Preclinical Evidence for the Interplay between Oxidative Stress and RIP1-Dependent Cell Death in Neurodegeneration: State of the Art and Possible Therapeutic Implications
Abstract
:1. Introduction
2. Mechanisms of Necroptosis
3. Necroptosis Inhibitors
3.1. RIP1-Targeted Inhibitors
3.2. RIP3-Targeted Inhibitors
3.3. MLKL-Targeted Inhibitors
4. In Vitro Evidence for the Interplay between Oxidative Stress and Necroptosis
4.1. Neuroprotective Effects of Necroptosis Inhibitors in Cellular Oxidative Stress Models
4.2. Neuroprotective Effects of Necroptosis Inhibitors in In Vitro Excitotoxicity Models
4.3. Neuroprotective Effects of Necroptosis Inhibitors in In Vitro Ischemia/Hypoxia Models
4.4. Neuroprotective Effects of Necroptosis Inhibitors in In Vitro Intracerebral Hemorrhage Models
4.5. Neuroprotective Effects of Necroptosis Inhibitors in In Vitro Models of Parkinson’s Disease
4.6. Neuroprotective Effects of Necroptosis Inhibitors in Other Cellular Models
Model | Inducer | Cell Type | Necroptosis Inhibitor | Ref. |
---|---|---|---|---|
Oxidative stress | 0.1–20 mM BSO 50–400 uM H2O2 + 200 uM BSO 2 mM H2O2 0.25 mM H2O2 0.5 mM H2O2 5 mM Glu 5 mM Glu 4 mM Glu 3 mM Glu 160 mM Glu 5 mM Glu/BSO 5 mM Glu/BSO 100 uM arachidonic acid cysteine deprivation 5 mM BSO 100 and 400 uM H2O2 | mouse HT-22 cells human SK-N-SH cells mouse HT-22 cells human UN-SH-SY5Y cells human RA-SH-SY5Y cells mouse HT-22 cells mouse HT-22 cells mouse HT-22 cells mouse HT-22 cells human RA-SH-SY5Y cells mouse RGC-5 cells mouse RGC-5 cells 7–9 DIV rat OPCs 7–9 DIV rat OPCs 7–9 DIV rat OPCs 7–9 DIV rat OPCs | Nec-1 10 uM-complete Nec-1 40 uM-complete Nec-1 10–40 uM-partial 10–40 uM-partial 20–40 uM-partial Nec-1 25–100 uM-complete Nec-1 10 uM-complete Nec- 1 50 uM-complete Nec-1 10–40 uM-partial Nec-1 50 uM-complete Nec-1 50–100 uM-partial Nec-1 25–50 uM-partial Nec-1 20 uM-complete Nec-1 20 uM-complete Nec-1 20 uM-complete Nec-1 no protection (20 uM) | [73] [74] [46] [46] [46] [73] [77] [76] [46] [78] [79] [80] [81] [81] [81] [81] |
Excitotoxicity | 100 uM NMDA 20 uM Glu | 10–12 DIV rat cx neurons 7–15 DIV rat hip. neurons | Nec-1 30–100 uM-partial Nec-1 100 uM | [83] [84] |
Ischemia/Hypoxia | 1 h OGD/24 h R 2 h OGD/24 h R 2 h OGD/3 h R 2 h OGD/0–8 h R 3–12 h OGD 3 h OGD/R 48 h 48 h hypoxia 8 h OGD/0–24 h R 4 h OGD/24 h R 8 h OGD/6–12 h R 3–12 h OGD 6–12 h OGD/ 24h R 3 h OGD + zVAD/24 h R CM from OGD + zVAD neu 12 OGD/4–48 h R 2 h OGD/24 h R 12 h OGD 6 h OGD/R 24 h 9 h OGD 4 h OGD/24 h R 4 h OGD/24 h R 6–24 h OGD/R 2 h OGD/2 h re-oxyg | 10 DIV mouse cx neurons 15 DIV rat hip. neurons 4 DIV rat cx neurons 8 DIV rat cx neurons 5–8 DIV rat cx neurons 7 DIV rat cx neurons 7 DIV rat cx neurons rat PC12 cells 2 DIV mouse RGCs mouse RGC-5 cells rat cx astrocytes mice cx astrocytes 10 DIV primary neurons mouse primary microglia cells mouse N9 cells 12 DIV mouse OPCs rat cx neurons/astrocytes; HT-22 cells rat cx neurons/astrocytes; HT-22 cells mouse RGC-5 cells mouse BV2 cells mouse co-culture HT-22+BV2 cells mouse BV2 cells mouse spinal cord neurons | Nec-1 25 uM-partial Nec-1 20 uM-partial Nec-1 2 uL of 1%-partial Nec-1 20 uM-partial Nec-1 1–100 uM-partial Nec-1 25 uM-partial Nec-1 6.25–50 uM-partial Nec-1 20 uM-partial Nec-1 20 uM-partial Nec-1 10 uM-partial Nec-1 1–100 uM-partial Nec-1 10 uM-partial Nec-1 no protection (20 uM) Nec-1 20 uM-complete Nec-1 20 uM-partial Nec-1 20 uM-partial DTIO 10 uM DTIO 10 uM RIC 3–20 uM Nec-1 20 uM-partial, rhTrx-1 Nec-1 20 uM-partial, rhTrx-1 Nec-1 30 uM-partial, PGRN Nec-1 20–50 uM-partial | [85] [86] [87] [88] [89] [90] [90] [88] [91] [92] [89] [93] [94] [94] [95] [96] [97] [97] [98] [99] [99] [100] [101] |
Intracerebral hemorrhage | 100 uM ferrus chloride 100 uM hemin 1.5 uM hemoglobin 50 uM hemin | 8 DIV mouse cx neurons 3 DIV mouse cx neurons 3 DIV mouse cx neurons mouse HT-22 cells | Nec-1 30 uM-partial Nec-1 50–100 uM-partial Nec-1 50–100 uM-partial Nec-1 30 uM-partial | [102] [103] [103] [104] |
PD-like models | 100 uM 6-OHDA 40 uM 6-OHDA 40 uM 6-OHDA 100 uM 6-OHDA 200 uM 6-OHDA 1 mM MPP+ 5 mM MPP+ 15–25 uM MPP+ CM from LPS-glia cells z-VAD-fmk/LPS/BV6 100 nM rotenonec 10 uM rotenone | rat PC12 cells 7 DIV rat mes. neurons 7 DIV rat cx neurons human UN-SH-SY5Y cells human RA-SH-SY5Y cells human UN-SH-SY5Y cells human RA-SH-SY5Y cells 7 DIV mouse cx neurons rat PC12 cells mouse BV2 and N9 microglia cells human SH-SY5Y cells mouse RGC-5 cells | Nec-1 5–30 uM-partial Nec-1s 30 uM Nec-1s 30 uM Nec-1 20–40 uM-partial Nec-1 40 uM-partial Nec-1 no protection (10 uM) Nec-1 and Nec-1i 20 uM-partial RIP3−/− cells Nec-1 no protection (20 uM) Nec-1 30 uM-complete Nec-1 no protection (20–30 uM) Nec-1 no protection (50–200 uM) | [108] [105] [105] [46] [46] [109] [110] [71] [48] [111] [112] [113] |
AD-like models | A-beta aggregation 10 uM A-beta1–42 10 uM A-beta1–42 2–8 mM Aluminum 2 mM Aluminum | Human MC65 cells (TC-control) Mouse HT-22 cells Mouse BV2 cells Human SH-SY5Y cells 5 DIV mouse cx neurons | Nec-1 30–100 uM-complete Nec-1 50–100 uM-complete Nec-1 50–100 uM-complete Nec-1 60–90 uM-complete Nec-1 60–90 uM-complete | [115] [116] [116] [117] [118] |
Other models | TNFa + zVAD TNFa + CHX + zVAD CM from TNFa + LPS + zVAD- astrocytes blue light (250 lx) light (1000 lx) sodium azide 200 uM myricetin or quercetin mechanical injury | mouse HT-22 cells mouse spinal cord astrocytes 7 DIV mouse spinal cord neurons mouse RGC-5 cells mouse RGC-5 cells mouse RGC-5 cells human retina epithelial cells 14–16 DIV mouse cx neurons | Nec-1 30 uM-complete Nec-1 20 uM-complete Nec-1 20 uM-complete Nec-1 50 uM-partial Nec-1 25–50 uM-partial Nec-1 no protection (25–50 uM) Nec-1 30 uM-complete Nec-1 100 uM-partial | [120] [121] [121] [122] [123] [123] [124] [125] |
5. In Vivo Studies Linking Oxidative Stress and Necroptosis in Relation to Neurodegenerative Diseases
Disease | Animal Model | Neuroprotective Compound | Ref. |
---|---|---|---|
Stroke | MCAO/R in C57 Bl mice MCAO/R in ICR mice MCAO/R in SD rats MCAO/R in SD rats | rhTrx1 10 mg/kg i.v. DTIO 1–10 mg/kg i.v. DTIO 10 mg/kg i.v. + i.p. for 7 or 28 d. Nec-1 1.5 uL/20 mM i.c.v. | [99] [97] [97] [128] |
Neonatal hypoxia/ischemia | Hypoxia in C57Bl mice Hypoxia in C57Bl mice Hypoxia in C57Bl mice | Nec-1 0.1 uL/80 uM i.c.v. Nec-1 0.1 uL/80 uM i.c.v. Nec-1 0.1 uL/80 uM i.c.v. | [129] [130] [131] |
Hemorrhagic stroke | SAH in SD rats SAH in SD rats | Nec-1 200 ug i.c.v. Nec-1 10.5 mg/kg i.p.; Mdivi-1 3.6 mg/kg i.p. | [132] [133] |
TBI/SCI | CCI in SD rats laminectomy/T10 in SD rats laminectomy/T10 in SD rats laminectomy/Th6–7 in C57Bl mice | Nec-1 6 uL/25 mM i.c.v.; melatonin 20 mg/kg i.p. Nec-1 1–50 ug i.t. Nec-1 25 ug i.t. Nec-1 5 mg/kg i.p.; GSK’872 2 mg/kg i.p. | [134] [135] [136] [101] |
Retina injury | Tg P23H rhodopsin rat and mice mutants retinal detachment in Norway rats and in C57BL WT and RIP3−/− mice | Nec-1 15 mg/kg/day s.c. NAC 150 mg/kg/day s.c. from PD21 to PD120 400 uM Nec-1 + 300 uM z-VAD-fmk i.r. in WT RIP3−/− | [137] [138] |
AD/aging | LPS i.c.v. in Wistar rats Hight fat diet in rats D-galactose+hepatoctomy in C57Bl mice | Nec-1 10 uM i.c.v. Nec-1 1.65 mg/kg/day s.c. from 13 to 21 week Nec-1 6.25 mg/kg i.p. | [139] [140] [141] |
PD | MPTP in C57Bl mice MPTP in C57Bl WT, RIP3−/− and MLKL−/− mice | Nec-1 1 ug/day i.c.v.; Nec-1s 10 mg/kg/day i.p.from 3–21 days Nec-1 1.65 mg/kg/day i.p. up to 21 days; RIP3−/− and MLKL−/− | [142] [143] |
Other | sciatic nerve chronic constriction (CCI) in SD rats EAE in C57Bl | Nec-1 0.2–0.4 mg/kg/day i.p. for 21 days Nec-1 1.65 mg/kg i.t. from day 2 every 3 days for 15 days | [144] [145] |
6. Multipotential Neuroprotectants for Future Treatment of Acute and Chronic Neurodegenerative Diseases
7. Conclusions
Funding
Conflicts of Interest
Abbreviations
References
- Sies, H. Oxidative stress: Introductory remarks. In Oxidative Stress; Sies, H., Ed.; Academic Press: London, UK, 1985; pp. 1–8. [Google Scholar]
- Sies, H.; Jones, D. Oxidative stress. In Encyclopedia of Stress, 2nd ed.; Fink, G., Ed.; Elsevier: Amsterdam, The Netherlands, 2007; Volume 3, pp. 45–48. [Google Scholar]
- Sies, H.; Jones, D.P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 2020, 21, 363–383. [Google Scholar] [CrossRef]
- Zorov, D.B.; Juhaszova, M.; Sollott, S.J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 2014, 94, 909–950. [Google Scholar] [CrossRef] [Green Version]
- Angelova, P.R.; Abramov, A.Y. Role of mitochondrial ROS in the brain: From physiology to neurodegeneration. FEBS Lett. 2018, 592, 692–702. [Google Scholar] [CrossRef] [PubMed]
- Popa-Wagner, A.; Mitran, S.; Sivanesan, S.; Chang, E.; Buga, A.M. ROS and brain diseases: The good, the bad, and the ugly. Oxid. Med. Cell Longev. 2013, 2013, 963520. [Google Scholar] [CrossRef] [PubMed]
- Adibhatla, R.M.; Hatcher, J.F. Altered lipid metabolism in brain injury and disorders. Subcell Biochem. 2008, 49, 241–268. [Google Scholar]
- Niedzielska, E.; Smaga, I.; Gawlik, M.; Moniczewski, A.; Stankowicz, P.; Pera, J.; Filip, M. Oxidative Stress in Neurodegenerative Diseases. Mol. Neurobiol. 2016, 53, 4094–4125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pisoschi, A.M.; Pop, A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Med. Chem. 2015, 97, 55–74. [Google Scholar] [CrossRef]
- Trushina, E.; McMurray, C.T. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 2007, 145, 1233–1248. [Google Scholar] [CrossRef]
- Singh, A.; Kukreti, R.; Saso, L.; Kukreti, S. Molecules. Oxidative Stress: A Key Modulator in Neurodegenerative Diseases. Molecules 2019, 24, 1583. [Google Scholar] [CrossRef] [Green Version]
- Lin, M.T.; Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443, 787–795. [Google Scholar] [CrossRef]
- Bokov, A.; Chaudhuri, A.; Richardson, A. The role of oxidative damage and stress in aging. Mech. Ageing Dev. 2004, 125, 811–826. [Google Scholar] [CrossRef]
- Damiano, M.; Galvan, L.; Déglon, N.; Brouillet, E. Mitochondria in Huntington’s disease. Biochim. Biophys. Acta 2010, 1802, 52–61. [Google Scholar] [CrossRef] [Green Version]
- Trist, B.G.; Hare, D.J.; Double, K.L. Oxidative stress in the aging substantia nigra and the etiology of Parkinson’s disease. Aging Cell. 2019, 18, e13031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dionísio, P.A.; Amaral, J.D.; Rodrigues, C.M.P. Oxidative stress and regulated cell death in Parkinson’s disease. Ageing Res. Rev. 2021, 67, 101263. [Google Scholar] [CrossRef]
- Tan, W.; Pasinelli, P.; Trotti, D. Role of mitochondria in mutant SOD1 linked amyotrophic lateral sclerosis. Biochim. Biophys. Acta 2014, 1842, 1295–1301. [Google Scholar] [CrossRef] [Green Version]
- Kelleher, R.J.; Shenb, J. Presenilin-1 mutations and Alzheimer’s disease. Proc. Natl. Acad. Sci. USA 2017, 114, 629–631. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parker, W.D., Jr.; Parks, J.; Filley, C.M.; Kleinschmidt-DeMasters, B.K. Electron transport chain defects in Alzheimer’s disease brain. Neurology 1994, 44, 1090–1096. [Google Scholar] [CrossRef] [PubMed]
- Hribljan, V.; Lisjak, D.; Petrović, D.J.; Mitrečić, D. Necroptosis is one of the modalities of cell death accompanying ischemic brain stroke: From pathogenesis to therapeutic possibilities. Croat. Med. J. 2019, 60, 121–126. [Google Scholar] [CrossRef] [PubMed]
- Mehta, S.L.; Manhas, N.; Raghubir, R. Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res. Rev. 2007, 54, 34–66. [Google Scholar] [CrossRef]
- Fang, Y.; Gao, S.; Wang, X.; Cao, Y.; Lu, J.; Chen, S.; Lenahan, C.; Zhang, J.H.; Shao, A.; Zhang, J. Programmed Cell Deaths and Potential Crosstalk with Blood-Brain Barrier Dysfunction After Hemorrhagic Stroke. Front. Cell Neurosci. 2020, 14, 68. [Google Scholar] [CrossRef]
- Ismail, H.; Shakkour, Z.; Tabet, M.; Abdelhady, S.; Kobaisi, A.; Abedi, R.; Nasrallah, L.; Pintus, G.; Al-Dhaheri, Y.; Mondello, S.; et al. Traumatic Brain Injury: Oxidative Stress and Novel Anti-Oxidants Such as Mitoquinone and Edaravone. Antioxidants 2020, 9, 943. [Google Scholar] [CrossRef] [PubMed]
- Anjum, A.; Yazid, M.D.; Fauzi Daud, M.; Idris, J.; Ng, A.M.H.; Selvi Naicker, A.; Ismail, O.H.R.; Athi Kumar, R.K.; Lokanathan, Y. Spinal Cord Injury: Pathophysiology, Multimolecular Interactions, and Underlying Recovery Mechanisms. Int. J. Mol. Sci. 2020, 21, 7533. [Google Scholar] [CrossRef]
- Liguori, I.; Russo, G.; Curcio, F.; Bulli, G.; Aran, L.; Della-Morte, D.; Gargiulo, G.; Testa, G.; Cacciatore, F.; Bonaduce, D.; et al. Oxidative stress, aging, and diseases. Clin. Interv. Aging 2018, 13, 757–772. [Google Scholar] [CrossRef] [Green Version]
- Tang, D.; Kang, R.; Berghe, T.V.; Vandenabeele, P.; Kroemer, G. The molecular machinery of regulated cell death. Cell Res. 2019, 29, 347–364. [Google Scholar] [CrossRef] [Green Version]
- Ma, Q. Role of Nrf2 in Oxidative Stress and Toxicity. Annu. Rev. Pharmacol. Toxicol. 2013, 53, 401–426. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maureen Redza-Dutordoir, M.; Averill-Bates, D.A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta BBA Mol. Cell Res. 2016, 1863, 2977–2992. [Google Scholar] [CrossRef]
- Salvadores, N.; Court, F.A. The necroptosis pathway and its role in age-related neurodegenerative diseases: Will it open up new therapeutic avenues in the next decade? Expert Opin. Ther. Targets 2020, 24, 679–693. [Google Scholar] [CrossRef] [PubMed]
- Conrad, M.; Angeli, J.P.; Vandenabeele, P.; Stockwell, B.R. Regulated necrosis: Disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 2016, 15, 348–366. [Google Scholar] [CrossRef] [PubMed]
- Galluzzi, L.; Vanden Berghe, T.; Vanlangenakker, N.; Buettner, S.; Eisenberg, T.; Vandenabeele, P.; Madeo, F.; Kroemer, G. Programmed necrosis from molecules to health and disease. Int. Rev. Cell Mol. Biol. 2011, 289, 1–35. [Google Scholar]
- Vandenabeele, P.; Galluzzim, L.; Vanden Berghem, T.; Kroemer, G. Molecular mechanisms of necroptosis: An ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11, 700–714. [Google Scholar] [CrossRef]
- Galluzzi, L.; Vitale, I. Molecular mechanisms of cell death: Recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018, 25, 486–541. [Google Scholar] [CrossRef] [PubMed]
- Vanden Berghe, T.; Kaiser, W.J.; Bertrand, M.J.; Vandenabeele, P. Molecular crosstalk between apoptosis, necroptosis, and survival signaling. Mol. Cell Oncol. 2015, 2, e975093. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Degterev, A.; Huang, Z.; Boyce, M.; Li, Y.; Jagtap, P.; Mizushima, N.; Cuny, G.D.; Mitchison, T.J.; Moskowitz, M.A.; Yuan, J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 2005, 1, 112–119. [Google Scholar] [CrossRef] [PubMed]
- Degterev, A.; Hitomi, J.; Germscheid, M.; Ch’en, I.L.; Korkina, O.; Teng, X.; Abbott, D.; Cuny, G.D.; Yuan, C.; Wagner, G.; et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 2008, 4, 313–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, S.; Wang, L.; Miao, L.; Wang, T.; Du, F.; Zhao, L.; Wang, X. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009, 137, 1100–1111. [Google Scholar] [CrossRef] [Green Version]
- Cho, Y.S.; Challa, S.; Moquin, D.; Genga, R.; Ray, T.D.; Guildford, M.; Chan, F.K. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009, 137, 1112–1123. [Google Scholar] [CrossRef] [Green Version]
- Zhao, H.; Jaffer, T.; Eguchi, S.; Wang, Z.; Linkermann, A.; Ma, D. Role of necroptosis in the pathogenesis of solid organ injury. Cell Death Dis. 2015, 6, e1975. [Google Scholar] [CrossRef] [Green Version]
- Mifflin, L.; Ofengeim, D.; Yuan, J. Receptor-interacting protein kinase 1 (RIPK1) as a therapeutic target. Nat. Rev. Drug Discov. 2020, 19, 553–571. [Google Scholar] [CrossRef]
- Thornton, C.; Hagberg, H. Role of mitochondria in apoptotic and necroptotic cell death in the developing brain. Clin. Chim. Acta 2015, 451, 35–38. [Google Scholar] [CrossRef] [Green Version]
- Degterev, A.; Ofengeim, D.; Yuan, J. Targeting RIPK1 for the treatment of human diseases. Proc. Natl. Acad. Sci. USA 2019, 116, 9714–9722. [Google Scholar] [CrossRef] [Green Version]
- Arrázola, M.S.; Saquel, C.; Catalán, R.J.; Barrientos, S.A.; Hernandez, D.E.; Martínez, N.W.; Catenaccio, A.; Court, F.A. Axonal Degeneration Is Mediated by Necroptosis Activation. J. Neurosci. 2019, 39, 3832–3844. [Google Scholar] [CrossRef] [Green Version]
- Baritaud, M.; Cabon, L.; Delavallée, L.; Galán-Malo, P.; Gilles, M.E.; Brunelle-Navas, M.N.; Susin, S.A. AIF-mediated caspase-independent necroptosis requires ATM and DNA-PK-induced histone H2AX Ser139 phosphorylation. Cell Death Dis. 2012, 3, e390. [Google Scholar] [CrossRef] [PubMed]
- Hu, W.; Wu, X.; Yu, D.; Zhao, L.; Zhu, X.; Li, X.; Huang, T.; Chu, Z.; Xu, Y. Regulation of JNK signaling pathway and RIPK3/AIF in necroptosis-mediated global cerebral ischemia/reperfusion injury in rats. Exp. Neurol. 2020, 331, 113374. [Google Scholar] [CrossRef] [PubMed]
- Jantas, D.; Chwastek, J.; Grygier, B.; Lasoń, W. Neuroprotective Effects of Necrostatin-1 Against Oxidative Stress-Induced Cell Damage: An Involvement of Cathepsin D Inhibition. Neurotox. Res. 2020, 37, 525–542. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oshima, R.; Hasegawa, T.; Tamai, K.; Sugeno, N.; Yoshida, S.; Kobayashi, J.; Kikuchi, A.; Baba, T.; Futatsugi, A.; Sato, I.; et al. ESCRT-0 dysfunction compromises autophagic degradation of protein aggregates and facilitates ER stress-mediated neurodegeneration via apoptotic and necroptotic pathways. Sci. Rep. 2016, 6, 24997. [Google Scholar] [CrossRef] [Green Version]
- Shao, L.; Liu, X.; Zhu, S.; Liu, C.; Gao, Y.; Xu, X. The Role of Smurf1 in Neuronal Necroptosis after Lipopolysaccharide-Induced Neuroinflammation. Cell Mol. Neurobiol. 2018, 38, 809–816. [Google Scholar] [CrossRef]
- Wang, Z.; Jiang, H.; Chen, S.; Du, F.; Wang, X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 2012, 148, 228–243. [Google Scholar] [CrossRef] [Green Version]
- Moujalled, D.M.; Cook, W.D.; Okamoto, T.; Murphy, J.; Lawlor, K.E.; Vince, J.E.; Vaux, D.L. TNF can activate RIPK3 and cause programmed necrosis in the absence of RIPK1. Cell Death Dis. 2013, 4, e465. [Google Scholar] [CrossRef]
- Upton, J.W.; Kaiser, W.J.; Mocarski, E.S. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 2010, 7, 302–313. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.; Tang, M.B.; Luo, H.Y.; Shi, C.H.; Xu, Y.M. Necroptosis in neurodegenerative diseases: A potential therapeutic target. Cell Death Dis. 2017, 8, e2905. [Google Scholar] [CrossRef] [Green Version]
- Wegner, K.W.; Saleh, D.; Degterev, A. Complex Pathologic Roles of RIPK1 and RIPK3: Moving Beyond Necroptosis. Trends Pharmacol. Sci. 2017, 38, 202–225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cao, L.; Mu, W. Necrostatin-1 and necroptosis inhibition: Pathophysiology and therapeutic implications. Pharmacol. Res. 2020, 163, 105297. [Google Scholar] [CrossRef]
- Teng, X.; Degterev, A.; Jagtap, P.; Xing, X.; Choi, S.; Denu, R.; Yuan, J.; Cuny, G.D. Structure-activity relationship study of novel necroptosis inhibitors. Bioorg. Med. Chem. Lett. 2005, 15, 5039–5044. [Google Scholar] [CrossRef]
- Degterev, A.; Maki, J.L.; Yuan, J. Activity and specificity of necrostatin-1, small molecule inhibitor of RIP1 kinase. Cell Death Differ. 2013, 20, 366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jagtap, P.G.; Degterev, A.; Choi, S.; Keys, H.; Yuan, J.; Cuny, G.D. Structure-activity relationship study of tricyclic necroptosis inhibitors. J. Med. Chem. 2007, 50, 1886–1895. [Google Scholar] [CrossRef]
- Takahashi, N.; Duprez, L.; Grootjans, S.; Cauwels, A.; Nerinckx, W.; DuHadaway, J.B.; Goossens, V.; Roelandt, R.; Van Hauwermeiren, F.; Libert, C.; et al. Necrostatin-1 analogues: Critical issues on the specificity, activity and in vivo use in experimental disease models. Cell Death Dis. 2012, 3, e437. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vandenabeele, P.; Grootjans, S.; Callewaert, N.; Takahashi, N. Necrostatin-1 blocks both RIPK1 and IDO: Consequences for the study of cell death in experimental disease models. Cell Death Differ. 2013, 20, 185–187. [Google Scholar] [CrossRef] [Green Version]
- Najjar, M.; Suebsuwong, C.; Ray, S.S.; Thapa, R.J.; Maki, J.L.; Nogusa, S.; Shah, S.; Saleh, D.; Gough, P.J.; Bertin, J.; et al. Structure guided design of potent and selective ponatinib-based hybrid inhibitors for RIPK1. Cell Rep. 2015, 10, 1850–1860. [Google Scholar] [CrossRef] [Green Version]
- Biton, S.; Ashkenazi, A. NEMO and RIP1 control cell fate in response to extensive DNA damage via TNF-α feedforward signaling. Cell 2011, 145, 92–103. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Du, F.; Wang, X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008, 113, 693–703. [Google Scholar] [CrossRef] [Green Version]
- Xie, T.; Peng, W.; Liu, Y.; Yan, C.; Maki, J.; Degterev, A.; Yuan, J.; Shi, Y. Structural basis of RIP1 inhibition by necrostatins. Structure 2013, 21, 493–499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fauster, A.; Rebsamen, M.; Huber, K.V.; Bigenzahn, J.W.; Stukalov, A.; Lardeau, C.H.; Scorzoni, S.; Bruckner, M.; Gridling, M.; Parapatics, K.; et al. A cellular screen identifies ponatinib and pazopanib as inhibitors of necroptosis. Cell Death Dis. 2015, 6, e1767. [Google Scholar] [CrossRef] [PubMed]
- Harris, P.A.; Bandyopadhyay, D.; Berger, S.B.; Campobasso, N.; Capriotti, C.A.; Cox, J.A.; Dare, L.; Finger, J.N.; Hoffman, S.J.; Kahler, K.M.; et al. Discovery of small molecule RIP1 kinase inhibitors for the treatment of pathologies associated with necroptosis. ACS Med. Chem. Lett. 2013, 4, 1238–1243. [Google Scholar] [CrossRef] [Green Version]
- Berger, S.B.; Harris, P.; Nagilla, R.; Kasparcova, V.; Hoffman, S.; Swift, B.; Dare, L.; Schaeffer, M.; Capriotti, C.; Ouellette, M.; et al. Characterization of GSK0963: A structurally distinct, potent and selective inhibitor of RIP1 kinase. Cell Death Discov. 2015, 1, 15009. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harris, P.A. Inhibitors of RIP1 kinase: A patent review (2016-present). Expert Opin. Ther. Pat. 2021, 31, 137–151. [Google Scholar] [CrossRef]
- Degterev, A.; Linkermann, A. Generation of small molecules to interfere with regulated necrosis. Cell Mol. Life Sci. 2016, 73, 2251–2267. [Google Scholar] [CrossRef] [PubMed]
- Mandal, P.; Berger, S.B.; Pillay, S.; Moriwaki, K.; Huang, C.; Guo, H.; Lich, J.D.; Finger, J.; Kasparcova, V.; Votta, B.; et al. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell. 2014, 56, 481–495. [Google Scholar] [CrossRef] [Green Version]
- Li, J.X.; Feng, J.M.; Wang, Y.; Li, X.H.; Chen, X.X.; Su, Y.; Shen, Y.Y.; Chen, Y.; Xiong, B.; Yang, C.H.; et al. The B-Raf(V600E) inhibitor dabrafenib selectively inhibits RIP3 and alleviates acetaminophen-induced liver injury. Cell Death Dis. 2014, 5, e1278. [Google Scholar] [CrossRef] [Green Version]
- Dionísio, P.A.; Oliveira, S.R.; Gaspar, M.M.; Gama, M.J.; Castro-Caldas, M.; Amaral, J.D.; Rodrigues, C.M.P. Ablation of RIP3 protects from dopaminergic neurodegeneration in experimental Parkinson’s disease. Cell Death Dis. 2019, 10, 840. [Google Scholar] [CrossRef] [Green Version]
- Newton, K.; Dugger, D.L.; Wickliffe, K.E.; Kapoor, N.; de Almagro, M.C.; Vucic, D.; Komuves, L.; Ferrando, R.E.; French, D.M.; Webster, J.; et al. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 2014, 343, 1357–1360. [Google Scholar] [CrossRef]
- Xu, X.; Chua, C.C.; Kong, J.; Kostrzewa, R.M.; Kumaraguru, U.; Hamdy, R.C.; Chua, B.H. Necrostatin-1 protects against glutamate-induced glutathione depletion and caspase-independent cell death in HT-22 cells. J. Neurochem. 2007, 103, 2004–2014. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.O.; Byun, Y.J.; Cho, K.O.; Kim, S.Y.; Lee, S.B.; Kim, H.S.; Kwon, O.J.; Jeong, S.W. GS28 Protects Neuronal Cell Death Induced by Hydrogen Peroxide under Glutathione-Depleted Condition. Korean J. Physiol. Pharmacol. 2011, 15, 149–156. [Google Scholar] [CrossRef] [Green Version]
- Kritis, A.A.; Stamoula, E.G.; Paniskaki, K.A.; Vavilis, T.D. Researching glutamate-induced cytotoxicity in different cell lines: A comparative/collective analysis/study. Front. Cell Neurosci. 2015, 9, 91. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, H.J.; Kwak, M.; Baek, S.H. Neuroprotective effects of Dendropanax morbifera leaves on glutamate-induced oxidative cell death in HT22 mouse hippocampal neuronal cells. J. Ethnopharmacol. 2020, 251, 112518. [Google Scholar] [CrossRef]
- Zhang, M.; Li, J.; Geng, R.; Ge, W.; Zhou, Y.; Zhang, C.; Cheng, Y.; Geng, D. The inhibition of ERK activation mediates the protection of necrostatin-1 on glutamate toxicity in HT-22 cells. Neurotox. Res. 2013, 24, 64–70. [Google Scholar] [CrossRef]
- Gonzalez, G.; Grúz, J.; D’Acunto, C.W.; Kaňovský, P.; Strnad, M. Cytokinin Plant Hormones Have Neuroprotective Activity in In Vitro Models of Parkinson’s Disease. Molecules 2021, 26, 361. [Google Scholar] [CrossRef] [PubMed]
- Majid, A.S.; Yin, Z.Q.; Ji, D. Sulphur antioxidants inhibit oxidative stress induced retinal ganglion cell death by scavenging reactive oxygen species but influence nuclear factor (erythroid-derived 2)-like 2 signalling pathway differently. Biol. Pharm. Bull. 2013, 36, 1095–1110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Osborne, N.N.; Ji, D.; Majid, A.S.; Del Soldata, P.; Sparatore, A. Glutamate oxidative injury to RGC-5 cells in culture is necrostatin sensitive and blunted by a hydrogen sulfide (H2S)-releasing derivative of aspirin (ACS14). Neurochem. Int. 2012, 60, 365–378. [Google Scholar] [CrossRef]
- Kim, S.; Dayani, L.; Rosenberg, P.A.; Li, J. RIP1 kinase mediates arachidonic acid-induced oxidative death of oligodendrocyte precursors. Int. J. Physiol. Pathophysiol. Pharmacol. 2010, 2, 137–147. [Google Scholar]
- Mehta, A.; Prabhakar, M.; Kumar, P.; Deshmukh, R.; Sharma, P.L. Excitotoxicity: Bridge to various triggers in neurodegenerative disorders. Eur. J. Pharmacol. 2013, 698, 6–18. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Yang, X.; Ma, C.; Qiao, J.; Zhang, C. Necroptosis contributes to the NMDA-induced excitotoxicity in rat’s cultured cortical neurons. Neurosci. Lett. 2008, 447, 120–123. [Google Scholar] [CrossRef] [PubMed]
- Hernández, D.E.; Salvadores, N.A.; Moya-Alvarado, G.; Catalán, R.J.; Bronfman, F.C.; Court, F.A. Axonal degeneration induced by glutamate excitotoxicity is mediated by necroptosis. J. Cell Sci. 2018, 131, jcs214684. [Google Scholar] [CrossRef] [Green Version]
- Xu, X.; Chua, K.W.; Chua, C.C.; Liu, C.F.; Hamdy, R.C.; Chua, B.H. Synergistic protective effects of humanin and necrostatin-1 on hypoxia and ischemia/reperfusion injury. Brain Res. 2010, 1355, 189–194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vieira, M.; Fernandes, J.; Carreto, L.; Anuncibay-Soto, B.; Santos, M.; Han, J.; Fernández-López, A.; Duarte, C.B.; Carvalho, A.L.; Santos, A.E. Ischemic insults induce necroptotic cell death in hippocampal neurons through the up-regulation of endogenous RIP3. Neurobiol. Dis. 2014, 68, 26–36. [Google Scholar] [CrossRef]
- Yuan, L.; Wang, Z.; Liu, L.; Jian, X. Inhibiting histone deacetylase 6 partly protects cultured rat cortical neurons from oxygen-glucose deprivation-induced necroptosis. Mol. Med. Rep. 2015, 12, 2661–2667. [Google Scholar] [CrossRef] [Green Version]
- Wang, Z.; Guo, L.M.; Wang, Y.; Zhou, H.K.; Wang, S.C.; Chen, D.; Huang, J.F.; Xiong, K. Inhibition of HSP90α protects cultured neurons from oxygen-glucose deprivation induced necroptosis by decreasing RIP3 expression. J. Cell Physiol. 2018, 233, 4864–4884. [Google Scholar] [CrossRef] [PubMed]
- Ni, Y.; Gu, W.W.; Liu, Z.H.; Zhu, Y.M.; Rong, J.G.; Kent, T.A.; Li, M.; Qiao, S.G.; An, J.Z.; Zhang, H.L. RIP1K Contributes to Neuronal and Astrocytic Cell Death in Ischemic Stroke via Activating Autophagic-lysosomal Pathway. Neuroscience 2018, 371, 60–74. [Google Scholar] [CrossRef]
- Mu, J.; Weng, J.; Yang, C.; Guan, T.; Deng, L.; Li, M.; Zhang, G.; Kong, J. Necrostatin-1 prevents the proapoptotic protein Bcl-2/adenovirus E1B 19-kDa interacting protein 3 from integration into mitochondria. J. Neurochem. 2021, 156, 929–942. [Google Scholar] [CrossRef] [PubMed]
- Dvoriantchikova, G.; Degterev, A.; Ivanov, D. Retinal ganglion cell (RGC) programmed necrosis contributes to ischemia-reperfusion-induced retinal damage. Exp. Eye Res. 2014, 123, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Ding, W.; Shang, L.; Huang, J.F.; Li, N.; Chen, D.; Xue, L.X.; Xiong, K. Receptor interacting protein 3-induced RGC-5 cell necroptosis following oxygen glucose deprivation. BMC Neurosci. 2015, 16, 49. [Google Scholar] [CrossRef] [Green Version]
- Zhu, J.; Yang, L.K.; Wang, Q.H.; Lin, W.; Feng, Y.; Xu, Y.P.; Chen, W.L.; Xiong, K.; Wang, Y.H. NDRG2 attenuates ischemia-induced astrocyte necroptosis via the repression of RIPK1. Mol. Med. Rep. 2020, 22, 3103–3110. [Google Scholar] [CrossRef]
- Li, J.; Zhang, J.; Zhang, Y.; Wang, Z.; Song, Y.; Wei, S.; He, M.; You, S.; Jia, J.; Cheng, J. TRAF2 protects against cerebral ischemia-induced brain injury by suppressing necroptosis. Cell Death Dis. 2019, 10, 328. [Google Scholar] [CrossRef] [Green Version]
- Fan, H.; Tang, H.-B.; Kang, J.; Shan, L.; Song, H.; Zhu, K.; Wang, J.; Ju, G.; Wang, Y.-Z. Involvement of endoplasmic reticulum stress in the necroptosis of microglia/macrophages after spinal cord injury. Neuroscience 2015, 311, 362–373. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Zhang, L.; Yu, H.; Song, K.; Shi, J.; Chen, L.; Cheng, J. Necrostatin-1 Improves Long-term Functional Recovery Through Protecting Oligodendrocyte Precursor Cells After Transient Focal Cerebral Ischemia in Mice. Neuroscience 2018, 371, 229–241. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Liu, J.; Chen, J.R.; Zhu, Y.M.; Gao, X.; Ni, Y.; Lin, B.; Li, H.; Qiao, S.G.; Wang, C.; et al. Neuroprotective effects of DTIO, a novel analogue of Nec-1, in acute and chronic stages after ischemic stroke. Neuroscience 2018, 390, 12–29. [Google Scholar] [CrossRef]
- Do, Y.J.; Sul, J.W.; Jang, K.H.; Kang, N.S.; Kim, Y.H.; Kim, Y.G.; Kim, E. A novel RIPK1 inhibitor that prevents retinal degeneration in a rat glaucoma model. Exp. Cell Res. 2017, 359, 30–38. [Google Scholar] [CrossRef] [PubMed]
- Jiao, Y.; Wang, J.; Zhang, H.; Cao, Y.; Qu, Y.; Huang, S.; Kong, X.; Song, C.; Li, J.; Li, Q.; et al. Inhibition of microglial receptor-interacting protein kinase 1 ameliorates neuroinflammation following cerebral ischaemic stroke. J. Cell Mol. Med. 2020, 24, 12585–12598. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Cheng, S.; Hu, H.; Zhang, X.; Xu, J.; Wang, R.; Zhang, P. Progranulin protects against cerebral ischemia-reperfusion (I/R) injury by inhibiting necroptosis and oxidative stress. Biochem. Biophys. Res. Commun. 2020, 521, 569–576. [Google Scholar] [CrossRef]
- Wang, Y.; Jiao, J.; Zhang, S.; Zheng, C.; Wu, M. RIP3 inhibition protects locomotion function through ameliorating mitochondrial antioxidative capacity after spinal cord injury. Biomed. Pharmacother. 2019, 116, 109019. [Google Scholar] [CrossRef]
- Dai, M.C.; Zhong, Z.H.; Sun, Y.H.; Sun, Q.F.; Wang, Y.T.; Yang, G.Y.; Bian, L.G. Curcumin protects against iron induced neurotoxicity in primary cortical neurons by attenuating necroptosis. Neurosci. Lett. 2013, 536, 41–46. [Google Scholar] [CrossRef]
- Zille, M.; Karuppagounder, S.S.; Chen, Y.; Gough, P.J.; Bertin, J.; Finger, J.; Milner, T.A.; Jonas, E.A.; Ratan, R.R. Neuronal death after hemorrhagic stroke in vitro and in vivo shares features of ferroptosis and necroptosis. Stroke 2017, 48, 1033–1043. [Google Scholar] [CrossRef] [Green Version]
- Su, X.; Wang, H.; Lin, Y.; Chen, F. RIP1 and RIP3 mediate hemin-induced cell death in HT22 hippocampal neuronal cells. Neuropsychiatr. Dis. Treat. 2018, 14, 3111–3119. [Google Scholar] [CrossRef] [Green Version]
- Oñate, M.; Catenaccio, A.; Salvadores, N.; Saquel, C.; Martinez, A.; Moreno-Gonzalez, I.; Gamez, N.; Soto, P.; Soto, C.; Hetz, C.; et al. The necroptosis machinery mediates axonal degeneration in a model of Parkinson disease. Cell Death Differ. 2020, 27, 1169–1185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lázaro, D.F.; Pavlou, M.A.S.; Outeiro, T.F. Cellular models as tools for the study of the role of alpha-synuclein in Parkinson’s disease. Exp. Neurol. 2017, 298, 162–171. [Google Scholar] [CrossRef]
- Airavaara, M.; Parkkinen, I.; Konovalova, J.; Albert, K.; Chmielarz, P.; Domanskyi, A. Back and to the Future: From Neurotoxin-Induced to Human Parkinson’s Disease Models. Curr. Protoc. Neurosci. 2020, 91, e88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, J.R.; Wang, J.; Zhou, S.K.; Yang, L.; Yin, J.L.; Cao, J.P.; Cheng, Y.B. Necrostatin-1 protection of dopaminergic neurons. Neural. Regen. Res. 2015, 10, 1120–1124. [Google Scholar]
- Jantas, D.; Greda, A.; Golda, S.; Korostynski, M.; Grygier, B.; Roman, A.; Pilc, A.; Lason, W. Neuroprotective effects of metabotropic glutamate receptor group II and III activators against MPP(+)-induced cell death in human neuroblastoma SH-SY5Y cells: The impact of cell differentiation state. Neuropharmacology 2014, 83, 36–53. [Google Scholar] [CrossRef] [PubMed]
- Ito, K.; Eguchi, Y.; Imagawa, Y.; Akai, S.; Mochizuki, H.; Tsujimoto, Y. MPP+ induces necrostatin-1- and ferrostatin-1-sensitive necrotic death of neuronal SH-SY5Y cells. Cell Death Discov. 2017, 3, 17013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dionísio, P.E.A.; Oliveira, S.R.; Amaral, J.S.J.D.; Rodrigues, C.M.P. Loss of Microglial Parkin Inhibits Necroptosis and Contributes to Neuroinflammation. Mol. Neurobiol. 2019, 56, 2990–3004. [Google Scholar] [CrossRef] [PubMed]
- Alegre-Cortés, E.; Muriel-González, A.; Canales-Cortés, S.; Uribe-Carretero, E.; Martínez-Chacón, G.; Aiastui, A.; López de Munain, A.; Niso-Santano, M.; Gonzalez-Polo, R.A.; Fuentes, J.M.; et al. Toxicity of Necrostatin-1 in Parkinson’s Disease Models. Antioxidants 2020, 9, 524. [Google Scholar] [CrossRef] [PubMed]
- Kamalden, T.A.; Ji, D.; Osborne, N.N. Rotenone-induced death of RGC-5 cells is caspase independent, involves the JNK and p38 pathways and is attenuated by specific green tea flavonoids. Neurochem. Res. 2012, 37, 1091–1101. [Google Scholar] [CrossRef]
- Caccamo, A.; Branca, C.; Piras, I.S.; Ferreira, E.; Huentelman, M.J.; Liang, W.S.; Readhead, B.; Dudley, J.T.; Spangenberg, E.E.; Green, K.N.; et al. Necroptosis activation in Alzheimer’s disease. Nat. Neurosci. 2017, 20, 1236–1246. [Google Scholar] [CrossRef] [PubMed]
- Liu, K.; Chojnacki, J.E.; Wade, E.E.; Saathoff, J.M.; Lesnefsky, E.J.; Chen, Q.; Zhang, S. Bivalent Compound 17MN Exerts Neuroprotection through Interaction at Multiple Sites in a Cellular Model of Alzheimer’s Disease. J. Alzheimers Dis. 2015, 47, 1021–1033. [Google Scholar] [CrossRef] [Green Version]
- Yang, S.H.; Shin, J.; Shin, N.N.; Hwang, J.H.; Hong, S.C.; Park, K.; Lee, J.W.; Lee, S.; Baek, S.; Kim, K.; et al. A small molecule Nec-1 directly induces amyloid clearance in the brains of aged APP/PS1 mice. Sci. Rep. 2019, 9, 4183. [Google Scholar] [CrossRef]
- Zhang, Q.L.; Niu, Q.; Ji, X.L.; Conti, P.; Boscolo, P. Is necroptosis a death pathway in aluminum-induced neuroblastoma cell demise? Int. J. Immunopathol. Pharmacol. 2008, 21, 787–796. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qinli, Z.; Meiqing, L.; Xia, J.; Li, X.; Weili, G.; Xiuliang, J.; Junwei, J.; Hailan, Y.; Ce, Z.; Qiao, N. Necrostatin-1 inhibits the degeneration of neural cells induced by aluminum exposure. Restor. Neurol. Neurosci. 2013, 31, 543–555. [Google Scholar] [CrossRef]
- Moosavi, F.; Hosseini, R.; Saso, L.; Firuzi, O. Modulation of neurotrophic signaling pathways by polyphenols. Drug Des. Dev. Ther. 2015, 10, 23–42. [Google Scholar]
- Liu, Q.; Qiu, J.; Liang, M.; Golinski, J.; van Leyen, K.; Jung, J.E.; You, Z.; Lo, E.H.; Degterev, A.; Whalen, M.J. Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis. 2014, 5, e1084. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fan, H.; Zhang, K.; Shan, L.; Kuang, F.; Chen, K.; Zhu, K.; Ma, H.; Ju, G.; Wang, Y.Z. Reactive astrocytes undergo M1 microglia/macrohpages-induced necroptosis in spinal cord injury. Mol. Neurodegener. 2016, 11, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Del Olmo-Aguado, S.; Núñez-Álvarez, C.; Osborne, N.N. Blue Light Action on Mitochondria Leads to Cell Death by Necroptosis. Neurochem. Res. 2016, 41, 2324–2335. [Google Scholar] [CrossRef]
- Ji, D.; Kamalden, T.A.; del Olmo-Aguado, S.; Osborne, N.N. Light- and sodium azide-induced death of RGC-5 cells in culture occurs via different mechanisms. Apoptosis 2011, 16, 425–437. [Google Scholar] [CrossRef]
- Chen, R.; Hollborn, M.; Grosche, A.; Reichenbach, A.; Wiedemann, P.; Bringmann, A.; Kohen, L. Effects of the vegetable polyphenols epigallocatechin-3-gallate, luteolin, apigenin, myricetin, quercetin, and cyanidin in primary cultures of human retinal pigment epithelial cells. Mol. Vis. 2014, 20, 242–258. [Google Scholar]
- Chen, T.; Zhu, J.; Wang, Y.H.; Hang, C.H. Arc silence aggravates traumatic neuronal injury via mGluR1-mediated ER stress and necroptosis. Cell Death Dis. 2020, 11, 4. [Google Scholar] [CrossRef] [PubMed]
- Royce, G.H.; Brown-Borg, H.M.; Deepa, S.S. The potential role of necroptosis in inflammaging and aging. Geroscience 2019, 41, 795–811. [Google Scholar] [CrossRef] [PubMed]
- Zeng, X.-S.; Geng, W.-S.; Chen, L.; Jia, J.-J. Thioredoxin as a Therapeutic Target in Cerebral Ischemia. Curr. Pharm. Des. 2018, 24, 2986–2992. [Google Scholar] [CrossRef]
- Deng, X.X.; Li, S.S.; Sun, F.Y. Necrostatin-1 Prevents Necroptosis in Brains after Ischemic Stroke via Inhibition of RIPK1-Mediated RIPK3/MLKL. Signal. Aging Dis. 2019, 10, 807–817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Northington, F.J.; Chavez-Valdez, R.; Graham, E.M.; Razdan, S.; Gauda, E.B.; Martin, L.J. Necrostatin decreases oxidative damage, inflammation, and injury after neonatal HI. J. Cereb. Blood Flow Metab. 2011, 31, 178–189. [Google Scholar] [CrossRef]
- Chavez-Valdez, R.; Martin, L.J.; Flock, D.L.; Northington, F.J. Necrostatin-1 attenuates mitochondrial dysfunction in neurons and astrocytes following neonatal hypoxia-ischemia. Neuroscience 2012, 219, 192–203. [Google Scholar] [CrossRef] [Green Version]
- Chavez-Valdez, R.; Flock, D.L.; Martin, L.J.; Northington, F.J. Endoplasmic reticulum pathology and stress response in neurons precede programmed necrosis after neonatal hypoxia-ischemia. Int. J. Dev. Neurosci. 2016, 48, 58–70. [Google Scholar] [CrossRef] [Green Version]
- Chen, F.; Su, X.; Lin, Z.; Lin, Y.; Yu, L.; Cai, J.; Kang, D.; Hu, L. Necrostatin-1 attenuates early brain injury after subarachnoid hemorrhage in rats by inhibiting necroptosis. Neuropsychiatr. Dis. Treat. 2017, 13, 1771–1782. [Google Scholar] [CrossRef] [Green Version]
- Zhou, K.; Shi, L.; Wang, Z.; Zhou, J.; Manaenko, A.; Reis, C.; Chen, S.; Zhang, J. RIP1-RIP3-DRP1 pathway regulates NLRP3 inflammasome activation following subarachnoid hemorrhage. Exp. Neurol. 2017, 295, 116–124. [Google Scholar] [CrossRef] [PubMed]
- Bao, Z.; Fan, L.; Zhao, L.; Xu, X.; Liu, Y.; Chao, H.; Liu, N.; You, Y.; Liu, Y.; Wang, X.; et al. Silencing of A20 Aggravates Neuronal Death and Inflammation After Traumatic Brain Injury: A Potential Trigger of Necroptosis. Front. Mol. Neurosci. 2019, 12, 222. [Google Scholar] [CrossRef]
- Wang, Y.; Wang, H.; Tao, Y.; Zhang, S.; Wang, J.; Feng, X. Necroptosis inhibitor necrostatin-1 promotes cell protection and physiological function in traumatic spinal cord injury. Neuroscience 2014, 266, 91–101. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wang, J.; Yang, H.; Zhou, J.; Feng, X.; Wang, H.; Tao, Y. Necrostatin-1 mitigates mitochondrial dysfunction post-spinal cord injury. Neuroscience 2015, 289, 224–232. [Google Scholar] [CrossRef]
- Viringipurampeer, I.A.; Metcalfe, A.L.; Bashar, A.E.; Sivak, O.; Yanai, A.; Mohammadi, Z.; Moritz, O.L.; Gregory-Evans, C.Y.; Gregory-Evans, K. NLRP3 inflammasome activation drives bystander cone photoreceptor cell death in a P23H rhodopsin model of retinal degeneration. Hum. Mol. Genet. 2016, 25, 1501–1516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trichonas, G.; Murakami, Y.; Thanos, A.; Morizane, Y.; Kayama, M.; Debouck, C.M.; Hisatomi, T.; Miller, J.W.; Vavvas, D.G. Receptor interacting protein kinases mediate retinal detachment-induced photoreceptor necrosis and compensate for inhibition of apoptosis. Proc. Natl. Acad. Sci. USA 2010, 107, 21695–21700. [Google Scholar] [CrossRef] [Green Version]
- Nikseresht, S.; Khodagholi, F.; Nategh, M.; Dargahi, L. RIP1 Inhibition Rescues from LPS-Induced RIP3-Mediated Programmed Cell Death, Distributed Energy Metabolism and Spatial Memory Impairment. J. Mol. Neurosci. 2015, 57, 219–230. [Google Scholar] [CrossRef]
- Jinawong, K.; Apaijai, N.; Wongsuchai, S.; Pratchayasakul, W.; Chattipakorn, N.; Chattipakorn, S.C. Necrostatin-1 Mitigates Cognitive Dysfunction in Prediabetic Rats with No Alteration in Insulin Sensitivity. Diabetes 2020, 69, 1411–1423. [Google Scholar] [CrossRef]
- Duan, S.; Wang, X.; Chen, G.; Quan, C.; Qu, S.; Tong, J. Inhibiting RIPK1 Limits Neuroinflammation and Alleviates Postoperative Cognitive Impairments in D-Galactose-Induced Aged Mice. Front. Behav. Neurosci. 2018, 12, 138. [Google Scholar] [CrossRef]
- Iannielli, A.; Bido, S.; Folladori, L.; Segnali, A.; Cancellieri, C.; Maresca, A.; Massimino, L.; Rubio, A.; Morabito, G.; Caporali, L.; et al. Pharmacological Inhibition of Necroptosis Protects from Dopaminergic Neuronal Cell Death in Parkinson’s Disease Models. Cell Rep. 2018, 22, 2066–2079. [Google Scholar] [CrossRef] [Green Version]
- Lin, Q.S.; Chen, P.; Wang, W.X.; Lin, C.C.; Zhou, Y.; Yu, L.H.; Lin, Y.X.; Xu, Y.F.; Kang, D.Z. RIP1/RIP3/MLKL mediates dopaminergic neuron necroptosis in a mouse model of Parkinson disease. Lab. Investig. 2020, 100, 503–511. [Google Scholar] [CrossRef]
- Liang, Y.X.; Wang, N.N.; Zhang, Z.Y.; Juan, Z.D.; Zhang, C. Necrostatin-1 Ameliorates Peripheral Nerve Injury-Induced Neuropathic Pain by Inhibiting the RIP1/RIP3 Pathway. Front. Cell Neurosci. 2019, 13, 211. [Google Scholar] [CrossRef]
- Wang, Y.; Guo, L.; Wang, J.; Shi, W.; Xia, Z.; Li, B. Necrostatin-1 ameliorates the pathogenesis of experimental autoimmune encephalomyelitis by suppressing apoptosis and necroptosis of oligodendrocyte precursor cells. Exp. Ther. Med. 2019, 18, 4113–4119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, T.; Perera, N.D.; Chiam, M.D.F.; Cuic, B.; Wanniarachchillage, N.; Tomas, D.; Samson, A.L.; Cawthorne, W.; Valor, E.N.; Murphy, J.M.; et al. Necroptosis is dispensable for motor neuron degeneration in a mouse model of ALS. Cell Death Differ. 2020, 27, 1728–1739. [Google Scholar] [CrossRef] [PubMed]
- Wu, X.; Hu, X.; Zhang, Q.; Liu, F.; Xiong, K. Regulatory Role of Chinese Herbal Medicine in Regulated Neuronal Death. CNS Neurol. Disord. Drug Targets 2020, 27, 1728–1739. [Google Scholar] [CrossRef] [PubMed]
- Qin, S.; Yang, C.; Huang, W.; Du, S.; Mai, H.; Xiao, J.; Lü, T. Sulforaphane attenuates microglia-mediated neuronal necroptosis through down-regulation of MAPK/NF-κB signaling pathways in LPS-activated BV-2 microglia. Pharmacol. Res. 2018, 133, 218–235. [Google Scholar] [CrossRef]
- Liu, Y.L.; Hsu, C.C.; Huang, H.J.; Chang, C.J.; Sun, S.H.; Lin, A.M. Gallic Acid Attenuated LPS-Induced Neuroinflammation: Protein Aggregation and Necroptosis. Mol. Neurobiol. 2020, 57, 96–104. [Google Scholar] [CrossRef] [PubMed]
- Xuan, M.; Okazaki, M.; Iwata, N.; Asano, S.; Kamiuchi, S.; Matsuzaki, H.; Sakamoto, T.; Miyano, Y.; Lizuka, H.; Hibino, Y. Chronic Treatment with a Water-Soluble Extract from the Culture Medium of Ganoderma lucidum Mycelia Prevents Apoptosis and Necroptosis in Hypoxia/Ischemia-Induced Injury of Type 2 Diabetic Mouse Brain. Evid. Based Complement Alternat. Med. 2015, 2015, 865986. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, W.Z.; Wang, H.T.; Huang, H.J.; Lo, Y.L.; Lin, A.M. Neuroprotective Effects of Baicalein on Acrolein-induced Neurotoxicity in the Nigrostriatal Dopaminergic System of Rat Brain. Mol. Neurobiol. 2018, 55, 130–137. [Google Scholar] [CrossRef]
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Jantas, D.; Lasoń, W. Preclinical Evidence for the Interplay between Oxidative Stress and RIP1-Dependent Cell Death in Neurodegeneration: State of the Art and Possible Therapeutic Implications. Antioxidants 2021, 10, 1518. https://doi.org/10.3390/antiox10101518
Jantas D, Lasoń W. Preclinical Evidence for the Interplay between Oxidative Stress and RIP1-Dependent Cell Death in Neurodegeneration: State of the Art and Possible Therapeutic Implications. Antioxidants. 2021; 10(10):1518. https://doi.org/10.3390/antiox10101518
Chicago/Turabian StyleJantas, Danuta, and Władysław Lasoń. 2021. "Preclinical Evidence for the Interplay between Oxidative Stress and RIP1-Dependent Cell Death in Neurodegeneration: State of the Art and Possible Therapeutic Implications" Antioxidants 10, no. 10: 1518. https://doi.org/10.3390/antiox10101518
APA StyleJantas, D., & Lasoń, W. (2021). Preclinical Evidence for the Interplay between Oxidative Stress and RIP1-Dependent Cell Death in Neurodegeneration: State of the Art and Possible Therapeutic Implications. Antioxidants, 10(10), 1518. https://doi.org/10.3390/antiox10101518