Constitutive Activation of p62/Sequestosome-1-Mediated Proteaphagy Regulates Proteolysis and Impairs Cell Death in Bortezomib-Resistant Mantle Cell Lymphoma.

TUBEs apoptosis autophagy proteasome inhibitor ubiquitin proteome verteporfin

Journal

Cancers
ISSN: 2072-6694
Titre abrégé: Cancers (Basel)
Pays: Switzerland
ID NLM: 101526829

Informations de publication

Date de publication:
12 Feb 2022
Historique:
received: 11 12 2021
revised: 01 02 2022
accepted: 07 02 2022
entrez: 25 2 2022
pubmed: 26 2 2022
medline: 26 2 2022
Statut: epublish

Résumé

Protein ubiquitylation coordinates crucial cellular events in physiological and pathological conditions. A comparative analysis of the ubiquitin proteome from bortezomib (BTZ)-sensitive and BTZ-resistant mantle cell lymphoma (MCL) revealed an enrichment of the autophagy-lysosome system (ALS) in BTZ-resistant cells. Pharmacological inhibition of autophagy at the level of lysosome-fusion revealed a constitutive activation of proteaphagy and accumulation of proteasome subunits within autophagosomes in different MCL cell lines with acquired or natural resistance to BTZ. Inhibition of the autophagy receptor p62/SQSTM1 upon verteporfin (VTP) treatment disrupted proteaphagosome assembly, reduced co-localization of proteasome subunits with autophagy markers and negatively impacted proteasome activity. Finally, the silencing or pharmacological inhibition of p62 restored the apoptosis threshold at physiological levels in BTZ-resistant cells both in vitro and in vivo. In total, these results demonstrate for the first time a proteolytic switch from the ubiquitin-proteasome system (UPS) to ALS in B-cell lymphoma refractory to proteasome inhibition, pointing out a crucial role for proteaphagy in this phenomenon and paving the way for the design of alternative therapeutic venues in treatment-resistant tumors.

Identifiants

pubmed: 35205670
pii: cancers14040923
doi: 10.3390/cancers14040923
pmc: PMC8869867
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : European Union
ID : Grant agreement No 765445.
Organisme : French National Cancer Institute
ID : PLBIO16-251
Organisme : Consejo Nacional de Ciencia y Tecnología
ID : CONACYT-SRE 0280365
Organisme : Ministry of Economy, Industry and Competitiveness
ID : SEV-2015-0522
Organisme : LASERLAB Europe
ID : 654148
Organisme : Instituto de Salud Carlos III
ID : PI15/00102 and PI18/01383

Références

Elife. 2015 Sep 01;4:e08153
pubmed: 26327694
Methods Mol Biol. 2016;1449:177-92
pubmed: 27613035
Molecules. 2020 May 18;25(10):
pubmed: 32443527
FEBS Open Bio. 2021 Jan;11(1):48-60
pubmed: 33410599
Blood. 2011 Jan 27;117(4):1270-9
pubmed: 21106982
Cancers (Basel). 2020 Jun 12;12(6):
pubmed: 32545704
EMBO Rep. 2009 Nov;10(11):1250-8
pubmed: 19798103
Trends Biochem Sci. 2019 Jul;44(7):599-615
pubmed: 30819414
Methods Enzymol. 2005;398:353-63
pubmed: 16275342
Proc Natl Acad Sci U S A. 2013 Nov 5;110(45):18250-5
pubmed: 24145436
Methods Mol Biol. 2012;832:173-83
pubmed: 22350885
Oncotarget. 2016 Oct 11;7(41):66360-66385
pubmed: 27626179
Cell Rep. 2016 Aug 9;16(6):1717-1732
pubmed: 27477278
Biomed Res Int. 2015;2015:172458
pubmed: 26579531
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Trends Biochem Sci. 2017 Nov;42(11):873-886
pubmed: 28947091
Hematol Oncol Clin North Am. 2019 Aug;33(4):613-626
pubmed: 31229158
Br J Haematol. 2018 Jun;181(5):703-706
pubmed: 28444739
Adv Exp Med Biol. 2020;1233:153-174
pubmed: 32274756
Methods Enzymol. 2005;398:364-78
pubmed: 16275343
Autophagy. 2015;11(7):1161-78
pubmed: 26043024
Mol Cell. 2015 Jun 18;58(6):1053-66
pubmed: 26004230
Adv Exp Med Biol. 2020;1233:55-100
pubmed: 32274753
Mol Cell Proteomics. 2014 Dec;13(12):3294-307
pubmed: 25128556
Oncogene. 2018 Apr;37(14):1830-1844
pubmed: 29353886
Sci Rep. 2017 Apr 21;7:46581
pubmed: 28429726
Methods Mol Biol. 2016;1449:161-75
pubmed: 27613034
Elife. 2015 Sep 01;4:
pubmed: 26327695
Ther Adv Hematol. 2016 Aug;7(4):196-208
pubmed: 27493710
Drug Resist Updat. 2015 Jan;18:18-35
pubmed: 25670156
Eur J Haematol. 2018 Mar 30;:
pubmed: 29603798
Clin Cancer Res. 2011 Aug 1;17(15):5101-12
pubmed: 21712452
PLoS One. 2014 Dec 10;9(12):e114964
pubmed: 25494214
Leukemia. 2019 Feb;33(2):447-456
pubmed: 30026573
Annu Rev Biochem. 2017 Jun 20;86:193-224
pubmed: 28460188
J Proteomics. 2012 Jun 6;75(10):2998-3014
pubmed: 22178446
Proteomics. 2010 Aug;10(16):3040-4
pubmed: 20641139
Leukemia. 2014 Oct;28(10):2049-59
pubmed: 24721791
Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):E7490-E7499
pubmed: 27791183
Front Endocrinol (Lausanne). 2018 Jun 29;9:344
pubmed: 30008697
Cancer Cell Int. 2021 Jan 14;21(1):52
pubmed: 33446200
J Proteomics. 2016 Apr 29;139:45-59
pubmed: 26972027
Autophagy. 2017 Apr 3;13(4):759-760
pubmed: 28121483
Autophagy. 2018;14(8):1435-1455
pubmed: 29940786
J Proteomics. 2012 Jul 16;75(13):4176-83
pubmed: 22626983
Free Radic Biol Med. 2011 Oct 1;51(7):1355-64
pubmed: 21767633
Leuk Lymphoma. 2018 Jul;59(7):1726-1729
pubmed: 29164964
Hematol Oncol. 2019 Jun;37 Suppl 1:66-69
pubmed: 31187531
BMC Bioinformatics. 2011 Jan 26;12:35
pubmed: 21269502
J Biol Chem. 2011 Mar 4;286(9):7290-300
pubmed: 21193398
Autophagy. 2015;11(10):1927-8
pubmed: 26291247
Cell. 2017 May 18;169(5):792-806
pubmed: 28525752

Auteurs

Grégoire Quinet (G)

Laboratoire de Chimie de Coordination (LCC) CNRS-UPR8241, UPS, 31400 Toulouse, France.

Wendy Xolalpa (W)

Proteomics Unit, CIC bioGUNE, Parque Tecnológico de Bizkaia, 48160 Derio, Spain.

Diana Reyes-Garau (D)

Lymphoma Translational Group, UBIRed, Josep Carreras Leukaemia Research Institute, 08916 Badalona, Spain.

Núria Profitós-Pelejà (N)

Lymphoma Translational Group, UBIRed, Josep Carreras Leukaemia Research Institute, 08916 Badalona, Spain.

Mikel Azkargorta (M)

Proteomics Platform CICbioGUNE, Basque Research and Technology Alliance (BRTA), CIBERehd, ProteoRed-ISCIII, Parque Tecnológico de Bizkaia, 31400 Derio, Spain.

Laurie Ceccato (L)

Laboratoire de Chimie de Coordination (LCC) CNRS-UPR8241, UPS, 31400 Toulouse, France.

Maria Gonzalez-Santamarta (M)

Laboratoire de Chimie de Coordination (LCC) CNRS-UPR8241, UPS, 31400 Toulouse, France.

Maria Marsal (M)

ICFO-Institut de Ciencies Fotoniques, The Barcelona Institute of Science and Technology, 08860 Castelldefels, Spain.

Jordi Andilla (J)

ICFO-Institut de Ciencies Fotoniques, The Barcelona Institute of Science and Technology, 08860 Castelldefels, Spain.

Fabienne Aillet (F)

Proteomics Unit, CIC bioGUNE, Parque Tecnológico de Bizkaia, 48160 Derio, Spain.

Francesc Bosch (F)

Laboratory of Experimental Hematology, Department of Hematology, Vall d'Hebron Institute of Oncology, Vall d'Hebron University Hospital, 08035 Barcelona, Spain.

Felix Elortza (F)

Proteomics Platform CICbioGUNE, Basque Research and Technology Alliance (BRTA), CIBERehd, ProteoRed-ISCIII, Parque Tecnológico de Bizkaia, 31400 Derio, Spain.

Pablo Loza-Alvarez (P)

ICFO-Institut de Ciencies Fotoniques, The Barcelona Institute of Science and Technology, 08860 Castelldefels, Spain.

Brigitte Sola (B)

INSERM UMR1245, Unicaen, 14000 Caen, France.

Olivier Coux (O)

Centre de Recherche de Biologie Cellulaire de Montpellier (CRBM) CNRS-UMR 5237, Université de Montpellier, 34293 Montpellier, France.

Rune Matthiesen (R)

Computational and Experimental Biology Group, CEDOC-Chronic Diseases Research Center, Faculdade de Ciências Médicas, Universidade Nova de Lisboa, 1150-082 Lisboa, Portugal.

Gaël Roué (G)

Lymphoma Translational Group, UBIRed, Josep Carreras Leukaemia Research Institute, 08916 Badalona, Spain.

Manuel S Rodriguez (MS)

Laboratoire de Chimie de Coordination (LCC) CNRS-UPR8241, UPS, 31400 Toulouse, France.

Classifications MeSH