Ferroptosis, a newly characterized form of cell death in Parkinson's disease that is regulated by PKC

Neurobiology of Disease

Volumn 94, Issue , 2016, Pages 169-178

  Do Van, Bruce ^a   Gouel, Flore ^a   Jonneaux, Aurélie ^a   Timmerman, Kelly ^a   Gelé, Patrick ^b   Pétrault, Maud ^a   Bastide, Michèle ^a   Laloux, Charlotte ^a   Moreau, Caroline ^c   Bordet, Régis ^a   Devos, David ^a,b,c   Devedjian, Jean Christophe ^a,b,c,d  

^a CHU Lille   (France)

^b LILLE UNIVERSITY HOSPITAL   (France)

^c UNIV LILLE   (France)

^d UNIVERSITÉ DU LITTORAL CÔTE D OPALE   (France)

Author keywords

1 Methyl 4 phenyl 1,2,3,6 tetrahydropyridine mouse model; Ferroptosis; Lund human mesencephalic cells; Parkinson's disease

Indexed keywords

FERROSTATIN 1; IRON CHELATING AGENT; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2; VOLTAGE DEPENDENT ANION CHANNEL 3; DOPAMINE; IRON;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CASE REPORT; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; EX VIVO STUDY; FEMALE; FERROPTOSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MIDDLE AGED; MOUSE; MPTP-INDUCED PARKINSONISM; NERVE CELL NECROSIS; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OCCIPITAL CORTEX; PARKINSON DISEASE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SUBSTANTIA NIGRA; ANIMAL; APOPTOSIS; CELL DEATH; MESENCEPHALON; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; CELL DEATH; DOPAMINE; DOPAMINERGIC NEURONS; HUMANS; IRON; MESENCEPHALON; PARKINSON DISEASE; PROTEIN KINASE C; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

EID: 84978481313     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.05.011     Document Type: Article

References (36)

1. Arthur, J.R., The glutathione peroxidases. Cell. Mol. Life Sci. CMLS 57 (2000), 1825–1835.
2. Ayton, S., Lei, P., Hare, D.J., Duce, J.A., George, J.L., Adlard, P.A., McLean, C., Rogers, J.T., Cherny, R.A., Finkelstein, D.I., Bush, A.I., Parkinson's disease iron deposition caused by nitric oxide-induced loss of β-amyloid precursor protein. J. Neurosci. 35 (2015), 3591–3597, 10.1523/JNEUROSCI.3439-14.2015.
3. Bellinger, F.P., Bellinger, M.T., Seale, L.A., Takemoto, A.S., Raman, A.V., Miki, T., Manning-Boğ, A.B., Berry, M.J., White, L.R., Ross, G.W., Glutathione peroxidase 4 is associated with neuromelanin in substantia nigra and dystrophic axons in putamen of Parkinson's brain. Mol. Neurodegener., 6, 2011, 8, 10.1186/1750-1326-6-8.
4. Blackinton, J., Kumaran, R., van der Brug, M.P., Ahmad, R., Olson, L., Galter, D., Lees, A., Bandopadhyay, R., Cookson, M.R., Post-transcriptional regulation of mRNA associated with DJ-1 in sporadic Parkinson disease. Neurosci. Lett. 452 (2009), 8–11, 10.1016/j.neulet.2008.12.053.
5. Cavaliere, F., Vicente, E.S., Matute, C., An organotypic culture model to study nigro-striatal degeneration. J. Neurosci. Methods 188 (2010), 205–212, 10.1016/j.jneumeth.2010.02.008.
6. Chen, J., Rusnak, M., Lombroso, P.J., Sidhu, A., Dopamine promotes striatal neuronal apoptotic death via ERK signaling cascades. Eur. J. Neurosci. 29 (2009), 287–306, 10.1111/j.1460-9568.2008.06590.x.
7. Devos, D., Moreau, C., Devedjian, J.C., Kluza, J., Petrault, M., Laloux, C., Jonneaux, A., Ryckewaert, G., Garçon, G., Rouaix, N., Duhamel, A., Jissendi, P., Dujardin, K., Auger, F., Ravasi, L., Hopes, L., Grolez, G., Firdaus, W., Sablonnière, B., Strubi-Vuillaume, I., Zahr, N., Destée, A., Corvol, J.-C., Pöltl, D., Leist, M., Rose, C., Defebvre, L., Marchetti, P., Cabantchik, Z.I., Bordet, R., Targeting chelatable iron as a therapeutic modality in Parkinson's disease. Antioxid. Redox Signal. 21 (2014), 195–210, 10.1089/ars.2013.5593.
8. Dixon, S.J., Lemberg, K.M., Lamprecht, M.R., Skouta, R., Zaitsev, E.M., Gleason, C.E., Patel, D.N., Bauer, A.J., Cantley, A.M., Yang, W.S., Morrison, B., Stockwell, B.R., Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149 (2012), 1060–1072, 10.1016/j.cell.2012.03.042.
9. Dolma, S., Lessnick, S.L., Hahn, W.C., Stockwell, B.R., Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 3 (2003), 285–296.
10. Fenton, H.J.H., LXXIII.—oxidation of tartaric acid in presence of iron. J. Chem. Soc. Trans. 65 (1894), 899–910, 10.1039/CT8946500899.
11. Friedmann Angeli, J.P., Schneider, M., Proneth, B., Tyurina, Y.Y., Tyurin, V.A., Hammond, V.J., Herbach, N., Aichler, M., Walch, A., Eggenhofer, E., Basavarajappa, D., Rådmark, O., Kobayashi, S., Seibt, T., Beck, H., Neff, F., Esposito, I., Wanke, R., Förster, H., Yefremova, O., Heinrichmeyer, M., Bornkamm, G.W., Geissler, E.K., Thomas, S.B., Stockwell, B.R., O'Donnell, V.B., Kagan, V.E., Schick, J.A., Conrad, M., Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat. Cell Biol. 16 (2014), 1180–1191, 10.1038/ncb3064.
12. Hare, D.J., Arora, M., Jenkins, N.L., Finkelstein, D.I., Doble, P.A., Bush, A.I., Is early-life iron exposure critical in neurodegeneration?. Nat. Rev. Neurol. 11 (2015), 536–544, 10.1038/nrneurol.2015.100.
13. Hemendinger, R.A., Armstrong, E.J., Persinski, R., Todd, J., Mougeot, J.-L., Volvovitz, F., Rosenfeld, J., Huperzine A provides neuroprotection against several cell death inducers using in vitro model systems of motor neuron cell death. Neurotox. Res. 13 (2008), 49–61.
14. Kanai, Y., Endou, H., Functional properties of multispecific amino acid transporters and their implications to transporter-mediated toxicity. J. Toxicol. Sci. 28 (2003), 1–17.
15. Kang, Y., Tiziani, S., Park, G., Kaul, M., Paternostro, G., Cellular protection using Flt3 and PI3Kα inhibitors demonstrates multiple mechanisms of oxidative glutamate toxicity. Nat. Commun., 5, 2014, 3672, 10.1038/ncomms4672.
16. Linert, W., Jameson, G.N.L., Redox reactions of neurotransmitters possibly involved in the progression of Parkinson's disease. J. Inorg. Biochem. 79 (2000), 319–326, 10.1016/S0162-0134(99)00238-X.
17. Lo, M., Ling, V., Wang, Y.Z., Gout, P.W., The xc-cystine/glutamate antiporter: a mediator of pancreatic cancer growth with a role in drug resistance. Br. J. Cancer 99 (2008), 464–472, 10.1038/sj.bjc.6604485.
18. Martel, C., Wang, Z., Brenner, C., VDAC phosphorylation, a lipid sensor influencing the cell fate. Mitochondrion 19:Pt A (2014), 69–77, 10.1016/j.mito.2014.07.009.
19. Napolitano, A., Manini, P., d'Ischia, M., Oxidation chemistry of catecholamines and neuronal degeneration: an update. Curr. Med. Chem. 18 (2011), 1832–1845.
20. Robert, G., Puissant, A., Dufies, M., Marchetti, S., Jacquel, A., Cluzeau, T., Colosetti, P., Belhacene, N., Kahle, P., Da Costa, C.A., Luciano, F., Checler, F., Auberger, P., The caspase 6 derived N-terminal fragment of DJ-1 promotes apoptosis via increased ROS production. Cell Death Differ. 19 (2012), 1769–1778, 10.1038/cdd.2012.55.
21. Schildknecht, S., Karreman, C., Pöltl, D., Efrémova, L., Kullmann, C., Gutbier, S., Krug, A., Scholz, D., Gerding, H.R., Leist, M., Generation of genetically-modified human differentiated cells for toxicological tests and the study of neurodegenerative diseases. ALTEX 30 (2013), 427–444.
22. Schmidt, M., Goebeler, M., Posern, G., Feller, S.M., Seitz, C.S., Bröcker, E.-B., Rapp, U.R., Ludwig, S., Ras-independent activation of the Raf/MEK/ERK pathway upon calcium-induced differentiation of keratinocytes. J. Biol. Chem. 275 (2000), 41011–41017, 10.1074/jbc.M003716200.
23. Skouta, R., Dixon, S.J., Wang, J., Dunn, D.E., Orman, M., Shimada, K., Rosenberg, P.A., Lo, D.C., Weinberg, J.M., Linkermann, A., Stockwell, B.R., Ferrostatins inhibit oxidative lipid damage and cell death in diverse disease models. J. Am. Chem. Soc. 136 (2014), 4551–4556, 10.1021/ja411006a.
24. Sun, Y., Vashisht, A.A., Tchieu, J., Wohlschlegel, J.A., Dreier, L., Voltage-dependent anion channels (VDACs) recruit Parkin to defective mitochondria to promote mitochondrial autophagy. J. Biol. Chem. 287 (2012), 40652–40660, 10.1074/jbc.M112.419721.
25. Triplett, J.C., Zhang, Z., Sultana, R., Cai, J., Klein, J.B., Büeler, H., Butterfield, D.A., Quantitative expression proteomics and phosphoproteomics profile of brain from PINK1 knockout mice: insights into mechanisms of familial Parkinson's disease. J. Neurochem. 133 (2015), 750–765, 10.1111/jnc.13039.
26. Uversky, V.N., Li, J., Fink, A.L., Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276 (2001), 44284–44296, 10.1074/jbc.M105343200.
27. Vaughn, A.E., Deshmukh, M., Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10 (2008), 1477–1483, 10.1038/ncb1807.
28. Weinreb, O., Mandel, S., Youdim, M.B.H., Amit, T., Targeting dysregulation of brain iron homeostasis in Parkinson's disease by iron chelators. Free Radic. Biol. Med. 62 (2013), 52–64, 10.1016/j.freeradbiomed.2013.01.017.
29. Wen-Sheng, W., Protein kinase C alpha trigger Ras and Raf-independent MEK/ERK activation for TPA-induced growth inhibition of human hepatoma cell HepG2. Cancer Lett. 239 (2006), 27–35, 10.1016/j.canlet.2005.07.034.
30. Wersinger, C., Chen, J., Sidhu, A., Bimodal induction of dopamine-mediated striatal neurotoxicity is mediated through both activation of D1 dopamine receptors and autoxidation. Mol. Cell. Neurosci. 25 (2004), 124–137, 10.1016/j.mcn.2003.10.002.
31. Yagoda, N., von Rechenberg, M., Zaganjor, E., Bauer, A.J., Yang, W.S., Fridman, D.J., Wolpaw, A.J., Smukste, I., Peltier, J.M., Boniface, J.J., Smith, R., Lessnick, S.L., Sahasrabudhe, S., Stockwell, B.R., RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447 (2007), 864–868, 10.1038/nature05859.
32. Yang, W.S., SriRamaratnam, R., Welsch, M.E., Shimada, K., Skouta, R., Viswanathan, V.S., Cheah, J.H., Clemons, P.A., Shamji, A.F., Clish, C.B., Brown, L.M., Girotti, A.W., Cornish, V.W., Schreiber, S.L., Stockwell, B.R., Regulation of ferroptotic cancer cell death by GPX4. Cell 156 (2014), 317–331, 10.1016/j.cell.2013.12.010.
33. Yoo, S.-E., Chen, L., Na, R., Liu, Y., Rios, C., Van Remmen, H., Richardson, A., Ran, Q., Gpx4 ablation in adult mice results in a lethal phenotype accompanied by neuronal loss in brain. Free Radic. Biol. Med. 52 (2012), 1820–1827, 10.1016/j.freeradbiomed.2012.02.043.
34. Youdim, M.B.H., Riederer, P.F., A review of the mechanisms and role of monoamine oxidase inhibitors in Parkinson's disease. Neurology 63 (2004), S32–S35.
35. Zeevalk, G.D., Razmpour, R., Bernard, L.P., Glutathione and Parkinson's disease: is this the elephant in the room?. Biomed. Pharmacother. 62 (2008), 236–249, 10.1016/j.biopha.2008.01.017.
36. Zhang, H.-M., Su, Q., PKC in developmental hypothyroid rat brain. Neurol. Sci. Off. J. Ital. Neurol. Soc. Ital. Soc. Clin. Neurophysiol. 35 (2014), 1161–1166, 10.1007/s10072-014-1716-6.