1.Department of Orthopaedics, Suzhou Dushu Lake Hospital, Dushu Lake Hospital Affiliated to Soochow University, Medical Centre of Soochow University, Suzhou 215001, Jiangsu, China
2.Department of Orthopaedics, the First Affiliated Hospital of Soochow University, Soochow University, Suzhou 215006, Jiangsu, China
3.Department of Infectious Diseases, the Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310058, China
* linjun@suda.edu.cn
纸质出版:2023-04
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Propionate and butyrate attenuate macrophage pyroptosis and osteoclastogenesis induced by CoCrMo alloy particles[J]. Military Medical Research, 2023,10(2):191-206.
Cite this article as: Wu YL, Zhang CH, Teng Y, Pan Y, Liu NC, Liu PX, et al. Propionate and butyrate attenuate macrophage pyroptosis and osteoclastogenesis induced by CoCrMo alloy particles. Mil Med Res. 2022;9(1):46.
Propionate and butyrate attenuate macrophage pyroptosis and osteoclastogenesis induced by CoCrMo alloy particles[J]. Military Medical Research, 2023,10(2):191-206. DOI: 10.1186/s40779-022-00404-0.
Cite this article as: Wu YL, Zhang CH, Teng Y, Pan Y, Liu NC, Liu PX, et al. Propionate and butyrate attenuate macrophage pyroptosis and osteoclastogenesis induced by CoCrMo alloy particles. Mil Med Res. 2022;9(1):46. DOI: 10.1186/s40779-022-00404-0.
Background:
2
Wear particles-induced osteolysis is a major long-term complication after total joint arthroplasty. Up to now
there is no effective treatment for wear particles-induced osteolysis except for the revision surgery
which is a heavy psychological and economic burden to patients. A metabolite of gut microbiota
short chain fatty acids (SCFAs)
has been reported to be beneficial for many chronic inflammatory diseases. This study aimed to investigate the therapeutic effect of SCFAs on osteolysis.
Methods:
2
A model of inflammatory osteolysis was established by applying CoCrMo alloy particles to mouse calvarium. After two weeks of intervention
the anti-inflammatory effects of SCFAs on wear particle-induced osteolysis were evaluated by micro-CT analysis and immunohistochemistry staining.
In vitro
study
lipopolysaccharide (LPS) primed bone marrow-derived macrophages (BMDMs) and Tohoku hospital pediatrics-1 (THP-1) macrophages were stimulated with CoCrMo particles to activate inflammasome in the presence of acetate (C2)
propionate (C3)
and butyrate (C4). Western blotting
enzyme-linked immunosorbent assay
and immunofluorescence were used to detect the activation of NLRP3 inflammasome. The effects of SCFAs on osteoclasts were evaluate by qRT-PCR
Western blotting
immunofluorescence
and tartrate-resistant acid phosphatase (TRAP) staining. Additionally
histone deacetylase (HDAC) inhibitors
agonists of GPR41
GPR43
and GPR109A were applied to confirm the underlying mechanism of SCFAs on the inflammasome activation of macrophages and osteoclastogenesis.
Results:
2
C3 and C4 but not C2 could alleviate wear particles-induced osteolysis with fewer bone erosion pits (
P
<
0.001)
higher level of bone volume to tissue volume (BV/TV
P
<
0.001)
bone mineral density (BMD
P
<
0.001)
and a lower total porosity (
P
<
0.001). C3 and C4 prevented CoCrMo alloy particles-induced ASC speck formation and nucleation-induced oligomerization
suppressing the cleavage of caspase-1 (
P
<
0.05) and IL-1β (
P
<
0.05) stimulated by CoCrMo alloy particles. C3 and C4 also inhibited the generation of gasdermin D-N-terminal fragment (GSDMD-NT) to regulate pyroptosis. Besides
C3 and C4 have a negative impact on osteoclast differentiation (
P
<
0.05) and its function (
P
<
0.05)
affecting the podosome arrangement and morphologically normal podosome belts formation.
Conclusions:
2
Our work showed that C3 and C4 are qualified candidates for the treatment of wear particle-induced osteolysis.
Willinger ML , Heimroth J , Sodhi N , Garbarino LJ , Gold PA , Rasquinha V , et al . Management of refractory pain after total joint replacement . Curr Pain Headache Rep. 2021 ; 25 ( 6 ): 42 .
Rivera MC , Perni S , Sloan A , Prokopovich P . Anti-inflammatory drug-eluting implant model system to prevent wear particle-induced periprosthetic osteolysis . Int J Nanomedicine. 2019 ; 14 : 1069 – 84 .
Ding C , Yang C , Cheng T , Wang X , Wang Q , He R , et al . Macrophage-biomimetic porous Se@SiO2 nanocomposites for dual modal immunotherapy against inflammatory osteolysis . J Nanobiotechnol. 2021 ; 19 ( 1 ): 382 .
Levescot A , Chang MH , Schnell J , Nelson-Maney N , Yan J , Martinez-Bonet M , et al . IL-1beta-driven osteoclastogenic Tregs accelerate bone erosion in arthritis . J Clin Invest. 2021 ; 131 ( 18 ):: e141008 .
Yokota K , Sato K , Miyazaki T , Aizaki Y , Tanaka S , Sekikawa M , et al . Characterization and function of tumor necrosis factor and interleukin-6-induced osteoclasts in rheumatoid arthritis . Arthritis Rheumatol. 2021 ; 73 ( 7 ): 1145 – 54 .
Carnovali M , Valli R , Banfi G , Porta G , Mariotti M . Soybean meal-dependent intestinal inflammation induces different patterns of bone-loss in adult zebrafish scale . Biomedicines. 2021 ; 9 ( 4 ): 393 .
Sharma BR , Kanneganti TD . NLRP3 inflammasome in cancer and metabolic diseases . Nat Immunol. 2021 ; 22 ( 5 ): 550 – 9 .
Hooftman A , Angiari S , Hester S , Corcoran SE , Runtsch MC , Ling C , et al . The immunomodulatory metabolite itaconate modifies NLRP3 and inhibits inflammasome activation . Cell Metab. 2020 ; 32 ( 3 ): 468 – 787 .
Wang L , Hauenstein AV . The NLRP3 inflammasome: mechanism of action, role in disease and therapies . Mol Aspects Med. 2020 ; 76 : 100889 .
He WT , Wan H , Hu L , Chen P , Wang X , Huang Z , et al . Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion . Cell Res. 2015 ; 25 ( 12 ): 1285 – 98 .
Conos SA , Chen KW , De Nardo D , Hara H , Whitehead L , Nunez G , et al . Active MLKL triggers the NLRP3 inflammasome in a cell-intrinsic manner . Proc Natl Acad Sci U S A. 2017 ; 114 ( 6 ): E961 – 9 .
Zhu S , Ding S , Wang P , Wei Z , Pan W , Palm NW , et al . Nlrp9b inflammasome restricts rotavirus infection in intestinal epithelial cells . Nature. 2017 ; 546 ( 7660 ): 667 – 70 .
Burdette BE , Esparza AN , Zhu H , Wang S . Gasdermin D in pyroptosis . Acta Pharm Sin B. 2021 ; 11 ( 9 ): 2768 – 82 .
Dick MS , Sborgi L , Ruhl S , Hiller S , Broz P . ASC filament formation serves as a signal amplification mechanism for inflammasomes . Nat Commun. 2016 ; 7 : 11929 .
Goh G , Ahn M , Zhu F , Lee LB , Luo D , Irving AT , et al . Complementary regulation of caspase-1 and IL-1beta reveals additional mechanisms of dampened inflammation in bats . Proc Natl Acad Sci U S A. 2020 ; 117 ( 46 ): 28939 – 49 .
Dostert C , Petrilli V , Van Bruggen R , Steele C , Mossman BT , Tschopp J . Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica . Science. 2008 ; 320 ( 5876 ): 674 – 7 .
Hornung V , Bauernfeind F , Halle A , Samstad EO , Kono H , Rock KL , et al . Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization . Nat Immunol. 2008 ; 9 ( 8 ): 847 – 56 .
Martinon F , Petrilli V , Mayor A , Tardivel A , Tschopp J . Gout-associated uric acid crystals activate the NALP3 inflammasome . Nature. 2006 ; 440 ( 7081 ): 237 – 41 .
Yan Y , Jiang W , Liu L , Wang X , Ding C , Tian Z , et al . Dopamine controls systemic inflammation through inhibition of NLRP3 inflammasome . Cell. 2015 ; 160 ( 1–2 ): 62 – 73 .
Jamsen E , Pajarinen J , Kouri VP , Rahikkala A , Goodman SB , Manninen M , et al . Tumor necrosis factor primes and metal particles activate the NLRP3 inflammasome in human primary macrophages . Acta Biomater. 2020 ; 108 : 347 – 57 .
Mridha AR , Wree A , Robertson AAB , Yeh MM , Johnson CD , Van Rooyen DM , et al . NLRP3 inflammasome blockade reduces liver inflammation and fibrosis in experimental NASH in mice . J Hepatol. 2017 ; 66 ( 5 ): 1037 – 46 .
Duewell P , Kono H , Rayner KJ , Sirois CM , Vladimer G , Bauernfeind FG , et al . NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals . Nature. 2010 ; 464 ( 7293 ): 1357 – 61 .
Grebe A , Hoss F , Latz E . NLRP3 inflammasome and the IL-1 pathway in atherosclerosis . Circ Res. 2018 ; 122 ( 12 ): 1722 – 40 .
Wu Y , Teng Y , Zhang C , Pan Y , Zhang Q , Zhu X , et al . The ketone body betahydroxybutyrate alleviates CoCrMo alloy particles induced osteolysis by regulating NLRP3 inflammasome and osteoclast differentiation . J Nanobiotechnol. 2022 ; 20 ( 1 ): 120 .
Lin TH , Tamaki Y , Pajarinen J , Waters HA , Woo DK , Yao Z , et al . Chronic inflammation in biomaterial-induced periprosthetic osteolysis: NFkappaB as a therapeutic target . Acta Biomater. 2014 ; 10 ( 1 ): 1 – 10 .
Gallo J , Vaculova J , Goodman SB , Konttinen YT , Thyssen JP . Contributions of human tissue analysis to understanding the mechanisms of loosening and osteolysis in total hip replacement . Acta Biomater. 2014 ; 10 ( 6 ): 2354 – 66 .
Mbalaviele G , Novack DV , Schett G , Teitelbaum SL . Inflammatory osteolysis: a conspiracy against bone . J Clin Invest. 2017 ; 127 ( 6 ): 2030 – 9 .
Wu Y , He F , Zhang C , Zhang Q , Su X , Zhu X , et al . Melatonin alleviates titanium nanoparticles induced osteolysis via activation of butyrate/GPR109A signaling pathway . J Nanobiotechnol. 2021 ; 19 ( 1 ): 170 .
Miller TL , Wolin MJ . Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora . Appl Environ Microbiol. 1996 ; 62 ( 5 ): 1589 – 92 .
Koh A , De Vadder F , Kovatcheva-Datchary P , Backhed F . From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites . Cell. 2016 ; 165 ( 6 ): 1332 – 45 .
Xu Y , Zhu Y , Li X , Sun B . Dynamic balancing of intestinal short-chain fatty acids: the crucial role of bacterial metabolism . Trends Food Sci Technol. 2020 ; 100 : 118 – 30 .
Tyagi AM , Yu M , Darby TM , Vaccaro C , Li JY , Owens JA , et al . The microbial metabolite butyrate stimulates bone formation via T regulatory cellmediated regulation of WNT10B expression . Immunity. 2018 ; 49 ( 6 ): 1116-31.e7 .
Rahman MM , Kukita A , Kukita T , Shobuike T , Nakamura T , Kohashi O . Two histone deacetylase inhibitors, trichostatin A and sodium butyrate, suppress differentiation into osteoclasts but not into macrophages . Blood. 2003 ; 101 ( 9 ): 3451 – 9 .
Yan J , Takakura A , Zandi-Nejad K , Charles JF . Mechanisms of gut microbiota-mediated bone remodeling . Gut Microbes. 2018 ; 9 ( 1 ): 84 – 92 .
Montalvany-Antonucci CC , Duffles LF , de Arruda JAA , Zicker MC , de Oliveira S , Macari S , et al . Short-chain fatty acids and FFAR2 as suppressors of bone resorption . Bone. 2019 ; 125 : 112 – 21 .
Lucas S , Omata Y , Hofmann J , Bottcher M , Iljazovic A , Sarter K , et al . Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss . Nat Commun. 2018 ; 9 ( 1 ): 55 .
Yuan X , Wang L , Bhat OM , Lohner H , Li PL . Differential effects of short chain fatty acids on endothelial Nlrp3 inflammasome activation and neointima formation: antioxidant action of butyrate . Redox Biol. 2018 ; 16 : 21 – 31 .
Zhang Y , Zhu X , Wang G , Chen L , Yang H , He F , et al . Melatonin rescues the Ti particle-impaired osteogenic potential of bone marrow mesenchymal stem cells via the SIRT1/SOD2 signaling pathway . Calcif Tissue Int. 2020 ; 107 ( 5 ): 474 – 88 .
Zhu X , Zhang Y , Yang H , He F , Lin J . Melatonin suppresses Ti-particleinduced inflammatory osteolysis via activation of the Nrf2/Catalase signaling pathway . Int Immunopharmacol. 2020 ; 88 : 106847 .
Pan H , Lin Y , Dou J , Fu Z , Yao Y , Ye S , et al . Wedelolactone facilitates Ser/Thr phosphorylation of NLRP3 dependent on PKA signalling to block inflammasome activation and pyroptosis . Cell Prolif. 2020 ; 53 ( 9 ): e12868 .
Hosseinkhani F , Heinken A , Thiele I , Lindenburg PW , Harms AC , Hankemeier T . The contribution of gut bacterial metabolites in the human immune signaling pathway of non-communicable diseases . Gut Microbes. 2021 ; 13 ( 1 ): 1 – 22 .
Kasubuchi M , Hasegawa S , Hiramatsu T , Ichimura A , Kimura I . Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation . Nutrients. 2015 ; 7 ( 4 ): 2839 – 49 .
Son HS , Lee J , Lee HI , Kim N , Jo YJ , Lee GR , et al . Benzydamine inhibits osteoclast differentiation and bone resorption via down-regulation of interleukin-1 beta expression . Acta Pharm Sin B. 2020 ; 10 ( 3 ): 462 – 74 .
Goodman SB , Gallo J . Periprosthetic osteolysis: mechanisms, prevention and treatment . J Clin Med. 2019 ; 8 ( 12 ): 2091 .
Eger M , Hiram-Bab S , Liron T , Sterer N , Carmi Y , Kohavi D , et al . Mechanism and prevention of titanium particle-induced inflammation and osteolysis . Front Immunol. 2018 ; 9 : 2963 .
Wang Z , Xue K , Bai M , Deng Z , Gan J , Zhou G , et al . Probiotics protect mice from CoCrMo particles-induced osteolysis . Int J Nanomed. 2017 ; 12 : 5387 – 97 .
Jonitz-Heincke A , Tillmann J , Ostermann M , Springer A , Bader R , Hol PJ , et al . Label-free monitoring of uptake and toxicity of endoprosthetic wear particles in human cell cultures . Int J Mol Sci. 2018 ; 19 ( 11 ): 3486 .
Zaveri TD , Dolgova NV , Lewis JS , Hamaker K , Clare-Salzler MJ , Keselowsky BG . Macrophage integrins modulate response to ultra-high molecular weight polyethylene particles and direct particle-induced osteolysis . Biomaterials. 2017 ; 115 : 128 – 40 .
Ormsby RT , Solomon LB , Yang D , Crotti TN , Haynes DR , Findlay DM , et al . Osteocytes respond to particles of clinically-relevant conventional and cross-linked polyethylene and metal alloys by up-regulation of resorptive and inflammatory pathways . Acta Biomater. 2019 ; 87 : 296 – 306 .
Burton L , Paget D , Binder NB , Bohnert K , Nestor BJ , Sculco TP , et al . Orthopedic wear debris mediated inflammatory osteolysis is mediated in part by NALP3 inflammasome activation . J Orthop Res. 2013 ; 31 ( 1 ): 73 – 80 .
Pan X , Fang X , Wang F , Li H , Niu W , Liang W , et al . Butyrate ameliorates caerulein-induced acute pancreatitis and associated intestinal injury by tissue-specific mechanisms . Br J Pharmacol. 2019 ; 176 ( 23 ): 4446 – 61 .
Cleophas MC , Crisan TO , Lemmers H , Toenhake-Dijkstra H , Fossati G , Jansen TL , et al . Suppression of monosodium urate crystal-induced cytokine production by butyrate is mediated by the inhibition of class I histone deacetylases . Ann Rheum Dis. 2016 ; 75 ( 3 ): 593 – 600 .
Xu M , Jiang Z , Wang C , Li N , Bo L , Zha Y , et al . Acetate attenuates inflammasome activation through GPR43-mediated Ca(2+)-dependent NLRP3 ubiquitination . Exp Mol Med. 2019 ; 51 ( 7 ): 1 – 13 .
Youm YH , Nguyen KY , Grant RW , Goldberg EL , Bodogai M , Kim D , et al . The ketone metabolite beta-hydroxybutyrate blocks NLRP3 inflammasomemediated inflammatory disease . Nat Med. 2015 ; 21 ( 3 ): 263 – 9 .
Shao H , Shen J , Wang M , Cui J , Wang Y , Zhu S , et al . Icariin protects against titanium particle-induced osteolysis and inflammatory response in a mouse calvarial model . Biomaterials. 2015 ; 60 : 92 – 9 .
Yang H , Xu Y , Zhu M , Gu Y , Zhang W , Shao H , et al . Inhibition of titaniumparticle-induced inflammatory osteolysis after local administration of dopamine and suppression of osteoclastogenesis via D2-like receptor signaling pathway . Biomaterials. 2016 ; 80 : 1 – 10 .
Mae M , Alam MI , Yamashita Y , Ozaki Y , Higuchi K , Ziauddin SM , et al . The role of cytokines produced via the NLRP3 inflammasome in mouse macrophages stimulated with dental calculus in osteoclastogenesis . Int J Mol Sci. 2021 ; 22 ( 22 ): 12434 .
Chen Y , Yang Q , Lv C , Chen Y , Zhao W , Li W , et al . NLRP3 regulates alveolar bone loss in ligature-induced periodontitis by promoting osteoclastic differentiation . Cell Prolif. 2021 ; 54 ( 2 ): e12973 .
Kimura I , Ichimura A , Ohue-Kitano R , Igarashi M . Free fatty acid receptors in health and disease . Physiol Rev. 2020 ; 100 ( 1 ): 171 – 210 .
Goodman SB , Gibon E , Pajarinen J , Lin TH , Keeney M , Ren PG , et al . Novel biological strategies for treatment of wear particle-induced periprosthetic osteolysis of orthopaedic implants for joint replacement . J R Soc Interface. 2014 ; 11 ( 93 ): 20130962 .
Kandahari AM , Yang X , Laroche KA , Dighe AS , Pan D , Cui Q . A review of UHMWPE wear-induced osteolysis: the role for early detection of the immune response . Bone Res. 2016 ; 4 : 16014 .
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