Bone- and cartilage-protective effects of a monoclonal antibody against colony-stimulating factor 1 receptor in experimental arthritis

Arthritis and Rheumatology

Volumn 66, Issue 11, 2014, Pages 2989-3000

  Toh, Myew Ling ^a   Bonnefoy, Jean Yves ^a,d   Accart, Nathalie ^a   Cochin, Sandrine ^a   Pohle, Sandy ^b   Haegel, Hélène ^a   De Meyer, Micael ^a   Zemmour, Christophe ^a   Preville, Xavier ^a   Guillen, Christine ^a   Thioudellet, Christine ^a   Ancian, Philippe ^a   Lux, Anja ^b   Sehnert, Bettina ^c   Nimmerjahn, Falk ^b   Voll, Reinhard E ^c   Schett, Georg ^b  

^a TRANSGENE S A   (France)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d ElsaLys Biotech   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AFS 98; CD11B ANTIGEN; CD68 ANTIGEN; COLONY STIMULATING FACTOR 1 RECEPTOR; CYTOKINE RECEPTOR; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIMENTIN; COLONY STIMULATING FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTHRITIS; ARTICLE; BONE EROSION; CARTILAGE DEGENERATION; CARTILAGE INJURY; CLINICAL ARTICLE; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; DAS28; DISEASE SEVERITY; DRUG EFFICACY; EXPERIMENTAL ARTHRITIS; FOLLICULAR DENDRITIC CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MONOCYTE; MORPHOMETRICS; MOUSE; NEUTROPHIL; NONHUMAN; OSTEOARTHRITIS; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERUM TRANSFER ARTHRITIS; SYNOVIOCYTE; SYNOVITIS; SYNOVIUM; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTHRITIS, EXPERIMENTAL; BONE; CARTILAGE; CASE CONTROL STUDY; DBA MOUSE; DENDRITIC CELL; DISEASE MODEL; DRUG EFFECTS; FEMALE; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; RHEUMATOID ARTHRITIS;

ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; BONE AND BONES; CARTILAGE; CASE-CONTROL STUDIES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED DBA; MIDDLE AGED; MONOCYTES; OSTEOARTHRITIS; OSTEOCLASTS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SYNOVIAL MEMBRANE;

EID: 84925582383     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38624     Document Type: Article

References (51)

1. Schett G, David JP,. The multiple faces of autoimmune-mediated bone loss. Nat Rev Endocrinol 2010; 6: 698-706.
2. Hamilton JA,. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 2008; 8: 533-44.
3. Firestein GS, Xu WD, Townsend K, Broide D, Alvaro-Gracia J, Glasebrook A, et al., Cytokines in chronic inflammatory arthritis. I. Failure to detect T cell lymphokines (interleukin 2 and interleukin 3) and presence of macrophage colony-stimulating factor (CSF-1) and a novel mast cell growth factor in rheumatoid synovitis. J Exp Med 1988; 168: 1573-86.
4. Hwang SJ, Choi B, Kang SS, Chang JH, Kim YG, Chung YH, et al., Interleukin-34 produced by human fibroblast-like synovial cells in rheumatoid arthritis supports osteoclastogenesis. Arthritis Res Ther 2012; 14: R14.
5. Chemel M, Le Goff B, Brion R, Cozic C, Berreur M, Amiaud J, et al., Interleukin 34 expression is associated with synovitis severity in rheumatoid arthritis patients. Ann Rheum Dis 2012; 71: 150-4.
6. Takasugi K, Yamamura M, Iwahashi M, Otsuka F, Yamana J, Sunahori K, et al., Induction of tumour necrosis factor receptor-expressing macrophages by interleukin-10 and macrophage colony-stimulating factor in rheumatoid arthritis. Arthritis Res Ther 2006; 8: R126.
7. Hodge JM, Collier FM, Pavlos NJ, Kirkland MA, Nicholson GC,. M-CSF potently augments RANKL-induced resorption activation in mature human osteoclasts. PLoS One 2011; 6: e21462.
8. Baud'huin M, Renault R, Charrier C, Riet A, Moreau A, Brion R, et al., Interleukin-34 is expressed by giant cell tumours of bone and plays a key role in RANKL-induced osteoclastogenesis. J Pathol 2010; 221: 77-86.
9. Kitaura H, Zhou P, Kim HJ, Novack DV, Ross FP, Teitelbaum SL,. M-CSF mediates TNF-induced inflammatory osteolysis. J Clin Invest 2005; 115: 3418-27.
10. Evans R, Kamdar SJ, Fuller JA, Krupke DM,. The potential role of the macrophage colony-stimulating factor, CSF-1, in inflammatory responses: characterization of macrophage cytokine gene expression. J Leukoc Biol 1995; 58: 99-107.
11. Chapoval AI, Kamdar SJ, Kremlev SG, Evans R,. CSF-1 (M-CSF) differentially sensitizes mononuclear phagocyte subpopulations to endotoxin in vivo: a potential pathway that regulates the severity of gram-negative infections. J Leukoc Biol 1998; 63: 245-52.
12. Leizer T, Cebon J, Layton JE, Hamilton JA,. Cytokine regulation of colony-stimulating factor production in cultured human synovial fibroblasts. I. Induction of GM-CSF and G-CSF production by interleukin-1 and tumor necrosis factor. Blood 1990; 76: 1989-96.
13. Chan J, Leenen PJ, Bertoncello I, Nishikawa SI, Hamilton JA,. Macrophage lineage cells in inflammation: characterization by colony-stimulating factor-1 (CSF-1) receptor (c-Fms), ER-MP58, and ER-MP20 (Ly-6C) expression. Blood 1998; 92: 1423-31.
14. MacDonald KP, Rowe V, Bofinger HM, Thomas R, Sasmono T, Hume DA, et al., The colony-stimulating factor 1 receptor is expressed on dendritic cells during differentiation and regulates their expansion. J Immunol 2005; 175: 1399-405.
15. Iwahashi M, Yamamura M, Aita T, Okamoto A, Ueno A, Ogawa N, et al., Expression of Toll-like receptor 2 on CD16+ blood monocytes and synovial tissue macrophages in rheumatoid arthritis. Arthritis Rheum 2004; 50: 1457-67.
16. Abd AH, Savage NW, Halliday WJ, Hume DA,. The role of macrophages in experimental arthritis induced by Streptococcus agalactiae sonicate: actions of macrophage colony-stimulating factor (CSF-1) and other macrophage-modulating agents. Lymphokine Cytokine Res 1991; 10: 43-50.
17. Bischof RJ, Zafiropoulos D, Hamilton JA, Campbell IK,. Exacerbation of acute inflammatory arthritis by the colony-stimulating factors CSF-1 and granulocyte macrophage (GM)-CSF: evidence of macrophage infiltration and local proliferation. Clin Exp Immunol 2000; 119: 361-7.
18. Campbell IK, Rich MJ, Bischof RJ, Hamilton JA,. The colony-stimulating factors and collagen-induced arthritis: exacerbation of disease by M-CSF and G-CSF and requirement for endogenous M-CSF. J Leukoc Biol 2000; 68: 144-50.
19. Wei S, Dai XM, Stanley ER,. Transgenic expression of CSF-1 in CSF-1 receptor-expressing cells leads to macrophage activation, osteoporosis, and early death. J Leukoc Biol 2006; 80: 1445-53.
20. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, et al., Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 2002; 99: 111-20.
21. Dai XM, Zong XH, Sylvestre V, Stanley ER,. Incomplete restoration of colony-stimulating factor 1 (CSF-1) function in CSF-1-deficient Csf1op/Csf1op mice by transgenic expression of cell surface CSF-1. Blood 2004; 103: 1114-23.
22. Cenci S, Weitzmann MN, Gentile MA, Aisa MC, Pacifici R,. M-CSF neutralization and egr-1 deficiency prevent ovariectomy-induced bone loss. J Clin Invest 2000; 105: 1279-87.
23. Paniagua RT, Sharpe O, Ho PP, Chan SM, Chang A, Higgins JP, et al., Selective tyrosine kinase inhibition by imatinib mesylate for the treatment of autoimmune arthritis. J Clin Invest 2006; 116: 2633-42.
24. Conway JG, Pink H, Bergquist ML, Han B, Depee S, Tadepalli S, et al., Effects of the cFMS kinase inhibitor 5-(3-methoxy-4-((4-methoxybenzyl)oxy)benzyl)pyrimidine-2,4-diamine (GW2580) in normal and arthritic rats. J Pharmacol Exp Ther 2008; 326: 41-50.
25. Ohno H, Uemura Y, Murooka H, Takanashi H, Tokieda T, Ohzeki Y, et al., The orally-active and selective c-Fms tyrosine kinase inhibitor Ki20227 inhibits disease progression in a collagen-induced arthritis mouse model. Eur J Immunol 2008; 38: 283-91.
26. Paniagua RT, Chang A, Mariano MM, Stein EA, Wang Q, Lindstrom TM, et al., c-Fms-mediated differentiation and priming of monocyte lineage cells play a central role in autoimmune arthritis. Arthritis Res Ther 2010; 12: R32.
27. Madan B, Goh KC, Hart S, William AD, Jayaraman R, Ethirajulu K, et al., SB1578, a novel inhibitor of JAK2, FLT3, and c-Fms for the treatment of rheumatoid arthritis. J Immunol 2012; 189: 4123-34.
28. Yang YH, Hamilton JA,. Dependence of interleukin-1-induced arthritis on granulocyte-macrophage colony-stimulating factor. Arthritis Rheum 2001; 44: 111-9.
29. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO III, et al., 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 2010; 62: 2569-81.
30. Prevoo ML, van 't Hof MA, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL,. Modified disease activity scores that include twenty-eight-joint counts: development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum 1995; 38: 44-8.
31. Toh ML, Marotte H, Blond JL, Jhumka U, Eljaafari A, Mougin B, et al., Overexpression of synoviolin in peripheral blood and synoviocytes from rheumatoid arthritis patients and continued elevation in nonresponders to infliximab treatment. Arthritis Rheum 2006; 54: 2109-18.
32. Haegel H, Thioudellet C, Hallet R, Geist M, Menguy T, Le Pogam F, et al., A unique anti-CD115 monoclonal antibody which inhibits osteolysis and skews human monocyte differentiation from M2-polarized macrophages toward dendritic cells. mAbs 2013; 5: 736-47.
33. Toh ML, Hong SS, van de Loo F, Franqueville L, Lindholm L, van den Berg W, et al., Enhancement of adenovirus-mediated gene delivery to rheumatoid arthritis synoviocytes and synovium by fiber modifications: role of arginine-glycine-aspartic acid (RGD)- and non-RGD-binding integrins. J Immunol 2005; 175: 7687-98.
34. Krenn V, Morawietz L, Haupl T, Neidel J, Petersen I, Konig A,. Grading of chronic synovitis-a histopathological grading system for molecular and diagnostic pathology. Pathol Res Pract 2002; 198: 317-25.
35. Hamilton JA, Cheung D, Filonzi EL, Piccoli DS, Wojta J, Gallichio M, et al., Independent regulation of plasminogen activator inhibitor 2 and plasminogen activator inhibitor 1 in human synovial fibroblasts. Arthritis Rheum 1992; 35: 1526-34.
36. Redlich K, Gortz B, Hayer S, Zwerina J, Doerr N, Kostenuik P, et al., Repair of local bone erosions and reversal of systemic bone loss upon therapy with anti-tumor necrosis factor in combination with osteoprotegerin or parathyroid hormone in tumor necrosis factor-mediated arthritis. Am J Pathol 2004; 164: 543-55.
37. Rao DS, Parfitt AM, Villanueva AR, Dorman PJ, Kleerekoper M,. Hypophosphatemic osteomalacia and adult Fanconi syndrome due to light-chain nephropathy: another form of oncogenous osteomalacia. Am J Med 1987; 82: 333-8.
38. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, et al., Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 1987; 2: 595-610.
39. Fuller K, Owens JM, Jagger CJ, Wilson A, Moss R, Chambers TJ,. Macrophage colony-stimulating factor stimulates survival and chemotactic behavior in isolated osteoclasts. J Exp Med 1993; 178: 1733-44.
40. Warren MK, Ralph P,. Macrophage growth factor CSF-1 stimulates human monocyte production of interferon, tumor necrosis factor, and colony stimulating activity. J Immunol 1986; 137: 2281-5.
41. Shin EK, Lee SH, Cho SH, Jung S, Yoon SH, Park SW, et al., Association between colony-stimulating factor 1 receptor gene polymorphisms and asthma risk. Hum Genet 2010; 128: 293-302.
42. Sasmono RT, Ehrnsperger A, Cronau SL, Ravasi T, Kandane R, Hickey MJ, et al., Mouse neutrophilic granulocytes express mRNA encoding the macrophage colony-stimulating factor receptor (CSF-1R) as well as many other macrophage-specific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1. J Leukoc Biol 2007; 82: 111-23.
43. Masaoka T, Shibata H, Ohno R, Katoh S, Harada M, Motoyoshi K, et al., Double-blind test of human urinary macrophage colony-stimulating factor for allogeneic and syngeneic bone marrow transplantation: effectiveness of treatment and 2-year follow-up for relapse of leukaemia. Br J Haematol 1990; 76: 501-5.
44. Hidaka T, Akada S, Teranishi A, Morikawa H, Sato S, Yoshida Y, et al., Mirimostim (macrophage colony-stimulating factor; M-CSF) improves chemotherapy-induced impaired natural killer cell activity, Th1/Th2 balance, and granulocyte function. Cancer Sci 2003; 94: 814-20.
45. Nakao K, Kubota S, Doi H, Eguchi T, Oka M, Fujisawa T, et al., Collaborative action of M-CSF and CTGF/CCN2 in articular chondrocytes: possible regenerative roles in articular cartilage metabolism. Bone 2005; 36: 884-92.
46. Fend L, Accart N, Kintz J, Cochin S, Reymann C, Le Pogam F, et al., Therapeutic effects of anti-CD115 monoclonal antibody in mouse cancer models through dual inhibition of tumor-associated macrophages and osteoclasts. PLoS One 2013; 8: e73310.
47. Murayama T, Yokode M, Kataoka H, Imabayashi T, Yoshida H, Sano H, et al., Intraperitoneal administration of anti-c-fms monoclonal antibody prevents initial events of atherogenesis but does not reduce the size of advanced lesions in apolipoprotein E-deficient mice. Circulation 1999; 99: 1740-6.
48. Jose MD, Le Meur Y, Atkins RC, Chadban SJ,. Blockade of macrophage colony-stimulating factor reduces macrophage proliferation and accumulation in renal allograft rejection. Am J Transplant 2003; 3: 294-300.
49. MacDonald KP, Palmer JS, Cronau S, Seppanen E, Olver S, Raffelt NC, et al., An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. Blood 2010; 116: 3955-63.
50. Lenzo JC, Turner AL, Cook AD, Vlahos R, Anderson GP, Reynolds EC, et al., Control of macrophage lineage populations by CSF-1 receptor and GM-CSF in homeostasis and inflammation. Immunol Cell Biol 2012; 90: 429-40.
51. ++) monocytes in rheumatoid arthritis patient. Blood 2012; 119: 5329-30.