IMMUNOREACT 6: weak immune surveillance characterizes early-onset rectal cancer.


Journal

The British journal of surgery
ISSN: 1365-2168
Titre abrégé: Br J Surg
Pays: England
ID NLM: 0372553

Informations de publication

Date de publication:
10 Oct 2023
Historique:
received: 17 02 2023
revised: 05 06 2023
accepted: 14 06 2023
pubmed: 21 7 2023
medline: 21 7 2023
entrez: 21 7 2023
Statut: ppublish

Résumé

Colon cancer in young patients is often associated with hereditary syndromes; however, in early-onset rectal cancer, mutations of these genes are rarely observed. The aim of this study was to analyse the features of the local immune microenvironment and the mutational pattern in early-onset rectal cancer. Commonly mutated genes were analysed within a rectal cancer series from the University Hospital of Padova. Mutation frequency and immune gene expression in a cohort from The Cancer Genome Atlas ('TCGA') were compared and immune-cell infiltration levels in the healthy rectal mucosa adjacent to rectal cancers were evaluated in the IMMUNOlogical microenvironment in REctal AdenoCarcinoma Treatment 1 and 2 ('IMMUNOREACT') series. In the authors' series, the mutation frequency of BRAF, KRAS, and NRAS, as well as microsatellite instability frequency, were not different between early- and late-onset rectal cancer. In The Cancer Genome Atlas series, among the genes with the most considerable difference in mutation frequency between young and older patients, seven genes are involved in the immune response and CD69, CD3, and CD8β expression was lower in early-onset rectal cancer. In the IMMUNOlogical microenvironment in REctal AdenoCarcinoma Treatment 1 and 2 series, young patients had a lower rate of CD4+ T cells, but higher T regulator infiltration in the rectal mucosa. Early-onset rectal cancer is rarely associated with common hereditary syndromes. The tumour microenvironment is characterized by a high frequency of mutations impairing the local immune surveillance mechanisms and low expression of immune editing-related genes. A constitutively low number of CD4 T cells associated with a high number of T regulators indicates an imbalance in the immune surveillance mechanisms.

Sections du résumé

BACKGROUND BACKGROUND
Colon cancer in young patients is often associated with hereditary syndromes; however, in early-onset rectal cancer, mutations of these genes are rarely observed. The aim of this study was to analyse the features of the local immune microenvironment and the mutational pattern in early-onset rectal cancer.
METHODS METHODS
Commonly mutated genes were analysed within a rectal cancer series from the University Hospital of Padova. Mutation frequency and immune gene expression in a cohort from The Cancer Genome Atlas ('TCGA') were compared and immune-cell infiltration levels in the healthy rectal mucosa adjacent to rectal cancers were evaluated in the IMMUNOlogical microenvironment in REctal AdenoCarcinoma Treatment 1 and 2 ('IMMUNOREACT') series.
RESULTS RESULTS
In the authors' series, the mutation frequency of BRAF, KRAS, and NRAS, as well as microsatellite instability frequency, were not different between early- and late-onset rectal cancer. In The Cancer Genome Atlas series, among the genes with the most considerable difference in mutation frequency between young and older patients, seven genes are involved in the immune response and CD69, CD3, and CD8β expression was lower in early-onset rectal cancer. In the IMMUNOlogical microenvironment in REctal AdenoCarcinoma Treatment 1 and 2 series, young patients had a lower rate of CD4+ T cells, but higher T regulator infiltration in the rectal mucosa.
CONCLUSION CONCLUSIONS
Early-onset rectal cancer is rarely associated with common hereditary syndromes. The tumour microenvironment is characterized by a high frequency of mutations impairing the local immune surveillance mechanisms and low expression of immune editing-related genes. A constitutively low number of CD4 T cells associated with a high number of T regulators indicates an imbalance in the immune surveillance mechanisms.

Identifiants

pubmed: 37478362
pii: 7227745
doi: 10.1093/bjs/znad219
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1490-1501

Subventions

Organisme : AIRC Investigator
ID : ID 23381
Organisme : Associazione Italiana per la Ricerca sul Cancro

Investigateurs

Giulia Capelli (G)
Michela Campi (M)
Luca Saadeh (L)
Dario Parini (D)
Daniela Prando (D)
Beatrice Salmaso (B)
Gianluca Buzzi (G)
Loretta Di Cristofaro (L)
Corrado Da Lio (C)
Giulia Becherucci (G)
Fabio Ricagna (F)
Roberto Cola (R)

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of BJS Society Ltd. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Auteurs

Gaya Spolverato (G)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Matteo Fassan (M)

Department of Medicine DIMED, University of Padua, Padua, Italy.
Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Melania Scarpa (M)

Immunology and Molecular Oncology Diagnostics Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Astghik Stepanyan (A)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Ottavia De Simoni (O)

Surgical Oncology of Digestive Tract Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Federico Scognamiglio (F)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Valentina Chiminazzo (V)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Clarissa De Nardi (C)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Giulia Tamponi (G)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Silvia Negro (S)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Imerio Angriman (I)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Andromachi Kotsafti (A)

Immunology and Molecular Oncology Diagnostics Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Cesare Ruffolo (C)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Chiara Vignotto (C)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Maurizio Zizzo (M)

Chirurgia ad indirizzo oncologico, Azienda Unità Sanitaria Locale-IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Francesco Marchegiani (F)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Luca Facci (L)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Francesca Bergamo (F)

Medical Oncology 1 Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Stefano Brignola (S)

UOC Anatomia e Istologia Patologica, Azienda ULSS 2 Marca Trevigiana, Treviso, Italy.

Gianluca Businello (G)

UOC Anatomia Patologica, Azienda ULSS 5 Polesana, Rovigo, Italy.

Vincenza Guzzardo (V)

Department of Medicine DIMED, University of Padua, Padua, Italy.

Luca Dal Santo (L)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Roberta Salmaso (R)

Department of Medicine DIMED, University of Padua, Padua, Italy.

Carlotta Ceccon (C)

Department of Medicine DIMED, University of Padua, Padua, Italy.

Marco Massani (M)

UOC Chirurgia 1, Azienda ULSS 2 Marca Trevigiana, Treviso, Italy.

Anna Pozza (A)

UOC Chirurgia 1, Azienda ULSS 2 Marca Trevigiana, Treviso, Italy.

Ivana Cataldo (I)

UOC Anatomia e Istologia Patologica, Azienda ULSS 2 Marca Trevigiana, Treviso, Italy.

Tommaso Stecca (T)

UOC Chirurgia 1, Azienda ULSS 2 Marca Trevigiana, Treviso, Italy.

Angelo Paolo Dei Tos (AP)

Department of Medicine DIMED, University of Padua, Padua, Italy.

Vittorina Zagonel (V)

Medical Oncology 1 Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Pierluigi Pilati (P)

Surgical Oncology of Digestive Tract Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Boris Franzato (B)

Surgical Oncology of Digestive Tract Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Antonio Scapinello (A)

Anatomy and Pathological Histology Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.

Giovanni Pirozzolo (G)

UOC Chirurgia Generale, Ospedale dell'Angelo, Azienda ULSS 3 Serenissima, Mestre Venezia, Italy.

Alfonso Recordare (A)

UOC Chirurgia Generale, Ospedale dell'Angelo, Azienda ULSS 3 Serenissima, Mestre Venezia, Italy.

Roberto Merenda (R)

UOC Chirurgia Generale, Ospedale SS. Giovanni e Paolo, Azienda ULSS 3 Serenissima, Venezia, Italy.

Giovanni Bordignon (G)

UOC Chirurgia Generale, Ospedale SS. Giovanni e Paolo, Azienda ULSS 3 Serenissima, Venezia, Italy.

Licia Laurino (L)

UOC Anatomia Patologica, Azienda ULSS 3 Serenissima, Mestre Venezia, Italy.

Silvio Guerriero (S)

UOC Chirurgia Generale, Ospedale Murri di Fermo, ASUR 4, Fermo, Italy.

Chiara Romiti (C)

UOC Chirurgia Generale, Ospedale Murri di Fermo, ASUR 4, Fermo, Italy.

Giuseppe Portale (G)

UOC Chirurgia Generale, Azienda ULSS 6 Euganea, Cittadella, Italy.

Chiara Cipollari (C)

UOC Chirurgia Generale, Azienda ULSS 6 Euganea, Cittadella, Italy.

Salvatore Candioli (S)

UOC Chirurgia, Azienda ULSS 1 Dolomiti, Belluno, Italy.

Laura Gavagna (L)

UOC Chirurgia, Azienda ULSS 1 Dolomiti, Belluno, Italy.

Giulia Pozza (G)

UOC Chirurgia Generale, Ospedale dell'Angelo, Azienda ULSS 3 Serenissima, Mestre Venezia, Italy.

Mario Godina (M)

UOC Chirurgia Generale, Ospedale dell'Angelo, Azienda ULSS 3 Serenissima, Mestre Venezia, Italy.

Isabella Mondi (I)

UOC Chirurgia Generale, Ospedale dell'Angelo, Azienda ULSS 3 Serenissima, Mestre Venezia, Italy.

Giulia Noaro (G)

UOC Chirurgia Generale, Azienda ULSS 2 Marca Trevigiana, Montebelluna, Italy.

Monica Ortenzi (M)

SOD Clinica Chirurgica Generale e D'Urgenza, Azienda Ospedaliero Universitaria delle Marche, Ancona, Italy.

Mario Guerrieri (M)

SOD Clinica Chirurgica Generale e D'Urgenza, Azienda Ospedaliero Universitaria delle Marche, Ancona, Italy.

Giovanni Tagliente (G)

UO Chirurgia Generale, Policlinico Abano, Abano, Italy.

Monica Tomassi (M)

UO Chirurgia Generale, Policlinico Abano, Abano, Italy.

Umberto Tedeschi (U)

UO Chirurgia Generale, Policlinico Abano, Abano, Italy.

Andrea Porzionato (A)

Department of Neurosciences DNS, University of Padua, Padua, Italy.

Marco Agostini (M)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Isacco Maretto (I)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Quoc Riccardo Bao (QR)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Francesco Cavallin (F)

Independent Statisti‌cian, Solagna, Italy.

Barbara Di Camillo (B)

Department of Information Engineering DEI, University of Padua, Padua, Italy.

Romeo Bardini (R)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Ignazio Castagliuolo (I)

Department of Molecular Medicine DMM, University of Padua, Padua, Italy.

Salvatore Pucciarelli (S)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Marco Scarpa (M)

UOC Chirurgia Generale 3, Azienda Ospedale-Università Padova, Padua, Italy.

Classifications MeSH