katherine

AU - Mpenge, Mbiye

AU - Mulla, Rohinton

AU - Murphy, Michael

AU - Nagel, Megan

AU - Nagarajan, Thapas

AU - Nelson, Mark

AU - Norris, Lillian

AU - O'Shea, Matthew K.

AU - Otahal, Igor

AU - Ostermann, Marlies

AU - Pais, Mark

AU - Panchatsharam, Selva

AU - Papakonstantinou, Danai

AU - Paraiso, Hassan

AU - Patel, Brij

AU - Pattison, Natalie

AU - Pepperell, Justin

AU - Peters, Mark

AU - Phull, Mandeep

AU - Pintus, Stefania

AU - Pooni, Jagtur Singh

AU - Planche, Tim

AU - Post, Frank

AU - Price, David

AU - Prout, Rachel

AU - Rae, Nikolas

AU - Reschreiter, Henrik

AU - Reynolds, Tim

AU - Richardson, Neil

AU - Roberts, Mark

AU - Roberts, Devender

AU - Rose, Alistair

AU - Rousseau, Guy

AU - Ruge, Bobby

AU - Ryan, Brendan

AU - Saluja, Taranprit

AU - Schmid, Matthias L.

AU - Shah, Aarti

AU - Shanmuga, Prad

AU - Sharma, Anil

AU - Shawcross, Anna

AU - Sizer, Jeremy

AU - Shankar-Hari, Manu

AU - Smith, Richard

AU - Snelson, Catherine

AU - Spittle, Nick

AU - Staines, Nikki

AU - Stambach, Tom

AU - Stewart, Richard

AU - Subudhi, Pradeep

AU - Szakmany, Tamas

AU - Tatham, Kate

AU - Thomas, Jo

AU - Thompson, Chris

AU - Thompson, Robert

AU - Tridente, Ascanio

AU - Tupper-Carey, Darell

AU - Twagira, Mary

AU - Vallotton, Nick

AU - Vancheeswaran, Rama

AU - Vincent-Smith, Lisa

AU - Visuvanathan, Shico

AU - Vuylsteke, Alan

AU - Waddy, Sam

AU - Wake, Rachel

AU - Walden, Andrew

AU - Welters, Ingeborg

AU - Whitehouse, Tony

AU - Whittaker, Paul

AU - Whittington, Ashley

AU - Papineni, Padmasayee

AU - Wijesinghe, Meme

AU - Williams, Martin

AU - Wilson, Lawrence

AU - Winchester, Stephen

AU - Wiselka, Martin

AU - Wolverson, Adam

AU - Wootton, Daniel G.

AU - Workman, Andrew

AU - Yates, Bryan

AU - Young, Peter

AU - Peng, Yanchun

AU - Rowland-Jones, Sarah L.

AU - Dong, Tao

N1 - Funding Information: This work is supported by the UK Medical Research Council (MRC); Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (CIFMS), China; National Institute for Health Research (NIHR) Oxford Biomedical Research Centre , and UK Research and Innovation (UKRI)/NIHR through the UK Coronavirus Immunology Consortium (UK-CIC). Sequencing of SARS-CoV-2 samples and collation of data was undertaken by the COG-UK CONSORTIUM. COG-UK is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR), and Genome Research Limited , operating as the Wellcome Sanger Institute. T.I.d.S. is supported by a Wellcome Trust Intermediate Clinical Fellowship ( 110058/Z/15/Z ). L.T. is supported by the Wellcome Trust (grant number 205228/Z/16/Z ) and by the University of Liverpool Centre for Excellence in Infectious Disease Research (CEIDR). S.D. is funded by an NIHR Global Research Professorship ( NIHR300791 ). L.T. and S.C.M. are also supported by the U.S. Food and Drug Administration Medical Countermeasures Initiative contract 75F40120C00085 and the National Institute for Health Research Health Protection Research Unit (HPRU) in Emerging and Zoonotic Infections ( NIHR200907 ) at University of Liverpool in partnership with Public Health England (PHE), in collaboration with Liverpool School of Tropical Medicine and the University of Oxford. L.T. is based at the University of Liverpool. M.D.P. is funded by the NIHR Sheffield Biomedical Research Centre (BRC – IS-BRC-1215-20017). ISARIC4C is supported by the MRC (grant no MC_PC_19059 ). J.C.K. is a Wellcome Investigator ( WT204969/Z/16/Z ) and supported by NIHR Oxford Biomedical Research Centre and CIFMS . The views expressed are those of the authors and not necessarily those of the NIHR or MRC. Funding Information: This work is supported by the UK Medical Research Council (MRC); Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (CIFMS), China; National Institute for Health Research (NIHR) Oxford Biomedical Research Centre, and UK Research and Innovation (UKRI)/NIHR through the UK Coronavirus Immunology Consortium (UK-CIC). Sequencing of SARS-CoV-2 samples and collation of data was undertaken by the COG-UK CONSORTIUM. COG-UK is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR), and Genome Research Limited, operating as the Wellcome Sanger Institute. T.I.d.S. is supported by a Wellcome Trust Intermediate Clinical Fellowship (110058/Z/15/Z). L.T. is supported by the Wellcome Trust (grant number 205228/Z/16/Z) and by the University of Liverpool Centre for Excellence in Infectious Disease Research (CEIDR). S.D. is funded by an NIHR Global Research Professorship (NIHR300791). L.T. and S.C.M. are also supported by the U.S. Food and Drug Administration Medical Countermeasures Initiative contract 75F40120C00085 and the National Institute for Health Research Health Protection Research Unit (HPRU) in Emerging and Zoonotic Infections (NIHR200907) at University of Liverpool in partnership with Public Health England (PHE), in collaboration with Liverpool School of Tropical Medicine and the University of Oxford. L.T. is based at the University of Liverpool. M.D.P. is funded by the NIHR Sheffield Biomedical Research Centre (BRC – IS-BRC-1215-20017). ISARIC4C is supported by the MRC (grant no MC_PC_19059). J.C.K. is a Wellcome Investigator (WT204969/Z/16/Z) and supported by NIHR Oxford Biomedical Research Centre and CIFMS. The views expressed are those of the authors and not necessarily those of the NIHR or MRC. T.I.d.S. and T.D. conceptualized the project; T.D. T.I.d.S. L.T. and Y.P. designed and supervised T cell experiments; B.B.L. N.S.H. and M.D.P. conducted the viral sequence analyses; D.S. conducted the literature review and collated T cell epitope information; G.L. D.D. and S.C.M. performed experiments and analyzed the data; X.Y. Z.Y. A.A. and R.B. provided critical reagents and technical assistance; J.C.K. and A.J.M. established clinical cohorts; T.I.d.S. and T.D. wrote and edited the original draft; all co-authors reviewed and edited the manuscript. The authors have no competing interests to declare. Publisher Copyright: © 2021 The Author(s)

PY - 2021/11/19

Y1 - 2021/11/19

N2 - We identify amino acid variants within dominant SARS-CoV-2 T cell epitopes by interrogating global sequence data. Several variants within nucleocapsid and ORF3a epitopes have arisen independently in multiple lineages and result in loss of recognition by epitope-specific T cells assessed by IFN-γ and cytotoxic killing assays. Complete loss of T cell responsiveness was seen due to Q213K in the A∗01:01-restricted CD8+ ORF3a epitope FTSDYYQLY207-215; due to P13L, P13S, and P13T in the B∗27:05-restricted CD8+ nucleocapsid epitope QRNAPRITF9-17; and due to T362I and P365S in the A∗03:01/A∗11:01-restricted CD8+ nucleocapsid epitope KTFPPTEPK361-369. CD8+ T cell lines unable to recognize variant epitopes have diverse T cell receptor repertoires. These data demonstrate the potential for T cell evasion and highlight the need for ongoing surveillance for variants capable of escaping T cell as well as humoral immunity.

AB - We identify amino acid variants within dominant SARS-CoV-2 T cell epitopes by interrogating global sequence data. Several variants within nucleocapsid and ORF3a epitopes have arisen independently in multiple lineages and result in loss of recognition by epitope-specific T cells assessed by IFN-γ and cytotoxic killing assays. Complete loss of T cell responsiveness was seen due to Q213K in the A∗01:01-restricted CD8+ ORF3a epitope FTSDYYQLY207-215; due to P13L, P13S, and P13T in the B∗27:05-restricted CD8+ nucleocapsid epitope QRNAPRITF9-17; and due to T362I and P365S in the A∗03:01/A∗11:01-restricted CD8+ nucleocapsid epitope KTFPPTEPK361-369. CD8+ T cell lines unable to recognize variant epitopes have diverse T cell receptor repertoires. These data demonstrate the potential for T cell evasion and highlight the need for ongoing surveillance for variants capable of escaping T cell as well as humoral immunity.

KW - Immune response

KW - Immunology

KW - Molecular biology

KW - Phylogenetics

KW - Virology

UR - http://www.scopus.com/inward/record.url?scp=85118773166&partnerID=8YFLogxK

U2 - 10.1016/j.isci.2021.103353

DO - 10.1016/j.isci.2021.103353

M3 - Article

AN - SCOPUS:85118773166

SN - 2589-0042

VL - 24

JO - iScience

JF - iScience

IS - 11

M1 - 103353

ER -

The impact of viral mutations on recognition by SARS-CoV-2 specific T cells

Abstract / Description of output

Keywords / Materials (for Non-textual outputs)

Access to Document

Other files and links

Fingerprint

Bioinformatics Analysis Core

Genetics Core, Edinburgh Clinical Research Facility

Cite this

The impact of viral mutations on recognition by SARS-CoV-2 specific T cells

Abstract / Description of output

Keywords / Materials (for Non-textual outputs)

Access to Document

Other files and links

Fingerprint

Equipment

Bioinformatics Analysis Core

Genetics Core, Edinburgh Clinical Research Facility

Cite this