Cited by 75

The DOI matches its Crossref record; 26 of the 26 references it cites were found in a registry or an index.

Microglial over-pruning of synapses during development in autism-associated SCN2A-deficient mice and human cerebral organoids

Wu, Jiaxiang, Zhang, Jingliang, Chen, Xiaoling, Wettschurack, Kyle, Que, Zhefu, Deming, Brody A., Olivero-Acosta, Maria I., Cui, Ningren, Eaton, Muriel, Zhao, Yuanrui, Li, Sophia M., Suzuki, Matthew, Chen, Ian, Xiao, Tiange, Halurkar, Manasi S., Mandal, Purba, Yuan, Chongli, Xu, Ranjie, Koss, Wendy A., Du, Dongshu, Chen, Fuxue, Wu, Long-jun, Yang, Yang·2024·Molecular Psychiatry

Published version of a preprint

Overview

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41380-024-02518-4

Cites

26 of 26 references verified0 citation errors · 0 not checkable

Statistics

Figures

Figure 1
Figure 1 CC-BY · From the PDF
Figure 2
Figure 2 CC-BY · From the PDF
Figure 3
Figure 3 CC-BY · From the PDF
Figure 4
Figure 4 CC-BY · From the PDF
Figure 5
Figure 5 CC-BY · From the PDF
Figure 6
Figure 6 CC-BY · From the PDF

Verification

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.

A few free checks a day · papers already verified open instantly · results are public

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 26 references

Research works printed but not linked: 78

  1. Rolland T, Cliquet F, Anney RJL, Moreau C, Traut N, Mathieu A, et al. Phenotypic effects of genetic variants associated with autism. Nat Med. 2023;29:1671–80. · DOI
  2. Qin Y, Kang J, Jiao Z, Wang Y, Wang J, Wang H, et al. Polygenic risk for autism spectrum disorder affects left amygdala activity and negative emotion in schizophrenia. Transl Psychiatry. 2020;10:322. · DOI
  3. Sanders SJ, Murtha MT, Gupta AR, Murdoch JD, Raubeson MJ, Willsey AJ, et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature. 2012;485:237–41. · DOI · Paper page
  4. Gazina EV, Leaw BT, Richards KL, Wimmer VC, Kim TH, Aumann TD, et al. 'Neonatal’ Nav1.2 reduces neuronal excitability and affects seizure susceptibility and behaviour. Hum Mol Genet. 2015;24:1457–68. · DOI · Paper page
  5. Sanders SJ, He X, Willsey AJ, Ercan-Sencicek AG, Samocha KE, Cicek AE, et al. Insights into autism spectrum disorder genomic architecture and biology from 71 risk loci. Neuron. 2015;87:1215–33. · DOI · Paper page
  6. Miyamoto H, Tatsukawa T, Shimohata A, Yamagata T, Suzuki T, Amano K, et al. Impaired cortico-striatal excitatory transmission triggers epilepsy. Nat Commun. 2019;10:1917. · DOI
  7. Middleton SJ, Kneller EM, Chen S, Ogiwara I, Montal M, Yamakawa K, et al. Altered hippocampal replay is associated with memory impairment in mice heterozygous for the Scn2a gene. Nat Neurosci. 2018;21:996–1003. · DOI
  8. Tatsukawa T, Raveau M, Ogiwara I, Hattori S, Miyamoto H, Mazaki E, et al. Scn2a haploinsufficient mice display a spectrum of phenotypes affecting anxiety, sociability, memory flexibility and ampakine CX516 rescues their hyperactivity. Mol Autism. 2019;10:15. · DOI
  9. Eaton M, Zhang J, Ma Z, Park AC, Lietzke E, Romero CM, et al. Generation and basic characterization of a gene-trap knockout mouse model of Scn2a with a substantial reduction of voltage-gated sodium channel Na(v) 1.2 expression. Genes Brain Behav. 2021;20:e12725. · DOI
  10. Ma Z, Eaton M, Liu Y, Zhang J, Chen X, Tu X, et al. Deficiency of autism-related Scn2a gene in mice disrupts sleep patterns and circadian rhythms. Neurobiol Dis. 2022;168:105690. · DOI
  11. Suzuki K, Sugihara G, Ouchi Y, Nakamura K, Futatsubashi M, Takebayashi K, et al. Microglial activation in young adults with autism spectrum disorder. JAMA Psychiatry. 2013;70:49–58. · DOI · Paper page
  12. Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, et al. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci. 2014;17:400–6. · DOI · Paper page
  13. Andoh M, Shibata K, Okamoto K, Onodera J, Morishita K, Miura Y, et al. Exercise reverses behavioral and synaptic abnormalities after maternal inflammation. Cell Rep. 2019;27:2817–25.e2815. · DOI
  14. Kim HJ, Cho MH, Shim WH, Kim JK, Jeon EY, Kim DH, et al. Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects. Mol Psychiatry. 2017;22:1576–84. · DOI · Paper page
  15. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR 3rd, Lafaille JJ, et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 2013;155:1596–609. · DOI · Paper page
  16. Jawaid S, Kidd GJ, Wang J, Swetlik C, Dutta R, Trapp BD. Alterations in CA1 hippocampal synapses in a mouse model of fragile X syndrome. Glia. 2018;66:789–800. · DOI
  17. Schafer DP, Heller CT, Gunner G, Heller M, Gordon C, Hammond T, et al. Microglia contribute to circuit defects in Mecp2 null mice independent of microglia-specific loss of Mecp2 expression. Elife. 2016;5:e15224. · DOI · Paper page
  18. Arsenault J, Hooper AWM, Gholizadeh S, Kong T, Pacey LK, Koxhioni E, et al. Interregulation between fragile X mental retardation protein and methyl CpG binding protein 2 in the mouse posterior cerebral cortex. Hum Mol Genet. 2021;29:3744–56. · DOI
  19. Bach S, Shovlin S, Moriarty M, Bardoni B, Tropea D. Rett syndrome and fragile X syndrome: different etiology with common molecular dysfunctions. Front Cell Neurosci. 2021;15:764761. · DOI
  20. Black JA, Liu S, Waxman SG. Sodium channel activity modulates multiple functions in microglia. Glia. 2009;57:1072–81. · DOI
  21. Lai MC, Lombardo MV, Baron-Cohen S. Autism. Lancet. 2014;383:896–910. · DOI · Paper page
  22. Kraeuter AK, Guest PC, Sarnyai Z. The Y-maze for assessment of spatial working and reference memory in mice. Methods Mol Biol. 2019;1916:105–11. · DOI
  23. Nisar S, Bhat AA, Masoodi T, Hashem S, Akhtar S, Ali TA, et al. Genetics of glutamate and its receptors in autism spectrum disorder. Mol Psychiatry. 2022;27:2380–92. · DOI
  24. Spratt PWE, Ben-Shalom R, Keeshen CM, Burke KJ Jr, Clarkson RL, Sanders SJ, et al. The autism-associated gene Scn2a contributes to dendritic excitability and synaptic function in the prefrontal cortex. Neuron. 2019;103:673–85.e675. · DOI · Paper page
  25. Shin W, Kweon H, Kang R, Kim D, Kim K, Kang M, et al. Scn2a haploinsufficiency in mice suppresses hippocampal neuronal excitability, excitatory synaptic drive, and long-term potentiation, and spatial learning and memory. Front Mol Neurosci. 2019;12:145. · DOI
  26. Zhang J, Chen X, Eaton M, Wu J, Ma Z, Lai S, et al. Severe deficiency of the voltage-gated sodium channel Na(V)1.2 elevates neuronal excitability in adult mice. Cell Rep. 2021;36:109495. · DOI
  27. Posfai B, Cserep C, Orsolits B, Denes A. New insights into microglia-neuron interactions: a neuron’s perspective. Neuroscience. 2019;405:103–17. · DOI · Paper page
  28. Choudhury ME, Miyanishi K, Takeda H, Islam A, Matsuoka N, Kubo M, et al. Phagocytic elimination of synapses by microglia during sleep. Glia. 2020;68:44–59. · DOI
  29. Matta SM, Hill-Yardin EL, Crack PJ. The influence of neuroinflammation in autism spectrum disorder. Brain Behav Immun. 2019;79:75–90. · DOI
  30. Andoh M, Koyama R. Microglia regulate synaptic development and plasticity. Dev Neurobiol. 2021;81:568–90. · DOI
  31. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, et al. The classical complement cascade mediates CNS synapse elimination. Cell. 2007;131:1164–78. · DOI · Paper page
  32. Wallace J, Lord J, Dissing-Olesen L, Stevens B, Murthy VN. Microglial depletion disrupts normal functional development of adult-born neurons in the olfactory bulb. Elife. 2020;9:e50531. · DOI
  33. Nguyen PT, Dorman LC, Pan S, Vainchtein ID, Han RT, Nakao-Inoue H, et al. Microglial remodeling of the extracellular matrix promotes synapse plasticity. Cell. 2020;182:388–403 e315. · DOI · Paper page
  34. Ben-Shalom R, Keeshen CM, Berrios KN, An JY, Sanders SJ, Bender KJ. Opposing effects on Na(V)1.2 function underlie differences between SCN2A variants observed in individuals with autism spectrum disorder or infantile seizures. Biol Psychiatry. 2017;82:224–32. · DOI · Paper page
  35. Ramos DM, Skarnes WC, Singleton AB, Cookson MR, Ward ME. Tackling neurodegenerative diseases with genomic engineering: a new stem cell initiative from the NIH. Neuron. 2021;109:1080–3. · DOI · Paper page
  36. Pantazis CB, Yang A, Lara E, McDonough JA, Blauwendraat C, Peng L, et al. A reference human induced pluripotent stem cell line for large-scale collaborative studies. Cell Stem Cell. 2022;29:1685–702 e1622. · DOI · Paper page
  37. Que Z, Olivero-Acosta MI, Zhang J, Eaton M, Tukker AM, Chen X, et al. Hyperexcitability and pharmacological responsiveness of cortical neurons derived from human iPSCs carrying epilepsy-associated sodium channel Nav1.2-L1342P genetic variant. J Neurosci. 2021;41:10194–208. · DOI
  38. Skarnes WC, Pellegrino E, McDonough JA. Improving homology-directed repair efficiency in human stem cells. Methods. 2019;164-165:18–28. · DOI
  39. Thion MS, Ginhoux F, Garel S. Microglia and early brain development: an intimate journey. Science. 2018;362:185–9. · DOI
  40. Tseng CJ, McDougle CJ, Hooker JM, Zurcher NR. Epigenetics of autism spectrum disorder: histone deacetylases. Biol Psychiatry. 2022;91:922–33. · DOI
  41. Hegarty JP 2nd, Pegoraro LFL, Lazzeroni LC, Raman MM, Hallmayer JF, Monterrey JC, et al. Genetic and environmental influences on structural brain measures in twins with autism spectrum disorder. Mol Psychiatry. 2020;25:2556–66. · DOI
  42. Spratt PWE, Alexander RPD, Ben-Shalom R, Sahagun A, Kyoung H, Keeshen CM, et al. Paradoxical hyperexcitability from Na(V)1.2 sodium channel loss in neocortical pyramidal cells. Cell Rep. 2021;36:109483. · DOI
  43. Ogiwara I, Miyamoto H, Tatsukawa T, Yamagata T, Nakayama T, Atapour N, et al. Nav1.2 haplodeficiency in excitatory neurons causes absence-like seizures in mice. Commun Biol. 2018;1:96. · DOI
  44. Witcher KG, Bray CE, Chunchai T, Zhao F, O’Neil SM, Gordillo AJ, et al. Traumatic brain injury causes chronic cortical inflammation and neuronal dysfunction mediated by microglia. J Neurosci. 2021;41:1597–616. · DOI · Paper page
  45. Hui CW, St-Pierre A, El Hajj H, Remy Y, Hebert SS, Luheshi GN, et al. Prenatal immune challenge in mice leads to partly sex-dependent behavioral, microglial, and molecular abnormalities associated with schizophrenia. Front Mol Neurosci. 2018;11:13. · DOI
  46. Sarn N, Jaini R, Thacker S, Lee H, Dutta R, Eng C. Cytoplasmic-predominant Pten increases microglial activation and synaptic pruning in a murine model with autism-like phenotype. Mol Psychiatry. 2021;26:1458–71. · DOI
  47. Bennett FC, Molofsky AV. The immune system and psychiatric disease: a basic science perspective. Clin Exp Immunol. 2019;197:294–307. · DOI
  48. Saitoh BY, Tanaka E, Yamamoto N, Kruining DV, Iinuma K, Nakamuta Y, et al. Early postnatal allergic airway inflammation induces dystrophic microglia leading to excitatory postsynaptic surplus and autism-like behavior. Brain Behav Immun. 2021;95:362–80. · DOI · Paper page
  49. Williams JA, Burgess S, Suckling J, Lalousis PA, Batool F, Griffiths SL, et al. Inflammation and brain structure in schizophrenia and other neuropsychiatric disorders: a Mendelian randomization study. JAMA Psychiatry. 2022;79:498–507. · DOI
  50. Onore CE, Schwartzer JJ, Careaga M, Berman RF, Ashwood P. Maternal immune activation leads to activated inflammatory macrophages in offspring. Brain Behav Immun. 2014;38:220–6. · DOI · Paper page
  51. Cieslik M, Gassowska-Dobrowolska M, Jesko H, Czapski GA, Wilkaniec A, Zawadzka A, et al. Maternal immune activation induces neuroinflammation and cortical synaptic deficits in the adolescent rat offspring. Int J Mol Sci. 2020;21:4097. · DOI
  52. Werneburg S, Jung J, Kunjamma RB, Ha SK, Luciano NJ, Willis CM, et al. Targeted complement inhibition at synapses prevents microglial synaptic engulfment and synapse loss in demyelinating disease. Immunity. 2020;52:167–82 e167. · DOI · Paper page
  53. Weinhard L, di Bartolomei G, Bolasco G, Machado P, Schieber NL, Neniskyte U, et al. Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction. Nat Commun. 2018;9:1228. · DOI · Paper page
  54. Cong Q, Soteros BM, Wollet M, Kim JH, Sia GM. The endogenous neuronal complement inhibitor SRPX2 protects against complement-mediated synapse elimination during development. Nat Neurosci. 2020;23:1067–78. · DOI
  55. Hammond JW, Bellizzi MJ, Ware C, Qiu WQ, Saminathan P, Li H, et al. Complement-dependent synapse loss and microgliosis in a mouse model of multiple sclerosis. Brain Behav Immun. 2020;87:739–50. · DOI
  56. Cao P, Chen C, Liu A, Shan Q, Zhu X, Jia C, et al. Early-life inflammation promotes depressive symptoms in adolescence via microglial engulfment of dendritic spines. Neuron. 2021;109:2573–89.e2579. · DOI
  57. Xu ZX, Kim GH, Tan JW, Riso AE, Sun Y, Xu EY, et al. Elevated protein synthesis in microglia causes autism-like synaptic and behavioral aberrations. Nat Commun. 2020;11:1797. · DOI
  58. Ding X, Wang J, Huang M, Chen Z, Liu J, Zhang Q, et al. Loss of microglial SIRPalpha promotes synaptic pruning in preclinical models of neurodegeneration. Nat Commun. 2021;12:2030. · DOI · Paper page
  59. Paolicelli RC, Jawaid A, Henstridge CM, Valeri A, Merlini M, Robinson JL, et al. TDP-43 depletion in microglia promotes amyloid clearance but also induces synapse loss. Neuron. 2017;95:297–308.e296. · DOI · Paper page
  60. Druart M, Le Magueresse C. Emerging roles of complement in psychiatric disorders. Front Psychiatry. 2019;10:573. · DOI
  61. Wei Y, Chen T, Bosco DB, Xie M, Zheng J, Dheer A, et al. The complement C3-C3aR pathway mediates microglia–astrocyte interaction following status epilepticus. Glia. 2021;69:1155–69. · DOI
  62. Wu J, Bie B, Foss JF, Naguib M. Amyloid fibril-induced astrocytic glutamate transporter disruption contributes to complement C1q-mediated microglial pruning of glutamatergic synapses. Mol Neurobiol. 2020;57:2290–2300. · DOI
  63. De Schepper S, Crowley G, Hong S. Understanding microglial diversity and implications for neuronal function in health and disease. Dev Neurobiol. 2021;81:507–23. · DOI
  64. Lehrman EK, Wilton DK, Litvina EY, Welsh CA, Chang ST, Frouin A, et al. CD47 protects synapses from excess microglia-mediated pruning during development. Neuron. 2018;100:120–34.e126. · DOI
  65. Li T, Chiou B, Gilman CK, Luo R, Koshi T, Yu D, et al. A splicing isoform of GPR56 mediates microglial synaptic refinement via phosphatidylserine binding. EMBO J. 2020;39:e104136. · DOI
  66. Scott-Hewitt N, Perrucci F, Morini R, Erreni M, Mahoney M, Witkowska A, et al. Local externalization of phosphatidylserine mediates developmental synaptic pruning by microglia. EMBO J. 2020;39:e105380. · DOI
  67. Eyo U, Molofsky AV. Defining microglial-synapse interactions. Science. 2023;381:1155–6. · DOI
  68. Kasahara Y, Koyama R, Ikegaya Y. Depth and time-dependent heterogeneity of microglia in mouse hippocampal slice cultures. Neurosci Res. 2016;111:64–69. · DOI
  69. Zhang W, Jiang J, Xu Z, Yan H, Tang B, Liu C, et al. Microglia-containing human brain organoids for the study of brain development and pathology. Mol Psychiatry. 2023;28:96–107. · DOI
  70. Ginhoux F, Garel S. The mysterious origins of microglia. Nat Neurosci. 2018;21:897–9. · DOI
  71. Abud EM, Ramirez RN, Martinez ES, Healy LM, Nguyen CHH, Newman SA, et al. iPSC-derived human microglia-like cells to study neurological diseases. Neuron. 2017;94:278–93.e279. · DOI · Paper page
  72. Sabate-Soler S, Nickels SL, Saraiva C, Berger E, Dubonyte U, Barmpa K, et al. Microglia integration into human midbrain organoids leads to increased neuronal maturation and functionality. Glia. 2022;70:1267–88. · DOI
  73. Xu R, Boreland AJ, Li X, Erickson C, Jin M, Atkins C, et al. Developing human pluripotent stem cell-based cerebral organoids with a controllable microglia ratio for modeling brain development and pathology. Stem Cell Rep. 2021;16:1923–37. · DOI
  74. Cakir B, Xiang Y, Tanaka Y, Kural MH, Parent M, Kang YJ, et al. Engineering of human brain organoids with a functional vascular-like system. Nat Methods. 2019;16:1169–75. · DOI
  75. Skarnes WC, von Melchner H, Wurst W, Hicks G, Nord AS, Cox T, et al. A public gene trap resource for mouse functional genomics. Nat Genet. 2004;36:543–4. · DOI
  76. Zhang J, Zhang C, Chen X, Wang B, Ma W, Yang Y, et al. PKA-RIIbeta autophosphorylation modulates PKA activity and seizure phenotypes in mice. Commun Biol. 2021;4:263. · DOI
  77. Miura Y, Li MY, Revah O, Yoon SJ, Narazaki G, Pasca SP. Engineering brain assembloids to interrogate human neural circuits. Nat Protoc. 2022;17:15–35. · DOI
  78. Madhu V, Dighe AS, Cui Q, Deal DN. Dual inhibition of activin/nodal/TGF-beta and BMP signaling pathways by SB431542 and dorsomorphin induces neuronal differentiation of human adipose derived stem cells. Stem Cells Int. 2016;2016:1035374. · DOI

Cited by

Sorted by citations

Metadata

Authors
Wu, J., Zhang, J., Chen, X., Wettschurack, K., Que, Z., Deming, B. A., Olivero-Acosta, M. I., Cui, N., Eaton, M., Zhao, Y., Li, S. M., Suzuki, M., Chen, I., Xiao, T., Halurkar, M. S., Mandal, P., Yuan, C., Xu, R., Koss, W. A., Du, D., Chen, F., Wu, L.-J., & Yang, Y.
Venue
Molecular Psychiatry
Published
2024-03-18
Volume
29
Issue
8
Pages
2424-2437
ISSN
  • 1359-4184
  • 1476-5578
Cited by
75
References
26
Language
en
Funders
  • U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (R01NS123154, R01NS117585)
  • the FamilieSCN2A Foundation for the Hodgkin-Huxley Award

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