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Integrins mediate placental extracellular vesicle trafficking to lung and liver in vivo.

ABSTRACT: Membrane-bound extracellular vesicles (EVs) mediate intercellular communication in all organisms, and those produced by placental mammals have become increasingly recognized as significant mediators of fetal-maternal communication. Here, we aimed to identify maternal cells targeted by placental EVs and elucidate the mechanisms by which they traffic to these cells. Exogenously administered pregnancy-associated EVs traffic specifically to the lung; further, placental EVs associate with lung interstitial macrophages and liver Kupffer cells in an integrin-dependent manner. Localization of EV to maternal lungs was confirmed in unmanipulated pregnancy using a transgenic reporter mouse model, which also provided in situ and in vitro evidence that fetally-derived EVs, rarely, may cause genetic alteration of maternal cells. These results provide for the first time direct in vivo evidence that placental EVs target maternal immune cells, and further, that EVs can alter cellular phenotype.

SUBMITTER: Nguyen SL

PROVIDER: S-EPMC7893009 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Integrins mediate placental extracellular vesicle trafficking to lung and liver in vivo.

Nguyen Sean L SL Ahn Soo Hyun SH Greenberg Jacob W JW Collaer Benjamin W BW Agnew Dalen W DW Arora Ripla R Petroff Margaret G MG

Scientific reports 20210218 1

Membrane-bound extracellular vesicles (EVs) mediate intercellular communication in all organisms, and those produced by placental mammals have become increasingly recognized as significant mediators of fetal-maternal communication. Here, we aimed to identify maternal cells targeted by placental EVs and elucidate the mechanisms by which they traffic to these cells. Exogenously administered pregnancy-associated EVs traffic specifically to the lung; further, placental EVs associate with lung inters ...[more]

PMID: 33602965

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Project description:Vesicle trafficking plays an important role in delivering a diverse range of cargoes between different membranous systems in eukaryotes. It is well documented that the brefeldin A (BFA)-inhibited guanine nucleotide exchange factor (GEF), named BIG, regulates vesicle budding at the trans-Golgi network (TGN) and recycling endosomes through activating the ADP-ribosylation factor (ARFs). Among the five BIGs in Arabidopsis, BIG5 is characterized to mediate ARF-dependent trafficking at the plasma membrane or endosomes while the members from BIG1 to BIG4 (BIG1-BIG4) at the TGN in the secretory pathway. However, evidence is increasing to suggest that BIG5 can function redundantly with BIG1-BIG4 to regulate vesicular trafficking in response to various intra- and extra-cellular stimuli. In this study, our genetic analysis showed that BIG5 played an overlapping role at least with BIG3 in cell proliferation. To elucidate molecular mechanisms underlying the BIG5- and BIG3-regulated biological processes, we examined the effect of BIGs on expression patterns of the two transmembrane proteins, PINFORMED 2 (PIN2) epically localized in root epidermal cells and the regulator of G protein signaling 1 (RGS1) localized in the plasma membrane. Our data showed that the PIN2 polar distribution was slightly reduced in big3 big5 in the absence of BFA, and it was significantly reduced by the treatment of 0.1 µM BFA in big3 big5. Further analysis revealed that BFA bodies derived from the plasma membrane were only observed in wild type (WT), big3 and big5 cells, but not in the big3 big5 cells. These results indicate that BIG5 and BIG3 are functionally redundant in the endosome recycling pathway from the plasma membrane to TGN. On the other hand, the single BIG3 or BIG5 mutation had no effect on the plasma membrane expression of RGS1, whereas the double mutations in BIG3 and BIG5 led to a significant amount of RGS1 retained in the vesicle, indicating that BIG3 and BIG5 act redundantly in mediating protein trafficking. Furthermore, transmission electron microscopy assays showed that Golgi ultrastructure in big3 big5 cells was abnormal and similar to that in BFA-treated WT cells. Taken together, our data provide several new lines of evidence supporting that BIGs play a redundant role in vesicular trafficking and probably also in maintaining the Golgi structural integrity in Arabidopsis.

Dataset Information

Integrins mediate placental extracellular vesicle trafficking to lung and liver in vivo.

Publications

Integrins mediate placental extracellular vesicle trafficking to lung and liver in vivo.

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