Login Register Cart 0
Review Article

The Study of Natural Compounds Targeting RANKL Signaling Pathway for the Treatment of Bone Diseases

Author(s): Chang Liu, Yuan He, Xiaobing Xu, Lijun He, Baorong He* and Lingbo Kong*

Volume 21, Issue 4, 2020

Page: [344 - 357] Pages: 14

DOI: 10.2174/1389450120666190930145144

Price: $65

Abstract

Millions of people, especially for the aging people, are suffered by bone-loss diseases, such as rheumatoid arthritis (RA) and osteoporosis. Therefore, better understanding the involved mechanisms of bone metabolism is required for further treat on such diseases. Particularly, during the pathological process of bone losing, RANKL as a member of the tumor necrosis factor (TNF) superfamily, could induce osteoclast precursor cells differentiate into mature osteoclast, which grant its essential role in osteolysis. In recent years, with the increased attention paid to the natural compounds discovering studies, the therapeutic application of natural plant-derivatives have been widely recognized. Therefore, our present study aim to summarize the current novel research progressions on RANKL and its downstream signaling pathways in bone cellular differentiation, and provide a further insight for RANKL as the important drug targets in bone loss diseases. Besides that, in our current study, we also aim to briefly introduce the current application of several natural compounds for treating RANKL-mediated osteoclastic activation by modulating the RANKL signaling pathway and their therapeutic effects on the prevention of osteoporosis, osteoarthritis (OA) and RA.

Keywords: RANKL, NF-κB, MAPKs, Akt, Ca2+, osteoporosis, osteoarthritis, rheumatoid arthritis, signaling pathways.

« Previous Next »
Graphical Abstract

[1]
Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature 2003; 423(6937): 337-42.
[http://dx.doi.org/10.1038/nature01658] [PMID: 12748652]
[2]
Teitelbaum SL. Bone resorption by osteoclasts. Science 2000; 289(5484): 1504-8.
[http://dx.doi.org/10.1126/science.289.5484.1504] [PMID: 10968780]
[3]
Asagiri M, Takayanagi H. The molecular understanding of osteoclast differentiation. Bone 2007; 40(2): 251-64.
[http://dx.doi.org/10.1016/j.bone.2006.09.023] [PMID: 17098490]
[4]
Rodan GA, Martin TJ. Therapeutic approaches to bone diseases. Science 2000; 289(5484): 1508-14.
[http://dx.doi.org/10.1126/science.289.5484.1508] [PMID: 10968781]
[5]
Akiyama T, Dass CR, Choong PF. Novel therapeutic strategy for osteosarcoma targeting osteoclast differentiation, bone-resorbing activity, and apoptosis pathway. Mol Cancer Ther 2008; 7(11): 3461-9.
[http://dx.doi.org/10.1158/1535-7163.MCT-08-0530] [PMID: 19001431]
[6]
Park JH, Lee NK, Lee SY. Current understanding of rank signaling in osteoclast differentiation and maturation. Mol Cells 2017; 40(10): 706-13.
[PMID: 29047262]
[7]
Bremer E, de Bruyn M, Wajant H, Helfrich W. Targeted cancer immunotherapy using ligands of the tumor necrosis factor super-family. Curr Drug Targets 2009; 10(2): 94-103.
[http://dx.doi.org/10.2174/138945009787354593] [PMID: 19199904]
[8]
Liu W, Zhang X. Receptor activator of nuclear factor-κB ligand (RANKL)/RANK/osteoprotegerin system in bone and other tissues. (review) Mol Med Rep 2015; 11(5): 3212-8.
[http://dx.doi.org/10.3892/mmr.2015.3152] [PMID: 25572286]
[9]
Martin TJ, Sims NA. RANKL/OPG; Critical role in bone physiology. Rev Endocr Metab Disord 2015; 16(2): 131-9.
[http://dx.doi.org/10.1007/s11154-014-9308-6] [PMID: 25557611]
[10]
Suda T, Kobayashi K, Jimi E, Udagawa N, Takahashi N. The molecular basis of osteoclast differentiation and activation. Novartis Found Symp 2001; 232: 235-47.
[http://dx.doi.org/10.1002/0470846658.ch16] [PMID: 11277084]
[11]
Koga T, Inui M, Inoue K, et al. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 2004; 428(6984): 758-63.
[http://dx.doi.org/10.1038/nature02444] [PMID: 15085135]
[12]
Kong L, Yang C, Yu L, et al. Pyrroloquinoline quinine inhibits RANKL-mediated expression of NFATc1 in part via suppression of c-Fos in mouse bone marrow cells and inhibits wear particle-induced osteolysis in mice. PLoS One 2013; 8(4)e61013
[http://dx.doi.org/10.1371/journal.pone.0061013] [PMID: 23613773]
[13]
Kong L, Zhao Q, Wang X, Zhu J, Hao D, Yang C. Angelica sinensis extract inhibits RANKL-mediated osteoclastogenesis by down-regulated the expression of NFATc1 in mouse bone marrow cells. BMC Complement Altern Med 2014; 14: 481.
[http://dx.doi.org/10.1186/1472-6882-14-481] [PMID: 25496242]
[14]
Yuan FL, Xu RS, Jiang DL, et al. Leonurine hydrochloride inhibits osteoclastogenesis and prevents osteoporosis associated with estrogen deficiency by inhibiting the NF-κB and PI3K/Akt signaling pathways. Bone 2015; 75: 128-37.
[http://dx.doi.org/10.1016/j.bone.2015.02.017] [PMID: 25708053]
[15]
Kong L, Wang Y, Smith W, Hao D. Macrophages in Bone Homeostasis. Curr Stem Cell Res Ther 2019; 14(6): 474-81.
[http://dx.doi.org/10.2174/1574888X14666190214163815] [PMID: 30767753]
[16]
Song C, Yang X, Lei Y, Zhang Z, Smith W, Yan J, et al. Evaluation of efficacy on RANKL induced osteoclast from RAW264.7 cells. J Cell Physiol 2019; 234(7): 11969-75.
[PMID: 30515780]
[17]
van Heerden B, Kasonga A, Kruger MC, Coetzee M. Palmitoleic Acid Inhibits RANKL-Induced Osteoclastogenesis and Bone Resorption by Suppressing NF-κB and MAPK Signalling Pathways. Nutrients 2017; 9(5)E441
[http://dx.doi.org/10.3390/nu9050441] [PMID: 28452958]
[18]
Yang X, Gao W, Wang B, et al. Picroside II inhibits rankl-mediated osteoclastogenesis by attenuating the nf-κb and mapks signaling pathway in vitro and prevents bone loss in lipopolysaccharide treatment mice. J Cell Biochem 2017; 118(12): 4479-86.
[http://dx.doi.org/10.1002/jcb.26105] [PMID: 28464271]
[19]
Takeshita S, Kaji K, Kudo A. Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J Bone Miner Res 2000; 15(8): 1477-88.
[http://dx.doi.org/10.1359/jbmr.2000.15.8.1477]
[20]
Kuehn BM. Prolonged bisphosphonate use linked to rare fractures, esophageal cancer. JAMA 2010; 304(19): 2114-5.
[http://dx.doi.org/10.1001/jama.2010.1653] [PMID: 21081719]
[21]
Wehrhan F, Gross C, Creutzburg K, et al. Osteoclastic expression of higher-level regulators NFATc1 and BCL6 in medication-related osteonecrosis of the jaw secondary to bisphosphonate therapy: a comparison with osteoradionecrosis and osteomyelitis. J Transl Med 2019; 17(1): 69.
[http://dx.doi.org/10.1186/s12967-019-1819-1] [PMID: 30832685]
[22]
Wang J, Fu B, Lu F, Hu X, Tang J, Huang L. Inhibitory activity of linarin on osteoclastogenesis through receptor activator of nuclear factor κB ligand-induced NF-κB pathway. Biochem Biophys Res Commun 2018; 495(3): 2133-8.
[http://dx.doi.org/10.1016/j.bbrc.2017.12.091] [PMID: 29269297]
[23]
Bae YS, Chang J, Park SM. Oral bisphosphonate use and the risk of female breast, ovarian, and cervical cancer: a nationwide population-based cohort study. Arch Osteoporos 2019; 14(1): 41.
[http://dx.doi.org/10.1007/s11657-019-0588-z] [PMID: 30888545]
[24]
Gallagher JC, Sai AJ. Bisphosphonate use in osteoporosis: Cardiovascular effects. Menopause 2010; 17(1): 5-7.
[http://dx.doi.org/10.1097/gme.0b013e3181c615f6] [PMID: 19934778]
[25]
Sharman MJ, Verdile G, Kirubakaran S, et al. Targeting inflammatory pathways in alzheimer’s disease: a focus on natural products and phytomedicines. CNS Drugs 2019; 33(5): 457-80.
[http://dx.doi.org/10.1007/s40263-019-00619-1] [PMID: 30900203]
[26]
Chen DQ, Hu HH, Wang YN, Feng YL, Cao G, Zhao YY. Natural products for the prevention and treatment of kidney disease. Phytomedicine 2018; 50: 50-60.
[http://dx.doi.org/10.1016/j.phymed.2018.09.182]
[27]
Doss HM, Samarpita S, Ganesan R, Rasool M. Ferulic acid, a dietary polyphenol suppresses osteoclast differentiation and bone erosion via the inhibition of RANKL dependent NF-κB signalling pathway. Life Sci 2018; 207: 284-95.
[http://dx.doi.org/10.1016/j.lfs.2018.06.013] [PMID: 29908722]
[28]
Vaira S, Johnson T, Hirbe AC, et al. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. Proc Natl Acad Sci USA 2008; 105(10): 3897-902.
[http://dx.doi.org/10.1073/pnas.0708576105] [PMID: 18322009]
[29]
Kong L, Wang B, Yang X, et al. Picrasidine i from picrasma quassioides suppresses osteoclastogenesis via inhibition of rankl induced signaling pathways and attenuation of ros production. Cell Physiol Biochem 2017; 43(4): 1425-35.
[http://dx.doi.org/10.1159/000481874] [PMID: 29017159]
[30]
Iotsova V, Caamaño J, Loy J, Yang Y, Lewin A, Bravo R. Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat Med 1997; 3(11): 1285-9.
[http://dx.doi.org/10.1038/nm1197-1285] [PMID: 9359707]
[31]
Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 2010; 1802(4): 396-405.
[http://dx.doi.org/10.1016/j.bbadis.2009.12.009] [PMID: 20079433]
[32]
Dhillon AS, Hagan S, Rath O, Kolch W. MAP kinase signalling pathways in cancer. Oncogene 2007; 26(22): 3279-90.
[http://dx.doi.org/10.1038/sj.onc.1210421] [PMID: 17496922]
[33]
Kraunz KS, Nelson HH, Liu M, Wiencke JK, Kelsey KT. Interaction between the bone morphogenetic proteins and Ras/MAP-kinase signalling pathways in lung cancer. Br J Cancer 2005; 93(8): 949-52.
[http://dx.doi.org/10.1038/sj.bjc.6602790] [PMID: 16175182]
[34]
Yu M, Chen X, Lv C, et al. Curcumol suppresses RANKL-induced osteoclast formation by attenuating the JNK signaling pathway. Biochem Biophys Res Commun 2014; 447(2): 364-70.
[http://dx.doi.org/10.1016/j.bbrc.2014.04.009] [PMID: 24732351]
[35]
Ikeda F, Nishimura R, Matsubara T, et al. Critical roles of c-Jun signaling in regulation of NFAT family and RANKL-regulated osteoclast differentiation. J Clin Invest 2004; 114(4): 475-84.
[http://dx.doi.org/10.1172/JCI200419657] [PMID: 15314684]
[36]
Matsumoto M, Sudo T, Saito T, Osada H, Tsujimoto M. Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J Biol Chem 2000; 275(40): 31155-61.
[http://dx.doi.org/10.1074/jbc.M001229200] [PMID: 10859303]
[37]
David JP, Sabapathy K, Hoffmann O, Idarraga MH, Wagner EF. JNK1 modulates osteoclastogenesis through both c-Jun phosphorylation-dependent and -independent mechanisms. J Cell Sci 2002; 115(Pt 22): 4317-25.
[http://dx.doi.org/10.1242/jcs.00082] [PMID: 12376563]
[38]
Zhu W, Yin Z, Zhang Q, et al. Proanthocyanidins inhibit osteoclast formation and function by inhibiting the NF-κB and JNK signaling pathways during osteoporosis treatment. Biochem Biophys Res Commun 2019; 509(1): 294-300.
[http://dx.doi.org/10.1016/j.bbrc.2018.12.125] [PMID: 30583865]
[39]
Nie S, Xu J, Zhang C, Xu C, Liu M, Yu D. Salicortin inhibits osteoclast differentiation and bone resorption by down-regulating JNK and NF-κB/NFATc1 signaling pathways. Biochem Biophys Res Commun 2016; 470(1): 61-7.
[http://dx.doi.org/10.1016/j.bbrc.2015.12.115] [PMID: 26740180]
[40]
Moon JB, Kim JH, Kim K, Youn BU, Ko A, Lee SY, et al. Akt induces osteoclast differentiation through regulating the GSK3beta/NFATc1 signaling cascade. Journal of immunology (Baltimore, Md : 1950) 2012; 188(1): 163-9.
[41]
Slattery ML, Mullany LE, Sakoda LC, et al. The PI3K/AKT signaling pathway: Associations of miRNAs with dysregulated gene expression in colorectal cancer. Mol Carcinog 2018; 57(2): 243-61.
[http://dx.doi.org/10.1002/mc.22752] [PMID: 29068474]
[42]
Izawa T, Zou W, Chappel JC, Ashley JW, Feng X, Teitelbaum SL. c-Src links a RANK/αvβ3 integrin complex to the osteoclast cytoskeleton. Mol Cell Biol 2012; 32(14): 2943-53.
[http://dx.doi.org/10.1128/MCB.00077-12] [PMID: 22615494]
[43]
Vergadi E, Ieronymaki E, Lyroni K, Vaporidi K, Tsatsanis C. Akt signaling pathway in macrophage activation and m1/m2 polarization. J Immunol 2017; 198(3): 1006-14.
[http://dx.doi.org/10.4049/jimmunol.1601515] [PMID: 28115590]
[44]
Humphrey MB, Nakamura MC. A comprehensive review of immunoreceptor regulation of osteoclasts. Clin Rev Allergy Immunol 2016; 51(1): 48-58.
[http://dx.doi.org/10.1007/s12016-015-8521-8] [PMID: 26573914]
[45]
Faccio R, Cremasco V. PLCgamma2: where bone and immune cells find their common ground. Ann N Y Acad Sci 2010; 1192: 124-30.
[http://dx.doi.org/10.1111/j.1749-6632.2009.05217.x] [PMID: 20392227]
[46]
Kim JM, Lee K, Jeong D. Selective regulation of osteoclast adhesion and spreading by PLCγ/PKCα-PKCδ/RhoA-Rac1 signaling. BMB Rep 2018; 51(5): 230-5.
[http://dx.doi.org/10.5483/BMBRep.2018.51.5.198] [PMID: 29301608]
[47]
Jakus Z, Simon E, Frommhold D, Sperandio M, Mócsai A. Critical role of phospholipase Cgamma2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis. J Exp Med 2009; 206(3): 577-93.
[http://dx.doi.org/10.1084/jem.20081859] [PMID: 19273622]
[48]
Patterson RL, van Rossum DB, Nikolaidis N, Gill DL, Snyder SH. Phospholipase C-gamma: diverse roles in receptor-mediated calcium signaling. Trends Biochem Sci 2005; 30(12): 688-97.
[http://dx.doi.org/10.1016/j.tibs.2005.10.005] [PMID: 16260143]
[49]
Park KH, Park B, Yoon DS, et al. Zinc inhibits osteoclast differentiation by suppression of Ca2+-Calcineurin-NFATc1 signaling pathway. Cell Commun Signal 2013; 11: 74.
[http://dx.doi.org/10.1186/1478-811X-11-74] [PMID: 24088289]
[50]
Negishi-Koga T, Takayanagi H. Ca2+-NFATc1 signaling is an essential axis of osteoclast differentiation. Immunol Rev 2009; 231(1): 241-56.
[http://dx.doi.org/10.1111/j.1600-065X.2009.00821.x] [PMID: 19754901]
[51]
Boyce BF, Yamashita T, Yao Z, Zhang Q, Li F, Xing L. Roles for NF-kappaB and c-Fos in osteoclasts. J Bone Miner Metab 2005; 23(Suppl.): 11-5.
[http://dx.doi.org/10.1007/BF03026317] [PMID: 15984408]
[52]
Baek JM, Park SH, Cheon YH, et al. Esculetin attenuates receptor activator of nuclear factor kappa-B ligand-mediated osteoclast differentiation through c-Fos/nuclear factor of activated T-cells c1 signaling pathway. Biochem Biophys Res Commun 2015; 461(2): 334-41.
[http://dx.doi.org/10.1016/j.bbrc.2015.04.034] [PMID: 25887803]
[53]
Wang ZQ, Ovitt C, Grigoriadis AE, Möhle-Steinlein U, Rüther U, Wagner EF. Bone and haematopoietic defects in mice lacking c-fos. Nature 1992; 360(6406): 741-5.
[http://dx.doi.org/10.1038/360741a0] [PMID: 1465144]
[54]
Kim JH, Kim N. Regulation of NFATc1 in osteoclast differentiation. J Bone Metab 2014; 21(4): 233-41.
[http://dx.doi.org/10.11005/jbm.2014.21.4.233] [PMID: 25489571]
[55]
Park CK, Kim HJ, Kwak HB, et al. Inhibitory effects of Stewartia koreana on osteoclast differentiation and bone resorption. Int Immunopharmacol 2007; 7(12): 1507-16.
[http://dx.doi.org/10.1016/j.intimp.2007.07.016] [PMID: 17920527]
[56]
Aliprantis AO, Ueki Y, Sulyanto R, et al. NFATc1 in mice represses osteoprotegerin during osteoclastogenesis and dissociates systemic osteopenia from inflammation in cherubism. J Clin Invest 2008; 118(11): 3775-89.
[http://dx.doi.org/10.1172/JCI35711] [PMID: 18846253]
[57]
Matsuo K, Ray N. Osteoclasts, mononuclear phagocytes, and c-Fos: new insight into osteoimmunology. Keio J Med 2004; 53(2): 78-84.
[http://dx.doi.org/10.2302/kjm.53.78] [PMID: 15247511]
[58]
NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA 2001; 285(6): 785-95.
[http://dx.doi.org/10.1001/jama.285.6.785] [PMID: 11176917]
[59]
Zhao XL, Chen LF, Wang Z. Aesculin modulates bone metabolism by suppressing receptor activator of NF-κB ligand (RANKL)-induced osteoclastogenesis and transduction signals. Biochem Biophys Res Commun 2017; 488(1): 15-21.
[http://dx.doi.org/10.1016/j.bbrc.2017.04.148] [PMID: 28465233]
[60]
Hsiao HB, Wu JB, Lin WC. (-)-Epicatechin 3-O-β-D-allopyranoside prevent ovariectomy-induced bone loss in mice by suppressing RANKL-induced NF-κB and NFATc-1 signaling pathways. BMC Complement Altern Med 2017; 17(1): 245.
[http://dx.doi.org/10.1186/s12906-017-1737-9] [PMID: 28468652]
[61]
Yang X, Hu G, Lv L, et al. Regulation of P-glycoprotein by Bajijiasu in vitro and in vivo by activating the Nrf2-mediated signalling pathway. Pharm Biol 2019; 57(1): 184-92.
[http://dx.doi.org/10.1080/13880209.2019.1582679] [PMID: 30929555]
[62]
Chen DL, Zhang P, Lin L, et al. Protective effect of Bajijiasu against β-amyloid-induced neurotoxicity in PC12 cells. Cell Mol Neurobiol 2013; 33(6): 837-50.
[http://dx.doi.org/10.1007/s10571-013-9950-7] [PMID: 23812758]
[63]
Wu ZQ, Chen DL, Lin FH, et al. Effect of bajijiasu isolated from Morinda officinalis F. C. how on sexual function in male mice and its antioxidant protection of human sperm. J Ethnopharmacol 2015; 164: 283-92.
[http://dx.doi.org/10.1016/j.jep.2015.02.016] [PMID: 25686781]
[64]
Chen DL, Zhang P, Lin L, Zhang HM, Deng SD, Wu ZQ, et al. Protective effects of bajijiasu in a rat model of Abeta(2)(5)(-)(3)(5)-induced neurotoxicity. J Ethnopharmacol 2014; 154(1): 206-17.
[http://dx.doi.org/10.1016/j.jep.2014.04.004] [PMID: 24742752]
[65]
Hong G, Zhou L, Shi X, et al. Bajijiasu abrogates osteoclast differentiation via the suppression of rankl signaling pathways through nf-κb and nfat. Int J Mol Sci 2017; 18(1)E203
[http://dx.doi.org/10.3390/ijms18010203] [PMID: 28106828]
[66]
Ma X, Liu Y, Zhang Y, Yu X, Wang W, Zhao D. Jolkinolide B inhibits RANKL-induced osteoclastogenesis by suppressing the activation NF-κB and MAPK signaling pathways. Biochem Biophys Res Commun 2014; 445(2): 282-8.
[http://dx.doi.org/10.1016/j.bbrc.2014.01.145] [PMID: 24491533]
[67]
Yang L, Liu X, Zhong L, et al. Dioscin inhibits virulence factors of candida albicans. BioMed Res Int 2018; 20184651726
[http://dx.doi.org/10.1155/2018/4651726] [PMID: 30598996]
[68]
Tao X, Sun X, Yin L, et al. Dioscin ameliorates cerebral ischemia/reperfusion injury through the downregulation of TLR4 signaling via HMGB-1 inhibition. Free Radic Biol Med 2015; 84: 103-15.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.03.003] [PMID: 25772012]
[69]
Yao H, Sun Y, Song S, et al. Protective effects of dioscin against lipopolysaccharide-induced acute lung injury through inhibition of oxidative stress and inflammation. Front Pharmacol 2017; 8: 120.
[http://dx.doi.org/10.3389/fphar.2017.00120] [PMID: 28377715]
[70]
Qiao Y, Xu L, Tao X, et al. Protective effects of dioscin against fructose-induced renal damage via adjusting Sirt3-mediated oxidative stress, fibrosis, lipid metabolism and inflammation. Toxicol Lett 2018; 284: 37-45.
[http://dx.doi.org/10.1016/j.toxlet.2017.11.031] [PMID: 29197622]
[71]
Xu T, Zhang S, Zheng L, Yin L, Xu L, Peng J. A 90-day subchronic toxicological assessment of dioscin, a natural steroid saponin, in Sprague-Dawley rats. Food Chem Toxicol 2012; 50(5): 1279-87.
[http://dx.doi.org/10.1016/j.fct.2012.02.027] [PMID: 22386816]
[72]
Qu X, Zhai Z, Liu X, et al. Dioscin inhibits osteoclast differentiation and bone resorption though down-regulating the Akt signaling cascades. Biochem Biophys Res Commun 2014; 443(2): 658-65.
[http://dx.doi.org/10.1016/j.bbrc.2013.12.029] [PMID: 24333429]
[73]
Yang L, Liu S, Mu S, et al. Leonurine hydrochloride promotes osteogenic differentiation and increases osteoblastic bone formation in ovariectomized mice by Wnt/β-catenin pathway. Biochem Biophys Res Commun 2018; 504(4): 941-8.
[http://dx.doi.org/10.1016/j.bbrc.2018.09.008] [PMID: 30224063]
[74]
Zhang X, Zhou Y, Gu YE. Tanshinone IIA induces apoptosis of ovarian cancer cells in vitro and in vivo through attenuation of PI3K/AKT/JNK signaling pathways. Oncol Lett 2019; 17(2): 1896-902.
[PMID: 30675253]
[75]
Li S, Jiao Y, Wang H, et al. Sodium tanshinone IIA sulfate adjunct therapy reduces high-sensitivity C-reactive protein level in coronary artery disease patients: a randomized controlled trial. Sci Rep 2017; 7(1): 17451.
[http://dx.doi.org/10.1038/s41598-017-16980-4] [PMID: 29234038]
[76]
Gao S, Liu Z, Li H, Little PJ, Liu P, Xu S. Cardiovascular actions and therapeutic potential of tanshinone IIA. Atherosclerosis 2012; 220(1): 3-10.
[http://dx.doi.org/10.1016/j.atherosclerosis.2011.06.041] [PMID: 21774934]
[77]
Gao H, Huang L, Ding F, et al. Simultaneous purification of dihydrotanshinone, tanshinone I, cryptotanshinone, and tanshinone IIA from Salvia miltiorrhiza and their anti-inflammatory activities investigation. Sci Rep 2018; 8(1): 8460.
[http://dx.doi.org/10.1038/s41598-018-26828-0] [PMID: 29855534]
[78]
Kwak HB, Yang D, Ha H, et al. Tanshinone IIA inhibits osteoclast differentiation through down-regulation of c-Fos and NFATc1. Exp Mol Med 2006; 38(3): 256-64.
[http://dx.doi.org/10.1038/emm.2006.31] [PMID: 16819284]
[79]
Kim HH, Kim JH, Kwak HB, et al. Inhibition of osteoclast differentiation and bone resorption by tanshinone IIA isolated from Salvia miltiorrhiza Bunge. Biochem Pharmacol 2004; 67(9): 1647-56.
[http://dx.doi.org/10.1016/j.bcp.2003.12.031] [PMID: 15081864]
[80]
Lee TH, Kwak HB, Kim HH, et al. Methanol extracts of Stewartia koreana inhibit cyclooxygenase-2 (COX-2) and inducible nitric oxide synthase (iNOS) gene expression by blocking NF-kappaB transactivation in LPS-activated RAW 264.7 cells. Mol Cells 2007; 23(3): 398-404.
[PMID: 17646715]
[81]
Calixto JB, Campos MM, Otuki MF, Santos AR. Anti-inflammatory compounds of plant origin. Part II. modulation of pro-inflammatory cytokines, chemokines and adhesion molecules. Planta Med 2004; 70(2): 93-103.
[http://dx.doi.org/10.1055/s-2004-815483] [PMID: 14994184]
[82]
Wang HB, Yu DQ, Liang XT, Watanabe N, Tamai M, Omura S. Structures of two nortriterpenoid saponins from Stauntonia chinensis. J Nat Prod 1990; 53(2): 313-8.
[http://dx.doi.org/10.1021/np50068a007] [PMID: 2380709]
[83]
Chen Z, Wen L, Martin M, et al. Oxidative stress activates endothelial innate immunity via sterol regulatory element binding protein 2 (SREBP2) transactivation of microRNA-92a. Circulation 2015; 131(9): 805-14.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.114.013675] [PMID: 25550450]
[84]
Gao H, Zhao F, Chen GD, et al. Bidesmoside triterpenoid glycosides from Stauntonia chinensis and relationship to anti-inflammation. Phytochemistry 2009; 70(6): 795-806.
[http://dx.doi.org/10.1016/j.phytochem.2009.04.005] [PMID: 19427657]
[85]
Zhao J, Yim SH, Um JI, Park SH, Oh ES, Jung DW, et al. Cytotoxic components in an extract from the leaves and stems of Stauntonia hexaphylla. Nat Prod Sci 2014; 20(2): 130-4.
[86]
Cheon YH, Baek JM, Park SH, et al. Stauntonia hexaphylla (Lardizabalaceae) leaf methanol extract inhibits osteoclastogenesis and bone resorption activity via proteasome-mediated degradation of c-Fos protein and suppression of NFATc1 expression. BMC Complement Altern Med 2015; 15: 280.
[http://dx.doi.org/10.1186/s12906-015-0801-6] [PMID: 26271279]
[87]
Zhu X, Gu J, Qian H. Esculetin attenuates the growth of lung cancer by downregulating wnt targeted genes and suppressing NF-κB. Arch Bronconeumol 2018; 54(3): 128-33.
[PMID: 29108761]
[88]
Ragazzi E, Froldi G, Fassina G. Effects of esculetin (6,7-dihydroxycoumarin) on guinea-pig tracheal chains in vitro. Pharmacol Res 1989; 21(2): 183-92.
[http://dx.doi.org/10.1016/1043-6618(89)90237-5] [PMID: 2501776]
[89]
Kim AD, Han X, Piao MJ, et al. Esculetin induces death of human colon cancer cells via the reactive oxygen species-mediated mitochondrial apoptosis pathway. Environ Toxicol Pharmacol 2015; 39(2): 982-9.
[http://dx.doi.org/10.1016/j.etap.2015.03.003] [PMID: 25818986]
[90]
Baek JM, Kim JY, Lee CH, Yoon KH, Lee MS. Methyl gallate inhibits osteoclast formation and function by suppressing akt and btk-plcγ2-ca2+ signaling and prevents lipopolysaccharide-induced bone loss. Int J Mol Sci 2017; 18(3): E58.1 .
[http://dx.doi.org/10.3390/ijms18030581] [PMID: 28272351]
[91]
Kim JY, Park SH, Baek JM, et al. Harpagoside inhibits rankl-induced osteoclastogenesis via syk-btk-plcγ2-ca(2+) signaling pathway and prevents inflammation-mediated bone loss. J Nat Prod 2015; 78(9): 2167-74.
[http://dx.doi.org/10.1021/acs.jnatprod.5b00233] [PMID: 26308264]
[92]
Durand M, Komarova SV, Bhargava A, et al. Monocytes from patients with osteoarthritis display increased osteoclastogenesis and bone resorption: The in vitro Osteoclast Differentiation in Arthritis study. Arthritis Rheum 2013; 65(1): 148-58.
[http://dx.doi.org/10.1002/art.37722] [PMID: 23044761]
[93]
Moon SM, Lee SA, Han SH, Park BR, Choi MS, Kim JS, et al. Aqueous extract of Codium fragile alleviates osteoarthritis through the MAPK/NF-kappaB pathways in IL-1beta-induced rat primary chondrocytes and a rat osteoarthritis model. Biomedicine pharmacother 2018; 97: 264-70.
[94]
Ran J, Ma C, Xu K, et al. Schisandrin B ameliorated chondrocytes inflammation and osteoarthritis via suppression of NF-κB and MAPK signal pathways. Drug Des Devel Ther 2018; 12: 1195-204.
[http://dx.doi.org/10.2147/DDDT.S162014] [PMID: 29785089]
[95]
Fu Y, Lei J, Zhuang Y, Zhang K, Lu D. Overexpression of HMGB1 A-box reduced IL-1β-induced MMP expression and the production of inflammatory mediators in human chondrocytes. Exp Cell Res 2016; 349(1): 184-90.
[http://dx.doi.org/10.1016/j.yexcr.2016.10.014] [PMID: 27771306]
[96]
Marcu KB, Otero M, Olivotto E, Borzi RM, Goldring MB. NF-kappaB signaling: multiple angles to target OA. Curr Drug Targets 2010; 11(5): 599-613.
[http://dx.doi.org/10.2174/138945010791011938] [PMID: 20199390]
[97]
Chen Y, Shou K, Gong C, Yang H, Yang Y, Bao T. Anti-inflammatory effect of geniposide on osteoarthritis by suppressing the activation of p38 mapk signaling pathway. BioMed Res Int 2018; 20188384576
[http://dx.doi.org/10.1155/2018/8384576] [PMID: 29682561]
[98]
Abnosi MH, Yari S. The toxic effect of gallic acid on biochemical factors, viability and proliferation of rat bone marrow mesenchymal stem cells was compensated by boric acid. J Trace Elem Med Biol 2018; 48: 246-53.
[http://dx.doi.org/10.1016/j.jtemb.2018.04.016] [PMID: 29773188]
[99]
Shruthi S, Bhasker Shenoy K. Genoprotective effects of gallic acid against cisplatin induced genotoxicity in bone marrow cells of mice. Toxicol Res (Camb) 2018; 7(5): 951-8.
[http://dx.doi.org/10.1039/C8TX00058A] [PMID: 30310672]
[100]
Huynh K, Reinhold D. Metabolism of Sulfamethoxazole by the model plant Arabidopsis thaliana. Environ Sci Technol 2019; 53(9): 4901-11.
[http://dx.doi.org/10.1021/acs.est.8b06657] [PMID: 30917276]
[101]
Lee SE, Chung WJ, Kwak HB, et al. Tumor necrosis factor-alpha supports the survival of osteoclasts through the activation of Akt and ERK. J Biol Chem 2001; 276(52): 49343-9.
[http://dx.doi.org/10.1074/jbc.M103642200] [PMID: 11675379]
[102]
Lu Z, Liu Q, Liu L, Wu H, Zheng L, Zhao JM. A novel synthesized sulfonamido-based gallate-jeztc blocks cartilage degradation on rabbit model of osteoarthritis: An in vitro and in vivo study. Cell Physiol Biochem 2018; 49(6): 2304-19.
[103]
Zhang Y, Yan M, Yu QF, et al. Puerarin prevents lps-induced osteoclast formation and bone loss via inhibition of akt activation. Biol Pharm Bull 2016; 39(12): 2028-35.
[http://dx.doi.org/10.1248/bpb.b16-00522] [PMID: 27904045]
[104]
Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010; 376(9746): 1094-108.
[http://dx.doi.org/10.1016/S0140-6736(10)60826-4] [PMID: 20870100]
[105]
Tanaka S, Tanaka Y, Ishiguro N, Yamanaka H, Takeuchi T. RANKL: A therapeutic target for bone destruction in rheumatoid arthritis. Mod Rheumatol 2018; 28(1): 9-16.
[http://dx.doi.org/10.1080/14397595.2017.1369491] [PMID: 28880683]
[106]
Harshan S, Dey P, Ragunathan S. Effects of rheumatoid arthritis associated transcriptional changes on osteoclast differentiation network in the synovium. PeerJ 2018; 6e5743.
[http://dx.doi.org/10.7717/peerj.5743] [PMID: 30324023]
[107]
Li X, He L, Hu Y, et al. Sinomenine suppresses osteoclast formation and Mycobacterium tuberculosis H37Ra-induced bone loss by modulating RANKL signaling pathways. PLoS One 2013; 8(9)e74274
[http://dx.doi.org/10.1371/journal.pone.0074274] [PMID: 24066131]
[108]
Kong X, Wu W, Yang Y, et al. Total saponin from Anemone flaccida Fr. Schmidt abrogates osteoclast differentiation and bone resorption via the inhibition of RANKL-induced NF-κB, JNK and p38 MAPKs activation. J Transl Med 2015; 13: 91.
[http://dx.doi.org/10.1186/s12967-015-0440-1] [PMID: 25889035]
[109]
Choi YS, Kang EH, Lee EY, et al. Joint-protective effects of compound K, a major ginsenoside metabolite, in rheumatoid arthritis: in vitro evidence. Rheumatol Int 2013; 33(8): 1981-90.
[http://dx.doi.org/10.1007/s00296-013-2664-9] [PMID: 23370854]
[110]
Sakai E, Aoki Y, Yoshimatsu M, et al. Sanguiin H-6, a constituent of Rubus parvifolius L., inhibits receptor activator of nuclear factor-κB ligand-induced osteoclastogenesis and bone resorption in vitro and prevents tumor necrosis factor-α-induced osteoclast formation in vivo. Phytomedicine 2016; 23(8): 828-37.
[http://dx.doi.org/10.1016/j.phymed.2016.04.002] [PMID: 27288918]

Rights & Permissions Print Cite
Article Metrics
40
3
© 2024 Bentham Science Publishers | Privacy Policy