IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression

Introduction: Angiogenesis plays a significant role in the development of tumor progression and inflammatory diseases. The role of IL-28A in angiogenesis and its precise regulatory mechanisms remain rarely elucidated. Objectives: We report the novel regulatory role of IL-28A in physiological angioge...

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Main Authors: Jun-Hui Song, Byungdoo Hwang, Sung Lyea Park, Hoon Kim, Soontag Jung, Changsun Choi, Hwan Myung Lee, Seok-Joong Yun, Yung Hyun Choi, Eun-Jong Cha, Cam Patterson, Wun-Jae Kim, Sung-Kwon Moon
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Journal of Advanced Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S2090123224003564
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author Jun-Hui Song
Byungdoo Hwang
Sung Lyea Park
Hoon Kim
Soontag Jung
Changsun Choi
Hwan Myung Lee
Seok-Joong Yun
Yung Hyun Choi
Eun-Jong Cha
Cam Patterson
Wun-Jae Kim
Sung-Kwon Moon
author_facet Jun-Hui Song
Byungdoo Hwang
Sung Lyea Park
Hoon Kim
Soontag Jung
Changsun Choi
Hwan Myung Lee
Seok-Joong Yun
Yung Hyun Choi
Eun-Jong Cha
Cam Patterson
Wun-Jae Kim
Sung-Kwon Moon
author_sort Jun-Hui Song
collection DOAJ
description Introduction: Angiogenesis plays a significant role in the development of tumor progression and inflammatory diseases. The role of IL-28A in angiogenesis and its precise regulatory mechanisms remain rarely elucidated. Objectives: We report the novel regulatory role of IL-28A in physiological angiogenesis. The study aimed to elucidate the regulatory mechanisms involved in IL-28A-mediated angiogenesis and identify key genes associated with IL-28A-induced angiogenic responses. Methods: To know the effect of IL-28A on angiogenesis, HUVECs were applied to perform proliferation, migration, invasion, tube formation, immunoblot, and EMSA. Gene expression changes in HUVECs following IL-28A treatment were analyzed by NGS. The functional role of HSP70-1 and IL-10Rβ in IL-28A-induced angiogenic responses was evaluated using PCR and siRNA knockdown. Animal studies were conducted by aortic ring ex vivo assays, Matrigel plug in vivo assays, and immunochemistry using HSP70-1 knockout and transgenic mice models. The efficacy of IL-28A in angiogenesis was confirmed in a hind-limb ischemia model. Results: Autocrine/paracrine actions in HUVECs regulated IL-28A protein expression. Exogenous IL-28A increased the proliferation of HUVECs via eNOS/AKT and ERK1/2 signaling. IL-28A treatment promoted migration, invasion, and capillary tube formation of HUVECs through induction of the AP-1/NF-κB/MMP-2 network, which was associated with eNOS/AKT and ERK1/2 signaling. The efficacy of IL-28A-induced angiogenic potential was confirmed by aortic ring and Matrigel plug assay. HSP70-1 was identified as an IL-28A-mediated angiogenic effector gene using bioinformatics. Knockdown of HSP70-1 abolished angiogenic responses and eNOS/AKT signaling in IL-28A-treated HUVECs. IL-28A-induced microvessel sprouting formation was testified in HSP70-1-deficient and HSP70-1 transgenic mice. Flow recovery in hind-limb ischemia mice was accelerated by IL-28A injection. Finally, ablation of the IL-10Rβ gene impeded the angiogenic responses and eNOS/AKT signaling stimulated by IL-28A in HUVECs. Conclusion: HSP70-1 drives the progression of angiogenesis by the IL-28A/IL-10Rβ axis via eNOS/AKT signaling and the AP-1/NF-κB/MMP-2 network.
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spelling doaj-art-619aa9c6b2584ced809b6fca3912cbc32025-08-20T02:10:35ZengElsevierJournal of Advanced Research2090-12322025-07-017324726310.1016/j.jare.2024.08.013IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expressionJun-Hui Song0Byungdoo Hwang1Sung Lyea Park2Hoon Kim3Soontag Jung4Changsun Choi5Hwan Myung Lee6Seok-Joong Yun7Yung Hyun Choi8Eun-Jong Cha9Cam Patterson10Wun-Jae Kim11Sung-Kwon Moon12Department of Food and Nutrition, Chung-Ang University, Anseong 456-756, KoreaDepartment of Food and Nutrition, Chung-Ang University, Anseong 456-756, KoreaDepartment of Food and Nutrition, Chung-Ang University, Anseong 456-756, KoreaDepartment of Food and Nutrition, Chung-Ang University, Anseong 456-756, KoreaDepartment of Food and Nutrition, Chung-Ang University, Anseong 456-756, KoreaDepartment of Food and Nutrition, Chung-Ang University, Anseong 456-756, KoreaDepartment of Cosmetic Science, Hoseo University, Asan-si 31499, Republic of KoreaPersonalized Tumor Engineering Research Center, Department of Urology, Chungbuk National University, Cheongju, Chungbuk 361-763, South KoreaDepartment of Biochemistry, College of Oriental Medicine, Dongeui University, Busan 614-052, South KoreaDepartment of Biomedical Engineering, Chungbuk National University, Cheongju 361-763, KoreaUniversity of Arkansas for Medical Sciences, Little Rock, AR, USAPersonalized Tumor Engineering Research Center, Department of Urology, Chungbuk National University, Cheongju, Chungbuk 361-763, South Korea; Institute of Urotech, Cheongju, Chungcheongbuk-do 361-763, KoreaDepartment of Food and Nutrition, Chung-Ang University, Anseong 456-756, Korea; Corresponding author at: Department of Food and Nutrition, Chung-Ang University, Anseong 456-756, Republic of Korea.Introduction: Angiogenesis plays a significant role in the development of tumor progression and inflammatory diseases. The role of IL-28A in angiogenesis and its precise regulatory mechanisms remain rarely elucidated. Objectives: We report the novel regulatory role of IL-28A in physiological angiogenesis. The study aimed to elucidate the regulatory mechanisms involved in IL-28A-mediated angiogenesis and identify key genes associated with IL-28A-induced angiogenic responses. Methods: To know the effect of IL-28A on angiogenesis, HUVECs were applied to perform proliferation, migration, invasion, tube formation, immunoblot, and EMSA. Gene expression changes in HUVECs following IL-28A treatment were analyzed by NGS. The functional role of HSP70-1 and IL-10Rβ in IL-28A-induced angiogenic responses was evaluated using PCR and siRNA knockdown. Animal studies were conducted by aortic ring ex vivo assays, Matrigel plug in vivo assays, and immunochemistry using HSP70-1 knockout and transgenic mice models. The efficacy of IL-28A in angiogenesis was confirmed in a hind-limb ischemia model. Results: Autocrine/paracrine actions in HUVECs regulated IL-28A protein expression. Exogenous IL-28A increased the proliferation of HUVECs via eNOS/AKT and ERK1/2 signaling. IL-28A treatment promoted migration, invasion, and capillary tube formation of HUVECs through induction of the AP-1/NF-κB/MMP-2 network, which was associated with eNOS/AKT and ERK1/2 signaling. The efficacy of IL-28A-induced angiogenic potential was confirmed by aortic ring and Matrigel plug assay. HSP70-1 was identified as an IL-28A-mediated angiogenic effector gene using bioinformatics. Knockdown of HSP70-1 abolished angiogenic responses and eNOS/AKT signaling in IL-28A-treated HUVECs. IL-28A-induced microvessel sprouting formation was testified in HSP70-1-deficient and HSP70-1 transgenic mice. Flow recovery in hind-limb ischemia mice was accelerated by IL-28A injection. Finally, ablation of the IL-10Rβ gene impeded the angiogenic responses and eNOS/AKT signaling stimulated by IL-28A in HUVECs. Conclusion: HSP70-1 drives the progression of angiogenesis by the IL-28A/IL-10Rβ axis via eNOS/AKT signaling and the AP-1/NF-κB/MMP-2 network.http://www.sciencedirect.com/science/article/pii/S2090123224003564IL-28AIL-10RβAngiogenesisHSP70-1
spellingShingle Jun-Hui Song
Byungdoo Hwang
Sung Lyea Park
Hoon Kim
Soontag Jung
Changsun Choi
Hwan Myung Lee
Seok-Joong Yun
Yung Hyun Choi
Eun-Jong Cha
Cam Patterson
Wun-Jae Kim
Sung-Kwon Moon
IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression
Journal of Advanced Research
IL-28A
IL-10Rβ
Angiogenesis
HSP70-1
title IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression
title_full IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression
title_fullStr IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression
title_full_unstemmed IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression
title_short IL-28A/IL-10Rβ axis promotes angiogenesis via eNOS/AKT signaling and AP-1/NF-κB/MMP-2 network by regulating HSP70-1 expression
title_sort il 28a il 10rβ axis promotes angiogenesis via enos akt signaling and ap 1 nf κb mmp 2 network by regulating hsp70 1 expression
topic IL-28A
IL-10Rβ
Angiogenesis
HSP70-1
url http://www.sciencedirect.com/science/article/pii/S2090123224003564
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