INTERACTIONS BETWEEN SKELETAL SYSTEM AND MACROPHAGES IN HOMEOSTASIS AND BONE INJURY

Jelena M Živković, Stevo J Najman, Sanja Stojanović

DOI Number
-
First page
6
Last page
11

Abstract


New insights about close connection between skeletal and immune systems have expanded vistas of modern medicine and tissue engineering. Intensive progress of osteoimmunology enabled the understanding of processes related to bone tissue from a completely new angle, both in physiological and pathological conditions. In this respect, macrophages stand out as cells which affect bone through the ability to secrete a range of different cytokines. Macrophages’ activation is directed by environmental conditions which determine the phenotype and function of these cells. Acquired phenotypic and functional characteristics of macrophages are changed according to changes in their environment. Thanks to these abilities, macrophages have great impact on bone development, bone homeostasis and osteoreparatory process. During bone development, macrophages can affect osteoblast differentiation and matrix mineralization. Coordinated action of osteoclasts and osteoblasts is important in bone tissue remodeling process. Also, during osteoreparation macrophages are among the first cells that will come to the site of bone injury. Their impact on bone is particularly visible during inflammatory phase of fracture healing. Better understanding of mechanisms by which macrophages exert their influence on bone would be an important step in approach to more specific therapies that would modulate activity of these cells and might accelerate healing of bone defects.


Keywords

macrophages, bone, bone homeostasis, osteogenesis, fracture, osteoreparation.

Full Text:

PDF

References


Crockett JC, Rogers MJ, Coxon FP, Hocking LJ, Helfrich MH. Bone remodelling at a glance. J Cell Sci 2011; 124:991–998.

Fernández-Tresguerres-Hernández-Gil I, Alobera-Gracia MA, del-Canto Pingarrón M and Blanco-Jerez L. Physiological bases of bone regeneration II. The remodeling process. Med Oral Patol Oral Cir Bucal 2006; 11:E151–157.

Guihard P, Danger Y, Brounais B, et al. Induction of osteogenesis in mesenchymal stem cells by activated monocytes/macrophages depends on oncostatin M signaling. Stem Cells 2012; 30:762-772.

Marzona L, Pavolini B. Play and players in bone fracture healing match. Clin Cases Miner Bone Metab 2009; 6:159–162.

Živković J, Najman S, Vukelić M, et al. Osteogenic effect of inflammatory macrophages loaded onto mineral bone substitute in subcutaneous implants. Arch Biol Sci 2015; 67:173–186.

Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011; 11:723–737.

Hume DA, Ross IL, Himes SR, Sasmono RT, Wells CA, Ravasi T. The mononuclear phagocyte system revisited. J Leukoc Biol 2002; 72:621–627.

Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5:953–964.

Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol 2005; 23:901–944.

Hume DA. The mononuclear phagocyte system. Curr Opin Immunol 2006; 18:49–53.

Italiani P, Boraschi D. From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Front Immunol 2014; 5:514.

Hu X, Chakravarty SD, Ivashkiv LB. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunol Rev 2008; 226:41–56.

Rutherford MS, Witsell A, Schook LB. Mechanisms generating functionally heterogeneous macrophages: chaos revisited. J Leukoc Biol 1993; 53:602–618.

Mosser D. The many faces of macrophage activation. J Leukoc Biol. 2003; 73:209–212.

Mills C, Kincaid K, Alt J, Heilman M, Hill A. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 2000; 164:6166–6173.

Kharraz Y, Guerra J, Mann CJ, Serrano AL, Muñoz-Cánoves P. Macrophage plasticity and the role of inflammation in skeletal muscle repair. Mediators Inflamm 2013; 2013:491497.

Aaron J, Choi Y. Bone versus immune system. Nature 2000; 408:535–536.

Mori G, D'Amelio P, Faccio R, Brunetti G. Bone-immune cell crosstalk: bone diseases. J Immunol Res 2015; 2015:108451.

Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol 2007; 7:292–304.

Jacome-Galarza CE, Lee SK, Lorenzo JA, Aguila HL. Identification, characterization, and isolation of a common progenitor for osteoclasts, macrophages, and dendritic cells from murine bone marrow and periphery. J Bone Miner Res 2013; 28:1203–1213.

Yavropoulou MP, Yovos JG. Osteoclastogenesis- Current knowledge and future perspectives. J Musculoskelet Neuronal Interact 2008; 8:204–216.

Vignery A. Macrophage fusion the making of osteoclasts and giant cells. JEM 2005; 202:337–340.

Wada T, Nakashima T, Hiroshi N, Penninger JM. RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol Med 2006; 12:17–25.

Pacifici R. The immune system and bone. Arch Biochem Biophys 2010; 503:41–53.

Quinn JM, Saleh H. Modulation of osteoclast function in bone by the immune system. Mol Cell Endocrinol 2009; 310:40–51.

Mori G, D’Amelio P, Faccio R, Brunetti G. Bone-immune cell crosstalk: bone diseases. J Immunol Res 2015; 2015: 108451.

Dong L, Wang C. Harnessing the power of macrophages/

monocytes for enhanced bone tissue engineering. Trends Biotechnol 2013; 31:342–346.

Vi L, Baht GS, Mylvaganam S, et al. Macrophages promote osteoblastic differentiation in-vivo: implications in fracture repair and bone homeostasis. J Bone Miner Res 2015; 30:1090–1102.

Chang MK, Raggatt LJ, Alexander KA, et al. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 2008; 181:1232–1244.

Pettit AR, Chang MK, Hume DA, Raggatt LJ. Osteal macrophages: A new twist on coupling during bone dynamics. Bone 2008; 43:976–982.

Najdanović J, Cvetković V, Stojanović, S, et al. The influence of adipose-derived stem cells induced into endothelial cells on ectopic vasculogenesis and osteogenesis. Cell Mol Bioeng 2015; 8:577–590.

Cvetković VJ, Najdanović JG, Vukelić-Nikolić MĐ, Stojanović S, Najman SJ. Osteogenic potential of in vitro osteo-induced adipose-derived mesenchymal stem cells combined with platelet-rich plasma in an ectopic model. Int Orthop 2015; 39:2173–2180.

Mountziaris PM, Spicer PP, Kasper FK, Mikos AG. Harnessing and modulating inflammation in strategies for bone regeneration. Tissue Eng Part B Rev 2011; 17:393–402.

Kinne R, Bräuer R, Stuhlmüller B, Palombo-Kinne E, Burmester G. Macrophages in rheumatoid arthritis. Arthritis Res 2000; 2:189–202.

Cho TJ, Gerstenfeld LC, Einhorn TA. Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. J Bone Miner Res 2002; 17:513–520.

Mountziaris PM, Mikos AG. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev 2008; 14:179–186.

Kalfas IH. Principles of bone healing. Neurosurg Focus 2001; 10:E1.

Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 2003; 88:873–884.

Rundle CH, Wang H, Yu H, et al. Microarray analysis of gene expression during the inflammation and endochondral bone formation stages of rat femur fracture repair. Bone 2006; 38:521–529.

Marsell R, Einhorn TA. The biology of fracture healing. Injury 2011; 42:551–555.

Butterfield TA, Best TM, Merrick MA. The dual roles of neutrophils and macrophages in inflammation: a critical balance between tissue damage and repair. J Athl Train 2006; 41:457–465.

Kon T, Cho TJ, Aizawa T, et al. Expression of osteoprotegerin, receptor activator of NF-kappaB ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. J Bone Miner Res 2001; 16:1004–1014.

Harbour ME, Gregory JW, Jenkins HR, Evans BA. Proliferative response of different human osteoblast-like cell models to proinflammatory cytokines. Pediatr Res 2000; 48:163–168.

Hess K, Ushmorov A, Fiedler J, Brenner RE, Wirth T. TNFalpha promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-kappaB signaling pathway. Bone 2009; 45:367–376.

Amable PR, Carias RB, Teixeira MV, et al. Platelet-rich plasma preparation for regenerative medicine: optimization and quantification of cytokines and growth factors. Stem Cell Res Ther 2013; 4:67.

Chen G, Deng C, Li YP. TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 2012; 8:272–288.

Pirraco RP, Reis RL, Marques AP. Effect of monocytes

/macrophages on the early osteogenic differentiation of hBMSCs. J Tissue Eng Regen Med 2013; 7:392–400.

Schlundt C, El Khassawna T, Serra A, et al. Macrophages in bone fracture healing: Their essential role in endochondral ossification. Bone 2015; pii:S8756-3282(15)00392-0. [Epub ahead of print]

Schmid J, Wallkamm B, Hammerle CH, Gogolewski S, Lang NP. The significance of angiogenesis in guided bone regeneration. A case report of a rabbit experiment. Clin Oral Implants Res 1997; 8:244–248.

Barbeck M, Najman S, Stojanović S, et al. Addition of blood to a phycogenic bone substitute leads to increased in vivo vascularization. Biomed Mater 2015; 10:055007.

Moldovan L, Moldovan NI. Role of monocytes and macrophages in angiogenesis. EXS 2005; 94:127–146.

Sunderkötter C, Goebeler M, Schulze-Osthoff K, Bhardwaj R, Sorg C. Macrophage-derived angiogenesis factors. Pharmacol Ther 1991; 51:195–216.

Dohle E, Bischoff I, Böse T, et al.Macrophage-mediated angiogenic activation of outgrowth endothelial cells in co-culture with primary osteoblasts. Eur Cell Mater 2014; 27:149–164.

Chang J, Koh AJ, Roca H, McCauley LK. Juxtacrine interaction of macrophages and bone marrow stromal cells induce interleukin-6 signals and promote cell migration. Bone Res 2015; 3:15014.

Arnold L, Henry A, Poron F, et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 2007; 204:1057–1069.

Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nature Immunol 2010; 11:889–896.

Loi F, Córdova LA, Zhang R, et al. The effects of immunomodulation by macrophage subsets on osteogenesis in vitro. Stem Cell Res Ther 2016; 7:15.

Laskin D, Sunil V, Gardner C, Laskin J. Macrophages and tissue injury: agents of defense or destruction? Annu Rev Pharmacol Toxicol 2011; 51:267–288.

Kelava T, Šućur A, Kuzmac S, Katavić V. Interactions between bone and immune systems: A focus on the role of inflammation in bone resorption and fracture healing. Period Biol 2014; 116:

–52.

Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996; 87:2095–2147.

Sonomoto K, Yamaoka K, Oshita K, et al. Interleukin-1β induces differentiation of human mesenchymal stem cells into osteoblasts via the Wnt-5a/receptor tyrosine kinase-like orphan receptor 2 pathway. Arthritis Rheum 2012; 64:3355–3363.

Zhang YH, Heulsmann A, Tondravi MM, Mukherjee A, Abu-Amer Y. Tumor necrosis factor-alpha (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways. J Biol Chem 2001; 276:563–568.

Pajarinen J, Kouri VP, Jämsen E, Li TF, Mandelin J, Konttinen YT. The response of macrophages to titanium particles is determined by macrophage polarization. Acta Biomater 2013; 9:9229–9240.

Antonios JK, Yao Z, Li C, Rao AJ, Goodman SB. Macrophage polarization in response to wear particles in vitro. Cell Mol Immunol 2013; 10:471–482.

Herd HL, Bartlett KT, Gustafson JA, McGill LD, Ghandehari H. Macrophage silica nanoparticle response is phenotypically dependent. Biomaterials 2015; 53:574–582.

Thomas V, Halloran BA, Ambalavanan N, Catledge SA, Vohra YK. In vitro studies on the effect of particle size on macrophage responses to nanodiamond wear debris. Acta Biomater 2012; 8:1939–1947.

Cui X, Wen J, Zhao X, Chen X, Shao Z, Jiang JJ. A pilot study of macrophage responses to silk fibroin particles. J Biomed Mater Res Part A 2013; 101A:1511–1517.

Ding H, Zhu Z, Tang T, Yu D, Yu B, Dai K. Comparison of the cytotoxic and inflammatory responses of titanium particles with different methods for endotoxin removal in RAW264.7 macrophages. J Mater Sci Mater Med 2012; 23:1055–1062.

VanOs R, Lildhar LL, Lehoux EA, Beaulé PE, Catelas I. In vitro macrophage response to nanometer-size chromium oxide particles. J Biomed Mater Res Part B 2014; 102B:149–159.

Panilaitis B, Altman GH, Chen J, Jin HJ, Karageorgiou V, Kaplan DL. Macrophage responses to silk. Biomaterials 2003; 24:3079–3085.

Chen Z, Wu C, Gu W, Klein T, Crawford R, Xiao Y. Osteogenic differentiation of bone marrow MSCs by β-tricalcium phosphate stimulating macrophages via BMP2 signalling pathway. Biomaterials 2014; 35:1507–1518.


Refbacks

  • There are currently no refbacks.


© University of Niš, Serbia
Creative Commons licence CC BY-NC-ND
ISSN 0354-4699 (Print)
ISSN 2406-050X (Online)