Developmental Bisphenol A Exposure Modulates Immune-Related Diseases
Abstract
:1. Introduction
2. Mechanisms of Immune Modulation and Disease Exacerbation Following Developmental BPA Exposure
2.1. Receptor Modification
2.2. Epigenetics
2.3. Microbiome
2.4. Cell Signaling Pathways
3. Immune System Alteration Following Developmental BPA Exposure
3.1. Innate Immune System
3.2. Adaptive Immune System
3.3. Cytokine/Chemokine, Antibody Production and Host Resistance
4. Diseases Related to Immune System Alteration Following Developmental BPA Exposure
4.1. Multiple Sclerosis
4.2. Type 1 Diabetes Mellitus
4.3. Type 2 Diabetes Mellitus
4.4. Allergies and Asthma
4.5. Mammary Cancer
5. Bisphenol S: An Alternative for BPA
6. Discussion
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Multiple Sclerosis Disease Models | Animal Model | Exposure Windows | BPA Dose | Routes of Administration | Diet | Effects | Reference |
---|---|---|---|---|---|---|---|
Autoimmune Encephalomyelitis (EAE) | Male and Female Mice (C57BL/6J and SJL/JCrHsd) | Gestation and Lactation | 10 μg/mL | 1% ethanol in drinking water | AIN-93G (casein-based phytoestrogen-free) | No Effect on EAE or INF-γ; decreased IL-17 in females | [77] |
Theiler’s Murine Encephalomyelitis Virus (TMEV) | Male and Female Mice (SJL) | Gestation and Lactation | 10 μg/kg BW | Charcoal-stripped corn oil via gavage | Not Specified | Earlier onset of disease; increased inflammation; decreased antibodies to virus | [80] |
Diabetes Disease Model | Animal Model | Exposure Windows | BPA Dose | Routes of Administration | Diet | Effects | Reference |
---|---|---|---|---|---|---|---|
Type 1 Diabetes | Female NOD/ShiLtJ Mice Offspring | Gestation and Lactation | 0.1, 1 or 10 mg/L | Deionized autoclaved drinking water | 2919X (minimal phytoestrogen content) | Increased insulitis, diabetes, Treg cells and apoptosis of β-cells, α-cells and macrophages in highest dose only | [83] |
Type 1 Diabetes | Female NOD/ShiLtJ Mice Offspring | From Gestation to End of Study | 1 mg/L | Deionized autoclaved drinking water | 2919X (minimal phytoestrogen content) | Increased insulitis, diabetes and apoptosis pancreatic cells macrophages; decreased phagocytic macrophages, IL-10, IL-4 and TNF-α | [52] |
Type 2 Diabetes | Male and Female Human Infants | 1st Trimester | ≤0.34 to >1.7 μg/L (measured, not dosed) | Measured exposure from environment, etc. | Not Specified | Lower adiponectins in male cord blood | [85] |
Type 2 Diabetes | Male Wistar Rat Offspring | Gestation and Lactation | 50 μg/kg | Gavage; dissolved in corn oil | Not Specified | Increased insulin and insulin resistance; reduced glycogen | [87] |
Type 2 Diabetes | Male and Female Wistar Rat Offspring | Gestation and Lactation | 50, 250 or 1250 μg/kg | Gavage; in corn oil | Standard or high-fat diet | Low dose only: increased body weight and insulin; altered β-cell function; high-fat diet and male had a greater effect | [88] |
Type 2 Diabetes | Male and Female OF-1 Mice Offspring | Prenatal (GD9-16) | 10 or 100 μg/kg | S.C. injection; in tocopherol-stripped corn oil | Soy/alfalfa-free | Low dose, males only: increased insulin, insulin sensitivity and glucose intolerance; altered β-cell function | [89] |
Type 2 Diabetes | Male and Female CD-1 Mice Offspring | Gestation and Lactation | About 0.25 μg/kg | In food | Phytoestrogen-free until weaning then LFD and half mice after 9 weeks old high-fat diet | No effect on glucose tolerance | [90] |
Type 2 Diabetes | Male OF-1 Mice Offspring | Prenatal (GD9-16) | 10 μg/kg | S.C. injection; in tocopherol-stripped corn oil | Soy/alfalfa-free | No effect for insulin sensitivity; glucose intolerance; increased NEFA | [86] |
OVA Sensitization | Animal Model/Sex | Exposure Windows | BPA Dose | Routes of Administration | Diet | Effects | Reference |
---|---|---|---|---|---|---|---|
Airway Sensitization | Male and Female C57BL/6 Offspring | GD6-PND21 | 0.5, 5, 50 or 500 μg/kg | Peanut oil via gavage | AIN76-semi-PD1RR chow (phytoestrogen-free) | Increased airway lymphocytes and lung inflammation in females; decreased airway neutrophils and lung inflammation in males; no effect on IgE, T cell subpopulations or BALF cytokines | [101] |
“Suboptimal” Peritoneal Sensitization | BALB/c offspring | Gestation and Lactation | 5 or 10 μg/mL | Drinking water | Phytoestrogen-free | Increased AHR, BALF eosinophils and IgE; no effect for IgG1 | [97] |
BALB/c offspring | Prenatal, perinatal or postnatal | 5 μg/mL | Drinking water | Phytoestrogen-free | Increased AHR and BALF eosinophils from prenatal and perinatal; no effect for postnatal only exposure | [102] | |
Peritoneal Sensitization | Female C57BL/6 Offspring | GD6-PND21 | 0.5, 5, 50 or 500 μg/kg | Peanut oil via gavage | AIN76-semi-PD1RR chow (phytoestrogen-free) | Decreased airway eosinophils and IgE; no effect on AHR | [101] |
Male and Female BALB/c Offspring | Gestation and Lactation | 50 ng, 50 μg or 50 mg/kg diet | In food | AIN-93G (phytoestrogen-free) | Increased IgE, IL-13 and INF-γ; decreased BALF leukocytes, eosinophils, IL-17 and CysLTs; decreased macrophages, PMN and lung inflammation in males; in females only: decreased BALF IL-4, IL-13 and TNF-α, increased lung RANTES and no effect on lung inflammation | [103] | |
BALB/cByJ Offspring | One week after mating period until birth or PND21 | 5 μg/mL | Drinking water | C1000 (phytoestrogen-free) | Prenatal: no effect on AHR or airway inflammation; perinatal: increased lung inflammation, IgE and IL-13 | [104] | |
Female Wistar rats offspring | GD15-PND21 | 0.5, 5 or 50 μg/kg | 4% ethanol in corn oil via oral | Rodent Diet 2018 (<20 pmol estrogen content) | Increased IgG, activated T cells, splenocyte proliferation, INF-γ, neutrophils and IL-10 (colon); no effect for IgE, Treg cells or IL-10 (spleen); decreased TGF-β (colon) | [105] | |
Gavage Sensitization | Male heterozygous offspring of OVA-TCR-Tg crossed with BALB/c | Gestation and Lactation | 0, 0.1 or 1 ppm BPA | In Food | Not Specified | Increased IL-13, INFγ, anti-OVA IgG1 and anti-OVA IgG2a; no change in IL-4; decreased OVA-specific T cells and Treg response to OVA | [99] |
Sex/Age | Time of BPA Measurement | BPA Measured | BPA Levels Assessed From | Effects | Reference |
---|---|---|---|---|---|
Male and Female Infants | 1st Trimester | 0.8 μg/L | Median urine concentration | Non-monotonic increase of TSLP, IL-33 and IgE in cord blood | [68] |
Male and Female Children | 16 weeks gestation, 26 weeks gestation and birth | 2.4 μg BPA/g creatinine | Median urine concentration | Increased wheeze risk of 6 months old, but not 3 years | [106] |
Male and Female Children | 3rd trimester, 3, 5 and 7 years old | 1.8 ng/mL (3rd trimester), 3.8 ng/mL (3 years), 3.1 ng/mL (5 years), 2.7 ng/mL (7 years) | Median urine concentration | Higher prenatal BPA levels inversely correlated with wheeze at 5 years and bronchodilator response; postnatal exposure increased wheeze, airway inflammation and aeroallergen sensitization at 7 years | [107] |
Male and Female Children | 12 and 32 weeks gestation | 2.4 μg BPA/g creatinine | Median urine concentration | Increased wheeze, respiratory tract infection and bronchitis risk from 6 months–7 years old; no change in atopy/IgE levels | [108] |
Male and Female Children | 16 weeks gestation, 26 weeks gestation and birth | 2.4 μg BPA/g creatinine | Median urine concentration | Decreased lung function at 4 years, but not 5 years; 16 week BPA only: increased wheeze and persistent wheeze risk | [109] |
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Xu, J.; Huang, G.; Guo, T.L. Developmental Bisphenol A Exposure Modulates Immune-Related Diseases. Toxics 2016, 4, 23. https://doi.org/10.3390/toxics4040023
Xu J, Huang G, Guo TL. Developmental Bisphenol A Exposure Modulates Immune-Related Diseases. Toxics. 2016; 4(4):23. https://doi.org/10.3390/toxics4040023
Chicago/Turabian StyleXu, Joella, Guannan Huang, and Tai L. Guo. 2016. "Developmental Bisphenol A Exposure Modulates Immune-Related Diseases" Toxics 4, no. 4: 23. https://doi.org/10.3390/toxics4040023