Astrocyte-Specific Inhibition of the Primary Cilium Suppresses C3 Expression in Reactive Astrocyte.
Astrocytes
Conditional knockout mouse
LPS
Primary cilium
TRPV4
Journal
Cellular and molecular neurobiology
ISSN: 1573-6830
Titre abrégé: Cell Mol Neurobiol
Pays: United States
ID NLM: 8200709
Informations de publication
Date de publication:
01 Jun 2024
01 Jun 2024
Historique:
received:
02
11
2023
accepted:
21
05
2024
medline:
1
6
2024
pubmed:
1
6
2024
entrez:
1
6
2024
Statut:
epublish
Résumé
C3-positive reactive astrocytes play a neurotoxic role in various neurodegenerative diseases. However, the mechanisms controlling C3-positive reactive astrocyte induction are largely unknown. We found that the length of the primary cilium, a cellular organelle that receives extracellular signals was increased in C3-positive reactive astrocytes, and the loss or shortening of primary cilium decreased the count of C3-positive reactive astrocytes. Pharmacological experiments suggested that Ca
Identifiants
pubmed: 38822888
doi: 10.1007/s10571-024-01482-5
pii: 10.1007/s10571-024-01482-5
doi:
Substances chimiques
Complement C3
0
Lipopolysaccharides
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
48Subventions
Organisme : Japan Society for the Promotion of Science
ID : JP21K06382
Organisme : Japan Society for the Promotion of Science
ID : JP21K15087
Organisme : Japan Society for the Promotion of Science
ID : JP21K06837
Informations de copyright
© 2024. The Author(s).
Références
Abdul-Majeed S, Moloney BC, Nauli SM (2012) Mechanisms regulating cilia growth and cilia function in endothelial cells. Cell Mol Life Sci 69(1):165–173
pubmed: 21671118
doi: 10.1007/s00018-011-0744-0
Alzahrani NA, Bahaidrah KA, Mansouri RA, Alsufiani HM, Alghamdi BS (2022) Investigation of the optimal dose for experimental lipopolysaccharide-induced recognition memory impairment: behavioral and histological studies. J Integr Neurosci 21(2):49
pubmed: 35364637
doi: 10.31083/j.jin2102049
Anvarian Z, Mykytyn K, Mukhopadhyay S, Pedersen LB, Christensen ST (2019) Cellular signalling by primary cilia in development, organ function and disease. Nat Rev Nephrol 15(4):199–219
pubmed: 30733609
pmcid: 6426138
doi: 10.1038/s41581-019-0116-9
Baek H, Shin HJ, Kim JJ, Shin N, Kim S, Yi MH et al (2017) Primary cilia modulate TLR4-mediated inflammatory responses in hippocampal neurons. J Neuroinflammation 14(1):189
pubmed: 28927423
pmcid: 5606072
doi: 10.1186/s12974-017-0958-7
Besschetnova TY, Kolpakova-Hart E, Guan Y, Zhou J, Olsen BR, Shah JV (2010) Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 20(2):182–187
pubmed: 20096584
pmcid: 2990526
doi: 10.1016/j.cub.2009.11.072
Borikar SP, Dongare SI, Danao KR (2022) Reversal of lipopolysaccharide-induced learning and memory deficits by agmatine in mice. Int J Neurosci 132(6):621–632
pubmed: 33089716
doi: 10.1080/00207454.2020.1830086
Brewer KM, Engle SE, Bansal R, Brewer KK, Jasso KR, McIntyre JC, et al (2023) Physiological condition-dependent changes in ciliary GPCR localization in the brain. eNeuro 10(3):ENEURO.0360–22.2023
Douaud G, Lee S, Alfaro-Almagro F, Arthofer C, Wang C, McCarthy P et al (2022) SARS-CoV-2 is associated with changes in brain structure in UK Biobank. Nature 604(7907):697–707
pubmed: 35255491
pmcid: 9046077
doi: 10.1038/s41586-022-04569-5
Fliegauf M, Benzing T, Omran H (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8(11):880–893
pubmed: 17955020
doi: 10.1038/nrm2278
Guemez-Gamboa A, Coufal NG, Gleeson JG (2014) Primary cilia in the developing and mature brain. Neuron 82(3):511–521
pubmed: 24811376
pmcid: 4104280
doi: 10.1016/j.neuron.2014.04.024
Guttenplan KA, Weigel MK, Prakash P, Wijewardhane PR, Hasel P, Rufen-Blanchette U et al (2021) Neurotoxic reactive astrocytes induce cell death via saturated lipids. Nature 599(7883):102–107
pubmed: 34616039
doi: 10.1038/s41586-021-03960-y
Hansen JN, Kaiser F, Klausen C, Stüven B, Chong R, Bönigk W et al (2020) Nanobody-directed targeting of optogenetic tools to study signaling in the primary cilium. Elife. https://doi.org/10.7554/eLife.57907
doi: 10.7554/eLife.57907
pubmed: 33258450
pmcid: 7707840
Haycraft CJ, Zhang Q, Song B, Jackson WS, Detloff PJ, Serra R et al (2007) Intraflagellar transport is essential for endochondral bone formation. Development 134(2):307–316
pubmed: 17166921
doi: 10.1242/dev.02732
Hilgendorf KI, Johnson CT, Jackson PK (2016) The primary cilium as a cellular receiver: organizing ciliary GPCR signaling. Curr Opin Cell Biol 39:84–92
pubmed: 26926036
pmcid: 4828300
doi: 10.1016/j.ceb.2016.02.008
Holmes C, Cunningham C, Zotova E, Woolford J, Dean C, Kerr S et al (2009) Systemic inflammation and disease progression in Alzheimer disease. Neurology 73(10):768–774
pubmed: 19738171
pmcid: 2848584
doi: 10.1212/WNL.0b013e3181b6bb95
Ishikawa H, Thompson J, Yates JR 3rd, Marshall WF (2012) Proteomic analysis of mammalian primary cilia. Curr Biol 22(5):414–419
pubmed: 22326026
pmcid: 3298568
doi: 10.1016/j.cub.2012.01.031
Jha MK, Jo M, Kim JH, Suk K (2019) Microglia-astrocyte crosstalk: an intimate molecular conversation. Neuroscientist 25(3):227–240
pubmed: 29931997
doi: 10.1177/1073858418783959
Ji RR, Berta T, Nedergaard M (2013) Glia and pain: is chronic pain a gliopathy? Pain 154(Suppl 1):S10–S28
pubmed: 23792284
pmcid: 3858488
doi: 10.1016/j.pain.2013.06.022
Jovasevic V, Zhang H, Sananbenesi F, Guedea AL, Soman KV, Wiktorowicz JE et al (2021) Primary cilia are required for the persistence of memory and stabilization of perineuronal nets. Science 24(6):102617
Kadam P, Bhalerao S (2010) Sample size calculation. Int J Ayurveda Res 1(1):55–57. https://doi.org/10.4103/0974-7788.59946
doi: 10.4103/0974-7788.59946
pubmed: 20532100
pmcid: 2876926
Kellendonk C, Tronche F, Monaghan AP, Angrand PO, Stewart F, Schütz G (1996) Regulation of Cre recombinase activity by the synthetic steroid RU 486. Nucleic Acids Res 24(8):1404–1411
pubmed: 8628671
pmcid: 145830
doi: 10.1093/nar/24.8.1404
Kohli P, Höhne M, Jüngst C, Bertsch S, Ebert LK, Schauss AC et al (2017) The ciliary membrane-associated proteome reveals actin-binding proteins as key components of cilia. EMBO Rep 18(9):1521–1535
pubmed: 28710093
pmcid: 5579364
doi: 10.15252/embr.201643846
Liddelow SA, Guttenplan KA, Clarke LE, Bennett FC, Bohlen CJ, Schirmer L et al (2017) Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541(7638):481–487
pubmed: 28099414
pmcid: 5404890
doi: 10.1038/nature21029
Macarelli V, Leventea E, Merkle FT (2023) Regulation of the length of neuronal primary cilia and its potential effects on signalling. Trends Cell Biol S0962-8924(23)00088-0
May EA, Kalocsay M, D’Auriac IG, Schuster PS, Gygi SP, Nachury MV et al (2021) Time-resolved proteomics profiling of the ciliary hedgehog response. J Cell Biol. https://doi.org/10.1083/jcb.202007207
doi: 10.1083/jcb.202007207
pubmed: 34427635
pmcid: 8404468
Mc Fie M, Koneva L, Collins I, Coveney CR, Clube AM, Chanalaris A et al (2020) Ciliary proteins specify the cell inflammatory response by tuning NFκB signalling, independently of primary cilia. J Cell Sci. https://doi.org/10.1242/jcs.239871
doi: 10.1242/jcs.239871
pubmed: 32503942
pmcid: 7358134
Mick DU, Rodrigues RB, Leib RD, Adams CM, Chien AS, Gygi SP et al (2015) Proteomics of primary cilia by proximity labeling. Dev Cell 35(4):497–512
pubmed: 26585297
pmcid: 4662609
doi: 10.1016/j.devcel.2015.10.015
Mill P, Christensen ST, Pedersen LB (2023) Primary cilia as dynamic and diverse signalling hubs in development and disease. Nat Rev Genet 24(7):421–441
pubmed: 37072495
pmcid: 7615029
doi: 10.1038/s41576-023-00587-9
Mishina M, Sakimura K (2007) Conditional gene targeting on the pure C57BL/6 genetic background. Neurosci Res 58(2):105–112
pubmed: 17298852
doi: 10.1016/j.neures.2007.01.004
Muhamad NA, Furukawa S, Yuri S, Toriyama M, Masutani K, Matsumoto C, Itoh S et al (2023) Astrocyte-specific inhibition of primary cilium functions improves cognitive impairment during neuroinflammation by suppressing A1 astrocyte differentiation”. bioRxiv. https://doi.org/10.1101/2023.10.01.560403
doi: 10.1101/2023.10.01.560403
Nachury MV, Mick DU (2019) Establishing and regulating the composition of cilia for signal transduction. Nat Rev Mol Cell Biol 20(7):389–405
pubmed: 30948801
pmcid: 6738346
doi: 10.1038/s41580-019-0116-4
Neary JT, Norenberg MD (1992) Signaling by extracellular ATP: physiological and pathological considerations in neuronal-astrocytic interactions. Prog Brain Res 94:145–151
pubmed: 1337610
doi: 10.1016/S0079-6123(08)61746-X
Ni H, Wang Y, An K, Liu Q, Xu L, Zhu C et al (2019) Crosstalk between NFκB-dependent astrocytic CXCL1 and neuron CXCR2 plays a role in descending pain facilitation. J Neuroinflammation 16(1):1
pubmed: 30606213
pmcid: 6317220
doi: 10.1186/s12974-018-1391-2
Pala R, Alomari N, Nauli SM (2017) Primary cilium-dependent signaling mechanisms. Int J Mol Sci 18(11):2272
pubmed: 29143784
pmcid: 5713242
doi: 10.3390/ijms18112272
Rizaldy D, Toriyama M, Kato H, Fukui R, Fujita F, Nakamura M et al (2021) Increase in primary cilia in the epidermis of patients with atopic dermatitis and psoriasis. Exp Dermatol 30(6):792–803
pubmed: 33455013
doi: 10.1111/exd.14285
Satir P, Christensen ST (2007) Overview of structure and function of mammalian cilia. Annu Rev Physiol 69:377–400
pubmed: 17009929
doi: 10.1146/annurev.physiol.69.040705.141236
Schildge S, Bohrer C, Beck K, Schachtrup C (2013) Isolation and culture of mouse cortical astrocytes. J vis Exp 71:50079
Sheu SH, Upadhyayula S, Dupuy V, Pang S, Deng F, Wan J et al (2022) A serotonergic axon-cilium synapse drives nuclear signaling to alter chromatin accessibility. Cell 185(18):3390-3407.e18
pubmed: 36055200
pmcid: 9789380
doi: 10.1016/j.cell.2022.07.026
Shibasaki K, Ikenaka K, Tamalu F, Tominaga M, Ishizaki Y (2014) A novel subtype of astrocytes expressing TRPV4 (transient receptor potential vanilloid 4) regulates neuronal excitability via release of gliotransmitters. J Biol Chem 289(21):14470–14480
pubmed: 24737318
pmcid: 4031503
doi: 10.1074/jbc.M114.557132
Skrzypczak-Wiercioch A, Sałat K (2022) Lipopolysaccharide-induced model of neuroinflammation: mechanisms of action, research application and future directions for its use. Molecules 27(17):5481
pubmed: 36080253
pmcid: 9457753
doi: 10.3390/molecules27175481
Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35
pubmed: 20012068
doi: 10.1007/s00401-009-0619-8
Squillace S, Salvemini D (2022) Toll-like receptor-mediated neuroinflammation: relevance for cognitive dysfunctions. Trends Pharmacol Sci 43(9):726–739
pubmed: 35753845
pmcid: 9378500
doi: 10.1016/j.tips.2022.05.004
Stella N, Estellés A, Siciliano J, Tencé M, Desagher S, Piomelli D et al (1997) Interleukin-1 enhances the ATP-evoked release of arachidonic acid from mouse astrocytes. J Neurosci 17(9):2939–2946
pubmed: 9096130
pmcid: 6573655
doi: 10.1523/JNEUROSCI.17-09-02939.1997
Toriyama M, Ishii KJ (2021) Primary cilia in the skin: functions in immunity and therapeutic potential. Front Cell Dev Biol 9:621318
pubmed: 33644059
pmcid: 7905053
doi: 10.3389/fcell.2021.621318
Toriyama M, Rizaldy D, Nakamura M, Atsumi Y, Toriyama M, Fujita F et al (2023) Dendritic cell proliferation by primary cilium in atopic dermatitis. Front Mol Biosci 10:1149828
pubmed: 37179569
pmcid: 10169737
doi: 10.3389/fmolb.2023.1149828
Tsyklauri O, Niederlova V, Forsythe E, Prasai A, Drobek A, Kasparek P et al (2021) Bardet-Biedl Syndrome ciliopathy is linked to altered hematopoiesis and dysregulated self-tolerance. EMBO Rep 22(2):e50785
pubmed: 33426789
pmcid: 7857422
doi: 10.15252/embr.202050785
Valente EM, Rosti RO, Gibbs E, Gleeson JG (2014) Primary cilia in neurodevelopmental disorders. Nat Rev Neurol 10(1):27–36
pubmed: 24296655
doi: 10.1038/nrneurol.2013.247
Wang Z, Zhou L, An D, Xu W, Wu C, Sha S et al (2019) TRPV4-induced inflammatory response is involved in neuronal death in pilocarpine model of temporal lobe epilepsy in mice. Cell Death Dis 10(6):386
pubmed: 31097691
pmcid: 6522539
doi: 10.1038/s41419-019-1612-3
Wann AKT, Knight MM (2012) Primary cilia elongation in response to interleukin-1 mediates the inflammatory response. Cell Mol Life Sci 69(17):2967–2977
pubmed: 22481441
pmcid: 3417094
doi: 10.1007/s00018-012-0980-y
Wann AK, Thompson CL, Chapple JP, Knight MM (2013) Interleukin-1β sequesters hypoxia inducible factor 2α to the primary cilium. Cilia 2(1):17
pubmed: 24330727
pmcid: 3886195
doi: 10.1186/2046-2530-2-17
Wann AKT, Chapple JP, Knight MM (2014) The primary cilium influences interleukin-1β-induced NFκB signalling by regulating IKK activity. Cell Signal 26(8):1735–1742
pubmed: 24726893
pmcid: 4064300
doi: 10.1016/j.cellsig.2014.04.004
Wheway G, Nazlamova L, Hancock JT (2018) Signaling through the primary cilium. Front Cell Dev Biol 6:8
pubmed: 29473038
pmcid: 5809511
doi: 10.3389/fcell.2018.00008
Zwirner J, Lier J, Franke H, Hammer N, Matschke J, Trautz F, Tse R, Ondruschka B (2021) GFAP positivity in neurons following traumatic brain injuries. Int J Legal Med 135(6):2323–2333. https://doi.org/10.1007/s00414-021-02568-1
doi: 10.1007/s00414-021-02568-1
pubmed: 34114049
pmcid: 8523453