Involvement of subchondral bone marrow in rheumatoid arthritis: Lymphoid neogenesis and in situ relationship to subchondral bone marrow osteoclast recruitment

Arthritis and Rheumatism

Volumn 52, Issue 11, 2005, Pages 3448-3459

  Bugatti, Serena ^a   Caporali, Roberto ^a   Manzo, Antonio ^b   Vitolo, Barbara ^a   Pitzalis, Costantino ^b   Montecucco, Carlomaurizio ^a,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ADDRESSIN; CATHEPSIN K; CHEMOKINE; COMPLEMENT COMPONENT C3D RECEPTOR; CXCL13 CHEMOKINE; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; BONE MARROW; BONE TISSUE; CELL AGGREGATION; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIAL VENULE; FEMALE; FOLLICULAR DENDRITIC CELL; HISTOGENESIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFLAMMATION; INFLAMMATORY INFILTRATE; JOINT SURGERY; LYMPH NODE; LYMPHOID NEOGENESIS; MALE; OSTEOCLAST; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SUBCHONDRAL BONE MARROW; SYNOVIUM; T LYMPHOCYTE; VENULE;

ADULT; AGED; ARTHRITIS, RHEUMATOID; BIOLOGICAL MARKERS; BONE MARROW CELLS; BONE RESORPTION; CHEMOKINES, CC; CHEMOKINES, CXC; FEMALE; HUMANS; IN SITU HYBRIDIZATION; MALE; MIDDLE AGED; OSTEOARTHRITIS, HIP; OSTEOCLASTS; SYNOVIAL MEMBRANE;

EID: 27744515760     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.21377     Document Type: Article

References (48)

1. Conaghan PG, Green MJ, Emery P. Established rheumatoid arthritis. Baillieres Best Pract Res Clin Rheumatol 1999;13:561-75.
2. Gravallese EM, 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.
3. 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.
4. Romas E, Bakharevski O. Hards DK, Kartsogiannis V, Quinn JM, Ryan PF, et al. Expression of osteoclast differentiation factor at sites of bone erosion in collagen-induced arthritis. Arthritis Rheum 2000;43:821-6.
5. Shigeyama Y, Pap T, Kunzler P, Simmen BR, Gay RE, Gay S. Expression of osteoclast differentiation factor in rheumatoid arthritis. Arthritis Rheum 2000;43:2523-30.
6. Takayanagi H, Iizuka H, Juji T, Nakagawa T, Yamamoto A, Miyazaki T, et al. Involvement of receptor activator of nuclear factor κB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum 2000;43:259-69.
7. Tak PP, Bresnihan B. The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis [review]. Arthritis Rheum 2000;43:2619-33.
8. Klimiuk PA, Sierakowski S, Latosiewicz R, Cylwik JP, Cylwik B, Skowronski J, et al. Circulating tumour necrosis factor α and soluble tumour necrosis factor receptors in patients with different patterns of rheumatoid synovitis. Ann Rheum Dis 2003;62:472-5.
9. Yanni G, Whelan A, Feighery C, Quinlan W, Symons J, Duff G, et al. Contrasting levels of in vitro cytokine production by rheumatoid synovial tissues demonstrating different patterns of mononuclear cell infiltration. Clin Exp Immunol 1993;93:387-95.
10. Klimiuk PA, Goronzy JJ. Bjornsson J, Beckenbaugh RD, Weyand CM. Tissue cytokine patterns distinguish variants of rheumatoid synovitis. Am J Pathol 1997;151:1311-9.
11. Rho J, Takami M, Choi Y. Osteoimmunology: interactions of the immune and skeletal systems. Mol Cells 2004;17:1-9.
12. 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.
13. Kotake S, Udagawa N, Hakoda M, Mogi M, Yano K, Tsuda E, et al. Activated human T cells directly induce osteoclastogenesis from human monocytes: possible role of T cells in bone destruction in rheumatoid arthritis patients. Arthritis Rheum 2001;44:1003-12.
14. Kirwan JR. The relationship between synovitis and erosions in rheumatoid arthritis. Br J Rheumatol 1997;36:225-8.
15. Fujii K, Tsuji M, Tajima M. Rheumatoid arthritis: a synovial disease? Ann Rheum Dis 1999;58:727-30.
16. McQueen FM, Stewart N, Crabbe J, Robinson E, Yeoman S, Tan PL, et al. Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals progression of erosions despite clinical improvement. Ann Rheum Dis 1999;58:156-63.
17. Han S, Cao S, Bheekha-Escura R, Zheng B. Germinal center reaction in the joints of mice with collagen-induced arthritis: an animal model of lymphocyte activation and differentiation in arthritic joints. Arthritis Rheum 2001;44:1438-43.
18. 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.
19. Conaghan PG, O'Connor P, McGonagle D, Astin P, Wakefield RJ, Gibbon WW, et al. Elucidation of the relationship between synovitis and bone damage: a randomized magnetic resonance imaging study of individual joints in patients with early rheumatoid arthritis. Arthritis Rheum 2003;48:64-71.
20. McQueen FM, Benton N, Perry D, Crabbe D, Robinson E, Yeoman S, et al. Bone edema scored on magnetic resonance imaging scans of the dominant carpus at presentation predicts radiographic joint damage of the hands and feet six years later in patients with rheumatoid arthritis. Arthritis Rheum 2003;48:1814-27.
21. Bromley M, Woolley DE. Chondroclasts and osteoclasts at subchondral sites of erosion in the rheumatoid joint. Arthritis Rheum 1984;27:968-75.
22. Wyllie JC. Histopathology of the subchondral bone lesion in rheumatoid arthritis. J Rheumatol Suppl 1983;11:26-8.
23. Watson WC, Tooms RE, Carnesale PG, Dutkowsky JP. A case of germinal center formation by CD45RO T and CD20 B lymphocytes in rheumatoid arthritic subchondral bone: proposal for a two-compartment model of immune-mediated disease with implications for immunotherapeutic strategies. Clin Immunol Immunopathol 1994;73:27-37.
24. O'Connell JX, Nielsen GP, Rosenberg AE. Subchondral acute inflammation in severe arthritis: a sterile osteomyelitis? Am J Surg Pathol 1999;23:192-7.
25. Kaneko M, Tomita T, Nakase T, Ohsawa Y, Seki H, Takeuchi E, et al. Expression of proteinases and inflammatory cytokines in subchondral bone regions in the destructive joint of rheumatoid arthritis. Rheumatology (Oxford) 2001;40:247-55.
26. Cyster J. Chemokines and cell migration in secondary lymphoid organs. Science 1999;286:2098-102.
27. Manzo A, Caporali R, Montecucco C, Pitzalis C. Role of chemokines and chemokine receptors in regulating specific leukocyte trafficking in the immune/inflammatory response. Clin Exp Rheumatol 2003;21:501-8.
28. 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.
29. Mazzucchelli L, Blaser A, Kappeler A, Scharli P, Laissue JA, Baggiolini M, et al. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J Clin Invest 1999;104:R49-54.
30. Bendele A, McAbee T, Sennello G, Frazier J, Chlipala E, McCabe D. Efficacy of sustained blood levels of interleukin-1 receptor antagonist in animal models of arthritis: comparison of efficacy in animal models with human clinical data. Arthritis Rheum 1999;42:498-506.
31. Wagner UG, Kurtin PJ, Wahner A, Brackertz M, Berry DJ, Goronzy JJ, et al. The role of CD8+ CD40L+ T cells in the formation of germinal centres in rheumatoid synovitis. J Immunol 1998;16:6390-7.
32. Manzo A, Paoletti S, Carulli M, Blades MC, Barone F, Yanni G, et al. Systematic microanatomical analysis of CXCL13 and CCL21 in situ production and progressive lymphoid organization in rheumatoid synovitis. Eur J Immunol 2005;35:1347-59.
33. Koenig H, Lucas D, Meissner R. The wrist: a preliminary report on high-resolution MR imaging. Radiology 1986;160:463-7.
34. Lisignoli G, Toneguzzi S, Pozzi C, Piacentini A, Riccio M, Ferruzzi A, et al. Proinflammatory cytokines and chemokine production and expression by human osteoblasts isolated from patients with rheumatoid arthritis and osteoarthritis. J Rheumatol 1999:26:791-9.
35. Lisignoli G, Toneguzzi S, Pozzi C, Piacentini A, Grassi F, Ferruzzi A, et al. Chemokine expression by subchondral bone marrow stromal cells isolated from osteoarthritis and rheumatoid arthritis patients. Clin Exp Immunol 1999;116:371-8.
36. Lisignoli G, Toneguzzi S, Grassi F, Piacentini A, Tschon M, Cristino S, et al. Different chemokines are expressed in human arthritic bone biopsies: IFN-γ and IL-6 differently modulate IL-8, MCP-1 and RANTES production by arthritic osteoblasts. Cytokine 2002;20:231-8.
37. Hamilton JA. Rheumatoid arthritis: opposing actions of haemopoietic growth factors and slow-acting anti-rheumatic drugs. Lancet 1993;342:536-9.
38. Hamilton JA. GM-CSF in inflammation and autoimmunity. Trends Immunol 2002;23:403-8.
39. 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.
40. Marinova-Mutafchieva L, Williams RO, Funa K, Maini RN, Zvaifler NJ. Inflammation is preceded by tumor necrosis factor-dependent infiltration of mesenchymal cells in experimental arthritis. Arthritis Rheum 2002;46:507-13.
41. Hjelmstrom P. Lymphoid neogenesis: de novo formation of lymphoid tissue in chronic inflammation through expression of homing chemokines. J Leukoc Biol 2001;69:331-9.
42. Buckley CD. Michael Mason prize essay 2003: why do leucocytes accumulate within chronically inflamed joints? Rheumatology (Oxford) 2003;42:1433-44.
43. Bromeley M, Bertfield H, Evanson JM, Woolley DE. Bidirectional erosion of cartilage in the rheumatoid knee joint. Ann Rheum Dis 1985;44:676-81.
44. Bossard MJ, Tomaszek TA, Thompson SK, Amegadzie BY, Hanning CR, Jones C, et al. Proteolytic activity of human osteoclast cathepsin K: expression, purification, activation, and substrate identification. J Biol Chem 1996;271:12517-24.
45. Sharp JT, van der Heijde D, Boers M, Boonen A, Bruynesteyn K, Emery P, et al. Repair of erosions in rheumatoid arthritis does occur: results from 2 studies by the OMERACT Subcommittee on Healing of Erosions. J Rheumatol 2003;30:1102-7.
46. Martin JT, Sims NA. Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 2005:11:76-81.
47. Rifas L, Arackal S, Neale Weitzmann M. Inflammatory T cells rapidly induce differentiation of human bone marrow stromal cells into mature osteoblasts. J Cell Biochem 2003;88:650-9.
48. Lisignoli G, Toneguzzi S, Piacentini A, Cattini L, Lend A, Tschon M, et al. Human osteoblasts express functional CXC chemokine receptors 3 and 5: activation by their ligands, CXCLlO and CXCL13. significantly induces alkaline phosphatase and β-N-acetylhexosaminidase release. J Cell Physiol 2002;194:71-9.