The decylTPP mitochondria-targeting moiety lowers electron transport chain supercomplex levels in primary human skin fibroblasts

Attachment of cargo molecules to lipophilic triphenylphosphonium (TPP+) cations is a widely applied strategy for mitochondrial targeting. We previously demonstrated that the vitamin E-derived antioxidant Trolox increases the levels of active mitochondrial complex I (CI), the first complex of the ele...

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Published inFree radical biology & medicine Vol. 188; pp. 434 - 446
Main Authors Bulthuis, Elianne P., Einer, Claudia, Distelmaier, Felix, Groh, Laszlo, van Emst - de Vries, Sjenet E., van de Westerlo, Els, van de Wal, Melissa, Wagenaars, Jori, Rodenburg, Richard J., Smeitink, Jan A.M., Riksen, Niels P., Willems, Peter H.G.M., Adjobo-Hermans, Merel J.W., Zischka, Hans, Koopman, Werner J.H.
Format Journal Article
LanguageEnglish
Published Elsevier Inc 01.08.2022
Subjects
Complex I
decylTPP
Glycolysis
Mitochondrial targeting
Supercomplexes
Trolox
CI
LS
decylTPP
OXPHOS
Complex I
MOM
PHSF
MIM
SC
Supercomplexes
Mitochondrial targeting
Δψ
Trolox
ETC
TPP
α-Toc
MD
ROS
Glycolysis
TPMP
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Abstract Attachment of cargo molecules to lipophilic triphenylphosphonium (TPP+) cations is a widely applied strategy for mitochondrial targeting. We previously demonstrated that the vitamin E-derived antioxidant Trolox increases the levels of active mitochondrial complex I (CI), the first complex of the electron transport chain (ETC), in primary human skin fibroblasts (PHSFs) of Leigh Syndrome (LS) patients with isolated CI deficiency. Primed by this finding, we here studied the cellular effects of mitochondria-targeted Trolox (MitoE10), mitochondria-targeted ubiquinone (MitoQ10) and their mitochondria-targeting moiety decylTPP (C10-TPP+). Chronic treatment (96 h) with these molecules of PHSFs from a healthy subject and an LS patient with isolated CI deficiency (NDUFS7-V122M mutation) did not greatly affect cell number. Unexpectedly, this treatment reduced CI levels/activity, lowered the amount of ETC supercomplexes, inhibited mitochondrial oxygen consumption, increased extracellular acidification, altered mitochondrial morphology and stimulated hydroethidine oxidation. We conclude that the mitochondria-targeting decylTPP moiety is responsible for the observed effects and advocate that every study employing alkylTPP-mediated mitochondrial targeting should routinely include control experiments with the corresponding alkylTPP moiety. [Display omitted] •DecylTPP lowers the level of complex I and electron transport chain supercomplexes.•DecylTPP alters mitochondrial membrane potential and size.•DecylTPP reduces mitochondrial oxygen consumption.•DecylTPP lowers mitochondrial ATP generation.•DecylTPP alters hydroethidine oxidation.
AbstractList Attachment of cargo molecules to lipophilic triphenylphosphonium (TPP+) cations is a widely applied strategy for mitochondrial targeting. We previously demonstrated that the vitamin E-derived antioxidant Trolox increases the levels of active mitochondrial complex I (CI), the first complex of the electron transport chain (ETC), in primary human skin fibroblasts (PHSFs) of Leigh Syndrome (LS) patients with isolated CI deficiency. Primed by this finding, we here studied the cellular effects of mitochondria-targeted Trolox (MitoE10), mitochondria-targeted ubiquinone (MitoQ10) and their mitochondria-targeting moiety decylTPP (C10-TPP+). Chronic treatment (96 h) with these molecules of PHSFs from a healthy subject and an LS patient with isolated CI deficiency (NDUFS7-V122M mutation) did not greatly affect cell number. Unexpectedly, this treatment reduced CI levels/activity, lowered the amount of ETC supercomplexes, inhibited mitochondrial oxygen consumption, increased extracellular acidification, altered mitochondrial morphology and stimulated hydroethidine oxidation. We conclude that the mitochondria-targeting decylTPP moiety is responsible for the observed effects and advocate that every study employing alkylTPP-mediated mitochondrial targeting should routinely include control experiments with the corresponding alkylTPP moiety.Attachment of cargo molecules to lipophilic triphenylphosphonium (TPP+) cations is a widely applied strategy for mitochondrial targeting. We previously demonstrated that the vitamin E-derived antioxidant Trolox increases the levels of active mitochondrial complex I (CI), the first complex of the electron transport chain (ETC), in primary human skin fibroblasts (PHSFs) of Leigh Syndrome (LS) patients with isolated CI deficiency. Primed by this finding, we here studied the cellular effects of mitochondria-targeted Trolox (MitoE10), mitochondria-targeted ubiquinone (MitoQ10) and their mitochondria-targeting moiety decylTPP (C10-TPP+). Chronic treatment (96 h) with these molecules of PHSFs from a healthy subject and an LS patient with isolated CI deficiency (NDUFS7-V122M mutation) did not greatly affect cell number. Unexpectedly, this treatment reduced CI levels/activity, lowered the amount of ETC supercomplexes, inhibited mitochondrial oxygen consumption, increased extracellular acidification, altered mitochondrial morphology and stimulated hydroethidine oxidation. We conclude that the mitochondria-targeting decylTPP moiety is responsible for the observed effects and advocate that every study employing alkylTPP-mediated mitochondrial targeting should routinely include control experiments with the corresponding alkylTPP moiety.
Attachment of cargo molecules to lipophilic triphenylphosphonium (TPP+) cations is a widely applied strategy for mitochondrial targeting. We previously demonstrated that the vitamin E-derived antioxidant Trolox increases the levels of active mitochondrial complex I (CI), the first complex of the electron transport chain (ETC), in primary human skin fibroblasts (PHSFs) of Leigh Syndrome (LS) patients with isolated CI deficiency. Primed by this finding, we here studied the cellular effects of mitochondria-targeted Trolox (MitoE10), mitochondria-targeted ubiquinone (MitoQ10) and their mitochondria-targeting moiety decylTPP (C10-TPP+). Chronic treatment (96 h) with these molecules of PHSFs from a healthy subject and an LS patient with isolated CI deficiency (NDUFS7-V122M mutation) did not greatly affect cell number. Unexpectedly, this treatment reduced CI levels/activity, lowered the amount of ETC supercomplexes, inhibited mitochondrial oxygen consumption, increased extracellular acidification, altered mitochondrial morphology and stimulated hydroethidine oxidation. We conclude that the mitochondria-targeting decylTPP moiety is responsible for the observed effects and advocate that every study employing alkylTPP-mediated mitochondrial targeting should routinely include control experiments with the corresponding alkylTPP moiety. [Display omitted] •DecylTPP lowers the level of complex I and electron transport chain supercomplexes.•DecylTPP alters mitochondrial membrane potential and size.•DecylTPP reduces mitochondrial oxygen consumption.•DecylTPP lowers mitochondrial ATP generation.•DecylTPP alters hydroethidine oxidation.
Author Zischka, Hans
Wagenaars, Jori
Groh, Laszlo
van Emst - de Vries, Sjenet E.
Riksen, Niels P.
Smeitink, Jan A.M.
Rodenburg, Richard J.
van de Westerlo, Els
Adjobo-Hermans, Merel J.W.
Bulthuis, Elianne P.
Einer, Claudia
Koopman, Werner J.H.
Willems, Peter H.G.M.
Distelmaier, Felix
van de Wal, Melissa
Author_xml – sequence: 1
  givenname: Elianne P.
  surname: Bulthuis
  fullname: Bulthuis, Elianne P.
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 2
  givenname: Claudia
  surname: Einer
  fullname: Einer, Claudia
  organization: Institute of Molecular Toxicology and Pharmacology, Helmholtz Center Munich, German Research Center for Environmental Health, Neuherberg, Germany
– sequence: 3
  givenname: Felix
  surname: Distelmaier
  fullname: Distelmaier, Felix
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 4
  givenname: Laszlo
  surname: Groh
  fullname: Groh, Laszlo
  organization: Department of Internal Medicine , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 5
  givenname: Sjenet E.
  surname: van Emst - de Vries
  fullname: van Emst - de Vries, Sjenet E.
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 6
  givenname: Els
  surname: van de Westerlo
  fullname: van de Westerlo, Els
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 7
  givenname: Melissa
  surname: van de Wal
  fullname: van de Wal, Melissa
  organization: Department of Pediatrics, Amalia Children's Hospital, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 8
  givenname: Jori
  surname: Wagenaars
  fullname: Wagenaars, Jori
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 9
  givenname: Richard J.
  surname: Rodenburg
  fullname: Rodenburg, Richard J.
  organization: Department of Pediatrics, Amalia Children's Hospital, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 10
  givenname: Jan A.M.
  surname: Smeitink
  fullname: Smeitink, Jan A.M.
  organization: Department of Pediatrics, Amalia Children's Hospital, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 11
  givenname: Niels P.
  surname: Riksen
  fullname: Riksen, Niels P.
  organization: Department of Internal Medicine , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 12
  givenname: Peter H.G.M.
  surname: Willems
  fullname: Willems, Peter H.G.M.
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 13
  givenname: Merel J.W.
  surname: Adjobo-Hermans
  fullname: Adjobo-Hermans, Merel J.W.
  organization: Department of Biochemistry , Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
– sequence: 14
  givenname: Hans
  surname: Zischka
  fullname: Zischka, Hans
  organization: Institute of Molecular Toxicology and Pharmacology, Helmholtz Center Munich, German Research Center for Environmental Health, Neuherberg, Germany
– sequence: 15
  givenname: Werner J.H.
  orcidid: 0000-0002-5340-6747
  surname: Koopman
  fullname: Koopman, Werner J.H.
  email: Werner.Koopman@radboudumc.nl
  organization: Department of Pediatrics, Amalia Children's Hospital, Radboud Institute for Molecular Life Sciences (RIMLS), Radboud Center for Mitochondrial Medicine (RCMM), Radboud University Medical Center (Radboudumc), Nijmegen, the Netherlands
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Keywords CI
LS
decylTPP
OXPHOS
Complex I
MOM
PHSF
MIM
SC
Supercomplexes
Mitochondrial targeting
Δψ
Trolox
ETC
TPP
α-Toc
MD
ROS
Glycolysis
TPMP
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Snippet Attachment of cargo molecules to lipophilic triphenylphosphonium (TPP+) cations is a widely applied strategy for mitochondrial targeting. We previously...
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SubjectTerms Complex I
decylTPP
Glycolysis
Mitochondrial targeting
Supercomplexes
Trolox
Title The decylTPP mitochondria-targeting moiety lowers electron transport chain supercomplex levels in primary human skin fibroblasts
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