Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity

Abstract The mitochondrial chaperone TRAP1 is a key regulator of cellular homeostasis and its activity has important implications in neurodegeneration, ischemia and cancer. Recent evidence has indicated that TRAP1 mutations are involved in several disorders, even though the structural basis for the...

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Main Authors: Claudio Laquatra, Alessia Magro, Federica Guarra, Matteo Lambrughi, Lavinia Ferrone, Giulio Fracasso, Melissa Bacchin, Martina La Spina, Elisabetta Moroni, Elena Papaleo, Giorgio Colombo, Andrea Rasola
Format: Article
Language:English
Published: Nature Publishing Group 2025-03-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07467-6
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author Claudio Laquatra
Alessia Magro
Federica Guarra
Matteo Lambrughi
Lavinia Ferrone
Giulio Fracasso
Melissa Bacchin
Martina La Spina
Elisabetta Moroni
Elena Papaleo
Giorgio Colombo
Andrea Rasola
author_facet Claudio Laquatra
Alessia Magro
Federica Guarra
Matteo Lambrughi
Lavinia Ferrone
Giulio Fracasso
Melissa Bacchin
Martina La Spina
Elisabetta Moroni
Elena Papaleo
Giorgio Colombo
Andrea Rasola
author_sort Claudio Laquatra
collection DOAJ
description Abstract The mitochondrial chaperone TRAP1 is a key regulator of cellular homeostasis and its activity has important implications in neurodegeneration, ischemia and cancer. Recent evidence has indicated that TRAP1 mutations are involved in several disorders, even though the structural basis for the impact of point mutations on TRAP1 functions has never been studied. By exploiting a modular structure-based framework and molecular dynamics simulations, we investigated the effect of five TRAP1 mutations on its structure and stability. Each mutation differentially impacts long-range interactions, intra and inter-protomer dynamics and ATPase activity. Changes in these parameters influence TRAP1 functions, as revealed by their effects on the activity of the TRAP1 interactor succinate dehydrogenase (SDH). In keeping with this, TRAP1 point mutations affect the growth and migration of aggressive sarcoma cells, and alter sensitivity to a selective TRAP1 inhibitor. Our work provides new insights on the structure-activity relationship of TRAP1, identifying crucial amino acid residues that regulate TRAP1 proteostatic functions and pro-neoplastic activity.
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publisher Nature Publishing Group
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series Cell Death and Disease
spelling doaj-art-b2573b22e46a46b6a64a87c72b7392bf2025-08-20T02:56:20ZengNature Publishing GroupCell Death and Disease2041-48892025-03-0116111210.1038/s41419-025-07467-6Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activityClaudio Laquatra0Alessia Magro1Federica Guarra2Matteo Lambrughi3Lavinia Ferrone4Giulio Fracasso5Melissa Bacchin6Martina La Spina7Elisabetta Moroni8Elena Papaleo9Giorgio Colombo10Andrea Rasola11Department of Biomedical Sciences, University of PadovaDepartment of Biomedical Sciences, University of PadovaDepartment of Chemistry, University of PaviaCancer Structural Biology, Danish Cancer InstituteDepartment of Biomedical Sciences, University of PadovaDepartment of Biomedical Sciences, University of PadovaDepartment of Biomedical Sciences, University of PadovaDepartment of Biomedical Sciences, University of PadovaSCITEC-CNRCancer Structural Biology, Danish Cancer InstituteDepartment of Chemistry, University of PaviaDepartment of Biomedical Sciences, University of PadovaAbstract The mitochondrial chaperone TRAP1 is a key regulator of cellular homeostasis and its activity has important implications in neurodegeneration, ischemia and cancer. Recent evidence has indicated that TRAP1 mutations are involved in several disorders, even though the structural basis for the impact of point mutations on TRAP1 functions has never been studied. By exploiting a modular structure-based framework and molecular dynamics simulations, we investigated the effect of five TRAP1 mutations on its structure and stability. Each mutation differentially impacts long-range interactions, intra and inter-protomer dynamics and ATPase activity. Changes in these parameters influence TRAP1 functions, as revealed by their effects on the activity of the TRAP1 interactor succinate dehydrogenase (SDH). In keeping with this, TRAP1 point mutations affect the growth and migration of aggressive sarcoma cells, and alter sensitivity to a selective TRAP1 inhibitor. Our work provides new insights on the structure-activity relationship of TRAP1, identifying crucial amino acid residues that regulate TRAP1 proteostatic functions and pro-neoplastic activity.https://doi.org/10.1038/s41419-025-07467-6
spellingShingle Claudio Laquatra
Alessia Magro
Federica Guarra
Matteo Lambrughi
Lavinia Ferrone
Giulio Fracasso
Melissa Bacchin
Martina La Spina
Elisabetta Moroni
Elena Papaleo
Giorgio Colombo
Andrea Rasola
Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity
Cell Death and Disease
title Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity
title_full Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity
title_fullStr Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity
title_full_unstemmed Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity
title_short Point mutations of the mitochondrial chaperone TRAP1 affect its functions and pro-neoplastic activity
title_sort point mutations of the mitochondrial chaperone trap1 affect its functions and pro neoplastic activity
url https://doi.org/10.1038/s41419-025-07467-6
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