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000139474 0247_ $$2doi$$a10.1093/brain/awx202
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000139474 037__ $$aDZNE-2020-05796
000139474 041__ $$aEnglish
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000139474 1001_ $$0P:(DE-2719)2812175$$aFitzgerald, Julia$$b0$$eFirst author
000139474 245__ $$aMetformin reverses TRAP1 mutation-associated alterations in mitochondrial function in Parkinson's disease.
000139474 260__ $$aOxford$$bOxford Univ. Press$$c2017
000139474 264_1 $$2Crossref$$3online$$bOxford University Press (OUP)$$c2017-08-24
000139474 264_1 $$2Crossref$$3print$$bOxford University Press (OUP)$$c2017-09-01
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000139474 520__ $$aThe mitochondrial proteins TRAP1 and HTRA2 have previously been shown to be phosphorylated in the presence of the Parkinson's disease kinase PINK1 but the downstream signalling is unknown. HTRA2 and PINK1 loss of function causes parkinsonism in humans and animals. Here, we identified TRAP1 as an interactor of HTRA2 using an unbiased mass spectrometry approach. In our human cell models, TRAP1 overexpression is protective, rescuing HTRA2 and PINK1-associated mitochondrial dysfunction and suggesting that TRAP1 acts downstream of HTRA2 and PINK1. HTRA2 regulates TRAP1 protein levels, but TRAP1 is not a direct target of HTRA2 protease activity. Following genetic screening of Parkinson's disease patients and healthy controls, we also report the first TRAP1 mutation leading to complete loss of functional protein in a patient with late onset Parkinson's disease. Analysis of fibroblasts derived from the patient reveal that oxygen consumption, ATP output and reactive oxygen species are increased compared to healthy individuals. This is coupled with an increased pool of free NADH, increased mitochondrial biogenesis, triggering of the mitochondrial unfolded protein response, loss of mitochondrial membrane potential and sensitivity to mitochondrial removal and apoptosis. These data highlight the role of TRAP1 in the regulation of energy metabolism and mitochondrial quality control. Interestingly, the diabetes drug metformin reverses mutation-associated alterations on energy metabolism, mitochondrial biogenesis and restores mitochondrial membrane potential. In summary, our data show that TRAP1 acts downstream of PINK1 and HTRA2 for mitochondrial fine tuning, whereas TRAP1 loss of function leads to reduced control of energy metabolism, ultimately impacting mitochondrial membrane potential. These findings offer new insight into mitochondrial pathologies in Parkinson's disease and provide new prospects for targeted therapies.
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000139474 650_7 $$2NLM Chemicals$$aHSP90 Heat-Shock Proteins
000139474 650_7 $$2NLM Chemicals$$aMitochondrial Proteins
000139474 650_7 $$2NLM Chemicals$$aReactive Oxygen Species
000139474 650_7 $$2NLM Chemicals$$aTRAP1 protein, human
000139474 650_7 $$00U46U6E8UK$$2NLM Chemicals$$aNAD
000139474 650_7 $$08L70Q75FXE$$2NLM Chemicals$$aAdenosine Triphosphate
000139474 650_7 $$09100L32L2N$$2NLM Chemicals$$aMetformin
000139474 650_7 $$0EC 2.7.-$$2NLM Chemicals$$aProtein Kinases
000139474 650_7 $$0EC 2.7.11.1$$2NLM Chemicals$$aPTEN-induced putative kinase
000139474 650_7 $$0EC 3.4.21.-$$2NLM Chemicals$$aSerine Endopeptidases
000139474 650_7 $$0EC 3.4.21.108$$2NLM Chemicals$$aHTRA2 protein, human
000139474 650_7 $$0EC 3.4.21.108$$2NLM Chemicals$$aHigh-Temperature Requirement A Serine Peptidase 2
000139474 650_2 $$2MeSH$$aAdenosine Triphosphate: metabolism
000139474 650_2 $$2MeSH$$aApoptosis: drug effects
000139474 650_2 $$2MeSH$$aCase-Control Studies
000139474 650_2 $$2MeSH$$aCells, Cultured
000139474 650_2 $$2MeSH$$aFibroblasts: metabolism
000139474 650_2 $$2MeSH$$aHSP90 Heat-Shock Proteins: biosynthesis
000139474 650_2 $$2MeSH$$aHSP90 Heat-Shock Proteins: genetics
000139474 650_2 $$2MeSH$$aHigh-Temperature Requirement A Serine Peptidase 2
000139474 650_2 $$2MeSH$$aHumans
000139474 650_2 $$2MeSH$$aMembrane Potential, Mitochondrial: physiology
000139474 650_2 $$2MeSH$$aMetformin: therapeutic use
000139474 650_2 $$2MeSH$$aMitochondria: drug effects
000139474 650_2 $$2MeSH$$aMitochondria: genetics
000139474 650_2 $$2MeSH$$aMitochondria: metabolism
000139474 650_2 $$2MeSH$$aMitochondrial Proteins: metabolism
000139474 650_2 $$2MeSH$$aMutation
000139474 650_2 $$2MeSH$$aNAD: metabolism
000139474 650_2 $$2MeSH$$aOrganelle Biogenesis
000139474 650_2 $$2MeSH$$aOxygen Consumption
000139474 650_2 $$2MeSH$$aParkinson Disease: drug therapy
000139474 650_2 $$2MeSH$$aParkinson Disease: genetics
000139474 650_2 $$2MeSH$$aParkinson Disease: metabolism
000139474 650_2 $$2MeSH$$aProtein Kinases: metabolism
000139474 650_2 $$2MeSH$$aReactive Oxygen Species: metabolism
000139474 650_2 $$2MeSH$$aSerine Endopeptidases: metabolism
000139474 7001_ $$0P:(DE-HGF)0$$aZimprich, Alexander$$b1
000139474 7001_ $$0P:(DE-HGF)0$$aCarvajal Berrio, Daniel A$$b2
000139474 7001_ $$0P:(DE-2719)9000285$$aSchindler, Kevin M$$b3
000139474 7001_ $$0P:(DE-2719)9000205$$aMaurer, Brigitte$$b4
000139474 7001_ $$0P:(DE-2719)9000366$$aSchulte, Claudia$$b5
000139474 7001_ $$0P:(DE-2719)2811284$$aBus, Christine$$b6
000139474 7001_ $$0P:(DE-2719)2351249$$aHauser, Ann-Kathrin$$b7
000139474 7001_ $$0P:(DE-2719)9000170$$aKübler, Manuela$$b8
000139474 7001_ $$0P:(DE-2719)9000185$$aLewin, Rahel$$b9
000139474 7001_ $$0P:(DE-HGF)0$$aBobbili, Dheeraj Reddy$$b10
000139474 7001_ $$0P:(DE-2719)9000438$$aSchwarz, Lisa M$$b11
000139474 7001_ $$0P:(DE-HGF)0$$aVartholomaiou, Evangelia$$b12
000139474 7001_ $$0P:(DE-2719)2811916$$aBrockmann, Kathrin$$b13
000139474 7001_ $$0P:(DE-2719)9000353$$aWüst, Richard$$b14
000139474 7001_ $$0P:(DE-HGF)0$$aMadlung, Johannes$$b15
000139474 7001_ $$0P:(DE-HGF)0$$aNordheim, Alfred$$b16
000139474 7001_ $$0P:(DE-HGF)0$$aRiess, Olaf$$b17
000139474 7001_ $$0P:(DE-HGF)0$$aMartins, L Miguel$$b18
000139474 7001_ $$0P:(DE-HGF)0$$aGlaab, Enrico$$b19
000139474 7001_ $$0P:(DE-HGF)0$$aMay, Patrick$$b20
000139474 7001_ $$0P:(DE-HGF)0$$aSchenke-Layland, Katja$$b21
000139474 7001_ $$0P:(DE-HGF)0$$aPicard, Didier$$b22
000139474 7001_ $$0P:(DE-HGF)0$$aSharma, Manu$$b23
000139474 7001_ $$0P:(DE-2719)2320009$$aGasser, Thomas$$b24
000139474 7001_ $$0P:(DE-2719)2811170$$aKrüger, Rejko$$b25$$eLast author
000139474 77318 $$2Crossref$$3journal-article$$a10.1093/brain/awx202$$b : Oxford University Press (OUP), 2017-08-24$$n9$$p2444-2459$$tBrain$$v140$$x0006-8950$$y2017
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