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Role of Hippocampal miR-132-3p in Modifying the Function of Protein Phosphatase Mg2+/Mn2+-dependent 1 F in Depression

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Abstract

Depression is a common, severe, and debilitating psychiatric disorder of unclear etiology. Our previous study has shown that protein phosphatase Mg2+/Mn2+-dependent 1F (PPM1F) in the hippocampal dentate gyrus (DG) displays significant regulatory effects in depression-related behaviors. miR-132-3p plays a potential role in the etiology of depression. This study explored the effect of miR-132-3p on the onset of depression and the possible underlying mechanism for modulating PPM1F expression during the pathology of depression. We found that miR-132-3p levels in the hippocampus of depressed mice subjected to chronic unpredictable stress (CUS) were dramatically reduced, which were correlated with depression-related behaviors. Knockdown of miR-132-3p in hippocampal DG resulted in depression-related phenotypes and increased susceptibility to stress. miR-132-3p overexpression in hippocampal DG alleviated CUS-induced depression-related performance. We then screened out the potential target genes of miR-132-3p, and we found that the expression profiles of sterol regulatory element-binding transcription factor 1 (Srebf1) and forkhead box protein O3a (FOXO3a) were positively correlated with PPM1F under the condition of miR-132-3p knockdown. Finally, as anticipated, we revealed that the activities of Ca2+/calmodulin-dependent protein kinase II (CAMKII) and adenosine 5’-monophosphate (AMP)-activated protein kinase (AMPK) were reduced, which underlies the target signaling pathway of PPM1F. In conclusion, our study suggests that miR-132-3p was designed to regulate depression-related behaviors by indirectly regulating PPM1F and targeting Srebf1 and FOXO3a, which have been linked to the pathogenesis and treatment of depression.

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Data Availability

The datasets generated and analyzed during the present study are available from the corresponding author upon reasonable request.

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Funding

This work was supported by the National Natural Science Foundation of China (82171521 to CL) and Shandong Provincial Natural Science Foundation (No. ZR2022YQ65; ZR2021MH073; ZR2019PH109). The Special Funds of Taishan Scholars Project of Shandong Province (NO.tsqn202211368 to CL). Innovation and entrepreneurship training program for College Students (202110440141; 202110440042). The Projects of Medical and Health Technology Development Program in Shandong Province, China (202003090720, 202003070728, 2019WS329). Scientific Research Foundation of Binzhou Medical University (BY2020KJ03 and BY2020KJ02).

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  1. Xiangxian Ma and Qiongyu Li contributed equally to this work.

Authors and Affiliations

  1. Department of Psychology, Binzhou Medical University Hospital, No. 661 Huanghe 2nd Road, Binzhou, Shandong, 256603, China

    Xiangxian Ma, Fantao Meng, Jing Liu, Di Zhao, Wentao Wang, Dan Wang, Cuilan Liu, Juanjuan Dai, Chen Li & Minghu Cui

  2. Medical research center, Binzhou Medical University Hospital, No. 661 Huanghe 2nd Road, Binzhou, Shandong, 256603, China

    Xiangxian Ma, Qiongyu Li, Guanhong Chen, Junjie Xie, Min Wu, Fantao Meng, Jing Liu, Yong Liu, Di Zhao, Wentao Wang, Dan Wang, Cuilan Liu, Juanjuan Dai, Chen Li & Minghu Cui

  3. Institute for Metabolic & Neuropsychiatric Disorders, Binzhou Medical University Hospital, Binzhou, Shandong, China

    Xiangxian Ma, Qiongyu Li, Guanhong Chen, Junjie Xie, Min Wu, Fantao Meng, Jing Liu, Yong Liu, Di Zhao, Wentao Wang, Dan Wang, Cuilan Liu, Juanjuan Dai, Chen Li & Minghu Cui

  4. Department of Gastroenterology, Binzhou Medical University Hospital, Binzhou, Shandong, China

    Qiongyu Li

  5. The first clinical medical college, Binzhou Medical University, Yantai, Shandong, China

    Guanhong Chen & Junjie Xie

  6. Department of Neurosurgery, Binzhou Medical University Hospital, Binzhou, Shandong, China

    Min Wu

  7. Department of Physiology, Binzhou Medical University, Shandong, China

    Yong Liu

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Contributions

CL and MHC contributed to the study conception and design. Material preparation, data collection, and analysis were performed by XXM, QYL and CL with assistance from GHC, JJX, MW, FTM, JL YL, DZ, WTW, DW, CLL and JJD. The first draft of the manuscript was written by XXM and MHC, and CL modified and approved the manuscript accordingly. All authors have read and approved the final manuscript.

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Correspondence to Chen Li or Minghu Cui.

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This study was conducted per the principles of the Declaration of Helsinki. The Experimental Animal Ethics Committee of the Binzhou Medical University Hospital approved the study.

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Ma, X., Li, Q., Chen, G. et al. Role of Hippocampal miR-132-3p in Modifying the Function of Protein Phosphatase Mg2+/Mn2+-dependent 1 F in Depression. Neurochem Res 48, 2514–2530 (2023). https://doi.org/10.1007/s11064-023-03926-8

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