Cited by 55Air Quality and Health ImpactsAutism Spectrum Disorder ResearchAnesthesia and Neurotoxicity Research

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Gestational B-vitamin supplementation alleviates PM2.5-induced autism-like behavior and hippocampal neurodevelopmental impairment in mice offspring

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Wang, Tingting, Zhang, Tianliang, Sun, Lijuan, Li, Wanwei, Zhang, Can, Yu, Li, Guan, Yingjun·2019·Ecotoxicology and Environmental Safety

Abstract

Gestational exposure to PM2.5 is a worldwide environmental issue associated with long-lasting behavior abnormalities and neurodevelopmental impairments in the hippocampus of offspring. PM2.5 may induce hippocampus injury and lead to autism-like behavior such as social communication deficits and stereotyped repetitive behavior in children through neuroinflammation and neurodegeneration. Here, we investigated the preventive effect of B-vitamin on PM2.5-induced deleterious effects by focusing on anti-inflammation, antioxidant, synaptic remodeling and neurodevelopment. Pregnant mice were randomly divided into three groups including control group (mice subject to PBS only), model group (mice subject to both 30 μL PM2.5 of 3.456 μg/μL and 10 mL/(kg·d) PBS), and intervention group (mice subject to both 30 μL PM2.5 of 3.456 μg/μL and 10 mL/(kg·d) B-vitamin supplementation (folic acid, vitamin B6 and vitamin B12 with concentrations at 0.06, 1.14 and 0.02 mg/mL, respectively)). In the current study B-vitamin significantly alleviated neurobehavioral impairment reflected in reduced social communication disorders, stereotyped repetitive behavior, along with learning and spatial memory impairment in PM2.5-stimulated mice offspring. Next, B-vitamin corrected synaptic loss and reduced mitochondrial damage in hippocampus of mice offspring, demonstrated by normalized synapse quantity, synaptic cleft, postsynaptic density (PSD) thickness and length of synaptic active area. Furthermore, significantly down-regulated expression of pro-inflammatory cytokines including NF-κB, TNF-α and IL-1β, and lipid peroxidation were found. We observed elevated levels of oxidant-related genes (SOD, GSH and GSH-Px). Moreover, decreased cleaved caspase-3 and TUNEL-positive cells suggested inhibited PM2.5-induced apoptosis by B-vitamin. Furthermore, B-vitamin increased neurogenesis by increasing EdU-positive cells in the subgranular zone (SGZ) of offspring. Collectively, our results suggest that B-vitamin supplementation exerts preventive effect on autism-like behavior and neurodevelopmental impairment in hippocampus of mice offspring gestationally exposed to PM2.5, to which alleviated mitochondrial damage, increased anti-inflammatory and antioxidant capacity and synaptic efficiency, reduced neuronal apoptosis and improved hippocampal neurogenesis may contribute.

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Research works printed but not linked: 49

  1. Abookasis, 2018, Optically derived metabolic and hemodynamic parameters predict hippocampal neurogenesis in the BTBR mouse model of autism, J. Biophot., 11, 10.1002/jbio.201600322 · DOI
  2. Alfawaz, 2018, The independent and combined effects of omega-3 and vitamin B12 in ameliorating propionic acid induced biochemical features in Juvenile Rats as rodent model of autism, J. Mol. Neurosci., 66, 403, 10.1007/s12031-018-1186-z · DOI
  3. Allen, 2013, Developmental exposure to concentrated ambient particles and preference for immediate reward in mice, Environ. Health Perspect., 121, 32, 10.1289/ehp.1205505 · DOI · Paper page
  4. Bjorklund, 2019, The role of vitamins in autism spectrum disorder: what do we know?, J. Mol. Neurosci., 67, 373, 10.1007/s12031-018-1237-5 · DOI
  5. Bhattacharjee, 2016, Possible involvement of iNOS and TNF-alpha in nutritional intervention against nicotine-induced pancreatic islet cell damage, Biomed. Pharmacother., 84, 1727, 10.1016/j.biopha.2016.10.079 · DOI
  6. Braden, 2017, Executive function and functional and structural brain differences in middle-age adults with autism spectrum disorder, Autism Res., 10, 1945, 10.1002/aur.1842 · DOI
  7. Cai, 2019, The liver X receptor agonist TO901317 ameliorates behavioral deficits in two mouse models of autism, Front. Cell. Neurosci., 13, 213, 10.3389/fncel.2019.00213 · DOI
  8. Chao, 2017, Exposure to PM2.5 causes genetic changes in fetal rat cerebral cortex and hippocampus, Environ. Toxicol., 32, 1412, 10.1002/tox.22335 · DOI
  9. Chen, 2015, Overexpression of the type 1 adenylyl cyclase in the forebrain leads to deficits of behavioral inhibition, J. Neurosci., 35, 339, 10.1523/JNEUROSCI.2478-14.2015 · DOI · Paper page
  10. Cianciulli, 2016, Folic acid is able to polarize the inflammatory response in LPS activated microglia by regulating multiple signaling pathways, Mediat. Inflamm., 2016, 5240127, 10.1155/2016/5240127 · DOI
  11. Cope, 2016, Immature neurons and Radial Glia, but not astrocytes or microglia, are altered in adult Cntnap2 and Shank 3 mice, models of autism, eNeuro, 3, 10.1523/ENEURO.0196-16.2016 · DOI
  12. Cory-Slechta, 2018, Developmental exposure to low level ambient ultrafine particle air pollution and cognitive dysfunction, Neurotoxicology (Little Rock), 69, 217, 10.1016/j.neuro.2017.12.003 · DOI · Paper page
  13. Degnan, 2014, Vitamin B12 as a modulator of gut microbial ecology, Cell Metabol., 20, 769, 10.1016/j.cmet.2014.10.002 · DOI
  14. Douaud, 2013, Preventing Alzheimer's disease-related gray matter atrophy by B-vitamin treatment, Proc. Natl. Acad. Sci. U. S. A., 110, 9523, 10.1073/pnas.1301816110 · DOI
  15. Fu, 2019, The association between PM2.5 exposure and neurological disorders: a systematic review and meta-analysis, Sci. Total Environ., 655, 1240, 10.1016/j.scitotenv.2018.11.218 · DOI
  16. Gilbert, 2017, Fundamental elements in autism. From neurogenesis and neurite growth to synaptic plasticity, Front. Cell. Neurosci., 11, 359, 10.3389/fncel.2017.00359 · DOI
  17. Goodrich, 2018, Joint effects of prenatal air pollutant exposure and maternal folic acid supplementation on risk of autism spectrum disorder, Autism Res., 11, 69, 10.1002/aur.1885 · DOI
  18. Guo, 2018, Long-term exposure to ambient PM2.5 associated with fall-related injury in six low- and middle-income countries, Environ. Pollut., 237, 961, 10.1016/j.envpol.2017.10.134 · DOI
  19. Guxens, 2018, Air pollution exposure during fetal life, brain morphology, and cognitive function in school-age children, Biol. Psychiatry, 84, 295, 10.1016/j.biopsych.2018.01.016 · DOI
  20. Hall, 2018, Nerve growth factor is responsible for exercise-induced recovery of septohippocampal cholinergic structure and function, Front. Neurosci., 12, 773, 10.3389/fnins.2018.00773 · DOI
  21. Hansel, 2019, Deregulation of synaptic plasticity in autism, Neurosci. Lett., 688, 58, 10.1016/j.neulet.2018.02.003 · DOI
  22. Hollis, 2017, Mitochondrial dysfunction in Autism Spectrum Disorder: clinical features and perspectives, Curr. Opin. Neurobiol., 45, 178, 10.1016/j.conb.2017.05.018 · DOI
  23. Hsiao, 2013, Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders, Cell, 155, 1451, 10.1016/j.cell.2013.11.024 · DOI · Paper page
  24. Kemse, 2016, Supplementation of maternal omega-3 fatty acids to pregnancy induced hypertension Wistar rats improves IL10 and VEGF levels, Prostaglandins Leukot. Essent. Fatty Acids, 104, 25, 10.1016/j.plefa.2015.11.003 · DOI
  25. Kern, 2015, Relevance of neuroinflammation and encephalitis in autism, Front. Cell. Neurosci., 9, 519
  26. Lammert, 2018, Cutting edge: critical roles for microbiota-mediated regulation of the immune system in a prenatal immune activation model of autism, J. Immunol., 201, 845, 10.4049/jimmunol.1701755 · DOI
  27. Levine, 2018, Association of maternal use of folic acid and multivitamin supplements in the periods before and during pregnancy with the risk of autism spectrum disorder in offspring, JAMA Psychiatr., 75, 176, 10.1001/jamapsychiatry.2017.4050 · DOI
  28. Li, 2018, PM2.5 exposure stimulates COX-2-mediated excitatory synaptic transmission via ROS-NF-kappaB pathway, Chemosphere, 190, 124, 10.1016/j.chemosphere.2017.09.098 · DOI
  29. Liu, 2017, At seeming safe concentrations, synergistic effects of PM2.5 and formaldehyde co-exposure induces Alzheimer-like changes in mouse brain, Onco Target, 8, 98567
  30. Mansvelder, 2019, Synaptic plasticity in human cortical circuits: cellular mechanisms of learning and memory in the human brain?, Curr. Opin. Neurobiol., 54, 186, 10.1016/j.conb.2018.06.013 · DOI
  31. Mitra, 2017, Antioxidant and anti-inflammatory nutrient status, supplementation, and mechanisms in patients with schizophrenia, Prog. Neuropsychopharmacol. Biol. Psychiatr., 78, 1, 10.1016/j.pnpbp.2017.05.005 · DOI
  32. Murakami, 2010, Dietary intake of folate, vitamin B6, vitamin B12 and riboflavin and risk of Parkinson's disease: a case-control study in Japan, Br. J. Nutr., 104, 757, 10.1017/S0007114510001005 · DOI
  33. Mutlu, 2018, Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome, Environ. Pollut., 240, 817, 10.1016/j.envpol.2018.04.130 · DOI
  34. Nam, 2017, Differential effects of low- and high-dose zinc supplementation on synaptic plasticity and neurogenesis in the hippocampus of control and high-fat diet-fed mice, Neurochem. Res., 42, 3149, 10.1007/s11064-017-2353-2 · DOI
  35. Sepehri, 2019, Activity enhancement of ammonia-oxidizing bacteria and nitrite-oxidizing bacteria in activated sludge process: metabolite reduction and CO2 mitigation intensification process, Appl. Water Sci., 9, 131, 10.1007/s13201-019-1017-6 · DOI
  36. Sorrells, 2018, Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults, Nature, 555, 377, 10.1038/nature25975 · DOI · Paper page
  37. Talbott, 2015, Fine particulate matter and the risk of autism spectrum disorder, Environ. Res., 140, 414, 10.1016/j.envres.2015.04.021 · DOI
  38. Teng, 2016, Fine particle-induced birth defects: impacts of size, payload, and beyond, Birth Defects Res. C Embryo Today, 108, 196, 10.1002/bdrc.21136 · DOI
  39. Tripathi, 2016, Hyperhomocysteinemia causes ER stress and impaired autophagy that is reversed by vitamin B supplementation, Cell Death Dis., 7, 10.1038/cddis.2016.374 · DOI
  40. Truchet, 2002, Learning and memory of cue-reward association meaning by modifications of synaptic efficacy in dentate gyrus and piriform cortex, Hippocampus, 12, 600, 10.1002/hipo.10097 · DOI
  41. Wang, 2018, Exposure to concentrated ambient PM2.5 alters the composition of gut microbiota in a murine model, Part. Fibre Toxicol., 15, 17, 10.1186/s12989-018-0252-6 · DOI
  42. Wang, 2018, Maternal folic acid supplementation during pregnancy improves neurobehavioral development in Rat offspring, Mol. Neurobiol., 55, 2676, 10.1007/s12035-017-0534-2 · DOI
  43. Xu, 2016, Nanoceria restrains PM2.5-induced metabolic disorder and hypothalamus inflammation by inhibition of astrocytes activation related NF-kappaB pathway in Nrf 2 deficient mice, Free Radic. Biol. Med., 99, 259, 10.1016/j.freeradbiomed.2016.08.021 · DOI
  44. Zhang, 2018, Analysis of gut microbiota profiles and microbe-disease associations in children with autism spectrum disorders in China, Sci. Rep., 8, 13981, 10.1038/s41598-018-32219-2 · DOI · Paper page
  45. Zhang, 2016, Vitamin B6 prevents IL-1 beta protein production by inhibiting NLRP3 inflammasome activation, J. Biol. Chem., 291, 24517, 10.1074/jbc.M116.743815 · DOI
  46. Zhang, 2018, Maternal exposure to PM2.5 during pregnancy induces impaired development of cerebral cortex in mice offspring, Int. J. Mol. Sci., 19
  47. Zheng, 2018, Gestational exposure to particulate matter 2.5 (PM2.5) leads to spatial memory dysfunction and neurodevelopmental impairment in Hippocampus of mice offspring, Front. Neurosci., 12, 1000, 10.3389/fnins.2018.01000 · DOI
  48. Zhong, 2017, Vitamin B attenuate the epigenetic effects of ambient fine particles in a pilot human intervention trial, Proc. Natl. Acad. Sci. U. S. A., 114, 3503, 10.1073/pnas.1618545114 · DOI
  49. Zhong, 2017, B-vitamin supplementation mitigates effects of fine particles on cardiac autonomic dysfunction and inflammation: a pilot human intervention trial, Sci. Rep., 7, 45322, 10.1038/srep45322 · DOI

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Metadata

Authors
Wang, T., Zhang, T., Sun, L., Li, W., Zhang, C., Yu, L., & Guan, Y.
Affiliations
  • Weifang Medical University (CN)
  • Harvard University (US)
Corresponding author
  • Yu, Li
  • Guan, Yingjun
Venue
Ecotoxicology and Environmental Safety
Publisher
Elsevier BV
Published
2019-12
Volume
185
Pages
109686
ISSN
0147-6513 (ISSN-L)
OpenAlex
W2974586741
Cited by
55
References
5
Citations by year
2026: 2 · 2025: 10 · 2024: 13 · 2023: 7 · 2022: 11 · 2021: 7 · 2020: 5
FWCI
2.49
Type
journal article
Language
en
Open access
Locations
  • Ecotoxicology and Environmental Safety (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
Shandong Provincial Natural Science Foundation, China (ZR2018MC012, ZR2015HL099)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Life Sciences › Neuroscience › Developmental Neuroscience › Anesthesia and Neurotoxicity Research
Keywords
PM2.5, prenatal exposure, vitamin B supplementation, autism-like behavior, folic acid, vitamin B6, vitamin B12, neuroinflammation, oxidative stress, mitochondrial damage, synaptic remodeling, neuronal apoptosis, neurogenesis, social communication deficits, spatial memory impairment, prenatal air pollution exposure, neuroprotection, inflammatory cytokines
MeSH terms
Air Pollutants, Animals, Autistic Disorder, Female, Hippocampus, Learning, Male, Mice, Inbred ICR, Pregnancy, Prenatal Exposure Delayed Effects, Synapses, Vitamin B Complex, Cytokines, Apoptosis, Dietary Supplements, Particulate Matter, Neurogenesis

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