Inflammatory arthritis increases mouse osteoclast precursors with myeloid suppressor function

Journal of Clinical Investigation

Volumn 122, Issue 12, 2012, Pages 4592-4605

  Charles, Julia F ^a,b,c,e   Hsu, Lih Yun ^a   Niemi, Erene C ^a,b   Weiss, Arthur ^a,d   Aliprantis, Antonios O ^c   Nakamura, Mary C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e Smith Building 614 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; BONE MARROW; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MONOCYTE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLAST PRECURSOR; PRECURSOR; PRIORITY JOURNAL; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD11B; ANTIGENS, DIFFERENTIATION; ANTIGENS, LY; ARTHRITIS; BONE DISEASES, METABOLIC; BONE MARROW; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; HUMANS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID PROGENITOR CELLS; OSTEOCLASTS; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECEPTORS, CHEMOKINE; ZYMOSAN;

EID: 84870535425     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI60920     Document Type: Article

References (52)

1. Kong YY, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397(6717):315-323.
2. Dougall WC, et al. RANK is essential for osteoclast and lymph node development. Genes Dev. 1999;13(18):2412-2424. (Pubitemid 29453612)
3. Li J, et al. RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism. Proc Natl Acad Sci U S A. 2000;97(4):1566-1571. (Pubitemid 30118482)
4. Kodama H, et al. Congenital osteoclast deficiency in osteopetrotic (op/op) mice is cured by injections of macrophage colony-stimulating factor. J Exp Med. 1991;173(1):269-272.
5. Felix R, Cecchini MG, Fleisch H. Macrophage colony stimulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse. Endocrinology. 1990;127(5):2592-2594. (Pubitemid 20381799)
6. Arai F, et al. Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J Exp Med. 1999;190(12):1741-1754. (Pubitemid 30013841)
7. Jacquin C, Gran DE, Lee SK, Lorenzo JA, Aguila HL. Identification of multiple osteoclast precursor populations in murine bone marrow. J Bone Miner Res. 2006;21(1):67-77. (Pubitemid 43023228)
8. Fogg DK, et al. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science. 2006;311(5757):83-87. (Pubitemid 43063063)
9. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science. 2010; 327(5966):656-661.
10. Miyamoto T, et al. Bifurcation of osteoclasts and dendritic cells from common progenitors. Blood. 2001;98(8):2544-2554.
11. Yao Z, et al. Tumor necrosis factor-alpha increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-Fms expression. J Biol Chem. 2006;281(17):11846-11855. (Pubitemid 43855445)
12. Muto A, et al. Lineage-committed osteoclast precursors circulate in blood and settle down into bone. J Bone Miner Res. 2011;26(12):2978-2990.
13. Speziani C, et al. Murine dendritic cell transdifferentiation into osteoclasts is differentially regulated by innate and adaptive cytokines. Eur J Immunol. 2007;37(3):747-757. (Pubitemid 46916941)
14. Sakaguchi N, et al. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature. 2003; 426(6965):454-460. (Pubitemid 37490133)
15. Yoshitomi H, et al. A role for fungal {beta}-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med. 2005;201(6):949-960. (Pubitemid 40524464)
16. Hata H, et al. Distinct contribution of IL-6, TNFalpha, IL-1, and IL-10 to T cell-mediated spontaneous autoimmune arthritis in mice. J Clin Invest. 2004;114(4):582-588. (Pubitemid 39572108)
17. Caetano-Lopes J, et al. Chronic arthritis leads to disturbances in the bone collagen network. Arthritis Res Ther. 2010;12(1):R9.
18. Keller KK, Stengaard-Pedersen K, Dagnaes-Hansen F, Nyengaard JR, Sakaguchi S, Hauge EM. Histological changes in chronic autoimmune SKG-arthritis evaluated by quantitative three-dimensional stereological estimators. Clin Exp Rheumatol. 2011;29(3):536-543.
19. Walsh NC, et al. Osteoblast function is compromised at sites of focal bone erosion in inflammatory arthritis. J Bone Miner Res. 2009;24(9):1572-1585.
20. Ritchlin CT, Haas-Smith SA, Li P, Hicks DG, Schwarz EM. Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest. 2003;111(6):821-831. (Pubitemid 37074957)
21. Park-Min KH, et al. Negative regulation of osteoclast precursor differentiation by CD11b and beta2 integrin-BCL6 signaling [published online ahead of print August 14, 2012]. J Bone Miner Res. doi:10.1002/jbmr.1739.
22. Takayanagi H. New immune connections in osteoclast formation. Ann N Y Acad Sci. 2010;1192:117-123.
23. Ishii M, et al. Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature. 2009;458(7237):524-528.
24. Maitra R, et al. Dendritic cell-mediated in vivo bone resorption. J Immunol. 2010;185(3):1485-1491.
25. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5(12):953-964. (Pubitemid 41746764)
26. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8(12):958-969.
27. Humphrey MB, et al. TREM2, a DAP12-associated receptor, regulates osteoclast differentiation and function. J Bone Miner Res. 2006;21(2):237-245. (Pubitemid 43265289)
28. Paloneva J, et al. DAP12/TREM2 deficiency results in impaired osteoclast differentiation and osteoporotic features. J Exp Med. 2003;198(4):669-675. (Pubitemid 37045349)
29. Peng Q, Malhotra S, Torchia JA, Kerr WG, Coggeshall KM, Humphrey MB. TREM2- and DAP12-dependent activation of PI3K requires DAP10 and is inhibited by SHIP1. Sci Signal. 2010; 3(122):ra38.
30. Joyce-Shaikh B, et al. Myeloid DAP12-associating lectin (MDL)-1 regulates synovial inflammation and bone erosion associated with autoimmune arthritis. J Exp Med. 2010;207(3):579-589.
31. Mori Y, et al. Inhibitory immunoglobulinlike receptors LILRB and PIR-B negatively regulate osteoclast development. J Immunol. 2008;181(7):4742-4751.
32. Ochi S, et al. Pathological role of osteoclast costimulation in arthritis-induced bone loss. Proc Natl Acad Sci U S A. 2007;104(27):11394-11399. (Pubitemid 47175151)
33. Richie Ehrlich LI, Serwold T, Weissman IL. In vitro assays misrepresent in vivo lineage potentials of murine lymphoid progenitors. Blood. 2011;117(9):2618-2624.
34. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45(9):593-605. (Pubitemid 350013057)
35. Aliprantis AO, et al. NFATc1 in mice represses osteoprotegerin during osteoclastogenesis and dissociates systemic osteopenia from inflammation in cherubism. J Clin Invest. 2008;118(11):3775-3789.
36. Sakaguchi S, Sakaguchi N, Yoshitomi H, Hata H, Takahashi T, Nomura T. Spontaneous development of autoimmune arthritis due to genetic anomaly of T cell signal transduction: Part 1. Semin Immunol. 2006;18(4):199-206. (Pubitemid 43903282)
37. Ma HL, et al. IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J Clin Invest. 2008;118(2):597-607.
38. Schon MP, Detmar M, Parker CM. Murine psoriasis- like disorder induced by naive CD4+ T cells. Nat Med. 1997;3(2):183-188. (Pubitemid 27064703)
39. Ma G, et al. Paired Immunoglobin-like receptor- B regulates the suppressive function and fate of myeloid-derived suppressor cells. Immunity. 2011;34(3):385-395.
40. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol. 2008;181(8):5791-5802.
41. Haile LA, Gamrekelashvili J, Manns MP, Korangy F, Greten TF. CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice. J Immunol. 2010;185(1):203-210.
42. Sato K, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006; 203(12):2673-2682. (Pubitemid 44833343)
43. Haile LA, et al. Myeloid-derived suppressor cells in inflammatory bowel disease: a new immunoregulatory pathway. Gastroenterology. 2008;135(3):871-881.
44. Zhu B, et al. CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J Immunol. 2007;179(8):5228-5237.
45. Rossner S, Voigtlander C, Wiethe C, Hanig J, Seifarth C, Lutz MB. Myeloid dendritic cell precursors generated from bone marrow suppress T cell responses via cell contact and nitric oxide production in vitro. Eur J Immunol. 2005;35(12):3533-3544. (Pubitemid 43025534)
46. Grassi F, et al. T cell suppression by osteoclasts in vitro. J Cell Physiol. 2011;226(4):982-990.
47. Karmakar S, Kay J, Gravallese EM. Bone damage in rheumatoid arthritis: mechanistic insights and approaches to prevention. Rheum Dis Clin North Am. 2010;36(2):385-404.
48. Gengenbacher M, Sebald HJ, Villiger PM, Hofstetter W, Seitz M. Infliximab inhibits bone resorption by circulating osteoclast precursor cells in patients with rheumatoid arthritis and ankylosing spondylitis. Ann Rheum Dis. 2008;67(5):620-624. (Pubitemid 351571924)
49. Duque G, et al. Interferon gamma plays a role in bone formation in vivo and rescues osteoporosis in ovariectomized mice. J Bone Miner Res. 2011;26(7):1472-1483.
50. Takayanagi H, et al. T-cell-mediated regulation of osteoclastogenesis by signalling crosstalk between RANKL and IFN-gamma. Nature. 2000;408(6812):600- 605.
51. Hsieh CL, et al. A role for TREM2 ligands in the phagocytosis of apoptotic neuronal cells by microglia. J Neurochem. 2009;109(4):1144-1156.
52. Erlebacher A, Derynck R. Increased expression of TGF-beta 2 in osteoblasts results in an osteoporosis-like phenotype. J Cell Biol. 1996;132(1-2):195-210.