Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells

Angiogenesis, primarily driven by the vascular endothelial growth factor (VEGF) and its receptor, the VEGFR, plays a key role in various pathological processes such as cancer progression. Here, we investigated the anti-angiogenic effects of Lucknolide A (LA), a marine <i>Streptomyces</i>...

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Main Authors: Byeoung-Kyu Choi, Min-Hee Jo, Hee Jae Shin, Sun Joo Park
Format: Article
Language:English
Published: MDPI AG 2025-02-01
Series:Molecules
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Online Access:https://www.mdpi.com/1420-3049/30/5/987
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author Byeoung-Kyu Choi
Min-Hee Jo
Hee Jae Shin
Sun Joo Park
author_facet Byeoung-Kyu Choi
Min-Hee Jo
Hee Jae Shin
Sun Joo Park
author_sort Byeoung-Kyu Choi
collection DOAJ
description Angiogenesis, primarily driven by the vascular endothelial growth factor (VEGF) and its receptor, the VEGFR, plays a key role in various pathological processes such as cancer progression. Here, we investigated the anti-angiogenic effects of Lucknolide A (LA), a marine <i>Streptomyces</i>-derived compound, and evaluated its potential as a VEGFR2 inhibitor. LA selectively inhibited the proliferation of human endothelial cells EA.hy926 and HUVEC while exhibiting minimal effects on normal fibroblasts and various tumor cells. LA induced S-phase cell cycle arrest and apoptosis in EA.hy926 cells, increasing apoptotic markers p53, Bax, and p21 and decreasing the anti-apoptotic protein Bcl-2, with these effects being further enhanced under VEGF stimulation. Additionally, LA suppressed VEGFR2 phosphorylation and its downstream signaling pathways, including Akt/mTOR/p70S6K, MEK/ERK, Src, FAK, and p38 MAPK, which are crucial for endothelial survival and angiogenesis. Molecular docking studies revealed that LA binds to both inactive (DFG-out, PDB: 4ASD) and active (DFG-in, PDB: 3B8R) VEGFR2 conformations, with a significantly stronger affinity for the active state (−107.96 kcal/mol) than the inactive state (−33.56 kcal/mol), suggesting its potential as a VEGFR2 kinase inhibitor. Functionally, LA significantly inhibited VEGF-induced endothelial migration, tube formation, and microvessel sprouting in both in vitro and ex vivo rat aortic ring assays. Additionally, LA reduced tumor-associated tube formation induced by human breast tumor cells (MDA-MB-231), indicating its potential to suppress VEGF-dependent tumor angiogenesis. These findings suggest that LA is a promising selective anti-angiogenic agent with potential therapeutic applications in angiogenesis-related diseases such as cancer.
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spelling doaj-art-73c85907ff8e4e0691908ba64a1c90cb2025-08-20T02:05:24ZengMDPI AGMolecules1420-30492025-02-0130598710.3390/molecules30050987Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial CellsByeoung-Kyu Choi0Min-Hee Jo1Hee Jae Shin2Sun Joo Park3Department of Bio-Convergence Engineering, Dongyang Mirae University, Seoul 08221, Republic of KoreaBB21 Plus Program, Department of Chemistry, Pukyong National University, Busan 48513, Republic of KoreaMarine Natural Products Laboratory, Korea Institute of Ocean Science and Technology, Busan 49111, Republic of KoreaBB21 Plus Program, Department of Chemistry, Pukyong National University, Busan 48513, Republic of KoreaAngiogenesis, primarily driven by the vascular endothelial growth factor (VEGF) and its receptor, the VEGFR, plays a key role in various pathological processes such as cancer progression. Here, we investigated the anti-angiogenic effects of Lucknolide A (LA), a marine <i>Streptomyces</i>-derived compound, and evaluated its potential as a VEGFR2 inhibitor. LA selectively inhibited the proliferation of human endothelial cells EA.hy926 and HUVEC while exhibiting minimal effects on normal fibroblasts and various tumor cells. LA induced S-phase cell cycle arrest and apoptosis in EA.hy926 cells, increasing apoptotic markers p53, Bax, and p21 and decreasing the anti-apoptotic protein Bcl-2, with these effects being further enhanced under VEGF stimulation. Additionally, LA suppressed VEGFR2 phosphorylation and its downstream signaling pathways, including Akt/mTOR/p70S6K, MEK/ERK, Src, FAK, and p38 MAPK, which are crucial for endothelial survival and angiogenesis. Molecular docking studies revealed that LA binds to both inactive (DFG-out, PDB: 4ASD) and active (DFG-in, PDB: 3B8R) VEGFR2 conformations, with a significantly stronger affinity for the active state (−107.96 kcal/mol) than the inactive state (−33.56 kcal/mol), suggesting its potential as a VEGFR2 kinase inhibitor. Functionally, LA significantly inhibited VEGF-induced endothelial migration, tube formation, and microvessel sprouting in both in vitro and ex vivo rat aortic ring assays. Additionally, LA reduced tumor-associated tube formation induced by human breast tumor cells (MDA-MB-231), indicating its potential to suppress VEGF-dependent tumor angiogenesis. These findings suggest that LA is a promising selective anti-angiogenic agent with potential therapeutic applications in angiogenesis-related diseases such as cancer.https://www.mdpi.com/1420-3049/30/5/987Lucknolide Amarine natural compoundmarine <i>Streptomyces</i>anti-angiogenesisVEGF/VEGFR2 signalinganti-tumor
spellingShingle Byeoung-Kyu Choi
Min-Hee Jo
Hee Jae Shin
Sun Joo Park
Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells
Molecules
Lucknolide A
marine natural compound
marine <i>Streptomyces</i>
anti-angiogenesis
VEGF/VEGFR2 signaling
anti-tumor
title Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells
title_full Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells
title_fullStr Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells
title_full_unstemmed Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells
title_short Anti-Angiogenic Potential of Marine <i>Streptomyces</i>-Derived Lucknolide A on VEGF/VEGFR2 Signaling in Human Endothelial Cells
title_sort anti angiogenic potential of marine i streptomyces i derived lucknolide a on vegf vegfr2 signaling in human endothelial cells
topic Lucknolide A
marine natural compound
marine <i>Streptomyces</i>
anti-angiogenesis
VEGF/VEGFR2 signaling
anti-tumor
url https://www.mdpi.com/1420-3049/30/5/987
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