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Exosomes from Inflamed Macrophages Promote the Progression of Parkinson’s Disease by Inducing Neuroinflammation

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Abstract

Inflammation is a common feature both for Parkinson’s disease (PD) and obesity-associated metabolic syndromes. Inflammation mediated by inflamed macrophages in white adipose tissue plays a pivotal role for the pathogenesis of metabolic syndromes. Exosomes are important carriers connecting peripheral tissues and the central nervous system (CNS). Therefore, we speculate that exosomes derived from inflamed macrophages may be involved in the pathological progression of PD. Here, we prepared exosomes from lipopolysaccharide (LPS) or interferon gamma (IFNγ) treated macrophages (inflamed macrophages) and examined their potential roles in PD. Our data showed that exosomes from inflamed macrophages stimulate proinflammatory cytokine expression in primary microglia and astrocytes. In vivo, inflamed macrophage exosomes induce behavioral defects in mice as evidenced by shortened duration in the rotarod test and prolonged latency in the pole test. The treatment of exosomes also reduces tyrosine hydroxylase (TH) positive cells in the substantia nigra pars compacta (SNpc) and striatum. All these PD-like phenotypes are likely due to the activation of microglia and astrocytes induced by exosomes from inflamed macrophages. Exosome sequencing, together with bioinformatics analysis and functional studies, revealed that exosomal miRNAs such as miR-155-5p are likely a key factor for inducing an inflammatory response in glial cells. These results indicate that exosomes derived from inflamed macrophages are likely a causative factor for developing PD. In this regard, inflamed macrophage exosomes might be a linker transducing the peripheral tissue inflammation into the CNS.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Funding

This work was provided by the National Key Research and Development Program of China (2017YFA0701304); the National Natural Science Foundation of China (81970747; 32271193); the Scientific Program of Changshu City (CS202236); the Scientific Program of Nantong City (MS22021010; MS22019005); the Nantong Science and Technology Foundation of China (JC2021058); and the Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Authors and Affiliations

  1. Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Co-Innovation Center of Neuroregeneration, NMPA Key Laboratory for Research and Evaluation of Tissue Engineering Technology Products, Nantong University, 19 Qixiu Road, Nantong, China

    Yan Jin, Li Li & Cheng Sun

  2. School of Life Science, Nantong University, Nantong, China

    Yan Jin

  3. Department of Endocrinology and Metabolism, Affiliated Hospital of Nantong University, Nantong, China

    Runze Wu & Yunjuan Gu

  4. Department of Endocrinology, Changshu No. 2 People’s Hospital, Changshu, China

    Runze Wu

  5. Department of Neurology, Affiliated Hospital of Nantong University, Nantong, Jiangsu Province, China

    Lihua Shen

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  1. Yan Jin
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Contributions

Y. J., R. W., and L. L. performed the experiments and analyzed the data. L. S. analyzed the data. Y. G. and C. S. designed the study. Y. J. and C. S. wrote the manuscript. C. S. supervised the study. All authors read and approved the final manuscript.

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Correspondence to Yunjuan Gu or Cheng Sun.

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Jin, Y., Wu, R., Li, L. et al. Exosomes from Inflamed Macrophages Promote the Progression of Parkinson’s Disease by Inducing Neuroinflammation. Mol Neurobiol 60, 1914–1928 (2023). https://doi.org/10.1007/s12035-022-03179-6

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