Crosstalk between cartilage and bone: When bone cytokines matter

Cytokine and Growth Factor Reviews

Volumn 22, Issue 2, 2011, Pages 91-97

  Funck Brentano, Thomas ^a   Cohen Solal, Martine ^a  

^a INSERM   (France)

Author keywords

Bone; Cartilage; Osteoarthritis; Osteoprotegerin; Wnt signaling

Indexed keywords

BETA CATENIN; CATHEPSIN K; CELECOXIB; COLLAGEN TYPE 1; COLLAGEN TYPE 2; DICKKOPF 1 PROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PARATHYROID HORMONE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; WNT PROTEIN;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; BIOMECHANICS; BONE; BONE CELL; BONE DENSITY; BONE LESION; BONE MINERALIZATION; BONE PLATE; BONE REMODELING; BONE STRUCTURE; CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CATABOLISM; CELL DIFFERENTIATION; CHONDROGENESIS; CYTOKINE RELEASE; DRUG TARGETING; HUMAN; MECHANICAL STRESS; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; NONHUMAN; ONSET AGE; OSTEOARTHRITIS; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; TRABECULAR BONE;

ANIMALS; BONE AND BONES; BONE REMODELING; CARTILAGE; CHONDROCYTES; CYTOKINES; HUMANS; OSTEOARTHRITIS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 79957769594     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2011.04.003     Document Type: Review

References (90)

1. Radin E.L., Rose R.M. Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 1986, 213:34-40.
2. Radin E.L., Paul I.L., Tolkoff M.J. Subchondral bone changes in patients with early degenerative joint disease. Arthritis Rheum 1970, 13:400-405.
3. Sambrook P., Naganathan V. What is the relationship between osteoarthritis and osteoporosis?. Baillieres Clin Rheumatol 1997, 11:695-710.
4. Dequeker J., Aerssens J., Luyten F.P. Osteoarthritis and osteoporosis: clinical and research evidence of inverse relationship. Aging Clin Exp Res 2003, 15:426-439.
5. Franklin J., Englund M., Ingvarsson T., Lohmander S. The association between hip fracture and hip osteoarthritis: a case-control study. BMC Musculoskelet Disord England 2010, 26:274.
6. Brandt K.D., Dieppe P., Radin E. Etiopathogenesis of osteoarthritis. Med Clin North Am 2009, 93:1-24. xv.
7. Burr D.B. Anatomy and physiology of the mineralized tissues: role in the pathogenesis of osteoarthrosis. Osteoarthritis Cartilage 2004, 12(Suppl. A):S20-S30.
8. Brown T.D., Radin E.L., Martin R.B., Burr D.B. Finite element studies of some juxtarticular stress changes due to localized subchondral stiffening. J Biomech 1984, 17:11-24.
9. Lajeunesse D., Reboul P. Subchondral bone in osteoarthritis: a biologic link with articular cartilage leading to abnormal remodeling. Curr Opin Rheumatol 2003, 15:628-633.
10. Sharma L. Local factors in osteoarthritis. Curr Opin Rheumatol 2001, 13:441-446.
11. Goldring M.B., Goldring S.R. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann N Y Acad Sci 2010, 1192:230-237.
12. Li B., Aspden R.M. Material properties of bone from the femoral neck and calcar femorale of patients with osteoporosis or osteoarthritis. Osteoporos Int 1997, 7:450-456.
13. Karvonen R.L., Miller P.R., Nelson D.A., Granda J.L., Fernandez-Madrid F. Periarticular osteoporosis in osteoarthritis of the knee. J Rheumatol 1998, 25:2187-2194.
14. Blair-Levy J.M., Watts C.E., Fiorentino N.M., Dimitriadis E.K., Marini J.C., Lipsky P.E. A type I collagen defect leads to rapidly progressive osteoarthritis in a mouse model. Arthritis Rheum 2008, 58:1096-1106.
15. Wluka A.E., Hanna F., Davies-Tuck M., Wang Y., Bell R.J., Davis S.R., et al. Bone marrow lesions predict increase in knee cartilage defects and loss of cartilage volume in middle-aged women without knee pain over 2 years. Ann Rheum Dis 2009, 68:850-855.
16. Crema M.D., Roemer F.W., Zhu Y., Marra M.D., Niu J., Zhang Y., et al. Radiology 2010, 256(3):855-862.
17. Roemer F.W., Neogi T., Nevitt M.C., Felson D.T., Zhu Y., Zhang Y., et al. Subchondral bone marrow lesions are highly associated with, and predict subchondral bone attrition longitudinally: the MOST study. Osteoarthritis Cartilage 2010, 18(1):47-53.
18. Hunter D.J., Felson D.T. Osteoarthritis. BMJ 2006, 332:639-642.
19. Javaid M.K., Lynch J.A., Tolstykh I., Guermazi A., Roemer F., Aliabadi P., et al. Pre-radiographic MRI findings are associated with onset of knee symptoms: the most study. Osteoarthritis Cartilage 2010, 18:323-328.
20. Roemer F.W., Frobell R., Hunter D.J., Crema M.D., Fischer W., Bohndorf K., et al. MRI-detected subchondral bone marrow signal alterations of the knee joint: terminology, imaging appearance, relevance and radiological differential diagnosis. Osteoarthritis Cartilage 2009, 17:1115-1131.
21. Beuf O., Ghosh S., Newitt D.C., Link T.M., Steinbach L., Ries M., et al. Magnetic resonance imaging of normal and osteoarthritic trabecular bone structure in the human knee. Arthritis Rheum 2002, 46:385-393.
22. Day J.S., Ding M., van der Linden J.C., Hvid I., Sumner D.R., Weinans H. A decreased subchondral trabecular bone tissue elastic modulus is associated with pre-arthritic cartilage damage. J Orthop Res 2001, 19:914-918.
23. Kamibayashi L., Wyss U.P., Cooke T.D., Zee B. Trabecular microstructure in the medial condyle of the proximal tibia of patients with knee osteoarthritis. Bone 1995, 17:27-35.
24. Bobinac D., Spanjol J., Zoricic S., Maric I. Changes in articular cartilage and subchondral bone histomorphometry in osteoarthritic knee joints in humans. Bone 2003, 32:284-290.
25. Ding M., Odgaard A., Hvid I. Changes in the three-dimensional microstructure of human tibial cancellous bone in early osteoarthritis. J Bone Joint Surg Br 2003, 85:906-912.
26. Ding M., Danielsen C.C., Hvid I. Age-related three-dimensional microarchitectural adaptations of subchondral bone tissues in guinea pig primary osteoarthrosis. Calcif Tissue Int 2006, 78:113-122.
27. Pelletier J.P., Boileau C., Brunet J., Boily M., Lajeunesse D., Reboul P. The inhibition of subchondral bone resorption in the early phase of experimental dog osteoarthritis by licofelone is associated with a reduction in the synthesis of MMP-13 and cathepsin K. Bone 2004, 34:527-538.
28. Boyd S.K., Matyas J.R., Wohl G.R., Kantzas A., Zernicke R.F. Early regional adaptation of periarticular bone mineral density after anterior cruciate ligament injury. J Appl Physiol 2000, 89:2359-2364.
29. Boyd S.K., Muller R., Zernicke R.F. Mechanical and architectural bone adaptation in early stage experimental osteoarthritis. J Bone Miner Res 2002, 17:687-694.
30. Hayami T., Pickarski M., Wesolowski G.A., McLane J., Bone A., Destefano J. The role of subchondral bone remodeling in osteoarthritis: reduction of cartilage degeneration and prevention of osteophyte formation by alendronate in the rat anterior cruciate ligament transection model. Arthritis Rheum 2004, 50:1193-1206.
31. Hayami T., Pickarski M., Zhuo Y., Wesolowski G.A., Rodan G.A., Duong le T. Characterization of articular cartilage and subchondral bone changes in the rat anterior cruciate ligament transection and meniscectomized models of osteoarthritis. Bone 2006, 38:234-243.
32. Kamekura S., Hoshi K., Shimoaka T., Chung U., Chikuda H., Yamada T. Osteoarthritis development in novel experimental mouse models induced by knee joint instability. Osteoarthritis Cartilage 2005, 13:632-641.
33. Kadri A., Ea H., Bazille C., Hannouche D., Lioté F., Cohen-Solal M. Osteoprotegerin inhibits cartilage degradation through an effect on trabecular bone in murine experimental osteoarthritis. Arthritis Rheum 2008, 58:2379-2386.
34. Kadri A., Funck-Brentano T., Lin H., et al. Inhibition of bone resorption blunts osteoarthritis in mice with high bone remodelling. Ann Rheum Dis 2010, 69(8):1533-1538.
35. Bingham C.O., Buckland-Wright J.C., Garnero P., Cohen S.B., Dougados M., Adami S. Risedronate decreases biochemical markers of cartilage degradation but does not decrease symptoms or slow radiographic progression in patients with medial compartment osteoarthritis of the knee: results of the two-year multinational knee osteoarthritis structural arthritis study. Arthritis Rheum 2006, 54:3494-3507.
36. Garnero P., Aronstein W.S., Cohen S.B., Conaghan P.G., Cline G.A., Christiansen C. Relationships between biochemical markers of bone and cartilage degradation with radiological progression in patients with knee osteoarthritis receiving risedronate: the Knee Osteoarthritis Structural Arthritis randomized clinical trial. Osteoarthritis Cartilage 2008, 16:660-666.
37. Seibel M.J., Duncan A., Robins S.P. Urinary hydroxy-pyridinium crosslinks provide indices of cartilage and bone involvement in arthritic diseases. J Rheumatol 1989, 16:964-970.
38. Bettica P., Cline G., Hart D.J., Meyer J., Spector T.D. Evidence for increased bone resorption in patients with progressive knee osteoarthritis: longitudinal results from the Chingford study. Arthritis Rheum 2002, 46:3178-3184.
39. Botter S.M., van Osch G.J., Waarsing J.H., Day J.S., Verhaar J.A., Pols H.A. Quantification of subchondral bone changes in a murine osteoarthritis model using micro-CT. Biorheology 2006, 43:379-388.
40. Hilal G., Martel-Pelletier J., Pelletier J.P., Ranger P., Lajeunesse D. Osteoblast-like cells from human subchondral osteoarthritic bone demonstrate an altered phenotype in vitro: possible role in subchondral bone sclerosis. Arthritis Rheum 1998, 41:891-899.
41. Massicotte F., Aubry I., Martel-Pelletier J., Pelletier J.P., Fernandes J., Lajeunesse D. Abnormal insulin-like growth factor 1 signaling in human osteoarthritic subchondral bone osteoblasts. Arthritis Res Ther 2006, 8:R177.
42. Mansell J.P., Bailey A.J. Abnormal cancellous bone collagen metabolism in osteoarthritis. J Clin Invest 1998, 101:1596-1603.
43. Bailey A.J., Sims T.J., Knott L. Phenotypic expression of osteoblast collagen in osteoarthritic bone: production of type I homotrimer. Int J Biochem Cell Biol 2002, 34:176-182.
44. Bailey A.J., Mansell J.P., Sims T.J., Banse X. Biochemical and mechanical properties of subchondral bone in osteoarthritis. Biorheology 2004, 41:349-358.
45. Massicotte F., Lajeunesse D., Benderdour M., Pelletier J.P., Hilal G., Duval N. Can altered production of interleukin-1beta, interleukin-6, transforming growth factor-beta and prostaglandin E(2) by isolated human subchondral osteoblasts identify two subgroups of osteoarthritic patients. Osteoarthritis Cartilage 2002, 10:491-500.
46. Serra R., Johnson M., Filvaroff E.H., LaBorde J., Sheehan D.M., Derynck R. Expression of a truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol 1997, 139:541-552.
47. Glover S.J., Eastell R., McCloskey E.V., Rogers A., Garnero P., Lowery J. Rapid and robust response of biochemical markers of bone formation to teriparatide therapy. Bone 2009, 45:1053-1058.
48. Miao D., He B., Karaplis A.C., Goltzman D. Parathyroid hormone is essential for normal fetal bone formation. J Clin Invest 2002, 109:1173-1182.
49. Greenfield E.M., Horowitz M.C., Lavish S.A. Stimulation by parathyroid hormone of interleukin-6 and leukemia inhibitory factor expression in osteoblasts is an immediate-early gene response induced by cAMP signal transduction. J Biol Chem 1996, 271:10984-10989.
50. Palmqvist P., Persson E., Conaway H.H., Lerner U.H. IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-kappa B ligand, osteoprotegerin, and receptor activator of NF-kappa B in mouse calvariae. J Immunol 2002, 169:3353-3362.
51. Lee M., Partridge N.C. Parathyroid hormone signaling in bone and kidney. Curr Opin Nephrol Hypertens 2009, 18:298-302.
52. Jilka R.L., O'Brien C.A., Bartell S.M., Weinstein R.S., Manolagas S.C. Continuous elevation of PTH increases the number of osteoblasts via both osteoclast-dependent and -independent mechanisms. J Bone Miner Res 2010, 25:2427-2437.
53. Hilal G., Massicotte F., Martel-Pelletier J., Fernandes J.C., Pelletier J.P., Lajeunesse D. Endogenous prostaglandin E2 and insulin-like growth factor 1 can modulate the levels of parathyroid hormone receptor in human osteoarthritic osteoblasts. J Bone Miner Res 2001, 16:713-721.
54. Gaissmaier C., Koh J.L., Weise K. Growth and differentiation factors for cartilage healing and repair. Injury Netherlands 2008, S88-S96.
55. Chang J.K., Chang L.H., Hung S.H., Wu S.C., Lee H.Y., Lin Y.S. Parathyroid hormone 1-34 inhibits terminal differentiation of human articular chondrocytes and osteoarthritis progression in rats. Arthritis Rheum 2009, 60:3049-3060.
56. Webb G.R., Westacott C.I., Elson C.J. Osteoarthritic synovial fluid and synovium supernatants up-regulate tumor necrosis factor receptors on human articular chondrocytes. Osteoarthritis Cartilage 1998, 6:167-176.
57. Sanchez C., Deberg M., Piccardi N., Msika P., Reginster J., Henrotin Y. Subchondral bone osteoblasts induce phenotypic changes in human osteoarthritic chondrocytes. Osteoarthritis Cartilage 2005, 13:988-997.
58. Sanchez C., Deberg M., Piccardi N., Msika P., Reginster J., Henrotin Y. Osteoblasts from the sclerotic subchondral bone downregulate aggrecan but upregulate metalloproteinases expression by chondrocytes. This effect is mimicked by interleukin-6, -1beta and oncostatin M pre-treated non-sclerotic osteoblasts. Osteoarthritis Cartilage 2005, 13:979-987.
59. Dreier R., Wallace S., Fuchs S., Bruckner P., Grassel S. Paracrine interactions of chondrocytes and macrophages in cartilage degradation: articular chondrocytes provide factors that activate macrophage-derived pro-gelatinase B (pro-MMP-9). J Cell Sci 2001, 114:3813-3822.
60. Kwan Tat S., Amiable N., Pelletier J.P., Boileau C., Lajeunesse D., Duval N. Modulation of OPG, RANK and RANKL by human chondrocytes and their implication during osteoarthritis. Rheumatology (Oxford) 2009, 48:1482-1490.
61. Kwan Tat S., Pelletier J.P., Lajeunesse D., Fahmi H., Lavigne M., Martel-Pelletier J. The differential expression of osteoprotegerin (OPG) and receptor activator of nuclear factor kappaB ligand (RANKL) in human osteoarthritic subchondral bone osteoblasts is an indicator of the metabolic state of these disease cells. Clin Exp Rheumatol 2008, 26:295-304.
62. Jiao K., Niu L.N., Wang M.Q., Dai J., Yu S.B., Liu X.D. Subchondral bone loss following orthodontically induced cartilage degradation in the mandibular condyles of rats. Bone 2011, 48:362-371.
63. Bellido M., Lugo L., Roman-Blas J.A., Castañeda S., Caeiro J.R., Dapia S. Subchondral bone microstructural damage by increased remodelling aggravates experimental osteoarthritis preceded by osteoporosis. Arthritis Res Ther 2010, 12:R152.
64. Moreno-Rubio J., Herrero-Beaumont G., Tardio L., Alvarez-Soria M.A., Largo R. Nonsteroidal antiinflammatory drugs and prostaglandin E(2) modulate the synthesis of osteoprotegerin and RANKL in the cartilage of patients with severe knee osteoarthritis. Arthritis Rheum 2010, 62:478-488.
65. Shimizu S., Asou Y., Itoh S., Chung U.I., Kawaguchi H., Shinomiya K. Prevention of cartilage destruction with intraarticular osteoclastogenesis inhibitory factor/osteoprotegerin in a murine model of osteoarthritis. Arthritis Rheum 2007, 56:3358-3365.
66. Vik A., Mathiesen E.B., Brox J., Wilsgaard T., Njølstad I., Jørgensen L. Relation between serum osteoprotegerin and carotid intima media thickness in a general population - the Tromsø Study. J Thromb Haemost 2010, 8:2133-2139.
67. Benslimane-Ahmim Z., Heymann D., Dizier B., Lokajczyk A., Brion R., Laurendeau I. Osteoprotegerin, a new actor in vasculogenesis, stimulates endothelial colony-forming cells properties. J Thromb Haemost 2011, 9(4).
68. Kafienah W., Bromme D., Buttle D.J., Croucher L.J., Hollander A.P. Human cathepsin K cleaves native type I and II collagens at the N-terminal end of the triple helix. Biochem J 1998, 331(Pt 3):727-732.
69. Konttinen Y.T., Mandelin J., Li T.F., Salo J., Lassus J., Liljeström M. Acidic cysteine endoproteinase cathepsin K in the degeneration of the superficial articular hyaline cartilage in osteoarthritis. Arthritis Rheum 2002, 46:953-960.
70. Moreau M., Boileau C., Martel-Pelletier J., Brunet J., Laufer S., Pelletier J.P. Licofelone reduces progression of structural changes in a canine model of osteoarthritis under curative conditions: effect on protease expression and activity. J Rheumatol 2006, 33:1176-1183.
71. Morko J.P., Soderstrom M., Saamanen A.M., Salminen H.J., Vuorio E.I. Up regulation of cathepsin K expression in articular chondrocytes in a transgenic mouse model for osteoarthritis. Ann Rheum Dis 2004, 63:649-655.
72. Morko J., Kiviranta R., Joronen K., Saamanen A.M., Vuorio E., Salminen-Mankonen H. Spontaneous development of synovitis and cartilage degeneration in transgenic mice overexpressing cathepsin K. Arthritis Rheum 2005, 52:3713-3717.
73. Blom A.B., van Lent P.L., van der Kraan P.M., van den Berg W.B. To seek shelter from the WNT in osteoarthritis? WNT-signaling as a target for osteoarthritis therapy. Curr Drug Targets 2010, 11:620-629.
74. Wu Q., Zhu M., Rosier R.N., Zuscik M.J., O'Keefe R.J., Chen D. Beta-catenin, cartilage, and osteoarthritis. Ann N Y Acad Sci 2010, 1192:344-350.
75. Hopwood B., Tsykin A., Findlay D.M., Fazzalari N.L. Microarray gene expression profiling of osteoarthritic bone suggests altered bone remodelling, WNT and transforming growth factor-beta/bone morphogenic protein signalling. Arthritis Res Ther 2007, 9:R100.
76. Kumarasinghe D.D., Perilli E., Tsangari H., Truong L., Kuliwaba J.S., Hopwood B. Critical molecular regulators, histomorphometric indices and their correlations in the trabecular bone in primary hip osteoarthritis. Osteoarthritis Cartilage 2010, 18(10).
77. Lane N.E., Nevitt M.C., Lui L.Y., de Leon P., Corr M. Wnt signaling antagonists are potential prognostic biomarkers for the progression of radiographic hip osteoarthritis in elderly Caucasian women. Arthritis Rheum 2007, 56:3319-3325.
78. Weng L.H., Wang C.J., Ko J.Y., Sun Y.C., Wang F.S. Control of Dkk-1 ameliorates chondrocyte apoptosis, cartilage destruction, and subchondral bone deterioration in osteoarthritic knees. Arthritis Rheum 2010, 62:1393-1402.
79. Weng L.H., Wang C.J., Ko J.Y., Sun Y.C., Su Y.S., Wang F.S. Inflammation induction of Dickkopf-1 mediates chondrocyte apoptosis in osteoarthritic joint. Osteoarthritis Cartilage 2009, 17:919-929.
80. Ryu J.H., Chun J.S. Opposing roles of WNT-5A and WNT-11 in interleukin-1beta regulation of type II collagen expression in articular chondrocytes. J Biol Chem 2006, 281:22039-22047.
81. Zhu M., Tang D., Wu Q., Hao S., Chen M., Xie C. Activation of beta-catenin signaling in articular chondrocytes leads to osteoarthritis-like phenotype in adult beta-catenin conditional activation mice. J Bone Miner Res 2008, 24(1).
82. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky M.S., Dwyer D. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007, 13:156-163.
83. Zhu M., Chen M., Zuscik M., Wu Q., Wang Y.J., Rosier R.N. Inhibition of beta-catenin signaling in articular chondrocytes results in articular cartilage destruction. Arthritis Rheum 2008, 58:2053-2064.
84. Lyons T.J., McClure S.F., Stoddart R.W., McClure J. The normal human chondro-osseous junctional region: evidence for contact of uncalcified cartilage with subchondral bone and marrow spaces. BMC Musculoskelet Disord 2006, 7:52.
85. Clark J.M. The structure of vascular channels in the subchondral plate. J Anat 1990, 171:105-115.
86. Sokoloff L. Microcracks in the calcified layer of articular cartilage. Arch Pathol Lab Med 1993, 117:191-195.
87. Imhof H., Breitenseher M., Kainberger F., Rand T., Trattnig S. Importance of subchondral bone to articular cartilage in health and disease. Top Magn Reson Imaging 1999, 10:180-192.
88. Pan J., Zhou X., Li W., Novotny J.E., Doty S.B., Wang L. In situ measurement of transport between subchondral bone and articular cartilage. J Orthop Res 2009, 27:1347-1352.
89. Lin Y.Y., Tanaka N., Ohkuma S., Iwabuchi Y., Tanne Y., Kamiya T. Applying an excessive mechanical stress alters the effect of subchondral osteoblasts on chondrocytes in a co-culture system. Eur J Oral Sci 2010, 118:151-158.
90. Burr D.B., Radin E.L. Microfractures and microcracks in subchondral bone: are they relevant to osteoarthrosis?. Rheum Dis Clin North Am 2003, 29:675-685.