Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts

Exosomes, small extracellular vesicles secreted by various cell types, have gained significant attention in cancer investigations. Isolation and characterization of exosomes derived from DOK (dysplastic oral keratinocyte), SCC (squamous cell carcinoma) and HaCaT (normal skin keratinocyte) cell lines...

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Main Authors: Dijana Mitic, Milica Jaksic Karisik, Milos Lazarevic, Jelena Carkic, Emilia Zivkovic, Olivera Mitrovic Ajtic, Jelena Milasin
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Current Issues in Molecular Biology
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Online Access:https://www.mdpi.com/1467-3045/47/7/568
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author Dijana Mitic
Milica Jaksic Karisik
Milos Lazarevic
Jelena Carkic
Emilia Zivkovic
Olivera Mitrovic Ajtic
Jelena Milasin
author_facet Dijana Mitic
Milica Jaksic Karisik
Milos Lazarevic
Jelena Carkic
Emilia Zivkovic
Olivera Mitrovic Ajtic
Jelena Milasin
author_sort Dijana Mitic
collection DOAJ
description Exosomes, small extracellular vesicles secreted by various cell types, have gained significant attention in cancer investigations. Isolation and characterization of exosomes derived from DOK (dysplastic oral keratinocyte), SCC (squamous cell carcinoma) and HaCaT (normal skin keratinocyte) cell lines and microRNA profiling were conducted. Magnetic sorting was applied to obtain pure exosomes. Morphology and size were characterized by transmission electron microscopy and nanoparticle tracking analysis. Validation of membrane exosomal markers (CD9, CD63) was performed via Western blotting. MiR-21, miR-31, and miR-133 levels were analyzed in exosomes and parent cells by qPCR. Biological effects of the exosomes were tested by adding them to fibroblast cultures and determining the expression of relevant carcinogenesis markers by qPCR. Exosomes appeared as cup-shaped nano-sized particles, and there was no difference regarding particle diameter and concentration between the three types of exosomes. The oncogenic miR-21 was significantly upregulated both in SCC and SCC-derived exosomes compared to DOK and HaCaT cells and their respective exosomes. However, miR-31 unexpectedly showed the highest expression in normal cells and the lowest in HaCaT exosomes. MiR-133, the tumor suppressor miRNA, was downregulated in both SCC and DOK cells compared to normal (HaCaT) cells, while the opposite situation was observed in exosomes, with HaCaT cells showing the lowest levels of miR-133. The differences in exosome content were reflected in signaling pathway activation in exosome-treated fibroblasts, with SCC exosomes exerting the most potent effect on several cancer-related pathways, notably PIK3/AKT, PTEN, and NOTCH signaling cascades.
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spelling doaj-art-9ae5d3fcc3a444fea3ab0e775d9668f62025-08-20T03:36:14ZengMDPI AGCurrent Issues in Molecular Biology1467-30371467-30452025-07-0147756810.3390/cimb47070568Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal FibroblastsDijana Mitic0Milica Jaksic Karisik1Milos Lazarevic2Jelena Carkic3Emilia Zivkovic4Olivera Mitrovic Ajtic5Jelena Milasin6School of Dental Medicine, University of Belgrade, Belgrade, Dr. Subotica 8, 11000 Belgrade, SerbiaSchool of Dental Medicine, University of Belgrade, Belgrade, Dr. Subotica 8, 11000 Belgrade, SerbiaSchool of Dental Medicine, University of Belgrade, Belgrade, Dr. Subotica 8, 11000 Belgrade, SerbiaSchool of Dental Medicine, University of Belgrade, Belgrade, Dr. Subotica 8, 11000 Belgrade, SerbiaInstitute for Medical Research, National Institute of Republic of Serbia, University of Belgrade, 11129 Belgrade, SerbiaInstitute for Medical Research, National Institute of Republic of Serbia, University of Belgrade, 11129 Belgrade, SerbiaSchool of Dental Medicine, University of Belgrade, Belgrade, Dr. Subotica 8, 11000 Belgrade, SerbiaExosomes, small extracellular vesicles secreted by various cell types, have gained significant attention in cancer investigations. Isolation and characterization of exosomes derived from DOK (dysplastic oral keratinocyte), SCC (squamous cell carcinoma) and HaCaT (normal skin keratinocyte) cell lines and microRNA profiling were conducted. Magnetic sorting was applied to obtain pure exosomes. Morphology and size were characterized by transmission electron microscopy and nanoparticle tracking analysis. Validation of membrane exosomal markers (CD9, CD63) was performed via Western blotting. MiR-21, miR-31, and miR-133 levels were analyzed in exosomes and parent cells by qPCR. Biological effects of the exosomes were tested by adding them to fibroblast cultures and determining the expression of relevant carcinogenesis markers by qPCR. Exosomes appeared as cup-shaped nano-sized particles, and there was no difference regarding particle diameter and concentration between the three types of exosomes. The oncogenic miR-21 was significantly upregulated both in SCC and SCC-derived exosomes compared to DOK and HaCaT cells and their respective exosomes. However, miR-31 unexpectedly showed the highest expression in normal cells and the lowest in HaCaT exosomes. MiR-133, the tumor suppressor miRNA, was downregulated in both SCC and DOK cells compared to normal (HaCaT) cells, while the opposite situation was observed in exosomes, with HaCaT cells showing the lowest levels of miR-133. The differences in exosome content were reflected in signaling pathway activation in exosome-treated fibroblasts, with SCC exosomes exerting the most potent effect on several cancer-related pathways, notably PIK3/AKT, PTEN, and NOTCH signaling cascades.https://www.mdpi.com/1467-3045/47/7/568exosomesmicroRNAsoral cancer cellsdysplastic cellsmagnetic sortingTEM analysis
spellingShingle Dijana Mitic
Milica Jaksic Karisik
Milos Lazarevic
Jelena Carkic
Emilia Zivkovic
Olivera Mitrovic Ajtic
Jelena Milasin
Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts
Current Issues in Molecular Biology
exosomes
microRNAs
oral cancer cells
dysplastic cells
magnetic sorting
TEM analysis
title Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts
title_full Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts
title_fullStr Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts
title_full_unstemmed Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts
title_short Oral Squamous Cell Carcinoma Exosomes Upregulate PIK3/AKT, PTEN, and NOTCH Signaling Pathways in Normal Fibroblasts
title_sort oral squamous cell carcinoma exosomes upregulate pik3 akt pten and notch signaling pathways in normal fibroblasts
topic exosomes
microRNAs
oral cancer cells
dysplastic cells
magnetic sorting
TEM analysis
url https://www.mdpi.com/1467-3045/47/7/568
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