Disease Modeling on Tumor Organoids Implicates AURKA as a Therapeutic Target in Liver Metastatic Colorectal Cancer.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2022
Historique:
received: 05 03 2021
revised: 13 10 2021
accepted: 13 10 2021
pubmed: 27 10 2021
medline: 5 4 2022
entrez: 26 10 2021
Statut: ppublish

Résumé

Patient-derived tumor organoids recapitulate the characteristics of colorectal cancer (CRC) and provide an ideal platform for preclinical evaluation of personalized treatment options. We aimed to model the acquisition of chemotolerance during first-line combination chemotherapy in metastatic CRC organoids. We performed next-generation sequencing to study the evolution of KRAS wild-type CRC organoids during adaptation to irinotecan-based chemotherapy combined with epidermal growth factor receptor (EGFR) inhibition. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated 9 protein (Cas9)-editing showed the specific effect of KRAS Adaptation to combination chemotherapy was accompanied by transcriptomic rather than gene mutational alterations in CRC organoids. Drug-tolerant cells evaded apoptosis and up-regulated MYC (c-myelocytomatosis oncogene product)/E2F1 (E2 family transcription factor 1) and/or interferon-α-related gene expression. Introduction of KRAS Our study emphasizes the potential of patient-derived CRC organoids in modeling chemotherapy tolerance ex vivo. The applied therapeutic strategy of dual EGFR pathway blockade in combination with AURKA inhibition may prove effective for second-line treatment of chemotolerant CRC liver metastases with acquired KRAS mutation and increased AURKA/c-MYC expression.

Sections du résumé

BACKGROUND & AIMS
Patient-derived tumor organoids recapitulate the characteristics of colorectal cancer (CRC) and provide an ideal platform for preclinical evaluation of personalized treatment options. We aimed to model the acquisition of chemotolerance during first-line combination chemotherapy in metastatic CRC organoids.
METHODS
We performed next-generation sequencing to study the evolution of KRAS wild-type CRC organoids during adaptation to irinotecan-based chemotherapy combined with epidermal growth factor receptor (EGFR) inhibition. Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated 9 protein (Cas9)-editing showed the specific effect of KRAS
RESULTS
Adaptation to combination chemotherapy was accompanied by transcriptomic rather than gene mutational alterations in CRC organoids. Drug-tolerant cells evaded apoptosis and up-regulated MYC (c-myelocytomatosis oncogene product)/E2F1 (E2 family transcription factor 1) and/or interferon-α-related gene expression. Introduction of KRAS
CONCLUSIONS
Our study emphasizes the potential of patient-derived CRC organoids in modeling chemotherapy tolerance ex vivo. The applied therapeutic strategy of dual EGFR pathway blockade in combination with AURKA inhibition may prove effective for second-line treatment of chemotolerant CRC liver metastases with acquired KRAS mutation and increased AURKA/c-MYC expression.

Identifiants

pubmed: 34700030
pii: S2352-345X(21)00222-8
doi: 10.1016/j.jcmgh.2021.10.008
pmc: PMC8688726
pii:
doi:

Substances chimiques

AURKA protein, human EC 2.7.11.1
Aurora Kinase A EC 2.7.11.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

517-540

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Sophie L Boos (SL)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung) Research Group, Oncogenic Signaling Pathways of Colorectal Cancer, Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany; Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Leon P Loevenich (LP)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung) Research Group, Oncogenic Signaling Pathways of Colorectal Cancer, Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany; Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Sebastian Vosberg (S)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Department of Medicine III, University Hospital Ludwig-Maximilians-University, Munich, Germany.

Thomas Engleitner (T)

Institute of Molecular Oncology and Functional Genomics, TUM School of Medicine, Technical University of Munich, Munich, Germany.

Rupert Öllinger (R)

Institute of Molecular Oncology and Functional Genomics, TUM School of Medicine, Technical University of Munich, Munich, Germany.

Jörg Kumbrink (J)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Matjaz Rokavec (M)

Experimental and Molecular Pathology, Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Marlies Michl (M)

Experimental and Molecular Pathology, Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany; Comprehensive Cancer Center, Ludwig-Maximilians-University, University Hospital, Munich, Germany.

Philipp A Greif (PA)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Department of Medicine III, University Hospital Ludwig-Maximilians-University, Munich, Germany.

Andreas Jung (A)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Heiko Hermeking (H)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Experimental and Molecular Pathology, Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Jens Neumann (J)

Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Thomas Kirchner (T)

German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany.

Roland Rad (R)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; Institute of Molecular Oncology and Functional Genomics, TUM School of Medicine, Technical University of Munich, Munich, Germany.

Peter Jung (P)

German Cancer Research Center, Deutsches Krebsforschungszentrum, Heidelberg, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung), Partner Site Munich, Germany; German Cancer Consortium (Deutsches Konsortium für Translationale Krebsforschung) Research Group, Oncogenic Signaling Pathways of Colorectal Cancer, Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany; Institute of Pathology, Ludwig-Maximilians-University, Munich, Germany. Electronic address: p.jung@dkfz.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH