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Heteronemin Suppresses Lymphangiogenesis Through ARF-1 and MMP-9/VE-Cadherin/Vimentin

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Heteronemin Suppresses Lymphangiogenesis Through ARF-1 and MMP-9/VE-Cadherin/Vimentin biomedicines Article Heteronemin Suppresses Lymphangiogenesis through ARF-1 and MMP-9/VE-Cadherin/Vimentin Hsien-Lin Chen 1,†, Yu-Chieh Su 2,3,†, Huang-Chi Chen 4,5, Jui-Hsin Su 6, Chang-Yi Wu 7,8, Shih-Wei Wang 9,10 , In-Pin Lin 11, Chung-Yi Chen 12 and Chien-Hsing Lee 13,14,15,* 1 Division of General Surgery, Department of Surgery, Liuying Chi-Mei Medical, Tainan 73657, Taiwan; [email protected] 2 Department of Medicine, School of Medicine, I-Shou University, Kaohsiung 840203, Taiwan; [email protected] 3 Division of Hematology-Oncology, Department of Internal Medicine, E-Da Hospital, Kaohsiung 824410, Taiwan 4 Department of Internal Medicine, Kaohsiung Municipal Siaogang Hospital, Kaohsiung 81267, Taiwan; [email protected] 5 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung 80708, Taiwan 6 National Museum of Marine Biology & Aquarium, Institute of Marine Biotechnology, National Dong Hwa University, Pingtung 94401, Taiwan; [email protected] 7 Department of Biotechnology, Kaohsiung Medical University, Kaohsiung 80708, Taiwan; [email protected] 8 Department of Biological Sciences, National Sun Yat-Sen University, Kaohsiung 804201, Taiwan 9 Department of Medicine, Mackay Medical College, New Taipei City 252005, Taiwan; [email protected] 10 Graduate Institute of Natural Products, College of Pharmacy, Kaohsiung Medical University, Citation: Chen, H.-L.; Su, Y.-C.; Kaohsiung 80708, Taiwan Chen, H.-C.; Su, J.-H.; Wu, C.-Y.; 11 Department of Pharmacology, College of Medicine, Kaohsiung Medical University, Kaohsiung 80708, Taiwan; Wang, S.-W.; Lin, I.-P.; Chen, C.-Y.; [email protected] Lee, C.-H. Heteronemin Suppresses 12 Department of Nutrition and Health Science, School of Medical and Health Sciences, Fooyin University, Lymphangiogenesis through ARF-1 Kaohsiung 83102, Taiwan; [email protected] 13 and MMP-9/VE-Cadherin/Vimentin. Department of Pharmacology, School of Post-Baccalaureate Medicine, College of Medicine, Biomedicines 2021, 9, 1109. https:// Kaohsiung Medical University, Kaohsiung 80708, Taiwan 14 doi.org/10.3390/biomedicines Department of Medical Research, Kaohsiung Medical University Hospital, Kaohsiung 80708, Taiwan 15 Department of Biological Science and Technology, National Pingtung University of Science and Technology, 9091109 Pingtung 91201, Taiwan * Correspondence: [email protected]; Tel.: +886-7312-1101 (ext. 2139); Fax: +886-7323-4686 Academic Editors: Jun Lu and † The author contributed equally to the work. Khalid Sossey-Alaoui Abstract: Lymphatic metastasis is a biological procedure associated with the pathogenesis of several Received: 26 July 2021 diseases, especially in tumor metastasis. Therefore, regulation of lymphangiogenesis has become a Accepted: 26 August 2021 promising strategy for cancer therapy. In this study, we aimed to investigate the anti-lymphangiogenic Published: 29 August 2021 effect of heteronemin (SP-1) isolated from the sponge Hyrtios sp. in vitro and in vivo. Human lym- Publisher’s Note: MDPI stays neutral phatic endothelial cells (LECs) were utilized to evaluate the anti-lymphangiogenic effect of SP-1 with regard to jurisdictional claims in in vitro. Molecular docking, western blotting, flow-cytometry, MTT and ELISA were performed to published maps and institutional affil- investigate the mechanism of action. For in vivo approaches, the transgenic (fli1:EGFP; gata1:DsRed) iations. zebrafish and mouse ear sponges were used. Molecular docking studies showed that SP-1 is a potent vascular endothelial growth factor receptor 3 (VEGFR-3)-binding compound. Treatment of LEC with SP-1 reduced the phosphorylation of VEGFR-3. SP-1 suppressed the development of the thoracic duct in zebrafish and mouse lymphangiogenesis ear sponges in vivo. Mechanistically, SP-1 induced the Copyright: © 2021 by the authors. cell cycle arrest of LECs in the G0/G1 phase and reduced the downstream of VEGFR-3, such as phos- Licensee MDPI, Basel, Switzerland. phorylated MEK/ERK and NF-κB. In addition, SP-1 inhibited LECs’ tubulogenesis and migration This article is an open access article through the ARF-1 and MMP-9/VE-cadherin/vimentin. Overall, anti-lymphangiogenic properties of distributed under the terms and SP-1 occur by downregulating the VEGFR-3 cascade, ARF-1 and MMP-9/VE-cadherin/vimentin. conditions of the Creative Commons Collectively, these results proposed that SP-1 might be a potential candidate for the treatment of Attribution (CC BY) license (https:// lymphangiogenesis-associated diseases. creativecommons.org/licenses/by/ 4.0/). Biomedicines 2021, 9, 1109. https://doi.org/10.3390/biomedicines9091109 https://www.mdpi.com/journal/biomedicines Biomedicines 2021, 9, 1109 2 of 15 Keywords: lymphangiogenesis; heteronemin; zebrafish; ARF-1; MMP-9/VE-cadherin/vimentin; endothelial-to-mesenchymal transition 1. Introduction The lymphatic system, composed of lymph nodes, lymph ducts and lymphatic vessels, plays an important role in maintaining interstitial fluid homeostasis through intestinal water and macromolecules absorption and returning them back to the bloodstream [1]. Lymphangiogenesis, the generation of new lymphatic vessels from the preexisted ones, oc- curs during pathological conditions including in inflammation and cancer progression [2]. This process was regulated by vascular endothelial growth factors’ (VEGF) family mem- bers through binding to their receptors (VEGFRs), which are expressed at the surface of lymphatic endothelial cells (LECs) [3], especially in the VEGF-C/VEGFR-3 signaling pathway [4]. The activation of the VEGF-C/VEGFR-3 axis resulted in the phosphorylation on serine kinases, such as mitogen-activated protein kinase (MEK) and its downstream signaling extracellular signal-regulated kinase (ERK), to mediate the proliferation, tube formation, migration and survival of LECs [5]. In addition, activation of nuclear factor kappa B (NF-κB) up-regulates the VEGF-C/VEGFR-3 axis in LEC resulting in robust lym- phangiogenesis [6]. Therefore, inhibition of lymphangiogenesis may be a potential strategy to reduce cancer growth and lymphatic metastasis. Several studies have reported that endothelial cells (ECs) are involved in cancer pro- gression through the endothelial-to-mesenchymal transition (EndoMT), a cellular process through which ECs are removed from their organized layer and migrate, occasionally intruding the surrounding connective tissue [7,8]. The EndoMT of ECs is a process to acquire a mesenchymal phenotype resulting in a loss of cell-cell junctions and endothelial markers, such as vascular endothelial (VE)-cadherin, and the gain of mesenchymal markers, such as matrix metallopeptidase 9 (MMP-9) and vimentin [9]. A recent study has also demonstrated that the EndoMT contributes to lymphangiogenesis [8]. Furthermore, the ADP-ribosylation factor (ARF) has demonstrated to mediate the migration of ECs resulting in the regulation of tumor lymphangiogenesis [10]. Heteronemin (SP-1) is a sesterterpene isolated from the sponge Hyrtios sp. and modulates the transcriptional level of several pathways, including cell cycle and apoptosis, and inflammation, against various cancer cells. SP-1 induces both the intrinsic and the extrinsic apoptotic pathways in human renal cell carcinoma [11] and chronic myeloid leukemia through the reduction in NF-κB[12]. In addition, SP-1 targeted NF-κB upstream protein mitogen-activated protein kinase (MAPK) and inhibited the phosphorylation of p38 and c-Jun NH2-terminal kinase (JNK) [11]. SP-1 suppressed the phosphoinositide 3-kinases (PI3K)/AKT pathway and the MAPK family member ERK in human renal cell carcinoma [11,12]. A recent study showed that SP-1 mediates the adhesion of the cell, angiogenic sprouting, transcription factors and vasculogenesis in cholangiocarcinoma cell lines [13]. Therefore, SP-1 seems to be a promising therapeutic compound to treat angiogenesis-related diseases or cancer. In this study, a series of in vitro and in vivo experimental models was used to eval- uate the anti-lymphangiogenic effects of SP-1. We demonstrated that SP-1 is a VEGFR-3 binding compound to reduce the phosphorylated VEGFR-3. In addition, it reduced the in vivo lymphangiogenic process of zebrafish and mouse ear sponges. Mechanistically, our results demonstrated that SP-1 possesses its anti-lymphangiogenic properties by the restraint of the downstream of VEGFR-3, such as MAPK (ERK and MEK) and NF-κB. In addition, SP-1 also inhibited LECs’ sprouting of new lymphatic vessels and migration associated with ARF1/MMP9/VE-cadherin/vimentin-mediated EndoMT. Overall, our data display novel pharmacological perspectives for using this compound in diseases related to abnormal lymphangiogenesis. Biomedicines 2021, 9, 1109 3 of 15 2. Materials and Methods 2.1. Materials and Reagents Heteronemin is a sesterterpene isolated from the sponge Hyrtios sp., as previously de- scribed [14]. Dimethylsulfoxide (DMSO), 3-[4,5-Dimethylthiazol-2-yl]-2,5-diphenyltetrazolium bromide (MTT) and other chemical agents were obtained from Sigma-Aldrich (St. Louis, MO, USA). Rabbit monoclonal antibodies specific for ARF-1, lymphatic vessel endothelial receptor-1 (LYVE-1), NF-κB, prospero homeobox 1 (PROX-1) and VE-cadherin were pur- chased from the Proteintech Group (Rosemont, IL, USA). Phospho-ERK (Thr202/Tyr204), phospho-MEK (Ser217/221), phospho-p65 (Ser536), ERK, MEK and β-actin were purchased from Cell Signaling Technologies (Boston, MA, USA). MMP-9 was purchased from Santa Cruz Biotechnology (Santa Cruz, CA, USA).
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