An integrated tumor, immune and microbiome atlas of colon cancer

<p dir="ltr">The lack of multi-omics cancer datasets with extensive follow-up information hinders the identification of accurate biomarkers of clinical outcome. In this cohort study, we performed comprehensive genomic analyses on fresh-frozen samples from 348 patients affected by pri...

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Main Author: Jessica Roelands (7516439) (author)
Other Authors: Peter J. K. Kuppen (9858902) (author), Eiman I. Ahmed (6595514) (author), Raghvendra Mall (581171) (author), Tariq Masoodi (8117702) (author), Parul Singh (191877) (author), Gianni Monaco (3411857) (author), Christophe Raynaud (1405585) (author), Noel F.C.C. de Miranda (14892242) (author), Luigi Ferraro (718764) (author), Tatiana C. Carneiro-Lobo (17449912) (author), Najeeb Syed (12561967) (author), Arun Rawat (185306) (author), Amany Awad (17449915) (author), Julie Decock (44558) (author), William Mifsud (1394) (author), Lance D. Miller (8444226) (author), Shimaa Sherif (12862990) (author), Mahmoud G. Mohamed (9327444) (author), Darawan Rinchai (742366) (author), Marc Van den Eynde (801790) (author), Rosalyn W. Sayaman (8089034) (author), Elad Ziv (1263) (author), Francois Bertucci (5851322) (author), Mahir Abdulla Petkar (14150211) (author), Stephan Lorenz (466378) (author), Lisa Sara Mathew (17886698) (author), Kun Wang (134525) (author), Selvasankar Murugesan (4376506) (author), Damien Chaussabel (26369) (author), Alexander L. Vahrmeijer (8449359) (author), Ena Wang (802) (author), Anna Ceccarelli (18317235) (author), Khalid A. Fakhro (3158862) (author), Gabriele Zoppoli (201733) (author), Alberto Ballestrero (212236) (author), Rob A.E.M. Tollenaar (14908674) (author), Francesco M. Marincola (8823902) (author), Jérôme Galon (14906664) (author), Souhaila Al Khodor (6807155) (author), Michele Ceccarelli (184154) (author), Wouter Hendrickx (44559) (author), Davide Bedognetti (2632474) (author)
Published: 2023
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_version_ 1864513507049865216
author Jessica Roelands (7516439)
author2 Peter J. K. Kuppen (9858902)
Eiman I. Ahmed (6595514)
Raghvendra Mall (581171)
Tariq Masoodi (8117702)
Parul Singh (191877)
Gianni Monaco (3411857)
Christophe Raynaud (1405585)
Noel F.C.C. de Miranda (14892242)
Luigi Ferraro (718764)
Tatiana C. Carneiro-Lobo (17449912)
Najeeb Syed (12561967)
Arun Rawat (185306)
Amany Awad (17449915)
Julie Decock (44558)
William Mifsud (1394)
Lance D. Miller (8444226)
Shimaa Sherif (12862990)
Mahmoud G. Mohamed (9327444)
Darawan Rinchai (742366)
Marc Van den Eynde (801790)
Rosalyn W. Sayaman (8089034)
Elad Ziv (1263)
Francois Bertucci (5851322)
Mahir Abdulla Petkar (14150211)
Stephan Lorenz (466378)
Lisa Sara Mathew (17886698)
Kun Wang (134525)
Selvasankar Murugesan (4376506)
Damien Chaussabel (26369)
Alexander L. Vahrmeijer (8449359)
Ena Wang (802)
Anna Ceccarelli (18317235)
Khalid A. Fakhro (3158862)
Gabriele Zoppoli (201733)
Alberto Ballestrero (212236)
Rob A.E.M. Tollenaar (14908674)
Francesco M. Marincola (8823902)
Jérôme Galon (14906664)
Souhaila Al Khodor (6807155)
Michele Ceccarelli (184154)
Wouter Hendrickx (44559)
Davide Bedognetti (2632474)
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author_facet Jessica Roelands (7516439)
Peter J. K. Kuppen (9858902)
Eiman I. Ahmed (6595514)
Raghvendra Mall (581171)
Tariq Masoodi (8117702)
Parul Singh (191877)
Gianni Monaco (3411857)
Christophe Raynaud (1405585)
Noel F.C.C. de Miranda (14892242)
Luigi Ferraro (718764)
Tatiana C. Carneiro-Lobo (17449912)
Najeeb Syed (12561967)
Arun Rawat (185306)
Amany Awad (17449915)
Julie Decock (44558)
William Mifsud (1394)
Lance D. Miller (8444226)
Shimaa Sherif (12862990)
Mahmoud G. Mohamed (9327444)
Darawan Rinchai (742366)
Marc Van den Eynde (801790)
Rosalyn W. Sayaman (8089034)
Elad Ziv (1263)
Francois Bertucci (5851322)
Mahir Abdulla Petkar (14150211)
Stephan Lorenz (466378)
Lisa Sara Mathew (17886698)
Kun Wang (134525)
Selvasankar Murugesan (4376506)
Damien Chaussabel (26369)
Alexander L. Vahrmeijer (8449359)
Ena Wang (802)
Anna Ceccarelli (18317235)
Khalid A. Fakhro (3158862)
Gabriele Zoppoli (201733)
Alberto Ballestrero (212236)
Rob A.E.M. Tollenaar (14908674)
Francesco M. Marincola (8823902)
Jérôme Galon (14906664)
Souhaila Al Khodor (6807155)
Michele Ceccarelli (184154)
Wouter Hendrickx (44559)
Davide Bedognetti (2632474)
author_role author
dc.creator.none.fl_str_mv Jessica Roelands (7516439)
Peter J. K. Kuppen (9858902)
Eiman I. Ahmed (6595514)
Raghvendra Mall (581171)
Tariq Masoodi (8117702)
Parul Singh (191877)
Gianni Monaco (3411857)
Christophe Raynaud (1405585)
Noel F.C.C. de Miranda (14892242)
Luigi Ferraro (718764)
Tatiana C. Carneiro-Lobo (17449912)
Najeeb Syed (12561967)
Arun Rawat (185306)
Amany Awad (17449915)
Julie Decock (44558)
William Mifsud (1394)
Lance D. Miller (8444226)
Shimaa Sherif (12862990)
Mahmoud G. Mohamed (9327444)
Darawan Rinchai (742366)
Marc Van den Eynde (801790)
Rosalyn W. Sayaman (8089034)
Elad Ziv (1263)
Francois Bertucci (5851322)
Mahir Abdulla Petkar (14150211)
Stephan Lorenz (466378)
Lisa Sara Mathew (17886698)
Kun Wang (134525)
Selvasankar Murugesan (4376506)
Damien Chaussabel (26369)
Alexander L. Vahrmeijer (8449359)
Ena Wang (802)
Anna Ceccarelli (18317235)
Khalid A. Fakhro (3158862)
Gabriele Zoppoli (201733)
Alberto Ballestrero (212236)
Rob A.E.M. Tollenaar (14908674)
Francesco M. Marincola (8823902)
Jérôme Galon (14906664)
Souhaila Al Khodor (6807155)
Michele Ceccarelli (184154)
Wouter Hendrickx (44559)
Davide Bedognetti (2632474)
dc.date.none.fl_str_mv 2023-05-01T00:00:00Z
dc.identifier.none.fl_str_mv 10.1038/s41591-023-02324-5
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/An_integrated_tumor_immune_and_microbiome_atlas_of_colon_cancer/26831203
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biomedical and clinical sciences
Clinical sciences
Immunology
Oncology and carcinogenesis
Multi-omics
Cancer Biomarkers
Colon Cancer
RNA Sequencing
Whole-Exome Sequencing
Genetic Immunoediting
dc.title.none.fl_str_mv An integrated tumor, immune and microbiome atlas of colon cancer
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr">The lack of multi-omics cancer datasets with extensive follow-up information hinders the identification of accurate biomarkers of clinical outcome. In this cohort study, we performed comprehensive genomic analyses on fresh-frozen samples from 348 patients affected by primary colon cancer, encompassing RNA, whole-exome, deep T cell receptor and 16S bacterial rRNA gene sequencing on tumor and matched healthy colon tissue, complemented with tumor whole-genome sequencing for further microbiome characterization. A type 1 helper T cell, cytotoxic, gene expression signature, called Immunologic Constant of Rejection, captured the presence of clonally expanded, tumor-enriched T cell clones and outperformed conventional prognostic molecular biomarkers, such as the consensus molecular subtype and the microsatellite instability classifications. Quantification of genetic immunoediting, defined as a lower number of neoantigens than expected, further refined its prognostic value. We identified a microbiome signature, driven by Ruminococcus bromii, associated with a favorable outcome. By combining microbiome signature and Immunologic Constant of Rejection, we developed and validated a composite score (mICRoScore), which identifies a group of patients with excellent survival probability. The publicly available multi-omics dataset provides a resource for better understanding colon cancer biology that could facilitate the discovery of personalized therapeutic approaches.</p><h2>Other Information</h2><p dir="ltr">Published in: Nature Medicine<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41591-023-02324-5" target="_blank">https://dx.doi.org/10.1038/s41591-023-02324-5</a></p>
eu_rights_str_mv openAccess
id Manara2_e2812bd60ab9b32b8e90692f75568970
identifier_str_mv 10.1038/s41591-023-02324-5
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26831203
publishDate 2023
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rights_invalid_str_mv CC BY 4.0
spelling An integrated tumor, immune and microbiome atlas of colon cancerJessica Roelands (7516439)Peter J. K. Kuppen (9858902)Eiman I. Ahmed (6595514)Raghvendra Mall (581171)Tariq Masoodi (8117702)Parul Singh (191877)Gianni Monaco (3411857)Christophe Raynaud (1405585)Noel F.C.C. de Miranda (14892242)Luigi Ferraro (718764)Tatiana C. Carneiro-Lobo (17449912)Najeeb Syed (12561967)Arun Rawat (185306)Amany Awad (17449915)Julie Decock (44558)William Mifsud (1394)Lance D. Miller (8444226)Shimaa Sherif (12862990)Mahmoud G. Mohamed (9327444)Darawan Rinchai (742366)Marc Van den Eynde (801790)Rosalyn W. Sayaman (8089034)Elad Ziv (1263)Francois Bertucci (5851322)Mahir Abdulla Petkar (14150211)Stephan Lorenz (466378)Lisa Sara Mathew (17886698)Kun Wang (134525)Selvasankar Murugesan (4376506)Damien Chaussabel (26369)Alexander L. Vahrmeijer (8449359)Ena Wang (802)Anna Ceccarelli (18317235)Khalid A. Fakhro (3158862)Gabriele Zoppoli (201733)Alberto Ballestrero (212236)Rob A.E.M. Tollenaar (14908674)Francesco M. Marincola (8823902)Jérôme Galon (14906664)Souhaila Al Khodor (6807155)Michele Ceccarelli (184154)Wouter Hendrickx (44559)Davide Bedognetti (2632474)Biomedical and clinical sciencesClinical sciencesImmunologyOncology and carcinogenesisMulti-omicsCancer BiomarkersColon CancerRNA SequencingWhole-Exome SequencingGenetic Immunoediting<p dir="ltr">The lack of multi-omics cancer datasets with extensive follow-up information hinders the identification of accurate biomarkers of clinical outcome. In this cohort study, we performed comprehensive genomic analyses on fresh-frozen samples from 348 patients affected by primary colon cancer, encompassing RNA, whole-exome, deep T cell receptor and 16S bacterial rRNA gene sequencing on tumor and matched healthy colon tissue, complemented with tumor whole-genome sequencing for further microbiome characterization. A type 1 helper T cell, cytotoxic, gene expression signature, called Immunologic Constant of Rejection, captured the presence of clonally expanded, tumor-enriched T cell clones and outperformed conventional prognostic molecular biomarkers, such as the consensus molecular subtype and the microsatellite instability classifications. Quantification of genetic immunoediting, defined as a lower number of neoantigens than expected, further refined its prognostic value. We identified a microbiome signature, driven by Ruminococcus bromii, associated with a favorable outcome. By combining microbiome signature and Immunologic Constant of Rejection, we developed and validated a composite score (mICRoScore), which identifies a group of patients with excellent survival probability. The publicly available multi-omics dataset provides a resource for better understanding colon cancer biology that could facilitate the discovery of personalized therapeutic approaches.</p><h2>Other Information</h2><p dir="ltr">Published in: Nature Medicine<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41591-023-02324-5" target="_blank">https://dx.doi.org/10.1038/s41591-023-02324-5</a></p>2023-05-01T00:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1038/s41591-023-02324-5https://figshare.com/articles/journal_contribution/An_integrated_tumor_immune_and_microbiome_atlas_of_colon_cancer/26831203CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/268312032023-05-01T00:00:00Z
spellingShingle An integrated tumor, immune and microbiome atlas of colon cancer
Jessica Roelands (7516439)
Biomedical and clinical sciences
Clinical sciences
Immunology
Oncology and carcinogenesis
Multi-omics
Cancer Biomarkers
Colon Cancer
RNA Sequencing
Whole-Exome Sequencing
Genetic Immunoediting
status_str publishedVersion
title An integrated tumor, immune and microbiome atlas of colon cancer
title_full An integrated tumor, immune and microbiome atlas of colon cancer
title_fullStr An integrated tumor, immune and microbiome atlas of colon cancer
title_full_unstemmed An integrated tumor, immune and microbiome atlas of colon cancer
title_short An integrated tumor, immune and microbiome atlas of colon cancer
title_sort An integrated tumor, immune and microbiome atlas of colon cancer
topic Biomedical and clinical sciences
Clinical sciences
Immunology
Oncology and carcinogenesis
Multi-omics
Cancer Biomarkers
Colon Cancer
RNA Sequencing
Whole-Exome Sequencing
Genetic Immunoediting