The genomic and evolutionary landscapes of anaplastic thyroid carcinoma
Summary: 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 a...
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-03-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724001542 |
| _version_ | 1797294292017872896 |
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| author | 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 C. 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 Clayman Paul C. Boutros Anthony C. Nichols |
| author_facet | 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 C. 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 Clayman Paul C. Boutros Anthony C. Nichols |
| author_sort | Peter Y.F. Zeng |
| collection | DOAJ |
| description | Summary: 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. |
| first_indexed | 2024-03-07T21:29:05Z |
| format | Article |
| id | doaj.art-c5a6abf2e7ba48ce977235cab50cb266 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-07T21:29:05Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-c5a6abf2e7ba48ce977235cab50cb2662024-02-27T04:19:43ZengElsevierCell Reports2211-12472024-03-01433113826The genomic and evolutionary landscapes of anaplastic thyroid carcinomaPeter Y.F. Zeng0Stephenie D. Prokopec1Stephen Y. Lai2Nicole Pinto3Michelle A. Chan-Seng-Yue4Roderick Clifton-Bligh5Michelle D. Williams6Christopher J. Howlett7Paul Plantinga8Matthew J. Cecchini9Alfred K. Lam10Iram Siddiqui11Jianxin Wang12Ren X. Sun13John D. Watson14Reju Korah15Tobias Carling16Nishant Agrawal17Nicole Cipriani18Douglas Ball19Barry Nelkin20Lisa M. Rooper21Justin A. Bishop22Cathie Garnis23Ken Berean24Norman G. Nicolson25Paul Weinberger26Ying C. Henderson27Christopher M. Lalansingh28Mao Tian29Takafumi N. Yamaguchi30Julie Livingstone31Adriana Salcedo32Krupal Patel33Frederick Vizeacoumar34Alessandro Datti35Liu Xi36Yuri E. Nikiforov37Robert Smallridge38John A. Copland39Laura A. Marlow40Martin D. Hyrcza41Leigh Delbridge42Stan Sidhu43Mark Sywak44Bruce Robinson45Kevin Fung46Farhad Ghasemi47Keith Kwan48S. Danielle MacNeil49Adrian Mendez50David A. Palma51Mohammed I. Khan52Mushfiq Shaikh53Kara M. Ruicci54Bret Wehrli55Eric Winquist56John Yoo57Joe S. Mymryk58James W. Rocco59David Wheeler60Steve Scherer61Thomas J. Giordano62John W. Barrett63William C. Faquin64Anthony J. Gill65Gary Clayman66Paul C. Boutros67Anthony C. Nichols68Department of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; London Regional Cancer Program, London, ON, Canada; Lawson Health Research Institute, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaOntario Institute for Cancer Research, Toronto, ON, Canada; Institute for Precision Health, University of California, Los Angeles, Los Angeles, CA, USA; Jonsson Comprehensive Cancer Center, University of California, Los Angeles, Los Angeles, CA, USADepartment of Head and Neck Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USADepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, CanadaOntario Institute for Cancer Research, Toronto, ON, CanadaDivision of Endocrinology, Royal North Shore Hospital, and University of Sydney, Sydney, NSW, AustraliaDepartment of Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USADepartment of Pathology, Western University, London, ON, CanadaDepartment of Pathology, Western University, London, ON, CanadaDepartment of Pathology, School of Medicine, Griffith University, Gold Coast, QLD, AustraliaDepartment of Pathology, School of Medicine, Griffith University, Gold Coast, QLD, AustraliaDepartment of Laboratory Medicine, Hospital for Sick Children, Toronto, ON, CanadaOntario Institute for Cancer Research, Toronto, ON, CanadaOntario Institute for Cancer Research, Toronto, ON, CanadaOntario Institute for Cancer Research, Toronto, ON, Canada; Institute for Precision Health, University of California, Los Angeles, Los Angeles, CA, USA; Jonsson Comprehensive Cancer Center, University of California, Los Angeles, Los Angeles, CA, USADepartment of Surgery, Yale University, New Haven, CT, USADepartment of Surgery, Yale University, New Haven, CT, USADepartment of Otolaryngology – Head and Neck Surgery, University of Chicago, Chicago, IL, USADepartment of Pathology, University of Chicago, Chicago, IL, USADivision of Endocrinology, Department of Medicine, Johns Hopkins University, Baltimore, MD, USASidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD, USADivision of Pathology, Johns Hopkins University, Baltimore, MD, USADepartment of Pathology, University of Texas Southwestern, Dallas, TX, USABC Cancer Agency, Vancouver, BC, CanadaBC Cancer Agency, Vancouver, BC, CanadaDepartment of Surgery, Yale University, New Haven, CT, USADepartment of Otolaryngology – Head and Neck Surgery, Louisiana State University Health Sciences Center, Shreveport, LA, USA; Feist-Weiller Cancer Center, Louisiana State University Health Sciences Center, Shreveport, LA, USADepartment of Head and Neck Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USAOntario Institute for Cancer Research, Toronto, ON, CanadaInstitute for Precision Health, University of California, Los Angeles, Los Angeles, CA, USA; Jonsson Comprehensive Cancer Center, University of California, Los Angeles, Los Angeles, CA, USAOntario Institute for Cancer Research, Toronto, ON, Canada; Institute for Precision Health, University of California, Los Angeles, Los Angeles, CA, USA; Jonsson Comprehensive Cancer Center, University of California, Los Angeles, Los Angeles, CA, USAOntario Institute for Cancer Research, Toronto, ON, Canada; Institute for Precision Health, University of California, Los Angeles, Los Angeles, CA, USA; Jonsson Comprehensive Cancer Center, University of California, Los Angeles, Los Angeles, CA, USAOntario Institute for Cancer Research, Toronto, ON, Canada; Department of Medical Biophysics, University of Toronto, Toronto, ON, Canada; Department of Human Genetics, University of California, Los Angeles, Los Angeles, CA, USADepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; Ontario Institute for Cancer Research, Toronto, ON, CanadaCancer Research Cluster, University of Saskatchewan, Saskatoon, SK, CanadaNetwork Biology Collaborative Centre, Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada; Department of Agricultural, Food, and Environmental Sciences, University of Perugia, Perugia, ItalyDepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USADepartment of Pathology, University of Pittsburgh Medical Center, Pittsburgh, PA, USADivision of Endocrinology, Department of Medicine, Mayo Clinic, Jacksonville, FL, USADepartment of Cancer Biology, Mayo Clinic, Jacksonville, FL, USADepartment of Cancer Biology, Mayo Clinic, Jacksonville, FL, USADepartment of Pathology and Molecular Medicine, McMaster University, Hamilton, ON, CanadaDepartment of Surgery, Royal North Shore Hospital, Sydney, NSW, Australia; University of Sydney, Sydney, NWS, AustraliaDepartment of Surgery, Royal North Shore Hospital, Sydney, NSW, Australia; University of Sydney, Sydney, NWS, AustraliaDepartment of Surgery, Royal North Shore Hospital, Sydney, NSW, Australia; University of Sydney, Sydney, NWS, AustraliaUniversity of Sydney, Sydney, NWS, Australia; Department of Endocrinology, Royal North Shore Hospital, Sydney, NSW, AustraliaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Pathology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaLondon Regional Cancer Program, London, ON, Canada; Lawson Health Research Institute, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Pathology, Western University, London, ON, CanadaLondon Regional Cancer Program, London, ON, Canada; Lawson Health Research Institute, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; Department of Oncology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; London Regional Cancer Program, London, ON, Canada; Department of Oncology, Western University, London, ON, Canada; Department of Microbiology and Immunology, Western University, London, ON, CanadaDepartment of Otolaryngology – Head and Neck Surgery, Ohio State University, Columbus, OH, USADepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USADepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USADepartment of Pathology, University of Michigan, Ann Arbor, MI, USADepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USAUniversity of Sydney, Sydney, NWS, Australia; Cancer Diagnosis and Pathology Group, Kolling Institute of Medicine, Royal North Shore Hospital, Sydney, NSW, Australia; NSW Health Pathology, Department of Anatomical Pathology, Royal North Shore Hospital, Sydney, NSW, AustraliaThe Clayman Thyroid Surgery and Thyroid Cancer Center, The Thyroid Institute, Tampa General Hospital, Tampa, FL, USADepartment of Medical Biophysics, University of Toronto, Toronto, ON, Canada; Department of Pharmacology and Toxicology, University of Toronto, Toronto, ON, Canada; Department of Human Genetics, University of California, Los Angeles, Los Angeles, CA, USA; Department of Urology, University of California, Los Angeles, Los Angeles, CA, USA; Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, University of California, Los Angeles, Los Angeles, CA, USA; Institute for Precision Health, University of California, Los Angeles, Los Angeles, CA, USA; Jonsson Comprehensive Cancer Center, University of California, Los Angeles, Los Angeles, CA, USA; Corresponding authorDepartment of Otolaryngology – Head and Neck Surgery, Western University, London, ON, Canada; London Regional Cancer Program, London, ON, Canada; Lawson Health Research Institute, London, ON, Canada; Department of Oncology, Western University, London, ON, Canada; Corresponding authorSummary: 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.http://www.sciencedirect.com/science/article/pii/S2211124724001542CP: CancerCP: Genomics |
| spellingShingle | 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 C. 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 Clayman Paul C. Boutros Anthony C. Nichols The genomic and evolutionary landscapes of anaplastic thyroid carcinoma Cell Reports CP: Cancer CP: Genomics |
| title | The genomic and evolutionary landscapes of anaplastic thyroid carcinoma |
| title_full | The genomic and evolutionary landscapes of anaplastic thyroid carcinoma |
| title_fullStr | The genomic and evolutionary landscapes of anaplastic thyroid carcinoma |
| title_full_unstemmed | The genomic and evolutionary landscapes of anaplastic thyroid carcinoma |
| title_short | The genomic and evolutionary landscapes of anaplastic thyroid carcinoma |
| title_sort | genomic and evolutionary landscapes of anaplastic thyroid carcinoma |
| topic | CP: Cancer CP: Genomics |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724001542 |
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