Mitophagy links oxidative stress conditions and neurodegenerative diseases
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摘要
Mitophagy is activated by a number of stimuli, including hypoxia, energy stress, and increased oxidative phosphorylation activity. Mitophagy is associated with oxidative stress conditions and central neurodegenerative diseases. Proper regulation of mitophagy is crucial for maintaining homeostasis; conversely, inadequate removal of mitochondria through mitophagy leads to the generation of oxidative species, including reactive oxygen species and reactive nitrogen species, resulting in various neurodegenerative diseases, such as Alzheimer's disease, Parkinson's disease, Huntington's disease, and amyotrophic lateral sclerosis. These diseases are most prevalent in older adults whose bodies fail to maintain proper mitophagic functions to combat oxidative species. As mitophagy is essential for normal body function, by targeting mitophagic pathways we can improve these disease conditions. The search for effective remedies to treat these disease conditions is an ongoing process, which is why more studies are needed. Additionally, more relevant studies could help establish therapeutic conditions, which are currently in high demand. In this review, we discuss how mitophagy plays a significant role in homeostasis and how its dysregulation causes neurodegeneration. We also discuss how combating oxidative species and targeting mitophagy can help treat these neurodegenerative diseases.
Mitophagy is activated by a number of stimuli, including hypoxia, energy stress, and increased oxidative phosphorylation activity. Mitophagy is associated with oxidative stress conditions and central neurodegenerative diseases. Proper regulation of mitophagy is crucial for maintaining homeostasis; conversely, inadequate removal of mitochondria through mitophagy leads to the generation of oxidative species, including reactive oxygen species and reactive nitrogen species, resulting in various neurodegenerative diseases, such as Alzheimer's disease, Parkinson's disease, Huntington's disease, and amyotrophic lateral sclerosis. These diseases are most prevalent in older adults whose bodies fail to maintain proper mitophagic functions to combat oxidative species. As mitophagy is essential for normal body function, by targeting mitophagic pathways we can improve these disease conditions. The search for effective remedies to treat these disease conditions is an ongoing process, which is why more studies are needed. Additionally, more relevant studies could help establish therapeutic conditions, which are currently in high demand. In this review, we discuss how mitophagy plays a significant role in homeostasis and how its dysregulation causes neurodegeneration. We also discuss how combating oxidative species and targeting mitophagy can help treat these neurodegenerative diseases.
Mitophagy is activated by a number of stimuli, including hypoxia, energy stress, and increased oxidative phosphorylation activity. Mitophagy is associated with oxidative stress conditions and central neurodegenerative diseases. Proper regulation of mitophagy is crucial for maintaining homeostasis; conversely, inadequate removal of mitochondria through mitophagy leads to the generation of oxidative species, including reactive oxygen species and reactive nitrogen species, resulting in various neurodegenerative diseases, such as Alzheimer's disease, Parkinson's disease, Huntington's disease, and amyotrophic lateral sclerosis. These diseases are most prevalent in older adults whose bodies fail to maintain proper mitophagic functions to combat oxidative species. As mitophagy is essential for normal body function, by targeting mitophagic pathways we can improve these disease conditions. The search for effective remedies to treat these disease conditions is an ongoing process, which is why more studies are needed. Additionally, more relevant studies could help establish therapeutic conditions, which are currently in high demand. In this review, we discuss how mitophagy plays a significant role in homeostasis and how its dysregulation causes neurodegeneration. We also discuss how combating oxidative species and targeting mitophagy can help treat these neurodegenerative diseases.
引文
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Albers DS,Beal MF(2000)Mitochondrial dysfunction and oxidative stress in aging and neurodegenerative disease.J Neural Transm Suppl59:133-154.
Aso E,Ferrer I(2014)Cannabinoids for treatment of Alzheimer’s disease:Moving toward the clinic.Front Pharmacol 5:37.
Barsoum MJ,Yuan H,Gerencser AA,Liot G,Kushnareva Y,Gr?ber S,Kovacs I,Lee WD,Waggoner J,Cui J(2006)Nitric oxide‐induced mitochondrial fission is regulated by dynamin‐related GTPases in neurons.EMBO J 25:3900-3911.
Butler D,Nixon RA,Bahr BA(2006)Potential compensatory responses through autophagic/lysosomal pathways in neurodegenerative diseases.Autophagy 2:234-237.
Butterfield DA,Lauderback CM(2002)Lipid peroxidation and protein oxidation in Alzheimer’s disease brain:potential causes and consequences involving amyloidβ-peptide-associated free radical oxidative stress 1,2.Free Radic Biol Med 32:1050-1060.
CarrìMT,D’Ambrosi N,Cozzolino M(2017)Pathways to mitochondrial dysfunction in ALS pathogenesis.Biochem Biophys Res Commun483:1187-1193.
Chu CT(2018)Multiple pathways for mitophagy:A neurodegenerative conundrum for Parkinson’s disease.Neurosci Lett pii:S0304-3940(18)30259-3.
Chu CT,Bayir H,Kagan VE(2014)LC3 binds externalized cardiolipin on injured mitochondria to signal mitophagy in neurons:Implications for Parkinson disease.Autophagy 10:376-378.
Chu CT,Ji J,Dagda RK,Jiang JF,Tyurina YY,Kapralov AA,Tyurin VA,Yanamala N,Shrivastava IH,Mohammadyani D(2013)Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells.Nat Cell Biol 15:1197-1205.
Chu CT,Zhu J,Dagda R(2007)Beclin 1-independent pathway of damage-induced mitophagy and autophagic stress:Implications for neurodegeneration and cell death.Autophagy 3:663-666.
Dagda RK,Cherra SJ,Kulich SM,Tandon A,Park D,Chu CT(2009)Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission.J Biol Chem 284:13843-13855.
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Davis SA,Itaman S,Khalid-Janney CM,Sherard JA,Dowell JA,Cairns NJ,Gitcho MA(2018)TDP-43 interacts with mitochondrial proteins critical for mitophagy and mitochondrial dynamics.Neurosci Lett678:8-15.
Devine MJ,Kittler JT(2018)Mitochondria at the neuronal presynapse in health and disease.Nat Rev Neurosci 19:63-80.
Di RA,D’Acunzo P,Simula L,Campello S,Strappazzon F,Cecconi F(2018)AMBRA1-mediated mitophagy counteracts oxidative stress and apoptosis induced by neurotoxicity in human neuroblastoma SH-SY5Y cells.Front Cell Neurosci 12:92.
Dikic I,Elazar Z(2018)Mechanism and medical implications of mammalian autophagy.Nat Rev Mol Cell Biol 19:349-364.
Duchen MR(2012)Mitochondria,calcium-dependent neuronal death and neurodegenerative disease.Pflugers Arch Eur J Physiol 464:111-121.
Eiyama A,Okamoto K(2015)PINK1/Parkin-mediated mitophagy in mammalian cells.Curr Opin Cell Biol 33:95-101.
Finkel T,Holbrook NJ(2000)Oxidants,oxidative stress and the biology of ageing.Nature 408:239-247.
Fivenson EM,Lautrup S,Sun N,Scheibye-Knudsen M,Stevnsner T,Nilsen H,Bohr VA,Fang EF(2017)Mitophagy in neurodegeneration and aging.Neurochem Int 109:202-209.
Gaki GS,Papavassiliou AG(2014)Oxidative stress-induced signaling pathways implicated in the pathogenesis of Parkinson’s disease.Neuromolecular Med 16:217-230.
García-Escudero V,Martín-Maestro P,Perry G,Avila J(2013)Deconstructing mitochondrial dysfunction in Alzheimer disease.Oxid Med Cell Longev 2013:162152.
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Guareschi S,Cova E,Cereda C,Ceroni M,Donetti E,Bosco DA,Trotti D,Pasinelli P(2012)An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1.Proc Natl Acad Sci U S A109:5074-5079.
Hetz C,Chevet E,Harding HP(2013)Targeting the unfolded protein response in disease.Nat Rev Drug Discov 12:703-719.
Hong K,Li Y,Duan W,Guo Y,Jiang H,Li W,Li C(2012)Full-length TDP-43 and its C-terminal fragments activate mitophagy in NSC34cell line.Neurosci Lett 530:144-149.
Hsieh CH,Shaltouki A,Gonzalez AE,da Cruz AB,Burbulla LF,Lawrence ES,Schüle B,Krainc D,Palmer TD,Wang X(2016)Functional impairment in Miro degradation and mitophagy is a shared feature in familial and sporadic Parkinson’s disease.Cell Stem Cell 19:709-724.
Iijima-Ando K,Sekiya M,Maruko-Otake A,Ohtake Y,Suzuki E,Lu B,Iijima KM(2012)Loss of axonal mitochondria promotes tau-mediated neurodegeneration and Alzheimer’s disease-related tau phosphorylation via PAR-1.PLoS Genet 8:e1002918.
Jahani-Asl A,Cheung ECC,Neuspiel M,MacLaurin JG,Fortin A,Park DS,McBride HM,Slack RS(2007)Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death.J Biol Chem282:23788-23798.
Johri A,Chandra A,Beal MF(2013)PGC-1α,mitochondrial dysfunction,and Huntington’s disease.Free Radic Biol Med 62:37-46.
Julien JP(2007)ALS:astrocytes move in as deadly neighbors.Nat Neurosci 10:535-537.
Kahle PJ,Waak J,Gasser T(2009)DJ-1 and prevention of oxidative stress in Parkinson’s disease and other age-related disorders.Free Radic Biol Med 47:1354-1361.
Kamat PK,Kalani A,Kyles P,Tyagi SC,Tyagi N(2014)Autophagy of mitochondria:a promising therapeutic target for neurodegenerative disease.Cell Biochem Biophys 70:707-719.
Kay L,Pienaar IS,Cooray R,Black G,Soundararajan M(2018)Understanding miro GTPases:implications in the treatment of neurodegenerative disorders.Mol Neurobiol 55:7352-7365.
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Kitagishi Y,Nakano N,Ogino M,Ichimura M,Minami A,Matsuda S(2017)PINK1 signaling in mitochondrial homeostasis and in aging.Int J Mol Med 39:3-8.
Koentjoro B,Park JS,Sue CM(2017)Nix restores mitophagy and mitochondrial function to protect against PINK1/Parkin-related Parkinson’s disease.Sci Rep 7:44373.
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Kubli DA,Gustafsson?B(2012)Mitochondria and mitophagy:The yin and yang of cell death control.Circ Res 111:1208-1221.
Lazarou M,Jin SM,Kane LA,Youle RJ(2012)Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin.Dev Cell 22:320-333.
Lee JA(2009)Autophagy in neurodegeneration:Two sides of the same coin.BMB Rep 42:324-330.
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Lemasters JJ(2005)Selective mitochondrial autophagy,or mitophagy,as a targeted defense against oxidative stress,mitochondrial dysfunction,and aging.Rejuvenation Res 8:3-5.
Li L,Hu G(2015)Pink1 protects cortical neurons from thapsigargin-induced oxidative stress and neuronal apoptosis.Biosci Rep 35.pii:e00174.
Li Q,Zhang T,Wang J,Zhang Z,Zhai Y,Yang GY,Sun X(2014)Rapamycin attenuates mitochondrial dysfunction via activation of mitophagy in experimental ischemic stroke.Biochem Biophys Res Commun444:182-188.
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CarrìMT,D’Ambrosi N,Cozzolino M(2017)Pathways to mitochondrial dysfunction in ALS pathogenesis.Biochem Biophys Res Commun483:1187-1193.
Chu CT(2018)Multiple pathways for mitophagy:A neurodegenerative conundrum for Parkinson’s disease.Neurosci Lett pii:S0304-3940(18)30259-3.
Chu CT,Bayir H,Kagan VE(2014)LC3 binds externalized cardiolipin on injured mitochondria to signal mitophagy in neurons:Implications for Parkinson disease.Autophagy 10:376-378.
Chu CT,Ji J,Dagda RK,Jiang JF,Tyurina YY,Kapralov AA,Tyurin VA,Yanamala N,Shrivastava IH,Mohammadyani D(2013)Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells.Nat Cell Biol 15:1197-1205.
Chu CT,Zhu J,Dagda R(2007)Beclin 1-independent pathway of damage-induced mitophagy and autophagic stress:Implications for neurodegeneration and cell death.Autophagy 3:663-666.
Dagda RK,Cherra SJ,Kulich SM,Tandon A,Park D,Chu CT(2009)Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission.J Biol Chem 284:13843-13855.
Dai DF,Chiao YA,Marcinek DJ,Szeto HH,Rabinovitch PS(2014)Mitochondrial oxidative stress in aging and healthspan.Longev Healthspan 3:6.
Davis SA,Itaman S,Khalid-Janney CM,Sherard JA,Dowell JA,Cairns NJ,Gitcho MA(2018)TDP-43 interacts with mitochondrial proteins critical for mitophagy and mitochondrial dynamics.Neurosci Lett678:8-15.
Devine MJ,Kittler JT(2018)Mitochondria at the neuronal presynapse in health and disease.Nat Rev Neurosci 19:63-80.
Di RA,D’Acunzo P,Simula L,Campello S,Strappazzon F,Cecconi F(2018)AMBRA1-mediated mitophagy counteracts oxidative stress and apoptosis induced by neurotoxicity in human neuroblastoma SH-SY5Y cells.Front Cell Neurosci 12:92.
Dikic I,Elazar Z(2018)Mechanism and medical implications of mammalian autophagy.Nat Rev Mol Cell Biol 19:349-364.
Duchen MR(2012)Mitochondria,calcium-dependent neuronal death and neurodegenerative disease.Pflugers Arch Eur J Physiol 464:111-121.
Eiyama A,Okamoto K(2015)PINK1/Parkin-mediated mitophagy in mammalian cells.Curr Opin Cell Biol 33:95-101.
Finkel T,Holbrook NJ(2000)Oxidants,oxidative stress and the biology of ageing.Nature 408:239-247.
Fivenson EM,Lautrup S,Sun N,Scheibye-Knudsen M,Stevnsner T,Nilsen H,Bohr VA,Fang EF(2017)Mitophagy in neurodegeneration and aging.Neurochem Int 109:202-209.
Gaki GS,Papavassiliou AG(2014)Oxidative stress-induced signaling pathways implicated in the pathogenesis of Parkinson’s disease.Neuromolecular Med 16:217-230.
García-Escudero V,Martín-Maestro P,Perry G,Avila J(2013)Deconstructing mitochondrial dysfunction in Alzheimer disease.Oxid Med Cell Longev 2013:162152.
Geisler S,Holmstr?m KM,Treis A,Skujat D,Weber SS,Fiesel FC,Kahle PJ,Springer W(2010)The PINK1/Parkin-mediated mitophagy is compromised by PD-associated mutations.Autophagy 6:871-878.
Greene AW,Grenier K,Aguileta MA,Muise S,Farazifard R,Haque ME,McBride HM,Park DS,Fon EA(2012)Mitochondrial processing peptidase regulates PINK1 processing,import and Parkin recruitment.EMBO Rep 13:378-385.
Guareschi S,Cova E,Cereda C,Ceroni M,Donetti E,Bosco DA,Trotti D,Pasinelli P(2012)An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1.Proc Natl Acad Sci U S A109:5074-5079.
Hetz C,Chevet E,Harding HP(2013)Targeting the unfolded protein response in disease.Nat Rev Drug Discov 12:703-719.
Hong K,Li Y,Duan W,Guo Y,Jiang H,Li W,Li C(2012)Full-length TDP-43 and its C-terminal fragments activate mitophagy in NSC34cell line.Neurosci Lett 530:144-149.
Hsieh CH,Shaltouki A,Gonzalez AE,da Cruz AB,Burbulla LF,Lawrence ES,Schüle B,Krainc D,Palmer TD,Wang X(2016)Functional impairment in Miro degradation and mitophagy is a shared feature in familial and sporadic Parkinson’s disease.Cell Stem Cell 19:709-724.
Iijima-Ando K,Sekiya M,Maruko-Otake A,Ohtake Y,Suzuki E,Lu B,Iijima KM(2012)Loss of axonal mitochondria promotes tau-mediated neurodegeneration and Alzheimer’s disease-related tau phosphorylation via PAR-1.PLoS Genet 8:e1002918.
Jahani-Asl A,Cheung ECC,Neuspiel M,MacLaurin JG,Fortin A,Park DS,McBride HM,Slack RS(2007)Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death.J Biol Chem282:23788-23798.
Johri A,Chandra A,Beal MF(2013)PGC-1α,mitochondrial dysfunction,and Huntington’s disease.Free Radic Biol Med 62:37-46.
Julien JP(2007)ALS:astrocytes move in as deadly neighbors.Nat Neurosci 10:535-537.
Kahle PJ,Waak J,Gasser T(2009)DJ-1 and prevention of oxidative stress in Parkinson’s disease and other age-related disorders.Free Radic Biol Med 47:1354-1361.
Kamat PK,Kalani A,Kyles P,Tyagi SC,Tyagi N(2014)Autophagy of mitochondria:a promising therapeutic target for neurodegenerative disease.Cell Biochem Biophys 70:707-719.
Kay L,Pienaar IS,Cooray R,Black G,Soundararajan M(2018)Understanding miro GTPases:implications in the treatment of neurodegenerative disorders.Mol Neurobiol 55:7352-7365.
Khalil B,El Fissi N,Aouane A,Cabirol-Pol MJ,Rival T,Liévens JC(2015)PINK1-induced mitophagy promotes neuroprotection in Huntington’s disease.Cell Death Dis 6:e1617.
Kitagishi Y,Nakano N,Ogino M,Ichimura M,Minami A,Matsuda S(2017)PINK1 signaling in mitochondrial homeostasis and in aging.Int J Mol Med 39:3-8.
Koentjoro B,Park JS,Sue CM(2017)Nix restores mitophagy and mitochondrial function to protect against PINK1/Parkin-related Parkinson’s disease.Sci Rep 7:44373.
Koike M,Shibata M,Tadakoshi M,Gotoh K,Komatsu M,Waguri S,Kawahara N,Kuida K,Nagata S,Kominami E(2008)Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury.Am J Pathol 172:454-469.
Komatsu M,Waguri S,Koike M,Sou Y,Ueno T,Hara T,Mizushima N,Iwata J,Ezaki J,Murata S(2007)Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.Cell 131:1149-1163.
Kubli DA,Gustafsson?B(2012)Mitochondria and mitophagy:The yin and yang of cell death control.Circ Res 111:1208-1221.
Lazarou M,Jin SM,Kane LA,Youle RJ(2012)Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin.Dev Cell 22:320-333.
Lee JA(2009)Autophagy in neurodegeneration:Two sides of the same coin.BMB Rep 42:324-330.
Lee JH,Yu WH,Kumar A,Lee S,Mohan PS,Peterhoff CM,Wolfe DM,Martinez-Vicente M,Massey AC,Sovak G(2010)Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations.Cell 141:1146-1158.
Lee JJ,Sanchez-Martinez A,Zarate AM,BenincáC,Mayor U,Clague MJ,Whitworth AJ(2018)Basal mitophagy is widespread in Drosophila but minimally affected by loss of Pink1 or parkin.J Cell Biol217:1613-1622.
Lemasters JJ(2005)Selective mitochondrial autophagy,or mitophagy,as a targeted defense against oxidative stress,mitochondrial dysfunction,and aging.Rejuvenation Res 8:3-5.
Li L,Hu G(2015)Pink1 protects cortical neurons from thapsigargin-induced oxidative stress and neuronal apoptosis.Biosci Rep 35.pii:e00174.
Li Q,Zhang T,Wang J,Zhang Z,Zhai Y,Yang GY,Sun X(2014)Rapamycin attenuates mitochondrial dysfunction via activation of mitophagy in experimental ischemic stroke.Biochem Biophys Res Commun444:182-188.
Lv M,Wang C,Li F,Peng J,Wen B,Gong Q,Shi Y,Tang Y(2017)Structural insights into the recognition of phosphorylated FUNDC1 by LC3B in mitophagy.Protein Cell 8:25-38.
MagranéJ,Cortez C,Gan W-B,Manfredi G(2013)Abnormal mitochondrial transport and morphology are common pathological denominators in SOD1 and TDP43 ALS mouse models.Hum Mol Genet23:1413-1424.
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