The Amyotrophic Lateral Sclerosis M114T PFN1 Mutation Deregulates Alternative Autophagy Pathways and Mitochondrial Homeostasis.

ALS NSC-34 cell line RAB9 alternative autophagy genetics lymphoblasts mitochondrial homeostasis mutations post-mortem spinal cord transgenic mice

Journal

International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791

Informations de publication

Date de publication:
19 May 2022
Historique:
received: 29 04 2022
revised: 13 05 2022
accepted: 15 05 2022
entrez: 28 5 2022
pubmed: 29 5 2022
medline: 1 6 2022
Statut: epublish

Résumé

Mutations in profilin 1 (PFN1) have been identified in rare familial cases of Amyotrophic Lateral Sclerosis (ALS). PFN1 is involved in multiple pathways that could intervene in ALS pathology. However, the specific pathogenic role of PFN1 mutations in ALS is still not fully understood. We hypothesized that PFN1 could play a role in regulating autophagy pathways and that PFN1 mutations could disrupt this function. We used patient cells (lymphoblasts) or tissue (post-mortem) carrying PFN1 mutations (M114T and E117G), and designed experimental models expressing wild-type or mutant PFN1 (cell lines and novel PFN1 mice established by lentiviral transgenesis) to study the effects of PFN1 mutations on autophagic pathway markers. We observed no accumulation of PFN1 in the spinal cord of one E117G mutation carrier. Moreover, in patient lymphoblasts and transfected cell lines, the M114T mutant PFN1 protein was unstable and deregulated the RAB9-mediated alternative autophagy pathway involved in the clearance of damaged mitochondria. In vivo, motor neurons expressing M114T mutant PFN1 showed mitochondrial abnormalities. Our results demonstrate that the M114T PFN1 mutation is more deleterious than the E117G variant in patient cells and experimental models and suggest a role for the RAB9-dependent autophagic pathway in ALS.

Identifiants

pubmed: 35628504
pii: ijms23105694
doi: 10.3390/ijms23105694
pmc: PMC9143529
pii:
doi:

Substances chimiques

PFN1 protein, human 0
Pfn1 protein, mouse 0
Profilins 0
RAB9A protein, human EC 3.6.1.-
rab9 protein, mouse EC 3.6.1.-
rab GTP-Binding Proteins EC 3.6.5.2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Association pour la recherche sur la Sclérose Latérale Amyotrophique
ID : R11010DD, R17050DD & S.3200.ARSLA.1
Organisme : Association Française contre les Myopathies
ID : #19466 & #19466
Organisme : Aide à la Recherche des Maladies du Cerveau association
ID : R16009DD
Organisme : Fédération pour la Recherche sur le Cerveau
ID : AO-FRC 2009 #33536
Organisme : Stafford Fox Medical Research Foundation

Références

Cell. 2006 Jan 27;124(2):423-35
pubmed: 16439214
Amyotroph Lateral Scler Other Motor Neuron Disord. 2000 Dec;1(5):293-9
pubmed: 11464847
Proc Natl Acad Sci U S A. 2014 Oct 21;111(42):E4439-48
pubmed: 25294927
Muscle Nerve. 1997 Jan;20(1):45-51
pubmed: 8995582
Hum Mol Genet. 2017 Feb 15;26(4):686-701
pubmed: 28040732
Autophagy. 2010 Feb;6(2):290-1
pubmed: 20104021
Nature. 2010 Aug 26;466(7310):1069-75
pubmed: 20740007
Autophagy. 2005 Jul;1(2):84-91
pubmed: 16874052
Nat Genet. 2006 Apr;38(4):411-3
pubmed: 16501576
EMBO J. 1998 Feb 16;17(4):967-76
pubmed: 9463375
Biochem J. 2016 Apr 1;473(7):859-72
pubmed: 26787927
Trends Mol Med. 2016 Sep;22(9):769-783
pubmed: 27498188
Acta Neuropathol. 2013 Apr;125(4):511-22
pubmed: 23417734
PLoS One. 2011;6(7):e22031
pubmed: 21779368
Hum Mol Genet. 2016 Apr 1;25(7):1420-33
pubmed: 26908597
Acta Neuropathol. 2004 Jul;108(1):81-7
pubmed: 15114487
J Neurosci. 2014 Jun 11;34(24):8083-97
pubmed: 24920614
Nat Commun. 2019 Aug 23;10(1):3827
pubmed: 31444357
Trends Genet. 2015 May;31(5):263-73
pubmed: 25869998
Brain. 2011 Sep;134(Pt 9):2456-77
pubmed: 21810890
Front Mol Neurosci. 2019 Sep 27;12:231
pubmed: 31611772
Autophagy. 2012 Nov;8(11):1590-603
pubmed: 22863730
Cancers (Basel). 2019 Aug 20;11(8):
pubmed: 31434275
J Med Genet. 2010 Aug;47(8):554-60
pubmed: 20577002
J Med Genet. 2012 Apr;49(4):258-63
pubmed: 22499346
Transl Proteom. 2014 Jun 1;3:10-21
pubmed: 26157646
Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):E107; author reply E108
pubmed: 20538972
Nature. 1980 Jul 3;286(5768):79-80
pubmed: 6993961
Nature. 2012 Aug 23;488(7412):499-503
pubmed: 22801503
Nature. 2009 Oct 1;461(7264):654-8
pubmed: 19794493
Neurobiol Aging. 2015 Mar;36(3):1602.e17-27
pubmed: 25499087
Int J Biochem Cell Biol. 2014 May;50:64-6
pubmed: 24569119
Trends Cell Biol. 2004 Aug;14(8):461-9
pubmed: 15308213
J Biol Chem. 2001 Sep 21;276(38):35243-6
pubmed: 11477064
Autophagy. 2010 Feb;6(2):217-27
pubmed: 20104022
J Immunol Methods. 1983 Dec 16;65(1-2):55-63
pubmed: 6606682
Neuron. 2010 Dec 9;68(5):857-64
pubmed: 21145000
Neurobiol Dis. 2019 Feb;122:35-40
pubmed: 29981842
J Vis Exp. 2018 Oct 7;(140):
pubmed: 30346378
J Immunol Methods. 1989 May 12;119(2):203-10
pubmed: 2470825
Clin Neurophysiol. 2008 Mar;119(3):497-503
pubmed: 18164242
J Neurol Neurosurg Psychiatry. 2014 May;85(5):506-8
pubmed: 24309268
Neurosci Bull. 2020 Feb;36(2):174-178
pubmed: 31802421
Hum Mol Genet. 2012 Sep 1;21(17):3776-84
pubmed: 22645277
Nature. 1993 Oct 28;365(6449):810-6
pubmed: 8413665
J Cell Physiol. 2009 Feb;218(2):436-43
pubmed: 18937284
Proc Natl Acad Sci U S A. 2008 Mar 11;105(10):4022-7
pubmed: 18296640
Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):3832-6
pubmed: 11274401
Neurobiol Aging. 2013 Sep;34(9):2235.e7-10
pubmed: 23635659
Proc Natl Acad Sci U S A. 2021 Jun 8;118(23):
pubmed: 34074767
J Cell Biol. 2009 Dec 14;187(6):875-88
pubmed: 20008565
Nat Biotechnol. 2001 May;19(5):446-50
pubmed: 11329014
Neurobiol Aging. 2013 Jul;34(7):1922.e1-5
pubmed: 23428184
Acta Neuropathol. 2009 Oct;118(4):561-73
pubmed: 19449021
Nucleic Acids Res. 1996 May 1;24(9):1787-8
pubmed: 8650001
Neuroreport. 1996 May 31;7(8):1427-31
pubmed: 8856691
Proc Natl Acad Sci U S A. 2015 Jun 30;112(26):7984-9
pubmed: 26056300
Front Cell Neurosci. 2019 Nov 07;13:489
pubmed: 31787882
Neurobiol Aging. 2014 Dec;35(12):2882.e13-2882.e15
pubmed: 25158920
Nat Commun. 2013;4:2130
pubmed: 23945651
Amyotroph Lateral Scler Frontotemporal Degener. 2013 Sep;14(5-6):463-9
pubmed: 23634771
Hum Mol Genet. 2013 Oct 1;22(19):3947-59
pubmed: 23736301
Biol Chem. 2016 Sep 1;397(9):927-37
pubmed: 27101547
Acta Pharmacol Sin. 2013 May;34(5):595-9
pubmed: 23474710
Autophagy. 2015;11(2):332-43
pubmed: 25831013
Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):E6209-E6218
pubmed: 27681617
J Neurochem. 2021 May;157(4):1244-1252
pubmed: 32754913
Curr Biol. 2017 Nov 20;27(22):3535-3543.e4
pubmed: 29129529
Metab Brain Dis. 2018 Dec;33(6):1975-1984
pubmed: 30203378
J Neurol Neurosurg Psychiatry. 2020 Feb;91(2):223-224
pubmed: 31401564
Neurobiol Aging. 2013 May;34(5):1517.e9-10
pubmed: 23063648
Neurobiol Aging. 2011 Mar;32(3):557.e11-3
pubmed: 21220178
J Biol Chem. 1994 Feb 11;269(6):4620-5
pubmed: 8308034
BMC Neurosci. 2015 Nov 16;16:77
pubmed: 26572741
Biology (Basel). 2019 May 11;8(2):
pubmed: 31083575
Nat Genet. 2016 Sep;48(9):1037-42
pubmed: 27455347
Int J Mol Sci. 2017 Aug 28;18(9):
pubmed: 28846632
Neuroreport. 1997 Sep 8;8(13):2861-5
pubmed: 9376520
Hum Mol Genet. 2017 Jun 1;26(11):2146-2155
pubmed: 28379367
EMBO J. 2000 Nov 1;19(21):5720-8
pubmed: 11060023
Nat Commun. 2016 Sep 30;7:12886
pubmed: 27686185
Neurochem Int. 2011 Nov;59(6):976-80
pubmed: 21802467
Ann Neurol. 2015 Jan;77(1):100-13
pubmed: 25382069
J Cell Biol. 1963 Apr;17:208-12
pubmed: 13986422
J Biol Chem. 2002 Aug 16;277(33):29626-33
pubmed: 12050154
Neurobiol Aging. 2013 Jun;34(6):1708.e1-6
pubmed: 23141414
Dev Dyn. 1992 Jul;194(3):209-21
pubmed: 1467557
PLoS One. 2014 Oct 31;9(10):e109916
pubmed: 25360519
Neurobiol Aging. 2014 May;35(5):1213.e9-1213.e12
pubmed: 24360741
Mol Cells. 2018 Jan 31;41(1):50-54
pubmed: 29370693

Auteurs

Elisa Teyssou (E)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Laura Chartier (L)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Delphine Roussel (D)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Nirma D Perera (ND)

The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3052, Australia.

Ivan Nemazanyy (I)

Platform for Metabolic Analyses, Structure Fédérative de Recherche Necker, INSERM US24/CNRS UAR 3633, F-75015 Paris, France.

Dominique Langui (D)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Mélanie Albert (M)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Thierry Larmonier (T)

Banque d'ADN et de Cellules du Généthon, F-91000 Evry, France.

Safaa Saker (S)

Banque d'ADN et de Cellules du Généthon, F-91000 Evry, France.

François Salachas (F)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.
Centre de Référence SLA Ile de France, Département de Neurologie, Hôpital de la Pitié-Salpêtrière, APHP, DMU Neuroscience, F-75013 Paris, France.

Pierre-François Pradat (PF)

Centre de Référence SLA Ile de France, Département de Neurologie, Hôpital de la Pitié-Salpêtrière, APHP, DMU Neuroscience, F-75013 Paris, France.
Laboratoire d'Imagerie Biomédicale, Sorbonne Université, INSERM UMRS1146, CNRS UMR7371, F-75013 Paris, France.
Northern Ireland Centre for Stratified Medicine, Biomedical Sciences Research Institute Ulster University, C-TRIC, Altnagelvin Hospital, Derry-Londonderry BT47 6SB, UK.

Vincent Meininger (V)

Hôpital des Peupliers, Ramsay Générale de Santé, F-75013 Paris, France.

Philippe Ravassard (P)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Francine Côté (F)

Institut Cochin, INSERM U1016, CNRS UMR8104, Université de Paris, F-75014 Paris, France.

Christian S Lobsiger (CS)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Séverine Boillée (S)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

Bradley J Turner (BJ)

The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3052, Australia.

Danielle Seilhean (D)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.
APHP, Département de Neuropathologie, Hôpital Pitié-Salpêtrière, DMU Neuroscience, F-75013 Paris, France.

Stéphanie Millecamps (S)

Institut du Cerveau-Paris Brain Institute-ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, Sorbonne Université, F-75013 Paris, France.

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