Nobiletin-loaded micelles reduce ovariectomy-induced bone loss by suppressing osteoclastogenesis

References

• Oftadeh R, Perez-Viloria M, Villa-Camacho JC, Vaziri A, Nazarian A. Biomechanics and mechanobiology of trabecular bone: a review. J Biomech Eng. 2015;137(1):010802. doi:10.1115/1.4029176
   Web of Science ®Google Scholar
• Paiva KBS, Granjeiro JM. Matrix metalloproteinases in bone resorption, remodeling, and repair. Prog Mol Biol Transl Sci. 2017;148:203–303.28662823
   PubMed Web of Science ®Google Scholar
• Bandeira L, Lewiecki EM, Bilezikian JP. Romosozumab for the treatment of osteoporosis. Expert Opin Biol Ther. 2017;17(2):255–263.28064540
   PubMed Web of Science ®Google Scholar
• Meeta RAA, Agashe SV, Wajahat A, Sarada CV, Vaidya AD, Vaidya RA. A clinical study of a standardized extract of leaves of Dalbergia sissoo (Roxb ex DC) in postmenopausal osteoporosis. J Midlife Health. 2019;10(1):37–42.31001055
   PubMedGoogle Scholar
• Dou C, Ding N, Zhao C, et al. Estrogen deficiency-mediated M2 macrophage osteoclastogenesis contributes to M1/M2 ratio alteration in ovariectomized osteoporotic mice. J Bone Miner Res. 2018;33(5):899–908.29281118
   PubMed Web of Science ®Google Scholar
• Du Z, Xiao Y, Hashimi S, Hamlet SM, Ivanovski S. The effects of implant topography on osseointegration under estrogen deficiency induced osteoporotic conditions: histomorphometric, transcriptional and ultrastructural analysis. Acta Biomater. 2016;42:351–363.27375286
   PubMed Web of Science ®Google Scholar
• Sharma D, Larriera AI, Palacio-Mancheno PE, et al. The effects of estrogen deficiency on cortical bone microporosity and mineralization. Bone. 2018;110:1–10.29357314
   PubMed Web of Science ®Google Scholar
• Cai M, Yang L, Zhang S, Liu J, Sun Y, Wang X. A bone-resorption surface-targeting nanoparticle to deliver anti-miR214 for osteoporosis therapy. Int J Nanomedicine. 2017;12:7469–7482.29075114
   PubMed Web of Science ®Google Scholar
• Offermanns V, Andersen OZ, Riede G, et al. Bone regenerating effect of surface-functionalized titanium implants with sustained-release characteristics of strontium in ovariectomized rats. Int J Nanomedicine. 2016;11:2431–2442.27313456
   PubMed Web of Science ®Google Scholar
• Teitelbaum SL. Bone resorption by osteoclasts. Science. 2000;289(5484):1504–1508. doi:10.1126/science.289.5484.150410968780
   PubMed Web of Science ®Google Scholar
• Bar-Shavit Z. The osteoclast: a multinucleated, hematopoietic-origin, bone-resorbing osteoimmune cell. J Cell Biochem. 2007;102(5):1130–1139. doi:10.1002/jcb.2155317955494
   PubMedGoogle Scholar
• Boyce BF. Advances in the regulation of osteoclasts and osteoclast functions. J Dent Res. 2013;92(10):860–867. doi:10.1177/002203451350030623906603
   PubMed Web of Science ®Google Scholar
• Kylmaoja E, Nakamura M, Tuukkanen J. Osteoclasts and remodeling based bone formation. Curr Stem Cell Res Ther. 2016;11(8):626–633.26477623
   PubMed Web of Science ®Google Scholar
• De Vries TJ, Schoenmaker T, Aerts D, et al. M-CSF priming of osteoclast precursors can cause osteoclastogenesis-insensitivity, which can be prevented and overcome on bone. J Cell Physiol. 2015;230(1):210–225. doi:10.1002/jcp.2470224962140
   PubMedGoogle Scholar
• Yamaguchi T, Movila A, Kataoka S, et al. Proinflammatory M1 macrophages inhibit RANKL-induced osteoclastogenesis. Infect Immun. 2016;84(10):2802–2812. doi:10.1128/IAI.00461-1627456834
   PubMed Web of Science ®Google Scholar
• Joo JH, Huh JE, Lee JH, et al. A novel pyrazole derivative protects from ovariectomy-induced osteoporosis through the inhibition of NADPH oxidase. Sci Rep. 2016;6:22389. doi:10.1038/srep2238926975635
   PubMed Web of Science ®Google Scholar
• Xia G, Wang X, Sun H, Qin Y, Fu M. Carnosic acid (CA) attenuates collagen-induced arthritis in db/db mice via inflammation suppression by regulating ROS-dependent p38 pathway. Free Radic Biol Med. 2017;108:418–432. doi:10.1016/j.freeradbiomed.2017.03.02328343998
   PubMed Web of Science ®Google Scholar
• Panteghini M, Pagani F. Reference intervals for two bone-derived enzyme activities in serum: bone isoenzyme of alkaline phosphatase (ALP) and tartrate-resistant acid phosphatase (TR-ACP). Clin Chem. 1989;35(1):180–181.2910567
   PubMed Web of Science ®Google Scholar
• Kyllonen L, D’Este M, Alini M, Eglin D. Local drug delivery for enhancing fracture healing in osteoporotic bone. Acta Biomater. 2015;11:412–434.25218339
   PubMed Web of Science ®Google Scholar
• Lone J, Parray HA, Yun JW. Nobiletin induces brown adipocyte-like phenotype and ameliorates stress in 3T3-L1 adipocytes. Biochimie. 2018;146:97–104.29217172
   PubMed Web of Science ®Google Scholar
• Sp N, Kang DY, Joung YH, et al. Nobiletin inhibits angiogenesis by regulating Src/FAK/STAT3-mediated signaling through PXN in ER(+) breast cancer cells. Int J Mol Sci. 2017;18(5):935.
   PubMed Web of Science ®Google Scholar
• Aoki K, Yokosuka A, Mimaki Y, Fukunaga K, Yamakuni T. Nobiletin induces inhibitions of Ras activity and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase signaling to suppress cell proliferation in C6 rat glioma cells. Biol Pharm Bull. 2013;36(4):540–547.23546290
   PubMed Web of Science ®Google Scholar
• Kanda K, Nishi K, Kadota A, Nishimoto S, Liu MC, Sugahara T. Nobiletin suppresses adipocyte differentiation of 3T3-L1 cells by an insulin and IBMX mixture induction. Biochim Biophys Acta. 2012;1820(4):461–468.22172985
   PubMed Web of Science ®Google Scholar
• Harada S, Tominari T, Matsumoto C, et al. Nobiletin, a polymethoxy flavonoid, suppresses bone resorption by inhibiting NFkappaB-dependent prostaglandin E synthesis in osteoblasts and prevents bone loss due to estrogen deficiency. J Pharmacol Sci. 2011;115(1):89–93.21258168
   PubMed Web of Science ®Google Scholar
• Khachane P, Date AA, Nagarsenker MS. Eudragit EPO nanoparticles: application in improving therapeutic efficacy and reducing ulcerogenicity of meloxicam on oral administration. J Biomed Nanotechnol. 2011;7(4):590–597.21870464
   PubMed Web of Science ®Google Scholar
• Gagliardi M, Bardi G, Bifone A. Polymeric nanocarriers for controlled and enhanced delivery of therapeutic agents to the CNS. Ther Deliv. 2012;3(7):875–887.22900468
   PubMedGoogle Scholar
• Dudhipala N, Veerabrahma K. Candesartan cilexetil loaded nanodelivery systems for improved oral bioavailability. Ther Deliv. 2017;8(2):79–88.28088883
   PubMedGoogle Scholar
• Zhang Y, He L, Yue S, Huang Q, Zhang Y, Yang J. Characterization and evaluation of a self-microemulsifying drug delivery system containing tectorigenin, an isoflavone with low aqueous solubility and poor permeability. Drug Deliv. 2017;24(1):632–640.28283000
   PubMed Web of Science ®Google Scholar
• e Silva C, de Oliveira D, Estevanato LL, et al. Successful strategy for targeting the central nervous system using magnetic albumin nanospheres. J Biomed Nanotechnol. 2012;8(1):182–189.22515106
   PubMed Web of Science ®Google Scholar
• Kesharwani SS, Kaur S, Tummala H, Sangamwar AT. Overcoming multiple drug resistance in cancer using polymeric micelles. Expert Opin Drug Deliv. 2018;15(11):1127–1142.30324813
   PubMed Web of Science ®Google Scholar
• Kesharwani SS, Kaur S, Tummala H, Sangamwar AT. Multifunctional approaches utilizing polymeric micelles to circumvent multidrug resistant tumors. Colloids Surf B Biointerfaces. 2019;173:581–590.30352379
   PubMed Web of Science ®Google Scholar
• Lei Y, Xu Z, Ke Q, et al. Strontium hydroxyapatite/chitosan nanohybrid scaffolds with enhanced osteoinductivity for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2017;72:134–142.28024569
   PubMed Web of Science ®Google Scholar
• Zhu C, Xiao J, Tang M, Feng H, Chen W, Du M. Platinum covalent shell cross-linked micelles designed to deliver doxorubicin for synergistic combination cancer therapy. Int J Nanomedicine. 2017;12:3697–3710.28553108
   PubMed Web of Science ®Google Scholar
• Shan F, Liu Y, Jiang H, Tong F. In vitro and in vivo protein release and anti-ischemia/reperfusion injury properties of bone morphogenetic protein-2-loaded glycyrrhetinic acid-poly(ethylene glycol)-b-poly(l-lysine) nanoparticles. Int J Nanomedicine. 2017;12:7613–7625.29089759
   PubMed Web of Science ®Google Scholar
• Oliveira MC, Di Ceglie I, Arntz OJ, et al. Milk-derived nanoparticle fraction promotes the formation of small osteoclasts but reduces bone resorption. J Cell Physiol. 2017;232(1):225–233.27138291
   PubMed Web of Science ®Google Scholar
• Grossen P, Witzigmann D, Sieber S, Huwyler J. PEG-PCL-based nanomedicines: a biodegradable drug delivery system and its application. J Control Release. 2017;260:46–60.28536049
   PubMed Web of Science ®Google Scholar
• Hu J, Zeng F, Wei J, Chen Y, Chen Y. Novel controlled drug delivery system for multiple drugs based on electrospun nanofibers containing nanomicelles. J Biomater Sci Polym Ed. 2014;25(3):257–268.24160558
   PubMed Web of Science ®Google Scholar
• Yao W, Xu P, Pang Z, et al. Local delivery of minocycline-loaded PEG-PLA nanoparticles for the enhanced treatment of periodontitis in dogs. Int J Nanomedicine. 2014;9:3963–3970.25170266
   PubMed Web of Science ®Google Scholar
• Gong CY, Wu QJ, Dong PW, et al. Acute toxicity evaluation of biodegradable in situ gel-forming controlled drug delivery system based on thermosensitive PEG-PCL-PEG hydrogel. J Biomed Mater Res B. 2009;91(1):26–36.
   Google Scholar
• Moon JY, Cho SK. Nobiletin induces protective autophagy accompanied by ER-stress mediated apoptosis in human gastric cancer SNU-16 cells. Molecules. 2016;21(7):914.
   PubMed Web of Science ®Google Scholar
• Murakami A, Nakamura Y, Torikai K, et al. Inhibitory effect of citrus nobiletin on phorbol ester-induced skin inflammation, oxidative stress, and tumor promotion in mice. Cancer Res. 2000;60(18):5059–5066.11016629
   PubMed Web of Science ®Google Scholar
• Murakami A, Song M, Katsumata S, Uehara M, Suzuki K, Ohigashi H. Citrus nobiletin suppresses bone loss in ovariectomized ddY mice and collagen-induced arthritis in DBA/1J mice: possible involvement of receptor activator of NF-kappaB ligand (RANKL)-induced osteoclastogenesis regulation. Biofactors. 2007;30(3):179–192.18525112
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang Z, Xie X, et al. Tatarinan N inhibits osteoclast differentiation through attenuating NF-kappaB, MAPKs and Ca(2+)-dependent signaling. Int Immunopharmacol. 2018;65:199–211.30316078
   PubMed Web of Science ®Google Scholar