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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2023
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| 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) |
| author2_role | author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author |
| 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 |
| repository.mail.fl_str_mv | |
| repository.name.fl_str_mv | |
| repository_id_str | |
| 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 |