Genotypic and phenotypic overlaps in Parkinson s disease and parkinsonisms

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1 Genotypic and phenotypic overlaps in Parkinson s disease and parkinsonisms Enza Maria Valente CSS-Mendel Institute, Rome University of Salerno

2 The «shaking palsy»: clinica features Involuntary tremulous motion, with lessened muscular power, with a propensity to bend the trunk forward, and to pass from a walking to a running pace: the senses and intellects being uninjured.» Motor signs resting tremor bradykinesia rigidity postural instability Non motor signs Cognitive impairment, dementia Psychiatric disturbances Autonomic dysfunctions «Plus» signs Dementia Dystonia Spasticity 2

3 A continuum from multifactorial to mendelian PD polymorphisms (++ in autosomal dominant PD genes: RR mutations in autosomal dominant PD genes: reduced penetrance (30%): RR late pure onset PD complicated PD (dementia, early onset dystonia, psychiatric etc) Heterozygous mutations in autosomal recessive PD genes: RR heterozygous mutations in other recessive genes: RR 4-6 mutations in autosomal recessive PD genes: full penetrance: 100% 3

4 Talk outline genotypic and phenotypic overlaps: the concept of «splitting and lumping» examples: autosomal recessive early onset parkinsonism PD-dementia and LBD conclusions and perspectives

5 «Splitting and lumping» in genetics LUMPING SPLITTING distinct phenotypes same gene same phenotype distinct genes

6 Autosomal recessive «pure» parkinsonisms Distinct genes, same phenotype early onset (<40 years) DJ1 < Parkin < PINK1 slow progression excellent and sustained response to treatment Variable phenotypic features, same gene dystonia at onset sleep benefit, diurnal fluctuations hyperreflexia Parkin >>> PINK1 > DJ-1 50% fam 10-15% spor 1-8% in different populations < 1% treatment-related complications (dyskinesias, behavioral problems)

7 PDD vs DLB: a single entity? average prevalence of dementia in PD: >30% (increasing with age) PD patients have a 6-fold higher risk to develop dementia than non PD dementia onset PD onset 1year Lewy Body Dementia Parkinson s disease Dementia - parkinsonian syndrome - dementia (++ impaired memory, executive and visuospatial functions) - behavioral symptoms (++ visual hallucinations, delusions, agitation) - REM sleep behavior disorder, dysautonomia - fluctuations of symptoms 7

8 the Contursi family and the discovery of α-synuclein Polimeropoulos et al, Science 1996 and

9 α-synuclein mutations and PD Five mutations reported after screening of thousands PD cases SNCA mutations p.a53t p.a30p p.e46k p.h50q p.g51d onset 40s 60s 60s 60s 40s parkinsonism ++, rapid progr , rapid progr. cognitive impairment psychiatric involvement autonomic disturbance /+ L-Dopa response /- pyramidal signs I:1 I:2 onset 27aa SNCA A53T mutation II:1 Onset 50 aa II:2 II:3 II:4 45aa 45aa 67aa onset III:1 III:2 III:3 III:4 III:5 III:6 III:7 III:14 III:15 50 aa 58 aa 57aa onset onset III:8-10 III: aa 26 aa IV:1 IV:2 IV:3 IV:4-5 IV:6 IV:7 IV:8 IV:9 IV:10 II:5 Psychiatric disease PD PD and psychiatric + SNCA mutation A53T SNCA mutation A53T Courtesy: M.C. Sensi, A. Fasano, L. Ricciardi

10 SNCA gene multiplications and PD phenotypes Multiplications of the genomic region containing the SNCA gene cause α-syn overexpression correlation between the number of SNCA copies and phenotypic severity Three SNCA copies Four SNCA copies Subjects Asymptomatic carriers 20 0 Age at onset 50 ± 12 (30-77) 37 ± 10 (24-60) Autonomic dysfunction 41% 100% Psychiatric disturbances 61% 87% Cognitive impairment 52% 96% Elia, Petrucci et al (submitted)

11 Glucocerebrosidase and PD Glucocerebrosidase deficiency Gaucher s disease heterozygous GBA mutations represent the most common genetic risk factor for PD identified to date (4-8% PD vs <1% controls) Clinical picture of GB-related PD : ++ earlier onset, positive family history ++ non-motor features; + severe PD OR = 5.43 Sidransky et al, NEJM, 2009; Brockmann et al, Neurology 2011

12 GBA mutations and DLB Heterozygous GBA mutations significantly increase the risk to develop PDD and DLB UK study (790 PD patients and 257 controls): - 4.2% PD vs 1.2% controls - visual hallucinations: 45% - cognitive decline / dementia: 48% - all cases had widespread and abundant Lewy body pathology, with frequent limbic / diffuse neocortex distribution (Braak stage 5-6) US autoptic study (75 specimes with various synucleinopathies): Goker-Alpan et al, Neurology 2006; Neumann et al, Brain

13 Overlap with genetics of dementia dementia PD PDD DLB 13

14 A novel PD-dementia gene: C9orf72 GGGGCC expansion in C9orf72 gene (>22) is the most frequent genetic cause of FTD+ ALS (± parkinsonism) - variable onset (29-64 yrs) - cognitive decline (2/3 patients) - family history for atypical parkinsonism with dementia / ALS Other genes of FTD ± parkinsonism MAPT (microtubule-associated protein tau, N279 mutation) PGRN (progranulin) TARDBP (TAR DNA binding protein) 14 Lesage et al, Brain 2013

15 Neuropathology of PDD and DLB assessment of α-syn, tau and amyloid-β pathology in 27 PD vs 29 PDD Predictors of dementia: cortical and striatal α-syn cortical Lewy Bodies and dendrites α-syn tau merge cortical and striatal amyloid-β (striatal) tau pathology tau α-syn 15 Duda et al, Acta Neuropathol 2003; Compta et al, Brain 2011; Jellinger, Exp Neurol 2011

16 Tau variants increase the risk of dementia in PD Cognitive decline and PDD are strongly associated with the MAPT H1 genotype This genotype interacts synergically with a 3 UTR variant in SNCA to increase PD (and PDD?) risk 16 Goris et al, Ann Neurol 2003

17 PARK8 - LRRK2 - Dardarin 2482 aminoacids, several active domains including a kinase domain 1-2% of sporadic PD G2019S mutation 5-8% of familial PD Founder effect among Ashkenazi Jews and North African Arabs other mutations are rare (about 10 different mutations reported) Phenotype of LRRK2 mutations: variable presentation, onset 3rd-8th decade reduced penetrance: 15-30%, increasing with age usually indistinguishable from idiopathic PD 17

18 Variability of LRRK2 pathology brainstem Lewy bodies cortical Lewy bodies neurofibrillary tangles extracellular tau deposits 18

19 abnormal ocular movements iron deposition in the BG and SN Complicated PD phenotypes dystonia PD PD spasticity dementia peripheral neuropathy psychiatric disturbances cerebral and/or cerebellar atrophy optic atrophy

20 Autosomal recessive complicated parkinsonisms - early onset (second-third decade), rapid progression (5-6 years) - rigido-akinetic parkinsonian syndrome - pyramidal signs, spasticity - occasional dystonia - sopranuclear upgaze palsy, abnormal saccades - rapid cognitive decline, dementia - visual hallucinations - behavioral problems - psychiatric problems shared features with PDD/DLB - generalized brain atrophy - abnormal DAT scan - responsive to L-dopa, frequent dyskinesias and fluctuations 20

21 A novel parkinson-plus phenotype: SINJ1 onset: third decade severe parkinsonism supranuclear vertical gaze limitation, abnormal saccades disarthria, dysphagia ± dystonia ± cognitive decline, dementia ± spasticity ± jerky facial and tongue movements ± epilepsy rapidly progressive variable response to therapy, ++ side effects (dystonia) brain atrophy 21

22 Dystonia-parkinsonism due to PLA2G6 mutations onset: second-third decade (range yrs) parkinsonism rapid cognitive decline dystonia (++ limbs and axial, focal or generalised) pyramidal signs psychiatric problems ± sopranuclear vertical gaze palsy, hypometric saccades relatively rapid progression (1-5 years) response to dopaminergic treatment, but ++ dyskinesias

23 Behrens et al, Mov Disord 2010; Guehl et al, Neurology 2008 Kufor-Rakeb syndrome (PARK9 / ATP13A2) Phenotypic variability of KRS: - later onset (III decade) - absence of pyramidal signs or dementia - Ataxia, axonal neuropathy and minimal signs of parkinsonism - One heterozygous carrier with early onset parkinsonism - onset: second decade (12-15yrs) - prominent parkinsonism - spasticity, pyramidal - occasional dystonia - rapid cognitive decline dementia - visual hallucinations - sopranuclear upgaze palsy - facial and finger minimyoclonus - responsive to L-dopa

24 Neuroimaging Kufor-Rakeb - cerebral atrophy - variable T2-hypointensity of the GP IRON 24

25 Syndromes with PD, dementia and dystonia neurodegeneration with brain iron accumulation PLAN (PLA2G6) DD delay BPAN (WDR45) PKAN (PANK2) MPAN (C19orf12) Kufor-Rakeb (ATP13A2) dystonia (focal, ++ bulbar districts, or generalized) optic atrophy, retinal degener. iron ± atrophy (!specific features!) MN, cer age at onset cognitive decline, dementia rigid-akinetic parkinsonism psychiatric symptoms, behavioral problems MN, cer piramidal signs, spasticity pallido-pyramidal syndromes dystonia-parkinson (PLA2G6) SN upgaze palsy, abn. saccades atrophy ± iron in SN

26 How can we explain the splitting and lumping?

27 Splitting Mutated proteins interact in common pathogenetic pathways

28 The PINK1 - Parkin axis and removal of damaged mitochondria Normal mitochondria: Parkin is recruited PINK1 is to cleaved the OMM by a protease and degraded Depolarized Ubiquitination mitochondria: of PINK1 several accumulates OMM proteins on the for OMM Perkin ubiquitinates VDAC the and damaged recruits mitochondrion proautophagic UPS degradation, is factors degraded to including initiate mitofusin: the selective damaged autophagic and mitochondria cannot digestion initiate do of the NOT the apoptosis mitochondrion fuse with cascade others Narendra and Youle, 2011

29 GBA deficiency reinforces a-synuclein pathology 29

30 GSK-3β: a pathological link between tau and α-syn GSK-3β is found within Lewy bodies and its levels are increased in the striatum of PD patients and mice models GSK-3β pathologically phosphorylates tau and α-syn α-syn directly stimulates the hyper-phosphorylation of tau by GSK-3β GSK-3β Kawakami et al, FEBS J 2011; Lei et al, Int J Alzh Dis 2011

31 and lumping

32 From mendelian to multifactorial inheritance gene B gene A gene C gene D environment Family 1 pta Family 1 ptb Family 1 ptc sporadic

33 Genome Wide Association Studies in PD ( cases each) SNCA LRRK2 MAPT Nat Genet 2009;41(12) & 2010 ;42(9)

34 Genetic variations as «modifiers» of PD risk mov disord 2009 mov disord 2011 Whole exome (and even whole genome) sequencing are likely to replace GWAS to search for genetic modifiers of the phenotype Tsuji 2010, Hum Mol Genet

35 The NGS-based revolution in genetic diagnosis DYSTONIA PANEL: Illumina MiSeq platform simultaneous sequencing of 14 genes up to 96 samples in a run approx. cost x sample: PD and PDD/LBD panel coming 35

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