Title
Age- and disease-dependent increase of the mitophagy marker phospho-ubiquitin in normal aging and Lewy body disease
Date Issued
03 August 2018
Access level
open access
Resource Type
journal article
Author(s)
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.
Mata I.F.
Graff-Radford N.R.
Wszolek Z.K.
Ross O.A.
Murray M.E.
Dickson D.W.
Springer W.
Publisher(s)
Taylor and Francis Inc.
Abstract
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.
Start page
1404
End page
1418
Volume
14
Issue
8
Language
English
OCDE Knowledge area
Geriatría, Gerontología Neurología clínica Neurociencias
Scopus EID
2-s2.0-85050984771
PubMed ID
Source
Autophagy
ISSN of the container
15548627
Sponsor(s)
This work was supported by multiple funding resources. W.S. is partially supported by the National Institutes of Health (NIH)/National Institute of Neurological Disorders and Stroke (NINDS) [R01 NS085070], the Michael J. Fox Foundation for Parkinson Research and the Foundation for Mitochondrial Medicine, Mayo Clinic Neuroscience Focused Research Team (NFRT) Award, Mayo Clinic Center for Individualized Medicine (CIM), Center for Regenerative Medicine (CRM) and the Center for Biomedical Discovery (CBD), the Marriott Family Foundation, and a Gerstner Family Foundation Career Development Award. Mayo Clinic Florida is a Morris K. Udall Parkinson Disease Research Center of Excellence [NIH/NINDS P50 NS072187 to Z.K.W., O.A.R. and D.W.D.]. X. H. is supported by a pilot grant from the Mayo Clinic Alzheimer Disease Research Center (ADRC) and a fellowship awarded by the American Parkinson Disease Association (APDA). F.C.F. is the recipient of a fellowship from the Younkin Scholar Program and has received support by the APDA. P.T. is supported by an Allergan Medical Educational Grant, a Jaye F. and Betty F. Dyer Foundation Fellowship in progressive supranuclear palsy research, and a Max Kade Foundation postdoctoral fellowship. O.A.R. is supported by NIH/NINDS [R01 NS078086]. Z.K.W. and O.A.R are supported by the Mayo Clinic Center for Individualized Medicine (CIM) and by the Mayo Clinic Center for Regenerative Medicine (CRM). D.W.D. is supported by the Mangurian Foundation for Lewy body research. O.A.R. and D.W.D. are supported by NIH/NINDS [U54 NS100693]. We thank the patients and their families who made this study possible. We thank Anneliese Hill for assistance with antibody testing. This work was supported by multiple funding resources. W.S. is partially supported by the National Institutes of Health (NIH)/National Institute of Neurological Disorders and Stroke (NINDS) [R01 NS085070], the Michael J. Fox Foundation for Parkinson Research and the Foundation for Mitochondrial Medicine, Mayo Clinic Neuroscience Focused Research Team (NFRT) Award, Mayo Clinic Center for Individualized Medicine (CIM), Center for Regenerative Medicine (CRM) and the Center for Biomedical Discovery (CBD), the Marriott Family Foundation, and a Gerstner Family Foundation Career Development Award. Mayo Clinic Florida is a Morris K. Udall Parkinson Disease Research Center of Excellence [NIH/NINDS P50 NS072187 to Z.K.W., O.A.R. and D.W.D.]. X. H. is supported by a pilot grant from the Mayo Clinic Alzheimer Disease Research Center (ADRC) and a fellowship awarded by the American Parkinson Disease Association (APDA). F.C. F. is the recipient of a fellowship from the Younkin Scholar Program and has received support by the APDA. P.T. is supported by an Allergan Medical Educational Grant, a Jaye F. and Betty F. Dyer Foundation Fellowship in progressive supranuclear palsy research, and a Max Kade Foundation postdoctoral fellowship. O.A.R. is supported by NIH/NINDS [R01 NS078086]. Z.K.W. and O.A.R are supported by the Mayo Clinic Center for Individualized Medicine (CIM) and by the Mayo Clinic Center for Regenerative Medicine (CRM). D.W.D. is supported by the Mangurian Foundation for Lewy body research. O.A.R. and D.W.D. are supported by NIH/NINDS [U54 NS100693].
Sources of information: Directorio de Producción Científica Scopus