Aucubin slows the development of osteoporosis by inhibiting osteoclast differentiation via the nuclear factor erythroid 2-related factor 2-mediated antioxidation pathway

References

• Al-Daghri NM, Aziz I, Yakout S, Aljohani NJ, Al-Saleh Y, Amer OE, Sheshah E, Younis GZ, Al-Badr FBM. 2017. Inflammation as a contributing factor among postmenopausal Saudi women with osteoporosis. Medicine. 96(4):e5780.
   PubMed Web of Science ®Google Scholar
• Almeida M, Laurent MR, Dubois V, Claessens F, O'Brien CA, Bouillon R, Vanderschueren D, Manolagas SC. 2017. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol Rev. 97(1):135–187.
   PubMed Web of Science ®Google Scholar
• Bogusław C, Adam K, Mateusz K, Daniel K, Krzysztof S, Violetta D, Andrzej B, Andrzej P. 2010. The association of IL-1beta, IL-2, and IL-6 gene polymorphisms with bone mineral density and osteoporosis in postmenopausal women. Eur J Obstet Gynecol Reprod Biol. 149:82–85.
   PubMed Web of Science ®Google Scholar
• Bonaccorsi G, Piva I, Greco P, Cervellati C. 2018. Oxidative stress as a possible pathogenic cofactor of post-menopausal osteoporosis: Existing evidence in support of the axis oestrogen deficiency-redox imbalance-bone loss. Indian J Med Res. 147(4):341–351.
   PubMedGoogle Scholar
• Cai WJ, Chen Y, Shi LX, Cheng HR, Banda I, Ji YH, Wang YT, Li XM, Mao YX, Zhang DF, et al. 2019. AKT-GSK3β signaling pathway regulates mitochondrial dysfunction-associated OPA1 cleavage contributing to osteoblast apoptosis: preventative effects of hydroxytyrosol. Oxid Med Cell Longev. 2019:4101738.
   PubMed Web of Science ®Google Scholar
• Chen C, Qin Y, Fang J-p, Ni X-y, Yao J, Wang H-y, Ding K. 2015. WSS25, a sulfated polysaccharide, inhibits RANKL-induced mouse osteoclast formation by blocking SMAD/ID1 signaling. Acta Pharmacol Sin. 36(9):1053–1064.
   PubMed Web of Science ®Google Scholar
• Chen S, Wang X, Nisar MF, Lin M, Zhong JL. 2019. Heme oxygenases: Cellular multifunctional and protective molecules against UV-induced oxidative stress. Oxid Med Cell Longev. 2019:5416728.
   PubMed Web of Science ®Google Scholar
• Chen X, Zhi X, Cao L, Weng W, Pan P, Hu H, Liu C, Zhao Q, Zhou Q, Cui J, et al. 2017. Matrine derivate MASM uncovers a novel function for ribosomal protein S5 in osteoclastogenesis and postmenopausal osteoporosis. Cell Death Dis. 8(9):e3037.
   PubMed Web of Science ®Google Scholar
• Compston J. 2018. Glucocorticoid-induced osteoporosis: an update. Endocrine. 61(1):7–16.
   PubMed Web of Science ®Google Scholar
• Compston J, Cooper A, Cooper C, Gittoes N, Gregson C, Harvey N, Hope S, Kanis JA, McCloskey EV, Poole KES, et al.; National Osteoporosis Guideline Group (NOGG). 2017. UK clinical guideline for the prevention and treatment of osteoporosis. Arch Osteoporos. 12(1):43.
   PubMed Web of Science ®Google Scholar
• Drake MT, Clarke BL, Oursler MJ, Khosla S. 2017. Cathepsin K inhibitors for osteoporosis: Biology, potential clinical utility, and lessons learned. Endocr Rev. 38(4):325–350.
   PubMed Web of Science ®Google Scholar
• Fraser JHE, Helfrich MH, Wallace HM, Ralston SH. 1996. Hydrogen peroxide, but not superoxide, stimulates bone resorption in mouse calvariae. Bone. 19(3):223–226.
   PubMed Web of Science ®Google Scholar
• Georgiou L, Kivell TL, Pahr DH, Skinner MM. 2018. Trabecular bone patterning in the hominoid distal femur. PeerJ. 6:e5156.
   PubMed Web of Science ®Google Scholar
• Hu L, Yin C, Zhao F, Ali A, Ma J, Qian A. 2018. Mesenchymal Stem Cells: Cell fate decision to osteoblast or adipocyte and application in osteoporosis treatment. IJMS. 19(2):360.
   Google Scholar
• Ibáñez L, Ferrándiz ML, Brines R, Guede D, Cuadrado A, Alcaraz MJ. 2014. Effects of Nrf2 deficiency on bone microarchitecture in an experimental model of osteoporosis. Oxid Med Cell Longev. 2014:726590.
   PubMed Web of Science ®Google Scholar
• Kanis JA, Burlet N, Cooper C, Delmas PD, Reginster JY, Borgstrom F, Rizzoli R, European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) 2008. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int. 19(4):399–428.
   PubMed Web of Science ®Google Scholar
• Lee NK, Choi YG, Baik JY, Han SY, Jeong D-W, Bae YS, Kim N, Lee SY. 2005. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood. 106(3):852–859.
   PubMed Web of Science ®Google Scholar
• Levy R, Mott RF, Iraqi FA, Gabet Y. 2015. Collaborative cross mice in a genetic association study reveal new candidate genes for bone microarchitecture. BMC Genomics. 16(1):1013.
   PubMedGoogle Scholar
• Li X, Yang L, Guo Z. 2019. miR-193-3p ameliorates bone resorption in ovariectomized mice by blocking NFATc1 signaling. Int J Clin Exp Pathol. 12(11):4077–4086.
   PubMed Web of Science ®Google Scholar
• Li Y, Hu W, Han G, Lu W, Jia D, Hu M, Wang D. 2018. Involvement of bone morphogenetic protein-related pathways in the effect of aucubin on the promotion of osteoblast differentiation in MG63 cells. Chem Biol Interact. 283:51–58.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhang Y, Zhang X, Lu W, Liu X, Hu M, Wang D. 2020. Aucubin exerts anti-osteoporotic effects by promoting osteoblast differentiation. Aging (Albany NY). 12(3):2226–2245.
   PubMedGoogle Scholar
• Liu S, Zhou H, Liu H, Ji H, Fei W, Luo E. 2019. Fluorine-contained hydroxyapatite suppresses bone resorption through inhibiting osteoclasts differentiation and function in vitro and in vivo. Cell Prolif. 52(3):e12613.
   PubMed Web of Science ®Google Scholar
• Luo K, Ma S, Guo J, Huang Y, Yan F, Xiao Y. 2014. Association between postmenopausal osteoporosis and experimental periodontitis. Biomed Res Int. 2014:316134.
   PubMed Web of Science ®Google Scholar
• Ma B, Zhang Q, Wu D, Wang Y-l, Hu Y-y, Cheng Y-p, Yang Z-d, Zheng Y-y, Ying H-J. 2012. Strontium fructose 1,6-diphosphate prevents bone loss in a rat model of postmenopausal osteoporosis via the OPG/RANKL/RANK pathway. Acta Pharmacol Sin. 33(4):479–489.
   PubMed Web of Science ®Google Scholar
• Manolagas SC. 2010. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev. 31(3):266–300.
   PubMed Web of Science ®Google Scholar
• Mo H, Zhang N, Li H, Li F, Pu R. 2019. Beneficial effects of Cuscuta chinensis extract on glucocorticoid-induced osteoporosis through modulation of RANKL/OPG signals. Braz J Med Biol Res. 52(12):e8754.
   PubMed Web of Science ®Google Scholar
• Motyl KJ, McCabe LR. 2009. Leptin treatment prevents type I diabetic marrow adiposity but not bone loss in mice. J Cell Physiol. 218(2):376–384.
   PubMed Web of Science ®Google Scholar
• Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, et al. 2011. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med. 17(10):1231–1234.
   PubMed Web of Science ®Google Scholar
• Nishikawa A, Ishida T, Taketsuna M, Yoshiki F, Enomoto H. 2016. Safety and effectiveness of daily teriparatide in a prospective observational study in patients with osteoporosis at high risk of fracture in Japan: final report. Clin Interv Aging. 11:913–925.
   PubMed Web of Science ®Google Scholar
• Ohishi T, Fujita T, Suzuki D, Nishida T, Yamamoto K, Okabayashi R, Ushirozako H, Banno T, Matsuyama Y. 2017. Changes of bone mineral density and serum pentosidine during a 27-month follow-up of monthly minodronate in osteoporotic patients. Endocr Res. 42(3):232–240.
   PubMed Web of Science ®Google Scholar
• Ohlsson C, Henning P, Nilsson KH, Wu J, Gustafsson KL, Sjögren K, Törnqvist A, Koskela A, Zhang F-P, Lagerquist MK, et al. 2018. Inducible Wnt16 inactivation: WNT16 regulates cortical bone thickness in adult mice. J Endocrinol. 237(2):113–122.
   PubMed Web of Science ®Google Scholar
• Qiu X-M, Wang L, Gui Y-Y, Xu Y-P, Li D-J. 2015. BSNXD modulates mesenchymal stem cell differentiation into osteoblasts in a postmenopausal osteoporotic mouse model. Int J Clin Exp Pathol. 8:4408–4417.
   PubMed Web of Science ®Google Scholar
• Scheffler JM, Grahnemo L, Engdahl C, Drevinge C, Gustafsson KL, Corciulo C, Lawenius L, Iwakura Y, Sjogren K, Lagerquist MK, et al. 2020. Interleukin 17A: a Janus-faced regulator of osteoporosis. Sci Rep. 10(1):5692.
   PubMed Web of Science ®Google Scholar
• Shen B, Zhao C, Wang Y, Peng Y, Cheng J, Li Z, Wu L, Jin M, Feng H. 2019. Aucubin inhibited lipid accumulation and oxidative stress via Nrf2/HO-1 and AMPK signalling pathways. J Cell Mol Med. 23(6):4063–4075.
   PubMed Web of Science ®Google Scholar
• Swanson C, Lorentzon M, Conaway HH, Lerner UH. 2006. Glucocorticoid regulation of osteoclast differentiation and expression of receptor activator of nuclear factor-kappaB (NF-kappaB) ligand, osteoprotegerin, and receptor activator of NF-kappaB in mouse calvarial bones. Endocrinology. 147(7):3613–3622.
   PubMed Web of Science ®Google Scholar
• Takahashi T, Watanabe T, Nakada H, Sato H, Tanimoto Y, Sakae T, Kimoto S, Mijares D, Zhang Y, Kawai Y. 2016. Improved bone micro architecture healing time after implant surgery in an ovariectomized rat. J Hard Tissue Biology. 25(3):257–262.
   PubMed Web of Science ®Google Scholar
• Tu W, Wang H, Li S, Liu Q, Sha H. 2019. The anti-inflammatory and anti-oxidant mechanisms of the Keap1/Nrf2/ARE signaling pathway in chronic diseases. Aging Dis. 10(3):637–651.
   PubMed Web of Science ®Google Scholar
• Vasikaran S. 2018. Assessment of bone turnover in osteoporosis: harmonization of the total testing process. Clin Chem Lab Med. 56(10):1603–1607.
   PubMed Web of Science ®Google Scholar
• Vijayan V, Khandelwal M, Manglani K, Gupta S, Surolia A. 2014. Methionine down-regulates TLR4/MyD88/NF-κB signalling in osteoclast precursors to reduce bone loss during osteoporosis. Br J Pharmacol. 171(1):107–121.
   PubMed Web of Science ®Google Scholar
• Wang C-Y, Tang L, Li L, Zhou Q, Li Y-J, Li J, Wang Y-Z. 2020. Geographic authentication of Eucommia ulmoides leaves using multivariate analysis and preliminary study on the compositional response to environment. Front Plant Sci. 11:79.
   PubMed Web of Science ®Google Scholar
• Wang L, Huang CL, Li Q, Xu XM, Liu L, Huang K, Cai XX, Xiao JG. 2017. Osteogenic differentiation potential of adipose-derived stem cells from ovariectomized mice. Cell Prolif. 50(2):e12328.
   PubMed Web of Science ®Google Scholar
• Wu X, Xie C-Q, Zhu Q-Q, Wang M-Y, Sun B, Huang Y-P, Shen C, An M-F, Zhao Y-L, Wang X-J, et al. 2018. Green tea (Camellia sinensis) aqueous extract alleviates postmenopausal osteoporosis in ovariectomized rats and prevents RANKL-induced osteoclastogenesis in vitro. Food Nutr Res. 62:1–11.
   Web of Science ®Google Scholar
• Xu Z-S, Dai F, Chen J, Lv M, Cheng J-W, Zhang X-M, Lin B-W. 2018. Experimental research into the potential therapeutic effect of GYY4137 on ovariectomy-induced osteoporosis. Cell Mol Biol Lett. 23:47–47.
   PubMed Web of Science ®Google Scholar
• Yan Y, Zhao H, Chen C, Zou L, Liu X, Chai C, Wang C, Shi J, Chen S. 2018. Comparison of multiple bioactive constituents in different parts of Eucommia ulmoides based on UFLC-QTRAP-MS/MS combined with PCA. Molecules. 23(3):643.
   PubMed Web of Science ®Google Scholar
• Zamani M, Zamani V, Heidari B, Parsian H, Esmaeilnejad-Ganji SM. 2018. Prevalence of osteoporosis with the World Health Organization diagnostic criteria in the Eastern Mediterranean Region: a systematic review and meta-analysis. Arch Osteoporos. 13(1):129.
   PubMed Web of Science ®Google Scholar
• Zhang H, Davies KJA, Forman HJ. 2015. Oxidative stress response and Nrf2 signaling in aging. Free Radic Biol Med. 88(Pt B):314–336.
   PubMedGoogle Scholar
• Zhang R, Liu ZG, Li C, Hu SJ, Liu L, Wang JP, Mei QB. 2009. Du-Zhong (Eucommia ulmoides Oliv.) cortex extract prevent OVX-induced osteoporosis in rats. Bone. 45(3):553–559.
   PubMed Web of Science ®Google Scholar
• Zhang W, Fujikawa T, Mizuno K, Ishida T, Ooi K, Hirata T, Wada A. 2012. Eucommia leaf extract (ELE) prevents OVX-induced osteoporosis and obesity in rats. Am J Chin Med. 40(4):735–752.
   PubMed Web of Science ®Google Scholar
• Zhong Z, Qian Z, Zhang X, Chen F, Ni S, Kang Z, Zhang F, Li D, Yu B. 2019. Tetrandrine prevents bone loss in ovariectomized mice by inhibiting RANKL-induced osteoclastogenesis. Front Pharmacol. 10:1530–1530.
   PubMed Web of Science ®Google Scholar
• Zhou QZ, Zhu L, Zhang DF, Li N, Li Q, Dai PP, Mao YX, Li XM, Ma JF, Huang SB. 2016. Oxidative stress-related biomarkers in postmenopausal osteoporosis: a systematic review and meta-analyses. Dis Markers. 2016:7067984.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Deng T, Zhang H, Guan Q, Zhao H, Yu C, Shao S, Zhao M, Xu J. 2019. Hypercholesterolaemia increases the risk of high‑turnover osteoporosis in men. Mol Med Rep. 19:4603–4612.
   PubMed Web of Science ®Google Scholar
• Zhu S, Wei W, Liu Z, Yang Y, Jia H. 2018. Tanshinone‑IIA attenuates the deleterious effects of oxidative stress in osteoporosis through the NF‑κB signaling pathway. Mol Med Rep. 17(5):6969–6976.
   PubMed Web of Science ®Google Scholar
• Zhuang Y, Sun X, Liu B, Hou H, Sun Y. 2020. Effects of rambutan peel (Nephelium lappaceum) phenolicextract on RANKL-induced differentiation of RAW264.7 cells into osteoclasts and retinoic acid-induced osteoporosis in rats. Nutrients. 12(4):883.
   PubMed Web of Science ®Google Scholar