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Microbiota Alters and Its Correlation with Molecular Regulation Underlying Depression in PCOS Patients

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Abstract

Depression is one of the complications in patients with polycystic ovary syndrome (PCOS) that leads to considerable mental health. Accumulating evidence suggests that human gut microbiomes are associated with the progression of PCOS and depression. However, whether microbiota influences depression development in PCOS patients is still uncharacterized. In this study, we employed metagenomic sequencing and transcriptome sequencing (RNA-seq) to profile the composition of the fecal microbiota and gene expression of peripheral blood mononuclear cells in depressed women with PCOS (PCOS-DP, n = 27) in comparison to mentally healthy women with PCOS (PCOS, n = 18) and compared with healthy control (HC, n = 27) and patients with major depressive disorder (MDD, n = 29). Gut microbiota assessment revealed distinct patterns in the relative abundance in the PCOS-DP compared to HC, MDD, and PCOS groups. Several gut microbes exhibited uniquely and significantly higher abundance in the PCOS-DP compared to PCOS patients, inducing EC Ruminococcus torques, Coprococcus comes, Megasphaera elsdenii, Acidaminococcus intestini, and Barnesiella viscericola. Bacteroides eggerthii was a potential gut microbial biomarker for the PCOS-DP. RNA-seq profiling identified that 35 and 37 genes were significantly elevated and downregulated in the PCOS-DP, respectively. The enhanced differential expressed genes (DEGs) in the PCOS-DP were enriched in pathways involved in signal transduction and endocrine and metabolic diseases, whereas several lipid metabolism pathways were downregulated. Intriguingly, genes correlated with the gut microbiota were found to be significantly enriched in pathways of neurodegenerative diseases and the immune system, suggesting that changes in the microbiota may have a systemic impact on the expression of neurodegenerative diseases and immune genes. Gut microbe–related DEGs of CREB3L3 and CCDC173 were possible molecular biomarkers and therapeutic targets of women with PCOS-DP. Our multi-omics data indicate shifts in the gut microbiome and host gene regulation in PCOS patients with depression, which is of possible etiological and diagnostic importance.

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Data Availability

Raw sequence datasets of metagenome and mRNA were deposited in the NCBI Sequence Read Archive (BioProject ID PRJNA994693).

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Acknowledgements

We wish to thank Seqhealth Technology Co., LTD (Wuhan, China), for RNA-seq.

Funding

This work was supported by the Fujian Provincial Natural Science Foundation (grant number 2022J01279), the doctoral research project of the Second Affiliated Hospital of Fujian Medical University (grant number BS202203), and the Fujian Provincial Health Research Talents Training Project (grant number 2019–1-48).

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Authors and Affiliations

  1. Central Laboratory, The Second Affiliated Hospital of Fujian Medical University, Quanzhou, 362000, China

    Liying Yu

  2. Department of Endocrinology, The Second Affiliated Hospital of Fujian Medical University, Quanzhou, 362000, China

    Xiaoyu Chen & Xuefeng Bai

  3. College of Life Science, Fujian Normal University, Fuzhou, 350117, China

    Jingping Fang

  4. Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Fujian Medical University, Quanzhou, 362000, China

    Ming Sui

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Contributions

LY and JF carried out the bioinformatic analyses. XB and XC collected samples and analyzed the clinical factors. LY and MS supervised the work and wrote the manuscript.

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Correspondence to Liying Yu or Ming Sui.

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This study was performed in line with the principles of the institutional research board. Approval was granted by the Ethics Committee of the Second Affiliated Hospital of Fujian Medical University (Date 26–11-2021 /No 498).

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Yu, L., Chen, X., Bai, X. et al. Microbiota Alters and Its Correlation with Molecular Regulation Underlying Depression in PCOS Patients. Mol Neurobiol (2023). https://doi.org/10.1007/s12035-023-03744-7

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