ATP6V1A is required for synaptic rearrangements and plasticity in murine hippocampal neurons.

ATP6V1A LTP autophagy lysosome neurodevelopment synapse v‐ATPase

Journal

Acta physiologica (Oxford, England)
ISSN: 1748-1716
Titre abrégé: Acta Physiol (Oxf)
Pays: England
ID NLM: 101262545

Informations de publication

Date de publication:
05 Jun 2024
Historique:
revised: 05 05 2024
received: 11 09 2023
accepted: 23 05 2024
medline: 5 6 2024
pubmed: 5 6 2024
entrez: 5 6 2024
Statut: aheadofprint

Résumé

Understanding the physiological role of ATP6V1A, a component of the cytosolic V Modeling loss of function of Atp6v1a in primary murine hippocampal neurons and studying neuronal morphology and function by immunoimaging, electrophysiological recordings and electron microscopy. Atp6v1a depletion affects neurite elongation, stabilization, and function of excitatory synapses and prevents synaptic rearrangement upon induction of plasticity. These phenotypes are due to an overall decreased expression of the V These data suggest a physiological role of ATP6V1A in the surveillance of synaptic integrity and plasticity and highlight the pathophysiological significance of ATP6V1A loss in the alteration of synaptic function that is associated with neurodevelopmental and neurodegenerative diseases. The data further support the pivotal involvement of lysosomal function and autophagy flux in maintaining proper synaptic connectivity and adaptive neuronal properties.

Identifiants

pubmed: 38837572
doi: 10.1111/apha.14186
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14186

Subventions

Organisme : #NEXTGENERATIONEU (NGEU) and funded by the Ministry of University and Research (MUR), National Recovery and Resilience Plan (NRRP), project MNESYS (PE0000006)-A multiscale inte- grated approach to the study of the nervous system in health and disease (DN. 1553 11.10.2022).
Organisme : The Italian Ministry of Health (Ricerca Finalizzata Giovani Ricercatori GR-2019-12 370 176)
Organisme : IRCCS Ospedale Policlinico San Martino (5x1000 and Ricerca Corrente)
Organisme : Tuscany Region Call for Health 2018 (grant DECODE-EE)
Organisme : Fondazione Cassa di Risparmio di Firenze (Human Brain Optical Mapping Project)
Organisme : University of Genoa (Grant D.R. 3404, Heavy Equipment)

Informations de copyright

© 2024 The Author(s). Acta Physiologica published by John Wiley & Sons Ltd on behalf of Scandinavian Physiological Society.

Références

Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol. 2007;8(11):917‐929. doi:10.1038/nrm2272
McGuire CM, Forgac M. Glucose starvation increases V‐ATPase assembly and activity in mammalian cells through AMP kinase and phosphatidylinositide 3‐kinase/Akt signaling. J Biol Chem. 2018;293(23):9113‐9123. doi:10.1074/jbc.RA117.001327
Ratto E, Chowdhury SR, Siefert NS, et al. Direct control of lysosomal catabolic activity by mTORC1 through regulation of V‐ATPase assembly. Nat Commun. 2022;13(1):4848. doi:10.1038/s41467-022-32515-6
Stransky L, Cotter K, Forgac M. The function of V‐ATPases in cancer. Physiol Rev. 2016;96(3):1071‐1091. doi:10.1152/physrev.00035.2015
Smith GA, Howell GJ, Phillips C, Muench SP, Ponnambalam S, Harrison MA. Extracellular and luminal pH regulation by vacuolar H+‐ATPase isoform expression and targeting to the plasma membrane and endosomes. J Biol Chem. 2016;291(16):8500‐8515. doi:10.1074/jbc.M116.723395
Toei M, Saum R, Forgac M. Regulation and isoform function of the V‐ATPases. Biochemistry. 2010;49(23):4715‐4723. doi:10.1021/bi100397s
Stavoe AKH, Holzbaur ELF. Autophagy in neurons. Annu Rev Cell Dev Biol. 2019;35:477‐500. doi:10.1146/annurev-cellbio-100818-125242
Gowrisankaran S, Milosevic I. Regulation of synaptic vesicle acidification at the neuronal synapse. IUBMB Life. 2020;72(4):568‐576. doi:10.1002/iub.2235
Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, et al. Molecular anatomy of a trafficking organelle. Cell. 2006;127(4):831‐846. doi:10.1016/j.cell.2006.10.030
Aoto K, Kato M, Akita T, et al. ATP6V0A1 encoding the a1‐subunit of the V0 domain of vacuolar H(+)‐ATPases is essential for brain development in humans and mice. Nat Commun. 2021;12(1):2107. doi:10.1038/s41467-021-22389-5
Beauregard‐Lacroix E, Pacheco‐Cuellar G, Ajeawung NF, et al. DOORS syndrome and a recurrent truncating ATP6V1B2 variant. Genet Med. 2021;23(1):149‐154. doi:10.1038/s41436-020-00950-9
Bott LC, Forouhan M, Lieto M, et al. Variants in ATP6V0A1 cause progressive myoclonus epilepsy and developmental and epileptic encephalopathy. Brain Commun. 2021;3(4):fcab245. doi:10.1093/braincomms/fcab245
Esposito A, Falace A, Wagner M, et al. Biallelic DMXL2 mutations impair autophagy and cause Ohtahara syndrome with progressive course. Brain. 2019;142(12):3876‐3891. doi:10.1093/brain/awz326
Fassio A, Esposito A, Kato M, et al. De novo mutations of the ATP6V1A gene cause developmental encephalopathy with epilepsy. Brain. 2018;141(6):1703‐1718. doi:10.1093/brain/awy092
Fassio A, Falace A, Esposito A, Aprile D, Guerrini R, Benfenati F. Emerging role of the autophagy/lysosomal degradative pathway in neurodevelopmental disorders with epilepsy. Front Cell Neurosci. 2020;14:39. doi:10.3389/fncel.2020.00039
Guerrini R, Mei D, Kerti‐Szigeti K, et al. Phenotypic and genetic spectrum of ATP6V1A encephalopathy: a disorder of lysosomal homeostasis. Brain. 2022;145(8):2687‐2703. doi:10.1093/brain/awac145
Hirose T, Cabrera‐Socorro A, Chitayat D, Lemonnier T, Feraud O, et al. ATP6AP2 variant impairs CNS development and neuronal survival to cause fulminant neurodegeneration. J Clin Invest. 2019;129(5):2145‐2162. doi:10.1172/JCI79990
Zhao W, Gao X, Qiu S, et al. A subunit of V‐ATPases, ATP6V1B2, underlies the pathology of intellectual disability. EBioMedicine. 2019;45:408‐421. doi:10.1016/j.ebiom.2019.06.035
Neff RA, Wang M, Vatansever S, et al. Molecular subtyping of Alzheimer's disease using RNA sequencing data reveals novel mechanisms and targets. Sci Adv. 2021;7:2. doi:10.1126/sciadv.abb5398
Wang M, Li A, Sekiya M, et al. Transformative network modeling of multi‐omics data reveals detailed circuits, key regulators, and potential therapeutics for Alzheimer's disease. Neuron. 2021;109:257‐272.e14. doi:10.1016/j.neuron.2020.11.002
Zhou Z, Bai J, Zhong S, et al. Downregulation of ATP6V1A involved in Alzheimer's disease via synaptic vesicle cycle, phagosome, and oxidative phosphorylation. Oxidative Med Cell Longev. 2021;2021:5555634. doi:10.1155/2021/5555634
Abbas YM, Wu D, Bueler SA, Robinson CV, Rubinstein JL. Structure of V‐ATPase from the mammalian brain. Science. 2020;367(6483):1240‐1246. doi:10.1126/science.aaz2924
Di Giovanni J, Boudkkazi S, Mochida S, Bialowas A, Samari N, et al. V‐ATPase membrane sector associates with synaptobrevin to modulate neurotransmitter release. Neuron. 2010;67(2):268‐279. doi:10.1016/j.neuron.2010.06.024
Leveque C, Maulet Y, Wang Q, Rame M, Rodriguez L, et al. A role for the V0 sector of the V‐ATPase in Neuroexocytosis: exogenous V0d blocks complexin and SNARE interactions with V0c. Cells. 2023;12:5. doi:10.3390/cells12050750
Bodzeta A, Kahms M, Klingauf J. The presynaptic v‐ATPase reversibly disassembles and thereby modulates exocytosis but is not part of the fusion machinery. Cell Rep. 2017;20(6):1348‐1359. doi:10.1016/j.celrep.2017.07.040
Farsi Z, Gowrisankaran S, Krunic M, et al. Clathrin coat controls synaptic vesicle acidification by blocking vacuolar ATPase activity. elife. 2018;7:e32569. doi:10.7554/eLife.32569
Colacurcio DJ, Nixon RA. Disorders of lysosomal acidification‐the emerging role of v‐ATPase in aging and neurodegenerative disease. Ageing Res Rev. 2016;32:75‐88. doi:10.1016/j.arr.2016.05.004
Qiu S, Zhao W, Gao X, et al. Syndromic deafness gene ATP6V1B2 controls degeneration of spiral ganglion neurons through modulating proton flux. Front Cell Dev Biol. 2021;9:742714. doi:10.3389/fcell.2021.742714
Wu JJ, Cai A, Greenslade JE, et al. ALS/FTD mutations in UBQLN2 impede autophagy by reducing autophagosome acidification through loss of function. Proc Natl Acad Sci USA. 2020;117(26):15230‐15241. doi:10.1073/pnas.1917371117
Cheng A, Tse KH, Chow HM, et al. ATM loss disrupts the autophagy‐lysosomal pathway. Autophagy. 2021;17(8):1998‐2010. doi:10.1080/15548627.2020.1805860
Compans B, Camus C, Kallergi E, et al. NMDAR‐dependent long‐term depression is associated with increased short term plasticity through autophagy mediated loss of PSD‐95. Nat Commun. 2021;12(1):2849. doi:10.1038/s41467-021-23133-9
Daskalaki AD, Kallergi E, Kolaxi A, Nikoletopoulou V. Local biogenesis of autophagic vesicles in neuronal dendrites facilitates long‐term synaptic depression. Autophagy. 2022;18(8):2011‐2012. doi:10.1080/15548627.2022.2061757
Glatigny M, Moriceau S, Rivagorda M, et al. Autophagy is required for memory formation and reverses age‐related memory decline. Curr Biol. 2019;29(3):435‐448.e8. doi:10.1016/j.cub.2018.12.021
Goo MS, Sancho L, Slepak N, et al. Activity‐dependent trafficking of lysosomes in dendrites and dendritic spines. J Cell Biol. 2017;216(8):2499‐2513. doi:10.1083/jcb.201704068
Hoffmann S, Orlando M, Andrzejak E, et al. Light‐activated ROS production induces synaptic autophagy. J Neurosci. 2019;39(12):2163‐2183. doi:10.1523/JNEUROSCI.1317-18.2019
Overhoff M, Tellkamp F, Hess S, et al. Autophagy regulates neuronal excitability by controlling cAMP/protein kinase a signaling at the synapse. EMBO J. 2022;41(22):e110963. doi:10.15252/embj.2022110963
Yang S, Park D, Manning L, et al. Presynaptic autophagy is coupled to the synaptic vesicle cycle via ATG‐9. Neuron. 2022;110:824‐840.e10. doi:10.1016/j.neuron.2021.12.031
Li B, Lan S, Liu XR, et al. ATP6V1A variants are associated with childhood epilepsy with favorable outcome. Seizure. 2023;116:81‐86. doi:10.1016/j.seizure.2023.08.004
Van Damme T, Gardeitchik T, Mohamed M, Guerrero‐Castillo S, Freisinger P, et al. Mutations in ATP6V1E1 or ATP6V1A cause autosomal‐recessive cutis Laxa. Am J Hum Genet. 2017;100(2):216‐227. doi:10.1016/j.ajhg.2016.12.010
Vogt G, El Choubassi N, Herczegfalvi A, Kolbel H, Lekaj A, et al. Expanding the clinical and molecular spectrum of ATP6V1A related metabolic cutis laxa. J Inherit Metab Dis. 2021;44(4):972‐986. doi:10.1002/jimd.12341
Gundelfinger ED, Karpova A, Pielot R, Garner CC, Kreutz MR. Organization of presynaptic autophagy‐related processes. Front Synaptic Neurosci. 2022;14:829354. doi:10.3389/fnsyn.2022.829354
Xuan Z, Yang S, Clark B, Hill SE, Manning L, Colón‐Ramos DA. The active zone protein clarinet regulates synaptic sorting of ATG‐9 and presynaptic autophagy. PLoS Biol. 2023;21(4):e3002030. doi:10.1371/journal.pbio.3002030
Wang H, Bueler SA, Rubinstein JL. Structural basis of V‐ATPase V(O) region assembly by Vma12p, 21p, and 22p. Proc Natl Acad Sci USA. 2023;120(6):e2217181120. doi:10.1073/pnas.2217181120
Nikoletopoulou V, Papandreou ME, Tavernarakis N. Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ. 2015;22(3):398‐407. doi:10.1038/cdd.2014.204
Kim D, Hwang HY, Kim JY, et al. FK506, an immunosuppressive drug, induces autophagy by binding to the V‐ATPase catalytic subunit a in neuronal cells. J Proteome Res. 2017;16(1):55‐64. doi:10.1021/acs.jproteome.6b00638
Chung CY, Shin HR, Berdan CA, Ford B, Ward CC, et al. Covalent targeting of the vacuolar H(+)‐ATPase activates autophagy via mTORC1 inhibition. Nat Chem Biol. 2019;15(8):776‐785. doi:10.1038/s41589-019-0308-4
Kim G, Nakayama L, Blum JA, et al. Genome‐wide CRISPR screen reveals v‐ATPase as a drug target to lower levels of ALS protein ataxin‐2. Cell Rep. 2022;41(4):111508. doi:10.1016/j.celrep.2022.111508
De Palma M, Naldini L. Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol. 2002;346:514‐529. doi:10.1016/s0076-6879(02)46074-0
Verstegen AM, Tagliatti E, Lignani G, Marte A, Stolero T, et al. Phosphorylation of synapsin I by cyclin‐dependent kinase‐5 sets the ratio between the resting and recycling pools of synaptic vesicles at hippocampal synapses. J Neurosci. 2014;34(21):7266‐7280. doi:10.1523/JNEUROSCI.3973-13.2014
Tagliatti E, Fadda M, Falace A, Benfenati F, Fassio A. Arf6 regulates the cycling and the readily releasable pool of synaptic vesicles at hippocampal synapse. elife. 2016;5:e10116. doi:10.7554/eLife.10116
Baldelli P, Fassio A, Valtorta F, Benfenati F. Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J Neurosci. 2007;27(49):13520‐13531. doi:10.1523/JNEUROSCI.3151-07.2007
Chiappalone M, Casagrande S, Tedesco M, et al. Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I‐deficient cortical networks. Cereb Cortex. 2009;19(6):1422‐1439. doi:10.1093/cercor/bhn182
Lu W, Man H, Ju W, Trimble WS, MacDonald JF, et al. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 2001;29(1):243‐254. doi:10.1016/s0896-6273(01)00194-5
Oh MC, Derkach VA. Dominant role of the GluR2 subunit in regulation of AMPA receptors by CaMKII. Nat Neurosci. 2005;8(7):853‐854. doi:10.1038/nn1476

Auteurs

Alessandro Esposito (A)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.

Sara Pepe (S)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.
IRCCS, Ospedale Policlinico San Martino, Genoa, Italy.

Maria Sabina Cerullo (MS)

Center for Synaptic Neuroscience and Technology, Italian Institute of Technology, Genoa, Italy.

Katia Cortese (K)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.

Hanako Tsushima Semini (HT)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.

Silvia Giovedì (S)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.
IRCCS, Ospedale Policlinico San Martino, Genoa, Italy.

Renzo Guerrini (R)

Children's Hospital A. Meyer IRCCS, Florence, Italy.
Dipartimento di Neuroscienze, Psicologia, Area del Farmaco e Salute del Bambino, University of Florence, Florence, Italy.

Fabio Benfenati (F)

IRCCS, Ospedale Policlinico San Martino, Genoa, Italy.
Center for Synaptic Neuroscience and Technology, Italian Institute of Technology, Genoa, Italy.

Antonio Falace (A)

Children's Hospital A. Meyer IRCCS, Florence, Italy.
Pediatric Neurology and Muscular Diseases Unit, IRCCS Istituto "Giannina Gaslini", Genoa, Italy.

Anna Fassio (A)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.
IRCCS, Ospedale Policlinico San Martino, Genoa, Italy.

Classifications MeSH