Prenatal Stress and Ethanol Exposure: Microbiota-Induced Immune Dysregulation and Psychiatric Risks
Abstract
:1. Introduction
2. Microbiota Host: From Passive Spectator to Essential Modulator in Health and Disease
2.1. Structural Components of Microbiota Host
2.2. Immunological Components of Microbiota Host
3. Maternal Microbiota Disturbance: Implications for Offspring Immune System and Beyond
3.1. Maternal DIET and Microbiota
3.2. Influence of Progesterone on Microbiota during Pregnancy
3.3. Maternal Microbiota and Immunity: Implications for Fetal and Neonatal Health
4. Exploring the Interplay between Prenatal Maternal Stress, Microbiota, and Depression
4.1. Stress, Gut Microbiota, and Depression
4.2. The Impact of Prenatal Maternal Stress on Maternal Offspring Microbiome Dynamics
4.3. The Impact of Maternal Microbiota and Prenatal Stress on Offspring Immune System
5. Ethanol-Induced Changes in Gut Microbiota: Understanding Consequences and Investigating Prenatal Exposure Effects
5.1. Consequences of Ethanol Consumption in Intestinal Dysbiosis
5.2. Effects of Prenatal Ethanol Exposure on Maternal and Offspring Microbiota
6. Connecting the Dots: Exploring the Link between Microbiota Dysbiosis, Maternal Immunological Changes, and Depression
7. Conclusions
Implications and Future Research Directions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
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Prenatal Maternal Stress and Microbiota | ||||
---|---|---|---|---|
Author | Prenatal Stress Exposure | Specie | Microbiota (Offspring) | Outcomes |
Zijlmans et al. (2015) doi: 10.1016/j.psyneuen.2015.01.006 [147] | Maternal prenatal stress (self-reports and/or salivary cortisol levels) | Humans | ↓ Lactic acid bacteria (Lactobacillus, Lactoccus, Aerococcus); ↓ Actinobacteria; ↑ Proteobacteria (Escherichia, Serratia and Enterobacter). | Specific colonization patterns were correlated with maternal-reported gastrointestinal symptoms and allergic reactions in the infant. |
Galley et al. (2023) doi: 10.1016/j.bbi.2022.10.005 [145] | Maternal anxiety, depression, or perceived stress | Humans | ↓ Bifidobacterium dentium in the offspring of mothers with higher anxiety, perceived stress, and depression. | B. dentium was positively associated with elevated IL-6 and IL-8 during pregnancy |
Naudé et al. (2020) doi: 10.1017/neu.2019.43 [151] | Prenatal distinct psychological profiles, including exposure to lifelong intimate partner violence (IPV) | Humans | Infants born to mothers that were exposed to high levels of IPV: ↑ Citrobacter and three unclassified genera (Enterobacteriaceae family) detected at birth. | - |
Weiss, Hamidi (2023) doi: 10.1080/14767058.2023.2214835 [152] | Stress during the third trimester of pregnancy | Humans | Lower stress levels: ↑ Bacteroides, Eggerthella, and Enterobacteriacea. Higher stress levels: ↑ Lactobacillus and Bifidobacterium. | - |
Golubeva et al. (2015) doi: 10.1016/j.psyneuen.2015.06.002 [155] | Restraint stress (gestational day 14–20) | Rats | ↑ Oscillibacter, Anaerotruncus, and Peptococcus; ↓ Lactobacillus (tendency). male offspring | - |
Gur et al. (2019) doi: 10.1016/j.bbr.2018.06.025 [158] | Restraint stress (gestational day 10–16) | Mice | ↓ Bacteroides and Parabacteroides. male offspring | - |
Sun et al. (2021) doi: 10.3389/fimmu.2021.700995 [160] | Variable stress beginning at gestational day 10 | Mice | ↓ anti-inflammatory probiotics: Bifidobacteriales, Bifidobacteriaceae, and Bifidobacterium. ↑ pro-inflammatory bacteria: Desulfovibrionales, Desulfovibrionaceae, and Desulfovibrio. | Prenatal maternal stress caused persistent overgrowth of Desulfovibrio resulting in exacerbated experimental colitis in adulthood. |
Bailey, Lubach, Coe (2004) doi: 10.1097/00005176-200404000-00009 [99] | Stressed during pregnancy using an acoustical startle paradigm | Monkeys | ↓ Bifidobacteria and Lactobacilli. | - |
Alcohol and Microbiota | ||||
---|---|---|---|---|
Author | Alcohol Exposure | Specie | Microbiota | Outcomes/Main Results |
Mutlu et al. (2009) doi: 10.1111/j.1530-0277.2009.01022.x [185] | Received alcohol or dextrose intragastrically by gavage twice daily for up to 10 weeks | Rats | Alterations in the composition of mucosa-associated microbiota in the colon | Little or no dysbiosis after 4–6 weeks of alcohol feeding, but dysbiosis after 10 weeks of alcohol exposure |
Bull-Otterson et al. (2013) doi: 10.1371/journal. pone.0053028 [175] | Mice were fed liquid Lieber–DeCarli diet without or with alcohol (5% v/v) for 6 weeks | Mice | ↑ Proteobacteria, Actinobacteria ↓ Bacteriodetes, Firmicutes | ↑ In plasma endotoxin ↑ Fecal pH ↑ Hepatic inflammation |
Leclercq et al. (2014) doi: 10.1073/pnas. 1415174111 [181] | Individuals with AUD | Humans | ↑ Lachnospiraceae (Dorea) and Blautia ↓ Ruminococcaceae (Ruminococcus, Faecalibacterium, Subdoligranulum, Oscillibacter and Anaerofilum) | ↑ Intestinal permeability (IP) ↑ Inflammatory markers (TNFα, IL-1β, IL-6, IL-8, and IL-10) AUD individuals with high IP presented higher depression, anxiety, and alcohol-craving scores |
Tsuruya et al. (2016) doi: 10.1038/srep27923 [193] | Individuals with AUD | Humans | ↑ Streptococcus and Coprobacillus ↓ Bacteroides and Ruminococcus (anaerobes) | Lower production of acetaldehyde from ethanol metabolism |
Peterson et al. (2017) doi: 10.1016/j.bbr.2017.01.049 [177] | C57BL/6J mice were exposed to 4 weeks of vaporized ethanol | Mice | ↑ Alistipes ↓ Clostridium IV and XIVb, Dorea and Coprococcus | ↓ α-diversity of microbiota |
Dubinkina et al. (2017) doi: 10.1186/s40168-017-0359-2 [180] | Individuals with AUD | Humans | ↑ Enterobacteriaceae, ↓ Clostridiales—Individuals with AUD without liver cirrhosis. | Strong negative influence of alcohol dependence and associated liver dysfunction on the intestinal microbiota |
Grander et al. (2018) doi: 10.1136/gutjnl-2016-313432 [182] | Individuals with acute alcoholic steatohepatitis | Humans | ↓ Akkermansia muciniphila | Oral administration of A. muciniphila protected against ethanol-induced hepatic injuries |
Wang et al. (2018) doi: 10.3389/fmicb. 2018.01874 [187] | Consumption of increasing alcohol concentration 3%, 6%, 10% (v/v) | Mice | ↑ Firmicutes, Clostridiales and Lachnospiraceae, Alistipes, Odoribacter | Groups exposed to alcohol or with alcohol abstinence presented anxiety and depression compared |
Xiao et al. (2018) doi: 10.1016/j.toxlet. 2018.01.021 [189] | Chronically fed alcohol | Mice | ↑ Erysipelotriquia, Erythrobacter, Allobaculum and Blautia | Increased gut microbiome diversity, with reduced commensal gut taxa. Anxiety behaviors associated with alcohol withdrawal |
Xu et al. (2019) doi: 10.1002/biof.1469 [188] | Exposure to 2–8% (v/v) ethanol was 21 days | Mice | ↑ Actinobacteria and Cyanobacteria ↑ Adlercreutzia spp., Allobaculum spp., Turicibacter spp. ↓ Helicobacter spp. | Animals exhibited anxiety/depression-like behaviors |
Leclercq et al. (2020) doi: 10.1016/j.celrep. 2020.108238 [202] | Individuals with alcohol dependence | Humans | ↑ Lachnospiraceae ↓ Faecalibacterium praustnizii | ↑ Intestinal Permeability ↑ Introversion and social anxiety |
Microbial transfer from human donors with alcohol dependence to mice | Mice | ↑ Firmicutes and Akkermansia muciniphila ↓ Blautia, Faecalibacterium, and Bacteroidetes | ↑ Depressive-like behavior ↑ Corticosterone level ↓ Social behavior | |
Cuesta et al. (2021) doi: 10.3390/ijms222312830 [191] | TLR4 knockout mice treated with 10% (v/v) alcohol for 3 months | Mice | ↓ Firmicutes | TLR4 is a key factor in determining the intestinal microbiota as TLR4 KO mice did not show the usual signs of ethanol-induced inflammation |
Singhal et al. (2021) doi: 10.1080/19490976.2021.1946367 [201] | C57BL/6 mice were fed a Lieber-DeCarli liquid diet containing ethanol 5%(v/v) for 7 weeks | Mice | ↓ Firmicutes, Lachnospiraceace, Clostridiaceae, Ruminococccaceae | Loss of butyrate-producing bacteria and butyrate genes |
Yang et al. (2021) doi: 10.1128/AEM.00834-21 [186] | 6% (v/v) alcohol was added to drinking water for 5 weeks | Rats | ↑ Firmicutes and Bacteroidetes ↓ Prevotellaceae, Ruminococcus-1, Lachnospiraceae, Roseburia, Prevotellaceae and Lachnoclostridium | ↓ Amino acids and lipids (serum metabolome disorders) ↓ Concentration of serotonin in the hippocampus ↓ Lipopolysaccharide ↑ Intestinal permeability biomarkers |
Du et al. (2022) doi: 10.3389/fpsyt. 2022.1054685 [183] | Individuals with alcohol dependence | Humans | ↑ Faecalibacterium, Gemmiger and Lachnospiracea incertae sedis ↓ Megamonas and Escherichia | The cognitive capacity of the participants was assessed using the Montreal Cognitive Assessment (MoCA) and the Mini-Mental State Examination (MMSE), revealing a negative correlation between the MoCA and MMSE scores with years of alcohol consumption and dependence on alcohol. |
Baltazar-Díaz et al. (2022) doi: 10.3390/microorganisms10061231 [184] | Individuals with alcoholic cirrhosis | Humans | ↑ Escherichia/Shigella e Prevotella ↓ Blautia, Faecalibacterium | ↓ α—diversity of microbiota ↓ Acetyl-CoA fermentation to butyrate |
Wang et al. (2023) doi: 10.1128/mbio.02392-23 [12] | Individuals with alcohol dependence | Humans | ↑ Saccharimonadaceae, Lachnospiraceae, and Fusobacterium ↓ Ruminococcaceae, Erysipelotrichaceae, and Roseburia | ↑ Anxiety and depression behaviors ↑ Preference for alcohol |
Microbial transfer from human donors with alcohol dependence to rats | Rats | |||
Wei et al. (2023) doi: 10.1016/j.biopha. 2023.114308 [198] | C57BL/6 J mice were fed Lieber-DeCarli liquid diets (28% ethanol) for 6 weeks | Mice | ↑ Streptococcus, Parasutterella, Dubosiella, Muribaculum, Bifidobacterium, Bacteroides, Odoribacter, Alistipes, Lactobacillus and Parabacteroides ↓ Ileibacterium, Lachnoclostridium, and Coriobacteriaceae | Neuronal necrosis in the hippocampus and prefrontal cortex Exacerbate neurodegeneration and cognitive dysfunction ↑ TNF-α, IL-6, IL-1β and IL-18 in the hippocampus |
Yao et al. (2023) doi: 10.1038/s41380-022-01841-y [211] | C57BL/6N mice were exposed to ethanol-free drinking model for 90 days (Fecal microbiota transplantation model) | Mice | ↑ Firmicutes, Actinobacteria, Erysipelotrichi, Erysipelotrichales, Bacillales, Erysipelotrichaceae, Staphylococcaceae, Allobaculum ↓ Bacteroidetes, Bacteroidia, Verrucomicrobiae | ↑ Intestinal permeability ↑ Serum inflammatory factor levels Activation of NLRP3 inflammasome in the hippocampus, leading to neuroinflammation and depressive-like behavior |
Carbia et al. (2023) doi: 10.1016/j.ebiom.2023.104442 [179] | Young people aged 18–25 years reported their alcohol use (at least 60 g or more of pure alcohol on at least one occasion in the last 30 days) | Humans | ↑ Veillonella dispar ↓ Alistipes | Difficulties in emotional recognition |
Prenatal Alcohol Exposure and Microbiota | |||
---|---|---|---|
Author | Alcohol Exposure | Specie | Microbiota/Microbe-Dependent Products |
Virdee et al. (2021) doi: 10.1038/s41598-020-80093-8 [235] | Pregnant C57BL/6 mice were gavaged with 3 g/kg alcohol during GD8.5-17.5 | Mice | Specific microbe-dependent products (MDP) in the microbiome might serve as a biosignature for identifying PAE Mothers: High levels of MDPs in plasma, most of them phenolic acids and indole derivatives Offspring: High levels of MDPs implicated in neuroinflammation, depression, and anxiety (4-ethylphenylsulfate, oxindole, indolepropionate, p-cresol sulfate, and salicylate) |
Wang et al. (2021) doi: 10.3390/biom11030369 [15] | Maternal alcohol consumption during pregnancy | Humans | Mothers: ↑ Phascolarctobacterium and Blautia ↓ Faecalibacterium Offspring: ↑ Megamonas |
Bodnar et al. (2022) doi: 10.1111/acer.14784 [229] | Pregnant Sprague-Dawley rats received an ethanol diet during GD17-GD21 | Rats | Offspring: ↑ Bacteroides, Roseburia (at the phylum Firmicutes), and Proteus PAE generated sex-specific changes in the microbiota. In males, α-diversity was higher in PAE, and in females, this difference was not detected. Significant alterations in Bacteroides, Bifidobacterium, Akkermansia, and Ruminiclostridium were found between PAE and control males. In females, Bacteroides, Proteobacteria, Faecalitalea, Proteus, Roseburia, and Gastranaerophilales were identified to be altered by PAE. |
Bodnar et al. (2024) doi: 10.1038/s41598-024-64313-z [17] | Pregnant Sprague-Dawley rats with ad libitum access to an alcohol-containing liquid diet with 36% of total calories derived from ethanol during GD1-GD21 | Rats | Mothers: ↑ Desulfovibrionaceae, Akkermansia Offspring: ↑ Firmicutes, Parabacterteroides, Alistipes ↓ Ruminococcus |
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Camarini, R.; Marianno, P.; Hanampa-Maquera, M.; Oliveira, S.d.S.; Câmara, N.O.S. Prenatal Stress and Ethanol Exposure: Microbiota-Induced Immune Dysregulation and Psychiatric Risks. Int. J. Mol. Sci. 2024, 25, 9776. https://doi.org/10.3390/ijms25189776
Camarini R, Marianno P, Hanampa-Maquera M, Oliveira SdS, Câmara NOS. Prenatal Stress and Ethanol Exposure: Microbiota-Induced Immune Dysregulation and Psychiatric Risks. International Journal of Molecular Sciences. 2024; 25(18):9776. https://doi.org/10.3390/ijms25189776
Chicago/Turabian StyleCamarini, Rosana, Priscila Marianno, Maylin Hanampa-Maquera, Samuel dos Santos Oliveira, and Niels Olsen Saraiva Câmara. 2024. "Prenatal Stress and Ethanol Exposure: Microbiota-Induced Immune Dysregulation and Psychiatric Risks" International Journal of Molecular Sciences 25, no. 18: 9776. https://doi.org/10.3390/ijms25189776