Reduced synaptic activity and dysregulated extracellular matrix pathways in midbrain neurons from Parkinson's disease patients.


Journal

NPJ Parkinson's disease
ISSN: 2373-8057
Titre abrégé: NPJ Parkinsons Dis
Pays: United States
ID NLM: 101675390

Informations de publication

Date de publication:
10 Aug 2022
Historique:
received: 12 05 2021
accepted: 11 07 2022
entrez: 10 8 2022
pubmed: 11 8 2022
medline: 11 8 2022
Statut: epublish

Résumé

Several mutations that cause Parkinson's disease (PD) have been identified over the past decade. These account for 15-25% of PD cases; the rest of the cases are considered sporadic. Currently, it is accepted that PD is not a single monolithic disease but rather a constellation of diseases with some common phenotypes. While rodent models exist for some of the PD-causing mutations, research on the sporadic forms of PD is lagging due to a lack of cellular models. In our study, we differentiated PD patient-derived dopaminergic (DA) neurons from the induced pluripotent stem cells (iPSCs) of several PD-causing mutations as well as from sporadic PD patients. Strikingly, we observed a common neurophysiological phenotype: neurons derived from PD patients had a severe reduction in the rate of synaptic currents compared to those derived from healthy controls. While the relationship between mutations in genes such as the SNCA and LRRK2 and a reduction in synaptic transmission has been investigated before, here we show evidence that the pathogenesis of the synapses in neurons is a general phenotype in PD. Analysis of RNA sequencing results displayed changes in gene expression in different synaptic mechanisms as well as other affected pathways such as extracellular matrix-related pathways. Some of these dysregulated pathways are common to all PD patients (monogenic or idiopathic). Our data, therefore, show changes that are central and convergent to PD and suggest a strong involvement of the tetra-partite synapse in PD pathophysiology.

Identifiants

pubmed: 35948563
doi: 10.1038/s41531-022-00366-z
pii: 10.1038/s41531-022-00366-z
pmc: PMC9365794
doi:

Types de publication

Journal Article

Langues

eng

Pagination

103

Subventions

Organisme : NCI NIH HHS
ID : P30 CA014195
Pays : United States
Organisme : Association for Academic Surgery Foundation (AASF)
ID : 0
Organisme : CSRD VA
ID : 1
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Cell Stem Cell. 2021 Sep 2;28(9):1533-1548.e6
pubmed: 33910058
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Exp Cell Res. 2008 Jun 10;314(10):2055-65
pubmed: 18445495
Science. 1997 Jun 27;276(5321):2045-7
pubmed: 9197268
Brain Res. 1977 May 13;126(3):397-42
pubmed: 861729
Nat Neurosci. 2007 Jun;10(6):702-11
pubmed: 17515902
Biomolecules. 2015 Jul 16;5(3):1467-79
pubmed: 26193328
Cereb Cortex. 2007 Jun;17(6):1292-306
pubmed: 16835294
Proc Natl Acad Sci U S A. 2017 May 2;114(18):E3679-E3688
pubmed: 28416701
J Vis Exp. 2017 May 7;(123):
pubmed: 28518110
Parkinsonism Relat Disord. 2009 Nov;15(9):627-32
pubmed: 19632874
J Neurosci Res. 2010 Jun;88(8):1764-76
pubmed: 20029978
Science. 2003 Oct 31;302(5646):841
pubmed: 14593171
J Biol Chem. 2004 Feb 6;279(6):4625-31
pubmed: 14627698
Science. 2012 Nov 16;338(6109):949-53
pubmed: 23161999
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
Brain. 2007 Mar;130(Pt 3):799-815
pubmed: 17303591
Cell. 2012 Jan 20;148(1-2):46-57
pubmed: 22265401
Neuron. 2018 Oct 10;100(1):75-90.e5
pubmed: 30308173
BMC Biol. 2018 Sep 10;16(1):100
pubmed: 30200940
Front Neurosci. 2018 Feb 19;12:80
pubmed: 29515354
J Neurosci. 2007 Feb 7;27(6):1405-10
pubmed: 17287515
J Neuropsychiatry Clin Neurosci. 2002 Spring;14(2):223-36; discussion 222
pubmed: 11983801
J Cell Biol. 1983 May;96(5):1374-88
pubmed: 6404912
Proc Natl Acad Sci U S A. 2015 May 19;112(20):E2725-34
pubmed: 25870293
Proc Natl Acad Sci U S A. 2008 Feb 19;105(7):2693-8
pubmed: 18258746
Nat Genet. 1998 Feb;18(2):106-8
pubmed: 9462735
Lancet. 2004 Sep 25-Oct 1;364(9440):1167-9
pubmed: 15451224
Stem Cell Reports. 2017 Jul 11;9(1):149-161
pubmed: 28579395
Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19492-7
pubmed: 19033459
J Biol Chem. 2002 Jan 4;277(1):486-91
pubmed: 11679592
Hippocampus. 2012 May;22(5):954-68
pubmed: 20882551
J Neurosci. 2011 Feb 9;31(6):2225-37
pubmed: 21307259
Nat Neurosci. 2009 Jul;12(7):826-8
pubmed: 19503083
Parkinsonism Relat Disord. 2016 Jan;22 Suppl 1:S1-6
pubmed: 26350119
J Neurosci. 2009 Jul 22;29(29):9210-8
pubmed: 19625511
Front Mol Neurosci. 2014 May 27;7:49
pubmed: 24904275
Channels (Austin). 2009 Jul-Aug;3(4):233-8
pubmed: 19690465
Neurobiol Aging. 2003 Mar-Apr;24(2):197-211
pubmed: 12498954
J Vis Exp. 2014 Sep 15;(91):51737
pubmed: 25285746
Clin Neuropharmacol. 1999 Jul-Aug;22(4):213-5
pubmed: 10442250
Neurology. 2009 Jul 28;73(4):279-86
pubmed: 19636047
Clin Genet. 2007 May;71(5):471-3
pubmed: 17489854
Handb Clin Neurol. 2018;147:211-227
pubmed: 29325612
Mol Neurodegener. 2014 Nov 12;9:47
pubmed: 25391693
Nat Neurosci. 2019 Feb;22(2):243-255
pubmed: 30617258
Neurochem Res. 2014;39(3):576-92
pubmed: 23729298
Trends Genet. 2018 Jan;34(1):65-78
pubmed: 29102406
Ann Neurol. 2010 Apr;67(4):550
pubmed: 20437592
Hum Mol Genet. 2009 Nov 15;18(22):4390-404
pubmed: 19692353
EMBO J. 2004 Nov 10;23(22):4506-16
pubmed: 15510220
Acta Neuropathol Commun. 2017 Feb 1;5(1):11
pubmed: 28143577
Adv Exp Med Biol. 2012;970:553-72
pubmed: 22351072
Brain Res Dev Brain Res. 1997 Mar 17;99(1):87-94
pubmed: 9088569
Eur Neurol. 1988;28 Suppl 1:15-23
pubmed: 3288478
Ann Neurol. 2004 Feb;55(2):164-73
pubmed: 14755719
Science. 1980 Aug 15;209(4458):809-10
pubmed: 7403847
N Engl J Med. 2000 May 25;342(21):1560-7
pubmed: 10824074
Neuron. 2010 Jan 14;65(1):66-79
pubmed: 20152114
Nature. 2011 Nov 06;480(7378):547-51
pubmed: 22056989
J Neurosci. 2002 Apr 1;22(7):2780-91
pubmed: 11923443
Biol Psychiatry. 2020 Jul 15;88(2):150-158
pubmed: 32278494
J Neurosci. 2019 Sep 11;39(37):7438-7449
pubmed: 31350261
Mol Psychiatry. 2016 Nov;21(11):1573-1588
pubmed: 27698428
Hum Mol Genet. 2017 Aug 1;26(15):2933-2948
pubmed: 28482024
Cell Stem Cell. 2015 Dec 3;17(6):705-718
pubmed: 26456686
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Biochem Soc Trans. 2010 Apr;38(2):493-7
pubmed: 20298209
J Neurosci. 2000 May 1;20(9):3214-20
pubmed: 10777786
Hum Mutat. 2010 Jul;31(7):763-80
pubmed: 20506312
Sci Rep. 2016 Jul 27;6:30509
pubmed: 27461410
J Neurochem. 2001 Jul;78(1):42-54
pubmed: 11432972
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Ann Neurol. 1990 Mar;27(3):276-82
pubmed: 2158268
Genome Biol. 2002;3(1):REVIEWS3002
pubmed: 11806835
Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14622-7
pubmed: 19667187
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Eur Neuropsychopharmacol. 2005 Aug;15(4):473-90
pubmed: 15963700
Mol Cell. 2009 Dec 25;36(6):1034-47
pubmed: 20064468
Brain. 2017 Sep 1;140(9):2265-2272
pubmed: 28335015
J Neurosci. 2004 Dec 8;24(49):11165-70
pubmed: 15590933
Nature. 2001 Feb 15;409(6822):860-921
pubmed: 11237011
Parkinsonism Relat Disord. 2011 Aug;17(7):501-8
pubmed: 21641266
PLoS One. 2011;6(11):e26159
pubmed: 22110584
PLoS One. 2013 Aug 01;8(8):e70274
pubmed: 23936403
EMBO J. 2018 Sep 14;37(18):
pubmed: 30065071
Transl Neurodegener. 2015 Nov 03;4:21
pubmed: 26535116
J Neural Transm (Vienna). 2017 Aug;124(8):901-905
pubmed: 28150045
Hum Genet. 2009 Jan;124(6):593-605
pubmed: 18985386
Nature. 2011 May 12;473(7346):221-5
pubmed: 21490598
J Neurosci. 2014 Feb 5;34(6):2037-50
pubmed: 24501346
Ann Neurol. 2010 Jun;67(6):715-25
pubmed: 20517933
Neurology. 1998 Aug;51(2 Suppl 2):S2-9
pubmed: 9711973
Ann Neurol. 2008 Nov;64(5):485-91
pubmed: 19067353
Elife. 2016 Aug 15;5:
pubmed: 27525480
J Parkinsons Dis. 2015;5(4):699-713
pubmed: 26407041
NPJ Parkinsons Dis. 2020 Apr 24;6:8
pubmed: 32352027
Hum Mol Genet. 2002 Oct 1;11(20):2395-407
pubmed: 12351575
Neurology. 2007 Mar 20;68(12):916-22
pubmed: 17251522
Cold Spring Harb Perspect Med. 2012 Feb;2(2):a009399
pubmed: 22355802
Mov Disord. 2012 Jun;27(7):831-42
pubmed: 22451330
Proc Natl Acad Sci U S A. 2012 Feb 28;109(9):3213-9
pubmed: 22315428
J Neurosci. 2012 Jul 25;32(30):10129-35
pubmed: 22836248
Exp Neurol. 2013 Aug;246:72-83
pubmed: 22285449
Neuron. 2018 Oct 24;100(2):276-293
pubmed: 30359597

Auteurs

Shani Stern (S)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA. sstern@univ.haifa.ac.il.
Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel. sstern@univ.haifa.ac.il.

Shong Lau (S)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Andreea Manole (A)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Idan Rosh (I)

Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Menachem Mendel Percia (MM)

Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Ran Ben Ezer (R)

Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Maxim N Shokhirev (MN)

Razavi Newman Integrative Genomics and Bioinformatics Core, Salk Institute for Biological Studies, La Jolla, CA, USA.

Fan Qiu (F)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Simon Schafer (S)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.
Department of Psychiatry, School of Medicine, Technical University of Munich, Munich, Germany.

Abed AlFatah Mansour (AA)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.
Department of Medical Neurobiology, Institute for Medical Research Israel-Canada, Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.

Kile P Mangan (KP)

Fujifilm Cellular Dynamics, In, Madison, WI, 53711, USA.

Tchelet Stern (T)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.
Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Polina Ofer (P)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.
Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Yam Stern (Y)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.
Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Ana Paula Diniz Mendes (AP)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Jose Djamus (J)

Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Lynne Randolph Moore (LR)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Ritu Nayak (R)

Sagol Department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.

Sapir Havusha Laufer (SH)

Department of Immunology and Regenerative Biology, Weizmann Institute of Science, Rehovot, Israel.

Aidan Aicher (A)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Amanda Rhee (A)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Thomas L Wong (TL)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Thao Nguyen (T)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Sara B Linker (SB)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA.

Beate Winner (B)

Department of Stem Cell Biology, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuernberg, Erlangen, Germany.

Beatriz C Freitas (BC)

Fujifilm Cellular Dynamics, In, Madison, WI, 53711, USA.

Eugenia Jones (E)

Fujifilm Cellular Dynamics, In, Madison, WI, 53711, USA.

Irit Sagi (I)

Department of Immunology and Regenerative Biology, Weizmann Institute of Science, Rehovot, Israel.

Cedric Bardy (C)

South Australian Health and Medical Research Institute (SAHMRI), Laboratory for Human Neurophysiology and Genetics, Adelaide, SA, Australia.
Flinders University, Flinders Health and Medical Research Institute (FHMRI), Adelaide, SA, Australia.

Alexis Brice (A)

Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, APHP, F-75013, Paris, France.

Juergen Winkler (J)

Department of Molecular Neurology, University Hospital Erlangen, Friedrich-Alexander-University Erlangen- Nürnberg, Nürnberg, Germany.

Maria C Marchetto (MC)

Department of Anthropology, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA.

Fred H Gage (FH)

Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA, USA. gage@salk.edu.

Classifications MeSH