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Encephalomyelitis Ameliorates Experimental Autoimmune And The Journal of Immunology Vibsanin B Preferentially Targets HSP90b, Inhibits Interstitial Leukocyte Migration, and Ameliorates Experimental Autoimmune Encephalomyelitis Bai-Xin Ye,*,1 Xu Deng,†,1 Li-Dong Shao,† Ying Lu,* Run Xiao,* Yi-Jie Liu,* Yi Jin,* Yin-Yin Xie,* Yan Zhao,* Liu-Fei Luo,* Shun Ma,‡ Ming Gao,x Lian-Ru Zhang,‡ Juan He,† Wei-Na Zhang,* Yi Chen,* Cheng-Feng Xia,† Min Deng,{ Ting-Xi Liu,*,{ Qin-Shi Zhao,† Sai-Juan Chen,* and Zhu Chen* Interstitial leukocyte migration plays a critical role in inflammation and offers a therapeutic target for treating inflammation- associated diseases such as multiple sclerosis. Identifying small molecules to inhibit undesired leukocyte migration provides promise for the treatment of these disorders. In this study, we identified vibsanin B, a novel macrocyclic diterpenoid isolated from Viburnum odoratissimum Ker-Gawl, that inhibited zebrafish interstitial leukocyte migration using a transgenic zebrafish line (TG:zlyz– enhanced GFP). We found that vibsanin B preferentially binds to heat shock protein (HSP)90b. At the molecular level, inacti- vation of HSP90 can mimic vibsanin B’s effect of inhibiting interstitial leukocyte migration. Furthermore, we demonstrated that vibsanin B ameliorates experimental autoimmune encephalomyelitis in mice with pathological manifestation of decreased leuko- cyte infiltration into their CNS. In summary, vibsanin B is a novel lead compound that preferentially targets HSP90b and inhibits interstitial leukocyte migration, offering a promising drug lead for treating inflammation-associated diseases. The Journal of Immunology, 2015, 194: 4489–4497. eukocyte trafficking is a multistep process consisting of moattractant signals, plays an important role in immune cell de- transendothelial and interstitial migration of leukocytes, velopment, immunosurveillance, and effector functions. Leukocyte L and it is required for efficient immune response. Interstitial migration is tightly regulated and its deregulation has been im- leukocyte migration, an amoeboid migration mode characterized plicated in several human diseases (1, 2). Mounting evidence in- by polarized cell morphology and redistribution of signaling dicates that inhibiting interstitial leukocyte migration is a prom- molecules under the guidance of soluble and tissue-bound che- ising strategy for treating inflammation-associated diseases (3). For example, inhibition of monocyte/macrophage infiltration offers a potential therapeutic strategy for the treatment of multiple scle- *State Key Laboratory of Medical Genomics and Shanghai Institute of Hematology, rosis (MS), an autoimmune inflammation-mediated demyelinating RuiJin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China; †State Key Laboratory of Phytochemistry and Plant Resources in disease partially caused by an abnormal monocyte/macrophage in- West China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming filtration into the CNS (4). 650201, China; ‡State Key Laboratory of Cellular Stress Biology, Xiamen University, Xiamen 361102, China; xDepartment of Immunology, School of Basic Medicine, Zebrafish is a widely used vertebrate animal model for disease Tongji Medical College, Huazhong University of Science and Technology, Wuhan modeling and phenotype-driven chemical screening because of its { 430030, China; and Institute of Health Sciences, Shanghai Institutes for Biological small size, transparent body, and morphological or physiological Sciences, Chinese Academy of Sciences and Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China similarity to mammals. This whole animal model could potentially 1B.-X.Y. and X.D. contributed equally to this work. benefit several steps of the drug development processes, including drug screening, lead discovery, target identification, as well as Received for publication November 17, 2014. Accepted for publication February 24, 2015. functional assays (5–7). Recently, the zebrafish model has been This work was supported by Chinese National Key Basic Research Project 973 Grant used to analyze the dynamic course of leukocyte chemotactic 2013CB966800, Chinese Ministry of Health Grant 201202003, Mega-Projects of migration in vivo, which facilitates novel insights into certain Scientific Research for the 12th Five-Year Plan Grant 2013ZX09303302, and by State Key Laboratories Project of Excellence Grant 81123005. inflammatory diseases that involve leukocytes. Thus, zebrafish is an ideal model organism to study the biological behavior of leu- Address correspondence and reprint requests to Dr. Zhu Chen, Dr. Sai-Juan Chen, or Dr. Qin-Shi Zhao, RuiJin Hospital, Shanghai Jiao Tong University School of Med- kocytes through live imaging techniques (8–11). We previously icine, 197 Rui Jin Road II, Shanghai 200025, China (Z.C. and S.-J.C.) or Kunming constructed a transgenic zebrafish line TG:zlyz–enhanced GFP Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Heilongtan, Kunming 650201, China (Q.-S.Z.). E-mail addresses: [email protected] (Z.C.), (EGFP) for tracking leukocyte migration in response to acute in- + [email protected] (S.-J.C.), or [email protected] (Q.-S.Z.) jury in vivo (9). In TG:zlyz-EGFP embryos, EGFP cells mainly The online version of this article contains supplemental material. represented primitive macrophages before 36 h postfertilization Abbreviations used in this article: Biotin-ViB, biotin-tagged vibsanin B; dHL60, (hpf), whereas in the later stage after 48 hpf of embryos, the differentiated HL60; dpf, days postfertilization; EAE, experimental autoimmune en- EGFP+ cells contained monocytes/macrophages and neutrophils, cephalomyelitis; EGFP, enhanced GFP; hpf, hours postfertilization; HSP, heat shock protein; MS, multiple sclerosis; siRNA, small interfering RNA; TRAP, TNFR- both of which are called “leukocytes” and play an important role + associated protein; ViB–18-F, vibsanin B derivative with conversion of the C-18 in innate immunity (9, 12). Thus, we refer these EGFP cells in hydroxyl group to fluorine; ViB–4-OH, vibsanin B derivative whose C4 carbonyl the TG:zlyz-EGFP embryos (at 3 d postfertilization [dpf]) as group was reduced to a hydroxyl group. leukocytes and use this zebrafish model to identify drug leads that Copyright Ó 2015 by The American Association of Immunologists, Inc. 0022-1767/15/$25.00 inhibit interstitial leukocyte migration (12, 13). www.jimmunol.org/cgi/doi/10.4049/jimmunol.1402798 4490 VIBSANIN B INHIBITS LEUKOCYTE MIGRATION AND AMELIORATES EAE Heat shock protein (HSP)90 is a highly conserved molecular presented as chemotaxis indexes referring to the fold increase in the total chaperone that regulates diverse physiological and pathological number of migrating cells in response to stimuli over the spontaneous cell processes. It dynamically distributes in almost every cellular com- migration to the control medium. partment: the cytoplasmic HSP90, which is the dominant form in the Pull-down assay and mass spectrum analysis cell and is comprised of a and b isoforms; the endoplasmic retic- As described in previous work (25), THP-1 cell lysates were incubated with ulum–localized HSP90 protein glucose-regulated protein 94; and biotin or biotin-tagged vibsanin B (Biotin-ViB) in the absence or presence the mitochondrial HSP90, which includes the TNF receptor- of vibsanin B at 4˚C, followed by incubation with streptavidin-agarose associated protein (TRAP) family member TRAP1 (14). Recently, beads (Sigma-Aldrich, catalog no. S1638). The agarose bead–bound pro- it was shown that HSP90 regulates the migration of endothelial cells teins were pulled down, separated by SDS-PAGE, and stained by Coo- or tumor cells by influencing cell membrane polarization, which is massie brilliant blue R250. The indicated band in the gel was excised, followed by in-gel digestion and analysis by mass spectrometry (ABI mainly mediated by the PI3K-AKT pathway (1, 15–17). Given the 4700; Applied Biosystems, Foster City, CA). similarity between tumor cells and leukocytes with respect to their amoeboid migration (18), HSP90 could also be involved in inter- Western blot analysis stitial leukocyte migration; thus, targeting HSP90 could ameliorate The proteins separated by SDS-PAGE electrophoresis were transferred to inflammation-associated diseases. As has been reported, HSP90 is ECL nitrocellulose membranes and incubated with the primary Ab over- considered to be a promising druggable target for treating inflam- night at 4˚C, followed by incubation of HRP-linked secondary Ab (Cell matory and neurodegenerative diseases (19, 20). Therefore, the Signaling Technology) for 1 h at room temperature. Detection was per- formed by an Immobilon Western chemiluminescent HRP substrate kit development of novel HSP90 inhibitors is necessary for the HSP90- (Millipore, catalog no. WBKLS0100) according to the manufacturer’s based therapy of inflammation-associated diseases, including MS. instructions (LAS 4000, Fujifilm). Signal intensity of protein was nor- Vibsane-type diterpenoids are a class of structurally diverse and malized against ubiquitously expressed proteins GAPDH or actin using rarely occurring natural products exclusively found in a few Vi- Quantity One (Bio-Rad, Hercules, CA) software. The primary Abs in this burnum species. However, the biological profile and the underlying study are specific for HSP90a, HSP90b, HSP70, His-tag, p-AKT, AKT, p-p38, p38, p-ERK, and ERK (Cell signaling Technology). Extraction of mechanism of action of these diterpenoids have not yet
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