MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions
In a previous study, we have demonstrated that p62, a selective receptor of autophagy, can regulate allergic inflammation. In the present study, microRNA array analysis showed that miR-154-5p was increased by antigen (DNP-HSA) in a p62-dependent manner in rat basophilic leukemia cells (RBL2H3). NF-k...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-05-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.663726/full |
| _version_ | 1819204155067072512 |
|---|---|
| author | Misun Kim Hyein Jo Yoojung Kwon Myeong Seon Jeong Myeong Seon Jeong Hyun Suk Jung Youngmi Kim Dooil Jeoung |
| author_facet | Misun Kim Hyein Jo Yoojung Kwon Myeong Seon Jeong Myeong Seon Jeong Hyun Suk Jung Youngmi Kim Dooil Jeoung |
| author_sort | Misun Kim |
| collection | DOAJ |
| description | In a previous study, we have demonstrated that p62, a selective receptor of autophagy, can regulate allergic inflammation. In the present study, microRNA array analysis showed that miR-154-5p was increased by antigen (DNP-HSA) in a p62-dependent manner in rat basophilic leukemia cells (RBL2H3). NF-kB directly increased the expression of miR-154-5p. miR-154-5p mediated in vivo allergic reactions, including passive cutaneous anaphylaxis and passive systemic anaphylaxis. Cytokine array analysis showed that antigen stimulation increased the expression of MCP1 in RBL2H3 cells in an miR-154-5p-dependent manner. Reactive oxygen species (ROS)-ERK-NF-kB signaling increased the expression of MCP1 in antigen-stimulated RBL2H3 cells. Recombinant MCP1 protein induced molecular features of allergic reactions both in vitro and in vivo. Anaphylaxis-promoted tumorigenic potential has been known to be accompanied by cellular interactions involving mast cells, and macrophages, and cancer cells. Our experiments employing culture medium, co-cultures, and recombinant MCP1 protein showed that miR-154 and MCP1 mediated these cellular interactions. MiR-154-5p and MCP1 were found to be present in exosomes of RBL2H3 cells. Exosomes from PSA-activated BALB/C mouse induced molecular features of passive cutaneous anaphylaxis in an miR-154-5p-dependent manner. Exosomes from antigen-stimulated RBL2H3 cells enhanced both tumorigenic and metastatic potentials of B16F1 melanoma cells in an miR-154-5p-dependent manner. Exosomes regulated both ROS level and ROS mediated cellular interactions during allergic inflammation. Our results indicate that the miR-154-5p-MCP1 axis might serve as a valuable target for the development of anti-allergy therapeutics. |
| first_indexed | 2024-12-23T04:31:18Z |
| format | Article |
| id | doaj.art-1bf732b307204d03821231347ade56ef |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-23T04:31:18Z |
| publishDate | 2021-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-1bf732b307204d03821231347ade56ef2022-12-21T18:00:01ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-05-011210.3389/fimmu.2021.663726663726MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular InteractionsMisun Kim0Hyein Jo1Yoojung Kwon2Myeong Seon Jeong3Myeong Seon Jeong4Hyun Suk Jung5Youngmi Kim6Dooil Jeoung7Department of Biochemistry, Kangwon National University, Chuncheon, South KoreaDepartment of Biochemistry, Kangwon National University, Chuncheon, South KoreaDepartment of Biochemistry, Kangwon National University, Chuncheon, South KoreaDepartment of Biochemistry, Kangwon National University, Chuncheon, South KoreaChuncheon Center, Korea Basic Science Institute (KBSI), Chuncheon, South KoreaDepartment of Biochemistry, Kangwon National University, Chuncheon, South KoreaInstitute of New Frontier Research, College of Medicine, Hallym University, Chuncheon, South KoreaDepartment of Biochemistry, Kangwon National University, Chuncheon, South KoreaIn a previous study, we have demonstrated that p62, a selective receptor of autophagy, can regulate allergic inflammation. In the present study, microRNA array analysis showed that miR-154-5p was increased by antigen (DNP-HSA) in a p62-dependent manner in rat basophilic leukemia cells (RBL2H3). NF-kB directly increased the expression of miR-154-5p. miR-154-5p mediated in vivo allergic reactions, including passive cutaneous anaphylaxis and passive systemic anaphylaxis. Cytokine array analysis showed that antigen stimulation increased the expression of MCP1 in RBL2H3 cells in an miR-154-5p-dependent manner. Reactive oxygen species (ROS)-ERK-NF-kB signaling increased the expression of MCP1 in antigen-stimulated RBL2H3 cells. Recombinant MCP1 protein induced molecular features of allergic reactions both in vitro and in vivo. Anaphylaxis-promoted tumorigenic potential has been known to be accompanied by cellular interactions involving mast cells, and macrophages, and cancer cells. Our experiments employing culture medium, co-cultures, and recombinant MCP1 protein showed that miR-154 and MCP1 mediated these cellular interactions. MiR-154-5p and MCP1 were found to be present in exosomes of RBL2H3 cells. Exosomes from PSA-activated BALB/C mouse induced molecular features of passive cutaneous anaphylaxis in an miR-154-5p-dependent manner. Exosomes from antigen-stimulated RBL2H3 cells enhanced both tumorigenic and metastatic potentials of B16F1 melanoma cells in an miR-154-5p-dependent manner. Exosomes regulated both ROS level and ROS mediated cellular interactions during allergic inflammation. Our results indicate that the miR-154-5p-MCP1 axis might serve as a valuable target for the development of anti-allergy therapeutics.https://www.frontiersin.org/articles/10.3389/fimmu.2021.663726/fullmiR-154-5pMCP1exosomescellular interactionsallergic inflammation |
| spellingShingle | Misun Kim Hyein Jo Yoojung Kwon Myeong Seon Jeong Myeong Seon Jeong Hyun Suk Jung Youngmi Kim Dooil Jeoung MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions Frontiers in Immunology miR-154-5p MCP1 exosomes cellular interactions allergic inflammation |
| title | MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions |
| title_full | MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions |
| title_fullStr | MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions |
| title_full_unstemmed | MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions |
| title_short | MiR-154-5p-MCP1 Axis Regulates Allergic Inflammation by Mediating Cellular Interactions |
| title_sort | mir 154 5p mcp1 axis regulates allergic inflammation by mediating cellular interactions |
| topic | miR-154-5p MCP1 exosomes cellular interactions allergic inflammation |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.663726/full |
| work_keys_str_mv | AT misunkim mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT hyeinjo mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT yoojungkwon mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT myeongseonjeong mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT myeongseonjeong mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT hyunsukjung mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT youngmikim mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions AT dooiljeoung mir1545pmcp1axisregulatesallergicinflammationbymediatingcellularinteractions |