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RANKL-responsive epigenetic mechanism reprograms macrophages into bone-resorbing osteoclasts

Cellular & Molecular Immunology 2023年第1期20卷 94-109页

作者： Seyeon Bae Kibyeong Kim Keunsoo Kang Haemin Kim Minjoon Lee Brian Oh Kaichi Kaneko Sungkook Ma Jae Hoon Choi Hojoong Kwak Eun Young Lee Sung Ho Park Kyung-Hyun Park-Min Arthritis and Tissue Degeneration Program David Z.Rosensweig Genomics Research CenterHospital for Special SurgeryNew YorkNY10021USA Department of Medicine Weill Cornell Medical CollegeNew YorkNY10065USA Department of Biological Science Ulsan National Institute of Science&Technology(UNIST)Ulsan44919Republic of Korea Department of Life Science College of Natural SciencesResearch Institute for Natural SciencesHanyang UniversitySeoulKorea Department of Microbiology Dankook UniversityCheonan3116Republic of Korea Department of Molecular Biology and Genetics Cornell UniversityIthacaUSA Division of Rheumatology Department of Internal MedicineSeoul National University College of MedicineSeoulKorea BCMB Allied Program Weill Cornell Graduate School of Medical SciencesNew YorkNY10021USA

Monocyte/macrophage lineage cells are highly plastic and can differentiate into various cells under different environmental stimuli. Bone-resorbing osteoclasts are derived from the monocyte/macrophage lineage in response to receptor activator of NF-κB ligand (RANKL). However, the epigenetic signature contributing to the fate commitment of monocyte/macrophage lineage differentiation into human osteoclasts is largely unknown. In this study, we identified RANKL-responsive human osteoclast-specific superenhancers (SEs) and SE-associated enhancer RNAs (SE-eRNAs) by integrating data obtained from ChIP-seq, ATAC-seq, nuclear RNA-seq and PRO-seq analyses. RANKL induced the formation of 200 SEs, which are large clusters of enhancers, while suppressing 148 SEs in macrophages. RANKL-responsive SEs were strongly correlated with genes in the osteoclastogenic program and were selectively increased in human osteoclasts but marginally presented in osteoblasts, CD4+ T cells, and CD34+ cells. In addition to the major transcription factors identified in osteoclasts, we found that BATF binding motifs were highly enriched in RANKL-responsive SEs. The depletion of BATF1/3 inhibited RANKL-induced osteoclast differentiation. Furthermore, we found increased chromatin accessibility in SE regions, where RNA polymerase II was significantly recruited to induce the extragenic transcription of SE-eRNAs, in human osteoclasts. Knocking down SE-eRNAs in the vicinity of the NFATc1 gene diminished the expression of NFATc1, a major regulator of osteoclasts, and osteoclast differentiation. Inhibiting BET proteins suppressed the formation of some RANKL-responsive SEs and NFATc1-associated SEs, and the expression of SE-eRNA:NFATc1. Moreover, SE-eRNA:NFATc1 was highly expressed in the synovial macrophages of rheumatoid arthritis patients exhibiting high-osteoclastogenic potential. Our genome-wide analysis revealed RANKL-inducible SEs and SE-eRNAs as osteoclast-specific signatures, which may contribute to the development of osteoclast-specific therapeuti

关键词： osteoclasts super-enhancers enhancer RNAs Rheumatoid arthritis

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Multi-functional osteoclasts in matrix-based tissue engineering bone

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Chinese Journal of Traumatology 2022年第3期25卷 132-137页

作者： Yue-Qi Chen Wen-Hui Hu Zi-Cai Dong Shi-Wu Dong Department of Orthopedics Southwest HospitalThird Military Medical University(Army Medical University)Chongqing400038China Department of Biomedical Materials Science Third Military Medical University(Army Medical University)Chongqing400038China State Key Laboratory of Trauma Bums and Combined InjuryThird Military Medical University(Army Medical University)Chongqing400038China

The repair of bone defects,especially for the large segment of bone defects,has always been an urgent problem in orthopedic clinic and attracted researchers'attention.Nowadays,the application of tissue engineering bone in the repair of bone defects has become the research hotspot.With the rapid development of tissue engineering,the novel and functional scaffold materials for bone repair have emerged.In this review,we have summarized the multi-functional roles of osteoclasts in bone remodeling.The development of matrix-based tissue engineering bone has laid a theoretical foundation for further investigation about the novel bone regeneration materials which could perform high bioactivity.From the point of view on preserving pre-osteoclasts and targeting mature osteoclasts,this review introduced the novel matrix-based tissue engineering bone based on osteoclasts in the field of bone tissue engineering,which provides a potential direction for the development of novel scaffold materials for the treatment of bone defects.

关键词： osteoclasts Matrix based-tissue engineering bone Bone regeneration Micro-environment

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Humulus lupulus L. Extract Prevents Ovariectomy-Induced Osteoporosis in Mice and Regulates Activities of Osteoblasts and osteoclasts

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Chinese Journal of Integrative Medicine 2021年第1期27卷 31-38页

作者： XIA Tian-shuang LIN Liu-yue ZHANG Qiao-yan JIANG Yi-ping LI Chang-hui LIU Xiao-yan QIN Lu-ping XIN Hai-liang Department of Pharmacognosy School of PharmacySecond Military Medical UniversityShanghai(200433)China Schoolof Pharmacy Fujian University of Traditional Chinese MedicineFuzhou(350108)China School of Pharmacy Zhejiang Chinese Medical UniversityHangzhou(310053)China

Objective:To systematically evaluate the protective effects of Humulus lupulus L.extract(HLE)on osteoporosis mice.Methods:In vivo experiment,a total of 3512-week-old female ICR mice were equally divided into 5 groups:the sham control group(sham);the ovariectomy with vehicle group(OVX);the OVX with estradiol valerate[EV,0.2 mg/(kg·d)];the OVX with low-or high-dose HLE groups[HLE,1 g/(kg·d)and 3 g/(kg·d)],7 in each group.Treatment began 1 week after the ovariectomized surgery and lasted for 12 weeks.Bone mass and trabecular bone mircoarchitecture were evaluated by micro computed tomography,and bone turnover markers in serum were evaluated using enzyme-linked immunosorbent assay(ELISA)kits.In vitro experiment,osteoblasts and osteoclasts were treated with HLE at doses of 0,4,20 and 100μg/mL.Biomarkers for bone formation in osteoblasts and bone resorption in osteoclasts were analyzed.Results:Compared with the OVX group,HLE exerted bone protective effects by the increase of estradiol(P<0.05),the improvement of cancellous bone structure,bone mineral density(P<0.01)and the reduction of serum alkaline phosphatase(ALP),tartrate resistant acid phosphatase(TRAP),bone gla-protein,c-terminal telopeptides of typeⅠcollagen(CTX-Ⅰ)and deoxypyridinoline levels(P<0.01 for all).In vitro experiment,compared with the control group,HLE at 20μg/mL promoted the cell proliferation(P<0.01),and increased the expression of bone morphogenetic protein-2 and osteopontin levels in osteoblasts(both P<0.05).HLE at 100μg/mL increased the osteoblastic ALP activities,and HLE at all dose enhanced the extracellular matrix mineralization(both P<0.01).Furthermore,compared with the control group,HLE at 20μg/m L and 100μg/m L inhibited osteoclastic TRAP activity(P<0.01),and reduced the expression of matrix metalloproteinase-9 and cathepsin K(both P<0.05).Conclusion:HLE may protect against bone loss,and have potentials in the treatment of osteoporosis.

关键词： Humulus lupulus L. osteoporosis ovariectomy-induced mice osteoblasts osteoclasts

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Complement C3a activates osteoclasts by regulating the PI3K/PDK1/SGK3 pathway in patients with multiple myeloma

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Cancer Biology & Medicine 2021年第3期18卷 721-733页

作者： Fengjuan Jiang Hui Liu Fengping Peng Zhaoyun Liu Kai Ding Jia Song Lijuan Li Jin Chen Qing Shao Siyang Yan Kim De Veirman Karin Vanderkerken Rong Fu Department of Hematology Tianjin Medical University General HospitalTianjin 300052China Department of Hematology and Immunology-Myeloma Center Brussels Vrije Universiteit BrusselBrussels 1090Belgium

Objective:Myeloma bone disease(MBD)is the most common complication of multiple myeloma(MM).Our previous study showed that the serum levels of C3/C4 in MM patients were significantly positively correlated with the severity of bone disease.However,the mechanism of C3 a/C4 a in osteoclasts MM patients remains unclear.Methods:The formation and function of osteoclasts were analyzed after adding C3 a/C4 a in vitro.RNA-seq analysis was used to screen the potential pathways affecting osteoclasts,and the results were verified by Western blot,q RT-PCR,and pathway inhibitors.Results:The osteoclast area per view induced by 1μg/m L(mean±SD:50.828±12.984%)and 10μg/m L(53.663±12.685%)of C3 a was significantly increased compared to the control group(0μg/m L)(34.635±8.916%)(Posteoclasts using the phosphoinositide 3-kinase(PI3 K)signaling pathway.The relative expressions of PIK3 CA/phosphoinositide dependent kinase-1(PDK1)/serum and glucocorticoid inducible protein kinases(SGK3)genes and PI3 K/PDK1/p-SGK3 protein in the C3 a group were significantly higher than in the control group.The activation role of C3 a in osteoclasts of MM patients was reduced by the SGK inhibitor(EMD638683).Conclusions:C3 a activated osteoc

关键词： Multiple myeloma complement C3a osteoclasts PI3K/PDK1/SGK3 pathways SGK inhibitor

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Effect of Lanthanum(Ⅲ) on Cytosolic Free Calcium in Isolated Rabbit Mature osteoclasts

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Journal of Rare Earths 2005年第5期23卷 580-583页

作者：张金超张天蓝许善锦王夔于世凤杨梦苏 Department of Chemistry College of Chemistry and Environmental Science Hebei University Baoding 071002 China Department of Chemical Biology School of Pharmaceutical Sciences Peking University Beijing 100083 ChinaSchool of Pharmaceutical Sciences Capital University of Medical Sciences Beijing 100054 China Department of Chemical Biology School of Pharmaceutical Sciences Peking University Beijing 100083 China Department of Oral Pathology Stomatological Hospital Peking University Beijing 100081 China Department of Biology and Chemistry City University of Hong Kong Hong Kong

The effect of lanthanum （ Ⅲ ）（La^3 ＋） on cytosolic free calcium （ [ Ca^2 ＋ ] i ） in isolated rabbit mature osteoclasts was studied with the employment of fluo-3/AM as an intracellular calcium-sensitive fluorescent probe by using a confocal laser scanning microscope. La^3＋ does not alter basal [Ca^2＋ ]i levels and cell spread area at the concentration of 1.00 × 10^- 8 mol· L ^- 1. However, La^3 ＋ at higher concentrations （ 1. 00 × 10^ - 5 and 1.00 × 10^- 7 mol· L^- 1 ） decreases [ Ca^2 ＋ ] i levels and cell spread area, and greater decreases are observed for the higher concentrations of La^3 ＋ . Since [Ca^2 ＋ ]i affects cytoskeleton and the adhesion properties of osteoclasts, our results seem to suggest that La^3 ＋ inhibit bone resorption by decreasing [Ca^2＋]i in rabbit mature osteoclasts.

关键词： lanthanum（ Ⅲ ） osteoclasts cytosolic free calcium fluo-3/AM rare earths

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The role of dendritic cells derived osteoclasts in bone destruction diseases

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Genes & Diseases 2021年第4期8卷 401-411页

作者： Bo Wang Yutong Dong Zhansong Tian Yueqi Chen Shiwu Dong Department of Biomedical Materials Science Third Military Medical University(Army Medical University)Chongqing400038PR China Battalion of Basic Medical Sciences Third Military Medical University(Army Medical University)Chongqing400038PR China Department of Orthopedics Southwest HospitalThird Military Medical University(Army Medical University)Chongqing400038PR China State Key Laboratory of Trauma Burns and Combined InjuryThird Military Medical University(Army Medical University)Chongqing400038PR China

The bone is previously considered as a dominant organ involved in the processes of locomotion.However,in the past two decades,a large number of studies have suggested that the skeletal system closely coordinated with the immune system so as to result in the emerging area of'osteoimmunology'.In the evolution of many kinds of bone destruction-related dis-eases,osteoclasts could differentiate from dendritic cells,which contributed to increased expression of osteoclast-related membrane receptors and relatively higher activity of bone destruction,inducing sewere bone destruction under inflammatory conditions.Numerous fac-tors could influence the interaction between osteoclasts and dendritic cells,contributing to the pathogenesis of several bone diseases in the context of inflammation,including both im-munocytes and a large number of cytokines.In addition,the products of osteoclasts released from bone destruction area serve as important signals for the differentiation and activation of immature dendritic cells.Therefore,the border between the dendritic cell-rela ted immune response and osteoclast-related bone destruction has gradually unravelled.Dendritic cells and osteoclasts cooperate with each other to mediate bone destruction and bone remodelling under inflammatory conditions.In this review,we will pay attention to the interactions be-tween dendritic cells and osteoclasts in physiological and pathological conditions to further understand the skeletal system and identifty potential new therapeutic targets for the future by summarizing their significant roles and molecular mechanisms in bone destruction.

关键词： Bone destruction diseases Dendritic cells osteoclasts Osteoimmunology Trans-differentiation

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Role of osteoclasts in regulating hematopoietic stem and progenitor cells

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World Journal of Orthopedics 2013年第4期4卷 198-206页

作者： Takeshi Miyamoto Department of Orthopedic Surgery Keio University School of Medicine 35 Shinano-machi Shinjuku-ku Tokyo 160-8582 Japan Keio Kanrinmaru Project Keio University School of Medicine 35 Shinano-machi Shinjuku-ku Tokyo 160-8582 Japan Department of Integrated Bone Metabolism and Immunology Keio University School of Medicine 35 Shina-no-machi Shinjuku-ku Tokyo 160-8582 Japan

Bone marrow(BM) cavities are utilized for hematopoiesis and to maintain hematopoietic stem cells(HSCs). HSCs have the ability to self-renew as well as to differentiate into multiple different hematopoietic lineage cells. HSCs produce their daughter cells throughout the lifespan of individuals and thus, maintaining HSCs is crucial for individual life. BM cavities provide a specialized microenvironment termed "niche" to support HSCs. Niches are composed of various types of cells such as osteoblasts, endothelial cells and reticular cells. osteoclasts are unique cells which resorb bones and are required for BM cavity formation. Loss of osteoclast function or differentiation results in inhibition of BM cavity formation, an osteopetrotic phenotype. osteoclasts are also reportedly required for hematopoietic stem and progenitor cell(HSPC) mobilization to the periphery from BM cavities. Thus, lack of osteoclasts likely results in inhibition of HSC maintenance and HSPC mobilization. However, we found that osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization by using three independent osteoclast-less animal models. In this review, I will discuss the roles of osteoclasts in hematopoietic stem cell maintenance and mobilization.

关键词： osteoclasts Hematopoietic stem and progenitor cell Mobilization Receptor activator of nuclear factor kappa B ligand Osteomac Osteopetrosis op/op C-Fos Osteoprotegerin

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Electroacupuncture stimulating Zusanli(ST36),Sanyinjiao(SP6)in mice with collagen-induced arthritis leads to adenosine A2A receptor-mediated alteration of p38αmitogen-activated protein kinase signaling and inhibition of osteoclastogenesis

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Journal of Traditional Chinese Medicine 2023年第6期43卷 1103-1109页

作者： DU Zhongheng CONG Wenjie TANG Kejing ZHENG Qiqi SONG Zhiwei CHEN Yong YANG Su ZHANG Chunwu YE Tianshen Department of Acupuncture the First Affiliated Hospital of Wenzhou Medical UniversityWenzhou 325000China Department of Traditional Chinese Orthopedics&Traumatology the First Affiliated Hospital of Wenzhou Medical UniversityWenzhou 325000China Zhejiang Provincial Key Laboratory of Aging and Neurological Disorder Research the First Affiliated Hospital of Wenzhou Medical UniversityWenzhou 325000China

OBJECTIVE:To observe the effect of electroacupuncture(EA)stimulating Zusanli(ST36),Sanyinjiao(SP6)on inhibition of osteoclastogenesis and the role of the adenosine A2A receptor(A2AR)and the p38αMitogen-Activated Protein Kinase(MAPK)signaling pathway in mediating this effect.METHODS:Mice with collagen induced arthritis(CIA)received different treatments.Immunohistochemistry and western blotting were used to determine the levels of multiple signaling molecules in these joints[receptor activator of nuclear transcription factor-κB(NF-κB)ligand(RANKL),receptor activator of NF-κB(RANK),tumor necrosis factor receptor associated factor 6(TRAF6),p38α,NF-κB,and nuclear factor of activated T cells C1(NFATc1)].osteoclasts were identified using tartrate-resistant acid phosphatase(TRAP)staining.RESULTS:The immunohistochemistry results indicated upregulation of p38α,NF-κB,and NFATc1 in the CIA-control and CIA-EA-SCH58261 groups,but reduced levels in the CIA-EA group.Western blotting indicated upregulation of RANKL,RANK,TRAF6,p38α,NF-κB,and NFATc1 in the CIA-control and CIA-EA-SCH58261 groups,but reduced expression in the CIA-EA group.osteoclasts were more abundant in the CIA-control and CIA-EA-SCH58261 groups than in the CIA-EA group.CONCLUSIONS:EA treatment enhanced the A2AR activity and inhibited osteoclast formation by inhibition of RANKL,RANK,TRAF6,p38α,NF-κB,and NFATc1.SCH58261 reversed the effect of EA.These results suggest that EA regulated p38α-MAPK signaling by increasing A2AR activity,which inhibited osteoclastogenesis.

关键词： electroacupuncture arthritis experimental receptor adenosine A2A mitogen-activated protein kinases signal transduction osteoclasts

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Mesenchymal stem/stromal cells-derived exosomes for osteoporosis treatment

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World Journal of Stem Cells 2023年第3期15卷 83-89页

作者： Kai-Lun Huo Tie-Yi Yang Wei-Wei Zhang Jin Shao Postgraduate Training Base in Shanghai Gongli Hospital Ningxia Medical UniversityYinchuan 750004the Ningxia Hui Autonomous RegionChina Department of Orthopedics Pudong New Area Gongli HospitalSchool of Medical TechnologyUniversity of Shanghai for Science and TechnologyShanghai 200135China Department of Urology Renji HospitalSchool of MedicineShanghai Jiao Tong UniversityShanghai 200127China

Osteoporosis is a systemic bone disease,which leads to decreased bone mass and an increased risk of fragility fractures.Currently,there are many anti-resorption drugs and osteosynthesis drugs,which are effective in the treatment of osteoporosis,but their usage is limited due to their contraindications and side effects.In regenerative medicine,the unique repair ability of mesenchymal stem cells(MSCs)has been favored by researchers.The exosomes secreted by MSCs have signal transduction and molecular delivery mechanisms,which may have therapeutic effects.In this review,we describe the regulatory effects of MSCs-derived exosomes on osteoclasts,osteoblasts,and bone immunity.We aim to summarize the preclinical studies of exosome therapy in osteoporosis.Furth-ermore,we speculate that exosome therapy can be a future direction to improve bone health.

关键词： Mesenchymal stem cells Exosome Osteoporosis Osteoblasts osteoclasts Bone immunity

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Role of Iron Accumulation in Osteoporosis and the Underlying Mechanisms

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当代医学科学(英文) 2023年第4期43卷 647-654页

作者： Guang-fei LI Yan GAO E.D.WEINBERG Xi HUANG You-jia XU Department of Orthopedics The Second Affiliated Hospital of Soochow UniversitySuzhou 2015004China Osteoporosis Institute of Soochow University Suzhou 215004China Department of Biology&Program in Medical Sciences Indiana UniversityBloomingtonIN 47405USA Department of Environmental Medicine New York UniversitySchool of MedicineNew YorkNY

Osteoporosis is prevalent in postmenopausal women.The underlying reason is mainly estrogen deficiency,but recent studies have indicated that osteoporosis is also associated with iron accumulation after menopause.It has been confirmed that some methods of decreasing iron accumulation can improve the abnormal bone metabolism associated with postmenopausal osteoporosis.However,the mechanism of iron accumulation-induced osteoporosis is still unclear.Iron accumulation may inhibit the canonical Wnt/β-catenin pathway via oxidative stress,leading to osteoporosis by decreasing bone formation and increasing bone resorption via the osteoprotegerin(OPG)/receptor activator of nuclear factor kappa-B ligand(RANKL)/receptor activator of nuclear factor kappa-B(RANK)system.In addition to oxidative stress,iron accumulation also has been reported to inhibit either osteoblastogenesis or osteoblastic function as well as to stimulate either osteoclastogenesis or osteoclastic function directly.Furthermore,serum ferritin has been widely used for the prediction of bone status,and nontraumatic measurement of iron content by magnetic resonance imaging may be a promising early indicator of postmenopausal osteoporosis.

关键词： menopause osteoblasts osteoclasts Wnt/Beta-catenin hedgehog

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