Proof of concept: Enthesitis and new bone formation in spondyloarthritis are driven by mechanical strain and stromal cells

Annals of the Rheumatic Diseases

Volumn 73, Issue 2, 2014, Pages 437-445

  Jacques, Peggy ^a   Lambrecht, Stijn ^a   Verheugen, Eveline ^a   Pauwels, Elin ^b   Kollias, George ^c   Armaka, Maria ^c   Verhoye, Marleen ^d   Van Der Linden, Annemie ^d   Achten, Rik ^a   Lories, Rik J ^e   Elewaut, Dirk ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^d UNIVERSITY OF ANTWERP   (Belgium)

^e SKELETAL BIOLOGY AND ENGINEERING RESEARCH CENTER   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ACHILLES TENDINITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; B LYMPHOCYTE; BONE STRESS; CONTROLLED STUDY; ENTHESITIS; MECHANICAL STRESS; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; SPONDYLARTHRITIS; STROMA CELL; T LYMPHOCYTE; WEIGHT BEARING;

EID: 84891747499     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2013-203643     Document Type: Article

References (44)

1. Braun J, Bollow M, Remlinger G, et al. Prevalence of spondylarthropathies in HLA-B27 positive and negative blood donors. Arthritis Rheum 1998;41:58-67. (Pubitemid 28041923)
2. Sieper J, Rudwaleit M, Khan MA, et al. Concepts and epidemiology of spondyloarthritis. Best Pract Res Clin Rheumatol 2006;20:401-17. (Pubitemid 43843063)
3. McGonagle D, Gibbon W, Emery P. Classification of inflammatory arthritis by enthesitis. Lancet 1998;352:1137-40. (Pubitemid 28448530)
4. Benjamin M, McGonagle D. The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites. J Anat 2001;199(Pt 5):503-26. (Pubitemid 33094612)
5. Machado P, Landewe R, Braun J, et al. Both structural damage and inflammation of the spine contribute to impairment of spinal mobility in patients with ankylosing spondylitis. Ann Rheum Dis 2010;69:1465-70.
6. McGonagle D, Stockwin L, Isaacs J, et al. An enthesitis based model for the pathogenesis of spondyloarthropathy additive effects of microbial adjuvant and biomechanical factors at disease sites. J Rheumatol 2001;28:2155-9. (Pubitemid 32947855)
7. McGonagle D, Lories RJ, Tan AL, et al. The concept of a "synovio-entheseal complex" and its implications for understanding joint inflammation and damage in psoriatic arthritis and beyond. Arthritis Rheum 2007;56:2482-91. (Pubitemid 47237267)
8. McGonagle D, Wakefield RJ, Tan AL, et al. Distinct topography of erosion and new bone formation in achilles tendon enthesitis: implications for understanding the link between inflammation and bone formation in spondylarthritis. Arthritis Rheum 2008;58:2694-9.
9. Van Der Heijde D, Salonen D, Weissman BN, et al. Assessment of radiographic progression in the spines of patients with ankylosing spondylitis treated with adalimumab for up to 2 years. Arthritis Res Ther 2009;11:R127.
10. Van Der Heijde D, Landewe R, Baraliakos X, et al. Radiographic findings following two years of infliximab therapy in patients with ankylosing spondylitis. Arthritis Rheum 2008;58:3063-70.
11. Van Der Heijde D, Landewe R, Einstein S, et al. Radiographic progression of ankylosing spondylitis after up to two years of treatment with etanercept. Arthritis Rheum 2008;58:1324-31. (Pubitemid 351705922)
12. Kontoyiannis D, Pasparakis M, Pizarro TT, et al. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 1999;10:387-98. (Pubitemid 29165293)
13. Armaka M, Apostolaki M, Jacques P, et al. Mesenchymal cell targeting by TNF as a common pathogenic principle in chronic inflammatory joint and intestinal diseases. J Exp Med 2008;205:331-7. (Pubitemid 351281599)
14. Jacques P, Venken K, Van Beneden K, et al. Invariant natural killer T cells are natural regulators of murine spondylarthritis. Arthritis Rheum 2010;62:988-99.
15. Parker DL. Optimal short scan convolution reconstruction for Fanbeam Ct. Med Phys 1982;9:254-7. (Pubitemid 12149642)
16. Masschaele BC, Cnudde V, Dierick M, et al. UGCT: new x-ray radiography and tomography facility. Nucl Instrum Meth A 2007;580:266-9. (Pubitemid 47331850)
17. Vlassenbroeck J, Dierick M, Masschaele B, et al. Software tools for quantification of X-ray microtomography. Nucl Instrum Meth A 2007;580:442-5. (Pubitemid 47331844)
18. Proulx ST, Kwok E, You Z, et al. Elucidating bone marrow edema and myelopoiesis in murine arthritis using contrast-enhanced magnetic resonance imaging. Arthritis Rheum 2008;58:2019-29. (Pubitemid 351988094)
19. Sherlock JP, Joyce-Shaikh B, Turner SP, et al. IL-23 induces spondyloarthropathy by acting on ROR-gammat+ CD3+CD4-CD8-entheseal resident T cells. Nat Med 2012;18:1069-76.
20. Morey-Holton ER, Globus RK. Hindlimb unloading of growing rats: a model for predicting skeletal changes during space flight. Bone 1998;22(5 Suppl):83S-8S. (Pubitemid 28223261)
21. Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol 2002;92:1367-77. (Pubitemid 34670888)
22. Cornelissen J, Armstrong J, Holt CM. Mechanical stretch induces phosphorylation of p38-MAPK and apoptosis in human saphenous vein. Arterioscler Thromb Vasc Biol 2004;24:451-6. (Pubitemid 38326137)
23. Correa-Meyer E, Pesce L, Guerrero C, et al. Cyclic stretch activates ERK1/2 via G proteins and EGFR in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002;282:L883-91. (Pubitemid 34654602)
24. Lal H, Verma SK, Smith M, et al. Stretch-induced MAP kinase activation in cardiac myocytes: differential regulation through beta1-integrin and focal adhesion kinase. J Mol Cell Cardiol 2007;43:137-47. (Pubitemid 47069384)
25. Papakrivopoulou J, Lindahl GE, Bishop JE, et al. Differential roles of extracellular signal-regulated kinase 1/2 and p38MAPK in mechanical load-induced procollagen alpha1 (I) gene expression in cardiac fibroblasts. Cardiovasc Res 2004;61:736-44. (Pubitemid 38249472)
26. Alessi DR, Cuenda A, Cohen P, et al. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem 1995;270:27489-94.
27. Cuenda A, Rouse J, Doza YN, et al. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS letters 1995;364:229-33.
28. Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007;13:156-63.
29. 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;304:126-36. (Pubitemid 41262227)
30. Nandakumar KS, Andren M, Martinsson P, et al. Induction of arthritis by single monoclonal IgG anti-collagen type II antibodies and enhancement of arthritis in mice lacking inhibitory FcgammaRIIB. Eur J Immunol 2003;33:2269-77. (Pubitemid 37010045)
31. Pauwels E, Van Loo D, Cornillie P, et al. An exploratory study of contrast agents for soft tissue visualization by means of high resolution X-ray computed tomography imaging. J Microsc 2013;250:21-31.
32. Ward MM, Reveille JD, Learch TJ, et al. Occupational physical activities and longterm functional and radiographic outcomes in patients with ankylosing spondylitis. Arthritis Rheum 2008;59:822-32. (Pubitemid 351847565)
33. Knies Y, Bernd A, Kaufmann R, et al. Mechanical stretch induces clustering of beta1-integrins and facilitates adhesion. Exp Dermatol 2006;15:347-55. (Pubitemid 44056481)
34. Thiel MJ, Schaefer CJ, Lesch ME, et al. Central role of the MEK/ERK MAP kinase pathway in a mouse model of rheumatoid arthritis: potential proinflammatory mechanisms. Arthritis Rheum 2007;56:3347-57. (Pubitemid 47585429)
35. Mihara K, Almansa C, Smeets RL, et al. A potent and selective p38 inhibitor protects against bone damage in murine collagen-induced arthritis: a comparison with neutralization of mouse TNFalpha. Br J Pharmacol 2008;154:153-64. (Pubitemid 351620394)
36. Schett G, Tohidast-Akrad M, Smolen JS, et al. Activation, differential localization, and regulation of the stress-activated protein kinases, extracellular signal-regulated kinase, c-JUN N-terminal kinase, and p38 mitogen-activated protein kinase, in synovial tissue and cells in rheumatoid arthritis. Arthritis Rheum 2000;43:2501-12.
37. Skinner SJ, Deleault KM, Fecteau R, et al. Extracellular signal-regulated kinase regulation of tumor necrosis factor-alpha mRNA nucleocytoplasmic transport requires TAP-NxT1 binding and the AU-rich element. J Biol Chem 2008;283:3191-9.
38. Braem K, Luyten FP, Lories RJ. Blocking p38 signalling inhibits chondrogenesis in vitro but not ankylosis in a model of ankylosing spondylitis in vivo. Ann Rheum Dis 2012;71:722-8.
39. Baraliakos X, Haibel H, Listing J, et al. Continuous long-term anti-TNF therapy does not lead to an increase in the rate of new bone formation over 8 years in patients with ankylosing spondylitis. Ann Rheum Dis Published Online First: 27 Mar. 2013. doi:10.1136/annrheumdis-2012-202698.
40. Haroon N, Inman RD, Learch TJ, et al. The impact of TNF-inhibitors on radiographic progression in ankylosing spondylitis. Arthritis Rheum Published Online First: 1 Jul. 2013. doi:10.1002/art.38070. ACR abstract 782. 2012.
41. Van Der Heijde D, Machado P, Braun J, et al. MRI inflammation at the vertebral unit only marginally predicts new syndesmophyte formation: a multilevel analysis in patients with ankylosing spondylitis. Ann Rheum Dis 2012;71:369-73.
42. Maksymowych WP, Chiowchanwisawakit P, Clare T, et al. Inflammatory lesions of the spine on magnetic resonance imaging predict the development of new syndesmophytes in ankylosing spondylitis: evidence of a relationship between inflammation and new bone formation. Arthritis Rheum 2009;60:93-102.
43. Maksymowych WP, Morency N, Conner-Spady B, et al. Suppression of inflammation and effects on new bone formation in ankylosing spondylitis: evidence for a window of opportunity in disease modification. Ann Rheum Dis 2013;72:23-8.
44. Chiowchanwisawakit P, Lambert RG, Conner-Spady B, et al. Focal fat lesions at vertebral corners on magnetic resonance imaging predict the development of new syndesmophytes in ankylosing spondylitis. Arthritis Rheum 2011;63:2215-25.