Age- and disease-dependent increase of the mitophagy marker phospho-ubiquitin in normal aging and Lewy body disease
Open accessAbstract
Although exact causes of Parkinson disease (PD) remain enigmatic, mitochondrial dysfunction is increasingly appreciated as a key determinant of dopaminergic neuron susceptibility in both familial and sporadic PD. Two genes associated with recessive, early-onset PD encode the ubiquitin (Ub) kinase PINK1 and the E3 Ub ligase PRKN/PARK2/Parkin, which together orchestrate a protective mitochondrial quality control (mitoQC) pathway. Upon stress, both enzymes cooperatively identify and decorate damaged mitochondria with phosphorylated poly-Ub (p-S65-Ub) chains. This specific label is subsequently recognized by autophagy receptors that further facilitate mitochondrial degradation in lysosomes (mitophagy). Here, we analyzed human post-mortem brain specimens and identified distinct pools of p-S65-Ub-positive structures that partially colocalized with markers of mitochondria, autophagy, lysosomes and/or granulovacuolar degeneration bodies. We further quantified levels and distribution of the 'mitophagy tag' in 2 large cohorts of brain samples from normal aging and Lewy body disease (LBD) cases using unbiased digital pathology. Somatic p-S65-Ub structures independently increased with age and disease in distinct brain regions and enhanced levels in LBD brain were age- and Braak tangle stage-dependent. Additionally, we observed significant correlations of p-S65-Ub with LBs and neurofibrillary tangle levels in disease. The degree of co-existing p-S65-Ub signals and pathological PD hallmarks increased in the pre-mature stage, but decreased in the late stage of LB or tangle aggregation. Altogether, our study provides further evidence for a potential pathogenic overlap among different forms of PD and suggests that p-S65-Ub can serve as a biomarker for mitochondrial damage in aging and disease. ABBREVIATIONS: BLBD: brainstem predominant Lewy body disease; CCCP: carbonyl cyanide m-chlorophenyl hydrazone; DLB: dementia with Lewy bodies; DLBD: diffuse neocortical Lewy body disease; EOPD: early-onset Parkinson disease; GVB: granulovacuolar degeneration body; LB: Lewy body; LBD: Lewy body disease; mitoQC: mitochondrial quality control; nbM: nucleus basalis of Meynert; PD: Parkinson disease; PDD: Parkinson disease with dementia; p-S65-Ub: PINK1-phosphorylated serine 65 ubiquitin; SN: substantia nigra; TLBD: transitional Lewy body disease; Ub: ubiquitin.
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?
Phospho-ubiquitin mitophagy markers label granulovacuolar bodies and their abundance correlates with neurofibrillary tangle density.
“Most recently, phospho-ubiquitin mitophagy markers label granulovacuolar bodies and their abundance has been shown to correlate with neurofibrillary tangle density, suggesting they may be a cellular response to damage in the neurons [80].”
From The neuropathological diagnosis of Alzheimer's disease (2019) · cites this paper as [80]
pS65-Ub accumulates during aging, stress, and disease.
“pS65-Ub has been shown to accumulate during aging, stress, and disease [13, 14]”
From miRNA family miR-29 inhibits PINK1-PRKN signaling via ATG9A (2026) · cites this paper as [14]
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
Staging of brain pathology related to sporadic Parkinson’s disease
Braak, H., Tredici, K. D., Rüb, U., de Vos, R. A. I., Jansen Steur, E. N. H., & Braak, E. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00065-9 · Cited by 10,777 · see citing works
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
Diagnosis and management of dementia with Lewy bodies: Fourth consensus report of the DLB Consortium
McKeith, I. G., Boeve, B. F., Dickson, D. W., Halliday, G., Taylor, J.-P., Weintraub, D., Aarsland, D., Galvin, J., Attems, J., Ballard, C. G., et al. (2017) · Neurology · doi:10.1212/wnl.0000000000004058 · Cited by 4,476 · see citing works
Self-citationClinical diagnostic criteria for dementia associated with Parkinson’s disease
Emre, M., Aarsland, D., Brown, R., Burn, D. J., Duyckaerts, C., Mizuno, Y., Broe, G. A., Cummings, J., Dickson, D. W., Gauthier, S., et al. (2007) · Movement Disorders · doi:10.1002/mds.21507 · Cited by 3,027 · see citing works
Self-citationPINK1 Is Selectively Stabilized on Impaired Mitochondria to Activate Parkin
Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D.-F., Gautier, C. A., Shen, J., Cookson, M. R., & Youle, R. J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000298 · Cited by 2,944 · see citing works
PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1
Geisler, S., Holmström, K. M., Skujat, D., Fiesel, F. C., Rothfuss, O. C., Kahle, P. J., & Springer, W. (2010) · Nature Cell Biology · doi:10.1038/ncb2012 · Cited by 2,835 · see citing works
Self-citationThe ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy
Lazarou, M., Sliter, D. A., Kane, L. A., Sarraf, S. A., Wang, C., Burman, J. L., Sideris, D. P., Fogel, A. I., & Youle, R. J. (2015) · Nature · doi:10.1038/nature14893 · Cited by 2,774 · see citing works
Stages of the Pathologic Process in Alzheimer Disease: Age Categories From 1 to 100 Years
Braak, H., Thal, D. R., Ghebremedhin, E., & Del Tredici, K. (2011) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e318232a379 · Cited by 2,194 · see citing works
Matsuda, N., Sato, S., Shiba, K., Okatsu, K., Saisho, K., Gautier, C. A., Sou, Y.-S., Saiki, S., Kawajiri, S., Sato, F., et al. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200910140 · Cited by 1,969 · see citing works
Lees, A. J., Hardy, J., & Revesz, T. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60492-x · Cited by 1,956 · see citing works
Genome-wide association study reveals genetic risk underlying Parkinson's disease
Simón‐Sánchez, J., Schulte, C., Brás, J., Sharma, M., Gibbs, J. R., Berg, D., Paisán‐Ruiz, C., Lichtner, P., Scholz, S. W., Hernandez, D. G., et al. (2009) · Nature Genetics · doi:10.1038/ng.487 · Cited by 1,916 · see citing works
Incidence of Parkinson's Disease: Variation by Age, Gender, and Race/Ethnicity
Eeden, S. K. V. D. (2003) · American Journal of Epidemiology · doi:10.1093/aje/kwg068 · Cited by 1,746 · see citing works
PINK1-dependent recruitment of Parkin to mitochondria in mitophagy
Vives-Bauza, C., Zhou, C., Huang, Y., Cui, M., de Vries, R. L. A., Kim, J., May, J., Tocilescu, M. A., Liu, W., Ko, H. S., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911187107 · Cited by 1,616 · see citing works
The mitochondrial basis of aging
Sun, N., Youle, R. J., & Finkel, T. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.01.028 · Cited by 1,441 · see citing works
Chu, C. T., Ji, J., Dagda, R. K., Jiang, J. F., Tyurina, Y. Y., Kapralov, A. A., Tyurin, V. A., Yanamala, N., Shrivastava, I. H., Mohammadyani, D., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2837 · Cited by 1,083 · see citing works
Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria
Dickson, D. W., Braak, H., Duda, J. E., Duyckaerts, C., Gasser, T., Halliday, G. M., Hardy, J., Leverenz, J. B., Del Tredici, K., Wszolek, Z. K., et al. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70238-8 · Cited by 972 · see citing works
Self-citationHeo, J.-M., Ordureau, A., Paulo, J. A., Rinehart, J., & Harper, J. W. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.08.016 · Cited by 906 · see citing works
Initiation and Synergistic Fibrillization of Tau and Alpha-Synuclein
Giasson, B. I., Forman, M. S., Higuchi, M., Golbe, L. I., Graves, C. L., Kotzbauer, P. T., Trojanowski, J. Q., & Lee, V. M.-Y. (2003) · Science · doi:10.1126/science.1082324 · Cited by 879 · cited 1× · see citing works
“Both SNCA and MAPT pathologies may act synergistically [9], and variants in genes encoding these 2 proteins are the most significant genetic PD risk factors known [10].”
BackgroundMitophagy and Alzheimer’s Disease: Cellular and Molecular Mechanisms
Kerr, J. S., Adriaanse, B. A., Greig, N. H., Mattson, M. P., Cader, M. Z., Bohr, V. A., & Fang, E. F. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.01.002 · Cited by 870 · see citing works
Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans
Palikaras, K., Lionaki, E., & Tavernarakis, N. (2015) · Nature · doi:10.1038/nature14300 · Cited by 770 · see citing works
Sun, N., Yun, J., Liu, J., Malide, D. A., Liu, C., Rovira, I. I., Holmström, K. M., Fergusson, M. M., Yoo, Y. H., Combs, C. A., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.10.009 · Cited by 696 · see citing works
Mitochondrial dysfunction in Parkinson's disease
Bose, A., & Beal, M. F. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13731 · Cited by 598 · see citing works
The parkinson's complex: Parkinsonism is just the tip of the iceberg
Langston, J. W. (2006) · Annals of Neurology · doi:10.1002/ana.20834 · Cited by 585 · see citing works
Gibb, W. R. G., & Lees, A. J. (1991) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.54.5.388 · Cited by 574 · see citing works
mito-QC illuminates mitophagy and mitochondrial architecture in vivo
McWilliams, T. G., Prescott, A. R., Allen, G. F. G., Tamjar, J., Munson, M. J., Thomson, C., Muqit, M. M. K., & Ganley, I. G. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201603039 · Cited by 541 · see citing works
Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy
Sentelle, R. D., Senkal, C. E., Jiang, W., Ponnusamy, S., Gencer, S., Panneer Selvam, S., Ramshesh, V. K., Peterson, Y. K., Lemasters, J. J., Szulc, Z. M., et al. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.1059 · Cited by 539 · cited 1× · see citing works
“These include different receptor[46] and lipid-mediated [47,48] pathways that recruit phagophores independent of ubiquitin via direct binding to MAP1LC3A family members.”
BackgroundMitochondrial dysfunction and mitophagy in Parkinson's: from familial to sporadic disease
Ryan, B. J., Hoek, S., Fon, E. A., & Wade-Martins, R. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.02.003 · Cited by 524 · see citing works
Ashrafi, G., Schlehe, J. S., LaVoie, M. J., & Schwarz, T. L. (2014) · Journal of Cell Biology · doi:10.1083/jcb.201401070 · Cited by 502 · see citing works
Inhibition of mitochondrial fusion by α‐synuclein is rescued by PINK1, Parkin and DJ‐1
Kamp, F., Exner, N., Lutz, A. K., Wender, N., Hegermann, J., Brunner, B., Nuscher, B., Bartels, T., Giese, A., Beyer, K., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.223 · Cited by 481 · see citing works
Living on the edge with too many mouths to feed: Why dopamine neurons die
Bolam, J. P., & Pissadaki, E. K. (2012) · Movement Disorders · doi:10.1002/mds.25135 · Cited by 439 · see citing works
Jin, S. M., & Youle, R. J. (2013) · Autophagy · doi:10.4161/auto.26122 · Cited by 411 · see citing works
Kosaka, K., Yoshimura, M., Ikeda, K., & Budka, H. (1984) · PubMed · Cited by 401 · see citing works
Parkin and PINK1: much more than mitophagy
Scarffe, L. A., Stevens, D. A., Dawson, V. L., & Dawson, T. M. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.03.004 · Cited by 392 · see citing works
Lysosomal impairment in Parkinson's disease
Dehay, B., Martinez‐Vicente, M., Caldwell, G. A., Caldwell, K. A., Yue, Z., Cookson, M. R., Klein, C., Vila, M., & Bezard, E. (2013) · Movement Disorders · doi:10.1002/mds.25462 · Cited by 340 · see citing works
Rana, A., Rera, M., & Walker, D. W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216197110 · Cited by 335 · see citing works
Cai, Q., Zakaria, H. M., Simone, A., & Sheng, Z. (2012) · Current Biology · doi:10.1016/j.cub.2012.02.005 · Cited by 332 · see citing works
Murray, M. E., Lowe, V. J., Graff-Radford, N. R., Liesinger, A. M., Cannon, A., Przybelski, S. A., Rawal, B., Parisi, J. E., Petersen, R. C., Kantarci, K., et al. (2015) · Brain · doi:10.1093/brain/awv050 · Cited by 324 · see citing works
Self-citationNeuronal vulnerability, pathogenesis, and Parkinson's disease
Sulzer, D. L., & Surmeier, D. J. (2012) · Movement Disorders · doi:10.1002/mds.25095 · Cited by 315 · see citing works
The Genetics of Parkinson Disease
Bekris, L. M., Mata, I. F., & Zabetian, C. P. (2010) · Journal of Geriatric Psychiatry and Neurology · doi:10.1177/0891988710383572 · Cited by 307 · see citing works
Self-citationAutophagy and A lpha‐ S ynuclein: R elevance to P arkinson's D isease and R elated S ynucleopathies
Xilouri, M., Brekk, O. R., & Stefanis, L. (2016) · Movement Disorders · doi:10.1002/mds.26477 · Cited by 266 · see citing works
Zhu, J., Guo, F., Shelburne, J. D., Watkins, S. C., & Chu, C. T. (2003) · Brain Pathology · doi:10.1111/j.1750-3639.2003.tb00478.x · Cited by 255 · see citing works
Truban, D., Hou, X., Caulfield, T. R., Fiesel, F. C., & Springer, W. (2016) · Journal of Parkinson’s Disease · doi:10.3233/jpd-160989 · Cited by 237 · see citing works
Self-citationAlterations in Mitochondrial Quality Control in Alzheimer’s Disease
Cai, Q., & Tammineni, P. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00024 · Cited by 215 · see citing works
Wills, J., Jones, J. M., Haggerty, T., Duka, V., Joyce, J. N., & Sidhu, A. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.06.017 · Cited by 211 · see citing works
(Patho‐)physiological relevance of PINK1‐dependent ubiquitin phosphorylation
Fiesel, F. C., Ando, M., Hudec, R., Hill, A. R., Castanedes‐Casey, M., Caulfield, T. R., Moussaud‐Lamodière, E. L., Stankowski, J. N., Bauer, P. O., Lorenzo‐Betancor, O., et al. (2015) · The EMBO Reports · doi:10.15252/embr.201540514 · Cited by 185 · cited 12× · see citing works
“For comparing different antibodies in the detection of peptide, N-terminal biotinylated p-S65-Ub (custom-made at Thinkpeptides) [25] was run on the gel at serial dilution from 10–500 ng and detected with 0.75 µg/ml p-S65Ub antibodies (in-house [25] or Millipore Sigma, ABS1513).”
BackgroundMethodInfluentialSelf-citationNeuronal vulnerability, pathogenesis, and Parkinson's disease
Sulzer, D., & Surmeier, D. J. (2013) · Movement Disorders · doi:10.1002/mds.25187 · Cited by 184 · see citing works
Lysosomal Dysfunction and α‐Synuclein Aggregation in Parkinson's Disease: Diagnostic Links
Moors, T. E., Paciotti, S., Chiasserini, D., Calabresi, P., Parnetti, L., Beccari, T., & van de Berg, W. D. J. (2016) · Movement Disorders · doi:10.1002/mds.26562 · Cited by 175 · see citing works
Hu, Y., Li, X., Wang, Z.-H., Luo, Y., Zhang, X., Liu, X., Feng, Q., Wang, Q., Yue, Z., Chen, Z., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.7861 · Cited by 171 · see citing works
Mitochondrial Proteostasis in the Control of Aging and Longevity
Jensen, M. B., & Jasper, H. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.05.006 · Cited by 164 · see citing works
Haddad, D., & Nakamura, K. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.10.021 · Cited by 162 · see citing works
Fujishiro, H., Ferman, T. J., Boeve, B. F., Smith, G. E., Graff‐Radford, N. R., Uitti, R. J., Wszołek, Z. K., Knopman, D. S., Petersen, R. C., Parisi, J. E., et al. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31817d7a1d · Cited by 161 · see citing works
Self-citationHeterozygous PINK1 p.G411S increases risk of Parkinson’s disease via a dominant-negative mechanism
Puschmann, A., Fiesel, F. C., Caulfield, T. R., Hudec, R., Ando, M., Fričová, D., Hou, X., Ogaki, K., Heckman, M. G., James, E. D., et al. (2016) · Brain · doi:10.1093/brain/aww261 · Cited by 137 · see citing works
Self-citationFunk, K. E., Mrak, R. E., & Kuret, J. (2010) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2010.01135.x · Cited by 123 · see citing works
Feany, M. Β., & Pallanck, L. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00201-0 · Cited by 115 · see citing works
How to get rid of mitochondria: crosstalk and regulation of multiple mitophagy pathways
Zimmermann, M., & Reichert, A. S. (2017) · Biological Chemistry · doi:10.1515/hsz-2017-0206 · Cited by 102 · see citing works
PINK1/Parkin-Dependent Mitochondrial Surveillance: From Pleiotropy to Parkinson's Disease
Mouton‐Liger, F., Jacoupy, M., Corvol, J., & Corti, O. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00120 · Cited by 97 · see citing works
Brooks, J. A., Ding, J., Simón‐Sánchez, J., Paisán‐Ruiz, C., Singleton, A., & Scholz, S. W. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2008.063917 · Cited by 87 · see citing works
Granulovacuolar degeneration: a neurodegenerative change that accompanies tau pathology
Köhler, C. N. (2016) · Acta Neuropathologica · doi:10.1007/s00401-016-1562-0 · Cited by 87 · see citing works
Parkin Plays a Role in Sporadic Parkinson's Disease
Dawson, T. M., & Dawson, V. L. (2013) · Neurodegenerative Diseases · doi:10.1159/000354307 · Cited by 82 · see citing works
Dickson, D. W., Ksiȩżak-Reding, H., Davies, P., & Yen, S. H. (1987) · Acta Neuropathologica · doi:10.1007/bf00686619 · Cited by 79 · see citing works
Self-citationSelect E2 enzymes differentially regulate parkin activation and mitophagy
Fiesel, F. C., Moussaud-Lamodière, E. L., Ando, M., & Springer, W. (2014) · Journal of Cell Science · doi:10.1242/jcs.147520 · Cited by 72 · see citing works
Self-citationFiesel, F. C., James, E. D., Hudec, R., & Springer, W. (2017) · Oncotarget · doi:10.18632/oncotarget.22287 · Cited by 67 · see citing works
Self-citationEvidence that phosphorylated ubiquitin signaling is involved in the etiology of Parkinson’s disease
Shiba‐Fukushima, K., Ishikawa, K., Inoshita, T., Izawa, N., Takanashi, M., Sato, S., Onodera, O., Akamatsu, W., Okano, H., Imai, Y., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx201 · Cited by 62 · see citing works
Dickson, D. W., Liu, W.-K., Kress, Y., Ku, J., DeJesus, O. T., & Yen, S.-H. C. (1993) · Acta Neuropathologica · doi:10.1007/bf00230483 · Cited by 32 · see citing works
Self-citationDisease relevance of phosphorylated ubiquitin (p-S65-Ub)
Fiesel, F. C., & Springer, W. (2015) · Autophagy · doi:10.1080/15548627.2015.1091912 · Cited by 28 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 4
- [54]Feany MB, Pallanck LJ Parkin: a multipurpose neuroprotective agent? Neuron. 2003; 38(1): 13– 16. 12691660
- [56]Xilouri M, Brekk OR, Stefanis L Autophagy and alpha-synuclein: relevance to Parkinson’s disease and related synucleopathies. Mov Disord. 2016; 31(2): 178– 192. 26813776
- [63]Fiesel FC, Moussaud-Lamodiere EL, Ando M, et al A specific subset of E2 ubiquitin-conjugating enzymes regulate Parkin activation and mitophagy differently. J Cell Sci. 2014; 127(Pt 16): 3488– 3504. 24928900 PMC4132391
- [64]van Elteren PH On the combination of independent two sample tests of Wilcoxon. Bull Inst Int Stat. 1960; 37: 351– 361.
Cited by
Sorted by citations
The neuropathological diagnosis of Alzheimer's disease
DeTure, M. A., & Dickson, D. W. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0333-5 · Cited by 3,329 · see citing works
“Most recently, phospho-ubiquitin mitophagy markers label granulovacuolar bodies and their abundance has been shown to correlate with neurofibrillary tangle density, suggesting they may be a cellular response to damage in the neurons [80].”
BackgroundSelf-citationPINK1/PARKIN signalling in neurodegeneration and neuroinflammation
Quinn, P. M. J., Moreira, P. I., Ambrósio, A. F., & Alves, C. H. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01062-w · Cited by 486 · see citing works
Mitochondrial dysfunction and mitophagy in parkinson’s disease: from mechanism to therapy
Malpartida, A. B., Williamson, M., Narendra, D. P., Wade-Martins, R., & Ryan, B. J. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.11.007 · Cited by 482 · see citing works
PINK1/Parkin-mediated mitophagy in neurodegenerative diseases
Li, J., Yang, D., Li, Z., Zhao, M., Wang, D., Sun, Z., Wen, P., Dai, Y., Gou, F., Ji, Y., et al. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101817 · Cited by 388 · see citing works
Mitophagy curtails cytosolic mtDNA-dependent activation of cGAS/STING inflammation during aging
Jiménez‐Loygorri, J. I., Villarejo‐Zori, B., Viedma-Poyatos, Á., Zapata‐Muñoz, J., Benítez‐Fernández, R., Frutos-Lisón, M. D., Tomás-Barberán, F. A., Espı́n, J. C., Área-Gómez, E., Gómez-Durán, A., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45044-1 · Cited by 381 · see citing works
Autophagy in Parkinson's Disease
Hou, X., Watzlawik, J. O., Fiesel, F. C., & Springer, W. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.01.037 · Cited by 355 · see citing works
Self-citationMoloney, C. M., Lowe, V. J., & Murray, M. E. (2021) · Alzheimer s & Dementia · doi:10.1002/alz.12321 · Cited by 337 · see citing works
Self-citationAutophagy, aging, and age-related neurodegeneration
Palmer, J. E., Wilson, N., Son, S. M., Obrocki, P., Wróbel, L., Rob, M., Takla, M., Korolchuk, V. I., & Rubinsztein, D. C. (2024) · Neuron · doi:10.1016/j.neuron.2024.09.015 · Cited by 255 · see citing works
Mitophagy in Parkinson’s Disease: From Pathogenesis to Treatment
Liu, J., Liu, W., Li, R., & Yang, H. (2019) · Cells · doi:10.3390/cells8070712 · Cited by 224 · see citing works
The RING finger protein family in health and disease
Cai, C., Tang, Y., Zhai, J., & Zheng, C. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01152-2 · Cited by 194 · see citing works
Picca, A., Guerra, F., Calvani, R., Romano, R., Coelho-Júnior, H. J., Bucci, C., & Marzetti, E. (2021) · Biomolecules · doi:10.3390/biom11101508 · Cited by 189 · see citing works
Autophagic and endo-lysosomal dysfunction in neurodegenerative disease
Malik, B. R., Maddison, D. C., Smith, G. A., & Peters, O. M. (2019) · Molecular Brain · doi:10.1186/s13041-019-0504-x · Cited by 180 · see citing works
Targeting autophagy, oxidative stress, and ER stress for neurodegenerative disease treatment
Esmaeili, Y., Yarjanli, Z., Paknia, F., Bidram, E., Łoś, M., Eshraghi, M., Klionsky, D. J., Ghavami, S., & Zarrabi, A. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.03.001 · Cited by 180 · see citing works
Targeting mitophagy in neurodegenerative diseases
Antico, O., Thompson, P. W., Hertz, N. T., Muqit, M. M. K., & Parton, L. E. (2025) · Nature Reviews Drug Discovery · doi:10.1038/s41573-024-01105-0 · Cited by 178 · see citing works
Recent update on the heterogeneity of the Alzheimer’s disease spectrum
Jellinger, K. A. (2021) · Journal of Neural Transmission · doi:10.1007/s00702-021-02449-2 · Cited by 150 · see citing works
Mitochondrial Dysfunction in Parkinson’s Disease: From Mechanistic Insights to Therapy
Gao, X., Yang, T., Gu, Y., & Sun, X.-H. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.885500 · Cited by 142 · see citing works
Targeting mitophagy in Parkinson's disease
Clark, E. H., de la Torre, A. V., Hoshikawa, T., & Briston, T. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.014294 · Cited by 128 · see citing works
Mechanisms of PINK1, ubiquitin and Parkin interactions in mitochondrial quality control and beyond
Bayne, A. N., & Trempe, J. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03203-4 · Cited by 113 · see citing works
Agarwal, S., & Muqit, M. M. K. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.09.005 · Cited by 103 · see citing works
Ren, H., Zhai, W., Lu, X., & Wang, G. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.691881 · Cited by 101 · see citing works
Autophagy in Parkinson’s Disease
Nechushtai, L., Frenkel, D., & Pinkas‐Kramarski, R. (2023) · Biomolecules · doi:10.3390/biom13101435 · Cited by 107 · see citing works
Mitochondrial dysfunction in chronic neuroinflammatory diseases (Review)
Qin, P., Sun, Y., & Li, L. (2024) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2024.5371 · Cited by 104 · see citing works
Neuropathological assessment of the Alzheimer spectrum
Jellinger, K. A. (2020) · Journal of Neural Transmission · doi:10.1007/s00702-020-02232-9 · Cited by 82 · see citing works
Hou, X., Watzlawik, J. O., Cook, C. N., Liu, C., Kang, S. S., Lin, W., Deture, M. A., Heckman, M. G., Diehl, N. N., Al‐Shaikh, F. S. H., et al. (2020) · Alzheimer s & Dementia · doi:10.1002/alz.12198 · Cited by 72 · see citing works
Self-citationLópez‐Doménech, G., Howden, J. H., Covill‐Cooke, C., Morfill, C., Patel, J. V., Bürli, R. W., Crowther, D. C., Birsa, N., Brandon, N. J., & Kittler, J. T. (2021) · The EMBO Journal · doi:10.15252/embj.2018100715 · Cited by 80 · see citing works
Swerdlow, N., & Wilkins, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249661 · Cited by 65 · see citing works
Jing, R., Hu, Z., Lin, F., he, S. T., Zhang, S., Ge, W., Dai, H., Du, X., Lin, J., & Pan, L. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00819 · Cited by 64 · see citing works
Guha, S. K., Fischer, S., Johnson, G. V. W., & Nehrke, K. W. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00410-7 · Cited by 60 · see citing works
Cheng, H., Gang, X., Liu, Y., Wang, G., Zhao, X., & Wang, G. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00179.2019 · Cited by 62 · see citing works
Soutar, M. P. M., Melandri, D., O’Callaghan, B., Annuario, E., Monaghan, A. E., Welsh, N. J., D’Sa, K., Guelfi, S., Zhang, D., Pittman, A. M., et al. (2022) · Brain · doi:10.1093/brain/awac325 · Cited by 62 · see citing works
Watzlawik, J. O., Hou, X., Fričová, D., Ramnarine, C., Barodia, S. K., Gendron, T. F., Heckman, M. G., Deture, M. A., Siuda, J. S., Wszołek, Z. K., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1834712 · Cited by 56 · see citing works
Self-citationStructural Mechanisms of Mitochondrial Quality Control Mediated by PINK1 and Parkin
Trempe, J., & Gehring, K. (2023) · Journal of Molecular Biology · doi:10.1016/j.jmb.2023.168090 · Cited by 58 · see citing works
Parkinson’s disease neurons exhibit alterations in mitochondrial quality control proteins
Chen, C., McDonald, D., Blain, A., Mossman, E., Atkin, K., Marusich, M., Capaldi, R., Bone, L., Smith, A., Filby, A., et al. (2023) · npj Parkinson's Disease · doi:10.1038/s41531-023-00564-3 · Cited by 54 · see citing works
How should we be using biomarkers in trials of disease modification in Parkinson’s disease?
Vijiaratnam, N., & Foltynie, T. (2023) · Brain · doi:10.1093/brain/awad265 · Cited by 56 · see citing works
Relevance of Autophagy and Mitophagy Dynamics and Markers in Neurodegenerative Diseases
Giorgi, C., Bouhamida, E., Danese, A., Previati, M., Pinton, P., & Patergnani, S. (2021) · Biomedicines · doi:10.3390/biomedicines9020149 · Cited by 50 · see citing works
Early-Onset Parkinson’s Disease: Creating the Right Environment for a Genetic Disorder
Kolicheski, A., Turcano, P., Tamvaka, N., McLean, P. J., Springer, W., Savica, R., & Ross, O. A. (2022) · Journal of Parkinson s Disease · doi:10.3233/jpd-223380 · Cited by 51 · see citing works
Self-citationCompromised autophagy and mitophagy in brain ageing and Alzheimer’s diseases.
Caponio, D., Veverová, K., Zhang, S.-Q., Shi, L., Wong, G., Vyhnalek, M., & Fang, E. F. (2022) · Aging Brain · doi:10.1016/j.nbas.2022.100056 · Cited by 45 · see citing works
The Long and the Short of PTEN in the Regulation of Mitophagy
Wang, L., Lu, G. X., & Shen, H. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00299 · Cited by 45 · see citing works
Neuropathology of the Alzheimer's continuum: an update
Jellinger, K. A. (2020) · Free Neuropathology · doi:10.17879/freeneuropathology-2020-3050 · Cited by 45 · see citing works
Alpha‐synuclein‐associated changes in PINK1‐PRKN‐mediated mitophagy are disease context dependent
Hou, X., Chen, T. H., Koga, S., Bredenberg, J. M., Faroqi, A. H., Delenclos, M., Bu, G., Wszołek, Z. K., Carr, J. A., Ross, O. A., et al. (2023) · Brain Pathology · doi:10.1111/bpa.13175 · Cited by 42 · see citing works
Self-citationMitophagy and Neurodegeneration: Between the Knowns and the Unknowns
Jetto, C. T., Nambiar, A., & Manjithaya, R. R. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.837337 · Cited by 44 · see citing works
Pharmacological PINK1 activation ameliorates Pathology in Parkinson’s Disease modelsPreprint
Chin, R., Rakhit, R., Ditsworth, D., Wang, C., Bartholoméüs, J., Liu, S., Mody, A., Laishu, A., Eastes, A., Tai, C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.14.528378 · Cited by 41 · see citing works
Discovery of small-molecule positive allosteric modulators of Parkin E3 ligase
Shlevkov, E., Murugan, P., Montagna, D., Stefan, E., Hadzipasic, A., Harvey, J. S., Kumar, P. R., Entova, S., Bansal, N., Bickford, S., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103650 · Cited by 40 · see citing works
Multimodal assessment of mitochondrial function in Parkinson's disease
Payne, T., Burgess, T., Bradley, S., Roscoe, S., Sassani, M., Dunning, M., Hernandez, D. G., Scholz, S. W., McNeill, A., Taylor, R. N., et al. (2023) · Brain · doi:10.1093/brain/awad364 · Cited by 39 · see citing works
Ma, Y., Song, R., & Duan, C. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1542369 · Cited by 37 · see citing works
PINK1-Dependent Mitophagy Inhibits Elevated Ubiquitin Phosphorylation Caused by Mitochondrial Damage
Lambourne, O. A., Bell, S., Wilhelm, L. P., Yarbrough, E. B., Holly, G., Russell, O., Alghamdi, A. M., Fdel, A. M., Varricchio, C., Lane, E., et al. (2023) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.3c00555 · Cited by 28 · see citing works
Rosencrans, W. M., Lee, R. W., McGraw, L., Horsburgh, I., Wang, T., Quan, B., Huynh, D., Johnston, J. A., Chan, D. C., & Chou, T. (2025) · Science Advances · doi:10.1126/sciadv.ady0240 · Cited by 39 · see citing works
N-degron-mediated degradation and regulation of mitochondrial PINK1 kinase
Eldeeb, M. A., & Ragheb, M. A. (2020) · Current Genetics · doi:10.1007/s00294-020-01062-2 · Cited by 36 · see citing works
Structure-based design and characterization of Parkin-activating mutations
Stevens, M., Croteau, N., Eldeeb, M. A., Antico, O., Zeng, Z. W., Toth, R. L., Durcan, T. M., Springer, W., Fon, E. A., Muqit, M. M. K., et al. (2023) · Life Science Alliance · doi:10.26508/lsa.202201419 · Cited by 32 · see citing works
Self-citationBasal activity of PINK1 and PRKN in cell models and rodent brain
Watzlawik, J., Fiesel, F. C., Fiorino, G., Bustillos, B. A., Baninameh, Z., Markham, B. N., Hou, X., Hayes, C. S., Bredenberg, J. M., Kurchaba, N. W., et al. (2023) · Autophagy · doi:10.1080/15548627.2023.2286414 · Cited by 28 · see citing works
Self-citationPitcairn, C., Murata, N., Zalon, A. J., Stojkovska, I., & Mazzulli, J. R. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0610-22.2023 · Cited by 29 · see citing works
Methamphetamine-induced dopaminergic neurotoxicity as a model of Parkinson’s disease
Shin, E., Jeong, J. H., Hwang, Y., Sharma, N., Dang, D., Nguyen, B.-T., Nah, S.-Y., Jang, C., Bing, G., Nabeshima, T., et al. (2021) · Archives of Pharmacal Research · doi:10.1007/s12272-021-01341-7 · Cited by 31 · see citing works
Jiao, F., Meng, L., Du, K., & Li, X. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01195 · Cited by 28 · see citing works
Wiersma, V. I., Hoozemans, J. J. M., & Scheper, W. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-00996-5 · Cited by 26 · see citing works
Dysregulation of Human Somatic piRNA Expression in Parkinson’s Disease Subtypes and Stages
Zhang, T., & Wong, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052469 · Cited by 29 · see citing works
Defects of Nutrient Signaling and Autophagy in Neurodegeneration
Ondaro, J., Hernández-Eguiazu, H., Garciandia-Arcelus, M., Loera‐Valencia, R., Rodríguez-Gómez, L., Jiménez-Zúñiga, A., Goikolea, J., Rodriguez‐Rodriguez, P., Ruiz‐Martínez, J., Moreno, F., et al. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.836196 · Cited by 27 · see citing works
Role of GBA variants in Lewy body disease neuropathology
Walton, R. L., Koga, S., Beasley, A., White, L. J., Griesacker, T., Murray, M., Kasanuki, K., Hou, X., Fiesel, F. C., Springer, W., et al. (2024) · Acta Neuropathologica · doi:10.1007/s00401-024-02699-w · Cited by 23 · see citing works
Self-citationPadmanabhan, S., Polinski, N. K., Menalled, L., Baptista, M. A. S., & Fiske, B. K. (2019) · Biomolecules · doi:10.3390/biom9080296 · Cited by 25 · see citing works
Pharmacological PINK1 activation ameliorates Pathology in Parkinson’s Disease modelsPreprint
Hertz, N. T., Chin, R., Rakhit, R., Ditsworth, D., Wang, C., Bartholoméüs, J., Liu, S., Mody, A., Laihsu, A., Eastes, A., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-4356493/v1 · Cited by 23 · see citing works
Mitophagy in the aging nervous system
Rappe, A., & McWilliams, T. G. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.978142 · Cited by 22 · see citing works
Lu, J., Florio, D. N. D., Boya, P., Maday, S., Springer, W., & Chu, C. T. (2025) · Autophagy · doi:10.1080/15548627.2025.2581217 · Cited by 21 · see citing works
Self-citationInterplay of Impaired Cellular Bioenergetics and Autophagy in PMM2-CDG
Ligezka, A., Budhraja, R., Nishiyama, Y., Fiesel, F. C., Preston, G., Edmondson, A., Ranatunga, W. K., Hove, J. V. V., Watzlawik, J., Springer, W., et al. (2023) · Genes · doi:10.3390/genes14081585 · Cited by 20 · see citing works
Self-citationAutophagy‑regulating miRNAs: Novel therapeutic targets for Parkinson's disease (Review)
Ma, Z., Liang, H., Hu, B., Cai, S., & Dong, Y. (2023) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2023.5253 · Cited by 19 · see citing works
Insights into the molecular mechanisms of malnutrition‐associated steatohepatitis: A review
Sharma, V., & Patial, V. (2024) · Liver International · doi:10.1111/liv.15932 · Cited by 20 · see citing works
Parkin drives pS65‐Ub turnover independently of canonical autophagy in Drosophila
Usher, J. L., Sánchez-Martínez, Á., Terriente-Félix, A., Chen, P., Lee, J. J., Chen, C., & Whitworth, A. J. (2022) · EMBO Reports · doi:10.15252/embr.202153552 · Cited by 17 · see citing works
Zhou, B., Li, J., Wu, A., Wang, X., Cheng, L., Yang, G., Gao, D., & Zhu, C. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1587986 · Cited by 17 · see citing works
NLRP3 Inflammasome Activation and Altered Mitophagy Are Key Pathways in Inclusion Body Myositis
Naddaf, E., Nguyen, T. K. O., Watzlawik, J. O., Gao, H., Hou, X., Fiesel, F. C., Mandrekar, J. N., Kokesh, E., Harmsen, W. S., Lanza, I. R., et al. (2024) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13672 · Cited by 17 · see citing works
Self-citationManaging risky assets – mitophagy in vivo
Narendra, D. P. (2021) · Journal of Cell Science · doi:10.1242/jcs.240465 · Cited by 16 · see citing works
The Ubiquitin Proteasome System as a Therapeutic Area in Parkinson’s Disease
Kumar, S., Mattern, M. R., Goldberg, M. S., & Butt, T. R. (2023) · NeuroMolecular Medicine · doi:10.1007/s12017-023-08738-1 · Cited by 16 · see citing works
Possible role of locus coeruleus neuronal loss in age-related memory and attention deficits
Gargano, A., Olabiyi, B. F., Palmisano, M., Zimmer, A., & Bilkei‐Gorzó, A. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1264253 · Cited by 14 · see citing works
Tang, C., & Zhang, W.-P. (2020) · Biochemistry · doi:10.1021/acs.biochem.9b00715 · Cited by 9 · see citing works
Canonical and noncanonical autophagy: involvement in Parkinson’s disease
Sakurai, M., & Kuwahara, T. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1518991 · Cited by 16 · see citing works
Tufi, R., Clark, E. H., Hoshikawa, T., Tsagkaraki, C., Stanley, J., Takeda, K., Staddon, J. M., & Briston, T. (2023) · SLAS DISCOVERY · doi:10.1016/j.slasd.2022.12.004 · Cited by 15 · see citing works
Stress-induced phospho-ubiquitin formation causes parkin degradation
Kovalchuke, L., Mosharov, E. V., Levy, O. A., & Greene, L. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-47952-5 · Cited by 15 · see citing works
Li, A., Huang, S., Cao, S., Lin, J., Zhao, L., Yu, F., Huang, M., Yang, L., Xin, J., Wen, J., et al. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-025-00323-2 · Cited by 14 · see citing works
Watzlawik, J. O., Hou, X., Richardson, T., Lewicki, S. L., Siuda, J. S., Wszołek, Z. K., Cook, C. N., Petrucelli, L., Deture, M. A., Dickson, D. W., et al. (2024) · Autophagy · doi:10.1080/15548627.2024.2356490 · Cited by 14 · see citing works
Self-citationJeong, D., Park, S. H., Kim, J., Kim, H., Jang, Y., Koh, J., Jeon, Y. K., Tasaki, T., Kwon, Y. T., Han, D., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2425015122 · Cited by 12 · see citing works
Alterations of PINK1-PRKN signaling in mice during normal aging
Baninameh, Z., Watzlawik, J. O., Hou, X., Richardson, T., Kurchaba, N. W., Yan, T., Florio, D. N. D., Fairweather, D., Kang, L., Nguyen, J. H., et al. (2024) · Autophagy Reports · doi:10.1080/27694127.2024.2434379 · Cited by 12 · see citing works
Self-citationInhibition of mTOR improves malnutrition induced hepatic metabolic dysfunction
Kvissberg, M. E. A., Hu, G., Chi, L., Bourdon, C., Ling, C., ChenMi, Y., Germain, K., van de Peppel, I. P., Weise, L., Zhang, L., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-24428-7 · Cited by 13 · see citing works
Ming, F., Tan, J., Qin, L., Zhang, H., Tang, J., Tan, X., & Wang, C. (2020) · BioMed Research International · doi:10.1155/2020/4658109 · Cited by 12 · see citing works
Ahmed, S., Pasam, T., & Afreen, F. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27010486 · Cited by 11 · see citing works
Buck, S. A., Malankhanova, T. B., Strader, S., Eileen, B., Yim, S., Pratt, H. W., Ervin, J. F., Lee, E. B., Wang, S. J., Cohen, T. J., et al. (2025) · Acta Neuropathologica · doi:10.1007/s00401-025-02951-x · Cited by 11 · see citing works
Miro ubiquitination is critical for efficient damage-induced PINK1/Parkin-mediated mitophagyPreprint
López‐Doménech, G., Covill‐Cooke, C., Howden, J. H., Birsa, N., Morfill, C., Brandon, N. J., & Kittler, J. T. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/414664 · Cited by 11 · see citing works
Parkinson’s Disease: Are PINK1 Activators Inching Closer to the Clinic?
Mehellou, Y. (2023) · ACS Medicinal Chemistry Letters · doi:10.1021/acsmedchemlett.3c00070 · Cited by 9 · see citing works
Granulovacuolar degeneration bodies are independently induced by tau and α-synuclein pathology
Jorge‐Oliva, M., Smits, J. F. M., Wiersma, V. I., Hoozemans, J. J. M., & Scheper, W. (2022) · Alzheimer s Research & Therapy · doi:10.1186/s13195-022-01128-y · Cited by 10 · see citing works
Gargano, A., Beins, E. C., Zimmer, A., & Bilkei‐Gorzó, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010005 · Cited by 10 · see citing works
Development and validation of a sensitive sandwich ELISA against human PINK1
Baninameh, Z., Watzlawik, J., Bustillos, B. A., Fiorino, G., Yan, T.-X., Lewicki, S. L., Zhang, H., Dickson, D. W., Siuda, J., Wszolek, Z., et al. (2025) · Autophagy · doi:10.1080/15548627.2025.2457915 · Cited by 7 · see citing works
Self-citationProteome Dynamics in iPSC-Derived Human Dopaminergic Neurons
Cavarischia-Rega, C., Sharma, K., Fitzgerald, J. C., & Maček, B. (2024) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2024.100838 · Cited by 8 · see citing works
Genome‐wide association analysis identifies APOE as a mitophagy modifier in Lewy body disease
Hou, X., Heckman, M. G., Fiesel, F. C., Koga, S., Soto‐Beasley, A. I., Watzlawik, J. O., Zhao, J., Valentino, R. R., Johnson, P. W., White, L. J., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70198 · Cited by 9 · see citing works
Self-citationAdvances in autophagy for Parkinson’s disease pathogenesis and treatment
Zhang, X., Zhang, H., Dong, J., Cai, H., & Le, W. (2025) · Ageing and Neurodegenerative Diseases · doi:10.20517/and.2024.33 · Cited by 9 · see citing works
Mitochondrial quality control in human ageing and longevity
Picca, A., & Ferrucci, L. (2026) · Nature Metabolism · doi:10.1038/s42255-026-01563-3 · Cited by 9 · see citing works
Monogenetic Forms of Parkinson’s Disease – Bridging the Gap Between Genetics and Biomarkers
Tönges, L., Kwon, E. H., & Klebe, S. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.822949 · Cited by 8 · see citing works
miRNA family miR-29 inhibits PINK1-PRKN dependent mitophagy via ATG9APreprint
Markham, B. N., Ramnarine, C., Kim, S., Grever, W. E., Soto‐Beasley, A. I., Heckman, M. G., Ren, Y., Osborne, A. C., Bhagwate, A. V., Liu, Y., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.17.576122 · Cited by 7 · see citing works
Self-citationRosado, A. M., Vizcarra, J. C., Sharma, S. R. R., Keene, C. D., White, C. L., Kim, A., Forrest, S. L., Kovács, G. G., Chuah, C., Flanagan, M. E., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70775 · Cited by 7 · see citing works
Fiesel, F. C., Bustillos, B. A., Watzlawik, J. O., Chen, C., Berryer, M. H., Zhang, J., Boneski, P. K., Hayes, C. S., Bredenberg, J. M., Deneault, É., et al. (2025) · Autophagy · doi:10.1080/15548627.2025.2531025 · Cited by 6 · see citing works
Self-citationHippocampal mitophagy alterations in MAPT-associated frontotemporal dementia with parkinsonism
Richardson, T., Hou, X., Fiesel, F. C., Wszolek, Z., Dickson, D. W., & Springer, W. (2025) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-01955-8 · Cited by 5 · see citing works
Self-citationQin, L., Gong, Z., Liu, K., Dong, X., & Tang, C. (2021) · Biomolecules · doi:10.3390/biom11071008 · Cited by 5 · see citing works
Hou, X., Heckman, M. G., Fiesel, F. C., Koga, S., Soto‐Beasley, A. I., Watzlawik, J. O., Zhao, J., Valentino, R. R., Johnson, P. W., White, L. J., et al. (2023) · medRxiv · doi:10.1101/2023.10.16.23297100 · Cited by 6 · see citing works
Self-citationChen, C., Gao, T.-Y., Yi, H., Zhang, Y., Wang, T., Lou, Z., Wei, T.-F., Lu, Y.-B., Li, T., Tang, C., et al. (2025) · bioRxiv · doi:10.7554/elife.103945 · Cited by 7 · see citing works
Gut Microbiota and Aging: Targets and Anti-aging Interventions
Singh, B., Catanzaro, R., Mal, G., Gautam, S., Mohania, He, F., Yadav, H., Bissi, L., & Marotta, F. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.62181-5 · Cited by 4 · see citing works
- Authors
- Hou, X., Fiesel, F. C., Truban, D., Castanedes Casey, M., Lin, W.-L., Soto, A. I., Tacik, P., Rousseau, L. G., Diehl, N. N., Heckman, M. G., Lorenzo-Betancor, O., Ferrer, I., Arbelo, J. M., Steele, J. C., Farrer, M. J., Cornejo-Olivas, M., Torres, L., Mata, I. F., Graff-Radford, N. R., Wszolek, Z. K., Ross, O. A., Murray, M. E., Dickson, D. W., & Springer, W.
- Affiliations
- Mayo Clinic in Florida (US)
- Mayo Clinic (US)
- Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA
- Institut de Neuropatologia, Servei d’Anatomia Patològica, Hospital Universitari de Bellvitge, Hospitalet del Llobregat, Barcelona, Spain
- Hospital Universitario Insular de Gran Canaria (ES)
- Micronesian Health Study II, Tamuning, Guam
- University of British Columbia (CA)
- Northern Pacific Global Health Research Fellows Training Consortium, Bethesda, MD, USA
- Instituto Nacional de Ciencias Neurológicas (PE)
- University of Washington (US)
- Department of Neurology, Mayo Clinic, Jacksonville, FL, USA
- Corresponding author
- Springer, Wolfdieter
- ORCID
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2018-07-28
- Volume
- 14
- Issue
- 8
- Pages
- 1404-1418
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC6372017
- OpenAlex
- W2810603360
- Cited by
- 147
- References
- 65
- Citations by year
- 2026: 18 · 2025: 28 · 2024: 16 · 2023: 19 · 2022: 17 · 2021: 13 · 2020: 25 · 2019: 10 · 2018: 1
- FWCI
- 8.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Autophagy (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (acceptedVersion)
- Acceda (Universidad de Las Palmas de Gran Canaria) (submittedVersion)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, public-domain)
- Funders
- HHS | NIH | National Institute of Neurological Disorders and Stroke (R01 NS085070, U54 NS100693, R01 NS078086, P50 NS072187)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- mitophagy, Parkinson's disease, Lewy body disease, normal aging, mitochondrial quality control, PINK1, Parkin, ubiquitin phosphorylation, lysosomes, neurofibrillary tangles, biomarkers, dopaminergic neurons, mitochondrial dysfunction
- MeSH terms
- Aged, Aged, 80 and over, Aging, Brain, Female, HeLa Cells, Humans, Male, Middle Aged, Mutation, Phosphorylation, Phosphoserine, Protein Binding, Cohort Studies, Biomarkers, tau Proteins, Lewy Body Disease, Ubiquitin, alpha-Synuclein, Mitophagy
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
