Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells
Abstract Extracellular vesicles (EVs) released from non-small cell lung cancer (NSCLC) cells are known to promote cancer progression. However, it remains unclear how EVs from various NSCLC cells differ in their secretion profile and their ability to promote phenotypic changes in non-tumorigenic cell...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2022-01-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-04940-6 |
| _version_ | 1798016305129848832 |
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| author | Humna Hasan Ikjot Singh Sohal Zulaida Soto-Vargas Anjali M. Byappanhalli Sean E. Humphrey Hana Kubo Sarunya Kitdumrongthum Sarah Copeland Feng Tian Arthit Chairoungdua Andrea L. Kasinski |
| author_facet | Humna Hasan Ikjot Singh Sohal Zulaida Soto-Vargas Anjali M. Byappanhalli Sean E. Humphrey Hana Kubo Sarunya Kitdumrongthum Sarah Copeland Feng Tian Arthit Chairoungdua Andrea L. Kasinski |
| author_sort | Humna Hasan |
| collection | DOAJ |
| description | Abstract Extracellular vesicles (EVs) released from non-small cell lung cancer (NSCLC) cells are known to promote cancer progression. However, it remains unclear how EVs from various NSCLC cells differ in their secretion profile and their ability to promote phenotypic changes in non-tumorigenic cells. Here, we performed a comparative analysis of EV release from non-tumorigenic cells (HBEC/BEAS-2B) and several NSCLC cell lines (A549, H460, H358, SKMES, and Calu6) and evaluated the potential impact of NSCLC EVs, including EV-encapsulated RNA (EV-RNA), in driving invasion and epithelial barrier impairment in HBEC/BEAS-2B cells. Secretion analysis revealed that cancer cells vary in their secretion level, with some cell lines having relatively low secretion rates. Differential uptake of NSCLC EVs was also observed, with uptake of A549 and SKMES EVs being the highest. Phenotypically, EVs derived from Calu6 and H358 cells significantly enhanced invasion, disrupted an epithelial barrier, and increased barrier permeability through downregulation of E-cadherin and ZO-1. EV-RNA was a key contributing factor in mediating these phenotypes. More nuanced analysis suggests a potential correlation between the aggressiveness of NSCLC subtypes and the ability of their respective EVs to induce cancerous phenotypes. |
| first_indexed | 2024-04-11T15:48:45Z |
| format | Article |
| id | doaj.art-0ae5ae319258460e925d72bd51b86a99 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-11T15:48:45Z |
| publishDate | 2022-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-0ae5ae319258460e925d72bd51b86a992022-12-22T04:15:27ZengNature PortfolioScientific Reports2045-23222022-01-0112111810.1038/s41598-022-04940-6Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cellsHumna Hasan0Ikjot Singh Sohal1Zulaida Soto-Vargas2Anjali M. Byappanhalli3Sean E. Humphrey4Hana Kubo5Sarunya Kitdumrongthum6Sarah Copeland7Feng Tian8Arthit Chairoungdua9Andrea L. Kasinski10Department of Biological Sciences, Purdue UniversityDepartment of Biological Sciences, Purdue UniversityDepartment of Biological Sciences, Purdue UniversityDepartment of Biological Sciences, Purdue UniversityDepartment of Biological Sciences, Purdue UniversityDepartment of Biological Sciences, Purdue UniversityToxicology Graduate Program, Faculty of Science, Mahidol UniversityDepartment of Biological Sciences, Purdue UniversityDepartment of Biological Sciences, Purdue UniversityDepartment of Physiology, Faculty of Science, Mahidol UniversityDepartment of Biological Sciences, Purdue UniversityAbstract Extracellular vesicles (EVs) released from non-small cell lung cancer (NSCLC) cells are known to promote cancer progression. However, it remains unclear how EVs from various NSCLC cells differ in their secretion profile and their ability to promote phenotypic changes in non-tumorigenic cells. Here, we performed a comparative analysis of EV release from non-tumorigenic cells (HBEC/BEAS-2B) and several NSCLC cell lines (A549, H460, H358, SKMES, and Calu6) and evaluated the potential impact of NSCLC EVs, including EV-encapsulated RNA (EV-RNA), in driving invasion and epithelial barrier impairment in HBEC/BEAS-2B cells. Secretion analysis revealed that cancer cells vary in their secretion level, with some cell lines having relatively low secretion rates. Differential uptake of NSCLC EVs was also observed, with uptake of A549 and SKMES EVs being the highest. Phenotypically, EVs derived from Calu6 and H358 cells significantly enhanced invasion, disrupted an epithelial barrier, and increased barrier permeability through downregulation of E-cadherin and ZO-1. EV-RNA was a key contributing factor in mediating these phenotypes. More nuanced analysis suggests a potential correlation between the aggressiveness of NSCLC subtypes and the ability of their respective EVs to induce cancerous phenotypes.https://doi.org/10.1038/s41598-022-04940-6 |
| spellingShingle | Humna Hasan Ikjot Singh Sohal Zulaida Soto-Vargas Anjali M. Byappanhalli Sean E. Humphrey Hana Kubo Sarunya Kitdumrongthum Sarah Copeland Feng Tian Arthit Chairoungdua Andrea L. Kasinski Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells Scientific Reports |
| title | Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells |
| title_full | Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells |
| title_fullStr | Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells |
| title_full_unstemmed | Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells |
| title_short | Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells |
| title_sort | extracellular vesicles released by non small cell lung cancer cells drive invasion and permeability in non tumorigenic lung epithelial cells |
| url | https://doi.org/10.1038/s41598-022-04940-6 |
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