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S41598-020-74916-X.Pdf www.nature.com/scientificreports OPEN Endoplasmic reticulum stress‑related neuroinfammation and neural stem cells decrease in mice exposure to paraquat Zhengli Yang1,4, Yiming Shao1,4, Yifan Zhao1, Qian Li1, Rui Li1,2, Hongxi Xiao1, Fen Zhang1, Yilan Zhang3, Xiuli Chang1, Yubin Zhang1* & Zhijun Zhou1* Paraquat (PQ), a widely used herbicide, could cause neurodegenerative diseases, yet the mechanism remains incompletely understood. This study aimed to investigate the direct efect of PQ on NSC in vivo and its possible mechanism. Adult C57BL/6 mice were subcutaneously injected with 2 mg/kg PQ, 20 mg/kg PQ or vehicle control once a week for 2 weeks, and sacrifced 1 week after the last PQ injection. Furthermore, extra experiments with Tauroursodeoxycholic Acid (TUDCA) intervention were performed to observe the relationship between ER stress, neuroinfammation and the neural stem cell (NSC) impairment. The results showed that 20 mg/kg PQ caused the NSC number decrease in both subgranular zones (SGZ) and subventricular zone (SVZ). Further analysis indicated that the 20 mg/kg PQ suppressed the proliferation of NSC, without afecting the apoptosis. Moreover, 20 mg/kg PQ also induced ER stress in microglia and caused neuroinfammation in SGZ and SVZ. Interestingly, the ER stress inhibitor could simultaneously ameliorate the neuroinfammation and NSC reduction. These data suggested that increased ER stress in microglia might be a possible pathway for PQ‑induced neuroinfammation and NSC impairment. That is a previously unknown mechanism for PQ neurotoxicity. Paraquat (PQ), a widely used non-selective herbicides in the world, is known for its potent neurotoxicant properties1. Indeed, the PQ toxicity has been widely discussed but is not yet fully clarifed. Te underlying mechanism may be associated with mitochondrial dysfunction, lipid peroxidation, and oxidative stress etc.2–5. In line with these data, epidemiological studies reported that PQ could result in cognitive and behavioral impairments and increase the risk of neurodegenerative diseases, such as autism spectrum disorders and Par- kinson’s disease6–8. In this context, experimental evidences showed that PQ exposure could cause permanent nerve damage in mice9,10. NSCs in the adult mammalian brain are regarded as a useful tool to regenerate neu- rons in pathological conditions such as neurodegenerative diseases or acute brain injury, indicating that the NSC impairments may be closely correlated with the nervous system diseases11. It was reported that exogenous hNSCs could improve the behavioral function in the model of Parkinson’s disease. Actually, as most primordial cell in the central nervous system, the NSC appeared to promote function preservation and/or restoration in neurodegenerative disease12. Besides, PQ-induced functional impairments in progenitor cell in vitro were also reported13–15. However, to date, there is no study evaluating the direct toxicity of PQ to NSC in vivo. In the adult rodent brain, NSCs persist in the SGZ and SVZ, which are specialized niches with a particular architecture, allowing NSCs to survive, proliferate and generate new neurons 16. NSCs generate the central nervous system (CNS) during development and persist in adult brains at the SGZ and SVZ to make and replenish difer- entiated cells lost during stress and injury17–19. Most CNS injuries elicit proliferation and migration of the NSCs toward the injury site, indicating the activation of a regenerative response. However, regeneration from NSC is incomplete, which could be due to detrimental cues encountered during infammation20. Diferent CNS diseases can cause activation of the innate and adaptive immune responses that could infuence the NSCs. Furthermore, 1School of Public Health/MOE Key Laboratory of Public Health Safety/NHC Key Lab of Health Technology Assessment, Fudan University, 130 Dong’an Road, Shanghai 200032, China. 2Pharmacology and Toxicology Department, Shanghai Institute for Food and Drug Control, Shanghai 201203, China. 3Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, Fudan University, Shanghai 200032, China. 4These authors contributed equally: Zhengli Yang and Yiming Shao. *email: [email protected]; [email protected] Scientifc Reports | (2020) 10:17757 | https://doi.org/10.1038/s41598-020-74916-x 1 Vol.:(0123456789) www.nature.com/scientificreports/ NSCs in the brain react diferently to infammatory cues than their counterparts in the spinal cord20. Tus, it is necessary to study the relation between PQ-induced infammatory and NSC in the brain. ER stress is a buildup of unfolded or misfolded proteins, which ofen happened when secreted and membrane- embedded protein translation increased or protein folding decreased in the ER lumen. In response to ER stress, the ER has evolved a capacity termed Unfolded Protein Response (UPR), which could alleviate ER stress by degrading unfolded and misfolded proteins 21. Te canonical UPR signaling is initiated by activation of three ER membrane-bound transducers: Inositol Requiring Enzyme 1 (IRE1), Activating Transcription Factor 6 (ATF6), and Protein Kinase-like ER kinase (PERK)21. Te relationship between ER stress response and infammation has gained a massive focus in biomedical research21. Regarding the PQ toxicity to NSC, numerous studies discussed its possible mechanism, but most experi- ments were based on in vitro designs. Tus, the infuences of PQ on NSC in particular regions in vivo remain incompletely defned. To date, the relationships between PQ-induced ER stress and neuroinfammation, NSC impairments are unknown. In this study, we especially focused on SGZ and SVZ where NSCs persist and found that PQ-induced NSC impairment and neuroinfammation, could be restored by an ER stress inhibitor–Tauro- ursodeoxycholic Acid (TUDCA)22,23. Results PQ reduced the number of NSC in SGZ and SVZ. To investigate the efects of PQ on NSC, the immu- nohistochemical experiments were performed to detect the NSC in SGZ and SVZ. As shown in Fig. 1a, b, 20 mg/ kg PQ decreased the number of NSC (marked by the black arrow). Next, using CD45 and SOX2 antibodies 24 in fow cytometry analysis, we quantifed the percentage of NSC. Consistently, the results confrmed the reduction in NSC of SGZ and SVZ (Fig. 1c, d). PQ infuenced the proliferation but not apoptosis of NSC in SGZ and SVZ. As the decrease of NSC was observed in SGZ and SVZ from mice treated with 20 mg/kg PQ, we hypothesized that the reduction was due to increased apoptosis or suppressed proliferation. To test this, we frstly measured the apoptosis of NSC in SGZ and SVZ, based on the cleaved (active) Caspase-3, a molecule driving cellular apoptosis25. We found that PQ did not infuence the apoptosis of NSC (Fig. 2a, b). Further analysis indicated that PQ also did not afect the expression of B-cell lymphoma-2 (Bcl-2) of NSC in the SGZ and SVZ. Bcl-2 is an anti-apoptotic protein that could prevent cellular apoptosis 26. Next, we further tested the proliferation of NSC in SGZ and SVZ, based on their nuclear expression of Ki6727. Te results showed that 20 mg/kg PQ inhibited the Ki67 expression of NSC in both zones (Fig. 2e, f). Moreover, immunohistochemistry staining also confrmed the suppressed proliferation of NSC in SGZ and SVZ (marked by white arrow) (Fig. 2g, h). PQ activated microglia and induced neuroinfammation in SGZ and SVZ. PQ-induce neuroin- fammation in mice have been widely discussed previously. Specially, we wanted to know whether the infamma- tion happened in SGZ and SVZ afer PQ exposure in our study. Terefore, we measured the level of infammatory cytokines, including IL-6, IL-1β and TNF-α, in both zones by ELISA. As predicted, 20 mg/kg PQ signifcantly increased the level of IL-6, IL-1β, and TNF-α in SGZ and SVZ (Fig. 3a, b), indicating neuroinfammation indeed happened in SVZ and SGZ where the NSC were mainly present. As microglia played a vital role in neuroinfam- mations diseases28, we next measured the activation of microglia in SGZ and SVZ by western blots, based on their surface expression of CD11b, and their cytoskeletal protein Iba1 (Fig. 3c, d). Te results revealed that the expression of CD11b and Iba1 in SGZ from mice treated with 20 mg/kg PQ was signifcantly increased. But, limited by the biological characteristics of SVZ, the total protein levels in SVZ were too low to detect a target protein. We failed to evaluate the expression of CD11b and Iba1 in SVZ. Te quantifcation of CD11b and Iba1 in SGZ were showed in Fig. 3e, f. To confrm the Iba1 increase, we further detected the microglia in SGZ and SVZ by immunohistochemistry staining. As expected, the Iba1 (marked by black arrow) in the mice treated with 20 mg/kg PQ had increased in both zones (Fig. 3g, h). Moreover, using fow cytometry, we quantifed the microglia by CD45 antibody29, and evaluated the activation of microglia by detecting the expression of the Major Histocompatibility Complex class II molecules (MHC-II; I-A). As shown in Fig. 3i–k, 20 mg/kg PQ did not infuence the percentage of microglia in the brain, but it resulted in the activation of microglia. PQ resulted in increased ER stress in microglia. It was reported that ER stress and microglia played a vital role in infammation-related diseases 30. ER stress is mainly composed of three fundamental branches, including IRE1, PERK and XBP-1s. First, using western blots, we measured the activated IRE1α (p-IRE1α) in SGZ but not SVZ because of the low protein levels in SVZ. Te results showed that in comparison with controls, the p-IRE1 was remarkably higher in mice treated with 20 mg/kg PQ (Fig. 4a, b). Ten, using fow cytometry, we found that 20 mg/kg PQ also raised the expression of p-PERK and XBP-1 s of microglia (CD45+cells) in SGZ (Fig. 4c, d). TUDCA alleviated the neuroinfammation and NSC impairments.
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