Stage-dependent suppression of the formation of dentin-resorbing multinuclear cells with migration inhibitory factor in vitro

Kikuiri,Takashi; Yoshimura,Yoshitaka; Tabata,Futoshi; Hasegawa,Tomokazu; Nishihira,Jun; Shirakawa,Tetsuo

doi:10.3892/etm.2011.362

Stage-dependent suppression of the formation of dentin-resorbing multinuclear cells with migration inhibitory factor in vitro

Authors:
- Takashi Kikuiri
- Yoshitaka Yoshimura
- Futoshi Tabata
- Tomokazu Hasegawa
- Jun Nishihira
- Tetsuo Shirakawa
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Affiliations: Department of Dentistry for Children and Disabled Person, Hokkaido University Graduate School of Dental Medicine, Sapporo 060-8586, Japan, Department of Molecular Cell Pharmacology, Hokkaido University Graduate School of Dental Medicine, Sapporo 060-8586, Japan, Department of Pediatric Dentistry, Iwate Medical University, Morioka, Japan, Department of Medical Management and Informatics, Hokkaido Information University, Ebetsu, Japan, Division of Oral and Craniomaxillofacial Research, Dental Research Center, Nihon University School of Dentistry, Tokyo, Japan
Published online on: October 7, 2011 https://doi.org/10.3892/etm.2011.362
Pages: 37-43

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Abstract

The macrophage migration inhibitory factor (MIF) is a crucial mediator of immune responses and is known to play a pivotal role in cell proliferation and differentiation. In this study, we assessed whether MIF exerts regulatory effects on osteoclast formation in bone marrow cells and, if so, by what mechanism. Bone marrow cells were either co-cultured with MC3T3-E1 cells or cultured with macrophage-colony stimulating factor (M-CSF) and the soluble form of the receptor activator of the nuclear factor-κB ligand (RANKL). Under the influence of MIF, the formation of osteoclastic multinuclear cells was examined. The number of multinuclear TRAP-positive cells formed in the co-culture was significantly reduced when MIF (≥0.1 µg/ml) was exogenously applied during the third and fourth days of the 6-day cultivation period. MIF affected neither the number of mononuclear TRAP-positive cells induced with M-CSF and RANKL, nor the expression of RANKL and osteoprotegerin in MC3T3-E1 cells. TRAP-positive cells cultured on dentin slices with MIF showed lower dentin-resorbing activity than those cultured without MIF. These results suggest that MIF has no regulatory roles in the differentiation of bone marrow cells to mononuclear TRAP-positive cells, but has inhibitory effects on the formation of mature osteoclasts by preventing cell fusion, which may eventually interfere with the osteoclast-mediated dentin resorption.

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1.	N SaharaA ToyokiY AshizawaT DeguchiK SuzukiCytodifferentiation of the odontoclast prior to the shedding of human deciduous teeth: an ultrastructural and cytochemical studyAnat Rec2443349199610.1002/(SICI)1097-0185(199601)244:1%3C33::AID-AR4%3E3.0.CO;2-G8838422
2.	T DomonM YasudaM OsanaiIncrease in odontoclast nuclei number by cell fusion: a three-dimensional reconstruction of cell fusion of human odontoclastsAnat Rec252462471199810.1002/(SICI)1097-0185(199811)252:3%3C462::AID-AR14%3E3.0.CO;2-29811224
3.	N UdagawaN TakahashiT AkatsuOrigin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cellsProc Natl Acad Sci USA8772607264199010.1073/pnas.87.18.7260
4.	T SudaN TakahashiN UdagawaE JimiMT GillespieTJ MartinModulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand familiesEndocr Rev20345357199910.1210/edrv.20.3.036710368775
5.	DL LaceyE TimmsHL TanOsteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activationCell93165176199810.1016/S0092-8674(00)81569-X9568710
6.	DM BiskobingX FanJ RubinCharacterization of MCSF-induced proliferation and subsequent osteoclast formation in murine marrow cultureJ Bone Miner Res1010251032199510.1002/jbmr.56501007067484277
7.	SK LeeJ KalinowskiS JastrzebskiJA Lorenzo1,25(OH)2 vitamin D3-stimulated osteoclast formation in spleen-osteoblast cocultures is mediated in part by enhanced IL-1α and receptor activator of NF-κB ligand production in osteoblastsJ Immunol16923742380200212193704
8.	O KudoA SabokbarA PocockI ItonagaY FujikawaNA AthanasouInterleukin-6 and interleukin-11 support human osteoclast formation by a RANKL-independent mechanismBone3217200310.1016/S8756-3282(02)00915-812584029
9.	J LamS TakeshitaJE BarkerO KanagawaFP RossSL TeitelbaumTNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligandJ Clin Invest160148114882000
10.	T CalandraT RogerMacrophage migration inhibitory factor: a regulator of innate immunityNat Rev Immunol3791800200310.1038/nri120014502271
11.	JR DavidDelayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interactionProc Natl Acad Sci USA567277199610.1073/pnas.56.1.725229858
12.	BR BloomB BennettMechanism of a reaction in vitro associated with delayed-type hypersensitivityScience1538082196610.1126/science.153.3731.805938421
13.	A LanahanJB WilliamsLK SandersD NathansGrowth factor-induced delayed early response genesMol Cell Biol123919392919921508193
14.	GJ WistowMP ShaughnessyDC LeeJ HodinPS ZelenkaA macrophage migration inhibitory factor is expressed in the differentiating cells of the eye lensProc Natl Acad Sci USA9012721275199310.1073/pnas.90.4.12727679497
15.	RA MitchellCN MetzT PengR BucalaSustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid actionJ Biol Chem2741810018106199910.1074/jbc.274.25.18100
16.	S OnoderaJ NishihiraK IwabuchiMacrophage migration inhibitory factor up-regulates matrix metalloproteinase-9 and -13 in rat osteoblastsJ Biol Chem27778657874200210.1074/jbc.M10602020011751895
17.	L DanksA SabokbarR GundleNA AthanasouSynovial macrophage-osteoclast differentiation in inflammatory arthritisAnn Rheum Dis61916921200210.1136/ard.61.10.91612228163
18.	S OnoderaS SasakiS OhshimaTransgenic mice overexpressing macrophage migration inhibitory factor (MIF) exhibit high-turnover osteoporosisJ Bone Miner Res21876885200610.1359/jbmr.06031016753018
19.	C JacquinB Koczon-JaremkoHL AguilaMacrophage migration inhibitory factor inhibits osteoclastogenesisBone45640649200910.1016/j.bone.2009.06.02819591967
20.	T KatagiriN TakahashiRegulatory mechanisms of osteoblast and osteoclast differentiationOral Dis8147159200210.1034/j.1601-0825.2002.01829.x12108759
21.	H YasudaN ShimaN NakagawaOsteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKLProc Natl Acad Sci USA9535973602199810.1073/pnas.95.7.3597
22.	AR Ten CateOral Histology: Development, Structure, and FunctionMosby-Year BookSt. Louis3253291994
23.	T HasegawaY YoshimuraT KikuiriExpression of receptor activator of NF-kappa B ligand and osteoprotegerin in culture of human periodontal ligament cellsJ Periodontal Res37405411200210.1034/j.1600-0765.2002.01603.x12472833
24.	J NishihiraT KuriyamaM SakaiThe structure and physiochemical properties of rat liver macrophage migration inhibitory factorBiochim Biophys Acta1247159162199510.1016/0167-4838(94)00215-37873586
25.	K ShibataY YoshimuraT KikuiriEffect of the release from mechanical stress on osteoclastogenesis in RAW264.7 cellInt J Mol Med287379201121491081
26.	H AmanoS YamadaR FelixColony-stimulating factor-1 stimulates the fusion process in osteoclastsJ Bone Miner Res13846853199810.1359/jbmr.1998.13.5.8469610749
27.	Y ShiraiY YoshimuraY YawakaEffect of extracellular calcium concentrations on osteoclast differentiation in vitroBiochem Biophys Res Commun265484488199910.1006/bbrc.1999.166410558894
28.	Y DeyamaS TakeyamaKoshikawaOsteoblast maturation suppressed osteoclastogenesis in coculture with bone marrow cellsBiochem Biophys Res Commun274249254200010.1006/bbrc.2000.312710903926
29.	H YasudaN ShimaN NakagawaA novel molecular mechanism modulating osteoclast differentiation and functionBone25109113199010.1016/S8756-3282(99)00121-010423033
30.	T TsurukaiN UdagawaK MatsuzakiN TakahashiT SudaRoles of macrophage-colony stimulating factor and osteoclast differentiation factor in osteoclastogenesisJ Bone Miner Metab18177184200010.1007/s00774007001810874596
31.	T KukitaN WadaA KukitaRANKL-induced DC-STAMP is essential for osteoclastogenesisJ Exp Med200941946200410.1084/jem.2004051815452179
32.	M YagiT MiyamotoY SawataniDC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cellsJ Exp Med202345351200510.1084/jem.2005064516061724
33.	A VigneryMacrophage fusion: the making of osteoclasts and giant cellsJ Exp Med202337340200510.1084/jem.2005112316061722
34.	RP DonnE ShelleyWE OllierW ThomsonA novel 5′-flanking region polymorphism of macrophage migration inhibitory factor is associated with systemic-onset juvenile idiopathic arthritisArthritis Rheum44178217852001
35.	F De BenedettiC MeazzaM VivarelliFunctional and prognostic relevance of the -173 polymorphism of the macrophage migration inhibitory factor gene in systemic-onset juvenile idiopathic arthritisArthritis Rheum4813981407200312746913
36.	A LehtinenT OksaH HeleniusO RönningAdvanced dental maturity in children with juvenile rheumatoid arthritisEur J Oral Sci108184188200010.1034/j.1600-0722.2000.108003184.x10872987