Appoptosin is a Novel Pro-Apoptotic Protein and Mediates Cell Death in Neurodegeneration
Open accessAbstract
Apoptosis is an essential cellular process in multiple diseases and a major pathway for neuronal death in neurodegeneration. The detailed signaling events/pathways leading to apoptosis, especially in neurons, require further elucidation. Here we identify a β-amyloid precursor protein (APP)-interacting protein, designated as appoptosin, whose levels are upregulated in brain samples from Alzheimer's disease and infarct patients, and in rodent stroke models, as well as in neurons treated with β-amyloid (Aβ) and glutamate. We further demonstrate that appoptosin induces reactive oxygen species release and intrinsic caspase-dependent apoptosis. The physiological function of appoptosin is to transport/exchange glycine/5-amino-levulinic acid across the mitochondrial membrane for heme synthesis. Downregulation of appoptosin prevents cell death and caspase activation caused by glutamate or Aβ insults. APP modulates appoptosin-mediated apoptosis through interaction with appoptosin. Our study identifies appoptosin as a crucial player in apoptosis and a novel pro-apoptotic protein involved in neuronal cell death, providing a possible new therapeutic target for neurodegenerative disorders.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Appoptosin expression is upregulated in AD, where it can activate the intrinsic caspase pathway; downregulation of appoptosin can protect against Aβ-induced neurotoxicity.
“We have recently identified a mitochondrial protein, appoptosin, as an important regulator for Aβ-induced neuronal cell death. The expression of appoptosin is upregulated in AD, where it can activate the intrinsic caspase pathway. Notably, downregulation of appoptosin can protect against Aβ-induced neurotoxicity [101].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [101]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Alzheimer's disease: the amyloid cascade hypothesis
Hardy, J. A., & Higgins, G. A. (1992) · Science · doi:10.1126/science.1566067 · Cited by 7,484 · see citing works
Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., & Selkoe, D. J. (2002) · Nature · doi:10.1038/416535a · Cited by 4,291 · see citing works
The Bcl2 family: regulators of the cellular life-or-death switch
Cory, S., & Adams, J. M. (2002) · Nature Reviews Cancer · doi:10.1038/nrc883 · Cited by 4,032 · see citing works
Proliferation, cell cycle and apoptosis in cancer
Evan, G. I., & Vousden, K. H. (2001) · Nature · doi:10.1038/35077213 · Cited by 3,383 · see citing works
Mediation of Poly(ADP-Ribose) Polymerase-1-Dependent Cell Death by Apoptosis-Inducing Factor
Yu, S.-W., Wang, H., Poitras, M. F., Coombs, C., Bowers, W. J., Federoff, H. J., Poirier, G. G., Dawson, T. M., & Dawson, V. L. (2002) · Science · doi:10.1126/science.1072221 · Cited by 1,826 · see citing works
Hu, C., Chinenov, Y. V., & Kerppola, T. K. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00496-3 · Cited by 1,537 · see citing works
Mitochondrial fragmentation in neurodegeneration.
Knott, A. B., Perkins, G., Schwarzenbacher, R., & Bossy-Wetzel, E. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2417 · Cited by 1,002 · see citing works
Free heme toxicity and its detoxification systems in human
Kumar, S., & Bandyopadhyay, U. (2005) · Toxicology Letters · doi:10.1016/j.toxlet.2005.03.004 · Cited by 852 · see citing works
The heme synthesis and degradation pathways: role in oxidant sensitivity
Ryter, S. W., & Tyrrell, R. M. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00223-3 · Cited by 822 · see citing works
Devi, L., Prabhu, B. M., Galati, D. F., Avadhani, N. G., & Anandatheerthavarada, H. K. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1469-06.2006 · Cited by 792 · see citing works
β-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity
Zheng, H., Jiang, M., Trumbauer, M. E., SIRINATHSINGHJI, D. J. S., Hopkins, R., Smith, D. W., HEAVENS, R. P., Dawson, G. R., Boyce, S., Conner, M. W., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90073-x · Cited by 699 · see citing works
Nitric oxide‐induced mitochondrial fission is regulated by dynamin‐related GTPases in neurons
Barsoum, M. J., Yuan, H., Gerencser, A. A., Liot, G., Kushnareva, Y., Gräber, S., Kovács, I., Lee, W. D., Waggoner, J., Cui, J., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601253 · Cited by 658 · see citing works
Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy
PSP Genetics Study Group, Höglinger, G. U., Melhem, N. M., Dickson, D. W., Sleiman, P. M. A., Wang, L.-S., Klei, L., Rademakers, R., de Silva, R., Litvan, I., et al. (2011) · Nature Genetics · doi:10.1038/ng.859 · Cited by 603 · see citing works
Anandatheerthavarada, H. K., Biswas, G., Robin, M.-A., & Avadhani, N. G. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200207030 · Cited by 571 · see citing works
Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria
Pamplona, A., Ferreira, A., Balla, J., Jeney, V., Balla, G., Epiphanio, S., Chora, Â., Rodrigues, C. D., Gregoire, I. P., Cunha-Rodrigues, M., et al. (2007) · Nature Medicine · doi:10.1038/nm1586 · Cited by 560 · see citing works
Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL
Degterev, A., Lugovskoy, A. A., Cardone, M. H., Mulley, B., Wagner, G., Mitchison, T. J., & Yuan, J. (2001) · Nature Cell Biology · doi:10.1038/35055085 · Cited by 550 · see citing works
Versatility of the mitochondrial protein import machinery
Pfanner, N., & Geissler, A. (2001) · Nature reviews. Molecular cell biology · doi:10.1038/35073006 · Cited by 521 · see citing works
Borg, J.-P., Ooi, J., Levy, E., & Margolis, B. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.11.6229 · Cited by 477 · see citing works
Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms
Belmokhtar, C. A., Hillion, J., & Ségal-Bendirdjian, E. (2001) · Oncogene · doi:10.1038/sj.onc.1204436 · Cited by 475 · see citing works
TNF-Induced Signaling in Apoptosis
Rath, P., & Aggarwal, B. (1999) · Journal of Clinical Immunology · doi:10.1023/a:1020546615229 · Cited by 454 · see citing works
Arnoult, D., Gaume, B. R., Karbowski, M., Sharpe, J. C., Cecconi, F., & Youle, R. J. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg423 · Cited by 451 · see citing works
Ring, S., Weyer, S. W., Kilian, S. B., Waldron, E., Pietrzik, C. U., Filippov, M. A., Herms, J., Buchholz, C., Eckman, C. B., Korte, M., et al. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1026-07.2007 · Cited by 390 · see citing works
Biology and pathophysiology of the amyloid precursor protein
Zheng, H., & Koo, E. H. (2011) · Molecular Neurodegeneration · doi:10.1186/1750-1326-6-27 · Cited by 346 · see citing works
Guernsey, D. L., Jiang, H., Campagna, D. R., Evans, S. C., Ferguson, M., Kellogg, M. D., Lachance, M., Matsuoka, M., Nightingale, M., Rideout, A., et al. (2009) · Nature Genetics · doi:10.1038/ng.359 · Cited by 244 · cited 6× · see citing works
“Appoptosin is highly abundantly expressed in blood cells (Guernsey et al., 2009).”
BackgroundInfluentialBax Protein Expression Is Increased in Alzheimerʼs Brain
Su, J. H., Deng, G., & Cotman, C. W. (1997) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199701000-00009 · Cited by 239 · see citing works
Targeting Heme Oxygenase-1 for Neuroprotection and Neuroinflammation in Neurodegenerative Diseases
Jaźwa, A., & Cuadrado, A. (2010) · Current Drug Targets · doi:10.2174/1389450111009011517 · Cited by 209 · see citing works
Passer, B. J., Pellegrini, L., Russo, C., Siegel, R. M., Lenardo, M. J., Schettini, G., Bachmann, M. F., Tabaton, M., & D'adamio, L. (2000) · Journal of Alzheimer s Disease · doi:10.3233/jad-2000-23-408 · Cited by 207 · see citing works
Caspase-3 Is Enriched in Postsynaptic Densities and Increased in Alzheimer's Disease
Louneva, N., Cohen, J. W., Han, L., Talbot, K., Wilson, R. S., Bennett, D. A., Trojanowski, J. Q., & Arnold, S. E. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.080434 · Cited by 207 · see citing works
Haitina, T., Lindblom, J., Renström, T., & Fredriksson, R. (2006) · Genomics · doi:10.1016/j.ygeno.2006.06.016 · Cited by 182 · see citing works
Presenilin-Dependent -Secretase-Mediated Control of p53-Associated Cell Death in Alzheimer's Disease
Alves da Costa, C., Sunyach, C., Pardossi-Piquard, R., Sevalle, J., Vincent, B., Boyer, N., Kawarai, T., Girardot, N., St. George-Hyslop, P., & Checler, F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0651-06.2006 · Cited by 168 · see citing works
Ryan, K. A., & Pimplikar, S. W. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200505078 · Cited by 166 · see citing works
Heme, iron, and the mitochondrial decay of ageing
Atamna, H. (2004) · Ageing Research Reviews · doi:10.1016/j.arr.2004.02.002 · Cited by 162 · see citing works
Apoptosis effector mechanisms: A requiem performed in different keys
Hail, N., Carter, B. Z., Konopleva, M. Y., & Andreeff, M. (2006) · APOPTOSIS · doi:10.1007/s10495-006-6712-8 · Cited by 156 · see citing works
Zhang, Y., Wang, R., Liu, Q., Zhang, H., Liao, F., & Xu, H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703903104 · Cited by 150 · see citing works
Self-citationMeasurement of Heme Concentration
Sinclair, P. R., Gorman, N., & Jacobs, J. M. (1999) · Current Protocols in Toxicology · doi:10.1002/0471140856.tx0803s00 · Cited by 140 · see citing works
Biederer, T., Cao, X., Südhof, T. C., & Liu, X. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07340.2002 · Cited by 117 · see citing works
Tamayev, R., Zhou, D., & D'adamio, L. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-28 · Cited by 103 · see citing works
Mitochondrial Uncoupling Proteins in the Central Nervous System
Kim‐Han, J. S., & Dugan, L. L. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.1173 · Cited by 95 · see citing works
Han, P., Dou, F., Li, F., Zhang, X., Zhang, Y., Zheng, H., Lipton, S. A., Xu, H., & Liao, F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3831-05.2005 · Cited by 85 · see citing works
Self-citationNeuronal Apoptosis in Neurodegenerative Diseases: From Basic Research to Clinical Application
Kermer, P., Liman, J., Weishaupt, J. H., & Bähr, M. (2004) · Neurodegenerative Diseases · doi:10.1159/000076665 · Cited by 84 · see citing works
Molecular and Cellular Mechanisms for Alzheimers Disease:Understanding APP Metabolism
Zhang, Y., & Xu, H. (2007) · Current Molecular Medicine · doi:10.2174/156652407782564462 · Cited by 82 · see citing works
Self-citationThe intracellular domain of the amyloid precursor protein (AICD) enhances the p53-mediated apoptosis
Ozaki, T., Li, Y., Kikuchi, H., Tomita, T., Iwatsubo, T., & Nakagawara, A. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.09.162 · Cited by 76 · see citing works
Apocytochrome c Blocks Caspase-9 Activation and Bax-induced Apoptosis
Martín, Á. G., & Fearnhead, H. O. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m209369200 · Cited by 61 · see citing works
Giliberto, L., Zhou, D., Weldon, R., Tamagno, E., Luca, P. D., Tabaton, M., & D'adamio, L. (2008) · Molecular Neurodegeneration · doi:10.1186/1750-1326-3-12 · Cited by 50 · see citing works
Ma, T., Zhao, Y., Kwak, Y. D., Yang, Z.-M., Thompson, R., Luo, Z., Xu, H., & Liao, F. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6150-08.2009 · Cited by 48 · see citing works
Self-citationApo cytochrome c inhibits caspases by preventing apoptosome formation
Martín, Á. G., Nguyen, J. T., Wells, J. A., & Fearnhead, H. O. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.05.084 · Cited by 36 · see citing works
Casella, L., Monzani, E., Roncone, R., Nicolis, S., Sala, A., & De Riso, A. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s5709 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease
Guo, T., Zhang, D., Zeng, Y., Huang, T. Y., Xu, H., & Zhao, Y. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00391-7 · Cited by 994 · see citing works
Self-citationOligomeric Aβ-induced synaptic dysfunction in Alzheimer’s disease
Tu, S., Okamoto, S., Lipton, S. A., & Xu, H. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-48 · Cited by 582 · see citing works
Self-citationPotential neuroprotective properties of epigallocatechin-3-gallate (EGCG)
Singh, N. A., Mandal, A. K. A., & Khan, Z. A. (2015) · Nutrition Journal · doi:10.1186/s12937-016-0179-4 · Cited by 319 · see citing works
Beneficial Effects of Green Tea Catechins on Neurodegenerative Diseases
Pervin, M., Unno, K., Ohishi, T., Tanabe, H., Miyoshi, N., & Nakamura, Y. (2018) · Molecules · doi:10.3390/molecules23061297 · Cited by 258 · see citing works
Neuroprotective Natural Products for Alzheimer’s Disease
Chen, X., Drew, J., Berney, W., & Lei, W. (2021) · Cells · doi:10.3390/cells10061309 · Cited by 236 · see citing works
Rösler, T. W., Marvian, A. T., Brendel, M., Nykänen, N.-P., Höllerhage, M., Schwarz, S. C., Hopfner, F., Koeglsperger, T., Respondek, G., Schweyer, K., et al. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.101644 · Cited by 219 · see citing works
Mitochondrial Dysfunction: Different Routes to Alzheimer’s Disease Therapy
Picone, P., Nuzzo, D., Caruana, L., Scafidi, V., & Carlo, M. D. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/780179 · Cited by 208 · see citing works
Tau Proteolysis in the Pathogenesis of Tauopathies: Neurotoxic Fragments and Novel Biomarkers
Quinn, J. P., Corbett, N. J., Kellett, K. A. B., & Hooper, N. M. (2018) · Journal of Alzheimer's Disease · doi:10.3233/jad-170959 · Cited by 170 · see citing works
Zhao, Y., Tseng, I.-C., Heyser, C. J., Rockenstein, E., Mante, M., Adame, A., Zheng, Q., Huang, T., Wang, X., Arslan, P. E., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.020 · Cited by 98 · see citing works
Self-citationMitochondria as pharmacological targets in Down syndrome
Valenti, D., Braidy, N., Rasmo, D. D., Signorile, A., Rossi, L., Atanasov, A. G., Volpicella, M., Henrion‐Caude, A., Nabavi, S. M., & Vacca, R. A. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.08.014 · Cited by 96 · see citing works
Olive oil phenols and neuroprotection
Khalatbary, A. R. (2013) · Nutritional Neuroscience · doi:10.1179/1476830513y.0000000052 · Cited by 89 · see citing works
Ratan, Y., Rajput, A., Maleysm, S., Pareek, A., Jain, V. K., Pareek, A., Kaur, R., & Singh, G. (2023) · Biomedicines · doi:10.3390/biomedicines11051398 · Cited by 87 · see citing works
Dharmalingam, P., & Sudhandiran, G. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.07.017 · Cited by 83 · see citing works
Allen, M., Burgess, J. D., Ballard, T., Serie, D., Wang, X., Younkin, C. S., Sun, Z., Kouri, N., Baheti, S., Wang, C., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-016-1576-7 · Cited by 78 · see citing works
Melatonin and Ischemic Stroke: Mechanistic Roles and Action
Andrabi, S. S., Parvez, S., & Tabassum, H. (2015) · Advances in Pharmacological Sciences · doi:10.1155/2015/384750 · Cited by 77 · see citing works
Human Tau Isoforms and Proteolysis for Production of Toxic Tau Fragments in Neurodegeneration
Boyarko, B., & HOOK, V. Y. H. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.702788 · Cited by 74 · see citing works
Fukutomi, R., Ohishi, T., Koyama, Y., Pervin, M., Nakamura, Y., & Isemura, M. (2021) · Molecules · doi:10.3390/molecules26020415 · Cited by 73 · see citing works
The Role of Mitochondrial Impairment in Alzheimer´s Disease Neurodegeneration: The Tau Connection
Quntanilla, R. A., & Tapia-Monsalves, C. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200525020259 · Cited by 59 · see citing works
BAD-mediated neuronal apoptosis and neuroinflammation contribute to Alzheimer's disease pathology
Zhang, L., Qian, Y., Li, J., Zhou, X., Xu, H. J., Yan, J., Xiang, J., Yuan, X., Sun, B., Sisodia, S. S., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102942 · Cited by 53 · see citing works
Self-citationGlucocorticoid-driven mitochondrial damage stimulates Tau pathology
Du, F., Yu, Q., Swerdlow, R. H., & Waites, C. L. (2023) · Brain · doi:10.1093/brain/awad127 · Cited by 51 · see citing works
A Review of Treatment Options for Progressive Supranuclear Palsy
Stamelou, M., & Höglinger, G. U. (2016) · CNS Drugs · doi:10.1007/s40263-016-0347-2 · Cited by 42 · see citing works
3-N-butylphthalide improves neuronal morphology after chronic cerebral ischemia
Wang, H., Zhao, W., Luo, C., Wang, J., Gong, J., Li, B., Gong, Y.-X., & Wang, J. (2014) · Neural Regeneration Research · doi:10.4103/1673-5374.131576 · Cited by 41 · see citing works
Shen, Y., Zhao, M., Zhao, P., Meng, L., Zhang, Y., Zhang, G., Taishi, Y., & Sun, L. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1408462 · Cited by 43 · see citing works
Self-citationProgressive supranuclear palsy
Giagkou, N., Höglinger, G. U., & Stamelou, M. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.10.013 · Cited by 41 · see citing works
Zhu, L.-Z., Hou, Y., Zhao, M., Yang, M., Fu, X., Sun, J., Fu, X., Shao, L.-R., Zhang, H., Fan, C., et al. (2016) · Cell Biology and Toxicology · doi:10.1007/s10565-016-9338-9 · Cited by 39 · see citing works
Self-citationZhang, C., Shi, Z., Zhang, L., Zhou, Z., Zheng, X., Liu, G., Bu, G., Fraser, P. E., Xu, H., & Zhang, Y. (2016) · Journal of Cell Science · doi:10.1242/jcs.176792 · Cited by 33 · see citing works
Self-citationDentate gyrus volume deficit in schizophrenia
Nakahara, S., Turner, J. A., Calhoun, V. D., Lim, K. O., Mueller, B., Bustillo, J. R., O'Leary, D. S., McEwen, S., Voyvodic, J. T., Belger, A., et al. (2019) · Psychological Medicine · doi:10.1017/s0033291719001144 · Cited by 33 · see citing works
Characterization of Mitochondrial Dysfunction in the 7PA2 Cell Model of Alzheimer's Disease
Jakovljevic, N. K., Magnifico, M. C., Arese, M., Meli, G., Forte, E., Lecci, A., Manca, A., Giuffrè, A., Mastronicola, D., Sarti, P., et al. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-130728 · Cited by 32 · see citing works
Dubey, K. K., Janve, M., Ray, A., & Singhal, R. S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816938-4.00004-5 · Cited by 30 · see citing works
Zheng, K.-M., Zhang, J., Zhang, C.-L., Zhang, Y., & Chen, X. (2015) · Acta Pharmacologica Sinica · doi:10.1038/aps.2014.166 · Cited by 28 · see citing works
Self-citationTatura, R., Buchholz, M., Dickson, D. W., Swieten, J. C. V., McLean, C., Höglinger, G. U., & Müller, U. (2016) · Neurogenetics · doi:10.1007/s10048-016-0480-6 · Cited by 27 · see citing works
Alzheimer's disease: the role of mitochondrial dysfunction and potential new therapies
Hawking, Z. L. (2016) · Bioscience Horizons The International Journal of Student Research · doi:10.1093/biohorizons/hzw014 · Cited by 27 · see citing works
Mitochondrial Dynamics in Brain Cells During Normal and Pathological Aging
Sukhorukov, V. S., Baranich, T. I., Egorova, A. V., Akateva, A. V., Okulova, K. M., Ryabova, M. S., Андреевна, С. К., Dmitriev, O. V., Mudzhiri, N. M., Воронков, Д. Н., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252312855 · Cited by 27 · see citing works
Kamrani-Sharif, R., Hayes, A. W., Gholami, M., Salehirad, M., Khani, M. A., Motaghinejad, M., & Emanuele, E. (2023) · Neuropeptides · doi:10.1016/j.npep.2023.102352 · Cited by 27 · see citing works
Li, Y., Tong, R., Li, Z., Zhang, X., Pan, L., Li, Y., & Zhang, N. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.163039 · Cited by 25 · see citing works
Self-citationDentate gyrus volume deficit in schizophrenia.
Nakahara, S., Turner, J. A., Calhoun, V. D., Lim, K. O., Mueller, B. A., Bustillo, J., OʼLeary, D. S., McEwen, S. C., Voyvodic, J. T., Belger, A., et al. (2020) · eScholarship (California Digital Library) · Cited by 24 · see citing works
Mini review: Mitochondrial dysfunction in Alzheimer's disease: Therapeutic implications of lithium
Singulani, M. P., Paula, V. J. R. D., & Forlenza, O. V. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.136078 · Cited by 23 · see citing works
Mitochondrial defects: An emerging theranostic avenue towards Alzheimer's associated dysregulations
Mani, S., Swargiary, G., Singh, M., Agarwal, S., Dey, A., Ojha, S. K., & Jha, N. K. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119985 · Cited by 23 · see citing works
Caspase-8 Mediates Amyloid-β-induced Apoptosis in Differentiated PC12 Cells
Qian, M., Liu, J., Yao, J., Wang, W., Yang, J., Wei, L., Shen, Y.-D., & Chen, W. (2015) · Journal of Molecular Neuroscience · doi:10.1007/s12031-015-0498-5 · Cited by 21 · see citing works
Self-citationExploring the role of mitochondrial proteins as molecular target in Alzheimer’s disease
Chadha, S., Behl, T., Sehgal, A., Kumar, A., & BUNGAU, S. G. (2020) · Mitochondrion · doi:10.1016/j.mito.2020.11.008 · Cited by 20 · see citing works
Novel Therapies for Parkinsonian Syndromes–Recent Progress and Future Perspectives
Przewodowska, D., Marzec, W. Z., & Madetko‐Alster, N. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.720220 · Cited by 19 · see citing works
Li, X., Wang, L., Cykowski, M. D., He, T., Liu, T., Chakranarayan, J., Rivera, A. L., Zhao, H., Powell, S. Z.-E., Xia, W., et al. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2019.11.030 · Cited by 18 · see citing works
Atypical parkinsonism – new advances
Stamelou, M., & Bhatia, K. P. (2016) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000355 · Cited by 18 · see citing works
Oxidative Stress and Alzheimer’s Disease
Wu, Y., Xu, Q., & Song, W. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_197 · Cited by 14 · see citing works
Appoptosin Mediates Lesions Induced by Oxidative Stress Through the JNK-FoxO1 Pathway
Zhang, C., Tan, Z., Xie, Y., Zhao, Y., Huang, T. Y., Lu, Z. C., Luo, H., Can, D., Xu, H., Zhang, Y., et al. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00243 · Cited by 12 · see citing works
Self-citationFiciarà, E., Stura, I., Vernone, A., Silvagno, F., Cavalli, R., & Guiot, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042337 · Cited by 11 · see citing works
Hu, H., Cui, Z., Li, H., Wang, Y., Chen, X. '., Li, J.-H., Xv, D., & Zheng, G. (2014) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2014/942917 · Cited by 11 · see citing works
Sun, N., Chu, L., Yuan, L., & Qi, Z. (2019) · Folia Neuropathologica · doi:10.5114/fn.2019.86295 · Cited by 10 · see citing works
Overexpression of SLC25A38 protein on acute lymphoblastic leukemia cells
Chen, H., Lu, Q., Zhang, Y., ZHANG, C., Zhang, H., & Xu, H. (2014) · Oncology Letters · doi:10.3892/ol.2014.1947 · Cited by 10 · see citing works
Self-citationEffect of Artesunate vs Memantine in Aluminum Chloride Induced Model of Neurotoxicity in Rats
Shata, A., Elkashef, W. F., Hamouda, M. A., & Eissa, H. (2020) · Advances in Alzheimer s Disease · doi:10.4236/aad.2020.91001 · Cited by 8 · see citing works
Shailaja, R., Tamilarasan, G., Parthasarathy, K., & Parameswaran, S. (2020) · Advanced Powder Technology · doi:10.1016/j.apt.2020.06.002 · Cited by 7 · see citing works
Marzetti, E., Lorenzo, R. D., Calvani, R., Coelho‐Júnior, H. J., D’Argento, E., Pesce, V., Landi, F., Bucci, C., Guerra, F., & Picca, A. (2026) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2026.112167 · Cited by 6 · see citing works
Yan, C., Yue, Y., Mu, H.-L., Wu, T., Huang, W.-S., Wu, Y., Sun, W., Liang, L., Duan, W., Ouyang, S., et al. (2023) · iScience · doi:10.1016/j.isci.2023.108690 · Cited by 6 · see citing works
Neuroprotection induced by epigallocatechin-3-gallate
Tripathi, S., Mishra, R., Shrivastava, R., Srivastava, V. K., & Singh, G. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23763-8.00029-4 · Cited by 5 · see citing works
Shome, A., Jha, K. T., Chahat, Chawla, V., & Chawla, P. A. (2024) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/0118715273315191241002115155 · Cited by 4 · see citing works
Liu, M., Zeng, C., & Si, Z. (2026) · Pharmaceuticals · doi:10.3390/ph19040629 · Cited by 3 · see citing works
Li, L., Wang, J., Tang, L. F. P., Yu, X., Sui, Y., & Zhang, C. (2012) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3421 · Cited by 3 · see citing works
Overexpression of appoptosin promotes mitochondrial damage in MIN6 cells
Wang, T., Wei, W., Mansai, H., Huang, C., Li, L., Ye, Q., Yin, H., Yang, C., Li, X.-J., Liu, S.-H., et al. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.8759 · Cited by 3 · see citing works
Overview and Applications of Nanocarrier-Based Drug Delivery for Alleviating Alzheimer’s Disease
Khan, S. A., Haider, M. F., & Naseem, N. (2025) · Journal of Bio-X Research · doi:10.34133/jbioxresearch.0042 · Cited by 2 · see citing works
ClC-3 chloride channel in hippocampal neuronal apoptosis.
Xu, L., Zhang, S., Fan, H., Zhong, Z., Li, X., Jin, X., & Quan-zhong, C. (2013) · PubMed Central · doi:10.3969/j.issn.1673-5374.2013.32.008 · Cited by 2 · see citing works
From a single nucleotide polymorphism to tau pathology: Appoptosin is the missing link
Respondek, G., Höglinger, G. U., & Stamelou, M. (2015) · Movement Disorders · doi:10.1002/mds.26464 · Cited by 2 · see citing works
Soleymaninejadian, E., & Dehkordi, M. S. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1619456 · Cited by 1 · see citing works
Monitoring of Single Vesicle Cytochrome-c Release Illuminates BAK as a Novel Target of Aβ Oligomers
Linseman, D. A. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2014.08.012
THE INFLUENCE OF ENVIRONMENTAL FACTORS ON THE ACTIVITY OF BLOOD CELL APOPTOSIS
Наурзбаевна, К. У., Sh., K. B., Makashev, E. K., & Кустова, Е. А. (2016) · Ecology & Safety
Differential Expression of SLC25A38 Gene in Patients of Acute Lymphoblastic Leukemia
Kumar, S., Prakash, P., Kumar, S., Raj, S., & Sinha, P. (2021) · Indian Journal of Medical Biochemistry · doi:10.5005/jp-journals-10054-0168
Differential Expression of SLC25A38 Gene in Patients of Acute Lymphoblastic Leukaemia
Prakash, P., Kumar, S., Kumar, S., Raj, H., & Sinha, P. (2022) · National Journal of Laboratory Medicine · doi:10.7860/njlm/2022/50387.2578
Data Mining and Biochemical Profiling Reveal Novel Biomarker Candidates in Alzheimer’s Disease
Vernone, A., Stura, I., Guiot, C., D’Agata, F., & Silvagno, F. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26157536
Morciano, G., Gorgoglione, R., Porcelli, V., Ahmed, A., Scarcia, P., Vozza, A., Lasorsa, F. M., Fiermonte, G., & Palmieri, L. (2026) · Biomolecules · doi:10.3390/biom16060842
- Authors
- Zhang, H., Zhang, Y.-W., Chen, Y., Huang, X., Zhou, F., Wang, W., Xian, B., Zhang, X., Masliah, E., Chen, Q., Han, J.-D. J., Bu, G., Reed, J. C., Liao, F.-F., Chen, Y.-G., & Xu, H.
- Affiliations
- Sanford Burnham Prebys Medical Discovery Institute (US)
- Tsinghua University (CN)
- Xiamen University (CN)
- Chinese Academy of Sciences (CN)
- University of California San Diego (US)
- University of Tennessee Health Science Center (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-10-31
- Volume
- 32
- Issue
- 44
- Pages
- 15565-15576
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3509748
- OpenAlex
- W2033166503
- Cited by
- 68
- References
- 47
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 5 · 2022: 1 · 2021: 8 · 2020: 7 · 2019: 6 · 2018: 3 · 2017: 1 · 2016: 8 · 2015: 7 · 2014: 7 · 2013: 3 · 2012: 1
- FWCI
- 2.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
- Funders
- Alzheimer's Association
- American Health Assistance Foundation
- National Natural Science Foundation of China (30930050)
- Natural Science Foundation of Fujian Province
- Fok Ying Tung Education Foundation
- National Institutes of Health
- Program for New Century Excellent Talents in University
- National Key Research and Development Program of China (2010CB833706)
- Fundamental Research Funds for the Central Universities
- National Institute on Aging (P01AG030128, R01AG038710, R01AG027924, R01AG030197, R37AG018440, R01AG018440, R03AG034366, P50AG005131, AG-5131, R01AG031893, R21AG038968, AG 18440, R01AG021173, R01AG035355)
- National Institute of Neurological Disorders and Stroke (R01NS046673, R01NS054880, P01NS074969)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- apoptosis, neurodegeneration, Alzheimer's disease, amyloid-beta, glutamate excitotoxicity, neuronal cell death, reactive oxygen species, caspase activation, heme biosynthesis, 5-aminolevulinic acid, glycine transport, stroke, therapeutic target
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Animals, Female, Genetic Complementation Test, Heme, Humans, Immunohistochemistry, Male, Microscopy, Fluorescence, Mitochondria, Nerve Degeneration, Neurons, Pregnancy, Amyloid beta-Protein Precursor, Cell Death, Apoptosis, Annexin A5, Reactive Oxygen Species, Caspases, Brain Infarction, RNA Interference, Cell Line, Tumor, Apoptosis Regulatory Proteins, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
