Targeting of mitochondrial fission through natural flavanones elicits anti-myeloma activity.

Flavanones Hesperitin Mitochondrial dynamics Multiple myeloma Naringenin

Journal

Journal of translational medicine
ISSN: 1479-5876
Titre abrégé: J Transl Med
Pays: England
ID NLM: 101190741

Informations de publication

Date de publication:
27 Feb 2024
Historique:
received: 25 01 2024
accepted: 21 02 2024
medline: 28 2 2024
pubmed: 28 2 2024
entrez: 27 2 2024
Statut: epublish

Résumé

Mitochondrial alterations, often dependent on unbalanced mitochondrial dynamics, feature in the pathobiology of human cancers, including multiple myeloma (MM). Flavanones are natural flavonoids endowed with mitochondrial targeting activities. Herein, we investigated the capability of Hesperetin (Hes) and Naringenin (Nar), two aglycones of Hesperidin and Naringin flavanone glycosides, to selectively target Drp1, a pivotal regulator of mitochondrial dynamics, prompting anti-MM activity. Molecular docking analyses were performed on the crystallographic structure of Dynamin-1-like protein (Drp1), using Hes and Nar molecular structures. Cell viability and apoptosis were assessed in MM cell lines, or in co-culture systems with primary bone marrow stromal cells, using Cell Titer Glo and Annexin V-7AAD staining, respectively; clonogenicity was determined using methylcellulose colony assays. Transcriptomic analyses were carried out using the Ion AmpliSeq™ platform; mRNA and protein expression levels were determined by quantitative RT-PCR and western blotting, respectively. Mitochondrial architecture was assessed by transmission electron microscopy. Real time measurement of oxygen consumption was performed by high resolution respirometry in living cells. In vivo anti-tumor activity was evaluated in NOD-SCID mice subcutaneously engrafted with MM cells. Hes and Nar were found to accommodate within the GTPase binding site of Drp1, and to inhibit Drp1 expression and activity, leading to hyperfused mitochondria with reduced OXPHOS. In vitro, Hes and Nar reduced MM clonogenicity and viability, even in the presence of patient-derived bone marrow stromal cells, triggering ER stress and apoptosis. Interestingly, Hes and Nar rewired MM cell metabolism through the down-regulation of master transcriptional activators (SREBF-1, c-MYC) of lipogenesis genes. An extract of Tacle, a Citrus variety rich in Hesperidin and Naringin, was capable to recapitulate the phenotypic and molecular perturbations of each flavanone, triggering anti-MM activity in vivo. Hes and Nar inhibit proliferation, rewire the metabolism and induce apoptosis of MM cells via antagonism of the mitochondrial fission driver Drp1. These results provide a framework for the development of natural anti-MM therapeutics targeting aberrant mitochondrial dependencies.

Sections du résumé

BACKGROUND BACKGROUND
Mitochondrial alterations, often dependent on unbalanced mitochondrial dynamics, feature in the pathobiology of human cancers, including multiple myeloma (MM). Flavanones are natural flavonoids endowed with mitochondrial targeting activities. Herein, we investigated the capability of Hesperetin (Hes) and Naringenin (Nar), two aglycones of Hesperidin and Naringin flavanone glycosides, to selectively target Drp1, a pivotal regulator of mitochondrial dynamics, prompting anti-MM activity.
METHODS METHODS
Molecular docking analyses were performed on the crystallographic structure of Dynamin-1-like protein (Drp1), using Hes and Nar molecular structures. Cell viability and apoptosis were assessed in MM cell lines, or in co-culture systems with primary bone marrow stromal cells, using Cell Titer Glo and Annexin V-7AAD staining, respectively; clonogenicity was determined using methylcellulose colony assays. Transcriptomic analyses were carried out using the Ion AmpliSeq™ platform; mRNA and protein expression levels were determined by quantitative RT-PCR and western blotting, respectively. Mitochondrial architecture was assessed by transmission electron microscopy. Real time measurement of oxygen consumption was performed by high resolution respirometry in living cells. In vivo anti-tumor activity was evaluated in NOD-SCID mice subcutaneously engrafted with MM cells.
RESULTS RESULTS
Hes and Nar were found to accommodate within the GTPase binding site of Drp1, and to inhibit Drp1 expression and activity, leading to hyperfused mitochondria with reduced OXPHOS. In vitro, Hes and Nar reduced MM clonogenicity and viability, even in the presence of patient-derived bone marrow stromal cells, triggering ER stress and apoptosis. Interestingly, Hes and Nar rewired MM cell metabolism through the down-regulation of master transcriptional activators (SREBF-1, c-MYC) of lipogenesis genes. An extract of Tacle, a Citrus variety rich in Hesperidin and Naringin, was capable to recapitulate the phenotypic and molecular perturbations of each flavanone, triggering anti-MM activity in vivo.
CONCLUSION CONCLUSIONS
Hes and Nar inhibit proliferation, rewire the metabolism and induce apoptosis of MM cells via antagonism of the mitochondrial fission driver Drp1. These results provide a framework for the development of natural anti-MM therapeutics targeting aberrant mitochondrial dependencies.

Identifiants

pubmed: 38413989
doi: 10.1186/s12967-024-05013-0
pii: 10.1186/s12967-024-05013-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

208

Subventions

Organisme : Associazione Italiana per la Ricerca sul Cancro
ID : IG24449

Informations de copyright

© 2024. The Author(s).

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Auteurs

Roberta Torcasio (R)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy.
Department of Biology, Ecology and Earth Sciences, University of Calabria, Cosenza, Italy.

Maria Eugenia Gallo Cantafio (ME)

Department of Biology, Ecology and Earth Sciences, University of Calabria, Cosenza, Italy.

Claudia Veneziano (C)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy.

Carmela De Marco (C)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy.

Ludovica Ganino (L)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy.

Ilenia Valentino (I)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy.

Maria Antonietta Occhiuzzi (MA)

Department of Pharmacy, Health and Nutritional Sciences, University of Calabria, 87036, Rende, CS, Italy.

Ida Daniela Perrotta (ID)

Department of Biology, Ecology and Earth Sciences, Centre for Microscopy and Microanalysis, University of Calabria, Cosenza, Italy.

Teresa Mancuso (T)

Annunziata" Regional Hospital Cosenza, 87100, Cosenza, Italy.

Filomena Conforti (F)

Department of Pharmacy, Health and Nutritional Sciences, University of Calabria, 87036, Rende, CS, Italy.

Bruno Rizzuti (B)

SS Rende (CS), Department of Physics, CNR-NANOTEC, University of Calabria, Via Pietro Bucci, 87036, Rende, CS, Italy.
Institute for Biocomputation and Physics of Complex Systems (BIFI), Joint Unit GBsC-CSIC-BIFI, University of Zaragoza, 50018, Saragossa, Spain.

Enrica Antonia Martino (EA)

Annunziata" Regional Hospital Cosenza, 87100, Cosenza, Italy.

Massimo Gentile (M)

Department of Pharmacy, Health and Nutritional Sciences, University of Calabria, 87036, Rende, CS, Italy.
Annunziata" Regional Hospital Cosenza, 87100, Cosenza, Italy.

Antonino Neri (A)

Scientific Directorate, IRCCS Di Reggio Emilia, Emilia Romagna, Reggio Emilia, Italy.

Giuseppe Viglietto (G)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy.

Fedora Grande (F)

Department of Pharmacy, Health and Nutritional Sciences, University of Calabria, 87036, Rende, CS, Italy.

Nicola Amodio (N)

Department of Experimental and Clinical Medicine, University Magna Graecia of Catanzaro, Viale Europa, Campus Germaneto, 88100, Catanzaro, Italy. amodio@unicz.it.

Classifications MeSH