Department of Chemical and Biomolecular Engineering, University of Notre Dame, Notre Dame, Indiana 46556, United States.
Department of Chemistry, Rutgers University─Camden, Camden, New Jersey 08102, United States.
ACS Appl Bio Mater. 2024 May 20;7(5):3358-3374. doi: 10.1021/acsabm.4c00296. Epub 2024 May 8.
Exosomes are promising nanocarriers for drug delivery. Yet, it is challenging to apply exosomes in clinical use due to the limited understanding of their physiological functions. While cellular uptake of exosomes is generally known through endocytosis and/or membrane fusion, the mechanisms of origin-dependent cellular uptake and subsequent cargo release of exosomes into recipient cells are still unclear. Herein, we investigated the intricate mechanisms of exosome entry into recipient cells and intracellular cargo release. In this study, we utilized chiral graphene quantum dots (GQDs) as representatives of exosomal cargo, taking advantage of the superior permeability of chiral GQDs into lipid membranes as well as their excellent optical properties for tracking analysis. We observed that the preferential cellular uptake of exosomes derived from the same cell-of-origin (intraspecies exosomes) is higher than that of exosomes derived from different cell-of-origin (cross-species exosomes). This uptake enhancement was attributed to receptor-ligand interaction-mediated endocytosis, as we identified the expression of specific ligands on exosomes that favorably interact with their parental cells and confirmed the higher lysosomal entrapment of intraspecies exosomes (intraspecies endocytic uptake). On the other hand, we found that the uptake of cross-species exosomes primarily occurred through membrane fusion, followed by direct cargo release into the cytosol (cross-species direct fusion uptake). We revealed the underlying mechanisms involved in the cellular uptake and subsequent cargo release of exosomes depending on their cell-of-origin and recipient cell types. Overall, this study envisions valuable insights into further advancements in effective drug delivery using exosomes, as well as a comprehensive understanding of cellular communication, including disease pathogenesis.
外泌体是很有前途的药物递送载体。然而,由于对其生理功能的了解有限,外泌体在临床应用中仍具有挑战性。虽然外泌体的细胞摄取通常是通过内吞作用和/或膜融合来实现的,但外泌体起源依赖性细胞摄取和随后将货物释放到受体细胞中的机制仍不清楚。在这里,我们研究了外泌体进入受体细胞和细胞内货物释放的复杂机制。在这项研究中,我们利用手性石墨烯量子点(GQDs)作为外泌体货物的代表,利用手性 GQDs 进入脂质膜的优异渗透性以及它们用于跟踪分析的出色光学性质。我们观察到,来自同一起源细胞(同种外泌体)的外泌体的优先细胞摄取高于来自不同起源细胞(异种外泌体)的外泌体。这种摄取增强归因于受体-配体相互作用介导的内吞作用,因为我们确定了外泌体上表达的特定配体,这些配体与它们的亲本细胞有利相互作用,并证实了同种外泌体(同种内吞摄取)的溶酶体捕获更高。另一方面,我们发现异种外泌体的摄取主要通过膜融合发生,随后直接将货物释放到细胞质中(异种直接融合摄取)。我们揭示了根据外泌体的起源细胞和受体细胞类型,外泌体摄取和随后货物释放所涉及的潜在机制。总的来说,这项研究为使用外泌体进行有效的药物递送的进一步进展以及对细胞通讯(包括疾病发病机制)的全面理解提供了有价值的见解。