The genomic and evolutionary landscapes of anaplastic thyroid carcinoma

Peter Y.F. Zeng; Stephenie D. Prokopec; Stephen Y. Lai; Nicole Pinto; Michelle A. Chan-Seng-Yue; Roderick Clifton-Bligh; Michelle D. Williams; Christopher J. Howlett; Paul Plantinga; Matthew J. Cecchini; Alfred K. Lam; Iram Siddiqui; Jianxin Wang; Ren X. Sun; John D. Watson; Reju Korah; Tobias Carling; Nishant Agrawal; Nicole Cipriani; Douglas Ball; Barry Nelkin; Lisa M. Rooper; Justin A. Bishop; Cathie Garnis; Ken Berean; Norman G. Nicolson; Paul Weinberger; Ying Henderson; Christopher M. Lalansingh; Mao Tian; Takafumi N. Yamaguchi; Julie Livingstone; Adriana Salcedo; Krupal Patel; Frederick Vizeacoumar; Alessandro Datti; Liu Xi; Yuri E. Nikiforov; Robert Smallridge; John A. Copland; Laura A. Marlow; Martin D. Hyrcza; Leigh Delbridge; Stan Sidhu; Mark Sywak; Bruce Robinson; Kevin Fung; Farhad Ghasemi; Keith Kwan; S. Danielle MacNeil; Adrian Mendez; David A. Palma; Mohammed I. Khan; Mushfiq Shaikh; Kara M. Ruicci; Bret Wehrli; Eric Winquist; John Yoo; Joe S. Mymryk; James W. Rocco; David Wheeler; Steve Scherer; Thomas J. Giordano; John W. Barrett; William C. Faquin; Anthony J. Gill; Gary L Clayman; Paul C. Boutros; Anthony C. Nichols

doi:10.1016/j.celrep.2024.113826

The genomic and evolutionary landscapes of anaplastic thyroid carcinoma

Peter Y.F. Zeng, Stephenie D. Prokopec, Stephen Y. Lai, Nicole Pinto, Michelle A. Chan-Seng-Yue, Roderick Clifton-Bligh, Michelle D. Williams, Christopher J. Howlett, Paul Plantinga, Matthew J. Cecchini, Alfred K. Lam, Iram Siddiqui, Jianxin Wang, Ren X. Sun, John D. Watson, Reju Korah, Tobias Carling, Nishant Agrawal, Nicole Cipriani, Douglas BallBarry Nelkin, Lisa M. Rooper, Justin A. Bishop, Cathie Garnis, Ken Berean, Norman G. Nicolson, Paul Weinberger, Ying Henderson, Christopher M. Lalansingh, Mao Tian, Takafumi N. Yamaguchi, Julie Livingstone, Adriana Salcedo, Krupal Patel, Frederick Vizeacoumar, Alessandro Datti, Liu Xi, Yuri E. Nikiforov, Robert Smallridge, John A. Copland, Laura A. Marlow, Martin D. Hyrcza, Leigh Delbridge, Stan Sidhu, Mark Sywak, Bruce Robinson, Kevin Fung, Farhad Ghasemi, Keith Kwan, S. Danielle MacNeil, Adrian Mendez, David A. Palma, Mohammed I. Khan, Mushfiq Shaikh, Kara M. Ruicci, Bret Wehrli, Eric Winquist, John Yoo, Joe S. Mymryk, James W. Rocco, David Wheeler, Steve Scherer, Thomas J. Giordano, John W. Barrett, William C. Faquin, Anthony J. Gill, Gary L Clayman, Paul C. Boutros, Anthony C. Nichols

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

Abstract

Anaplastic thyroid carcinoma is arguably the most lethal human malignancy. It often co-occurs with differentiated thyroid cancers, yet the molecular origins of its aggressivity are unknown. We sequenced tumor DNA from 329 regions of thyroid cancer, including 213 from patients with primary anaplastic thyroid carcinomas. We also whole genome sequenced 9 patients using multi-region sequencing of both differentiated and anaplastic thyroid cancer components. Using these data, we demonstrate thatanaplastic thyroid carcinomas have a higher burden of mutations than other thyroid cancers, with distinct mutational signatures and molecular subtypes. Further, different cancer driver genes are mutated in anaplastic and differentiated thyroid carcinomas, even those arising in a single patient. Finally, we unambiguously demonstrate that anaplastic thyroid carcinomas share a genomic origin with co-occurring differentiated carcinomas and emerge from a common malignant field through acquisition of characteristic clonal driver mutations.

Original language	English (US)
Article number	113826
Journal	Cell Reports
Volume	43
Issue number	3
DOIs	https://doi.org/10.1016/j.celrep.2024.113826
State	Published - Mar 26 2024

Keywords

anaplastic thyroid cancer
cancer progression
CP: Cancer
CP: Genomics
genomics
tumour evolution
tumour heterogeneity

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2024.113826

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Zeng, P. Y. F., Prokopec, S. D., Lai, S. Y., Pinto, N., Chan-Seng-Yue, M. A., Clifton-Bligh, R., Williams, M. D., Howlett, C. J., Plantinga, P., Cecchini, M. J., Lam, A. K., Siddiqui, I., Wang, J., Sun, R. X., Watson, J. D., Korah, R., Carling, T., Agrawal, N., Cipriani, N., ... Nichols, A. C. (2024). The genomic and evolutionary landscapes of anaplastic thyroid carcinoma. Cell Reports, 43(3), Article 113826. https://doi.org/10.1016/j.celrep.2024.113826

Zeng, PYF, Prokopec, SD, Lai, SY, Pinto, N, Chan-Seng-Yue, MA, Clifton-Bligh, R, Williams, MD, Howlett, CJ, Plantinga, P, Cecchini, MJ, Lam, AK, Siddiqui, I, Wang, J, Sun, RX, Watson, JD, Korah, R, Carling, T, Agrawal, N, Cipriani, N, Ball, D, Nelkin, B, Rooper, LM, Bishop, JA, Garnis, C, Berean, K, Nicolson, NG, Weinberger, P, Henderson, Y, Lalansingh, CM, Tian, M, Yamaguchi, TN, Livingstone, J, Salcedo, A, Patel, K, Vizeacoumar, F, Datti, A, Xi, L, Nikiforov, YE, Smallridge, R, Copland, JA, Marlow, LA, Hyrcza, MD, Delbridge, L, Sidhu, S, Sywak, M, Robinson, B, Fung, K, Ghasemi, F, Kwan, K, MacNeil, SD, Mendez, A, Palma, DA, Khan, MI, Shaikh, M, Ruicci, KM, Wehrli, B, Winquist, E, Yoo, J, Mymryk, JS, Rocco, JW, Wheeler, D, Scherer, S, Giordano, TJ, Barrett, JW, Faquin, WC, Gill, AJ, Clayman, GL, Boutros, PC & Nichols, AC 2024, 'The genomic and evolutionary landscapes of anaplastic thyroid carcinoma', Cell Reports, vol. 43, no. 3, 113826. https://doi.org/10.1016/j.celrep.2024.113826

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title = "The genomic and evolutionary landscapes of anaplastic thyroid carcinoma",

abstract = "Anaplastic thyroid carcinoma is arguably the most lethal human malignancy. It often co-occurs with differentiated thyroid cancers, yet the molecular origins of its aggressivity are unknown. We sequenced tumor DNA from 329 regions of thyroid cancer, including 213 from patients with primary anaplastic thyroid carcinomas. We also whole genome sequenced 9 patients using multi-region sequencing of both differentiated and anaplastic thyroid cancer components. Using these data, we demonstrate thatanaplastic thyroid carcinomas have a higher burden of mutations than other thyroid cancers, with distinct mutational signatures and molecular subtypes. Further, different cancer driver genes are mutated in anaplastic and differentiated thyroid carcinomas, even those arising in a single patient. Finally, we unambiguously demonstrate that anaplastic thyroid carcinomas share a genomic origin with co-occurring differentiated carcinomas and emerge from a common malignant field through acquisition of characteristic clonal driver mutations.",

keywords = "anaplastic thyroid cancer, cancer progression, CP: Cancer, CP: Genomics, genomics, tumour evolution, tumour heterogeneity",

author = "Zeng, {Peter Y.F.} and Prokopec, {Stephenie D.} and Lai, {Stephen Y.} and Nicole Pinto and Chan-Seng-Yue, {Michelle A.} and Roderick Clifton-Bligh and Williams, {Michelle D.} and Howlett, {Christopher J.} and Paul Plantinga and Cecchini, {Matthew J.} and Lam, {Alfred K.} and Iram Siddiqui and Jianxin Wang and Sun, {Ren X.} and Watson, {John D.} and Reju Korah and Tobias Carling and Nishant Agrawal and Nicole Cipriani and Douglas Ball and Barry Nelkin and Rooper, {Lisa M.} and Bishop, {Justin A.} and Cathie Garnis and Ken Berean and Nicolson, {Norman G.} and Paul Weinberger and Ying Henderson and Lalansingh, {Christopher M.} and Mao Tian and Yamaguchi, {Takafumi N.} and Julie Livingstone and Adriana Salcedo and Krupal Patel and Frederick Vizeacoumar and Alessandro Datti and Liu Xi and Nikiforov, {Yuri E.} and Robert Smallridge and Copland, {John A.} and Marlow, {Laura A.} and Hyrcza, {Martin D.} and Leigh Delbridge and Stan Sidhu and Mark Sywak and Bruce Robinson and Kevin Fung and Farhad Ghasemi and Keith Kwan and MacNeil, {S. Danielle} and Adrian Mendez and Palma, {David A.} and Khan, {Mohammed I.} and Mushfiq Shaikh and Ruicci, {Kara M.} and Bret Wehrli and Eric Winquist and John Yoo and Mymryk, {Joe S.} and Rocco, {James W.} and David Wheeler and Steve Scherer and Giordano, {Thomas J.} and Barrett, {John W.} and Faquin, {William C.} and Gill, {Anthony J.} and Clayman, {Gary L} and Boutros, {Paul C.} and Nichols, {Anthony C.}",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s)",

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doi = "10.1016/j.celrep.2024.113826",

language = "English (US)",

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AU - Zeng, Peter Y.F.

AU - Prokopec, Stephenie D.

AU - Lai, Stephen Y.

AU - Pinto, Nicole

AU - Chan-Seng-Yue, Michelle A.

AU - Clifton-Bligh, Roderick

AU - Williams, Michelle D.

AU - Howlett, Christopher J.

AU - Plantinga, Paul

AU - Cecchini, Matthew J.

AU - Lam, Alfred K.

AU - Siddiqui, Iram

AU - Wang, Jianxin

AU - Sun, Ren X.

AU - Watson, John D.

AU - Korah, Reju

AU - Carling, Tobias

AU - Agrawal, Nishant

AU - Cipriani, Nicole

AU - Ball, Douglas

AU - Nelkin, Barry

AU - Rooper, Lisa M.

AU - Bishop, Justin A.

AU - Garnis, Cathie

AU - Berean, Ken

AU - Nicolson, Norman G.

AU - Weinberger, Paul

AU - Henderson, Ying

AU - Lalansingh, Christopher M.

AU - Tian, Mao

AU - Yamaguchi, Takafumi N.

AU - Livingstone, Julie

AU - Salcedo, Adriana

AU - Patel, Krupal

AU - Vizeacoumar, Frederick

AU - Datti, Alessandro

AU - Xi, Liu

AU - Nikiforov, Yuri E.

AU - Smallridge, Robert

AU - Copland, John A.

AU - Marlow, Laura A.

AU - Hyrcza, Martin D.

AU - Delbridge, Leigh

AU - Sidhu, Stan

AU - Sywak, Mark

AU - Robinson, Bruce

AU - Fung, Kevin

AU - Ghasemi, Farhad

AU - Kwan, Keith

AU - MacNeil, S. Danielle

AU - Mendez, Adrian

AU - Palma, David A.

AU - Khan, Mohammed I.

AU - Shaikh, Mushfiq

AU - Ruicci, Kara M.

AU - Wehrli, Bret

AU - Winquist, Eric

AU - Yoo, John

AU - Mymryk, Joe S.

AU - Rocco, James W.

AU - Wheeler, David

AU - Scherer, Steve

AU - Giordano, Thomas J.

AU - Barrett, John W.

AU - Faquin, William C.

AU - Gill, Anthony J.

AU - Clayman, Gary L

AU - Boutros, Paul C.

AU - Nichols, Anthony C.

PY - 2024/3/26

Y1 - 2024/3/26

N2 - Anaplastic thyroid carcinoma is arguably the most lethal human malignancy. It often co-occurs with differentiated thyroid cancers, yet the molecular origins of its aggressivity are unknown. We sequenced tumor DNA from 329 regions of thyroid cancer, including 213 from patients with primary anaplastic thyroid carcinomas. We also whole genome sequenced 9 patients using multi-region sequencing of both differentiated and anaplastic thyroid cancer components. Using these data, we demonstrate thatanaplastic thyroid carcinomas have a higher burden of mutations than other thyroid cancers, with distinct mutational signatures and molecular subtypes. Further, different cancer driver genes are mutated in anaplastic and differentiated thyroid carcinomas, even those arising in a single patient. Finally, we unambiguously demonstrate that anaplastic thyroid carcinomas share a genomic origin with co-occurring differentiated carcinomas and emerge from a common malignant field through acquisition of characteristic clonal driver mutations.

AB - Anaplastic thyroid carcinoma is arguably the most lethal human malignancy. It often co-occurs with differentiated thyroid cancers, yet the molecular origins of its aggressivity are unknown. We sequenced tumor DNA from 329 regions of thyroid cancer, including 213 from patients with primary anaplastic thyroid carcinomas. We also whole genome sequenced 9 patients using multi-region sequencing of both differentiated and anaplastic thyroid cancer components. Using these data, we demonstrate thatanaplastic thyroid carcinomas have a higher burden of mutations than other thyroid cancers, with distinct mutational signatures and molecular subtypes. Further, different cancer driver genes are mutated in anaplastic and differentiated thyroid carcinomas, even those arising in a single patient. Finally, we unambiguously demonstrate that anaplastic thyroid carcinomas share a genomic origin with co-occurring differentiated carcinomas and emerge from a common malignant field through acquisition of characteristic clonal driver mutations.

KW - anaplastic thyroid cancer

KW - cancer progression

KW - CP: Cancer

KW - CP: Genomics

KW - genomics

KW - tumour evolution

KW - tumour heterogeneity

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DO - 10.1016/j.celrep.2024.113826

M3 - Article

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AN - SCOPUS:85188026350

SN - 2211-1247

VL - 43

JO - Cell Reports

JF - Cell Reports

IS - 3

M1 - 113826

ER -

The genomic and evolutionary landscapes of anaplastic thyroid carcinoma

Abstract

Keywords

ASJC Scopus subject areas

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