Prenatally VPA exposure is likely to cause autistic-like behavior in the rats offspring via TREM2 down-regulation to affect the microglial activation and synapse alterations

Environmental Toxicology and Pharmacology - Tập 99 - Trang 104090 - 2023
Lijuan Luo1, Jie Chen1, Qionghui Wu1, Binlin Yuan1, Chaoqun Hu1, Ting Yang1, Hua Wei1,2, Tingyu Li1,2
1Children’s Nutrition Research Center, Children’s Hospital of Chongqing Medical University, Chongqing Key Laboratory of Child Nutrition and Health, National Clinical Research Center for Child Health and Disorders, Ministry of Education Key Laboratory of Child Development and Disorders, Chongqing, China
2Department of Child Health Care, Children’s Hospital of Chongqing Medical University, Chongqing, China

Tài liệu tham khảo

Banerjee, 2016, Overexpression of Homer1a in the basal and lateral amygdala impairs fear conditioning and induces an autism-like social impairment, Mol. Autism, 7, 16, 10.1186/s13229-016-0077-9 Beggiato, 2017, Gender differences in autism spectrum disorders: divergence among specific core symptoms, Autism Res. Off. J. Int. Soc. Autism Res., 10, 680, 10.1002/aur.1715 Bilimoria, 2015, Microglia function during brain development: new insights from animal models, Brain Res., 1617, 7, 10.1016/j.brainres.2014.11.032 Bronzuoli, 2018, Neuroglia in the autistic brain: evidence from a preclinical model, Mol. Autism, 9, 66, 10.1186/s13229-018-0254-0 Cady, 2014, TREM2 variant p.R47H as a risk factor for sporadic amyotrophic lateral sclerosis, JAMA Neurol., 71 Casaletto, 2022, Sex-specific effects of microglial activation on Alzheimer's disease proteinopathy in older adults, Brain: J. Neurol., 145, 3536, 10.1093/brain/awac257 Cheng, 2020, Vitamin A deficiency exacerbates autism-like behaviors and abnormalities of the enteric nervous system in a valproic acid-induced rat model of autism, Neurotoxicology, 79, 184, 10.1016/j.neuro.2020.06.004 Chu, 2022, Generational synaptic functions of GABA(A) receptor β3 subunit deteriorations in an animal model of social deficit, J. Biomed. Sci., 29, 51, 10.1186/s12929-022-00835-w Codagnone, 2015, Differential local connectivity and neuroinflammation profiles in the medial prefrontal cortex and hippocampus in the valproic acid rat model of autism, Dev. Neurosci., 37, 215, 10.1159/000375489 Colonna, 2017, Microglia function in the central nervous system during health and neurodegeneration, Annu. Rev. Immunol., 35, 441, 10.1146/annurev-immunol-051116-052358 Davoli-Ferreira, 2021, Microbiota and microglia interactions in ASD, Front. Immunol., 12, 10.3389/fimmu.2021.676255 Druart, 2019, Emerging roles of complement in psychiatric disorders, Front. Psychiatry, 10, 573, 10.3389/fpsyt.2019.00573 Feng, 2015, von Willebrand factor is a cofactor in complement regulation, Blood, 125, 1034, 10.1182/blood-2014-06-585430 Filipello, 2018, The microglial innate immune receptor TREM2 is required for synapse elimination and normal brain connectivity, Immunity, 48, 979, 10.1016/j.immuni.2018.04.016 Gąssowska-Dobrowolska, 2020, Prenatal exposure to valproic acid affects microglia and synaptic ultrastructure in a brain-region-specific manner in young-adult male rats: relevance to autism spectrum disorders, Int. J. Mol. Sci., 21 Geloso, 2021, Microglial pruning: relevance for synaptic dysfunction in multiple sclerosis and related experimental models, Cells, 10 Gerlach, 2016, Persistent gliosis interferes with neurogenesis in organotypic hippocampal slice cultures, Front. Cell. Neurosci., 10, 131, 10.3389/fncel.2016.00131 Guerreiro, 2013, TREM2 variants in Alzheimer's disease, New Engl. J. Med., 368, 117, 10.1056/NEJMoa1211851 Guerreiro, 2013, Using exome sequencing to reveal mutations in TREM2 presenting as a frontotemporal dementia-like syndrome without bone involvement, JAMA Neurol., 70, 78, 10.1001/jamaneurol.2013.579 Guo, 2019, TREM2 deficiency aggravates α-synuclein-induced neurodegeneration and neuroinflammation in Parkinson's disease models, FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol., 33, 12164, 10.1096/fj.201900992R Hamzawy, 2018, Leptin and camel milk abate oxidative stress status, genotoxicity induced in valproic acid rat model of autism, Int. J. Immunopathol. Pharmacol., 32, 10.1177/2058738418785514 Hong, 2016, Complement and microglia mediate early synapse loss in Alzheimer mouse models, Science, 352, 712, 10.1126/science.aad8373 Howell, 2019, Synaptic structural protein dysfunction leads to altered excitation inhibition ratios in models of autism spectrum disorder, Pharm. Res., 139, 207, 10.1016/j.phrs.2018.11.019 Hutsler, 2010, Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders, Brain Res., 1309, 83, 10.1016/j.brainres.2009.09.120 Jeckel, 2021, Autism spectrum disorder risk factor met regulates the organization of inhibitory synapses, Front. Mol. Neurosci., 14, 10.3389/fnmol.2021.659856 Ji, 2018, Antagonizing peroxisome proliferator-activated receptor γ facilitates M1-to-M2 shift of microglia by enhancing autophagy via the LKB1-AMPK signaling pathway, Aging Cell, 17, 10.1111/acel.12774 Jiang, 2016, TREM2 modifies microglial phenotype and provides neuroprotection in P301S tau transgenic mice, Neuropharmacology, 105, 196, 10.1016/j.neuropharm.2016.01.028 Jiang, 2022, TREM2 ameliorates anesthesia and surgery-induced cognitive impairment by regulating mitophagy and NLRP3 inflammasome in aged C57/BL6 mice, Neurotoxicology, 90, 216, 10.1016/j.neuro.2022.04.005 Kataoka, 2013, Autism-like behaviours with transient histone hyperacetylation in mice treated prenatally with valproic acid, Int. J. Neuropsychopharmacol., 16, 91, 10.1017/S1461145711001714 Kazlauskas, 2019, Sex-specific effects of prenatal valproic acid exposure on sociability and neuroinflammation: Relevance for susceptibility and resilience in autism, Psychoneuroendocrinology, 110, 10.1016/j.psyneuen.2019.104441 Kim, 2017, Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects, Mol. Psychiatry, 22, 1576, 10.1038/mp.2016.103 Lan, 2021, Abnormal spatiotemporal expression pattern of progranulin and neurodevelopment impairment in VPA-induced ASD rat model, Neuropharmacology, 196, 10.1016/j.neuropharm.2021.108689 Lee, 2020, Targeted delivery of mesenchymal stem cell-derived nanovesicles for spinal cord injury treatment, Int. J. Mol. Sci., 21, 10.7150/ijms.39074 Linnartz-Gerlach, 2019, TREM2 triggers microglial density and age-related neuronal loss, Glia, 67, 539, 10.1002/glia.23563 Liu, 2022, Apelin alleviated neuroinflammation and promoted endogenous neural stem cell proliferation and differentiation after spinal cord injury in rats, J. Neuroinflamm., 19, 160, 10.1186/s12974-022-02518-7 Lukens, 2022, Microglia and neurodevelopmental disorders, Annu. Rev. Neurosci., 45, 425, 10.1146/annurev-neuro-110920-023056 Maenner, M.J., Shaw, K.A., Bakian, A.V., Bilder, D.A., Durkin, M.S., Esler, A., Furnier, S.M., Hallas, L., Hall-Lande, J., Hudson, A., et al. (2021). Prevalence and Characteristics of Autism Spectrum Disorder Among Children Aged 8 Years - Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2018. Morbidity and mortality weekly report Surveillance summaries (Washington, DC: 2002) 70, 1–16. Matcovitch-Natan, 2016, Microglia development follows a stepwise program to regulate brain homeostasis, Science, 353, 10.1126/science.aad8670 McQuade, 2020, Gene expression and functional deficits underlie TREM2-knockout microglia responses in human models of Alzheimer's disease, Nat. Commun., 11, 5370, 10.1038/s41467-020-19227-5 Melancia, 2018, Sex-specific autistic endophenotypes induced by prenatal exposure to valproic acid involve anandamide signalling, Br. J. Pharmacol., 175, 3699, 10.1111/bph.14435 Nayak, 2014, Microglia development and function, Annu. Rev. Immunol., 32, 367, 10.1146/annurev-immunol-032713-120240 Paloneva, 2002, Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype, Am. J. Hum. Genet., 71, 656, 10.1086/342259 Paolicelli, 2011, Synaptic pruning by microglia is necessary for normal brain development, Science, 333, 1456, 10.1126/science.1202529 Park, 2019, Abnormal mitochondria in a non-human primate model of MPTP-induced Parkinson's disease: Drp1 and CDK5/p25 signaling, Exp. Neurobiol., 28, 414, 10.5607/en.2019.28.3.414 Qin, 2018, Enhanced topological network efficiency in preschool autism spectrum disorder: a diffusion tensor imaging study, Front. Psychiatry, 9, 278, 10.3389/fpsyt.2018.00278 Rezayat, 2021, Frontotemporal coordination predicts working memory performance and its local neural signatures, Nat. Commun., 12, 1103, 10.1038/s41467-021-21151-1 Ruganzu, 2021, TREM2 overexpression rescues cognitive deficits in APP/PS1 transgenic mice by reducing neuroinflammation via the JAK/STAT/SOCS signaling pathway, Exp. Neurol., 336, 10.1016/j.expneurol.2020.113506 Sahu, 2001, Structure and biology of complement protein C3, a connecting link between innate and acquired immunity, Immunol. Rev., 180, 35, 10.1034/j.1600-065X.2001.1800103.x Sandin, 2014, The familial risk of autism, JAMA, 311, 1770, 10.1001/jama.2014.4144 Schafer, 2012, Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner, Neuron, 74, 691, 10.1016/j.neuron.2012.03.026 Silawal, 2018, Osteoarthritis and the complement cascade, Clin. Med. Insights Arthritis Musculoskelet. Disord., 11, 10.1177/1179544117751430 Südhof, 2017, Synaptic neurexin complexes: a molecular code for the logic of neural circuits, Cell, 171, 745, 10.1016/j.cell.2017.10.024 Suzuki, 2013, Microglial activation in young adults with autism spectrum disorder, JAMA Psychiatry, 70, 49, 10.1001/jamapsychiatry.2013.272 Taleb, 2021, Emerging mechanisms of valproic acid-induced neurotoxic events in autism and its implications for pharmacological treatment, Biomed. Pharmacother., 137, 10.1016/j.biopha.2021.111322 Trapp, 2007, Evidence for synaptic stripping by cortical microglia, Glia, 55, 360, 10.1002/glia.20462 Triyasakorn, K., Ubah, U.D.B., Roan, B., Conlin, M., Aho, K., and Awale, P.S. (2022). The Antiepileptic Drug and Toxic Teratogen Valproic Acid Alters Microglia in an Environmental Mouse Model of Autism. Toxics 10. Vargas, 2005, Neuroglial activation and neuroinflammation in the brain of patients with autism, Ann. Neurol., 57, 67, 10.1002/ana.20315 Walker, 2020, Patterns of expression of purinergic receptor P2RY12, a putative marker for non-activated microglia, in aged and Alzheimer's disease brains, Int. J. Mol. Sci., 21 Wang, 2021, Vitamin A supplementation ameliorates motor incoordination via modulating RORα in the cerebellum in a valproic acid-treated rat autism model with vitamin A deficiency, Neurotoxicology, 85, 90, 10.1016/j.neuro.2021.05.004 Wang, 2021, HIF-1 α may play a role in late pregnancy hypoxia-induced autism-like behaviors in offspring rats, Behav. Brain Res., 411, 10.1016/j.bbr.2021.113373 Wostradowski, 2016, In vitro evaluation of physiologically relevant concentrations of teriflunomide on activation and proliferation of primary rodent microglia, J. Neuroinflamm., 13, 250, 10.1186/s12974-016-0715-3 Wu, 2022, Hippocampal overexpression of TREM2 ameliorates high fat diet induced cognitive impairment and modulates phenotypic polarization of the microglia, Genes Dis., 9, 401, 10.1016/j.gendis.2020.05.005 Xia, 2021, Altered relationship between parvalbumin and perineuronal nets in an autism model, Front. Mol. Neurosci., 14, 10.3389/fnmol.2021.597812 Xu, 2019, Microglial TREM-1 receptor mediates neuroinflammatory injury via interaction with SYK in experimental ischemic stroke, Cell Death Dis., 10, 555, 10.1038/s41419-019-1777-9 Xu, 2021, Activation of liver X receptors prevents emotional and cognitive dysfunction by suppressing microglial M1-polarization and restoring synaptic plasticity in the hippocampus of mice, Brain Behav. Immun., 94, 111, 10.1016/j.bbi.2021.02.026 Yang, 2018, The extended application of The Rat Brain in Stereotaxic Coordinates in rats of various body weight, J. Neurosci. Methods, 307, 60, 10.1016/j.jneumeth.2018.06.026 Yeh, 2017, TREM2, microglia, and neurodegenerative diseases, Trends Mol. Med., 23, 512, 10.1016/j.molmed.2017.03.008 Zamberletti, 2019, Cannabidivarin treatment ameliorates autism-like behaviors and restores hippocampal endocannabinoid system and glia alterations induced by prenatal valproic acid exposure in rats, Front. Cell. Neurosci., 13, 367, 10.3389/fncel.2019.00367 Zhai, 2017, Triggering receptor expressed on myeloid cells 2, a novel regulator of immunocyte phenotypes, confers neuroprotection by relieving neuroinflammation, Anesthesiology, 127, 98, 10.1097/ALN.0000000000001628 Zhang, 2018, TREM2 modulates microglia phenotypes in the neuroinflammation of Parkinson's disease, Biochem.. Biophys. Res. Commun., 499, 797, 10.1016/j.bbrc.2018.03.226 Zhang, 2019, The Notch signaling pathway inhibitor dapt alleviates autism-like behavior, autophagy and dendritic spine density abnormalities in a valproic acid-induced animal model of autism, Prog. Neuropsychopharmacol. Biol. Psychiatry, 94, 10.1016/j.pnpbp.2019.109644