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Abou Diwan, M.; Lahimer, M.; Bach, V.; Gosselet, F.; Khorsi-Cauet, H.; Candela, P. Pesticide Residues on the Gut-Microbiota–Blood–Brain Barrier Axis. Encyclopedia. Available online: https://encyclopedia.pub/entry/43093 (accessed on 21 December 2024).
Abou Diwan M, Lahimer M, Bach V, Gosselet F, Khorsi-Cauet H, Candela P. Pesticide Residues on the Gut-Microbiota–Blood–Brain Barrier Axis. Encyclopedia. Available at: https://encyclopedia.pub/entry/43093. Accessed December 21, 2024.
Abou Diwan, Maria, Marwa Lahimer, Véronique Bach, Fabien Gosselet, Hafida Khorsi-Cauet, Pietra Candela. "Pesticide Residues on the Gut-Microbiota–Blood–Brain Barrier Axis" Encyclopedia, https://encyclopedia.pub/entry/43093 (accessed December 21, 2024).
Abou Diwan, M., Lahimer, M., Bach, V., Gosselet, F., Khorsi-Cauet, H., & Candela, P. (2023, April 16). Pesticide Residues on the Gut-Microbiota–Blood–Brain Barrier Axis. In Encyclopedia. https://encyclopedia.pub/entry/43093
Abou Diwan, Maria, et al. "Pesticide Residues on the Gut-Microbiota–Blood–Brain Barrier Axis." Encyclopedia. Web. 16 April, 2023.
Pesticide Residues on the Gut-Microbiota–Blood–Brain Barrier Axis
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This entry is adapted from the peer-reviewed paper 10.3390/ijms24076147

The intestinal barrier (IB) and blood–brain barrier (BBB) are considered immunological and physical barriers. Each barrier not only provides protection against invading pathogens but is also important for controlling the microenvironment of the tissue and, therefore, tightly regulates the movement of the molecules and ions between the cellular spaces. These barriers have many similarities in their mechanisms of action despite providing defense in very different environments. Unlike the BBB, the IB is constantly exposed to food antigens and contaminants and is colonized by a collection of bacteria and microorganisms’ antigens of the microbiota. The gut microbiota (GM) is a real organ system that includes a diverse and complex population of microorganisms colonizing the digestive tract and having a symbiotic host’s relationship that helps to maintain a dynamic metabolic and ecological balance.

barriers pesticides gut

1. Pesticide Residues Exposure and Effects on the Gut and Blood–Brain Barrier

One important connection between the gut and the brain is the microbiota. This means that any dysregulation of the microbiota (named dysbiosis) can affect the two parts of this axis. Oral-exposure substances that can disrupt microbiota can be in diet, drugs, antibiotics, and, most importantly in this review, pesticide residues.
Pesticide residues are food and water contaminants. Some of them alter the composition of the gut microbiota (GM) and disrupt and cross the IB [1][2][3]. They are defined by the Food and Agriculture Organization (FAO) as any substance or mixture of substances intended for preventing, destroying, or controlling any pest, including vectors of human or animal disease, unwanted species of plants or animals, causing harm during or otherwise interfering with human activities (production, processing, storage, transport, marketing of food, agricultural commodities, etc.) [4]. These substances are classified based on various criteria, such as the targeted pest organism type (fungicide, herbicide, insecticide, etc.), chemical composition (e.g., synthetic organic insecticides: organochlorines, organophosphates, carbamates, and pyrethroids), and mode of entry in the body [5][6]. The mode of action of pesticides targets the physiological systems of the pests they kill, but this can result in poisoning nontarget species, such as humans (phylogenetic similarities in digestive, respiratory, and nervous systems). Since the beginning of the 20th century, the use of pesticides and fertilizers is intensive to ensure large agriculture production to adapt with demographic growth. The most frequently used chemical families in agriculture are the synthetic organic insecticides mentioned above and triazines [7]. This means that researchers are not only exposed to one or two but to a mixture of environmentally persistent pesticides daily. Thus, the assessment of the impact of these substances nowadays should consider the chronic cumulative effect as well as the cocktail effect [8][9][10]. The concept of metabolization (biotransformation by microbiota bacteria and liver detoxification enzymes) is also a point of interest because the pesticide metabolite can be more harmful than the parent compound, indicating a metabolic activation. Generally, oxon-type intermediate metabolites are more hazardous than their parent pesticide. Organophosphates oxon-metabolites are an example of more toxic metabolites than the corresponding pesticide: Chlorpyrifos-oxon (CPF-oxon) is more potent than Chlorpyrifos (CPF) itself, same as for paraoxon and parathion [11][12][13]. The neurotoxic effects and impact on the gut-microbiota-blood–brain barrier (BBB) axis of the most detected pesticides in food (according to the EFSA European Food Safety Authority) [14] are detailed in Table 1. This research details the effects of the most used organophosphate insecticide, CPF, on the gut-microbiota-BBB axis.
Table 1. Neurotoxic effects and impact of pesticides on the gut-microbiota-BBB axis. AChE: acetylcholinesterase; BBB: blood–brain barrier; C57BL/6: C57 black cellCaE: carboxylesterase; ChE: cholinesterase; CPF: Chlorpyrifos; IB: intestinal barrier; IL: interleukin; IMZ: imazalil; IFN-ɣ: Interferon gamma; ppm: parts per million; Lcn-2: Lipocaline 2; N2a: mouse neuroblastoma cells; PC12: rat Pheochromocytoma cells; SHIME: Simulator of Human Intestinal Microbial Ecosystem; TEER: transendothelial electrical resistance; TJs: tight junctions; TNF-α: tumor necrosis factor; TRPC4: transient receptor potential canonical channels; ZOs: zonula occludens. ↓ and ↑ symbols refer to decrease and increase, respectively.
Pesticides Effect on Gut Effect on Microbiota Effect on BBB Neurotoxic Effect References
Organophosaphates          
Chlorpyrifos (CPF) a. ↓ in epithelial thickness of ileum and colon of rats after exposure to 1 mg/kg/day of CPF
↓ of tight junction gene expression of the intestinal barrier and ↑ of proinflammatory cytokines		 c. Exposure to 1 mg/kg/day of CPF-induced (1) microbial dysbiosis in pregnant rats and offspring, a ↓ in potentially beneficial flora and an ↑ of the potentially pathogen one, and (2) bacterial translocation to sterile organs d. Altered gene expression levels of claudin 5, ZO-1, and TRPC4 genes disrupting the barrier integrity in an in vitro BBB model e. Exposure to 1.5 (low dose) and 3 (high dose) mg/kg/day of CPF-induced inhibition of cholinesterase in rats in a dose-related manner
f. Inhibition of carboxylesterase (CaE) and cholinesterase (ChE) activities by 43–100% in an vitro BBB model treated with (0.1 to 10 µM) of CPF		 a. [15][16][17]
b. [18][19][20]
c. [16][21][22][23]
d and f. [24]
e. [25]
  b. ↓ of TJs gene expression of the IB (Caco-2/TC-7 model treated with SHIME supernatant exposed to 3.5 mg of CPF for 30 days)     g. Exposure of pregnant rats to 1 and 5 mg/kg/day of CPF-induced inhibition of AChE of juvenile and adult offspring leading to high sleep apnea index g. [26]
Diazinon   h. Exposure to 4 ppm for 13 weeks in drinking water had an impact on bacterial populations and composition of Lachnospiraceae, Ruminococcaceae, Clostridiaceae, and Erysipelotrichaceae in male mice   i. Exposure to 0.5 and 2 mg/kg/day induced long-lasting alterations in cognitive function in adolescence and extending into adulthood of rats h. [27][28][29]
i. [30]
Malathion   j. ↓ in bacterial populations (depletion of 4 genera) in male mice exposed to 2 mg/mL in drinking water for 13 weeks k. ↓ in the TEER in two BBB in vitro models treated with malathion (10−3 to 10−8 M) l. Induces neurotoxicity through ChE inhibition and non-cholinergic mode: apoptotic cell death by targeting mitochondria in N2a neuroblastoma mouse cells (at 0.25, 0.5, or 1 mM for 8 h) j. [27][29]
k. [31]
l. [32]
Herbicides          
Glyphosate m. ↑ in proinflammatory cytokines transcriptomic expression (IL-1β, IL-6, and TNF-α) after exposure to 5, 50, and 500 mg/kg for 35 days in male rats n. ↓ in the relative abundance of Firmicutes and Lactobacillus but increased Fusobacteria in male rats exposed to 500 mg/kg for 35 days o. ↑ in barrier permeability to fluorescein (at 1 and 10 µM of glyphosate) and ↓ in claudin-5 fluorescence intensity (at 100 and 1000 µM) after 24 h treatment of the BBB model p. 24 h of treatment with high doses of glyphosate (100 µM) can affect neurons metabolic activity m and n. Q. [3]
o and p. [33]
Fungicides          
Imazalil q. ↑ in a colonic inflammation biomarker (Lcn-2)
↑ in mRNA levels of TNF-α, IL-1β, IL-22, and IFN-ɣ in the colon after exposure to 100 mg/kg bw/day IMZ for 28 days in mice		 r. ↓ in Bacteroidetes, Firmicutes, and Actinobacteria in the colon after exposure to 100 mg/kg bw/day IMZ for 28 days in mice   s. ↑ in oxidative stress ↑basal calcium ions Ca2+ (indicating inhibition of depolarization-evoked
calcium influx) in an in vitro model of rat dopaminergic PC12 cells treated with 100 µM of IMZ		 q and r. [1]
s. [34][35]
  t. 15 weeks administration of IMZ at doses of 0.1, 0.5, and 2.5 mg/kg/day to C57BL/6 mice led to:   u. 48% inhibition of AChE by IMZ (at 500 µM, in vitro enzymatic inhibition assays) t. [36]
u. [37]
  IB dysfunction gut-microbiota dysbiosis  

1.1. Chlorpyrifos (CPF)

1.1.1. Chlorpyrifos Utilizations until 2022

Organophosphorus pesticides are extensively used worldwide because of the wide range of pests they kill, the broad spectrum of applications (food trees, wheat, corn, almonds, tea, etc.), and their persistence in soil [11][38]. Chlorpyrifos (CPF) is the most commonly used thionophosphorus organophosphate insecticide, available on the market at a low price since 1965, especially in France, one of the first pesticide consumers in Europe. In 1998, only one study was sufficient for the European Union (EU) to give use approval of CPF, but it took more than hundreds of studies showing neurotoxic, metabolic, and endocrine effects to make the decision in 2019 limiting its use. Nonetheless, CPF production has not been banned. Therefore, pollution in the environment is still present. After the ban of CPF use in the EU by the EFSA, except for the culture of spinach in France, the EPA (United States Environmental Protection Agency) made a recent regulatory decision banning CPF for food uses in the United States in February 2022 (EPA final rule) [39]. However, on one hand, it is still allowed for mosquito control, on tobacco, on plantations not for feed purposes, and on food destined to export when it complies with foreign purchaser specifications (updates on CPF uses in 2022, Iowa State University) [40]. Therefore, these limitations do not prevent the accumulation of CPF in the soil and then in water and thus its uptake by aquatic species and its entry into the food chain of human beings [41]. And still, many other regions of the world including China and India continue allowing CPF on crops. On the other hand, it has been demonstrated by many studies on the biotransformation of CPF in soil that its half-life has a very wide range, from 360 days to 17 years, because its fate depends on the initial concentration used on plants and the biodegradation rate. This means that even after limitations, measures should be taken concerning the control of CPF residues in soil, local and imported food, and most importantly in human blood or urine. In addition, strict measures should be adopted in countries where residents have easy access to this dangerous pesticide: in Iran, CPF residues are found in the milk of breast-feeding mothers, their urine, and even their children’s urine [42]. A total of 92% of these mothers confirmed pesticides’ house use, an activity banned since 2001 in the US [43]. Rathod and Garg reported a scenario in India where the commonest method of suicide (40.5%) is organophosphorus compound (OPC) intake [11][44]. Therefore, limitations are essential in these countries to protect residents and their future generations.

1.1.2. Chlorpyrifos Mechanism of Toxicity and Toxicokinetic

Chlorpyrifos is absorbed by all routes of exposure. Urinalyses of exposed human volunteers indicate that approximately 70% is absorbed by the oral route [11][45]. After CPF exposure and then distribution throughout the body, cytochrome P450 (CYP) in the liver metabolizes CPF, replacing the sulfur group with oxygen, to CPF-oxon, a metabolite that is more toxic than CPF itself. The detoxification of CPF-oxon consists of oxidase enzymes hydrolyzing it to diethylphosphate (DEP), diethyl thiophosphate (DETP), and 3,5,6-trichloro-2-pyridinol (TCP) [11]. TCP is a specific metabolite of CPF, whereas DEP and DETP can be detected after exposure to other organophosphates [46][47]. It is the metabolic bioactivation to CPF-oxon that leads to the irreversible inhibition of acetylcholinesterase (AChE) preventing the breakdown of acetylcholine (ACh), a neurotransmitter that ensures nerve cells communication. The accumulation of ACh in the synaptic cleft overstimulates the neuronal cells, leading to a collapse in the nervous system of insects (National Pesticide Information Center) [48]. Similarly, in higher vertebrae, in particular humans, CPF has a cholinergic effect and has been demonstrated to have a plethora of non-cholinergic effects.

1.1.3. Chlorpyrifos Biotransformation by Intestinal and Soil Bacteria

The research on xenobiotics degradation in the human body mostly focuses on detoxification by CYP and other liver enzymes, but based on the literature, a minority of the studies focus on their degradation by intestinal microorganisms and specifically bacteria. A 2013 study by Harishankar and colleagues found that 70% of CPF was degraded to TCP by Lactobacillus fermentum, 61% to CPF-oxon by Lactobacillus lactis, and 16% of CPF to CPF-oxon and DEP by Escherichia coli [49]. Recently, insect experimental studies were conducted to investigate the fate of pesticides by an intestinal microorganism [50]. A 2021 study assessed the biodegradation of organophosphorus including CPF by isolating insect gut microbial species. Four potential bacterial endosymbionts such as Bacillus subtilis, Bacillus licheniformis, Pseudomonas putida, and Pseudomonas cereus used CPF as a unique source of carbon and energy for their growth and enzymatic function. They found that Pseudomonas cereus and Pseudomonas putida have more potential to degrade the CPF [51].
Similarly, in soils, the researchers suggested that CPF is totally degraded by microorganisms and especially by Pseudomonas putida MB285 to form the primary products TCP and DETP, which are further decomposed into non-toxic metabolites, such as CO2, H2O, and NH3 [52]. Pseudomonas is a diverse genus with multiple degradation pathways. It was reported that Pseudomonas putida MAS-1 had the highest degradation efficiency for CPF in Pseudomonas genus, with a 90% degradation rate within 24 h [53]. Furthermore, another study published in 2008 reported that different bacteria contribute to the biodegradation of CPF in five aerobic consortia, based on antibiotic resistance survival and REP-PCR (Repetitive Extragenic Palindromic Polymerase Chain Reaction). The results illustrated that 75–87% of the CPF was degraded to TCP after 20 days of incubation by Pseudomonas aeruginosa, Pseudomonas fluorescence, Bacillus subtilis, Brucella melitensis, Klebsiella sp., Bacillus cereus, and Serratia marcescens. However, the results also showed that the TCP disappeared after 30 days of incubation [54]. A mini review published by Supreeth in 2017 evaluated the biotransformation of CPF and endosulfan by bacteria and fungi and discussed the aftereffects of their transformed byproducts (metabolites) [38]. The degradation of CPF to TCP was executed by different bacteria species, Enterobacter sp., Stenotrophomonas sp., Sphingomonas sp. [55], Pseudomonas aeruginosa, Bacillus cereus, Klebsiella sp., Serratia marscecens [56], Bacillus subtilis inaquosorum strain KCTC13429, B. cereus ATCC 14579, and B. safensis F0-36b [57], and to CPF-oxon 3,6-Dihydroxypyridine-2,5-dione and DETP by Pseudomonas putida (NII 1117) Klebsiella sp. (NII 1118) P. stutzeri (NII 1119), P.aeruginosa (NII 1120) [58], and Ralstonia sp. Strain T6 [59].

1.1.4. Chlorpyrifos Effects on Gut-Microbiota-Blood–Brain Barrier Axis

As the gut and microbiota have an impact on the absorption and metabolization of pesticides, these pesticides can have serious effects on all parts of the gut–brain axis. Prenatal pesticide exposure studies detected parent molecules of organophosphates and/or their metabolites, CPF in particular, in meconium [60][61][62][63]. In fact, meconium has become a biomarker of in utero pollutants exposure. At this stage of rapid growth and development, especially of the brain, humans are more vulnerable and sensitive to the toxic effects of pesticides [64][65]. The message behind these analyses is that even before birth, which means before gut microbial colonization, researchers are exposed to CPF, which seems to cross the placental barrier. In addition, considering the oral route, before reaching the brain to inhibit acetylcholinesterase, the first organ to encounter CPF or any food contaminant is the digestive tract. Thus, it is necessary to investigate the organophosphate effects on the intestinal tract. Working on the rat offspring NOAEL of 1 mg/kg/day, Joly et al. studied the effect of 1 mg/kg/day or 5 mg/kg/day of CPF perinatal exposure on the GM of the rats’ progeny at two developmental time points: weaning (D21) and adulthood (D60) [16]. Their results show that CPF exposure induces microbial dysbiosis: a decrease in Lactobacillus spp. counts in the ileum, cecum, and colon as well as a decrease in Bifidobacterium spp. at D21 in the ileum and D60 in the colon, and an increase in Clostridium spp. and Staphylococcus spp. counts in the cecum and colon at D21. This means that CPF exposure reduces potentially beneficial bacteria and increases potentially pathogenic ones. The epithelial thickness of the ileum and colon was decreased by CPF treatment. Because the first study was based on classical microbiology tests, they researched further to identify more specifically intestinal bacteria by MALDI-TOF-MS and investigate bacterial translocation from intestinal segments to sterile organs [22]. By molecular typing, they were able to confirm the translocation of Staphylococcus aureus to adipose tissues, kidney, and Peyer’s patch from 12.5% of CPF-exposed rats’ intestinal segments and a 5% translocation of Enterococcus faecalis to the liver. This is logically explained by the increase in gut permeability induced by the decrease in ZO-1 and claudin 4 transcriptional expression in the ileum and colon, especially on D21 [66]. CPF exposure of an in vitro artificial human intestine (SHIME®) combined with a Caco-2/TC-7 model was associated with a decrease in the tight junction gene expression, occludin and ZO-1, and an increase in the proinflammatory chemokine interleukin-8 (IL-8) [20]. Zhao et al. also confirmed abnormal intestinal permeability in CPF-exposed mice and reported microbiota dysbiosis (a decrease in Lactobacillaceae and Firmicutes and an increase in Bacteroidaceae and Bacteroides) and alterations in the metabolism of SCFAs that led to intestinal inflammation [2]. This is an expected result because CPF treatment alters the microbial community that produces these metabolites. In addition, an analysis of serum showed an increase in LPS by CPF treatment. J. W. Li and colleagues showed that chronic exposure to 0.3 mg CPF/ kg body weight/day induced a significant increase in TNF-α and IL-6 in the serum of exposed rats [67]. These observations might explain the alterations in the functional integrity and structure of the BBB by CPF, highlighted by Parran et al. who worked on an in vitro BBB model (bovine endothelial cells and neonatal rat astrocytes) [24]. Another study on an in vitro BBB model (rat brain endothelial cells and neonatal rat astrocytes) showed that the short-term CPF treatment at low concentrations alters the expression levels of the claudin 5, ZO-1, and TRPC4 (transient receptor potential canonical channels) genes, disrupting the BBB integrity (TRPC regulates the calcium influx that modulates the paracellular permeability of the endothelial cells of the BBB) [68]. The claudin 5 gene is the main tight junction gene involved in the BBB tightness and ZO-1 ensures the support to the TJs’ architecture [69][70]. Thus, CPF targets the most important actors of the BBB integrity.
Because the exposure to pesticides is often accompanied with saturated fats and refined sugars (an unbalanced diet based on fast food and processed food), other studies assessed the impact of the association of CPF to a High Fat Diet (HFD) on intestinal microbiota and the IB. Guibourdenche and colleagues confirmed that the chronic perinatal exposure to the NOAEL dose of CPF alone induced a decrease in transcriptional TJs expression and also demonstrated an increase in proinflammatory cytokines and is aggravated by the association to an HFD [15][23].
These experimentations all together point to the impact of CPF on the entire gut-BBB axis even though its main mechanism is the inhibition of acetylcholinesterase in neurons. Further investigations are necessary to identify molecular pathways that explain the barriers’ disruption by organophosphates.

1.1.5. Chlorpyrifos Molecular Pathways Underlying Its Effects

In parallel to studies analyzing the effects of organophosphates on the gut–brain axis, there are several studies investigating the molecular pathways associated to them. It has been demonstrated that organophosphates induce apoptosis by affecting signaling molecules, including c-Jun NH2-terminal protein kinase (JNK), p38 MAP kinase, and extracellular signal regulated protein kinase (ERK1/2) [71][72]. ERK1/2 is activated by neurotrophic factors and growth factors, whereas environmental stresses such as reactive oxygen species (ROS) activate JNK and p38 MAP kinases. The activation of JNK and p38 MAP kinases induces apoptosis, while the activation of ERK1/2 is protective against it [73]. In fact, CPF increases JNK, ERK1/2, and p38 MAPK phosphorylation [74]. It is known that mitogen-activated protein kinases (MAPKs) regulate matrix metalloproteinases (MMPs). MMP9 is regulated by ERK1/2 [75]. MMP9 activation yet increased the IB permeability in a Caco-2 in vitro model [76]. MMP9 upregulation leads to BBB leakage as well, through the rearrangement and/or degradation of the tight junctions [77][78]. Moreover, MAPKs have a role in the inflammatory response. Interestingly, CPF can upregulate cyclooxygenase 2 (COX-2) through MAPK activation [74]. In addition, CPF upregulates inflammation-related genes and the protein level of NF-κB and TNF-α [79] which in turn can deteriorate the BBB permeability [80]. A possible explanation for the CPF implication in these pathways is as follows: CPF increases NADPH oxidases (NOXs) and superoxide levels which increase ROS signaling and oxidative stress in cells [81]. The increase in ROS signaling induces, on one hand, the upregulation of TNF-α and NF-κB and, on the other hand, the increase in the ASK1 expression responsible for the activation of JNK upregulation which is one of the MAPKs that regulates MMPs.

2. Beneficial Modulation of the Gut-Microbiota–Brain Axis

Recent studies on pesticide effects are focusing on a new concept: the recovery. In fact, a study of the effect of different doses of imazalil on mice GM evaluated the time of recovery after 2 and 15 weeks of exposure. They found that 30 or 45 days after impregnation with this fungicide, the bacterial composition at the phylum level recovered to the control level [36]. This highlights the fact that a change in the microbiota composition is flexible and tends to regain balance. In addition, new clinical trials indicated that the gut-microbiota–brain axis pathways and mechanisms are prone to dietary modulation and are of vital interest in clinical nutrition. As a matter of fact, dietary interventions and supplementation with probiotics and prebiotics can reshape the bacterial composition and are now administered as “psychobiotics” to treat neurological disorders because of their beneficial effects on the brain [82]. This means that by reshaping the GM, the whole gut-microbiota-BBB axis is positively modulated. The concept of probiotic use in the modulation of gut microflora was initiated in the 19th century by Elie Metchnikoff who theorized that “health and longevity could be achieved by manipulating intestinal microflora, i.e., replacing harmful microbes with beneficial microbes” while prebiotics were introduced by Gibson and Roberfroid in 1995 [83].
Their supplementation is now considered a promising approach that alleviates the negative effects of food contaminants [84]. In effect, bacterial strains that are considered probiotic strains (mostly Lactobacillus strains) can bind to xenobiotics and reduce their toxicity (through biotransformation) and the amount absorbed by the host [85]. Lactobacilli spp. are known to have the highest anti-inflammatory effects [86]. To exert their beneficial roles, probiotic strains need substrates. Prebiotics partially provide probiotic strains with substrates that are “nondigestible food ingredients which selectively stimulate the growth and activity of beneficial bacterial species already implanted in the colon, and thus improve the health of the host” [87]. Prebiotics are fructo-oligosaccharides (FOS) such as inulin, galacto-oligosaccharides (GOS), trans-galacto-oligosaccharides (TOS), and resistant starch which can be found in many fruits, vegetables, grains, and milk [88][89].
Arabinoxylo-oligosaccharides and inulin induced an increase in some SCFAs (acetate, propionate, and butyrate) and a shift in the microbial composition from Firmicutes to Bacteroidetes [90]. Similarly, Sialyllactose (isolated from milk) and GOS induced the differentiation of the epithelial cells in the Caco-2 model, the modulation of the microbial composition (an increase in Bacteroides and Bifidobacteria), and consequently the production of SCFAs [91]. In fact, the fermentation of prebiotics by gut bacteria produces SCFAs which can reach the bloodstream by diffusing through gut enterocytes and have beneficial effects on the host [88]. In effect, an in vitro study linking the Caco-2 model and SHIME demonstrated that arabinogalactan and FOS decreased proinflammatory cytokines (IL-6 and IL-8), increased the anti-inflammatory cytokine IL-10, and improved the gut barrier permeability (the TEER measurements of the Caco-2 model) [92]. These findings emphasize the direct effect of prebiotics on IB function through the modulation of the microbiota composition. However, these oligosaccharides and the products of their fermentation (SCFAs) can improve IB function through TJs modulation [93]. Many studies underline the role of inulin [94] and FOS [95] in enhancing IB through TJs assembly.
Because they have a beneficial effect on the IB and microbial composition, researchers investigated if pretreatment or supplementation with prebiotics could attenuate damage in an inflammatory environment or intestinal harm caused by food contaminants exposure. As an example, GOS pretreatment can alleviate damage of the IB in an inflammatory environment (in LPS-challenged mice) [96]. Additionally, inulin supplementation to rats exposed to CPF, an HFD, or the association of both CPF and a HFD and in in vitro models (SHIME and Caco-2) reversed their effects on microbial composition by increasing potentially beneficial flora (Lactobacillus and Bifidobacterium), decreasing potentially pathogenic ones (Enterococcus and Enterobacteriacea) and improving the IB integrity [19][20][21][23]. Thus, prebiotics use through nutrition can modulate the GM with beneficial outcomes. New methods are now emerging such as fecal transplantation, a strategy to deal with dysbiosis, that has been shown to have a positive effect on the treatment of Parkinson’s disease [97].

References

  1. Jin, C.; Zeng, Z.; Fu, Z.; Jin, Y. Oral Imazalil Exposure Induces Gut Microbiota Dysbiosis and Colonic Inflammation in Mice. Chemosphere 2016, 160, 349–358.
  2. Zhao, Y.; Zhang, Y.; Wang, G.; Han, R.; Xie, X. Effects of Chlorpyrifos on the Gut Microbiome and Urine Metabolome in Mouse (Mus musculus). Chemosphere 2016, 153, 287–293.
  3. Tang, Q.; Tang, J.; Ren, X.; Li, C. Glyphosate Exposure Induces Inflammatory Responses in the Small Intestine and Alters Gut Microbial Composition in Rats. Environ. Pollut. 2020, 261, 114129.
  4. FAO; WHO. International Code of Conduct on the Distribution and Use of Pesticides Guidelines on Developing a Reporting System for Health and Environmental Incidents Resulting from Exposure to Pesticide; FAO: Rome, Italy; WHO: Geneva, Switzerland, 2009; ISBN 9789251068311.
  5. Akashe, M.M.; Pawade, U.V.; Nikam, A.V. Classification of Pesticides: A Review. Int. J. Res. Ayurveda Pharm. 2018, 9, 144–150.
  6. Kaur, R.; Mavi, G.K.; Raghav, S.; Khan, I. Pesticides Classification and Its Impact on Environment. Int. J. Curr. Microbiol. Appl. Sci. 2017, 8, 1889–1897.
  7. Carvalho, F.P. Pesticides, Environment, and Food Safety. Food Energy Secur. 2017, 6, 48–60.
  8. Aroonvilairat, S.; Tangjarukij, C.; Sornprachum, T.; Chaisuriya, P.; Siwadune, T.; Ratanabanangkoon, K. Effects of Topical Exposure to a Mixture of Chlorpyrifos, Cypermethrin and Captan on the Hematological and Immunological Systems in Male Wistar Rats. Environ. Toxicol. Pharmacol. 2018, 59, 53–60.
  9. Lukowicz, C.; Ellero-simatos, S.; Régnier, M.; Polizzi, A.; Lasserre, F.; Montagner, A.; Lippi, Y.; Jamin, E.L.; Martin, J.; Naylies, C.; et al. Metabolic Effects of a Chronic Dietary Exposure to a Low-Dose Pesticide Cocktail in Mice: Sexual Dimorphism and Role of the Constitutive Androstane Receptor. Environ. Health Perspect. 2018, 126, 067007.
  10. Smith, L.; Klément, W.; Dopavogui, L.; De Bock, F.; Lasserre, F.; Barretto, S.; Lukowicz, C.; Fougerat, A.; Polizzi, A.; Schaal, B.; et al. Perinatal Exposure to a Dietary Pesticide Cocktail Does Not Increase Susceptibility to High-Fat Diet-Induced Metabolic Perturbations at Adulthood but Modi Fi Es Urinary and Fecal Metabolic Fi Ngerprints in C57Bl6/J Mice. Environ. Int. 2020, 144, 106010.
  11. Rathod, A.L.; Garg, R.K. Chlorpyrifos Poisoning and Its Implications in Human Fatal Cases: A Forensic Perspective with Reference to Indian Scenario. J. Forensic Leg. Med. 2017, 47, 29–34.
  12. Kaur, R. Metabolism of Pesticides by Human Cytocrome P450 (CYPs). Int. J. Creat. Res. Thoughts 2018, 6, 1293–1300.
  13. Parathion|ToxFAQsTM|ATSDR. Available online: https://wwwn.cdc.gov/TSP/ToxFAQs/ToxFAQsDetails.aspx?faqid=1426&toxid=246 (accessed on 15 March 2023).
  14. Carrasco Cabrera, L.; Medina Pastor, P. The 2019 European Union Report on Pesticide Residues in Food. EFSA J. 2021, 19, e06491.
  15. Guibourdenche, M.; El Khayat El Sabbouri, H.; Djekkoun, N.; Khorsi-Cauet, H.; Bach, V.; Anton, P.M.; Gay-Quéheillard, J. Programming of Intestinal Homeostasis in Male Rat Offspring after Maternal Exposure to Chlorpyrifos and/or to a High Fat Diet. Sci. Rep. 2021, 11, 11420.
  16. Joly Condette, C.; Bach, V.; Mayeur, C.; Gay-Quéheillard, J.; Khorsi-Cauet, H. Chlorpyrifos Exposure during Perinatal Period Affects Intestinal Microbiota Associated with Delay of Maturation of Digestive Tract in Rats. J. Pediatr. Gastroenterol. Nutr. 2015, 61, 30–40.
  17. Reygner, J.; Condette, C.J.; Bruneau, A.; Delanaud, S.; Rhazi, L.; Depeint, F.; Abdennebi-Najar, L.; Bach, V.; Mayeur, C.; Khorsi-Cauet, H. Changes in Composition and Function of Human Intestinal Microbiota Exposed to Chlorpyrifos in Oil as Assessed by the SHIME® Model. Int. J. Environ. Res. Public Health 2016, 13, 1088.
  18. Tirelli, V.; Catone, T.; Turco, L.; Di Consiglio, E.; Testai, E.; De Angelis, I. Effects of the Pesticide Clorpyrifos on an in Vitro Model of Intestinal Barrier. Toxicol. Vitr. 2007, 21, 308–313.
  19. Reygner, J.; Lichtenberger, L.; Elmhiri, G.; Dou, S.; Bahi-Jaber, N.; Rhazi, L.; Depeint, F.; Bach, V.; Khorsi-Cauet, H.; Abdennebi-Najar, L. Inulin Supplementation Lowered the Metabolic Defects of Prolonged Exposure to Chlorpyrifos from Gestation to Young Adult Stage in Offspring Rats. PLoS ONE 2016, 11, e0164614.
  20. Réquilé, M.; Gonzàlez Alvarez, D.O.; Delanaud, S.; Rhazi, L.; Bach, V.; Depeint, F.; Khorsi-Cauet, H. Use of a Combination of in Vitro Models to Investigate the Impact of Chlorpyrifos and Inulin on the Intestinal Microbiota and the Permeability of the Intestinal Mucosa. Environ. Sci. Pollut. Res. 2018, 25, 22529–22540.
  21. Djekkoun, N.; Depeint, F.; Guibourdenche, M.; El Khayat El Sabbouri, H.; Corona, A.; Rhazi, L.; Gay-Queheillard, J.; Rouabah, L.; Hamdad, F.; Bach, V.; et al. Chronic Perigestational Exposure to Chlorpyrifos Induces Perturbations in Gut Bacteria and Glucose and Lipid Markers in Female Rats and Their Offspring. Toxics 2022, 10, 138.
  22. Joly Condette, C.; Elion Dzon, B.; Hamdad, F.; Biendo, M.; Bach, V.; Khorsi-Cauet, H. Use of Molecular Typing to Investigate Bacterial Translocation from the Intestinal Tract of Chlorpyrifos-Exposed Rats. Gut Pathog. 2016, 8, 50.
  23. Djekkoun, N.; Depeint, F.; Guibourdenche, M.; El, H.; Et, K.; Aurélie, S.; Rhazi, L.; Gay, J.; Leila, Q.; Maurice, R.; et al. Perigestational Exposure of a Combination of a High-Fat Diet and Pesticide Impacts the Metabolic and Microbiotic Status of Dams and Pups; a Preventive Strategy Based on Prebiotics. Eur. J. Nutr. 2022, 62, 1253–1265.
  24. Parran, D.K.; Magnin, G.; Li, W.; Jortner, B.S.; Ehrich, M. Chlorpyrifos Alters Functional Integrity and Structure of an in Vitro BBB Model: Co-Cultures of Bovine Endothelial Cells and Neonatal Rat Astrocytes. Neurotoxicology 2005, 26, 77–88.
  25. Betancourt, A.M.; Carr, R.L. The Effect of Chlorpyrifos and Chlorpyrifos-Oxon on Brain Cholinesterase, Muscarinic Receptor Binding, and Neurotrophin Levels in Rats Following Early Postnatal Exposure. Toxicol. Sci. 2004, 71, 63–71.
  26. El, H.; El, K.; Darwiche, W. Impact of Chronic Exposure to the Pesticide Chlorpyrifos on Respiratory Parameters and Sleep Apnea in Juvenile and Adult Rats. PLoS ONE 2018, 13, e0191237.
  27. Gao, A.B.; Chi, L.; Tu, P.; Bian, X.; Thomas, J.; Ru, H.; Lu, K. The Organophosphate Malathion Disturbs Gut Microbiome Development and the Quorum-Sensing System. Toxicol. Lett. 2017, 283, 52–57.
  28. Gao, B.; Bian, X.; Chi, L.; Tu, P.; Ru, H.; Lu, K. Organophosphate Diazinon Altered Quorum Sensing, Cell Motility, Stress Response, and Carbohydrate Metabolism of Gut Microbiome. Toxicol. Sci. 2017, 157, 354–364.
  29. Meng, Z.; Liu, L.; Yan, S.; Sun, W.; Jia, M.; Tian, S.; Huang, S.; Zhou, Z.; Zhu, W. Gut Microbiota: A Key Factor in the Host Health Effects Induced by Pesticide Exposure. J. Agric. Food Chem. 2020, 68, 10517–10531.
  30. Timofeeva, O.A.; Roegge, C.S.; Seidler, F.J.; Slotkin, T.A.; Levin, E.D. Persistent Cognitive Alterations in Rats after Early Postnatal Exposure to Low Doses of the Organophosphate Pesticide, Diazinon. Neurotoxicol. Teratol. 2008, 30, 38–45.
  31. Balbuena, P.; Li, W.; Magnin-bissel, G.; Meldrum, J.B.; Ehrich, M. Comparison of Two Blood-Brain Barrier In Vitro Systems: Cytotoxicity and Transfer Assessments of Malathion/Oxon and Lead Acetate. Toxicol. Sci. 2010, 114, 260–271.
  32. Venkatesan, R.; Park, Y.U.; Ji, E.; Yeo, E.; Kim, S.Y. Malathion Increases Apoptotic Cell Death by Inducing Lysosomal Membrane Permeabilization in N2a Neuroblastoma Cells: A Model for Neurodegeneration in Alzheimer’s Disease. Cell Death Discov. 2017, 11, 17007.
  33. Martinez, A.; Al-ahmad, A.J. Effects of Glyphosate and Aminomethylphosphonic Acid on an Isogeneic Model of the Human Blood-Brain Barrier. Toxicol. Lett. 2018, 304, 39–49.
  34. Heusinkveld, H.J.; Molendijk, J.; Van Den Berg, M.; Westerink, R.H.S. Azole Fungicides Disturb Intracellular Ca2+ in an Additive Manner in Dopaminergic PC12 Cells. Toxicol. Sci. 2013, 134, 374–381.
  35. Heusinkveld, H.J.; Westerink, R.H.S. Comparison of Different in Vitro Cell Models for the Assessment of Pesticide-Induced Dopaminergic Neurotoxicity Authors. Toxicol. Vitr. 2017, 45, 81–88.
  36. Jin, C.; Xia, J.; Wu, S.; Tu, W.; Pan, Z.; Fu, Z.; Wang, Y.; Jin, Y. Insights into a Possible Influence on Gut Microbiota and Intestinal Barrier Function During Chronic Exposure of Mice to Imazalil. Toxicol. Sci. 2018, 162, 113–123.
  37. Martins-gomes, C.; Coutinho, T.E.; Silva, T.L.; Andreani, T.; Silva, M. In Vitro Enzymatic Inhibition Assays. Toxics 2022, 10, 448.
  38. Supreeth, M.; Raju, N. Biotransformation of Chlorpyrifos and Endosulfan by Bacteria and Fungi. Appl. Microbiol. Biotechnol. 2017, 101, 5961–5971.
  39. EPA. Frequent Questions about the Chlorpyrifos 2021 Final Rule|US EPA. Available online: https://www.epa.gov/ingredients-used-pesticide-products/frequent-questions-about-chlorpyrifos-2021-final-rule (accessed on 5 March 2023).
  40. Iowa State University. Updates on Chlorpyrifos Uses in 2022|Integrated Crop Management. Available online: https://crops.extension.iastate.edu/cropnews/2022/03/updates-chlorpyrifos-uses-2022 (accessed on 5 March 2023).
  41. Zhang, Q.; Zheng, S.; Wang, S.; Wang, W.; Xing, H.; Xu, S. Chlorpyrifos Induced Oxidative Stress to Promote Apoptosis and Autophagy through the Regulation of MiR-19a-AMPK Axis in Common Carp. Fish Shellfish Immunol. 2019, 93, 1093–1099.
  42. Brahmand, M.B.; Yunesian, M.; Nabizadeh, R.; Nasseri, S.; Alimohammadi, M. Evaluation of Chlorpyrifos Residue in Breast Milk and Its Metabolite in Urine of Mothers and Their Infants Feeding Exclusively by Breast Milk in North of Iran. J. Environ. Heal. Sci. Eng. 2019, 17, 817–825.
  43. Zhao, K.; Song, X.; Huang, Y.; Yao, J.; Zhou, M.; Li, Z.; You, Q.; Guo, Q.; Lu, N. Wogonin Inhibits LPS-Induced Tumor Angiogenesis via Suppressing PI3K/Akt/NF-ΚB Signaling. Eur. J. Pharmacol. 2014, 737, 57–69.
  44. Prasad, J.; Abraham, V.J.; Minz, S.; Abraham, S.; Joseph, A.; Muliyil, J.P.; George, K.; Jacob, K.S. Rates and Factors Associated with Suicide in Kaniyambadi Block, Tamil Nadu, South India, 2000−2002. Int. J. Soc. Psychiatry 2006, 52, 65–71.
  45. Nolan, R.J.; Rick, D.L.; Freshour, N.L.; Saunders, J.H. Chlorpyrifos: Pharmacokinetics in human volunteers. Toxicol. Appl. Pharmacol. 1984, 15, 8–15.
  46. Sancho, J.V.; Pozo, O.J. Direct Determination of Chlorpyrifos and Its Main Serum and Urine by Coupled-Column Liquid Chromatography/Electrospray-Tandem Mass Spectrometry. Rapid Commun. Mass Spectrom. 2000, 1490, 1485–1490.
  47. Yang, F.; Li, J.; Pang, G.; Ren, F.; Fang, B. Effects of Diethyl Phosphate, a Non-Specific Metabolite of Organophosphorus Pesticides, on Serum Lipid, Hormones, Inflammation, and Gut Microbiota. Molecules 2019, 24, 2003.
  48. NPIC. Chlorpyrifos Technical Fact Sheet by the National Pesticide Information Center. Available online: http://npic.orst.edu/factsheets/archive/chlorptech.html (accessed on 5 March 2023).
  49. Harishankar, M.K.; Sasikala, C.; Ramya, M. Efficiency of the Intestinal Bacteria in the Degradation of the Toxic Pesticide, Chlorpyrifos. 3 Biotech 2013, 3, 137–142.
  50. Wang, Z.; Wang, W.; Lu, Y. Biodegradation of Insecticides by Gut Bacteria Isolated from Stored Grain Beetles and Its Implication in Host Insecticide Resistance. J. Stored Prod. Res. 2022, 96, 101943.
  51. Ibrahim, S.; Gupta, R.K.; War, A.R.; Hussain, B.; Kumar, A.; Sofi, T.; Noureldeen, A.; Darwish, H. Degradation of Chlorpyriphos and Polyethylene by Endosymbiotic Bacteria from Citrus Mealybug. Saudi J. Biol. Sci. 2021, 28, 3214–3224.
  52. Liu, J.; Tan, L.; Wang, J.; Wang, Z.; Ni, H.; Li, L. Complete Biodegradation of Chlorpyrifos by Engineered Pseudomonas Putida Cells Expressing Surface-Immobilized Laccases. Chemosphere 2016, 157, 200–207.
  53. Gilani, R.A.; Rafique, M.; Rehman, A.; Munis, M.F.H.; Rehman, S.U.; Chaudhary, H.J. Biodegradation of Chlorpyrifos by Bacterial Genus Pseudomonas. J. Basic Microbiol. 2016, 56, 105–119.
  54. Vidya Lakshmi, C.; Kumar, M.; Khanna, S. Biotransformation of Chlorpyrifos and Bioremediation of Contaminated Soil. Int. Biodeterior. Biodegrad. 2008, 62, 204–209.
  55. Li, X.; Jiang, J.; Gu, L.; Ali, S.W.; He, J.; Li, S. Diversity of Chlorpyrifos-Degrading Bacteria Isolated from Chlorpyrifos-Contaminated Samples. Int. Biodeterior. Biodegrad. 2008, 62, 331–335.
  56. Vidya Lakshmi, C.; Kumar, M.; Khanna, S. Biodegradation of Chlorpyrifos in Soil by Enriched Cultures. Curr. Microbiol. 2009, 58, 35–38.
  57. Ishag, A.E.S.A.; Abdelbagi, A.O.; Hammad, A.M.A.; Elsheikh, E.A.E.; Elsaid, O.E.; Hur, J.H.; Laing, M.D. Biodegradation of Chlorpyrifos, Malathion, and Dimethoate by Three Strains of Bacteria Isolated from Pesticide-Polluted Soils in Sudan. J. Agric. Food Chem. 2016, 64, 8491–8498.
  58. Sasikala, C.; Jiwal, S.; Rout, P.; Ramya, M. Biodegradation of Chlorpyrifos by Bacterial Consortium Isolated from Agriculture Soil. World J. Microbiol. Biotechnol. 2012, 28, 1301–1308.
  59. Li, J.; Liu, J.; Shen, W.; Zhao, X.; Hou, Y.; Cao, H.; Cui, Z. Isolation and Characterization of 3,5,6-Trichloro-2-Pyridinol-Degrading Ralstonia sp. Strain T6. Bioresour. Technol. 2010, 101, 7479–7483.
  60. Ostrea, E.M.; Morales, V.; Ngoumgna, E.; Prescilla, R.; Tan, E.; Hernandez, E.; Ramirez, G.B.; Cifra, H.L.; Manlapaz, M.L. Prevalence of Fetal Exposure to Environmental Toxins as Determined by Meconium Analysis. Neurotoxicology 2002, 23, 329–339.
  61. Berton, T.; Mayhoub, F.; Chardon, K.; Duca, R.C.; Lestremau, F.; Bach, V.; Tack, K. Development of an Analytical Strategy Based on LC-MS/MS for the Measurement of Different Classes of Pesticides and Theirs Metabolites in Meconium: Application and Characterisation of Foetal Exposure in France. Environ. Res. 2014, 132, 311–320.
  62. El-Baz, M.A.; El-Deek, S.E.; Nsar, A.Y.; El-Maali, N.A.; AbdelHafez, F.F.; Amin, A.F. Prenatal Pesticide Exposure: Meconium as a Biomarker and Impact on Fetal Weight. J. Environ. Anal. Toxicol. 2015, 5, 1000268.
  63. Onchoi, C.; Kongtip, P.; Nankongnab, N.; Chantanakul, S.; Sujirarat, D.; Woskie, S. Organophosphates in Meconium of Newborn Babies Whose Mothers Resided in Agricultural Areas of Thailand. Southeast Asian J. Trop. Med. Public Health 2020, 51, 77–87.
  64. Bruckner, J.V. Differences in Sensitivity of Children and Adults to Chemical Toxicity: The NAS Panel Report. Regul. Toxicol. Pharmacol. 2000, 31, 280–285.
  65. Richardson, J.R.; Fitsanakis, V.; Westerink, R.H.S.; Kanthasamy, A.G. Neurotoxicity of Pesticides. Acta Neuropathol. 2019, 138, 343–362.
  66. Condette, C.J.; Khorsi-Cauet, H.; Morlière, P.; Zabijak, L.; Reygner, J.; Bach, V.; Gay-Quéheillard, J. Increased Gut Permeability and Bacterial Translocation after Chronic Chlorpyrifos Exposure in Rats. PLoS ONE 2014, 9, e102217.
  67. Li, J.W.; Fang, B.; Pang, G.F.; Zhang, M.; Ren, F.Z. Age- and Diet-Specific Effects of Chronic Exposure to Chlorpyrifos on Hormones, Inflammation and Gut Microbiota in Rats. Pestic. Biochem. Physiol. 2019, 159, 68–79.
  68. Li, W.; Ehrich, M. Transient Alterations of the Blood-Brain Barrier Tight Junction and Receptor Potential Channel Gene Expression by Chlorpyrifos. J. Appl. Toxicol. 2013, 33, 1187–1191.
  69. Abbott, N.J.; Patabendige, A.A.K.; Dolman, D.E.M.; Yusof, S.R.; Begley, D.J. Structure and Function of the Blood-Brain Barrier. Neurobiol. Dis. 2010, 37, 13–25.
  70. Profaci, C.P.; Munji, R.N.; Pulido, R.S.; Daneman, R. The Blood–Brain Barrier in Health and Disease: Important Unanswered Questions. J. Exp. Med. 2020, 217, e20190062.
  71. Chang, A.Y. Pro-Life Role for c-Jun N-Terminal Kinase and P38 Mitogen-Activated Protein Kinase at Rostral Ventrolateral Medulla in Experimental Brain Stem Death. J. Biomed. Sci. 2012, 19, 96.
  72. Farkhondeh, T.; Mehrpour, O.; Buhrmann, C.; Pourbagher-Shahri, A.M.; Shakibaei, M.; Samarghandian, S. Organophosphorus Compounds and MAPK Signaling Pathways. Int. J. Mol. Sci. 2020, 21, 4258.
  73. Yue, J.; López, J.M. Understanding MAPK Signaling Pathways in Apoptosis. Int. J. Mol. Sci. 2020, 21, 2346.
  74. Ki, Y.W.; Park, J.H.; Lee, J.E.; Shin, I.C.; Koh, H.C. JNK and P38 MAPK Regulate Oxidative Stress and the Inflammatory Response in Chlorpyrifos-Induced Apoptosis. Toxicol. Lett. 2013, 218, 235–245.
  75. Vandooren, J.; Van Den Steen, P.E.; Opdenakker, G. Biochemistry and Molecular Biology of Gelatinase B or Matrix Metalloproteinase-9 (MMP-9): The next Decade. Crit. Rev. Biochem. Mol. Biol. 2013, 48, 222–272.
  76. Al-Sadi, R.; Youssef, M.; Rawat, M.; Guo, S.; Dokladny, K.; Haque, M.; Watterson, M.D.; Ma, T.Y. MMP-9-Induced Increase in Intestinal Epithelial Tight Permeability Is Mediated by P38 Kinase Signaling Pathway Activation of MLCK Gene. Am. J. Physiol.-Gastrointest. Liver Physiol. 2019, 316, G278–G290.
  77. Bauer, A.T.; Bürgers, H.F.; Rabie, T.; Marti, H.H. Matrix Metalloproteinase-9 Mediates Hypoxia-Induced Vascular Leakage in the Brain via Tight Junction Rearrangement. J. Cereb. Blood Flow Metab. 2010, 30, 837–848.
  78. Turner, R.J.; Sharp, F.R. Implications of MMP9 for Blood Brain Barrier Disruption and Hemorrhagic Transformation Following Ischemic Stroke. Front. Cell. Neurosci. 2016, 10, 56.
  79. Chen, J.; Shao, B.; Wang, J.; Shen, Z.; Liu, H.; Li, S. Chlorpyrifos Caused Necroptosis via MAPK/NF-ΚB/TNF-α Pathway in Common Carp (Cyprinus carpio L.) Gills. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2021, 249, 109126.
  80. Versele, R.; Sevin, E.; Gosselet, F.; Fenart, L.; Candela, P. TNF-α and IL-1 β Modulate Blood-Brain Barrier Permeability and Decrease Amyloid- β Peptide Efflux in a Human Blood-Brain Barrier Model. Int. J. Mol. Sci. 2022, 23, 10235.
  81. Sule, R.O.; Condon, L.; Gomes, A.V. A Common Feature of Pesticides: Oxidative Stress—The Role of Oxidative Stress in Pesticide-Induced Toxicity. Oxid. Med. Cell. Longev. 2022, 2022, 5563759.
  82. Ribeiro, G.; Ferri, A.; Clarke, G.; Cryan, J.F. Diet and the Microbiota–Gut–Brain-Axis: A Primer for Clinical Nutrition. Curr. Opin. Clin. Nutr. Metab. Care 2022, 25, 443–450.
  83. Idrees, M.; Imran, M.; Atiq, N.; Zahra, R.; Abid, R.; Alreshidi, M.; Roberts, T.; Abdelgadir, A.; Tipu, M.K.; Farid, A.; et al. Probiotics, Their Action Modality and the Use of Multi-Omics in Metamorphosis of Commensal Microbiota into Target-Based Probiotics. Front. Nutr. 2022, 9, 1–21.
  84. Akimowicz, M.; Srednicka, P.; Juszczuk-kubiak, E.; Micha, W.; Roszko, M.Ł. Probiotics as a Biological Detoxification Tool of Food Chemical Contamination: A Review. Food Chem. Toxicol. 2021, 153, 112306.
  85. Daisley, B.A.; Monachese, M.; Trinder, M.; Bisanz, J.E.; John, A.; Burton, J.P.; Reid, G.; Daisley, B.A.; Monachese, M.; Trinder, M.; et al. Immobilization of Cadmium and Lead by Lactobacillus rhamnosus GR-1 Mitigates Apical-to-Basolateral Heavy Metal Translocation in a Caco-2 Model of the Intestinal Epithelium Intestinal Epithelium. Gut Microbes 2019, 10, 321–333.
  86. D’Amelio, P.D. Gut Microbiota, Immune System, and Bone. Calcif. Tissue Int. 2017, 102, 415–425.
  87. Gibson, G.R.; Roberfroid, M.B. Dietary Modulation of the Human Colonic Microbiota: Introducing the Concept of Prebiotics. J. Nutr. 1995, 125, 1401–1412.
  88. Davani-Davari, D.; Negahdaripour, M.; Karimzadeh, I.; Seifan, M.; Mohkam, M.; Masoumi, S.J.; Berenjian, A.; Ghasemi, Y. Prebiotics: Definition, Types, Sources, Mechanisms, and Clinical Applications. Foods 2019, 8, 92.
  89. Long-Smith, C.; O’Riordan, K.J.; Clarke, G.; Stanton, C.; Dinan, T.G.; Cryan, J.F. Microbiota-Gut-Brain Axis: New Therapeutic Opportunities. Annu. Rev. Pharmacol. Toxicol. 2020, 60, 477–502.
  90. Van Den Abbeele, P.; Taminiau, B.; Pinheiro, I.; Duysburgh, C.; Jacobs, H.; Pijls, L.; Marzorati, M. Arabinoxylo-Oligosaccharides and Inulin Impact Inter-Individual Variation on Microbial Metabolism and Composition, Which Immunomodulates Human Cells. J. Agric. Food Chem. 2018, 66, 1121–1130.
  91. Perdijk, O.; Van Baarlen, P.; Fernandez-gutierrez, M.M.; Van Den Brink, E. Sialyllactose and Galactooligosaccharides Promote Epithelial Barrier Functioning and Distinctly Modulate Microbiota Composition and Short Chain Fatty Acid Production In Vitro. Front. Immunol. 2019, 10, 94.
  92. Daguet, D.; Pinheiro, I.; Verhelst, A.; Possemiers, S. Arabinogalactan and Fructooligosaccharides Improve the Gut Barrier Function in Distinct Areas of the Colon in the Simulator of the Human Intestinal Microbial Ecosystem. J. Funct. Foods 2016, 20, 369–379.
  93. Rose, E.C.; Odle, J.; Blikslager, A.T.; Ziegler, A.L. Probiotics, Prebiotics and Epithelial Tight Junctions: A Promising Approach to Modulate Intestinal Barrier Function. Int. J. Mol. Sci. 2021, 22, 6729.
  94. Uerlings, J.; Schroyen, M.; Willems, E.; Tanghe, S.; Bruggeman, G. Differential Effects of Inulin or Its Fermentation Metabolites on Gut Barrier and Immune Function of Porcine Intestinal Epithelial Cells. J. Funct. Foods 2020, 67, 103855.
  95. Wongkrasant, P.; Pongkorpsakol, P.; Ariyadamrongkwan, J.; Muanprasat, C. Biomedicine & Pharmacotherapy Original Article A Prebiotic Fructo-Oligosaccharide Promotes Tight Junction Assembly in Intestinal Epithelial Cells via an AMPK-Dependent Pathway. Biomed. Pharmacother. 2020, 129, 110415.
  96. Wang, G.; Sun, W.; Pei, X.; Jin, Y.; Wang, H.; Tao, W.; Xiao, Z.; Liu, L.; Wang, M. Function Galactooligosaccharide Pretreatment Alleviates Damage of the Intestinal Barrier and inflammatory Responses in LPS-Challenged Mice. Food Funct. 2021, 12, 1569–1579.
  97. Smith, L.M.; Parr-Brownlie, L.C. A Neuroscience Perspective of the Gut Theory of Parkinson’s Disease. Eur. J. Neurosci. 2019, 49, 817–823.
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Maria Abou Diwan
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