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Exosomes: efficient macrophage-related immunomodulators in chronic lung diseases

Kang, Jianxiong, Hua, Peiyan, Wu, Xiaojing, Wang, Bin·2024·Frontiers in Cell and Developmental Biology
DOI 10.3389/fcell.2024.1271684PMC PMC11035777
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Abstract

Macrophages, the predominant immune cells in the lungs, play a pivotal role in maintaining the delicate balance of the pulmonary immune microenvironment. However, in chronic inflammatory lung diseases and lung cancer, macrophage phenotypes undergo distinct transitions, with M1-predominant macrophages promoting inflammatory damage and M2-predominant macrophages fostering cancer progression. Exosomes, as critical mediators of intercellular signaling and substance exchange, participate in pathological reshaping of macrophages during development of pulmonary inflammatory diseases and lung cancer. Specifically, in inflammatory lung diseases, exosomes promote the pro-inflammatory phenotype of macrophages, suppress the anti-inflammatory phenotype, and subsequently, exosomes released by reshaped macrophages further exacerbate inflammatory damage. In cancer, exosomes promote pro-tumor tumor-associated macrophages (TAMs); inhibit anti-tumor TAMs; and exosomes released by TAMs further enhance tumor proliferation, metastasis, and resistance to chemotherapy. Simultaneously, exosomes exhibit a dual role, holding the potential to transmit immune-modulating molecules and load therapeutic agents and offering prospects for restoring immune dysregulation in macrophages during chronic inflammatory lung diseases and lung cancer. In chronic inflammatory lung diseases, this is manifested by exosomes reshaping anti-inflammatory macrophages, inhibiting pro-inflammatory macrophages, and alleviating inflammatory damage post-reshaping. In lung cancer, exosomes reshape anti-tumor macrophages, inhibit pro-tumor macrophages, and reshaped macrophages secrete exosomes that suppress lung cancer development. Looking ahead, efficient and targeted exosome-based therapies may emerge as a promising direction for treatment of pulmonary diseases.

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FIGURE 1 Exosome production process, contents, and delivery: the process initiates with invagination of the plasma membrane, forming early sorting endosomes (ESEs) that encapsulate extracellular components. These ESEs can fuse with intracellularly synthesized substances or exchange biomaterials, leading to the formation of late sorting endosomes (LSEs). Further maturation gives rise to intracellular multivesicular bodies (MVBs), from which intraluminal vesicles (ILVs) are selectively sorted and eventually released into the extracellular space as extracellular vesicles. In addition, three forms of extracellular vesicle uptake by recipient cells were described, including membrane fusion, receptor binding (signal transduction), and endocytosis.
FIGURE 1 Exosome production process, contents, and delivery: the process initiates with invagination of the plasma membrane, forming early sorting endosomes (ESEs) that encapsulate extracellular components. These ESEs can fuse with intracellularly synthesized substances or exchange biomaterials, leading to the formation of late sorting endosomes (LSEs). Further maturation gives rise to intracellular multivesicular bodies (MVBs), from which intraluminal vesicles (ILVs) are selectively sorted and eventually released into the extracellular space as extracellular vesicles. In addition, three forms of extracellular vesicle uptake by recipient cells were described, including membrane fusion, receptor binding (signal transduction), and endocytosis.CC BY · PubMed Central
FIGURE 2 Pathogenesis and treatment of exosome-associated inflammatory lung disease: in inflammatory lung diseases, exosomes can be secreted by damaged airway epithelial cells, prompting macrophages to differentiate toward the pro-inflammatory phenotype and suppressing anti-inflammatory differentiation; while pro-inflammatory macrophages in turn use exosomes for further airway epithelial damage, fibroblast activation, and activation of other immune cells, forming a vicious circle to amplify inflammation and injury. However, the treatment of inflammatory lung diseases is delivered to macrophages through a variety of stem cell exosomes and synthetic drug-encapsulated exosomes, which induce anti-inflammatory differentiation and inhibit pro-inflammatory differentiation of macrophages, or the use of anti-inflammatory macrophage-secreted exosomes that act on other cells to mitigate the damage and destruction of lung tissue.
FIGURE 2 Pathogenesis and treatment of exosome-associated inflammatory lung disease: in inflammatory lung diseases, exosomes can be secreted by damaged airway epithelial cells, prompting macrophages to differentiate toward the pro-inflammatory phenotype and suppressing anti-inflammatory differentiation; while pro-inflammatory macrophages in turn use exosomes for further airway epithelial damage, fibroblast activation, and activation of other immune cells, forming a vicious circle to amplify inflammation and injury. However, the treatment of inflammatory lung diseases is delivered to macrophages through a variety of stem cell exosomes and synthetic drug-encapsulated exosomes, which induce anti-inflammatory differentiation and inhibit pro-inflammatory differentiation of macrophages, or the use of anti-inflammatory macrophage-secreted exosomes that act on other cells to mitigate the damage and destruction of lung tissue.CC BY · PubMed Central
FIGURE 3 Pathogenesis and treatment of exosome-associated lung cancer: lung cancer cells use exosomes to alter macrophage subpopulations to form a tumor microenvironment, and dysregulated macrophages facilitate a variety of malignant behaviors such as growth, metastasis, and drug resistance of lung cancer cells through exosomes. In contrast, treatment of lung cancer can begin by awakening anti-tumor macrophages in macrophages and inhibiting tumor-assisting macrophages, and anti-tumor macrophages will also inhibit the proliferation and development of tumor cells through exosomes.
FIGURE 3 Pathogenesis and treatment of exosome-associated lung cancer: lung cancer cells use exosomes to alter macrophage subpopulations to form a tumor microenvironment, and dysregulated macrophages facilitate a variety of malignant behaviors such as growth, metastasis, and drug resistance of lung cancer cells through exosomes. In contrast, treatment of lung cancer can begin by awakening anti-tumor macrophages in macrophages and inhibiting tumor-assisting macrophages, and anti-tumor macrophages will also inhibit the proliferation and development of tumor cells through exosomes.CC BY · PubMed Central

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Metadata

Authors
Kang, J., Hua, P., Wu, X., & Wang, B.
Venue
Frontiers in Cell and Developmental Biology
Publisher
Frontiers Media SA
Published
2024-04-09
Volume
12
ISSN
2296-634X
DOI
10.3389/fcell.2024.1271684
PMC
PMC11035777
Cited by
22
References
3
Licence
creativecommons.org/licenses/by/4.0/ (vor)

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

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