Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Calcified Tissue International
Published in: Calcified Tissue International 1/2014

01-01-2014 | Review

Cells of the Immune System Orchestrate Changes in Bone Cell Function

Authors: Sarah E. Wythe, Vicky Nicolaidou, Nicole J. Horwood

Published in: Calcified Tissue International | Issue 1/2014

Login to get access

Abstract

There is a complex interplay between the cells of the immune system and bone. Immune cells, such as T and NK cells, are able to enhance osteoclast formation via the production of RANKL. Yet there is increasing evidence to show that during the resolution of inflammation or as a consequence of increased osteoclastogenesis there is an anabolic response via the formation of more osteoblasts. Furthermore, osteoblasts themselves are involved in the control of immune cell function, thus promoting the resolution of inflammation. Hence, the concept of “coupling”—how bone formation is linked to resorption—needs to be more inclusive rather than restricting our focus to osteoblast–osteoclast interactions as in a whole organism these cells are never in isolation. This review will investigate the role of immune cells in normal bone homeostasis and in inflammatory diseases where the balance between resorption and formation is lost.
Literature
1.
Howard GA et al (1981) Parathyroid hormone stimulates bone formation and resorption in organ culture: evidence for a coupling mechanism. Proc Natl Acad Sci USA 78(5):3204–3208PubMed
2.
Martin TJ, Sims NA (2005) Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 11(2):76–81PubMed
3.
Tamma R, Zallone A (2012) Osteoblast and osteoclast crosstalks: from OAF to Ephrin. Inflamm Allergy Drug Targets 11(3):196–200PubMed
4.
Takayanagi H (2012) New developments in osteoimmunology. Nat Rev Rheumatol 8(11):684–689PubMed
5.
Horton MA et al (1985) On the origin of the osteoclast: the cell surface phenotype of rodent osteoclasts. Calcif Tissue Int 37(1):46–50PubMed
6.
Quinn JM et al (2000) Fibroblastic stromal cells express receptor activator of NF-kappaB ligand and support osteoclast differentiation. J Bone Miner Res 15(8):1459–1466PubMed
7.
Soderstrom K et al (2010) Natural killer cells trigger osteoclastogenesis and bone destruction in arthritis. Proc Natl Acad Sci USA 107(29):13028–13033PubMed
8.
Horwood NJ et al (1999) Activated T lymphocytes support osteoclast formation in vitro. Biochem Biophys Res Commun 265(1):144–150PubMed
9.
Kong YY et al (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402(6759):304–309PubMed
10.
Shinoda K et al (2003) Resting T cells negatively regulate osteoclast generation from peripheral blood monocytes. Bone 33(4):711–720PubMed
11.
Rifas L, Arackal S, Weitzmann MN (2003) Inflammatory T cells rapidly induce differentiation of human bone marrow stromal cells into mature osteoblasts. J Cell Biochem 88(4):650–659 PubMed
12.
Gough AK et al (1994) Generalised bone loss in patients with early rheumatoid arthritis. Lancet 344(8914):23–27PubMed
13.
Loftus EV Jr et al (2003) Risk of fracture in ulcerative colitis: a population-based study from Olmsted County, Minnesota. Clin Gastroenterol Hepatol 1(6):465–473PubMed
14.
Magrey M, Khan MA (2010) Osteoporosis in ankylosing spondylitis. Curr Rheumatol Rep 12(5):332–336PubMed
15.
Spector TD et al (1993) Risk of vertebral fracture in women with rheumatoid arthritis. BMJ 306(6877):558PubMed
16.
Eyerich S et al (2009) Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 119(12):3573–3585PubMedCentralPubMed
17.
Murphy CA et al (2003) Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198(12):1951–1957PubMedCentralPubMed
18.
Takayanagi H et al (2000) T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 408(6812):600–605PubMed
19.
Sato K, Takayanagi H (2006) Osteoclasts, rheumatoid arthritis, and osteoimmunology. Curr Opin Rheumatol 18(4):419–426PubMed
20.
Takayanagi H (2005) Inflammatory bone destruction and osteoimmunology. J Periodontal Res 40(4):287–293PubMed
21.
Kotake S et al (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103(9):1345–1352PubMedCentralPubMed
22.
Zaiss MM et al (2010) Regulatory T cells protect from local and systemic bone destruction in arthritis. J Immunol 184(12):7238–7246PubMed
23.
Kim YG et al (2007) Human CD4+CD25+ regulatory T cells inhibit the differentiation of osteoclasts from peripheral blood mononuclear cells. Biochem Biophys Res Commun 357(4):1046–1052PubMed
24.
Wythe SE et al (2013) Targeted delivery of cytokine therapy to rheumatoid tissue by a synovial targeting peptide. Ann Rheum Dis 72(1):129–135PubMedCentralPubMed
25.
Appel H et al (2006) Immunohistologic analysis of zygapophyseal joints in patients with ankylosing spondylitis. Arthritis Rheum 54(9):2845–2851PubMed
26.
Bowness P et al (2011) Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol 186(4):2672–2680PubMedCentralPubMed
27.
Daoussis D et al (2010) Evidence that Dkk-1 is dysfunctional in ankylosing spondylitis. Arthritis Rheum 62(1):150–158PubMed
28.
Appel H et al (2009) Altered skeletal expression of sclerostin and its link to radiographic progression in ankylosing spondylitis. Arthritis Rheum 60(11):3257–3262PubMed
29.
Chen HA et al (2010) Association of bone morphogenetic proteins with spinal fusion in ankylosing spondylitis. J Rheumatol 37(10):2126–2132PubMed
30.
Vosse D et al (2008) Association of markers of bone- and cartilage-degradation with radiological changes at baseline and after 2 years follow-up in patients with ankylosing spondylitis. Rheumatology (Oxford) 47(8):1219–1222
31.
Braun J, Baraliakos X (2011) Imaging of axial spondyloarthritis including ankylosing spondylitis. Ann Rheum Dis 70(Suppl 1):i97–i103PubMed
32.
Byrne FR et al (2005) CD4+CD45RBHi T cell transfer induced colitis in mice is accompanied by osteopenia which is treatable with recombinant human osteoprotegerin. Gut 54(1):78–86PubMed
33.
Ruutu M et al (2012) Beta-glucan triggers spondylarthritis and Crohn’s disease-like ileitis in SKG mice. Arthritis Rheum 64(7):2211–2222PubMed
34.
35.
Zaidi M (2007) Skeletal remodeling in health and disease. Nat Med 13(7):791–801PubMed
36.
Jilka RL et al (1998) Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 101(9):1942–1950PubMedCentralPubMed
37.
Kimble RB et al (1996) Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1 and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production. J Biol Chem 271(46):28890–28897PubMed
38.
Cenci S et al (2000) Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 106(10):1229–1237PubMedCentralPubMed
39.
Lee SK et al (2006) T lymphocyte-deficient mice lose trabecular bone mass with ovariectomy. J Bone Miner Res 21(11):1704–1712PubMed
40.
Yamaza T et al (2008) Pharmacologic stem cell based intervention as a new approach to osteoporosis treatment in rodents. PLoS One 3(7):e2615PubMedCentralPubMed
41.
Roggia C et al (2001) Up-regulation of TNF-producing T cells in the bone marrow: a key mechanism by which estrogen deficiency induces bone loss in vivo. Proc Natl Acad Sci USA 98(24):13960–13965PubMed
42.
Li JY et al (2011) Ovariectomy disregulates osteoblast and osteoclast formation through the T-cell receptor CD40 ligand. Proc Natl Acad Sci USA 108(2):768–773PubMed
43.
Grassi F et al (2007) Oxidative stress causes bone loss in estrogen-deficient mice through enhanced bone marrow dendritic cell activation. Proc Natl Acad Sci USA 104(38):15087–15092PubMed
44.
Li Y et al (2007) B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood 109(9):3839–3848PubMed
45.
DeSelm CJ et al (2012) IL-17 mediates estrogen-deficient osteoporosis in an Act1-dependent manner. J Cell Biochem 113(9):2895–2902PubMedCentralPubMed
46.
Fox SW, Chambers TJ (2000) Interferon-gamma directly inhibits TRANCE-induced osteoclastogenesis. Biochem Biophys Res Commun 276(3):868–872PubMed
47.
Kotake S et al (2005) IFN-gamma-producing human T cells directly induce osteoclastogenesis from human monocytes via the expression of RANKL. Eur J Immunol 35(11):3353–3363PubMed
48.
Madyastha PR et al (2000) IFN-gamma enhances osteoclast generation in cultures of peripheral blood from osteopetrotic patients and normalizes superoxide production. J Interferon Cytokine Res 20(7):645–652PubMed
49.
Sato K et al (1992) Prolonged decrease of serum calcium concentration by murine gamma-interferon in hypercalcemic, human tumor (EC-GI)-bearing nude mice. Cancer Res 52(2):444–449PubMed
50.
Tohkin M et al (1994) Comparative study of inhibitory effects by murine interferon gamma and a new bisphosphonate (alendronate) in hypercalcemic, nude mice bearing human tumor (LJC-1-JCK). Cancer Immunol Immunother 39(3):155–160PubMed
51.
Arnoldi J, Gerdes J, Flad HD (1990) Immunohistologic assessment of cytokine production of infiltrating cells in various forms of leprosy. Am J Pathol 137(4):749–753PubMed
52.
Baker PJ et al (1999) CD4+ T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67(6):2804–2809PubMedCentralPubMed
53.
Cenci S et al (2003) Estrogen deficiency induces bone loss by increasing T cell proliferation and lifespan through IFN-gamma-induced class II transactivator. Proc Natl Acad Sci USA 100(18):10405–10410PubMed
54.
Goodman GR et al (1999) Interferon-alpha, unlike interferon-gamma, does not cause bone loss in the rat. Bone 25(4):459–463PubMed
55.
Key LL Jr et al (1995) Long-term treatment of osteopetrosis with recombinant human interferon gamma. N Engl J Med 332(24):1594–1599PubMed
56.
Mann GN et al (1994) Interferon-gamma causes loss of bone volume in vivo and fails to ameliorate cyclosporin A-induced osteopenia. Endocrinology 135(3):1077–1083PubMed
57.
Rodriguiz RM, Key LL Jr, Ries WL (1993) Combination macrophage-colony stimulating factor and interferon-gamma administration ameliorates the osteopetrotic condition in microphthalmic (mi/mi) mice. Pediatr Res 33(4 Pt 1):384–389PubMed
58.
Duque G et al (2011) Interferon-gamma plays a role in bone formation in vivo and rescues osteoporosis in ovariectomized mice. J Bone Miner Res 26(7):1472–1483PubMed
59.
Gao Y et al (2007) IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 117(1):122–132PubMedCentralPubMed
60.
Tyagi AM et al (2012) Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: a new candidate in the pathogenesis of osteoporosis. PLoS One 7(9):e44552PubMedCentralPubMed
61.
Goswami J et al (2009) A bone-protective role for IL-17 receptor signaling in ovariectomy-induced bone loss. Eur J Immunol 39(10):2831–2839PubMedCentralPubMed
62.
Rivollier A et al (2004) Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 104(13):4029–4037PubMed
63.
Speziani C et al (2007) Murine dendritic cell transdifferentiation into osteoclasts is differentially regulated by innate and adaptive cytokines. Eur J Immunol 37(3):747–757PubMed
64.
Teitelbaum SL (2000) Bone resorption by osteoclasts. Science 289(5484):1504–1508PubMed
65.
Alnaeeli M, Penninger JM, Teng YT (2006) Immune interactions with CD4+ T cells promote the development of functional osteoclasts from murine CD11c+ dendritic cells. J Immunol 177(5):3314–3326PubMed
66.
67.
Jacome-Galarza CE et al (2013) Identification, characterization and isolation of a common progenitor for osteoclasts, macrophages and dendritic cells from murine bone marrow and periphery. J Bone Miner Res 28:1203–1213PubMed
68.
Mizoguchi T et al (2009) Identification of cell cycle-arrested quiescent osteoclast precursors in vivo. J Cell Biol 184(4):541–554PubMed
69.
Charles JF et al (2012) Inflammatory arthritis increases mouse osteoclast precursors with myeloid suppressor function. J Clin Invest 122(12):4592–4605PubMedCentralPubMed
70.
Grcevic D et al (2006) Activated T lymphocytes suppress osteoclastogenesis by diverting early monocyte/macrophage progenitor lineage commitment towards dendritic cell differentiation through down-regulation of receptor activator of nuclear factor-kappaB and c-Fos. Clin Exp Immunol 146(1):146–158PubMedCentralPubMed
71.
Gupta N et al (2010) IL-3 inhibits human osteoclastogenesis and bone resorption through downregulation of c-Fms and diverts the cells to dendritic cell lineage. J Immunol 185(4):2261–2272PubMed
72.
Paust S, von Andrian UH (2011) Natural killer cell memory. Nat Immunol 12(6):500–508PubMed
73.
74.
Grom AA et al (2003) Natural killer cell dysfunction in patients with systemic-onset juvenile rheumatoid arthritis and macrophage activation syndrome. J Pediatr 142(3):292–296PubMed
75.
Pridgeon C et al (2003) Natural killer cells in the synovial fluid of rheumatoid arthritis patients exhibit a CD56bright, CD94bright, CD158negative phenotype. Rheumatology (Oxford) 42(7):870–878
76.
Lo CK et al (2008) Natural killer cell degeneration exacerbates experimental arthritis in mice via enhanced interleukin-17 production. Arthritis Rheum 58(9):2700–2711PubMed
77.
Brennan PJ, Brigl M, Brenner MB (2013) Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 13(2):101–117PubMed
78.
79.
Hu M et al (2011) Activated invariant NKT cells regulate osteoclast development and function. J Immunol 186(5):2910–2917PubMed
80.
Mauri C, Bosma A (2012) Immune regulatory function of B cells. Annu Rev Immunol 30:221–241PubMed
81.
Blin-Wakkach C et al (2004) Characterization of a novel bipotent hematopoietic progenitor population in normal and osteopetrotic mice. J Bone Miner Res 19(7):1137–1143PubMed
82.
Dougall WC et al (1999) RANK is essential for osteoclast and lymph node development. Genes Dev 13(18):2412–2424PubMed
83.
Kong YY et al (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397(6717):315–323PubMed
84.
Yun TJ et al (2001) Osteoprotegerin, a crucial regulator of bone metabolism, also regulates B cell development and function. J Immunol 166(3):1482–1491PubMed
85.
Weitzmann MN et al (2000) B lymphocytes inhibit human osteoclastogenesis by secretion of TGFbeta. J Cell Biochem 78(2):318–324PubMed
86.
Li Y et al (2007) Ovariectomy-induced bone loss occurs independently of B cells. J Cell Biochem 100(6):1370–1375PubMed
87.
Raggatt LJ et al (2013) Absence of B cells does not compromise intramembranous bone formation during healing in a tibial injury model. Am J Pathol 182(5):1501–1508PubMed
88.
Nakken B et al (2011) B-cells and their targeting in rheumatoid arthritis—current concepts and future perspectives. Autoimmun Rev 11(1):28–34PubMed
89.
90.
Loutis N, Bruckner P, Pataki A (1988) Induction of erosive arthritis in mice after passive transfer of anti-type II collagen antibodies. Agents Actions 25(3–4):352–359PubMed
91.
Taylor PC, Plater-Zyberk C, Maini RN (1995) The role of the B cells in the adoptive transfer of collagen-induced arthritis from DBA/1 (H-2q) to SCID (H-2d) mice. Eur J Immunolo 25(3):763–769
92.
Svensson L et al (1998) B cell–deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol 111(3):521–526PubMedCentralPubMed
93.
Edwards JC, Leandro MJ, Cambridge G (2002) B-lymphocyte depletion therapy in rheumatoid arthritis and other autoimmune disorders. Biochem Soc Trans 30(4):824–828PubMed
94.
Moore J et al (2004) A phase II study of rituximab in rheumatoid arthritis patients with recurrent disease following haematopoietic stem cell transplantation. Bone Marrow Transplant 34(3):241–247PubMed
95.
Horwood NJ, Urbaniak AM, Danks L (2012) Tec family kinases in inflammation and disease. Int Rev Immunol 31(2):87–103PubMed
96.
Bedi B et al (2012) Silencing of parathyroid hormone (PTH) receptor 1 in T cells blunts the bone anabolic activity of PTH. Proc Natl Acad Sci USA 109(12):E725–E733PubMed
97.
Bar-Shavit Z (2007) The osteoclast: a multinucleated, hematopoietic-origin, bone-resorbing osteoimmune cell. J Cell Biochem 102(5):1130–1139PubMed
98.
Nakagawa H et al (1993) Influence of monocyte–macrophage lineage cells on alkaline phosphatase activity of developing osteoblasts derived from rat bone marrow stromal cells. Nippon Seikeigeka Gakkai Zasshi 67(5):480–489PubMed
99.
Rifas L et al (1989) Monokines produced by macrophages stimulate the growth of osteoblasts. Connect Tissue Res 23(2–3):163–178PubMed
100.
Champagne CM et al (2002) Macrophage cell lines produce osteoinductive signals that include bone morphogenetic protein-2. Bone 30(1):26–31PubMed
101.
Hume DA, Loutit JF, Gordon S (1984) The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of bone and associated connective tissue. J Cell Sci 66:189–194PubMed
102.
Chang MK et al (2008) Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 181(2):1232–1244PubMed
103.
Alexander KA et al (2011) Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J Bone Miner Res 26(7):1517–1532PubMed
104.
Nicolaidou V et al (2012) Monocytes induce STAT3 activation in human mesenchymal stem cells to promote osteoblast formation. PLoS One 7(7):e39871PubMedCentralPubMed
105.
Guihard P et al (2012) Induction of osteogenesis in mesenchymal stem cells by activated monocytes/macrophages depends on oncostatin M signaling. Stem Cells 30(4):762–772PubMed
106.
Zarling JM et al (1986) Oncostatin M: a growth regulator produced by differentiated histiocytic lymphoma cells. Proc Natl Acad Sci USA 83(24):9739–9743PubMed
107.
Walker EC et al (2010) Oncostatin M promotes bone formation independently of resorption when signaling through leukemia inhibitory factor receptor in mice. J Clin Invest 120(2):582–592PubMedCentralPubMed
108.
Malik N et al (1995) Developmental abnormalities in mice transgenic for bovine oncostatin M. Mol Cell Biol 15(5):2349–2358PubMedCentralPubMed
109.
de Hooge AS et al (2002) Adenoviral transfer of murine oncostatin M elicits periosteal bone apposition in knee joints of mice, despite synovial inflammation and up-regulated expression of interleukin-6 and receptor activator of nuclear factor-kappa B ligand. Am J Pathol 160(5):1733–1743PubMed
110.
Levy JB et al (1996) Activation of the JAK-STAT signal transduction pathway by oncostatin-M cultured human and mouse osteoblastic cells. Endocrinology 137(4):1159–1165PubMed
111.
Bellido T et al (1997) Activation of the Janus kinase/STAT (signal transducer and activator of transcription) signal transduction pathway by interleukin-6-type cytokines promotes osteoblast differentiation. Endocrinology 138(9):3666–3676PubMed
112.
Fujio Y et al (2004) Signals through gp130 upregulate Wnt5a and contribute to cell adhesion in cardiac myocytes. FEBS Lett 573(1–3):202–206PubMed
113.
Katoh M (2007) STAT3-induced WNT5A signaling loop in embryonic stem cells, adult normal tissues, chronic persistent inflammation, rheumatoid arthritis and cancer. Int J Mol Med 19(2):273–278PubMed
114.
Botelho FM, Edwards DR, Richards CD (1998) Oncostatin M stimulates c-Fos to bind a transcriptionally responsive AP-1 element within the tissue inhibitor of metalloproteinase-1 promoter. J Biol Chem 273(9):5211–5218PubMed
115.
Jochum W et al (2000) Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1. Nat Med 6(9):980–984PubMed
116.
Sabatakos G et al (2000) Overexpression of DeltaFosB transcription factor(s) increases bone formation and inhibits adipogenesis. Nat Med 6(9):985–990PubMed
117.
Sims NA, Walsh NC (2010) GP130 cytokines and bone remodelling in health and disease. BMB Rep 43(8):513–523PubMed
118.
Hamilton TA (2002) Molecular basis of macrophage activation: from gene expression to phenotypic diversity. In: Bourke BL (ed) The macrophage, 2nd edn. Oxford University Press, Oxford
119.
Porta C et al (2009) Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci USA 106(35):14978–14983PubMed
120.
121.
Gordon S, Martinez FO (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32(5):593–604PubMed
122.
123.
Fleetwood AJ et al (2007) Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J Immunol 178(8):5245–5252PubMed
124.
Smith W, Feldmann M, Londei M (1998) Human macrophages induced in vitro by macrophage colony-stimulating factor are deficient in IL-12 production. Eur J Immunol 28(8):2498–2507PubMed
125.
Tadokoro CE, de Almeida AI (2001) Bone marrow–derived macrophages grown in GM-CSF or M-CSF differ in their ability to produce IL-12 and to induce IFN-gamma production after stimulation with Trypanosoma cruzi antigens. Immunol Lett 77(1):31–38PubMed
126.
Verreck FA et al (2006) Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-gamma- and CD40L-mediated costimulation. J Leukoc Biol 79(2):285–293PubMed
127.
Hamilton JA (2008) Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 8(7):533–544PubMed
128.
Groh ME et al (2005) Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol 33(8):928–934PubMed
129.
Francois M et al (2012) Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Mol Ther 20(1):187–195PubMed
130.
Kim J, Hematti P (2009) Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol 37(12):1445–1453PubMedCentralPubMed
131.
Maggini J et al (2010) Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One 5(2):e9252PubMedCentralPubMed
132.
Nemeth K et al (2009) Bone marrow stromal cells attenuate sepsis via prostaglandin E2-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15(1):42–49PubMedCentralPubMed
133.
Jones S et al (2007) The antiproliferative effect of mesenchymal stem cells is a fundamental property shared by all stromal cells. J Immunol 179(5):2824–2831PubMed
134.
Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4):1815–1822PubMed
135.
Kawaguchi H et al (1995) The role of prostaglandins in the regulation of bone metabolism. Clin Orthop Relat Res 313:36–46PubMed
136.
Li L et al (2006) Regulation of bone biology by prostaglandin endoperoxide H synthases (PGHS): a rose by any other name. Cytokine Growth Factor Rev 17(3):203–216PubMed
137.
Xie C et al (2008) COX-2 from the injury milieu is critical for the initiation of periosteal progenitor cell mediated bone healing. Bone 43(6):1075–1083PubMedCentralPubMed
138.
Nagata T et al (1994) Effect of prostaglandin E2 on mineralization of bone nodules formed by fetal rat calvarial cells. Calcif Tissue Int 55(6):451–457PubMed
139.
Ninomiya T et al (2011) Prostaglandin E2 receptor EP4-selective agonist (ONO-4819) increases bone formation by modulating mesenchymal cell differentiation. Eur J Pharmacol 650(1):396–402PubMed
140.
Weinreb M, Suponitzky I, Keila S (1997) Systemic administration of an anabolic dose of PGE2 in young rats increases the osteogenic capacity of bone marrow. Bone 20(6):521–526PubMed
141.
Repovic P, Benveniste EN (2002) Prostaglandin E2 is a novel inducer of oncostatin-M expression in macrophages and microglia. J Neurosci 22(13):5334–5343PubMed
142.
Bystrom J et al (2008) Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 112(10):4117–4127PubMed
143.
Rajakariar R et al (2008) Novel biphasic role for lymphocytes revealed during resolving inflammation. Blood 111(8):4184–4192PubMed
144.
Pettit AR et al (2008) Osteal macrophages: a new twist on coupling during bone dynamics. Bone 43(6):976–982PubMed
145.
Ren G et al (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2(2):141–150PubMed
146.
Chen L et al (2008) Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 3(4):e1886PubMedCentralPubMed
147.
Xu W et al (2006) IL-10-producing macrophages preferentially clear early apoptotic cells. Blood 107(12):4930–4937PubMed
148.
Kawanaka N et al (2002) CD14+, CD16+ blood monocytes and joint inflammation in rheumatoid arthritis. Arthritis Rheum 46(10):2578–2586PubMed
149.
Rossol M et al (2012) The CD14(bright) CD16+ monocyte subset is expanded in rheumatoid arthritis and promotes expansion of the Th17 cell population. Arthritis Rheum 64(3):671–677PubMed
150.
Chiappetta N, Gruber B (2006) The role of mast cells in osteoporosis. Semin Arthritis Rheum 36(1):32–36PubMed
151.
Seitz S et al (2013) Increased osteoblast and osteoclast indices in individuals with systemic mastocytosis. Osteoporos Int 24:2325–2334PubMed
152.
Martin T, Gooi JH, Sims NA (2009) Molecular mechanisms in coupling of bone formation to resorption. Crit Rev Eukaryot Gene Expr 19(1):73–88PubMed
Metadata
Title
Cells of the Immune System Orchestrate Changes in Bone Cell Function
Authors
Sarah E. Wythe
Vicky Nicolaidou
Nicole J. Horwood
Publication date
01-01-2014
Publisher
Springer US
Published in
Calcified Tissue International / Issue 1/2014
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-013-9764-0

Other articles of this Issue 1/2014

Calcified Tissue International 1/2014 Go to the issue

Original Research

Osteoclast-Derived Coupling Factors in Bone Remodeling

Original Research

Control of Bone Remodeling by the Peripheral Sympathetic Nervous System

Original Research

Talking among Ourselves: Paracrine Control of Bone Formation within the Osteoblast Lineage

Erratum

Erratum to: Cell–Cell Signaling: Broadening Our View of the Basic Multicellular Unit

Review

Adipocytes and the Regulation of Bone Remodeling: A Balancing Act

Review

Osteocytes: Master Orchestrators of Bone
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits