Primary cilia are required for the persistence of memory and stabilization of perineuronal nets
Open accessAbstract
It is well established that the formation of episodic memories requires multiple hippocampal mechanisms operating on different time scales. Early mechanisms of memory formation (synaptic consolidation) have been extensively characterized. However, delayed mechanisms, which maintain hippocampal activity as memories stabilize in cortical circuits, are not well understood. Here we demonstrate that contrary to the transient expression of early- and delayed-response genes, the expression of cytoskeleton- and extracellular matrix-associated genes remains dynamic even at remote time points. The most profound expression changes clustered around primary cilium-associated and collagen genes. These genes most likely contribute to memory by stabilizing perineuronal nets in the dorsohippocampal CA1 subfield, as revealed by targeted disruptions of the primary cilium or perineuronal nets. The findings show that nonsynaptic, primary cilium-mediated mechanisms are required for the persistence of context memory.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Neuron-specific inhibition of primary cilium formation has no impact on short-term memory but impairs long-term memory retention.
“Furthermore, the neuron-specific inhibition of primary cilium formation showed no impact on short-term memory but resulted in impaired long-term memory retention (Jovasevic et al. 2021).”
From Astrocyte-specific inhibition of the primary cilium suppresses C3 expression in reactive astrocyte (2024) · cites this paper as Jovasevic et al. 2021
The Results (Figure 2 and accompanying text; page unavailable) report that depleting primary cilia in mouse hippocampal CA1 did not impair recent memory tested at day 4, but impaired remote memory at days 21–35. This supports the retention finding, but the paper tested recent versus remote memory, not short-term memory in the usual sense. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function
Fawcett, J. W., Oohashi, T., & Pizzorusso, T. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0196-3 · Cited by 589 · see citing works
Radulovic, J., Rühmann, A., Liepold, T., & Spiess, J. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-12-05016.1999 · Cited by 402 · see citing works
Hylin, M. J., Orsi, S. A., Moore, A. N., & Dash, P. K. (2013) · Learning & Memory · doi:10.1101/lm.030197.112 · Cited by 143 · see citing works
Riga, D., Kramvis, I., Koskinen, M. K., van Bokhoven, P., van der Harst, J. E., Heistek, T. S., Jaap Timmerman, A., van Nierop, P., van der Schors, R. C., Pieneman, A. W., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aai8753 · Cited by 128 · see citing works
Wang, Z., Phan, T., & Storm, D. R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6561-10.2011 · Cited by 100 · see citing works
Mehta, D., Bruenig, D., Carrillo‐Roa, T., Lawford, B., Harvey, W., Morris, C. P., Smith, A. K., Binder, E. B., Young, R. M., & Voisey, J. (2017) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12778 · Cited by 78 · see citing works
Hippocampal and Cortical Primary Cilia Are Required for Aversive Memory in Mice
Berbari, N. F., Malarkey, E. B., Yazdi, S. M. Z. R., McNair, A. D., Kippe, J. M., Croyle, M. J., Kraft, T. W., & Yoder, B. K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106576 · Cited by 69 · see citing works
Rhee, S., Kirschen, G. W., Gu, Y., & Ge, S. (2016) · Scientific Reports · doi:10.1038/srep34370 · Cited by 39 · see citing works
Radulovic, J., Lee, R., & Ortony, A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00259 · Cited by 26 · see citing works
Flagged first, then by citations
Research works printed but not linked: 90
- Abel T. Nguyen P.V. Barad M. Deuel T.A. Kandel E.R. Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory Cell 88 1997 615 626 9054501
- Amador-Arjona A. Elliott J. Miller A. Ginbey A. Pazour G.J. Enikolopov G. Roberts A.J. Terskikh A.V. Primary cilia regulate proliferation of amplifying progenitors in adult Hippocampus: implications for learning and memory J. Neurosci. 31 2011 9933 21734285 PMC3758574
- Banerjee S.B. Gutzeit V.A. Baman J. Aoued H.S. Doshi N.K. Liu R.C. Ressler K.J. Perineuronal nets in the adult sensory cortex are necessary for fear learning Neuron 95 2017 169 179.e163 28648500 PMC5548423
- Barnes P. Kirtley A. Thomas K.L. Quantitatively and qualitatively different cellular processes are engaged in CA1 during the consolidation and reconsolidation of contextual fear memory Hippocampus 22 2012 149 171 21080409
- Basu S. Lamprecht R. The role of actin cytoskeleton in dendritic spines in the maintenance of long-term memory Front. Mol. Neurosci. 11 2018 143 29765302 PMC5938600
- Bezard E. Baufreton J. Owens G. Crossman A.R. Dudek H. Taupignon A. Brotchie J.M. Sonic hedgehog is a neuromodulator in the adult subthalamic nucleus FASEB J. 17 2003 2337 2338 14525941
- Bi A.L. Wang Y. Li B.Q. Wang Q.Q. Ma L. Yu H. Zhao L. Chen Z.Y. Region-specific involvement of actin rearrangement-related synaptic structure alterations in conditioned taste aversion memory Learn. Mem. (Cold Spring Harbor, NY) 17 2010 420 427 20729290
- Breunig J.J. Sarkisian M.R. Arellano J.I. Morozov Y.M. Ayoub A.E. Sojitra S. Wang B. Flavell R.A. Rakic P. Town T. Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling Proc. Natl. Acad. Sci. U S A 105 2008 13127 18728187 PMC2529104
- Chang C.F. Ramaswamy G. Serra R. Depletion of primary cilia in articular chondrocytes results in reduced Gli3 repressor to activator ratio, increased Hedgehog signaling, and symptoms of early osteoarthritis Osteoarthritis Cartilage 20 2012 152 161 22173325 PMC3260404
- Cho J. Yu N.K. Choi J.H. Sim S.E. Kang S.J. Kwak C. Lee S.W. Kim J.I. Choi D.I. Kim V.N. Multiple repressive mechanisms in the hippocampus during memory formation Science 350 2015 82 87 26430118
- Choi H. Tostes R.C. Webb R.C. S-nitrosylation Inhibits protein kinase C-mediated contraction in mouse aorta J. Cardiovasc. Pharmacol. 57 2011 65 71 20966762 PMC3022953
- Coultrap S.J. Bayer K.U. Nitric oxide induces Ca2+-independent activity of the Ca2+/calmodulin-dependent protein kinase II (CaMKII) J. Biol. Chem. 289 2014 19458 19465 24855644 PMC4094056
- Daumas S. Halley H. Francés B. Lassalle J.M. Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions Learn.Mem. (Cold Spring Harbor, NY) 12 2005 375 382 PMC1183255 16027176
- Dhiman M. Zago M.P. Nunez S. Amoroso A. Rementeria H. Dousset P. Nunez Burgos F. Garg N.J. Cardiac-oxidized antigens are targets of immune recognition by antibodies and potential molecular determinants in chagas disease pathogenesis PLoS One 7 2012 e28449 22238578 PMC3251564
- Dityatev A. Rusakov D.A. Molecular signals of plasticity at the tetrapartite synapse Curr. Opin. Neurobiol. 21 2011 353 359 21277196 PMC3368316
- Fanara P. Husted K.H. Selle K. Wong P.Y. Banerjee J. Brandt R. Hellerstein M.K. Changes in microtubule turnover accompany synaptic plasticity and memory formation in response to contextual fear conditioning in mice Neuroscience 168 2010 167 178 20332016
- Federighi G. Traina G. Macchi M. Ciampini C. Bernardi R. Baldi E. Bucherelli C. Brunelli M. Scuri R. Modulation of gene expression in contextual fear conditioning in the rat PLoS One 8 2013 e80037 24278235 PMC3837011
- Fischer A. Sananbenesi F. Schrick C. Spiess J. Radulovic J. Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear J. Neurosci. 24 2004 1962 1966 14985438 PMC6730386
- Frankland P.W. Bontempi B. The organization of recent and remote memories Nat. Rev. Neurosci. 6 2005 119 130 15685217
- Franklin K.B.J. Paxinos G. Paxinos and Franklin’s the Mouse Brain in Stereotaxic Coordinates 2013 Academic Press
- Gao C. Gill M.B. Tronson N.C. Guedea A.L. Guzman Y.F. Huh K.H. Corcoran K.A. Swanson G.T. Radulovic J. Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation Hippocampus 20 2010 1072 1082 19806658 PMC2891656
- Halder R. Hennion M. Vidal R.O. Shomroni O. Rahman R.-U. Rajput A. Centeno T.P. van Bebber F. Capece V. Vizcaino J.C.G. DNA methylation changes in plasticity genes accompany the formation and maintenance of memory Nat. Neurosci. 19 2016 102 110 26656643
- Halder R. Hennion M. Vidal R.O. Shomroni O. Rahman R.U. Rajput A. Centeno T.P. van Bebber F. Capece V. Garcia Vizcaino J.C. DNA methylation changes in plasticity genes accompany the formation and maintenance of memory Nat. Neurosci. 19 2016 102 110 26656643
- Haycraft C.J. Zhang Q. Song B. Jackson W.S. Detloff P.J. Serra R. Yoder B.K. Intraflagellar transport is essential for endochondral bone formation Development 134 2007 307 316 17166921
- Hou Y.Y. Lu B. Li M. Liu Y. Chen J. Chi Z.Q. Liu J.G. Involvement of actin rearrangements within the amygdala and the dorsal hippocampus in aversive memories of drug withdrawal in acute morphine-dependent rats J. Neurosci. 29 2009 12244 12254 19793983 PMC6666133
- Impey S. Smith D.M. Obrietan K. Donahue R. Wade C. Storm D.R. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning Nat. Neurosci. 1 1998 595 601 10196567
- Jaworski J. Kapitein L.C. Gouveia S.M. Dortland B.R. Wulf P.S. Grigoriev I. Camera P. Spangler S.A. Di Stefano P. Demmers J. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity Neuron 61 2009 85 100 19146815
- Ji J. Maren S. Differential roles for hippocampal areas CA1 and CA3 in the contextual encoding and retrieval of extinguished fear Learn. Mem. (Cold Spring Harbor, NY) 15 2008 244 251 PMC2327266 18391185
- Jones M.E. Sillivan S.E. Jamieson S. Rumbaugh G. Miller C.A. microRNA mir-598-3p mediates susceptibility to stress enhancement of remote fear memory Learn. Mem. (Cold Spring Harbor, NY) 26 2019 363 372 PMC6699414 31416909
- Jovasevic V. Corcoran K.A. Leaderbrand K. Yamawaki N. Guedea A.L. Chen H.J. Shepherd G.M. Radulovic J. GABAergic mechanisms regulated by miR-33 encode state-dependent fear Nat. Neurosci. 18 2015 1265 1271 26280760 PMC4880671
- Kelwick R. Desanlis I. Wheeler G.N. Edwards D.R. The ADAMTS (A disintegrin and metalloproteinase with thrombospondin motifs) family Genome Biol. 16 2015 113 26025392 PMC4448532
- Kim I.H. Wang H. Soderling S.H. Yasuda R. Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall eLife 3 2014 e02839 PMC4115656 25006034
- Koskinen M.K. van Mourik Y. Smit A.B. Riga D. Spijker S. From stress to depression: development of extracellular matrix-dependent cognitive impairment following social stress Sci. Rep. 10 2020 17308 33057053 PMC7560730
- Kuan P.F. Waszczuk M.A. Kotov R. Clouston S. Yang X. Singh P.K. Glenn S.T. Cortes Gomez E. Wang J. Bromet E. Gene expression associated with PTSD in World Trade Center responders: an RNA sequencing study Transl Psychiatry 7 2017 1297 29249826 PMC5802695
- Kypri E. Christodoulou A. Maimaris G. Lethan M. Markaki M. Lysandrou C. Lederer C.W. Tavernarakis N. Geimer S. Pedersen L.B. The nucleotide-binding proteins Nubp1 and Nubp2 are negative regulators of ciliogenesis Cell Mol. Life Sci. 71 2014 517 538 23807208 PMC11113914
- Lee I. Kesner R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning Hippocampus 14 2004 301 310 15132429
- Levenson J.M. Choi S. Lee S.Y. Cao Y.A. Ahn H.J. Worley K.C. Pizzi M. Liou H.C. Sweatt J.D. A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel J. Neurosci. 24 2004 3933 3943 15102909 PMC6729420
- Levy A.D. Omar M.H. Koleske A.J. Extracellular matrix control of dendritic spine and synapse structure and plasticity in adulthood Front. Neuroanat. 8 2014 116 25368556 PMC4202714
- Li H. Handsaker B. Wysoker A. Fennell T. Ruan J. Homer N. Marth G. Abecasis G. Durbin R. The sequence alignment/map format and SAMtools Bioinformatics 25 2009 2078 2079 19505943 PMC2723002
- Lienhard M. Grimm C. Morkel M. Herwig R. Chavez L. MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments Bioinformatics (Oxford, England) 30 2014 284 286 PMC3892689 24227674
- Louvi A. Grove E.A. Cilia in the CNS: the quiet organelle claims center stage Neuron 69 2011 1046 1060 21435552 PMC3070490
- Malicki J.J. Johnson C.A. The cilium: cellular antenna and central processing unit Trends Cell Biol. 27 2017 126 140 27634431 PMC5278183
- Matus A. Actin-based plasticity in dendritic spines Science 290 2000 754 758 11052932
- Mei B. Li C. Dong S. Jiang C.H. Wang H. Hu Y. Distinct gene expression profiles in hippocampus and amygdala after fear conditioning Brain Res. Bull. 67 2005 1 12 16140156
- Meyer M.A.A. Corcoran K.A. Chen H.J. Gallego S. Li G. Tiruveedhula V.V. Cook J.M. Radulovic J. Neurobiological correlates of state-dependent context fear Learn. Mem. (Cold Spring Harbor, NY) 24 2017 385 391 PMC5580530 28814463
- Mizuno K. Jeffries A.R. Abel T. Giese K.P. Long-lasting transcription in hippocampal area CA1 after contextual fear conditioning Neurobiol. Learn. Mem. 172 2020 107250 32422278 PMC7325482
- Murakami T. Murakami T. Su W.D. Ohtsuka A. Abe K. Ninomiya Y. Perineuronal nets of proteoglycans in the adult mouse brain are digested by collagenase Arch. Histol. Cytol. 62 1999 199 204 10399544
- Nelson B.S. Witty C.F. Williamson E.A. Daniel J.M. A role for hippocampal actin rearrangement in object placement memory in female rats Neurobiol. Learn. Mem. 98 2012 284 290 23010136
- Nestler E.J. Greengard P. Protein phosphorylation is of fundamental importance in biological regulation Siegel G.J. Agranoff B.W. Albers R.W. Fisher S.K. Uhler M.D. Basic Neurochemistry: Molecular, Cellular and Medical Aspects 1999 Lippincott-Raven
- Nguyen P.T. Dorman L.C. Pan S. Vainchtein I.D. Han R.T. Nakao-Inoue H. Taloma S.E. Barron J.J. Molofsky A.B. Kheirbek M.A. Microglial remodeling of the extracellular matrix promotes synapse plasticity Cell 182 2020 388 403.e315 32615087 PMC7497728
- Noda K. Kitami M. Kitami K. Kaku M. Komatsu Y. Canonical and noncanonical intraflagellar transport regulates craniofacial skeletal development Proc. Natl. Acad. Sci. U S A 113 2016 E2589 E2597 27118846 PMC4868419
- Novak U. Kaye A.H. Extracellular matrix and the brain: components and function J. Clin.Neurosci. 7 2000 280 290 10938601
- Parato J. Shen H. Smith S.S. alpha4betadelta GABAA receptors trigger synaptic pruning and reduce dendritic length of female mouse CA3 hippocampal pyramidal cells at puberty Neuroscience 398 2019 23 36 30496825 PMC6411036
- Peixoto L.L. Wimmer M.E. Poplawski S.G. Tudor J.C. Kenworthy C.A. Liu S. Mizuno K. Garcia B.A. Zhang N.R. Giese K. Memory acquisition and retrieval impact different epigenetic processes that regulate gene expression BMC Genomics 16 Suppl 5 2015 S5 PMC4460846 26040834
- Petrova R. Joyner A.L. Roles for Hedgehog signaling in adult organ homeostasis and repair Development (Cambridge, England) 141 2014 3445 3457 PMC4197719 25183867
- Poplawski S.G. Peixoto L. Porcari G.S. Wimmer M.E. McNally A.G. Mizuno K. Giese K.P. Chatterjee S. Koberstein J.N. Risso D. Contextual fear conditioning induces differential alternative splicing Neurobiol. Learn. Mem. 134 Pt B 2016 221 235 27451143 PMC5028328
- Poulos A.M. Mehta N. Lu B. Amir D. Livingston B. Santarelli A. Zhuravka I. Fanselow M.S. Conditioning- and time-dependent increases in context fear and generalization Learn. Mem. (Cold Spring Harbor, NY) 23 2016 379 385 PMC4918784 27317198
- Pushpakom S. Iorio F. Eyers P.A. Escott K.J. Hopper S. Wells A. Doig A. Guilliams T. Latimer J. McNamee C. Drug repurposing: progress, challenges and recommendations Nat. Rev. Drug Discov. 18 2018 41 58 30310233
- Radulovic J. Tronson N.C. Molecular specificity of multiple hippocampal processes governing fear extinction Rev. Neurosci. 21 2010 1 17 20458884 PMC2922903
- Rao-Ruiz P. Couey J.J. Marcelo I.M. Bouwkamp C.G. Slump D.E. Matos M.R. van der Loo R.J. Martins G.J. van den Hout M. van I.W.F. Engram-specific transcriptome profiling of contextual memory consolidation Nat. Commun. 10 2019 2232 31110186 PMC6527697
- Reichelt A.C. Hare D.J. Bussey T.J. Saksida L.M. Perineuronal nets: plasticity, protection, and therapeutic potential Trends Neurosci. 42 2019 458 470 31174916
- Remondes M. Schuman E.M. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory Nature 431 2004 699 703 15470431
- Revest J.M. Kaouane N. Mondin M. Le Roux A. Rouge-Pont F. Vallee M. Barik J. Tronche F. Desmedt A. Piazza P.V. The enhancement of stress-related memory by glucocorticoids depends on synapsin-Ia/Ib Mol. Psychiatry 15 2010 1140 1151 1125 PMC2990189 20368707
- Rockel J.S. Yu C. Whetstone H. Craft A.M. Reilly K. Ma H. Tsushima H. Puviindran V. Al-Jazrawe M. Keller G.M. Hedgehog inhibits β-catenin activity in synovial joint development and osteoarthritis J. Clin. Invest. 126 2016 1649 1663 27018594 PMC4855923
- Romberg C. Yang S. Melani R. Andrews M.R. Horner A.E. Spillantini M.G. Bussey T.J. Fawcett J.W. Pizzorusso T. Saksida L.M. Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex J. Neurosci. 33 2013 7057 7065 23595763 PMC3655688
- Satir P. Satir B.H. The conserved ancestral signaling pathway from cilium to nucleus J. Cell Sci. 132 2019 31375541
- Schlessinger J. Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225 11057895
- Sethi M.K. Zaia J. Extracellular matrix proteomics in schizophrenia and Alzheimer's disease Anal. Bioanal. Chem. 409 2017 379 394 27601046 PMC5203946
- Shumyatsky G.P. Malleret G. Shin R.M. Takizawa S. Tully K. Tsvetkov E. Zakharenko S.S. Joseph J. Vronskaya S. Yin D. stathmin, a gene enriched in the amygdala, controls both learned and innate fear Cell 123 2005 697 709 16286011
- Sillivan S.E. Joseph N.F. Jamieson S. King M.L. Chevere-Torres I. Fuentes I. Shumyatsky G.P. Brantley A.F. Rumbaugh G. Miller C.A. Susceptibility and resilience to posttraumatic stress disorder-like behaviors in inbred mice Biol. Psychiatry 82 2017 924 933 28778658 PMC5683920
- Smits P. Bolton A.D. Funari V. Hong M. Boyden E.D. Lu L. Manning D.K. Dwyer N.D. Moran J.L. Prysak M. Lethal skeletal dysplasia in mice and humans lacking the golgin GMAP-210 N. Engl. J. Med. 362 2010 206 216 20089971 PMC3108191
- Su J. Cole J. Fox M.A. Loss of interneuron-derived collagen XIX leads to a reduction in perineuronal nets in the mammalian telencephalon ASN Neuro 9 2017 1759091416689020 PMC5298462 28090790
- Szklarczyk D. Gable A.L. Lyon D. Junge A. Wyder S. Huerta-Cepas J. Simonovic M. Doncheva N.T. Morris J.H. Bork P. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets Nucleic Acids Res. 47 2019 D607 D613 30476243 PMC6323986
- Tada T. Sheng M. Molecular mechanisms of dendritic spine morphogenesis Curr. Opin. Neurobiol. 16 2006 95 101 16361095
- Thompson E.H. Lensjø K.K. Wigestrand M.B. Malthe-Sørenssen A. Hafting T. Fyhn M. Removal of perineuronal nets disrupts recall of a remote fear memory Proc. Natl. Acad. Sci. U S A 115 2018 607 612 29279411 PMC5776974
- Tonegawa S. Morrissey M.D. Kitamura T. The role of engram cells in the systems consolidation of memory Nat. Rev. Neurosci. 19 2018 485 498 29970909
- Toyama B.H. Hetzer M.W. Protein homeostasis: live long, won't prosper Nat. Rev. Mol.Cell Biol. 14 2013 55 61 23258296 PMC3570024
- Tsien R.Y. Very long-term memories may be stored in the pattern of holes in the perineuronal net Proc. Natl. Acad. Sci. U S A 110 2013 12456 12461 23832785 PMC3725115
- Uchida S. Martel G. Pavlowsky A. Takizawa S. Hevi C. Watanabe Y. Kandel E.R. Alarcon J.M. Shumyatsky G.P. Learning-induced and stathmin-dependent changes in microtubule stability are critical for memory and disrupted in ageing Nat. Commun. 5 2014 4389 25007915 PMC4137320
- Uddin B. Partscht P. Chen N.P. Neuner A. Weiss M. Hardt R. Jafarpour A. Hessling B. Ruppert T. Lorenz H. The human phosphatase CDC14A modulates primary cilium length by regulating centrosomal actin nucleation EMBO Rep. 20 2019 e46544 30467237 PMC6322383
- van Marle H. PTSD as a memory disorder Eur. J.Psychotraumatol. 6 2015 10.3402/ejpt.v3406.27633 · DOI
- Warde-Farley D. Donaldson S.L. Comes O. Zuberi K. Badrawi R. Chao P. Franz M. Grouios C. Kazi F. Lopes C.T. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function Nucleic Acids Res. 38 2010 W214 W220 20576703 PMC2896186
- Wen J.J. Zago M.P. Nunez S. Gupta S. Burgos F.N. Garg N.J. Serum proteomic signature of human chagasic patients for the identification of novel potential protein biomarkers of disease Mol. Cell. Proteomics 11 2012 435 452 22543060 PMC3412973
- Wheway G. Nazlamova L. Hancock J.T. Signaling through the primary cilium Front. Cell Dev. Biol. 6 2018 8 29473038 PMC5809511
- Wiktorowicz J.E. Chowdhury I.H. Stafford S. Choudhuri S. Dey N. Garg N.J. Integrated functional analysis of the nuclear proteome of classically and alternatively activated macrophages Mediators Inflamm. 2019 2019 19 PMC6515079 31182931
- Wiktorowicz J.E. Stafford S.J. Garg N.J. Protein cysteinyl-S-nitrosylation: analysis and quantification Methods Enzymol. 586 2017 1 14 28137558
- Wingett S.W. Andrews S. FastQ Screen: a tool for multi-genome mapping and quality control F1000Res. 7 2018 1338 30254741 PMC6124377
- Yao P.J. Petralia R.S. Mattson M.P. Sonic hedgehog signaling and hippocampal neuroplasticity Trends Neurosci. 39 2016 840 850 27865563 PMC5148655
- Yasukawa T. Tokunaga E. Ota H. Sugita H. Martyn J.A. Kaneki M. S-nitrosylation-dependent inactivation of Akt/protein kinase B in insulin resistance J. Biol. Chem. 280 2005 7511 7518 15632167
- Zago M.P. Wiktorowicz J.E. Spratt H. Koo S.J. Barrientos N. Nunez Burgos A. Nunez Burgos J. Iniguez F. Botelli V. Leon de la Fuente R. Potential utility of protein targets of cysteine-S-nitrosylation in identifying clinical disease status in human chagas disease Front. Microbiol. 9 2018 3320 30697201 PMC6340995
Cited by
Sorted by citations
A primary cilia-autophagy axis in hippocampal neurons is essential to maintain cognitive resilience
Rivagorda, M., Romeo-Guitart, D., Blanchet, V., Mailliet, F., Boitez, V., Barry, N., Milunov, D., Siopi, E., Goudin, N., Moriceau, S., et al. (2025) · Nature Aging · doi:10.1038/s43587-024-00791-0 · Cited by 24 · see citing works
Astrocyte-specific inhibition of the primary cilium suppresses C3 expression in reactive astrocyte
Muhamad, N. A., Masutani, K., Furukawa, S., Yuri, S., Toriyama, M., Matsumoto, C., Itoh, S., Shinagawa, Y., Isotani, A., Toriyama, M., et al. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01482-5 · Cited by 8 · see citing works
Temporal ablation of the ciliary protein IFT88 alters normal brainwave patterns
Strobel, M. R., Zhou, Y., Qiu, L., Hofer, A. M., & Chen, X. (2025) · Scientific Reports · doi:10.1038/s41598-024-83432-1 · Cited by 9 · see citing works
- Authors
- Jovasevic, V., Zhang, H., Sananbenesi, F., Guedea, A. L., Soman, K. V., Wiktorowicz, J. E., Fischer, A., & Radulovic, J.
- Affiliations
- Northwestern University (US)
- Albert Einstein College of Medicine (US)
- German Center for Neurodegenerative Diseases (DE)
- The University of Texas Medical Branch at Galveston (US)
- Corresponding author
- Jovasevic, Vladimir
- ORCID
- Venue
- iScience
- Publisher
- Elsevier BV
- Published
- 2021-06
- Volume
- 24
- Issue
- 6
- Pages
- 102617
- ISSN
- 2589-0042 (ISSN-L)
- PMC
- PMC8185192
- OpenAlex
- W3165518847
- Cited by
- 32
- References
- 9
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 9 · 2023: 2 · 2022: 2 · 2021: 1
- FWCI
- 1.83
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- iScience (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DZNE Pub (submittedVersion, cc-by-nc-nd)
- Funders
- National Institute of Mental Health (MH078064)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- primary cilia, perineuronal nets, memory consolidation, episodic memory, hippocampus, CA1, contextual memory, extracellular matrix, collagen genes, cytoskeletal genes, gene expression dynamics, memory stabilization
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review