The Interleukin-11/IL-11 Receptor Promotes Glioblastoma Survival and Invasion under Glucose-Starved Conditions through Enhanced Glutaminolysis.


Journal

International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791

Informations de publication

Date de publication:
08 Feb 2023
Historique:
received: 06 12 2022
revised: 31 01 2023
accepted: 01 02 2023
entrez: 25 2 2023
pubmed: 26 2 2023
medline: 3 3 2023
Statut: epublish

Résumé

Glioblastoma cells adapt to changes in glucose availability through metabolic plasticity allowing for cell survival and continued progression in low-glucose concentrations. However, the regulatory cytokine networks that govern the ability to survive in glucose-starved conditions are not fully defined. In the present study, we define a critical role for the IL-11/IL-11Rα signalling axis in glioblastoma survival, proliferation and invasion when cells are starved of glucose. We identified enhanced IL-11/IL-11Rα expression correlated with reduced overall survival in glioblastoma patients. Glioblastoma cell lines over-expressing IL-11Rα displayed greater survival, proliferation, migration and invasion in glucose-free conditions compared to their low-IL-11Rα-expressing counterparts, while knockdown of IL-11Rα reversed these pro-tumorigenic characteristics. In addition, these IL-11Rα-over-expressing cells displayed enhanced glutamine oxidation and glutamate production compared to their low-IL-11Rα-expressing counterparts, while knockdown of IL-11Rα or the pharmacological inhibition of several members of the glutaminolysis pathway resulted in reduced survival (enhanced apoptosis) and reduced migration and invasion. Furthermore, IL-11Rα expression in glioblastoma patient samples correlated with enhanced gene expression of the glutaminolysis pathway genes GLUD1, GSS and c-Myc. Overall, our study identified that the IL-11/IL-11Rα pathway promotes glioblastoma cell survival and enhances cell migration and invasion in environments of glucose starvation via glutaminolysis.

Identifiants

pubmed: 36834778
pii: ijms24043356
doi: 10.3390/ijms24043356
pmc: PMC9960532
pii:
doi:

Substances chimiques

Glucose IY9XDZ35W2
Interleukin-11 0
Receptors, Interleukin-11 0
IL11 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Rebecca L. Cooper Medical Research Foundation
ID : NA
Organisme : International Foundation for Ethical Research
ID : NA

Références

Genes Dev. 2011 May 15;25(10):1041-51
pubmed: 21576264
Cytokine Growth Factor Rev. 2015 Oct;26(5):489-98
pubmed: 26209885
Cancer Res. 2009 Oct 15;69(20):7986-93
pubmed: 19826036
Clin Cancer Res. 2017 Oct 15;23(20):6292-6304
pubmed: 28720668
J Cell Biochem. 2019 Oct;120(10):16824-16839
pubmed: 31111555
Cell Metab. 2012 Jan 4;15(1):110-21
pubmed: 22225880
Oncogene. 2020 Apr;39(14):2975-2986
pubmed: 32034306
Nutr Metab (Lond). 2005 Oct 21;2:30
pubmed: 16242042
Mol Med Rep. 2018 Mar;17(3):3972-3978
pubmed: 29286137
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
PLoS One. 2014 Mar 19;9(3):e92444
pubmed: 24647355
J Biol Chem. 2020 Jun 12;295(24):8285-8301
pubmed: 32332100
Cancer Cell. 2010 Sep 14;18(3):207-19
pubmed: 20832749
Exp Cell Res. 2018 Jul 15;368(2):184-193
pubmed: 29709516
Oncogene. 2016 Jun 16;35(24):3201-8
pubmed: 26455325
Biology (Basel). 2017 Feb 08;6(1):
pubmed: 28208702
Cell Metab. 2012 Jun 6;15(6):827-37
pubmed: 22682223
Nat Cell Biol. 2015 Dec;17(12):1556-68
pubmed: 26595383
Oncol Lett. 2018 Oct;16(4):4095-4104
pubmed: 30250528
Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19345-50
pubmed: 18032601
J Neurooncol. 2011 Apr;102(2):317-21
pubmed: 20683757
BMC Cancer. 2021 Jan 20;21(1):83
pubmed: 33472598
Annu Rev Biomed Eng. 2017 Jun 21;19:163-194
pubmed: 28301735
Cells. 2020 May 18;9(5):
pubmed: 32443613
Cells. 2019 Dec 18;9(1):
pubmed: 31861356
Mol Cell. 2014 Oct 23;56(2):205-218
pubmed: 25242145
Front Oncol. 2018 Aug 24;8:333
pubmed: 30197878
Mol Cell. 2014 Nov 6;56(3):414-424
pubmed: 25458842
Mol Syst Biol. 2014 May 05;10:728
pubmed: 24799285
Mol Cancer Ther. 2016 Nov;15(11):2609-2619
pubmed: 27535971
Clin Cancer Res. 2016 Sep 1;22(17):4452-65
pubmed: 27076630
Biochim Biophys Acta Mol Cell Res. 2017 Nov;1864(11 Pt B):2105-2117
pubmed: 28630024
Cancers (Basel). 2021 Nov 29;13(23):
pubmed: 34885110
Genes Dev. 2007 Nov 1;21(21):2683-710
pubmed: 17974913
Cell Metab. 2019 Aug 6;30(2):274-289.e5
pubmed: 31056285
Cell Death Dis. 2019 Apr 30;10(5):353
pubmed: 31040267
J Clin Invest. 2008 May;118(5):1727-38
pubmed: 18431520
Onco Targets Ther. 2019 Mar 28;12:2397-2408
pubmed: 30992675
Trends Biochem Sci. 2010 Aug;35(8):427-33
pubmed: 20570523
Cell Metab. 2011 Dec 7;14(6):724-38
pubmed: 22152301
Cancers (Basel). 2018 Dec 19;10(12):
pubmed: 30572654
Cell Metab. 2019 Aug 6;30(2):229-230
pubmed: 31390546
Clin Cancer Res. 2009 Oct 1;15(19):6002-7
pubmed: 19755387
Proc Natl Acad Sci U S A. 2008 Dec 2;105(48):18782-7
pubmed: 19033189
EMBO Mol Med. 2019 Apr;11(4):
pubmed: 30885958
J Clin Invest. 2015 Apr;125(4):1591-602
pubmed: 25798620
Int J Mol Sci. 2015 Sep 22;16(9):22830-55
pubmed: 26402672
Curr Mol Med. 2013 May;13(4):514-34
pubmed: 22934847
J Exp Clin Cancer Res. 2019 Feb 8;38(1):63
pubmed: 30736824
J Biol Chem. 2008 Jul 25;283(30):20621-7
pubmed: 18364355
Cold Spring Harb Perspect Med. 2013 Aug 01;3(8):
pubmed: 23906881
Cancers (Basel). 2019 Oct 24;11(11):
pubmed: 31652923
Exp Mol Med. 2020 Sep;52(9):1496-1516
pubmed: 32943735
Cancer Cell. 2013 Aug 12;24(2):257-71
pubmed: 23948300
BMC Biotechnol. 2012 Mar 21;12:8
pubmed: 22433466
Nature. 2009 Apr 9;458(7239):762-5
pubmed: 19219026
Semin Immunol. 2014 Feb;26(1):54-74
pubmed: 24552665
Nat Neurosci. 2013 Oct;16(10):1373-82
pubmed: 23995067
Front Immunol. 2014 Feb 19;5:58
pubmed: 24600449

Auteurs

Sarah F Stuart (SF)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.
Fiona Elsey Cancer Research Institute, Ballarat, VIC 3350, Australia.

Ayenachew Bezawork-Geleta (A)

Department of Physiology, The University of Melbourne, Melbourne, VIC 3010, Australia.

Zammam Areeb (Z)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Juliana Gomez (J)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Vanessa Tsui (V)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Ahmad Zulkifli (A)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Lucia Paradiso (L)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Jordan Jones (J)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.
Department of Neurosurgery, The Royal Melbourne Hospital, Parkville, VIC 3050, Australia.

Hong P T Nguyen (HPT)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Tracy L Putoczki (TL)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.
The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC 3050, Australia.
Department of Medical Biology, The University of Melbourne, Parkville, VIC 3050, Australia.

Paul V Licciardi (PV)

Murdoch Children's Research Institute, Melbourne, VIC 3052, Australia.
Department of Paediatrics, The University of Melbourne, Melbourne, VIC 3052, Australia.

George Kannourakis (G)

Fiona Elsey Cancer Research Institute, Ballarat, VIC 3350, Australia.
Health, Innovation and Transformation Centre, Federation University, Ballarat, VIC 3350, Australia.

Andrew P Morokoff (AP)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.
Department of Neurosurgery, The Royal Melbourne Hospital, Parkville, VIC 3050, Australia.

Adrian A Achuthan (AA)

Department of Medicine, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.

Rodney B Luwor (RB)

Department of Surgery, The Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.
Fiona Elsey Cancer Research Institute, Ballarat, VIC 3350, Australia.
Health, Innovation and Transformation Centre, Federation University, Ballarat, VIC 3350, Australia.

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Classifications MeSH