Literature DB >> 26282470

Chronic and acute LRRK2 silencing has no long-term behavioral effects, whereas wild-type and mutant LRRK2 overexpression induce motor and cognitive deficits and altered regulation of dopamine release.

Mattia Volta1, Stefano Cataldi1, Dayne Beccano-Kelly1, Lise Munsie1, Igor Tatarnikov1, Patrick Chou1, Sabrina Bergeron1, Emma Mitchell1, Roscoe Lim1, Jaskaran Khinda1, Alejandro Lloret2, C Frank Bennett2, Carmela Paradiso3, Michele Morari3, Matthew J Farrer4, Austen J Milnerwood5.   

Abstract

INTRODUCTION: Germline silencing of the PD-related protein LRRK2 does not alter glutamate or dopamine release in adult mice, but some exploratory abnormalities have been reported with ageing. Contrastingly, high levels of human LRRK2 cause locomotor alterations and cognitive deficits accompanied by reduced striatal dopamine levels, with the latter also observed in G2019S mutant mice. Comparative cognitive and motor behavioral testing of LRRK2 KO, overexpressor and mutant overexpressor mice has not previously been reported.
METHODS: Parallel, comparative behavioral characterization was performed assessing motor and cognitive abilities. Striatal antisense oligonucleotide injections were conducted to investigate the effects of acute LRRK2 silencing on behavior and dopamine fiber density. Striatal synaptosomes prepared from hG2019S mice assessed vesicular release of dopamine and its sensitivity to D2 autoreceptor stimulation.
RESULTS: Genetic ablation of LRRK2 has no long-term consequences on motor or cognitive function. Consistently, no effects on behavior or dopaminergic fiber density were observed following acute striatal silencing. Conversely, 12-month OE mice show persistent locomotor deficits and worsening of cognitive abilities; whereas, hG2019S mice display early hyperactivity and effective learning and memory that progress to decreased motor and cognitive deficits at older ages. The G2019S mutation does not affect vesicular dopamine release, but decreases its sensitivity to D2-mediated inhibition.
CONCLUSION: LRRK2 silencing is well tolerated in mouse, arguing PD does not result from LRRK2 loss of function. High levels of WT and G2019S LRRK2 produce similar but temporally distinct phenotypes, potentially modeling different stages of disease progression. The data implicate gain of LRRK2 function in the pathogenesis of PD.
Copyright © 2015 Elsevier Ltd. All rights reserved.

Entities:  

Keywords:  Behavior; Cognition; Genetic models; LRRK2; Parkinson's disease; Synaptosomes

Mesh:

Substances:

Year:  2015        PMID: 26282470     DOI: 10.1016/j.parkreldis.2015.07.025

Source DB:  PubMed          Journal:  Parkinsonism Relat Disord        ISSN: 1353-8020            Impact factor:   4.891


  17 in total

Review 1.  Functional and behavioral consequences of Parkinson's disease-associated LRRK2-G2019S mutation.

Authors:  Deanna L Benson; Bridget A Matikainen-Ankney; Ayan Hussein; George W Huntley
Journal:  Biochem Soc Trans       Date:  2018-12-04       Impact factor: 5.407

2.  Mitochondrial Calcium Dysregulation Contributes to Dendrite Degeneration Mediated by PD/LBD-Associated LRRK2 Mutants.

Authors:  Manish Verma; Jason Callio; P Anthony Otero; Israel Sekler; Zachary P Wills; Charleen T Chu
Journal:  J Neurosci       Date:  2017-10-16       Impact factor: 6.167

3.  Human LRRK2 G2019S mutation represses post-synaptic protein PSD95 and causes cognitive impairment in transgenic mice.

Authors:  Samuel O Adeosun; Xu Hou; Baoying Zheng; Heather L Melrose; Thomas Mosley; Jun Ming Wang
Journal:  Neurobiol Learn Mem       Date:  2017-05-06       Impact factor: 2.877

Review 4.  Lysosomal Pathogenesis of Parkinson's Disease: Insights From LRRK2 and GBA1 Rodent Models.

Authors:  Mattia Volta
Journal:  Neurotherapeutics       Date:  2022-09-09       Impact factor: 6.088

5.  Robust kinase- and age-dependent dopaminergic and norepinephrine neurodegeneration in LRRK2 G2019S transgenic mice.

Authors:  Yulan Xiong; Stewart Neifert; Senthilkumar S Karuppagounder; Qinfang Liu; Jeannette N Stankowski; Byoung Dae Lee; Han Seok Ko; Yunjong Lee; Jonathan C Grima; Xiaobo Mao; Haisong Jiang; Sung-Ung Kang; Deborah A Swing; Lorraine Iacovitti; Lino Tessarollo; Ted M Dawson; Valina L Dawson
Journal:  Proc Natl Acad Sci U S A       Date:  2018-01-31       Impact factor: 11.205

6.  Parkinson's Disease-Linked LRRK2-G2019S Mutation Alters Synaptic Plasticity and Promotes Resilience to Chronic Social Stress in Young Adulthood.

Authors:  Bridget A Matikainen-Ankney; Nebojsa Kezunovic; Caroline Menard; Meghan E Flanigan; Yue Zhong; Scott J Russo; Deanna L Benson; George W Huntley
Journal:  J Neurosci       Date:  2018-09-24       Impact factor: 6.167

7.  Combined Knockout of Lrrk2 and Rab29 Does Not Result in Behavioral Abnormalities in vivo.

Authors:  Melissa Conti Mazza; Victoria Nguyen; Alexandra Beilina; Ema Karakoleva; Michael Coyle; Jinhui Ding; Christopher Bishop; Mark R Cookson
Journal:  J Parkinsons Dis       Date:  2021       Impact factor: 5.520

8.  A proteomic analysis of LRRK2 binding partners reveals interactions with multiple signaling components of the WNT/PCP pathway.

Authors:  Alena Salašová; Chika Yokota; David Potěšil; Zbyněk Zdráhal; Vítězslav Bryja; Ernest Arenas
Journal:  Mol Neurodegener       Date:  2017-07-11       Impact factor: 14.195

9.  Initial elevations in glutamate and dopamine neurotransmission decline with age, as does exploratory behavior, in LRRK2 G2019S knock-in mice.

Authors:  Mattia Volta; Dayne A Beccano-Kelly; Sarah A Paschall; Stefano Cataldi; Sarah E MacIsaac; Matthew J Farrer; Austen J Milnerwood; Naila Kuhlmann; Chelsie A Kadgien; Igor Tatarnikov; Jesse Fox; Jaskaran Khinda; Emma Mitchell; Sabrina Bergeron; Heather Melrose
Journal:  Elife       Date:  2017-09-20       Impact factor: 8.140

10.  Classification of Parkinson's Disease Genotypes in Drosophila Using Spatiotemporal Profiling of Vision.

Authors:  Ryan J H West; Christopher J H Elliott; Alex R Wade
Journal:  Sci Rep       Date:  2015-11-24       Impact factor: 4.379

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