Gene expression analyses of subchondral bone in early experimental osteoarthritis by microarray

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Zhang, RongKai ^a   Fang, Hang ^a   Chen, YuXian ^a   Shen, Jun ^a   Lu, HuaDing ^a   Zeng, Chun ^a   Ren, JianHua ^a   Zeng, Hua ^a   Li, ZhiFu ^a   Chen, ShaoMing ^a   Cai, DaoZhang ^a   Zhao, Qing ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ASPORIN; MEMBRANE PROTEIN; STROMELYSIN; UNCLASSIFIED DRUG;

ACCURACY; ACP5 GENE; ALP GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPN GENE; BMP5 GENE; BONE DEVELOPMENT; BONE REMODELING; CARTILAGE; CONTROLLED STUDY; DNA MICROARRAY; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; IGF1 GENE; IHH GENE; IMMUNOCHEMISTRY; KNEE; MMP3 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PATHOGENESIS; POSTN GENE; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA DEGRADATION; SUBCHONDRAL BONE; TGF BETA1 GENE; TIME; TISSUE SECTION; TNSF11 GENE; UNINDEXED SEQUENCE; VALIDATION PROCESS; ANIMAL; BODY WEIGHT; BONE; CLUSTER ANALYSIS; CYTOLOGY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; METHODOLOGY; OSTEOCLAST; PATHOLOGY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; BODY WEIGHT; BONE AND BONES; BONE REMODELING; CARTILAGE; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOARTHRITIS; OSTEOCLASTS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; TIME FACTORS;

EID: 84863262534     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032356     Document Type: Article

References (79)

1. Lohmander LS, (2000) What can we do about osteoarthritis? Arthritis Res 2: 95-100.
2. Felson DT, Neogi T, (2004) Osteoarthritis: is it a disease of cartilage or of bone? Arthritis Rheum 50: 341-344 doi:10.1002/art.20051.
3. Mansell JP, Bailey AJ, (1998) Abnormal cancellous bone collagen metabolism in osteoarthritis. J Clin Invest 101: 1596-1603 doi:10.1172/JCI867.
4. Westacott CI, Webb GR, Warnock MG, Sims JV, Elson CJ, (1997) Alteration of cartilage metabolism by cells from osteoarthritic bone. Arthritis Rheum 40: 1282-1291 doi:10.1002/1529-0131(199707)40:7&1282::AID-ART13>3.0.CO;2-E.
5. Bogoch ER, Moran E, (1998) Abnormal bone remodelling in inflammatory arthritis. Can J Surg 41: 264-271.
6. Radin EL, Rose RM, (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res pp. 34-40.
7. Madry H, van Dijk CN, Mueller-Gerbl M, (2010) The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc 18: 419-433 doi:10.1007/s00167-010-1054-z.
8. Sanchez C, Deberg MA, Piccardi N, Msika P, Reginster J-YL, et al. (2005) 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. Osteoarthr Cartil 13: 979-987 doi:10.1016/j.joca.2005.03.008.
9. Sanchez C, Deberg MA, Piccardi N, Msika P, Reginster J-YL, et al. (2005) Subchondral bone osteoblasts induce phenotypic changes in human osteoarthritic chondrocytes. Osteoarthr Cartil 13: 988-997 doi:10.1016/j.joca.2005.07.012.
10. Bailey AJ, Mansell JP, (1997) Do subchondral bone changes exacerbate or precede articular cartilage destruction in osteoarthritis of the elderly? Gerontology 43: 296-304.
11. Hayami T, Pickarski M, Wesolowski GA, McLane J, Bone A, et al. (2004) 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 50: 1193-1206 doi:10.1002/art.20124.
12. Aigner T, Fundel K, Saas J, Gebhard PM, Haag J, et al. (2006) Large-scale gene expression profiling reveals major pathogenetic pathways of cartilage degeneration in osteoarthritis. Arthritis Rheum 54: 3533-3544 doi:10.1002/art.22174.
13. James CG, Appleton CTG, Ulici V, Underhill TM, Beier F, (2005) Microarray analyses of gene expression during chondrocyte differentiation identifies novel regulators of hypertrophy. Mol Biol Cell 16: 5316-5333 doi:10.1091/mbc.E05-01-0084.
14. Hopwood B, Tsykin A, Findlay DM, Fazzalari NL, (2007) Microarray gene expression profiling of osteoarthritic bone suggests altered bone remodelling, WNT and transforming growth factor-beta/bone morphogenic protein signalling. Arthritis Res Ther 9: R100 doi:10.1186/ar2301.
15. Appleton CTG, Pitelka V, Henry J, Beier F, (2007) Global analyses of gene expression in early experimental osteoarthritis. Arthritis Rheum 56: 1854-1868 doi:10.1002/art.22711.
16. Sanchez C, Deberg MA, Bellahcène A, Castronovo V, Msika P, et al. (2008) Phenotypic characterization of osteoblasts from the sclerotic zones of osteoarthritic subchondral bone. Arthritis Rheum 58: 442-455 doi:10.1002/art.23159.
17. Hopwood B, Gronthos S, Kuliwaba JS, Robey PG, Findlay DM, et al. (2005) Identification of differentially expressed genes between osteoarthritic and normal trabecular bone from the intertrochanteric region of the proximal femur using cDNA microarray analysis. Bone 36: 635-644 doi:10.1016/j.bone.2005.02.003.
18. Sánchez-Sabaté E, Alvarez L, Gil-Garay E, Munuera L, Vilaboa N, (2009) Identification of differentially expressed genes in trabecular bone from the iliac crest of osteoarthritic patients. Osteoarthr Cartil 17: 1106-1114 doi:10.1016/j.joca.2009.01.010.
19. Hilal G, Martel-Pelletier J, Pelletier JP, Ranger P, Lajeunesse D, (1998) Osteoblast-like cells from human subchondral osteoarthritic bone demonstrate an altered phenotype in vitro: possible role in subchondral bone sclerosis. Arthritis Rheum 41: 891-899 doi:10.1002/1529-0131(199805)41:5&891::AID-ART17>3.0.CO;2-X.
20. Brandt KD, (2002) Animal models of osteoarthritis. Biorheology 39: 221-235.
21. Hayami T, Pickarski M, Zhuo Y, Wesolowski GA, Rodan GA, et al. (2006) Characterization of articular cartilage and subchondral bone changes in the rat anterior cruciate ligament transection and meniscectomized models of osteoarthritis. Bone 38: 234-243 doi:10.1016/j.bone.2005.08.007.
22. Kamekura S, Hoshi K, Shimoaka T, Chung U, Chikuda H, et al. (2005) Osteoarthritis development in novel experimental mouse models induced by knee joint instability. Osteoarthr Cartil 13: 632-641 doi:10.1016/j.joca.2005.03.004.
23. Manacu CA, Martel-Pelletier J, Roy-Beaudry M, Pelletier J-P, Fernandes JC, et al. (2005) Endothelin-1 in osteoarthritic chondrocytes triggers nitric oxide production and upregulates collagenase production. Arthritis Res Ther 7: R324-332 doi:10.1186/ar1489.
24. Hanada T, Yoshimura A, (August) Regulation of cytokine signaling and inflammation. Cytokine & Growth Factor Reviews 13: 413-421 doi:16/S1359-6101(02)00026-6.
25. Malemud CJ, (2010) Anticytokine therapy for osteoarthritis: evidence to date. Drugs Aging 27: 95-115 doi:10.2165/11319950-000000000-00000.
26. So JS, Song M-K, Kwon H-K, Lee C-G, Chae C-S, et al. (2011) Lactobacillus casei enhances type II collagen/glucosamine-mediated suppression of inflammatory responses in experimental osteoarthritis. Life Sci 88: 358-366 doi:10.1016/j.lfs.2010.12.013.
27. Karam MC, Al-Kouba JE, Bazzi SI, Smith CB, Leung L, (2011) Interleukin-13 reduces hyperalgesia and the level of interleukin-1β in BALB/c mice infected with Leishmania major with an up-regulation of interleukin-6. J Neuroimmunol 234: 49-54 doi:10.1016/j.jneuroim.2011.02.003.
28. Ahmad R, El Mabrouk M, Sylvester J, Zafarullah M, (2009) Human osteoarthritic chondrocytes are impaired in matrix metalloproteinase-13 inhibition by IFN-gamma due to reduced IFN-gamma receptor levels. Osteoarthr Cartil 17: 1049-1055 doi:10.1016/j.joca.2009.02.008.
29. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, et al. (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359: 693-699 doi:10.1038/359693a0.
30. de Andrés MC, Imagawa K, Hashimoto K, Gonzalez A, Goldring MB, et al. (2011) Suppressors of cytokine signalling (SOCS) are reduced in osteoarthritis. Biochem Biophys Res Commun 407: 54-59 doi:10.1016/j.bbrc.2011.02.101.
31. Fernandes JC, Martel-Pelletier J, Pelletier JP, (2002) The role of cytokines in osteoarthritis pathophysiology. Biorheology 39: 237-246.
32. Kusano K, Miyaura C, Inada M, Tamura T, Ito A, et al. (1998) Regulation of matrix metalloproteinases (MMP-2,-3,-9, and-13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology 139: 1338-1345.
33. Shibakawa A, Yudoh K, Masuko-Hongo K, Kato T, Nishioka K, et al. (2005) The role of subchondral bone resorption pits in osteoarthritis: MMP production by cells derived from bone marrow. Osteoarthr Cartil 13: 679-687 doi:10.1016/j.joca.2005.04.010.
34. Dew G, Murphy G, Stanton H, Vallon R, Angel P, et al. (2000) Localisation of matrix metalloproteinases and TIMP-2 in resorbing mouse bone. Cell Tissue Res 299: 385-394.
35. Sakao K, Takahashi KA, Arai Y, Saito M, Honjo K, et al. (2009) Osteoblasts derived from osteophytes produce interleukin-6, interleukin-8, and matrix metalloproteinase-13 in osteoarthritis. J Bone Miner Metab 27: 412-423 doi:10.1007/s00774-009-0058-6.
36. Bord S, Horner A, Hembry RM, Reynolds JJ, Compston JE, (1997) Distribution of matrix metalloproteinases and their inhibitor, TIMP-1, in developing human osteophytic bone. J Anat 191 (Pt 1): 39-48.
37. Anandarajah AP, (2009) Role of RANKL in bone diseases. Trends Endocrinol Metab 20: 88-94 doi:10.1016/j.tem.2008.10.007.
38. Logar DB, Komadina R, Prezelj J, Ostanek B, Trost Z, et al. (2007) Expression of bone resorption genes in osteoarthritis and in osteoporosis. J Bone Miner Metab 25: 219-225 doi:10.1007/s00774-007-0753-0.
39. Pastoureau PC, Chomel AC, Bonnet J, (1999) Evidence of early subchondral bone changes in the meniscectomized guinea pig. A densitometric study using dual-energy X-ray absorptiometry subregional analysis. Osteoarthr Cartil 7: 466-473 doi:10.1053/joca.1999.0241.
40. Bailey AJ, Sims TJ, Knott L, (2002) Phenotypic expression of osteoblast collagen in osteoarthritic bone: production of type I homotrimer. Int J Biochem Cell Biol 34: 176-182.
41. Couchourel D, Aubry I, Delalandre A, Lavigne M, Martel-Pelletier J, et al. (2009) Altered mineralization of human osteoarthritic osteoblasts is attributable to abnormal type I collagen production. Arthritis Rheum 60: 1438-1450 doi:10.1002/art.24489.
42. Lamas JR, Rodríguez-Rodríguez L, Vigo AG, Alvarez-Lafuente R, López-Romero P, et al. (2010) Large-scale gene expression in bone marrow mesenchymal stem cells: a putative role for COL10A1 in osteoarthritis. Ann Rheum Dis 69: 1880-1885 doi:10.1136/ard.2009.122564.
43. Matyas JR, Sandell LJ, Adams ME, (1997) Gene expression of type II collagens in chondro-osteophytes in experimental osteoarthritis. Osteoarthr Cartil 5: 99-105.
44. Klatt AR, Paul-Klausch B, Klinger G, Kühn G, Renno JH, et al. (2009) A critical role for collagen II in cartilage matrix degradation: collagen II induces pro-inflammatory cytokines and MMPs in primary human chondrocytes. J Orthop Res 27: 65-70 doi:10.1002/jor.20716.
45. Rollins BJ, (1997) Chemokines. Blood 90: 909-928.
46. Vergunst CE, van de Sande MGH, Lebre MC, Tak PP, (2005) The role of chemokines in rheumatoid arthritis and osteoarthritis. Scand J Rheumatol 34: 415-425 doi:10.1080/03009740500439159.
47. Sánchez-Madrid F, del Pozo MA, (1999) Leukocyte polarization in cell migration and immune interactions. EMBO J 18: 501-511 doi:10.1093/emboj/18.3.501.
48. Lisignoli G, Toneguzzi S, Pozzi C, Piacentini A, Grassi F, et al. (1999) Chemokine expression by subchondral bone marrow stromal cells isolated from osteoarthritis (OA) and rheumatoid arthritis (RA) patients. Clin Exp Immunol 116: 371-378.
49. Endres M, Andreas K, Kalwitz G, Freymann U, Neumann K, et al. (2010) Chemokine profile of synovial fluid from normal, osteoarthritis and rheumatoid arthritis patients: CCL25, CXCL10 and XCL1 recruit human subchondral mesenchymal progenitor cells. Osteoarthr Cartil 18: 1458-1466 doi:10.1016/j.joca.2010.08.003.
50. Borzì RM, Mazzetti I, Cattini L, Uguccioni M, Baggiolini M, et al. (2000) Human chondrocytes express functional chemokine receptors and release matrix-degrading enzymes in response to C-X-C and C-C chemokines. Arthritis Rheum 43: 1734-1741 doi:10.1002/1529-0131(200008)43:8&1734::AID-ANR9>3.0.CO;2-B.
51. Yuan GH, Masuko-Hongo K, Sakata M, Tsuruha J, Onuma H, et al. (2001) The role of C-C chemokines and their receptors in osteoarthritis. Arthritis Rheum 44: 1056-1070 doi:10.1002/1529-0131(200105)44:5&1056::AID-ANR186>3.0.CO;2-U.
52. Lisignoli G, Toneguzzi S, Grassi F, Piacentini A, Tschon M, et al. (2002) Different chemokines are expressed in human arthritic bone biopsies: IFN-gamma and IL-6 differently modulate IL-8, MCP-1 and rantes production by arthritic osteoblasts. Cytokine 20: 231-238.
53. Lande R, Giacomini E, Serafini B, Rosicarelli B, Sebastiani GD, et al. (2004) Characterization and recruitment of plasmacytoid dendritic cells in synovial fluid and tissue of patients with chronic inflammatory arthritis. J Immunol 173: 2815-2824.
54. Lisignoli G, Toneguzzi S, Piacentini A, Cristino S, Grassi F, et al. (2006) CXCL12 (SDF-1) and CXCL13 (BCA-1) chemokines significantly induce proliferation and collagen type I expression in osteoblasts from osteoarthritis patients. J Cell Physiol 206: 78-85 doi:10.1002/jcp.20435.
55. Haringman JJ, Smeets TJM, Reinders-Blankert P, Tak PP, (2006) Chemokine and chemokine receptor expression in paired peripheral blood mononuclear cells and synovial tissue of patients with rheumatoid arthritis, osteoarthritis, and reactive arthritis. Ann Rheum Dis 65: 294-300 doi:10.1136/ard.2005.037176.
56. Meikle MC, Bord S, Hembry RM, Compston J, Croucher PI, et al. (1992) Human osteoblasts in culture synthesize collagenase and other matrix metalloproteinases in response to osteotropic hormones and cytokines. J Cell Sci 103 (Pt 4): 1093-1099.
57. Blavier L, Delaissé JM, (1995) Matrix metalloproteinases are obligatory for the migration of preosteoclasts to the developing marrow cavity of primitive long bones. J Cell Sci 108 (Pt 12): 3649-3659.
58. Hill PA, Murphy G, Docherty AJ, Hembry RM, Millican TA, et al. (1994) The effects of selective inhibitors of matrix metalloproteinases (MMPs) on bone resorption and the identification of MMPs and TIMP-1 in isolated osteoclasts. J Cell Sci 107 (Pt 11): 3055-3064.
59. Brown TD, Johnston RC, Saltzman CL, Marsh JL, Buckwalter JA, (2006) Posttraumatic osteoarthritis: a first estimate of incidence, prevalence, and burden of disease. J Orthop Trauma 20: 739-744 doi:10.1097/01.bot.0000246468.80635.ef.
60. Wu Q, Zhang Y, Chen Q, (2001) Indian hedgehog is an essential component of mechanotransduction complex to stimulate chondrocyte proliferation. J Biol Chem 276: 35290-35296 doi:10.1074/jbc.M101055200.
61. Tang GH, Rabie ABM, Hägg U, (2004) Indian hedgehog: a mechanotransduction mediator in condylar cartilage. J. Dent. Res 83: 434-438.
62. Ng TCS, Chiu KWK, Rabie ABM, Hägg U, (2006) Repeated mechanical loading enhances the expression of Indian hedgehog in condylar cartilage. Front Biosci 11: 943-948.
63. Lin AC, Seeto BL, Bartoszko JM, Khoury MA, Whetstone H, et al. (2009) Modulating hedgehog signaling can attenuate the severity of osteoarthritis. Nat Med 15: 1421-1425 doi:10.1038/nm.2055.
64. Botter SM, Glasson SS, Hopkins B, Clockaerts S, Weinans H, et al. (2009) ADAMTS5-/- mice have less subchondral bone changes after induction of osteoarthritis through surgical instability: implications for a link between cartilage and subchondral bone changes. Osteoarthr Cartil 17: 636-645 doi:10.1016/j.joca.2008.09.018.
65. Takeshita S, Kikuno R, Tezuka K, Amann E, (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294 (Pt 1): 271-278.
66. Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, et al. (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14: 1239-1249 doi:10.1359/jbmr.1999.14.7.1239.
67. Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, et al. (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res 62: 5358-5364.
68. Ma D, Zhang R, Sun Y, Rios HF, Haruyama N, et al. (2011) A novel role of periostin in postnatal tooth formation and mineralization. J. Biol. Chem 286: 4302-4309 doi:10.1074/jbc.M110.140202.
69. Lindner V, Wang Q, Conley BA, Friesel RE, Vary CPH, (2005) Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration. Arterioscler Thromb Vasc Biol 25: 77-83 doi:10.1161/01.ATV.0000149141.81230.c6.
70. Chen D, Zhao M, Mundy GR, (2004) Bone morphogenetic proteins. Growth Factors 22: 233-241 doi:10.1080/08977190412331279890.
71. Rountree RB, Schoor M, Chen H, Marks ME, Harley V, et al. (2004) BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol 2: e355 doi:10.1371/journal.pbio.0020355.
72. Goldring MB, Tsuchimochi K, Ijiri K, (2006) The control of chondrogenesis. J Cell Biochem 97: 33-44 doi:10.1002/jcb.20652.
73. Li X, Cao X, (2006) BMP signaling and skeletogenesis. Ann N Y Acad Sci 1068: 26-40 doi:10.1196/annals.1346.006.
74. Einhorn TA, (2003) Clinical applications of recombinant human BMPs: early experience and future development. J Bone Joint Surg Am 85-A (Suppl 3): 82-88.
75. Urist MR, (2002) Bone: formation by autoinduction. 1965. Clin Orthop Relat Res pp. 4-10.
76. Reddi AH, Huggins C, (1972) Biochemical sequences in the transformation of normal fibroblasts in adolescent rats. Proc Natl Acad Sci U S A 69: 1601-1605.
77. Glaser DL, Economides AN, Wang L, Liu X, Kimble RD, et al. (2003) In vivo somatic cell gene transfer of an engineered Noggin mutein prevents BMP4-induced heterotopic ossification. J Bone Joint Surg Am 85-A: 2332-2342.
78. King JA, Marker PC, Seung KJ, Kingsley DM, (1994) BMP5 and the molecular, skeletal, and soft-tissue alterations in short ear mice. Dev Biol 166: 112-122 doi:10.1006/dbio.1994.1300.
79. Mailhot G, Yang M, Mason-Savas A, Mackay CA, Leav I, et al. (2008) BMP-5 expression increases during chondrocyte differentiation in vivo and in vitro and promotes proliferation and cartilage matrix synthesis in primary chondrocyte cultures. J Cell Physiol 214: 56-64 doi:10.1002/jcp.21164.