Genetic Screens Identify a Context-Specific PI3K/p27Kip1 Node Driving Extrahepatic Biliary Cancer.


Journal

Cancer discovery
ISSN: 2159-8290
Titre abrégé: Cancer Discov
Pays: United States
ID NLM: 101561693

Informations de publication

Date de publication:
01 12 2021
Historique:
received: 12 02 2021
revised: 25 05 2021
accepted: 01 07 2021
pubmed: 21 7 2021
medline: 6 4 2022
entrez: 20 7 2021
Statut: ppublish

Résumé

Biliary tract cancer ranks among the most lethal human malignancies, representing an unmet clinical need. Its abysmal prognosis is tied to an increasing incidence and a fundamental lack of mechanistic knowledge regarding the molecular basis of the disease. Here, we show that the Pdx1-positive extrahepatic biliary epithelium is highly susceptible toward transformation by activated PIK3CAH1047R but refractory to oncogenic KrasG12D. Using genome-wide transposon screens and genetic loss-of-function experiments, we discover context-dependent genetic interactions that drive extrahepatic cholangiocarcinoma (ECC) and show that PI3K signaling output strength and repression of the tumor suppressor p27Kip1 are critical context-specific determinants of tumor formation. This contrasts with the pancreas, where oncogenic Kras in concert with p53 loss is a key cancer driver. Notably, inactivation of p27Kip1 permits KrasG12D-driven ECC development. These studies provide a mechanistic link between PI3K signaling, tissue-specific tumor suppressor barriers, and ECC pathogenesis, and present a novel genetic model of autochthonous ECC and genes driving this highly lethal tumor subtype. We used the first genetically engineered mouse model for extrahepatic bile duct carcinoma to identify cancer genes by genome-wide transposon-based mutagenesis screening. Thereby, we show that PI3K signaling output strength and p27Kip1 function are critical determinants for context-specific ECC formation. This article is highlighted in the In This Issue feature, p. 2945.

Identifiants

pubmed: 34282029
pii: 2159-8290.CD-21-0209
doi: 10.1158/2159-8290.CD-21-0209
pmc: PMC7612573
mid: EMS132018
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3158-3177

Subventions

Organisme : European Research Council
ID : 648521
Pays : International
Organisme : Cancer Research UK
ID : A21139
Pays : United Kingdom
Organisme : Cancer Research UK
ID : A17196
Pays : United Kingdom

Informations de copyright

©2021 The Authors; Published by the American Association for Cancer Research.

Références

Nature. 2011 Mar 17;471(7338):316-7
pubmed: 21412332
Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):246-51
pubmed: 20018721
Genesis. 2007 Sep;45(9):593-605
pubmed: 17868096
Nat Rev Cancer. 2005 Dec;5(12):921-9
pubmed: 16341083
Hepatology. 2014 Feb;59(2):544-54
pubmed: 24002901
Science. 2010 Nov 19;330(6007):1104-7
pubmed: 20947725
Oncotarget. 2013 Feb;4(2):277-88
pubmed: 23470560
Cancer Cell. 2003 Dec;4(6):437-50
pubmed: 14706336
Nat Genet. 2015 Sep;47(9):1003-10
pubmed: 26258846
Lancet. 2014 Jun 21;383(9935):2168-79
pubmed: 24581682
Nat Rev Cancer. 2011 Oct 13;11(11):761-74
pubmed: 21993244
Oncotarget. 2016 Jul 19;7(29):46750-46767
pubmed: 27102149
Nat Commun. 2015 Jan 30;6:6120
pubmed: 25636086
Nat Commun. 2014 Dec 15;5:5696
pubmed: 25526346
J Clin Oncol. 2006 Mar 1;24(7):1152-60
pubmed: 16505435
Clin Cancer Res. 2001 Dec;7(12):3994-9
pubmed: 11751492
Biomark Med. 2015;9(8):763-75
pubmed: 26223884
Genes Dev. 2014 Dec 1;28(23):2621-35
pubmed: 25452273
Oncogene. 2009 Oct 15;28(41):3652-62
pubmed: 19648963
Nat Genet. 2015 Jan;47(1):47-56
pubmed: 25485836
Cancer Res. 2014 Sep 1;74(17):4752-61
pubmed: 24958469
Nat Rev Mol Cell Biol. 2010 Jan;11(1):9-22
pubmed: 20027184
Gastroenterology. 2009 Jul;137(1):361-71, 371.e1-5
pubmed: 19362090
Nat Neurosci. 2010 Jan;13(1):133-40
pubmed: 20023653
Nat Genet. 2001 Dec;29(4):418-25
pubmed: 11694875
Nat Rev Gastroenterol Hepatol. 2020 Sep;17(9):557-588
pubmed: 32606456
Nucleic Acids Res. 2015 Jan;43(Database issue):D447-52
pubmed: 25352553
Cancer Cell. 2013 Mar 18;23(3):406-20
pubmed: 23453624
Immunity. 2001 May;14(5):523-34
pubmed: 11371355
Dev Cell. 2009 Jul;17(1):62-74
pubmed: 19619492
BMC Bioinformatics. 2012 Jun 29;13:154
pubmed: 22748055
Oncol Lett. 2020 Apr;19(4):3101-3110
pubmed: 32256810
CA Cancer J Clin. 2020 Jan;70(1):7-30
pubmed: 31912902
Cell Res. 2016 Apr;26(4):484-98
pubmed: 27002218
Semin Liver Dis. 2014 Nov;34(4):456-64
pubmed: 25369307
Cancer Discov. 2011 Sep;1(4):326-37
pubmed: 22586611
Nat Cell Biol. 2012 Dec;14(12):1322-9
pubmed: 23143395
CA Cancer J Clin. 2011 Mar-Apr;61(2):69-90
pubmed: 21296855
Tumour Biol. 2016 Apr;37(4):4331-41
pubmed: 26494000
Oncogene. 2012 Mar 22;31(12):1599-608
pubmed: 21860420
Mod Pathol. 2007 Jun;20(6):701-9
pubmed: 17431410
Transl Oncol. 2016 Jun;9(3):173-8
pubmed: 27267833
PLoS One. 2013 May 31;8(5):e64832
pubmed: 23741402
BMC Cancer. 2011 Feb 08;11:60
pubmed: 21303542
Cancer Cell. 2009 Apr 7;15(4):304-14
pubmed: 19345329
J Biol Chem. 2012 Jul 20;287(30):25325-34
pubmed: 22535956
Cell. 1996 May 31;85(5):733-44
pubmed: 8646781
JCI Insight. 2018 Jan 25;3(2):
pubmed: 29367463
HPB (Oxford). 2008;10(2):83-6
pubmed: 18773061
Cancer Res. 2012 Mar 15;72(6):1557-67
pubmed: 22266220
Ann Surg Oncol. 2014 Feb;21(2):487-500
pubmed: 24081803
Nat Rev Cancer. 2002 Apr;2(4):251-65
pubmed: 12001987
Gastroenterology. 2013 Dec;145(6):1215-29
pubmed: 24140396
Nat Rev Cancer. 2017 Apr;17(4):239-253
pubmed: 28256574
Genes Dev. 2001 Dec 15;15(24):3243-8
pubmed: 11751630
Cancer Res. 2006 Jan 1;66(1):95-106
pubmed: 16397221
Clin Cancer Res. 2018 Sep 1;24(17):4154-4161
pubmed: 29848569
Nat Cell Biol. 2009 Apr;11(4):420-32
pubmed: 19270694
Nature. 2018 Feb 1;554(7690):62-68
pubmed: 29364867
Int J Biochem Cell Biol. 2011 Feb;43(2):257-64
pubmed: 20601079
Nat Rev Drug Discov. 2014 Feb;13(2):140-56
pubmed: 24481312
Proc Natl Acad Sci U S A. 2011 Jun 14;108(24):9945-50
pubmed: 21628592
PLoS One. 2014 Dec 23;9(12):e115383
pubmed: 25536104
J Cell Biochem. 2011 Aug;112(8):2138-48
pubmed: 21465537
Nature. 2010 Mar 18;464(7287):374-9
pubmed: 20237562
Oncogene. 2010 Mar 25;29(12):1798-809
pubmed: 20023701
Hepatology. 2011 Jul;54(1):173-84
pubmed: 21488076
J Clin Pathol. 2016 May;69(5):403-8
pubmed: 26500333
Nat Rev Cancer. 2008 Apr;8(4):253-67
pubmed: 18354415

Auteurs

Chiara Falcomatà (C)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Stefanie Bärthel (S)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Angelika Ulrich (A)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.

Sandra Diersch (S)

Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

Christian Veltkamp (C)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Lena Rad (L)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Fabio Boniolo (F)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Myriam Solar (M)

Cancer Research UK Beatson Institute, Glasgow, United Kingdom.

Katja Steiger (K)

Institute of Pathology, Klinikum rechts der Isar, Technische Universität München, München, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.

Barbara Seidler (B)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

Magdalena Zukowska (M)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

Joanna Madej (J)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Mingsong Wang (M)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

Rupert Öllinger (R)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, Munich, Germany.

Roman Maresch (R)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, Munich, Germany.

Maxim Barenboim (M)

German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, Munich, Germany.
Department of Pediatrics and Children's Cancer Research Center, Klinikum rechts der Isar, Technische Universität München, School of Medicine, Munich, Germany.

Stefan Eser (S)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

Markus Tschurtschenthaler (M)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.

Arianeb Mehrabi (A)

Department of Surgery, Universität Heidelberg, Heidelberg, Germany.

Stephanie Roessler (S)

Institute of Pathology, Universität Heidelberg, Heidelberg, Germany.

Benjamin Goeppert (B)

Institute of Pathology, Universität Heidelberg, Heidelberg, Germany.

Alexander Kind (A)

Livestock Biotechnology, Technische Universität München, Freising, Germany.

Angelika Schnieke (A)

Livestock Biotechnology, Technische Universität München, Freising, Germany.

Maria S Robles (MS)

Institute of Medical Psychology, Faculty of Medicine, LMU Munich, Munich, Germany.

Allan Bradley (A)

Wellcome Trust Sanger Institute, Genome Campus, Hinxton-Cambridge, United Kingdom.

Roland M Schmid (RM)

Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

Marc Schmidt-Supprian (M)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Experimental Hematology, School of Medicine, Technische Universität München, Munich, Germany.

Maximilian Reichert (M)

Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Center for Protein Assemblies (CPA), Technische Universität München, Garching, Germany.

Wilko Weichert (W)

Institute of Pathology, Klinikum rechts der Isar, Technische Universität München, München, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.

Owen J Sansom (OJ)

Cancer Research UK Beatson Institute, Glasgow, United Kingdom.
Institute of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.

Jennifer P Morton (JP)

Cancer Research UK Beatson Institute, Glasgow, United Kingdom.
Institute of Cancer Sciences, University of Glasgow, Glasgow, United Kingdom.

Roland Rad (R)

Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Institute of Molecular Oncology and Functional Genomics, School of Medicine, Technische Universität München, Munich, Germany.

Günter Schneider (G)

Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.
German Cancer Consortium (DKTK), Heidelberg, Germany.
Department of General, Visceral and Pediatric Surgery, University Medical Center Göttingen, Göttingen, Germany.

Dieter Saur (D)

Division of Translational Cancer Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany.
Chair of Translational Cancer Research and Institute for Experimental Cancer Therapy, Klinikum rechts der Isar, School of Medicine, Technische Universität München, Munich, Germany.
Center for Translational Cancer Research (TranslaTUM), School of Medicine, Technical University of Munich, Munich, Germany.
Department of Internal Medicine II, Klinikum rechts der Isar, Technische Universität München, Munich, Germany.

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