Sex hormone-related neurosteroids differentially rescue bioenergetic deficits induced by amyloid-β or hyperphosphorylated tau protein
Identifieur interne : 002841 ( Main/Exploration ); précédent : 002840; suivant : 002842Sex hormone-related neurosteroids differentially rescue bioenergetic deficits induced by amyloid-β or hyperphosphorylated tau protein
Auteurs : Amandine Grimm [Suisse, France] ; Emily E. Biliouris [Suisse] ; Undine E. Lang [Suisse] ; Jürgen Götz ; Ayikoe Guy Mensah-Nyagan [France] ; Anne Eckert [Suisse]Source :
- Cellular and Molecular Life Sciences [ 1420-682X ] ; 2015.
Descripteurs français
- KwdFr :
- Adénosine triphosphate (métabolisme), Agents neuromédiateurs (métabolisme), Hormones sexuelles stéroïdiennes (métabolisme), Humains, Lignée cellulaire, Maladie d'Alzheimer (anatomopathologie), Maladie d'Alzheimer (génétique), Maladie d'Alzheimer (métabolisme), Mutation ponctuelle, Métabolisme énergétique, Neurones (anatomopathologie), Neurones (métabolisme), Phosphorylation, Potentiel de membrane mitochondriale, Protéines tau (génétique), Protéines tau (métabolisme), Précurseur de la protéine bêta-amyloïde (génétique), Précurseur de la protéine bêta-amyloïde (métabolisme), Régulation positive.
- MESH :
- anatomopathologie : Maladie d'Alzheimer, Neurones.
- génétique : Maladie d'Alzheimer, Protéines tau, Précurseur de la protéine bêta-amyloïde.
- métabolisme : Adénosine triphosphate, Agents neuromédiateurs, Hormones sexuelles stéroïdiennes, Maladie d'Alzheimer, Neurones, Protéines tau, Précurseur de la protéine bêta-amyloïde.
- Humains, Lignée cellulaire, Mutation ponctuelle, Métabolisme énergétique, Phosphorylation, Potentiel de membrane mitochondriale, Régulation positive.
English descriptors
- KwdEn :
- Adenosine Triphosphate (metabolism), Alzheimer Disease (genetics), Alzheimer Disease (metabolism), Alzheimer Disease (pathology), Amyloid beta-Protein Precursor (genetics), Amyloid beta-Protein Precursor (metabolism), Cell Line, Energy Metabolism, Gonadal Steroid Hormones (metabolism), Humans, Membrane Potential, Mitochondrial, Neurons (metabolism), Neurons (pathology), Neurotransmitter Agents (metabolism), Phosphorylation, Point Mutation, Up-Regulation, tau Proteins (genetics), tau Proteins (metabolism).
- MESH :
- chemical , genetics : Amyloid beta-Protein Precursor, tau Proteins.
- chemical , metabolism : Adenosine Triphosphate, Amyloid beta-Protein Precursor, Gonadal Steroid Hormones, Neurotransmitter Agents, tau Proteins.
- genetics : Alzheimer Disease.
- metabolism : Alzheimer Disease, Neurons.
- pathology : Alzheimer Disease, Neurons.
- Cell Line, Energy Metabolism, Humans, Membrane Potential, Mitochondrial, Phosphorylation, Point Mutation, Up-Regulation.
Abstract
Alzheimer’s disease (AD) is an age-related neurodegenerative disease marked by a progressive cognitive decline. Metabolic impairments are common hallmarks of AD, and amyloid-β (Aβ) peptide and hyperphosphorylated tau protein—the two foremost histopathological signs of AD—have been implicated in mitochondrial dysfunction. Neurosteroids have recently shown promise in alleviating cognitive and neuronal sequelae of AD. The present study evaluates the impact of neurosteroids belonging to the sex hormone family (progesterone, estradiol, estrone, testosterone, 3α-androstanediol) on mitochondrial dysfunction in cellular models of AD: human neuroblastoma cells (SH-SY5Y) stably transfected with constructs encoding (1) the human amyloid precursor protein (APP) resulting in overexpression of APP and Aβ, (2) wild-type tau (wtTau), and (3) mutant tau (P301L), that induces abnormal tau hyperphosphorylation. We show that while APP and P301L cells both display a drop in ATP levels, they present distinct mitochondrial impairments with regard to their bioenergetic profiles. The P301L cells presented a decreased maximal respiration and spare respiratory capacity, while APP cells exhibited, in addition, a decrease in basal respiration, ATP turnover, and glycolytic reserve. All neurosteroids showed beneficial effects on ATP production and mitochondrial membrane potential in APP/Aβ overexpressing cells while only progesterone and estradiol increased ATP levels in mutant tau cells. Of note, testosterone was more efficient in alleviating Aβ-induced mitochondrial deficits, while progesterone and estrogen were the most effective neurosteroids in our model of AD-related tauopathy. Our findings lend further support to the neuroprotective effects of neurosteroids in AD and may open new avenues for the development of gender-specific therapeutic approaches in AD.
The online version of this article (doi:10.1007/s00018-015-1988-x) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1007/s00018-015-1988-x
PubMed: 26198711
PubMed Central: 4700074
Affiliations:
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last="Grimm">Amandine Grimm</name><affiliation wicri:level="1"><nlm:aff id="Aff1">Neurobiology Laboratory for Brain Aging and Mental Health, Transfaculty Research Platform, Molecular and Cognitive Neuroscience, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Neurobiology Laboratory for Brain Aging and Mental Health, Transfaculty Research Platform, Molecular and Cognitive Neuroscience, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2">Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="Aff3">Biopathologie de la Myéline, Neuroprotection et Stratégies Thérapeutiques, INSERM U1119, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Bâtiment 3 de la Faculté de Médecine, 11 rue Humann, 67 000 Strasbourg, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biopathologie de la Myéline, Neuroprotection et Stratégies Thérapeutiques, INSERM U1119, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Bâtiment 3 de la Faculté de Médecine, 11 rue Humann, 67 000 Strasbourg</wicri:regionArea><wicri:noRegion>67 000 Strasbourg</wicri:noRegion><orgName type="university">Université de Strasbourg</orgName><placeName><settlement type="city">Strasbourg</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Alsace (région administrative)</region></placeName></affiliation></author><author><name sortKey="Biliouris, Emily E" sort="Biliouris, Emily E" uniqKey="Biliouris E" first="Emily E." last="Biliouris">Emily E. Biliouris</name><affiliation wicri:level="1"><nlm:aff id="Aff1">Neurobiology Laboratory for Brain Aging and Mental Health, Transfaculty Research Platform, Molecular and Cognitive Neuroscience, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Neurobiology Laboratory for Brain Aging and Mental Health, Transfaculty Research Platform, Molecular and Cognitive Neuroscience, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2">Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation></author><author><name sortKey="Lang, Undine E" sort="Lang, Undine E" uniqKey="Lang U" first="Undine E." last="Lang">Undine E. Lang</name><affiliation wicri:level="1"><nlm:aff id="Aff2">Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation></author><author><name sortKey="Gotz, Jurgen" sort="Gotz, Jurgen" uniqKey="Gotz J" first="Jürgen" last="Götz">Jürgen Götz</name><affiliation><nlm:aff id="Aff4">Clem Jones Centre for Ageing Dementia Research (CJCADR), Queensland Brain Institute (QBI), The University of Queensland, Brisbane, 4072 QLD Australia</nlm:aff><wicri:noCountry code="subfield">4072 QLD Australia</wicri:noCountry></affiliation></author><author><name sortKey="Mensah Nyagan, Ayikoe Guy" sort="Mensah Nyagan, Ayikoe Guy" uniqKey="Mensah Nyagan A" first="Ayikoe Guy" last="Mensah-Nyagan">Ayikoe Guy Mensah-Nyagan</name><affiliation wicri:level="4"><nlm:aff id="Aff3">Biopathologie de la Myéline, Neuroprotection et Stratégies Thérapeutiques, INSERM U1119, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Bâtiment 3 de la Faculté de Médecine, 11 rue Humann, 67 000 Strasbourg, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Biopathologie de la Myéline, Neuroprotection et Stratégies Thérapeutiques, INSERM U1119, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Bâtiment 3 de la Faculté de Médecine, 11 rue Humann, 67 000 Strasbourg</wicri:regionArea><wicri:noRegion>67 000 Strasbourg</wicri:noRegion><orgName type="university">Université de Strasbourg</orgName><placeName><settlement type="city">Strasbourg</settlement><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Alsace (région administrative)</region></placeName></affiliation></author><author><name sortKey="Eckert, Anne" sort="Eckert, Anne" uniqKey="Eckert A" first="Anne" last="Eckert">Anne Eckert</name><affiliation wicri:level="1"><nlm:aff id="Aff1">Neurobiology Laboratory for Brain Aging and Mental Health, Transfaculty Research Platform, Molecular and Cognitive Neuroscience, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Neurobiology Laboratory for Brain Aging and Mental Health, Transfaculty Research Platform, Molecular and Cognitive Neuroscience, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2">Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel, Switzerland</nlm:aff><country xml:lang="fr">Suisse</country><wicri:regionArea>Psychiatric University Clinics, University of Basel, Wilhelm Klein-Str. 27, 4012 Basel</wicri:regionArea><wicri:noRegion>4012 Basel</wicri:noRegion></affiliation></author></analytic><series><title level="j">Cellular and Molecular Life Sciences</title><idno type="ISSN">1420-682X</idno><idno type="eISSN">1420-9071</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adenosine Triphosphate (metabolism)</term><term>Alzheimer Disease (genetics)</term><term>Alzheimer Disease (metabolism)</term><term>Alzheimer Disease (pathology)</term><term>Amyloid beta-Protein Precursor (genetics)</term><term>Amyloid beta-Protein Precursor (metabolism)</term><term>Cell Line</term><term>Energy Metabolism</term><term>Gonadal Steroid Hormones (metabolism)</term><term>Humans</term><term>Membrane Potential, Mitochondrial</term><term>Neurons (metabolism)</term><term>Neurons (pathology)</term><term>Neurotransmitter Agents (metabolism)</term><term>Phosphorylation</term><term>Point Mutation</term><term>Up-Regulation</term><term>tau Proteins (genetics)</term><term>tau Proteins (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Adénosine triphosphate (métabolisme)</term><term>Agents neuromédiateurs (métabolisme)</term><term>Hormones sexuelles stéroïdiennes (métabolisme)</term><term>Humains</term><term>Lignée cellulaire</term><term>Maladie d'Alzheimer (anatomopathologie)</term><term>Maladie d'Alzheimer (génétique)</term><term>Maladie d'Alzheimer (métabolisme)</term><term>Mutation ponctuelle</term><term>Métabolisme énergétique</term><term>Neurones (anatomopathologie)</term><term>Neurones (métabolisme)</term><term>Phosphorylation</term><term>Potentiel de membrane mitochondriale</term><term>Protéines tau (génétique)</term><term>Protéines tau (métabolisme)</term><term>Précurseur de la protéine bêta-amyloïde (génétique)</term><term>Précurseur de la protéine bêta-amyloïde (métabolisme)</term><term>Régulation positive</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Amyloid beta-Protein Precursor</term><term>tau Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Adenosine Triphosphate</term><term>Amyloid beta-Protein Precursor</term><term>Gonadal Steroid Hormones</term><term>Neurotransmitter Agents</term><term>tau Proteins</term></keywords><keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr"><term>Maladie d'Alzheimer</term><term>Neurones</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Alzheimer Disease</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Maladie d'Alzheimer</term><term>Protéines tau</term><term>Précurseur de la protéine bêta-amyloïde</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Alzheimer Disease</term><term>Neurons</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Adénosine triphosphate</term><term>Agents neuromédiateurs</term><term>Hormones sexuelles stéroïdiennes</term><term>Maladie d'Alzheimer</term><term>Neurones</term><term>Protéines tau</term><term>Précurseur de la protéine bêta-amyloïde</term></keywords><keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Alzheimer Disease</term><term>Neurons</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Cell Line</term><term>Energy Metabolism</term><term>Humans</term><term>Membrane Potential, Mitochondrial</term><term>Phosphorylation</term><term>Point Mutation</term><term>Up-Regulation</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Humains</term><term>Lignée cellulaire</term><term>Mutation ponctuelle</term><term>Métabolisme énergétique</term><term>Phosphorylation</term><term>Potentiel de membrane mitochondriale</term><term>Régulation positive</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Alzheimer’s disease (AD) is an age-related neurodegenerative disease marked by a progressive cognitive decline. Metabolic impairments are common hallmarks of AD, and amyloid-β (Aβ) peptide and hyperphosphorylated tau protein—the two foremost histopathological signs of AD—have been implicated in mitochondrial dysfunction. Neurosteroids have recently shown promise in alleviating cognitive and neuronal sequelae of AD. The present study evaluates the impact of neurosteroids belonging to the sex hormone family (progesterone, estradiol, estrone, testosterone, 3α-androstanediol) on mitochondrial dysfunction in cellular models of AD: human neuroblastoma cells (SH-SY5Y) stably transfected with constructs encoding (1) the human amyloid precursor protein (APP) resulting in overexpression of APP and Aβ, (2) wild-type tau (wtTau), and (3) mutant tau (P301L), that induces abnormal tau hyperphosphorylation. We show that while APP and P301L cells both display a drop in ATP levels, they present distinct mitochondrial impairments with regard to their bioenergetic profiles. The P301L cells presented a decreased maximal respiration and spare respiratory capacity, while APP cells exhibited, in addition, a decrease in basal respiration, ATP turnover, and glycolytic reserve. All neurosteroids showed beneficial effects on ATP production and mitochondrial membrane potential in APP/Aβ overexpressing cells while only progesterone and estradiol increased ATP levels in mutant tau cells. Of note, testosterone was more efficient in alleviating Aβ-induced mitochondrial deficits, while progesterone and estrogen were the most effective neurosteroids in our model of AD-related tauopathy. Our findings lend further support to the neuroprotective effects of neurosteroids in AD and may open new avenues for the development of gender-specific therapeutic approaches in AD.</p><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1007/s00018-015-1988-x) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Prince, M" uniqKey="Prince M">M Prince</name></author><author><name sortKey="Bryce, R" uniqKey="Bryce R">R Bryce</name></author><author><name sortKey="Albanese, E" uniqKey="Albanese E">E Albanese</name></author><author><name sortKey="Wimo, A" uniqKey="Wimo A">A Wimo</name></author><author><name sortKey="Ribeiro, W" uniqKey="Ribeiro W">W Ribeiro</name></author><author><name sortKey="Ferri, Cp" uniqKey="Ferri C">CP Ferri</name></author></analytic></biblStruct><biblStruct><analytic><author><name 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Pr" uniqKey="Asih P">PR Asih</name></author><author><name sortKey="Wahjoepramono, Ej" uniqKey="Wahjoepramono E">EJ Wahjoepramono</name></author><author><name sortKey="Aniwiyanti, V" uniqKey="Aniwiyanti V">V Aniwiyanti</name></author><author><name sortKey="Wijaya, Lk" uniqKey="Wijaya L">LK Wijaya</name></author><author><name sortKey="Ruyck, K" uniqKey="Ruyck K">K Ruyck</name></author><author><name sortKey="Taddei, K" uniqKey="Taddei K">K Taddei</name></author><author><name sortKey="Fuller, Sj" uniqKey="Fuller S">SJ Fuller</name></author><author><name sortKey="Sohrabi, H" uniqKey="Sohrabi H">H Sohrabi</name></author><author><name sortKey="Dhaliwal, Ss" uniqKey="Dhaliwal S">SS Dhaliwal</name></author><author><name sortKey="Verdile, G" uniqKey="Verdile G">G Verdile</name></author><author><name sortKey="Carruthers, M" uniqKey="Carruthers M">M Carruthers</name></author><author><name sortKey="Martins, Rn" uniqKey="Martins R">RN Martins</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rocca, Wa" uniqKey="Rocca W">WA Rocca</name></author><author><name sortKey="Grossardt, Br" uniqKey="Grossardt B">BR Grossardt</name></author><author><name sortKey="Shuster, Lt" uniqKey="Shuster L">LT Shuster</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>France</li><li>Suisse</li></country><region><li>Alsace (région administrative)</li><li>Grand Est</li></region><settlement><li>Strasbourg</li></settlement><orgName><li>Université de Strasbourg</li></orgName></list><tree><noCountry><name sortKey="Gotz, Jurgen" sort="Gotz, Jurgen" uniqKey="Gotz J" first="Jürgen" last="Götz">Jürgen Götz</name></noCountry><country name="Suisse"><noRegion><name sortKey="Grimm, Amandine" sort="Grimm, Amandine" uniqKey="Grimm A" first="Amandine" last="Grimm">Amandine Grimm</name></noRegion><name sortKey="Biliouris, Emily E" sort="Biliouris, Emily E" uniqKey="Biliouris E" first="Emily E." last="Biliouris">Emily E. Biliouris</name><name sortKey="Biliouris, Emily E" sort="Biliouris, Emily E" uniqKey="Biliouris E" first="Emily E." last="Biliouris">Emily E. Biliouris</name><name sortKey="Eckert, Anne" sort="Eckert, Anne" uniqKey="Eckert A" first="Anne" last="Eckert">Anne Eckert</name><name sortKey="Eckert, Anne" sort="Eckert, Anne" uniqKey="Eckert A" first="Anne" last="Eckert">Anne Eckert</name><name sortKey="Grimm, Amandine" sort="Grimm, Amandine" uniqKey="Grimm A" first="Amandine" last="Grimm">Amandine Grimm</name><name sortKey="Lang, Undine E" sort="Lang, Undine E" uniqKey="Lang U" first="Undine E." last="Lang">Undine E. Lang</name></country><country name="France"><region name="Grand Est"><name sortKey="Grimm, Amandine" sort="Grimm, Amandine" uniqKey="Grimm A" first="Amandine" last="Grimm">Amandine Grimm</name></region><name sortKey="Mensah Nyagan, Ayikoe Guy" sort="Mensah Nyagan, Ayikoe Guy" uniqKey="Mensah Nyagan A" first="Ayikoe Guy" last="Mensah-Nyagan">Ayikoe Guy Mensah-Nyagan</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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