In vitro anticancer effects of a RAGE inhibitor discovered using a structure-based drug design system
- Authors:
- Ali Hafez Ali Mohammed El‑Far
- Seiichi Munesue
- Ai Harashima
- Akira Sato
- Mika Shindo
- Shingo Nakajima
- Mana Inada
- Mariko Tanaka
- Akihiko Takeuchi
- Hiroyuki Tsuchiya
- Hiroshi Yamamoto
- Hazem M.E. Shaheen
- Yasser S. El‑Sayed
- Shuhei Kawano
- Sei‑Ichi Tanuma
- Yasuhiko Yamamoto
-
Affiliations: Department of Biochemistry and Molecular Vascular Biology, Kanazawa University Graduate School of Medical Sciences, Kanazawa, Ishikawa 920‑8640, Japan, Department of Biochemistry, Faculty of Pharmaceutical Sciences, Tokyo University of Science, Chiba 278‑8510, Japan, Department of Orthopedic Surgery, Kanazawa University Graduate School of Medical Sciences, Kanazawa, Ishikawa 920‑8641, Japan, Department of Pharmacology, Faculty of Veterinary Medicine, Damanhour University, Damanhour 22511, Egypt, Department of Veterinary Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Damanhour University, Damanhour 22511, Egypt - Published online on: January 29, 2018 https://doi.org/10.3892/ol.2018.7902
- Pages: 4627-4634
This article is mentioned in:
Abstract
Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, Kao J, Esposito C, Hegarty H, Hurley W, Clauss M, et al: Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J Biol Chem. 267:14987–14997. 1992.PubMed/NCBI | |
Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, et al: RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell. 97:889–901. 1999. View Article : Google Scholar : PubMed/NCBI | |
Yamamoto Y, Harashima A, Saito H, Tsuneyama K, Munesue S, Motoyoshi S, Han D, Watanabe T, Asano M, Takasawa S, et al: Septic shock is associated with receptor for advanced glycation endproducts (RAGE) ligation of LPS. J Immunol. 186:3248–3257. 2011. View Article : Google Scholar : PubMed/NCBI | |
He M, Kubo H, Morimoto K, Fujino N, Suzuki T, Takahasi T, Yamada M, Yamaya M, Maekawa T, Yamamoto Y and Yamamoto H: Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep. 12:358–364. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, et al: RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature. 382:685–691. 1996. View Article : Google Scholar : PubMed/NCBI | |
Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen J, Nagashima M, Lundh ER, Vijay S, Nitecki D, et al: The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin: Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J Biol Chem. 270:25752–25761. 1995. View Article : Google Scholar : PubMed/NCBI | |
Yamamoto Y, Kato I, Doi T, Yonekura H, Ohashi S, Takeuchi M, Watanabe T, Yamagishi S, Sakurai S, Takasawa S, et al: Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest. 108:261–268. 2001. View Article : Google Scholar : PubMed/NCBI | |
Schmidt AM, Yan SD, Yan SF and Stern DM: The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest. 108:949–955. 2001. View Article : Google Scholar : PubMed/NCBI | |
Sims GP, Rowe DC, Rietdijk ST, Herbst R and Coyle AJ: HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol. 28:367–388. 2010. View Article : Google Scholar : PubMed/NCBI | |
Takeuchi A, Yamamoto Y, Munesue S, Harashima A, Watanabe T, Yonekura H, Yamamoto H and Tsuchiya H: Low molecular weight heparin suppresses receptor for advanced glycation end products-mediated expression of malignant phenotype in human fibrosarcoma cells. Cancer Sci. 104:740–749. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kuniyasu H, Oue N, Wakikawa A, Shigeishi H, Matsutani N, Kuraoka K, Ito R, Yokozaki H and Yasui W: Expression of receptors for advanced glycation end-products (RAGE) is closely associated with the invasive and metastatic activity of gastric cancer. J Pathol. 196:163–170. 2002. View Article : Google Scholar : PubMed/NCBI | |
Fuentes MK, Nigavekar SS, Arumugam T, Logsdon CD, Schmidt AM, Park JC and Huang EH: RAGE activation by S100P in colon cancer stimulates growth, migration, and cell signaling pathways. Dis Colon Rectum. 50:1230–1240. 2007. View Article : Google Scholar : PubMed/NCBI | |
Onyeagucha BC, Mercado-Pimentel ME, Hutchison J, Flemington EK and Nelson MA: S100P/RAGE signaling regulates microRNA-155 expression via AP-1 activation in colon cancer. Exp Cell Res. 319:2081–2090. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mercado-Pimentel ME, Onyeagucha BC, Li Q, Pimentel AC, Jandova J and Nelson MA: The S100P/RAGE signaling pathway regulates expression of microRNA-21 in colon cancer cells. FEBS Lett. 589:2388–2393. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ishiguro H, Nakaigawa N, Miyoshi Y, Fujinami K, Kubota Y and Uemura H: Receptor for advanced glycation end products (RAGE) and its ligand, amphoterin are overexpressed and associated with prostate cancer development. Prostate. 64:92–100. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kwak T, Drews-Elger K, Ergonul A, Miller PC, Braley A, Hwang GH, Zhao D, Besser A, Yamamoto Y, Yamamoto H, et al: Targeting of RAGE-ligand signaling impairs breast cancer cell invasion and metastasis. Oncogene. 36:1559–1572. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Jin Y, Zhao CF, Wang WJ and Liu GY: Receptor for advanced glycation end-products (RAGE) is overexpressed in human osteosarcoma and promotes the proliferation of osteosarcoma U-2OS cells in vitro. Genet Mol Res. 15:2016. | |
Sakai J, Yoshimori A, Nose Y, Mizoroki A, Okita N, Takasawa R and Tanuma S: Structure-based discovery of a novel non-peptidic small molecular inhibitor of caspase-3. Bioorg Med Chem. 16:4854–4859. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kukovetz WR and Pöch G: Inhibition of cyclic-3′, 5′-nucleotide-phosphodiesterase as a possible mode of action of papaverine and similarly acting drugs. Naunyn Schmiedebergs Arch Pharmakol. 267:189–194. 1970. View Article : Google Scholar : PubMed/NCBI | |
Iguchi M, Nakajima T, Hisada T, Sugimoto T and Kurachi Y: On the mechanism of papaverine inhibition of the voltage-dependent Ca++ current in isolated smooth muscle cells from the guinea pig trachea. J Pharmacol Exp Ther. 263:194–200. 1992.PubMed/NCBI | |
Myint KM, Yamamoto Y, Doi T, Kato I, Harashima A, Yonekura H, Watanabe T, Shinohara H, Takeuchi M, Tsuneyama K, et al: RAGE control of diabetic nephropathy in a mouse model: Effects of RAGE gene disruption and administration of low-molecular weight heparin. Diabetes. 55:2510–2522. 2006. View Article : Google Scholar : PubMed/NCBI | |
Huttunen HJ, Fages C and Rauvala H: Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different down signaling pathways. J Biol Chem. 274:19919–19924. 1999. View Article : Google Scholar : PubMed/NCBI | |
Huttunen HJ, Fages C, Kuja-Panula J, Ridley AJ and Rauvala H: Receptor for advanced glycation end products-binding COOH-terminal motif of amphoterin inhibits invasive migration and metastasis. Cancer Res. 62:4805–4811. 2002.PubMed/NCBI | |
Wajsman Z, Williams P and Murphy GP: A study of the effect of papaverine in neuroblastoma using the experimental C1300 murine system. Oncology. 35:1–4. 1978. View Article : Google Scholar : PubMed/NCBI | |
Wolf S, Haase-Kohn C, Lenk J, Hoppmann S, Bergmann R, Steinbach J and Pietzsch J: Expression, purification and fluorine-18 radiolabeling of recombinant S100A4: A potential probe for molecular imaging of receptor for advanced glycation endproducts in vivo? Amino Acids. 41:809–820. 2011. View Article : Google Scholar : PubMed/NCBI | |
Leclerc E, Fritz G, Weibel M, Heizmann CW and Galichet A: S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem. 282:31317–31331. 2007. View Article : Google Scholar : PubMed/NCBI | |
Wolf R, Howard OM, Dong HF, Voscopoulos C, Boeshans K, Winston J, Divi R, Gunsior M, Goldsmith P, Ahvazi B, et al: Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end products and potentiates inflammation with highly homologous but functionally distinct S100A15. J Immunol. 181:1499–1506. 2008. View Article : Google Scholar : PubMed/NCBI | |
Jin Q, Chen H, Luo A, Ding F and Liu Z: S100A14 stimulates cell proliferation and induces cell apoptosis at different concentrations via receptor for advanced glycation end products (RAGE). PLoS One. 6:e193752011. View Article : Google Scholar : PubMed/NCBI | |
Padilla L, Dakhel S and Hernández JL: S100 to receptor for advanced glycation end-products binding assay: Looking for inhibitors. Biochem Biophys Res Commun. 446:404–409. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Zhang L, Zhang IY, Liang J, Wang H, Ouyang M, Wu S, da Fonseca AC, Weng L, Yamamoto Y, et al: RAGE expression in tumor-associated macrophages promotes angiogenesis in glioma. Cancer Res. 74:7285–7297. 2014. View Article : Google Scholar : PubMed/NCBI | |
Khorramdelazad H, Bagheri V, Hassanshahi G, Karami H, Moogooei M, Zeinali M and Abedinzadeh M: S100A12 and RAGE expression in human bladder transitional cell carcinoma: A role for the ligand/RAGE axis in tumor progression? Asian Pac J Cancer Prev. 16:2725–2729. 2015. View Article : Google Scholar : PubMed/NCBI | |
Meghnani V, Wagh A, Indurthi VS, Koladia M, Vetter SW, Law B and Leclerc E: The receptor for advanced glycation end products influences the expression of its S100 protein ligands in melanoma tumors. Int J Biochem Cell Biol. 57:54–62. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kostova N, Zlateva S, Ugrinova I and Pasheva E: The expression of HMGB1 protein and its receptor RAGE in human malignant tumors. Mol Cell Biochem. 337:251–258. 2010. View Article : Google Scholar : PubMed/NCBI | |
Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, Rutledge R, Lin B, Amoscato AA, Zeh HJ and Lotze MT: RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med. 7:172009. View Article : Google Scholar : PubMed/NCBI | |
Wu R, Duan L, Cui F, Cao J, Xiang Y, Tang Y and Zhou L: S100A9 promotes human hepatocellular carcinoma cell growth and invasion through RAGE-mediated ERK1/2 and p38 MAPK pathways. Exp Cell Res. 334:228–238. 2015. View Article : Google Scholar : PubMed/NCBI | |
Iotzova-Weiss G, Dziunycz PJ, Freiberger SN, Läuchli S, Hafner J, Vogl T, French LE and Hofbauer GF: S100A8/A9 stimulates keratinocyte proliferation in the development of squamous cell carcinoma of the skin via the receptor for advanced glycation-end products. PLoS One. 10:e01209712015. View Article : Google Scholar : PubMed/NCBI | |
Hudson BI, Kalea AZ, Del Mar Arriero M, Harja E, Boulanger E, D'Agati V and Schmidt AM: Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J Biol Chem. 283:34457–34468. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kalea AZ, See F, Harja E, Arriero M, Schmidt AM and Hudson BI: Alternatively spliced RAGEv1 inhibits tumorigenesis through suppression of JNK signaling. Cancer Res. 70:5628–5638. 2010. View Article : Google Scholar : PubMed/NCBI | |
Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, Tanji N, Lu Y, Lalla E, Fu C, et al: Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 405:354–360. 2000. View Article : Google Scholar : PubMed/NCBI | |
Mizumoto S, Takahashi J and Sugahara K: Receptor for advanced glycation end products (RAGE) functions as receptor for specific sulfated glycosaminoglycans, and anti-RAGE antibody or sulfated glycosaminoglycans delivered in vivo inhibit pulmonary metastasis of tumor cells. J Biol Chem. 287:18985–18994. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sugihara T, Munesue S, Yamamoto Y, Sakurai S, Akhter N, Kitamura Y, Shiba K, Watanabe T, Yonekura H, Hayashi Y, et al: Endogenous secretory receptor for advanced glycation end-products inhibits amyloid-β1-42 uptake into mouse brain. J Alzheimers Dis. 28:709–720. 2012.PubMed/NCBI | |
Hong Y, Shen C, Yin Q, Sun M, Ma Y and Liu X: Effects of RAGE-specific inhibitor FPS-ZM1 on amyloid-β metabolism and AGEs-induced inflammation and oxidative stress in rat hippocampus. Neurochem Res. 41:1192–1199. 2016. View Article : Google Scholar : PubMed/NCBI | |
Cai C, Dai X, Zhu Y, Lian M, Xiao F, Dong F, Zhang Q, Huang Y and Zheng Q: A specific RAGE-binding peptide biopanning from phage display random peptide library that ameliorates symptoms in amyloid β peptide-mediated neuronal disorder. Appl Microbiol Biotechnol. 100:825–835. 2016. View Article : Google Scholar : PubMed/NCBI | |
Han YT, Kim K, Son D, An H, Kim H, Lee J, Park HJ, Lee J and Suh YG: Fine tuning of 4,6-bisphenyl-2-(3-alkoxyanilino)pyrimidine focusing on the activity-sensitive aminoalkoxy moiety for a therapeutically useful inhibitor of receptor for advanced glycation end products (RAGE). Bioorg Med Chem. 23:579–587. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kalea AZ, Schmidt AM and Hudson BI: RAGE: A novel biological and genetic marker for vascular disease. Clin Sci (Lond). 116:621–637. 2009. View Article : Google Scholar : PubMed/NCBI |