Substance-Induced Psychiatric Disorders, Epigenetic and Microbiome Alterations, and Potential for Therapeutic Interventions
Abstract
:1. Introduction
2. Association between Substance Use and the Development of Psychotic Symptoms and Depressive-Like Behaviors
3. The Effects of Substance Use on Changing Brain Functions via Epigenetic Alterations
4. Paternal and Maternal Substance Use and Epigenetic Alterations in the Brains of the Offspring
Type of Substance/Type of Study | Brain Area | Epigenetic Changes | Effects on the Brains of Offspring | Ref. |
---|---|---|---|---|
Long-term parental methamphetamine exposure in mice | Hippocampus | DNA methylation | Presence of DMSs in the brains of offspring exposed to methamphetamine during embryonic development compared to control | [126] |
Maternal methamphetamine exposure in mice | NA | DNA methylation | DMSs of some genes involved in neurodevelopmental process | [127] |
Maternal cocaine exposure in mice | Hippocampus | DNA methylation | Reducing global DNA methylation at 3 and elevation of global DNA methylation at 30 days postpartum | [128] |
Prenatal cocaine exposure in mice | Hippocampus | DNA methylation | Cognitive deficits in offspring due to overexpression of DNMT 1 and L-methionine and subsequently elevating DNA methylation of IGF-2 | [129] |
Maternal alcohol consumption | Hippocampus | DNA methylation | Alterations in DNA methylation, gene expression, and brain function in offspring | [130] |
Maternal alcohol consumption | Hippocampus | DNA methylation | Elevated levels of dnmt1, dnmt3a, and hdac2 in offspring | [131] |
Paternal cocaine exposure in rats | Hippocampus | Histone acetylation/methylation | Elevated levels of a single methylated lysine 4 on histone H3 (H3K4me1) and acetylated histone H3 (H3Ac) near the Dao1 gene responsible for the oxidative deamination of D-serine (an amino acid with antipsychotic activity) | [132] |
Prenatal cocaine exposure in mice | Frontal cortex | Histone acetylation | Hyperacetylation of histone H3 at the BDNF promoter and thereby elevating the mRNA and protein levels of BDNF at adult postnatal day 60 | [133] |
Parental morphine exposure in rats | PFC and hippocampus. | Histone acetylation | Decrease in histone H3 acetylation and ΔFosB in the offspring of morphine-withdrawn parents during postnatal days 5, 21, 30, and 60 | [134] |
Prenatal morphine exposure in rats | VTA | Histone acetylation | Overexpression of HDAC5 | [135] |
Maternal cannabis exposure | NA | Histone lysine methylation | Reduced 3meH3K4 and elevated 2meH3K9 repressive marks at the DRD2 gene locus in the cannabis-exposed offspring | [136] |
Perinatal alcohol and nicotine–alcohol exposure in rats | VTA | miRNA | Alterations in the expression of miRNAs in dopaminergic neurons | [137] |
Prenatal alcohol exposure in mice | Brain cortex and microvascular endothelium at embryonic day 18 | miRNA | Elevated levels of MicroRNA-150-5p and suppressing the angiogenic factor Vezf1 | [138] |
5. Therapeutic Approaches Using Diet Modification or Epigenetic Drugs to Improve Psychotic Symptoms, Learning Deficits, and Memory Impairments in Animal Models and Patients with SUDs
6. Substance Use-Induced Gut Microbiome Alterations May Intensify Psychopathology via Epigenetic Aberrations
7. Challenges and Potentials for Clinical Translation
8. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Type of Substance/Type of Study | Brain Region | Key Findings | Ref. |
---|---|---|---|
Methamphetamine/in male rats | Nucleus accumbens (NA) and dorsal striatum | Elevated expression of DNA (cytosine-5-)-methyltransferase 1 (DNMT1) | [52] |
Methamphetamine/in male mice | Prefrontal cortex (PFC) and hippocampus | Alterations in the DNA methylation of several CpG sites of the Arc and the Fos in the PFC as well as klf10 and the Nr4a1 in the hippocampus of chronic methamphetamine-administrated mice | [53] |
Methamphetamine/in male mice | PFC | Reduced levels of total histone 3 and 4 tail acetylation/elevated levels of DNA methylation | [54] |
Methamphetamine/in male mice | Striatum | Demethylation within α-syn (SNCA) promoter | [55] |
Methamphetamine/in male rats | NA | Elevated levels of DNA methylation of some K+ channel genes following methamphetamine self-administration | [56] |
Methamphetamine/in male rats | PFC | Hypomethylation of BDNF-associated CpG islands | [57] |
Methamphetamine/in human and male rats | PFC and hippocampus | Increased levels of BDNF methylation in human methamphetamine dependence and in the PFCs of methamphetamine-administered rats/decreased BDNF methylation in the hippocampi of methamphetamine-administered rats | [58] |
Cocaine/in male mice | NA | DNA hypermethylation and elevated binding of MeCP2 at PP1c promoter/overexpression of DNMTs like DNMT3A and DNMT3B | [59] |
Cocaine/in male rats | Caudate putamen | Elevated levels of DNA methylation at the PP1Cβ gene plus its binding to Mecp2 | [60] |
Cocaine/in honey bees | Central brain (excluding gnathal ganglia and optic lobes) | Changes in DNA methylation and, hence, derangements in consolidation of extinction memory | [61] |
Cocaine/in male rats | NA/lateral habenula | Changes in methylation levels of TAAR7B, PPP1CC, and A2AR in high or low explorer rats | [62] |
Cocaine/in male mice | Dorsal striatum | Hypomethylation in exon 3 of IRX2 in neuronal nuclei | [63] |
Cocaine/in human | Striatum | Hypermethylation in a cluster of CpGs present in the body of tyrosine hydroxylase gene, including a putative EGR1-binding site | [64] |
Cocaine/in human | Human PFC | The presence of differentially methylated regions relevant to genes involved in synaptic signaling and neuroplasticity | [65] |
Nicotine or amphetamine/in male rats | mPFC, OFC, and nucleus accumbens | A reduction in global DNA methylation | [66] |
Morphine/in male rats | Hippocampus | Hypermethylation of glucocorticoid receptor 17 promoter after chronic morphine exposure and its association with hypothalamus–pituitary–adrenal axis dysfunction | [67] |
Morphine/in male rats | Cerebellum/hippocampus/pons/medulla oblongata | Differential methylation of IL1B in the hippocampus, Nr3c1 in the cerebellum, and BDNF and Il6 in the pons after acute exposure to morphine/differential methylation of NR3C1 in the hippocampus, BDNF and COMT in the pons, and l1b in the medulla oblongata after chronic exposure to morphine | [68] |
Morphine/in male rats | Basolateral amygdala | Association between the DNA hypermethylation of Gnas and the reconsolidation of morphine reward memories | [69] |
Heroin/in human | PFC | Detection of 1298 differentially methylated CpG sites (DMSs) between healthy individuals and heroin users | [70] |
Heroin/in male rats | NA | Hypomethylation of the GABRD gene following heroin self-administration | [71] |
oxycodone/in male rats | Hippocampus | DNA hypomethylation | [72] |
Type of Substance/Type of Study | Brain Region | Key Findings | Ref. |
---|---|---|---|
Cocaine/in male rats | Striatum | H4 hyperacetylation at the cFos promoter after 30 min of a single injection of cocaine/H3 hyperacetylation at the Cdk5 and BDNF promoters after chronic cocaine injection | [73] |
Cocaine/in male rats | NA | Transcriptional activation of genes relevant to addiction by H3 acetylation | [74] |
Cocaine/in male rats | Ventral tegmental area (VTA) | Association between elevated acetylation of histone 3 and cocaine-induced alterations in BDNF mRNA | [75] |
Cocaine/in male rats | NA/hippocampus | Reducing expression-activity of class IIa HDACs in the NA following high-cocaine intake and reducing expression/activity in hippocampus following low-cocaine intake | [76] |
Amphetamine/in mice | Striatum | Increased level of histone H4 acetylation after repeated treatment with amphetamine | [77] |
Methamphetamine/in male rats | NA | Time-related elevations in acetylated H4K5 and H4K8/down-regulation of HDAC1 and up-regulation of HDAC2 | [78] |
Methamphetamine/in male rats | Striatum | Elevated acetylation levels of H4K5 and H4K8 in gene promoter regions | [79] |
Methamphetamine/in male rats | Striatum | Reduction in HDAC6, 8, 9, 10 and 11 mRNA levels | [80] |
Methamphetamine/in male mice | NA | Elevation of mRNA levels of HDAC3, HDAC4, HDAC7, HDAC8, and HDAC11 in HDAC2KO mice after methamphetamine injection | [81] |
Methamphetamine/in male mice | PFC | Elevated acetylation status of histone 4 at class I HDAC1 and class IIb HDAC10 and reducing it at class IIa HDAC4 and HDAC5 | [82] |
Methamphetamine/in male rats | PFC | Hyper-acetylation of a number of genes (10 genes with H4 acetylation and 821 genes with H3 acetylation) | [83] |
Heroin /in human | Striatum | Hyperacetylation of histone H3 at specific lysine residues (K27 and K23) at discrete genomic locations (GRIA1 and several genes involved in glutamatergic synaptic plasticity) | [84] |
Heroin /in male rats | mPFC | Elevated levels of H3K9ac at the promoter region of brahma/SWI2-related gene-1 (BRG1) | [85] |
Morphine/in male rats | Hippocampus | Enhanced binding of STAT3 to the CXCL12 gene promoter and elevating the acetylation of histone H4 in the CXCL12 gene promoter following repeated context exposure with morphine conditioning | [86] |
Morphine/in male rats | Dorsomedial prefrontal cortex (dmPFC) | Enrichment of H3 acetylation at promoter regions of three genes (Cdk5r1, Gabrb2, and Grm5) in male animals | [87] |
Morphine/in male rats | Hippocampus/basolateral amygdala | Association between morphine-withdrawal aversive memories and elevation of H4K5 acetylation and p-Brd4 activation | [88] |
Oxycodone/in male rats | Dorsal striatum | Elevated levels of histone H3, phosphorylated at serine 10 and acetylated at lysine 14 (H3S10pK14Ac) in self-administered oxycodone animals using long-access paradigms | [89] |
Type of Substance/Type of Study | Brain Region | Key Findings | Ref. |
---|---|---|---|
Methamphetamine/in mice | Nucleus accumbens (NA) | Expression changes of 47 miRNA responsible for regulation of genes involved in modulation of metabolism, autophagy, and immune response | [90] |
Methamphetamine/in rats | VTA | Alterations in the expression of 78 miRNA involved in addiction | [91] |
Methamphetamine/in rats | NA | Overexpression of 166 miRNAs and down-regulation of 4 miRNAs following chronic treatment with methamphetamine | [92] |
Methamphetamine/in rats | NA | Overexpression of 17 miRNAs and down-regulation of 23 miRNAs | [93] |
Methamphetamine/in mice | NA | Elevated levels of miR-128, a miRNA responsible for regulating proteins involved in neuroplasticity, after repeated-intermittent methamphetamine use | [94] |
Methamphetamine/in rats | Dorsal striatum | Reductions in the expression of miR-181a-5p and miR-181b-5p | [95] |
Methamphetamine/in mice | NA | Down-regulation of novel-m009C expression, a novel microRNA involved in modulating methamphetamine-rewarding effects | [96] |
Methamphetamine/in human (postmortem human brain tissue) | NA/VTA | Up-regulation of microRNA let-7b-3p in brain tissues of methamphetamine users | [50] |
Cocaine/in rats | Dorsal striatum | Overexpression of miR-212 and, hence, regulating controlling the cocaine activity in brain reward circuitries | [97] |
Cocaine/in rats | Dorsal striatum | Homeostatic interplays between miR-212 and MeCP2 for controlling the effects of cocaine on striatal BDNF | [98] |
Cocaine/in rats | NA/striatum | Elevated expression of miR-212 and miR-137 in the dorsomedial and dorsolateral striatum, respectively, and miR-132, miR-137, miR-101b, and miR-212 in the NA shell | [99] |
Cocaine/in mice | Striatum | Down-regulation of miR-124 by cocaine and thereby elevated levels of pro-inflammatory cytokines due to microglial activation in a TLR4-dependent mechanism | [100] |
Cocaine/in mice | NA | Reduced levels of miR-124 following acute or chronic cocaine exposure | [101] |
Cocaine/in mice | NA | Reductions of mmu-miR-34b-5p in vulnerable animals with high motivation for cocaine; reduction of mmu-miR-1249-3p in animals with high motor disinhibition | [102] |
Heroin/in rats | NA | Mediating incubation of heroin craving by down-regulation of miR-181a | [103] |
Heroin/in rats | Orbitofrontal cortex | Regulation of long-lasting heroin seeking by miR-485-5p | [104] |
Morphine/in mice | NA | Alterations in the expression of 62 miRNAs | [105] |
Morphine/in rats | Dentate gyrus | Overexpression of miR-132 following morphine treatment and its role in modulating the structural plasticity | [106] |
Alcohol/in rats | Hippocampus | Overexpression of miR-3541, miR-125a-3p, and let-7a-5p and hypo-expression of their target genes (Nras, Prdm5, Suv39h1, Rnf152, Ptprz1, Apbb3, Mapk9, Ing4, Wt1, Nkx3-1, Dab2ip, Ripk1, Lin28a, and Acvr1c) in male alcohol-treated rats/decreased levels of miR-881-3p and miR-504, and overexpression of their target genes (Ube2g1, Naa50, Clock, Arih1, Cbfb, and Gng7) in female alcohol-treated rats | [107] |
Alcohol/in human (postmortem brain tissues) | Hippocampus | Elevated levels of miR-34a and miR-34c in subjects with alcohol use disorder | [108] |
Alcohol/in human (postmortem brain tissues) | Amygdala, NA, caudate nucleus, cerebellum, VTA, hippocampus, PFC, and putamen | Changes in the expression of 19 miRNAs | [109] |
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Nohesara, S.; Mostafavi Abdolmaleky, H.; Thiagalingam, S. Substance-Induced Psychiatric Disorders, Epigenetic and Microbiome Alterations, and Potential for Therapeutic Interventions. Brain Sci. 2024, 14, 769. https://doi.org/10.3390/brainsci14080769
Nohesara S, Mostafavi Abdolmaleky H, Thiagalingam S. Substance-Induced Psychiatric Disorders, Epigenetic and Microbiome Alterations, and Potential for Therapeutic Interventions. Brain Sciences. 2024; 14(8):769. https://doi.org/10.3390/brainsci14080769
Chicago/Turabian StyleNohesara, Shabnam, Hamid Mostafavi Abdolmaleky, and Sam Thiagalingam. 2024. "Substance-Induced Psychiatric Disorders, Epigenetic and Microbiome Alterations, and Potential for Therapeutic Interventions" Brain Sciences 14, no. 8: 769. https://doi.org/10.3390/brainsci14080769