A study on the prevention and treatment of murine calvarial inflammatory osteolysis induced by ultra‑high‑molecular‑weight polyethylene particles with neomangiferin

Wang,Hong‑Tao; Li,Jia; Ma,Shi‑Ting; Feng,Wen‑Yu; Wang,Qi; Zhou,Hong‑Yan; Zhao,Jin‑Min; Yao,Jun

doi:10.3892/etm.2018.6725

A study on the prevention and treatment of murine calvarial inflammatory osteolysis induced by ultra‑high‑molecular‑weight polyethylene particles with neomangiferin

Authors:
- Hong‑Tao Wang
- Jia Li
- Shi‑Ting Ma
- Wen‑Yu Feng
- Qi Wang
- Hong‑Yan Zhou
- Jin‑Min Zhao
- Jun Yao
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Affiliations: Research Centre for Regenerative Medicine and Guangxi Key Laboratory of Regenerative Medicine, Guangxi Medical University, Nanning, Guangxi 530021, P.R. China, Orthopedic Department, The First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi 530021, P.R. China
Published online on: September 11, 2018 https://doi.org/10.3892/etm.2018.6725
Pages: 3889-3896
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The present study aimed to examine the influence of neomangiferin on murine calvarial inflammatory osteolysis induced by ultra‑high‑molecular‑weight polyethylene (UHMWPE) particles. Eight‑week‑old male C57BL/J6 mice served as an inflammatory osteolysis model, in which UHMWPE particles were implanted into the calvarial subperiosteal space. The mice were randomly distributed into four groups and treated with different interventions; namely, a sham group [phosphate‑buffered saline (PBS) injection and no UHMWPE particles], model group (PBS injection and implantation of UHMWPE particles), low‑dose neomangiferin group (UHMWPE particles +2.5 mg/kg neomangiferin), and high‑dose neomangiferin group (UHMWPE particles +5 mg/kg neomangiferin). Following 3 weeks of feeding according to the above regimens, celiac artery blood samples were collected for an enzyme‑linked immunosorbent assay (ELISA) to determine the expression of receptor activator of nuclear factor‑κB ligand (RANKL), osteoclast‑related receptor (OSCAR), cross‑linked C‑telopeptide of type I collagen (CTX‑1); osteoprotegerin (OPG), tumor necrosis factor (TNF)‑α, and interleukin (IL)‑1β. Subsequently, the mice were sacrificed by cervical dislocation following ether‑inhalation anesthesia, and the skull was separated for osteolysis analysis by micro‑computed tomography (micro‑CT). Following hematoxylin and eosin staining, tartrate‑resistant acid phosphatase (TRAP) staining was performed to observe the dissolution and destruction of the skull. The micro‑CT results suggested that neomangiferin significantly inhibited the murine calvarial osteolysis and bone resorption induced by UHMWPE particles. In addition, the ELISA results showed that neomangiferin decreased the expression levels of osteoclast markers RANKL, OSCAR, CTX‑1, TNF‑α and IL‑1β. By contrast, the levels of OPG increased with the neomangiferin dose. Histopathological examination revealed that the TRAP‑positive cell count was significantly reduced in the neomangiferin‑treated animals compared with that in the positive control group, and the degree of bone resorption was also markedly reduced. Neomangiferin was found to have significant anti‑inflammatory effects and to inhibit osteoclastogenesis. Therefore, it has the potential to prevent the aseptic loosening of a prosthesis following artificial joint replacement.

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1	Sabokbar A, Kudo O and Athanasou NA: Two distinct cellular mechanisms of osteoclast formation and bone resorption in periprosthetic osteolysis. J Orthop Res. 21:73–80. 2003. View Article : Google Scholar : PubMed/NCBI
2	Shin DK, Kim MH, Lee SH, Kim TH and Kim SY: Inhibitory effects of luteolin on titanium particle-induced osteolysis in a mouse model. Acta Biomater. 8:3524–3531. 2012. View Article : Google Scholar : PubMed/NCBI
3	Goodman SB, Gibon E, Pajarinen J, Lin TH, Keeney M, Ren PG, Nich C, Yao Z, Egashira K, Yang F and Konttinen YT: Novel biological strategies for treatment of wear particle-induced periprosthetic osteolysis of orthopaedic implants for joint replacement. J R Soc Interface. 11:201309622014. View Article : Google Scholar : PubMed/NCBI
4	Goodman SB, Gibon E and Yao Z: The basic science of periprosthetic osteolysis. Instr Course Lect. 62:201–206. 2013.PubMed/NCBI
5	Warme BA, Epstein NJ, Trindade MC, Miyanishi K, Ma T, Saket RR, Regula D, Goodman SB and Smith RL: Proinflammatory mediator expression in a novel murine model of titanium-particle-induced intramedullary inflammation. J Biomed Mater Res B Appl Biomater. 71:360–366. 2004. View Article : Google Scholar : PubMed/NCBI
6	Yang SY, Wu B, Mayton L, Mukherjee P, Robbins PD, Evans CH and Wooley PH: Protective effects of IL-1Ra or vIL-10 gene transfer on a murine model of wear debris-induced osteolysis. Gene Ther. 11:483–491. 2004. View Article : Google Scholar : PubMed/NCBI
7	Pacifici R: Role of T cells in ovariectomy induced bone loss-revisited. J Bone Miner Res. 27:231–239. 2012. View Article : Google Scholar : PubMed/NCBI
8	Jonitz-Heincke A, Lochner K, Schulze C, Pohle D, Pustlauk W, Hansmann D and Bader R: Contribution of human osteoblasts and macrophages to bone matrix degradation and proinflammatory cytokine release after exposure to abrasive endoprosthetic wear particles. Mol Med Rep. 14:1491–1500. 2016. View Article : Google Scholar : PubMed/NCBI
9	Yagil-Kelmer E, Kazmier P, Rahaman MN, Bal BS, Tessman RK and Estes DM: Comparison of the response of primary human blood monocytes and the U937 human monocytic cell line to two different sizes of alumina ceramic particles. J Orthop Res. 22:832–838. 2004. View Article : Google Scholar : PubMed/NCBI
10	Petit A, Mwale F, Antoniou J, Zukor DJ and Huk OL: Effect of bisphosphonates on the stimulation of macrophages by alumina ceramic particles: A comparison with ultra-high-molecular-weight polyethylene. J Mater Sci Mater Med. 17:667–673. 2006. View Article : Google Scholar : PubMed/NCBI
11	Lim SM, Kang GD, Jeong JJ, Choi HS and Kim DH: Neomangiferin modulates the Th17/Treg balance and ameliorates colitis in mice. Phytomedicine. 23:131–140. 2016. View Article : Google Scholar : PubMed/NCBI
12	Li J, Chen L, Wu H, Lu Y, Hu Z, Lu B, Zhang L, Chai Y and Zhang J: The mixture of salvianolic acids from salvia miltiorrhiza and total flavonoids from anemarrhena asphodeloides attenuate sulfur mustard-induced injury. Int J Mol Sci. 16:24555–24573. 2015. View Article : Google Scholar : PubMed/NCBI
13	Seo CS, Ha H, Kim YJ and Jungb JY: HPLC-pDA simultaneous determination and protective effect of Anemarrhena asphodeloides against acute renal failure. Nat Prod Commun. 9:829–832. 2014.PubMed/NCBI
14	Zhou C, Zhou J, Han N, Liu Z, Xiao B and Yin J: Beneficial effects of neomangiferin on high fat diet-induced nonalcoholic fatty liver disease in rats. Int Immunopharmacol. 25:218–228. 2015. View Article : Google Scholar : PubMed/NCBI
15	Zhu X, Gao JJ, Landao-Bassonga E, Pavlos NJ, Qin A, Steer JH, Zheng MH, Dong Y and Cheng TS: Thonzonium bromide inhibits RANKL-induced osteoclast formation and bone resorption in vitro and prevents LPS-induced bone loss in vivo. Biochem Pharmacol. 104:118–130. 2016. View Article : Google Scholar : PubMed/NCBI
16	Zhu X, Gao J, Ng PY, Qin A, Steer JH, Pavlos NJ, Zheng MH, Dong Y and Cheng TS: Alexidine dihydrochloride attenuates osteoclast formation and bone resorption and protects against LPS-induced osteolysis. J Bone Miner Res. 31:560–572. 2016. View Article : Google Scholar : PubMed/NCBI
17	Chen H, Guo T, Wang D and Qin R: Vaccaria hypaphorine impairs RANKL-induced osteoclastogenesis by inhibition of ERK, p38, JNK and NF-κB pathway and prevents inflammatory bone loss in mice. Biomed Pharmacother. 97:1155–1163. 2018. View Article : Google Scholar : PubMed/NCBI
18	Song F, Wei C, Zhou L, Qin A, Yang M, Tickner J, Huang Y, Zhao J and Xu J: Luteoloside prevents lipopolysaccharide-induced osteolysis and suppresses RANKL-induced osteoclastogenesis through attenuating RANKL signaling cascades. J Cell Physiol. 233:1723–1735. 2018. View Article : Google Scholar : PubMed/NCBI
19	Al-Quhali AM, Sun Y, Bai X, Jin Z and Yu G: Surgical modification of the murine calvaria osteolysis model. Biomed Res Int. 2015:8026972015. View Article : Google Scholar : PubMed/NCBI
20	Wedemeyer C, Xu J, Neuerburg C, Landgraeber S, Malyar NM, von Knoch F, Gosheger G, von Knoch M, Löer F and Saxler G: Particle-induced osteolysis in three-dimensional micro-computed tomography. Calcif Tissue Int. 81:394–402. 2007. View Article : Google Scholar : PubMed/NCBI
21	Sun Q, Fu Y, Sun A, Shou Y, Zheng M, Li X and Fan D: Correlation of E-selectin gene polymorphisms with risk of ischemic stroke A meta-analysis. Neural Regenerat Res. 6:1731–1735. 2011.
22	Chiu R, Ma T, Smith RL and Goodman SB: Ultrahigh molecular weight polyethylene wear debris inhibits osteoprogenitor proliferation and differentiation in vitro. J Biomed Mater Res A. 89:242–247. 2009.PubMed/NCBI
23	Chiu R, Ma T, Smith RL and Goodman SB: Polymethylmethacry late particles inhibit osteoblastic differentiation of bone marrow osteoprogenitor cells. J Biomed Mater Res A. 77:850–856. 2006. View Article : Google Scholar : PubMed/NCBI
24	Kadoya Y, Revell PA, al-Saffar N, Kobayashi A, Scott G and Freeman MA: Bone formation and bone resorption in failed total joint arthroplasties: Histomorphometric analysis with histochemical and immunohistochemical technique. J Orthop Res. 14:473–482. 1996. View Article : Google Scholar : PubMed/NCBI
25	Schmalzried TP, Kwong LM, Jasty M, Sedlacek RC, Haire TC, O'Connor DO, Bragdon CR, Kabo JM, Malcolm AJ and Harris WH: The mechanism of loosening of cemented acetabular components in total hip arthroplasty. Analysis of specimens retrieved at autopsy. Clin Orthop Relat Res. 274:60–78. 1992.
26	Kotian P, Boloor A and Sreenivasan S: Study of adverse effect profile of parenteral zoledronic acid in female patients with osteoporosis. J Clin Diagn Res. 10:OC04–OC06. 2016.PubMed/NCBI
27	Beaudoin C, Jean S, Bessette L, Ste-Marie LG, Moore L and Brown JP: Denosumab compared to other treatments to prevent or treat osteoporosis in individuals at risk of fracture: A systematic review and meta-analysis. Osteoporos Int. 27:2835–2844. 2016. View Article : Google Scholar : PubMed/NCBI
28	Tsubaki M, Komai M, Itoh T, Imano M, Sakamoto K, Shimaoka H, Takeda T, Ogawa N, Mashimo K, Fujiwara D, et al: Nitrogen-containing bisphosphonates inhibit RANKL- and M-CSF-induced osteoclast formation through the inhibition of ERK1/2 and Akt activation. J Biomed Sci. 21:102014. View Article : Google Scholar : PubMed/NCBI
29	He LG, Li XL, Zeng XZ, Duan H, Wang S, Lei LS, Li XJ and Liu SW: Sinomenine induces apoptosis in RAW 264.7 cell-derived osteoclasts in vitro via caspase-3 activation. Acta Pharmacol Sin. 35:203–210. 2014. View Article : Google Scholar : PubMed/NCBI
30	Zheng M, Ge Y, Li H, Yan M, Zhou J and Zhang Y: Bergapten prevents lipopolysaccharide mediated osteoclast formation, bone resorption and osteoclast survival. Int Orthop. 38:627–634. 2014. View Article : Google Scholar : PubMed/NCBI
31	Newman DJ and Cragg GM: Natural products as sources of new drugs from 1981 to 2014. J Nat Prod. 79:629–661. 2016. View Article : Google Scholar : PubMed/NCBI
32	Wang J, Fu B, Lu F, Hu X, Tang J and Huang L: Inhibitory activity of linarin on osteoclastogenesis through receptor activator of nuclear factor κB ligand-induced NF-κB pathway. Biochem Biophys Res Commun. 495:2133–2138. 2018. View Article : Google Scholar : PubMed/NCBI
33	Liu G, Ma C, Wang P, Zhang P, Qu X, Liu S, Zhai Z, Yu D, Gao J, Liang J, et al: Pilose antler peptide potentiates osteoblast differentiation and inhibits osteoclastogenesis via manipulating the NF-κB pathway. Biochem Biophys Res Commun. 491:388–395. 2017. View Article : Google Scholar : PubMed/NCBI
34	Nie S, Xu J, Zhang C, Xu C, Liu M and Yu D: Salicortin inhibits osteoclast differentiation and bone resorption by down-regulating JNK and NF-κB/NFATc1 signaling pathways. Biochem Biophys Res Commun. 470:61–67. 2016. View Article : Google Scholar : PubMed/NCBI
35	Henc I, Kokotkiewicz A, Łuczkiewicz P, Bryl E, Łuczkiewicz M and Witkowski JM: Naturally occurring xanthone and benzophenone derivatives exert significant anti-proliferative and proapoptotic effects in vitro on synovial fibroblasts and macrophages from rheumatoid arthritis patients. Int Immunopharmacol. 49:148–154. 2017. View Article : Google Scholar : PubMed/NCBI
36	Liao HL, Wu QY, HU HG, Zang ZH, Song L and Yang Q: Structure modification of mangiferin. West China J Pharma Sci. 23:385–387. 2008.
37	Hong YF, Han GY and Guo XM: Isolation and structure determination of xanthone glycosides of Anemarrhena asphodeloides. Yao Xue Xue Bao. 32:473–475. 1997.(In Chinese). PubMed/NCBI
38	Broadhead ML, Clark JC, Dass CR, Choong PF and Myers DE: Therapeutic targeting of osteoclast function and pathways. Expert Opin Ther Targets. 15:169–181. 2011. View Article : Google Scholar : PubMed/NCBI
39	Landgraeber S, Quint U, Classen T and Totsch M: Senescence in cells in aseptic loosening after total hip replacement. Acta Biomater. 7:1364–1368. 2011. View Article : Google Scholar : PubMed/NCBI
40	Boyle WJ, Simonet WS and Lacey DL: Osteoclast differentiation and activation. Nature. 423:337–342. 2003. View Article : Google Scholar : PubMed/NCBI
41	Zhai Z, Qu X, Li H, Yang K, Wan P, Tan L, Ouyang Z, Liu X, Tian B, Xiao F, et al: The effect of metallic magnesium degradation products on osteoclast-induced osteolysis and attenuation of NF-κB and NFATc1 signaling. Biomaterials. 35:6299–6310. 2014. View Article : Google Scholar : PubMed/NCBI
42	Cadosch D, Gautschi OP, Chan E, Simmen HP and Filgueira L: Titanium induced production of chemokines CCL17/TARC and CCL22/MDC in human osteoclasts and osteoblasts. J Biomed Mater Res A. 92:475–483. 2010.PubMed/NCBI
43	Jämsen E, Kouri VP, Olkkonen J, Cör A, Goodman SB, Konttinen YT and Pajarinen J: Characterization of macrophage polarizing cytokines in the aseptic loosening of total hip replacements. J Orthop Res. 32:1241–1246. 2014. View Article : Google Scholar : PubMed/NCBI
44	Jablonski H, Rekasi H and Jäger M: The influence of calcitonin gene-related peptide on markers of bone metabolism in MG-63 osteoblast-like cells co-cultured with THP-1 macrophage-like cells under virtually osteolytic conditions. BMC Musculoskelet Disord. 17:1992016. View Article : Google Scholar : PubMed/NCBI
45	Park SJ, Lee EJ, Kim YH, Shin JE and Kang YH: Inhibitory effects of gossypin on RANKL-induced osteoclast differentiation and bone resorption in murine macrophages (LB364). FASEB J 28. 2014.
46	Nich C, Takakubo Y, Pajarinen J, Ainola M, Salem A, Sillat T, Rao AJ, Raska M, Tamaki Y, Takagi M, et al: Macrophages-Key cells in the response to wear debris from joint replacements. J Biomed Mater Res A. 101:3033–3045. 2013. View Article : Google Scholar : PubMed/NCBI
47	Ingham E and Fisher J: The role of macrophages in osteolysis of total joint replacement. Biomaterials. 26:1271–1286. 2005. View Article : Google Scholar : PubMed/NCBI
48	Lin TH, Yao Z, Sato T, Keeney M, Li C, Pajarinen J, Yang F, Egashira K and Goodman SB: Suppression of wear-particle-induced pro-inflammatory cytokine and chemokine production in macrophages via NF-κB decoy oligodeoxynucleotide: A preliminary report. Acta Biomater. 10:3747–3755. 2014. View Article : Google Scholar : PubMed/NCBI
49	Liu X, Zhu S, Cui J, Shao H, Zhang W, Yang H, Xu Y, Geng D and Yu L: Strontium ranelate inhibits titanium-particle-induced osteolysis by restraining inflammatory osteoclastogenesis in vivo. Acta Biomater. 10:4912–4918. 2014. View Article : Google Scholar : PubMed/NCBI