Abrogated RANKL expression in properdin-deficient mice is associated with better outcome from collagen-antibody-induced arthritis

Arthritis Research and Therapy

Volumn 14, Issue 4, 2012, Pages

  Dimitrova, Petya ^a   Ivanovska, Nina ^a   Belenska, Lyudmila ^a   Milanova, Viktoriya ^a   Schwaeble, Wilhelm ^b   Stover, Cordula ^b  

^a INSTITUTE OF MICROBIOLOGY   (Bulgaria)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD86 ANTIGEN; COLLAGEN ANTIBODY; COMPLEMENT COMPONENT C5A; GAMMA INTERFERON; INTERLEUKIN 17; OSTEOCLAST DIFFERENTIATION FACTOR; PROPERDIN; TNFSF11 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DOWN REGULATION; FEMALE; IMMUNOCOMPETENT CELL; MALE; MOUSE; NEUTROPHIL; NONHUMAN; OSTEOCLAST; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DEFICIENCY; EXPERIMENTAL ARTHRITIS; GENE EXPRESSION REGULATION; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOCLASTS; PROPERDIN; RANK LIGAND;

EID: 84865305084     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3926     Document Type: Article

References (55)

1. Nandakumar KS, Holmdahl R. Efficient promotion of collagen antibody induced arthritis (CAIA) using four monoclonal antibodies specific for the major epitopes recognized in both collagen induced arthritis and rheumatoid arthritis. J Immunol Methods 2005, 304:126-136. 10.1016/j.jim.2005.06.017, 16125192.
2. Terato K, Harper DS, Griffiths MM, Hasty DL, Ye XJ, Cremer MA, Seyer JM. Collagen-induced arthritis in mice: synergistic effect of E. coli lipopolysaccharide bypasses epitope specificity in the induction of arthritis with monoclonal antibodies to type II collagen. Autoimmunity 1995, 22:137-147. 10.3109/08916939508995311, 8734568.
3. Nandakumar KS, Svensson L, Holmdahl R. Collagen type II-specific monoclonal antibody-induced arthritis in mice: description of the disease and the influence of age, sex, and genes. Am J Pathol 2003, 163:1827-1837. 10.1016/S0002-9440(10)63542-0, 1892447, 14578183.
4. Hutamekalin P, Saito T, Yamaki K, Mizutani N, Brand DD, Waritani T, Terato K, Yoshino S. Collagen antibody-induced arthritis in mice: development of a new arthritogenic 5-clone cocktail of monoclonal anti-type II collagen antibodies. J Immunol Methods 2009, 343:49-55. 10.1016/j.jim.2009.01.009, 19330909.
5. Jelezarova E, Vogt A, Lutz HU. Interaction of C3b(2)-IgG complexes with complement proteins properdin, factor B and factor H: implications for amplification. Biochem J 2000, 349:217-223. 10.1042/0264-6021:3490217, 1221140, 10861231.
6. Spitzer D, Mitchell LM, Atkinson JP, Hourcade DE. Properdin can initiate complement activation by binding specific target surfaces and providing a platform for de novo convertase assembly. J Immunol 2007, 179:2600-2608.
7. Hourcade DE. The role of properdin in the assembly of the alternative pathway C3 convertases of complement. J Biol Chem 2006, 281:2128-2132.
8. Schwaeble W, Dippold WG, Schafer MK, Pohla H, Jonas D, Luttig B, Weihe E, Huemer HP, Dierich MP, Reid KB. Properdin, a positive regulator of complement activation, is expressed in human T cell lines and peripheral blood T cells. J Immunol 1993, 151:2521-2528.
9. Schwaeble W, Huemer HP, Most J, Dierich MP, Strobel M, Claus C, Reid KB, Ziegler-Heitbrock HW. Expression of properdin in human monocytes. Eur J Biochem 1994, 219:759-764. 10.1111/j.1432-1033.1994.tb18555.x, 8112326.
10. Wirthmueller U, Dewald B, Thelen M, Schafer MK, Stover C, Whaley K, North J, Eggleton P, Reid KB, Schwaeble WJ. Properdin, a positive regulator of complement activation, is released from secondary granules of stimulated peripheral blood neutrophils. J Immunol 1997, 158:4444-4451.
11. Wu X, Xu TQ, Atkinson JP. Properdin homeostasis requires turnover of the alternative complement pathway. Proc Natl Acad Sci USA 2010, 107:19444-19448. 10.1073/pnas.1006608107, 2984156, 20974943.
12. Banda NK, Takahashi K, Wood AK, Holers VM, Arend WP. Pathogenic complement activation in collagen antibody-induced arthritis in mice requires amplification by the alternative pathway. J Immunol 2007, 179:4101-4109.
13. Hietala MA, Nandakumar KS, Persson L, Fahlen S, Holmdahl R, Pekna M. Complement activation by both classical and alternative pathways is critical for the effector phase of arthritis. Eur J Immunol 2004, 34:1208-1216. 10.1002/eji.200424895, 15048732.
14. Banda NK, Levitt B, Glogowska MJ, Thurman JM, Takahashi K, Stahl GL, Tomlinson S, Arend WP, Holers VM. Targeted inhibition of the complement alternative pathway with complement receptor 2 and factor H attenuates collagen antibody-induced arthritis in mice. J Immunol 2009, 183:5928-5937. 10.4049/jimmunol.0901826, 2828354, 19828624.
15. Wang Y, Kristan J, Hao L, Lenkoski CS, Shen Y, Matis LA. A role for complement in antibody-mediated inflammation: C5-deficient DBA/1 mice are resistant to collagen-induced arthritis. J Immunol 2000, 164:4340-4347.
16. Takai T. Fc receptors and their role in immune regulation and autoimmunity. J Clin Immunol 2005, 25:1-18. 10.1007/s10875-005-0353-8, 15742153.
17. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 2006, 6:173-182. 10.1038/nri1785, 16498448.
18. Kagari T, Tanaka D, Doi H, Shimozato T. Essential role of Fc gamma receptors in anti-type II collagen antibody-induced arthritis. J Immunol 2003, 170:4318-4324.
19. Tan Sardjono C, Mottram PL, van de Velde NC, Powell MS, Power D, Slocombe RF, Wicks IP, Campbell IK, McKenzie SE, Brooks M, Stevenson AW, Hogarth PM. Development of spontaneous multisystem autoimmune disease and hypersensitivity to antibody-induced inflammation in Fcgamma receptor IIa-transgenic mice. Arthritis Rheum 2005, 52:3220-3229. 10.1002/art.21344, 16200626.
20. Rowley MJ, Nandakumar KS, Holmdahl R. The role of collagen antibodies in mediating arthritis. Mod Rheumatol 2008, 18:429-441. 10.1007/s10165-008-0080-x, 18521704.
21. Nabbe KC, Blom AB, Holthuysen AE, Boross P, Roth J, Verbeek S, van Lent PL, van den Berg WB. Coordinate expression of activating Fc gamma receptors I and III and inhibiting Fc gamma receptor type II in the determination of joint inflammation and cartilage destruction during immune complex-mediated arthritis. Arthritis Rheum 2003, 48:255-265. 10.1002/art.10721, 12528127.
22. van Lent PL, Grevers L, Lubberts E, de Vries TJ, Nabbe KC, Verbeek S, Oppers B, Sloetjes A, Blom AB, van den Berg WB. Fcgamma receptors directly mediate cartilage, but not bone, destruction in murine antigen-induced arthritis: uncoupling of cartilage damage from bone erosion and joint inflammation. Arthritis Rheum 2006, 54:3868-3877. 10.1002/art.22253, 17133594.
23. Kleinau S. The impact of Fc receptors on the development of autoimmune diseases. Curr Pharm Des 2003, 9:1861-1870. 10.2174/1381612033454414, 12871190.
24. Chakravarti A, Raquil MA, Tessier P, Poubelle PE. Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 2009, 114:1633-1644. 10.1182/blood-2008-09-178301, 19546479.
25. Yeo L, Toellner KM, Salmon M, Filer A, Buckley CD, Raza K, Scheel-Toellner D. Cytokine mRNA profiling identifies B cells as a major source of RANKL in rheumatoid arthritis. Ann Rheum Dis 2011, 70:2022-2028. 10.1136/ard.2011.153312, 3184241, 21742639.
26. Lee SJ, Nam KI, Jin HM, Cho YN, Lee SE, Kim TJ, Lee SS, Kee SJ, Lee KB, Kim N, Park YW. Bone destruction by receptor activator of nuclear factor kappaB ligand-expressing T cells in chronic gouty arthritis. Arthritis Res Ther 2011, 13:R164. 10.1186/ar3483, 3308097, 21992185.
27. Ashley JW, McCoy EM, Clements DA, Shi Z, Chen T, Feng X. Development of cell-based high-throughput assays for the identification of inhibitors of receptor activator of nuclear factor-kappa B signaling. Assay Drug Dev Technol 2011, 9:40-49. 10.1089/adt.2010.0307, 3033204, 21050071.
28. Dimitrova P, Ivanovska N, Schwaeble W, Gyurkovska V, Stover C. The role of properdin in murine zymosan-induced arthritis. Mol Immunol 2010, 47:1458-1466. 10.1016/j.molimm.2010.02.007, 20226532.
29. Stover CM, Luckett JC, Echtenacher B, Dupont A, Figgitt SE, Brown J, Mannel DN, Schwaeble WJ. Properdin plays a protective role in polymicrobial septic peritonitis. J Immunol 2008, 180:3313-3318.
30. Ivanovska ND, Dimitrova PA, Luckett JC, El-Rachkidy Lonnen R, Schwaeble WJ, Stover CM. Properdin deficiency in murine models of nonseptic shock. J Immunol 2008, 180:6962-6969.
31. Takahashi N, Udagawa N, Kobayashi Y, Suda T. Generation of osteoclasts in vitro, and assay of osteoclast activity. Methods Mol Med 2007, 135:285-301. 10.1007/978-1-59745-401-8_18, 17951666.
32. Edwards DR, Murphy G, Reynolds JJ, Whitham SE, Docherty AJ, Angel P, Heath JK. Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J 1987, 6:1899-1904. 553574, 2820711.
33. de Hooge AS, van de Loo FA, Koenders MI, Bennink MB, Arntz OJ, Kolbe T, van den Berg WB. Local activation of STAT-1 and STAT-3 in the inflamed synovium during zymosan-induced arthritis: exacerbation of joint inflammation in STAT-1 gene-knockout mice. Arthritis Rheum 2004, 50:2014-2023. 10.1002/art.20302, 15188379.
34. Scheinman RI, Trivedi R, Vermillion S, Kompella UB. Functionalized STAT1 siRNA nanoparticles regress rheumatoid arthritis in a mouse model. Nanomedicine (Lond) 2011, 6:1669-1682.
35. Kimura Y, Zhou L, Miwa T, Song WC. Genetic and therapeutic targeting of properdin in mice prevents complement-mediated tissue injury. J Clin Invest 2010, 120:3545-3554. 10.1172/JCI41782, 2947218, 20941861.
36. Kemper C, Hourcade DE. Properdin: New roles in pattern recognition and target clearance. Mol Immunol 2008, 45:4048-4056. 10.1016/j.molimm.2008.06.034, 2628304, 18692243.
37. Schwaeble WJ, Reid KB. Does properdin crosslink the cellular and the humoral immune response?. Immunol Today 1999, 20:17-21. 10.1016/S0167-5699(98)01376-0, 10081225.
38. Camous L, Roumenina L, Bigot S, Brachemi S, Fremeaux-Bacchi V, Lesavre P, Halbwachs-Mecarelli L. Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood 2011, 117:1340-1349. 10.1182/blood-2010-05-283564, 21063021.
39. Gerard C, Gerard NP. C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu Rev Immunol 1994, 12:775-808. 10.1146/annurev.iy.12.040194.004015, 8011297.
40. Lee H, Whitfeld PL, Mackay CR. Receptors for complement C5a: the importance of C5aR and the enigmatic role of C5L2. Immunol Cell Biol 2008, 86:153-160. 10.1038/sj.icb.7100166, 18227853.
41. Shushakova N, Skokowa J, Schulman J, Baumann U, Zwirner J, Schmidt RE, Gessner JE. C5a anaphylatoxin is a major regulator of activating versus inhibitory FcgammaRs in immune complex-induced lung disease. J Clin Invest 2002, 110:1823-1830. 151656, 12488432.
42. Tsuboi N, Ernandez T, Li X, Nishi H, Cullere X, Mekala D, Hazen M, Kohl J, Lee DM, Mayadas TN. Regulation of human neutrophil Fcgamma receptor IIa by C5a receptor promotes inflammatory arthritis in mice. Arthritis Rheum 2011, 63:467-478. 10.1002/art.30141, 3128197, 21280001.
43. Bruhns P, Samuelsson A, Pollard JW, Ravetch JV. Colony-stimulating factor-1-dependent macrophages are responsible for IVIG protection in antibody-induced autoimmune disease. Immunity 2003, 18:573-581. 10.1016/S1074-7613(03)00080-3, 12705859.
44. Ignatius A, Schoengraf P, Kreja L, Liedert A, Recknagel S, Kandert S, Brenner RE, Schneider M, Lambris JD, Huber-Lang M. Complement C3a and C5a modulate osteoclast formation and inflammatory response of osteoblasts in synergism with IL-1beta. J Cell Biochem 2011, 112:2594-2605. 10.1002/jcb.23186, 21598302.
45. Sato T, Abe E, Jin CH, Hong MH, Katagiri T, Kinoshita T, Amizuka N, Ozawa H, Suda T. The biological roles of the third component of complement in osteoclast formation. Endocrinology 1993, 133:397-404. 10.1210/en.133.1.397, 8319587.
46. Tu Z, Bu H, Dennis JE, Lin F. Efficient osteoclast differentiation requires local complement activation. Blood 2010, 116:4456-4463. 10.1182/blood-2010-01-263590, 2996112, 20709903.
47. Schwarzenberger P, Huang W, Oliver P, Byrne P, La Russa V, Zhang Z, Kolls JK. IL-17 mobilizes peripheral blood stem cells with short- and long-term repopulating ability in mice. J Immunol 2001, 167:2081-2086.
48. Chabaud M, Durand JM, Buchs N, Fossiez F, Page G, Frappart L, Miossec P. Human interleukin-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum 1999, 42:963-970. 10.1002/1529-0131(199905)42:5<963::AID-ANR15>3.0.CO;2-E, 10323452.
49. Grevers LC, van Lent PL, Koenders MI, Walgreen B, Sloetjes AW, Nimmerjahn F, Sjef Verbeek J, van den Berg WB. Different amplifying mechanisms of interleukin-17 and interferon-gamma in Fcgamma receptor-mediated cartilage destruction in murine immune complex-mediated arthritis. Arthritis Rheum 2009, 60:396-407. 10.1002/art.24288, 19180490.
50. Svensson L, Nandakumar KS, Johansson A, Jansson L, Holmdahl R. IL-4-deficient mice develop less acute but more chronic relapsing collagen-induced arthritis. Eur J Immunol 2002, 32:2944-2953. 10.1002/1521-4141(2002010)32:10<2944::AID-IMMU2944>3.0.CO;2-4, 12355448.
51. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY. Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol 2011, 23:317-326. 10.1093/intimm/dxr007, 3082529, 21422151.
52. Culshaw S, Millington OR, Brewer JM, McInnes IB. Murine neutrophils present Class II restricted antigen. Immunol Lett 2008, 118:49-54. 10.1016/j.imlet.2008.02.008, 2430030, 18400308.
53. Hashimoto M, Hirota K, Yoshitomi H, Maeda S, Teradaira S, Akizuki S, Prieto-Martin P, Nomura T, Sakaguchi N, Kohl J, Heyman B, Takahashi M, Fujita T, Mimori T, Sakaguchi S. Complement drives Th17 cell differentiation and triggers autoimmune arthritis. J Exp Med 2010, 207:1135-1143. 10.1084/jem.20092301, 2882841, 20457757.
54. Fang C, Zhang X, Miwa T, Song WC. Complement promotes the development of inflammatory T-helper 17 cells through synergistic interaction with Toll-like receptor signaling and interleukin-6 production. Blood 2009, 114:1005-1015. 10.1182/blood-2009-01-198283, 2721782, 19491392.
55. Strainic MG, Liu J, Huang D, An F, Lalli PN, Muqim N, Shapiro VS, Dubyak GR, Heeger PS, Medof ME. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 2008, 28:425-435. 10.1016/j.immuni.2008.02.001, 2646383, 18328742.