Low expression of ANT1 confers oncogenic properties to rhabdomyosarcoma tumor cells by modulating metabolism and death pathways.

Cell death Paediatric cancer

Journal

Cell death discovery
ISSN: 2058-7716
Titre abrégé: Cell Death Discov
Pays: United States
ID NLM: 101665035

Informations de publication

Date de publication:
2020
Historique:
received: 29 04 2020
revised: 17 06 2020
accepted: 06 07 2020
entrez: 31 7 2020
pubmed: 31 7 2020
medline: 31 7 2020
Statut: epublish

Résumé

Rhabdomyosarcoma (RMS) is the most frequent form of pediatric soft-tissue sarcoma. It is divided into two main subtypes: ERMS (embryonal) and ARMS (alveolar). Current treatments are based on chemotherapy, surgery, and radiotherapy. The 5-year survival rate has plateaued at 70% since 2000, despite several clinical trials. RMS cells are thought to derive from the muscle lineage. During development, myogenesis includes the expansion of muscle precursors, the elimination of those in excess by cell death and the differentiation of the remaining ones into myofibers. The notion that these processes may be hijacked by tumor cells to sustain their oncogenic transformation has emerged, with RMS being considered as the dark side of myogenesis. Thus, dissecting myogenic developmental programs could improve our understanding of RMS molecular etiology. We focused herein on ANT1, which is involved in myogenesis and is responsible for genetic disorders associated with muscle degeneration. ANT1 is a mitochondrial protein, which has a dual functionality, as it is involved both in metabolism via the regulation of ATP/ADP release from mitochondria and in regulated cell death as part of the mitochondrial permeability transition pore. Bioinformatics analyses of transcriptomic datasets revealed that ANT1 is expressed at low levels in RMS. Using the CRISPR-Cas9 technology, we showed that reduced ANT1 expression confers selective advantages to RMS cells in terms of proliferation and resistance to stress-induced death. These effects arise notably from an abnormal metabolic switch induced by ANT1 downregulation. Restoration of ANT1 expression using a Tet-On system is sufficient to prime tumor cells to death and to increase their sensitivity to chemotherapy. Based on our results, modulation of ANT1 expression and/or activity appears as an appealing therapeutic approach in RMS management.

Identifiants

pubmed: 32728477
doi: 10.1038/s41420-020-00302-1
pii: 302
pmc: PMC7382490
doi:

Types de publication

Journal Article

Langues

eng

Pagination

64

Informations de copyright

© The Author(s) 2020.

Déclaration de conflit d'intérêts

Conflict of interestThe authors declare that they have no conflict of interest.

Références

J Cell Biol. 1999 Dec 27;147(7):1493-502
pubmed: 10613907
J Biol Chem. 1992 Jul 25;267(21):14592-7
pubmed: 1378836
J Cell Sci. 2018 Jul 27;131(14):
pubmed: 30054310
Curr Drug Targets. 2011 Jun;12(6):894-901
pubmed: 21269262
Nature. 2004 Aug 26;430(7003):1 p following 983
pubmed: 15332302
Curr Med Chem. 2003 Aug;10(16):1507-25
pubmed: 12871123
FEBS J. 2010 Jul;277(13):2853-67
pubmed: 20528917
Cell Signal. 2016 Jan;28(1):152-9
pubmed: 26548633
JIMD Rep. 2015;22:39-45
pubmed: 25732997
BMC Cancer. 2008 Jun 04;8:160
pubmed: 18522758
Oncogene. 2018 Sep;37(39):5325-5339
pubmed: 29858601
EMBO J. 2019 May 15;38(10):
pubmed: 30979776
Mitochondrion. 2018 Mar;39:26-29
pubmed: 28823815
Science. 2012 May 25;336(6084):1040-4
pubmed: 22628656
Sarcoma. 2012;2012:326210
pubmed: 22294874
FASEB J. 2005 Mar;19(3):404-6
pubmed: 15629888
Trends Mol Med. 2013 Sep;19(9):546-54
pubmed: 23890422
Trends Cell Biol. 2016 Sep;26(9):655-667
pubmed: 27161573
Oncogene. 2015 Mar 19;34(12):1608
pubmed: 25790189
Exp Mol Med. 2020 Jan;52(1):15-30
pubmed: 31980738
Acta Biochim Pol. 2003;50(2):389-404
pubmed: 12833165
NMR Biomed. 2019 Oct;32(10):e4112
pubmed: 31184789
Autophagy. 2019 Sep;15(9):1606-1619
pubmed: 30859901
Development. 2014 Jan;141(1):219-23
pubmed: 24346702
J Med Genet. 2012 Feb;49(2):146-50
pubmed: 22187496
J Biol Chem. 2004 Sep 10;279(37):38415-23
pubmed: 15231833
J Cell Biochem. 2009 Jul 1;107(4):834-44
pubmed: 19415683
Curr Top Dev Biol. 2011;94:197-234
pubmed: 21295688
Sci Adv. 2019 Aug 28;5(8):eaaw4597
pubmed: 31489369
J Vet Med Sci. 2009 Sep;71(9):1161-8
pubmed: 19801895
Oncogene. 2011 Feb 24;30(8):883-95
pubmed: 21076465
Metabolomics. 2020 Jan 10;16(1):13
pubmed: 31925544
Biochim Biophys Acta. 2014 Dec;1843(12):2926-36
pubmed: 25205454
Am J Pathol. 2010 Jan;176(1):416-34
pubmed: 20019182
Biochim Biophys Acta. 2011 Apr;1813(4):616-22
pubmed: 20888866
Science. 2000 Aug 4;289(5480):782-5
pubmed: 10926541
Neurol Genet. 2018 Jul 20;4(4):e256
pubmed: 30046662
Nat Med. 2019 Mar;25(3):367-376
pubmed: 30842674
Cell Death Dis. 2016 Mar 31;7:e2168
pubmed: 27031965
Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11025-30
pubmed: 12177420
Cancer Res. 1991 Oct 1;51(19):5100-6
pubmed: 1717137
Methods Mol Biol. 2009;559:313-32
pubmed: 19609766
FASEB J. 2007 Jul;21(9):2195-204
pubmed: 17360850
Nat Rev Cancer. 2005 Mar;5(3):231-7
pubmed: 15738985
J Biol Chem. 2012 Feb 24;287(9):6860-7
pubmed: 22223649
Nature. 2004 Jan 29;427(6973):461-5
pubmed: 14749836
Nat Rev Cancer. 2014 Apr;14(4):277-89
pubmed: 24599217
Cell Death Differ. 2018 Mar;25(3):486-541
pubmed: 29362479
Biochim Biophys Acta. 2011 Jun;1807(6):562-7
pubmed: 20950584
Biochem J. 2014 Sep 1;462(2):267-77
pubmed: 24865278

Auteurs

J Vial (J)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

P Huchedé (P)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

S Fagault (S)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

F Basset (F)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

M Rossi (M)

Aix-Marseille Université, Inserm UMR_S 911, Centre de Recherche en Oncologie biologique et Oncopharmacologie, Faculté de pharmacie, Marseille, France.

J Geoffray (J)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

H Soldati (H)

Department of Cell Physiology and Metabolism, University of Geneva, CMU, CH-1211 Geneva, Switzerland.

J Bisaccia (J)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

M H Elsensohn (MH)

Service de Biostatistique-Bioinformatique, Pôle Santé Publique, Hospices Civils de Lyon, F-69003 Lyon, France.

M Creveaux (M)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

D Neves (D)

Netris Pharma, Lyon, France.

J Y Blay (JY)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

F Fauvelle (F)

Université Grenoble Alpes, INSERM, US17, MRI facility IRMaGe, 38000 Grenoble, France.

F Bouquet (F)

Roche Institute, Boulogne-Billancourt, France.

N Streichenberger (N)

Hospices Civils de Lyon, Lyon, France.
INMG CNRS UMR 5310, INSERM U1217, Université Claude Bernard Lyon, Lyon, France.

N Corradini (N)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

C Bergeron (C)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

D Maucort-Boulch (D)

Service de Biostatistique-Bioinformatique, Pôle Santé Publique, Hospices Civils de Lyon, F-69003 Lyon, France.

P Castets (P)

Department of Cell Physiology and Metabolism, University of Geneva, CMU, CH-1211 Geneva, Switzerland.

M Carré (M)

Aix-Marseille Université, Inserm UMR_S 911, Centre de Recherche en Oncologie biologique et Oncopharmacologie, Faculté de pharmacie, Marseille, France.

K Weber (K)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

M Castets (M)

Cell death and Childhood Cancers Laboratory-Equipe labellisée LabEx DEV2CAN, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon, Centre Léon Bérard, 69008 Lyon, France.

Classifications MeSH