Production of RANKL by Memory B Cells: A Link between B Cells and Bone Erosion in Rheumatoid Arthritis

Arthritis and Rheumatology

Volumn 68, Issue 4, 2016, Pages 805-816

  Meednu, Nida ^a   Zhang, Hengwei ^a   Owen, Teresa ^a   Sun, Wen ^a   Wang, Victor ^a   Cistrone, Christopher ^a   Rangel Moreno, Javier ^a   Xing, Lianping ^a   Anolik, Jennifer H ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD20 ANTIGEN; CD27 ANTIGEN; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; FAS ANTIGEN; IMMUNOGLOBULIN D; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TUMOR NECROSIS FACTOR; ACID PHOSPHATASE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ISOENZYME; TNFSF11 PROTEIN, HUMAN;

ADULT; ARTICLE; BONE EROSION; CD3+ T LYMPHOCYTE; CELL COUNT; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EX VIVO STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; MIDDLE AGED; MOLECULAR INTERACTION; MONOCYTE; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; SYNOVIUM; B LYMPHOCYTE; CASE CONTROL STUDY; CELL DIFFERENTIATION; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; OSTEOLYSIS; REAL TIME POLYMERASE CHAIN REACTION;

ACID PHOSPHATASE; ARTHRITIS, RHEUMATOID; B-LYMPHOCYTES; BONE RESORPTION; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; IN VITRO TECHNIQUES; ISOENZYMES; MONOCYTES; OSTEOCLASTS; RANK LIGAND; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYNOVIAL FLUID; SYNOVIAL MEMBRANE; TARTRATE-RESISTANT ACID PHOSPHATASE;

EID: 84962124860     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39489     Document Type: Article

References (47)

1. Scott DL, Pugner K, Kaarela K, Doyle DV, Woolf A, Holmes J, et al., The links between joint damage and disability in rheumatoid arthritis. Rheumatology (Oxford) 2000; 39: 122-32.
2. Hirayama T, Danks L, Sabokbar A, Athanasou NA., Osteoclast formation and activity in the pathogenesis of osteoporosis in rheumatoid arthritis. Rheumatology (Oxford) 2002; 41: 1232-9.
3. Gravallese EN, Harada Y, Wang JT, Gorn AH, Thornhill TS, Goldring SR., Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis. Am J Pathol 1998; 152: 943-51.
4. Gravallese EM, Manning C, Tsay A, Naito A, Pan C, Amento E, et al., Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor. Arthritis Rheum 2000; 43: 250-8.
5. Pettit AR, Ji H, von Stechow D, Muller R, Goldring SR, Choi Y, et al., TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol 2001; 159: 1689-99.
6. Li P, Schwarz EM, O'Keefe RJ, Ma L, Boyce BF, Xing L., RANK signaling is not required for TNFalpha-mediated increase in CD11(hi) osteoclast precursors but is essential for mature osteoclast formation in TNFalpha-mediated inflammatory arthritis. J Bone Miner Res 2004; 19: 207-13.
7. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, et al., Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A 1998; 95: 3597-602.
8. Nakagawa N, Kinosaki M, Yamaguchi K, Shima N, Yasuda H, Yano K, et al., RANK is the essential signaling receptor for osteoclast differentiation factor in osteoclastogenesis. Biochem Biophys Res Commun 1998; 253: 395-400.
9. Schett G., Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur J Clin Invest 2011; 41: 1361-6.
10. Okamoto K, Takayanagi H., Osteoclasts in arthritis and Th17 cell development. Int Immunopharmacol 2011; 11: 543-8.
11. Engel P, Gomez-Puerta JA, Ramos-Casals M, Lozano F, Bosch X., Therapeutic targeting of B cells for rheumatic autoimmune diseases. Pharmacol Rev 2011; 63: 127-56.
12. Marston B, Palanichamy A, Anolik JH., B cells in the pathogenesis and treatment of rheumatoid arthritis. Curr Opin Rheumatol 2010; 22: 307-15.
13. Keystone E, Emery P, Peterfy CG, Tak PP, Cohen S, Genovese MC, et al., Rituximab inhibits structural joint damage in patients with rheumatoid arthritis with an inadequate response to tumour necrosis factor inhibitor therapies. Ann Rheum Dis 2009; 68: 216-21.
14. Wheater G, Hogan VE, Teng YK, Tekstra J, Lafeber FP, Huizinga TW, et al., Suppression of bone turnover by B-cell depletion in patients with rheumatoid arthritis. Osteoporos Int 2011; 22: 3067-72.
15. Boumans MJ, Thurlings RM, Yeo L, Scheel-Toellner D, Vos K, Gerlag DM, et al., Rituximab abrogates joint destruction in rheumatoid arthritis by inhibiting osteoclastogenesis. Ann Rheum Dis 2012; 71: 108-13.
16. Harre U, Georgess D, Bang H, Bozec A, Axmann R, Ossipova E, et al., Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 2012; 122: 1791-802.
17. Lund F., Cytokine-producing B lymphocytes: key regulators of immunity. Curr Opin Immunol 2008; 20: 332-8.
18. Anolik JH, Looney RJ, Lund FE, Randall TD, Sanz I., Insights into the heterogeneity of human B cells: diverse functions, roles in autoimmunity, and use as therapeutic targets. Immunol Res 2009; 45: 144-58.
19. Cambridge G, Leandro MJ, Edwards JC, Ehrenstein MR, Salden M, Bodman-Smith M, et al., Serologic changes following B lymphocyte depletion therapy for rheumatoid arthritis. Arthritis Rheum 2003; 48: 2146-54.
20. Bugatti S, Caporali R, Manzo A, Vitolo B, Pitzalis C, Montecucco C., Involvement of subchondral bone marrow in rheumatoid arthritis: lymphoid neogenesis and in situ relationship to subchondral bone marrow osteoclast recruitment. Arthritis Rheum 2005; 52: 3448-59.
21. Ehrhardt GR, Hijikata A, Kitamura H, Ohara O, Wang JY, Cooper MD., Discriminating gene expression profiles of memory B cell subpopulations. J Exp Med 2008; 205: 1807-17.
22. Kawai T, Matsuyama T, Hosokawa Y, Makihira S, Seki M, Karimbux NY, et al., B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 2006; 169: 987-98.
23. Shibata H, Abe M, Hiura K, Wilde J, Moriyama K, Sano T, et al., Malignant B-lymphoid cells with bone lesions express receptor activator of nuclear factor-kappaB ligand and vascular endothelial growth factor to enhance osteoclastogenesis. Clin Cancer Res 2005; 11: 6109-15.
24. Yeo L, Toellner KM, Salmon M, Filer A, Buckley CD, Raza K, et al., Cytokine mRNA profiling identifies B cells as a major source of RANKL in rheumatoid arthritis. Ann Rheum Dis 2011; 70: 2022-8.
25. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al., The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988; 31: 315-24.
26. Anandarajah A, Giampoli E, Thiele R, Monu J, Seo G, Feng C, et al., Rheumatoid arthritis patients in clinical remission manifest persistent joint inflammation on histology and imaging studies. J Rheumatol 2014; 41: 2153-60.
27. Wei C, Anolik J, Cappione A, Zheng B, Pugh-Bernard A, Brooks J, et al., A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol 2007; 178: 6624-33.
28. Palanichamy A, Barnard J, Zheng B, Owen T, Quach T, Wei C, et al., Novel human transitional B cell populations revealed by B cell depletion therapy. J Immunol 2009; 182: 5982-93.
29. 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: 1633-44.
30. Usui M, Xing L, Drissi H, Zuscik M, O'Keefe R, Chen D, et al., Murine and chicken chondrocytes regulate osteoclastogenesis by producing RANKL in response to BMP2. J Bone Miner Res 2008; 23: 314-25.
31. Chiu YG, Shao T, Feng C, Mensah KA, Thullen M, Schwarz EM, et al., CD16 (FcRgammaIII) as a potential marker of osteoclast precursors in psoriatic arthritis. Arthritis Res Ther 2010; 12: R14.
32. Chiu YH, Mensah KA, Schwarz EM, Ju Y, Takahata M, Feng C, et al., Regulation of human osteoclast development by dendritic cell-specific transmembrane protein (DC-STAMP). J Bone Miner Res 2012; 27: 79-92.
33. Adlowitz D, Barnard J, Biear J, Cistrone C, Owen T, Wang W, et al., Expansion of activated memory B cells in RA and impact of B cell depletion therapy. PloS One 2015; 10: e0128269.
34. Vandooren B, Cantaert T, Noordenbos T, Tak PP, Baeten D., The abundant synovial expression of the RANK/RANKL/osteoprotegerin system in peripheral spondylarthritis is partially disconnected from inflammation. Arthritis Rheum 2008; 58: 718-29.
35. Karmakar S, Kay J, Gravallese EM., Bone damage in rheumatoid arthritis: mechanistic insights and approaches to prevention. Rheum Dis Clin North Am 2010; 36: 385-404.
36. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, et al., IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 1999; 103: 1345-52.
37. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, et al., Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999; 402: 304-9.
38. Zhao L, Huang J, Zhang H, Wang Y, Matesic LE, Takahata M, et al., Tumor necrosis factor inhibits mesenchymal stem cell differentiation into osteoblasts via the ubiquitin E3 ligase Wwp1. Stem Cells 2011; 29: 1601-10.
39. Zhang H, Hilton MJ, Anolik JH, Welle SL, Zhao C, Yao Z, et al., NOTCH inhibits osteoblast formation in inflammatory arthritis via noncanonical NF-kappaB. J Clin Invest 2014; 124: 3200-14.
40. Yeo L, Lom H, Juarez M, Snow M, Buckley CD, Filer A, et al., Expression of FcRL4 defines a pro-inflammatory, RANKL-producing B cell subset in rheumatoid arthritis. Ann Rheum Dis 2015; 74: 928-35.
41. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O'Fallon WM, et al., Lymphoid neogenesis in rheumatoid synovitis. J Immunol 2001; 167: 1072-80.
42. Dalbeth N, Smith T, Gray S, Doyle A, Antill P, Lobo M, et al., Cellular characterisation of magnetic resonance imaging bone oedema in rheumatoid arthritis; implications for pathogenesis of erosive disease. Ann Rheum Dis 2009; 68: 279-82.
43. Jimenez-Boj E, Redlich K, Turk B, Hanslik-Schnabel B, Wanivenhaus A, Chott A, et al., Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J Immunol 2005; 175: 2579-88.
44. Gortz B, Hayer S, Redlich K, Zwerina J, Tohidast-Akrad M, Tuerk B, et al., Arthritis induces lymphocytic bone marrow inflammation and endosteal bone formation. J Bone Miner Res 2004; 19: 990-8.
45. Hayer S, Polzer K, Brandl A, Zwerina J, Kireva T, Smolen JS, et al., B-cell infiltrates induce endosteal bone formation in inflammatory arthritis. J Bone Miner Res 2008; 23: 1650-60.
46. Li Y, Toraldo G, Li A, Yang X, Zhang H, Qian WP, et al., B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood 2007; 109: 3839-48.
47. Onal M, Xiong J, Chen X, Thostenson JD, Almeida M, Manolagas SC, et al., Receptor activator of nuclear factor kappaB ligand (RANKL) protein expression by B lymphocytes contributes to ovariectomy-induced bone loss. J Biol Chem 2012; 287: 29851-60.