Hypoxia and vitamin D differently contribute to leptin and dickkopf-related protein 2 production in human osteoarthritic subchondral bone osteoblasts

Arthritis Research and Therapy

Volumn 16, Issue 1, 2014, Pages

  Bouvard, Béatrice ^a,b   Abed, Elie ^c   Yéléhé Okouma, Mélissa ^a   Bianchi, Arnaud ^a   Mainard, Didier ^a,d   Netter, Patrick ^a,d   Jouzeau, Jean Yves ^a,d   Lajeunesse, Daniel ^c   Reboul, Pascal ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b ANGERS UNIVERSITY HOSPITAL   (France)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITY HOSPITAL OF NANCY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; DICKKOPF RELATED PROTEIN 2; GLYCOPROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; OSTEOCALCIN; PHOSPHATIDYLINOSITOL 3 KINASE; SIRTUIN 1; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DKK2 PROTEIN, HUMAN; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HIF1A PROTEIN, HUMAN; SIGNAL PEPTIDE; VITAMIN; VITAMIN D;

AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DKK2 GENE; DOWN REGULATION; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HYPOXIA; MALE; OSTEOARTHRITIS; OSTEOBLAST; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SIRT1 GENE; TGFB1 GENE; TIBIAL PLATEAU; UPREGULATION; VEGF GENE; BONE; CELL CULTURE; CELL HYPOXIA; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOBLOTTING; METABOLISM; MIDDLE AGED; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

AGED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE AND BONES; CELL HYPOXIA; CELLS, CULTURED; FEMALE; GENE EXPRESSION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOBLOTTING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LEPTIN; MALE; MIDDLE AGED; OSTEOARTHRITIS; OSTEOBLASTS; OSTEOCALCIN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VITAMIN D; VITAMINS;

EID: 84990985937     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-014-0459-3     Document Type: Article

References (59)

1. Burr DB: The importance of subchondral bone in the progression of osteoarthritis. J Rheumatol Suppl 2004, 70:77-80.
2. Oehler S, Neureiter D, Meyer-Scholten C, Aigner T: Subtyping of osteoarthritic synoviopathy. Clin Exp Rheumatol 2002, 20:633-640.
3. Burr DB, Gallant MA: Bone remodelling in osteoarthritis. Nat Rev Rheumatol 2012, 8:665-673.
4. Heinegård D, Saxne T: The role of the cartilage matrix in osteoarthritis. Nat Rev Rheumatol 2011, 7:50-56.
5. Bellido M, Lugo L, Roman-Blas JA, Castañeda S, Caeiro JR, Dapia S, Calvo E, Largo R, Herrero-Beaumont G: Subchondral bone microstructural damage by increased remodelling aggravates experimental osteoarthritis preceded by osteoporosis. Arthritis Res Ther 2010, 12:R152.
6. Imhof H, Breitenseher M, Kainberger F, Trattnig S: Degenerative joint disease: cartilage or vascular disease? Skeletal Radiol 1997, 26:398-403.
7. 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.
8. Pesesse L, Sanchez C, Henrotin Y: Osteochondral plate angiogenesis: a new treatment target in osteoarthritis. Joint Bone Spine 2011, 78:144-149.
9. Walsh DA, McWilliams DF, Turley MJ, Dixon MR, Fransès RE, Mapp PI, Wilson D: Angiogenesis and nerve growth factor at the osteochondral junction in rheumatoid arthritis and osteoarthritis. Rheumatology (Oxford) 2010, 49:1852-1861.
10. Burr DB, Schaffler MB: The involvement of subchondral mineralized tissues in osteoarthrosis: quantitative microscopic evidence. Microsc Res Tech 1997, 37:343-357.
11. Arnoldi CC, Linderholm H, Müssbichler H: Venous engorgement and intraosseous hypertension in osteoarthritis of the hip. J Bone Joint Surg Br 1972, 54:409-421.
12. Aaron RK, Dyke JP, Ciombor DM, Ballon D, Lee J, Jung E, Tung GA: Perfusion abnormalities in subchondral bone associated with marrow edema, osteoarthritis, and avascular necrosis. Ann N Y Acad Sci 2007, 1117:124-137.
13. Dyke JP, Aaron RK: Noninvasive methods of measuring bone blood perfusion. Ann N Y Acad Sci 2010, 1192:95-102.
14. Lee JH, Dyke JP, Ballon D, Ciombor DM, Rosenwasser MP, Aaron RK: Subchondral fluid dynamics in a model of osteoarthritis: use of dynamic contrast-enhanced magnetic resonance imaging. Osteoarthritis Cartilage 2009, 17:1350-1355.
15. Hunter DJ, Zhang W, Conaghan PG, Hirko K, Menashe L, Li L, Reichmann WM, Losina E: Systematic review of the concurrent and predictive validity of MRI biomarkers in OA. Osteoarthritis Cartilage 2011, 19:557-588.
16. Pelletier JP, Cooper C, Peterfy C, Reginster JY, Brandi ML, Bruyère O, Chapurlat R, Cicuttini F, Conaghan PG, Doherty M, Genant H, Giacovelli G, Hochberg MC, Hunter DJ, Kanis JA, Kloppenburg M, Laredo JD, McAlindon T, Nevitt M, Raynauld JP, Rizzoli R, Zilkens C, Roemer FW, Martel-Pelletier J, Guermazi A: What is the predictive value of MRI for the occurrence of knee replacement surgery in knee osteoarthritis? Ann Rheum Dis 2013, 72:1594-1604.
17. Xu L, Hayashi D, Roemer FW, Felson DT, Guermazi A: Magnetic resonance imaging of subchondral bone marrow lesions in association with osteoarthritis. Semin Arthritis Rheum 2012, 42:105-118.
18. Driban JB, Lo GH, Price L, Pang J, Miller E, Ward RJ, Hunter DJ, Eaton CB, Lynch JA, McAlindon TE, the OAI Investigators Group: Bone marrow lesion volume reduction is not associated with improvement of other periarticular bone measures: data from the Osteoarthritis Initiative. Arthritis Res Ther 2013, 15:R153.
19. Pedersen NW, Kiaer T, Kristensen KD, Starklint H: Intraosseous pressure, oxygenation, and histology in arthrosis and osteonecrosis of the hip. Acta Orthop Scand 1989, 60:415-417.
20. Findlay DM: Vascular pathology and osteoarthritis. Rheumatology (Oxford) 2007, 46:1763-1768.
21. Chang J, Jackson SG, Wardale J, Jones SW: Hypoxia modulates the phenotype of osteoblasts isolated from knee osteoarthritis patients, leading to undermineralized bone nodule formation. Arthritis Rheumatol 2014, 66:1789-1799.
22. Leijten JC, Moreira Teixeira LS, Landman EB, van Blitterswijk CA, Karperien M: Hypoxia inhibits hypertrophic differentiation and endochondral ossification in explanted tibiae. PLoS One 2012, 7:e49896.
23. Maes C, Carmeliet G, Schipani E: Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol 2012, 8:358-366.
24. Husa M, Liu-Bryan R, Terkeltaub R: Shifting HIFs in osteoarthritis. Nat Med 2010, 16:641-644.
25. Rankin EB, Wu C, Khatri R, Wilson TL, Andersen R, Araldi E, Rankin AL, Yuan J, Kuo CJ, Schipani E, Giaccia AJ: The HIF signaling pathway in osteoblasts directly modulates erythropoiesis through the production of EPO. Cell 2012, 149:63-74.
26. Huang LE, Arany Z, Livingston DM, Bunn HF: Activation of hypoxiainducible transcription factor depends primarily upon redox-sensitive stabilization of its a subunit. J Biol Chem 1996, 271:32253-32259.
27. Zhuo Q, Yang W, Chen J, Wang Y: Metabolic syndrome meets osteoarthritis. Nat Rev Rheumatol 2012, 8:729-737.
28. Gabay O, Hall DJ, Berenbaum F, Henrotin Y, Sanchez C: Osteoarthritis and obesity: experimental models. Joint Bone Spine 2008, 75:675-679.
29. Mutabaruka MS, Aoulad Aissa M, Delalandre A, Lavigne M, Lajeunesse D: Local leptin production in osteoarthritis subchondral osteoblasts may be responsible for their abnormal phenotypic expression. Arthritis Res Ther 2010, 12:R20.
30. Dumond H, Presle N, Terlain B, Mainard D, Loeuille D, Netter P, Pottie P: Evidence for a key role of leptin in osteoarthritis. Arthritis Rheum 2003, 48:3118-3129.
31. Chan TF, Couchourel D, Abed E, Delalandre A, Duval N, Lajeunesse D: Elevated Dickkopf-2 levels contribute to the abnormal phenotype of human osteoarthritic osteoblasts. J Bone Miner Res 2011, 26:1399-1410.
32. Corrado A, Neve A, Macchiarola A, Gaudio A, Marucci A, Cantatore FP: RANKL/ OPG ratio and DKK-1 expression in primary osteoblastic cultures from osteoarthritic and osteoporotic subjects. J Rheumatol 2013, 40:684-694.
33. Gómez R, Conde J, Scotece M, Gómez-Reino JJ, Lago F, Gualillo O: What's new in our understanding of the role of adipokines in rheumatic diseases? Nat Rev Rheumatol 2011, 7:528-536.
34. Pottie P, Presle N, Terlain B, Netter P, Mainard D, Berenbaum F: Obesity and osteoarthritis: more complex than predicted! Ann Rheum Dis 2006, 65:1403-1405.
35. Conde J, Scotece M, López V, Gómez R, Lago F, Pino J, Gómez-Reino JJ, Gualillo O: Adipokines: novel players in rheumatic diseases. Discov Med 2013, 15:73-83.
36. Wree A, Mayer A, Westphal S, Beilfuss A, Canbay A, Schick RR, Gerken G, Vaupel P: Adipokine expression in brown and white adipocytes in response to hypoxia. J Endocrinol Invest 2012, 35:522-527.
37. Larsen H, Muz B, Khong TL, Feldmann M, Paleolog EM: Differential effects of Th1 versus Th2 cytokines in combination with hypoxia on HIFs and angiogenesis in RA. Arthritis Res Ther 2012, 14:R180.
38. Wu MH, Chen KF, Lin SC, Lgu CW, Tsai SJ: Aberrant expression of leptin in human endometriotic stromal cells is induced by elevated levels of hypoxia inducible factor-1α. Am J Pathol 2007, 170:590-598.
39. Hong SJ, Jin DP, Buck DW 2nd, Galiano RD, Mustoe TA: Impaired response of mature adipocytes of diabetic mice to hypoxia. Exp Cell Res 2011, 317:2299-2307.
40. Meissner U, Ostreicher I, Allabauer I, Rascher W, Dötsch J: Synergistic effects of hypoxia and insulin are regulated by different transcriptional elements of the human leptin promoter. Biochem Biophys Res Commun 2003, 303:707-712.
41. Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, Christy W, Cooke TD, Greenwald R, Hochberg M, Howell D, Kaplan D, Koopman W, Longley S 3rd, Mankin H, McShane DJ, Medsger TA Jr, Meehan R, Mikkelsen W, Moskowitz R, Murphy W, Rothschild B, Segal M, Sokoloff L, Wolfe F: Development of criteria for the classification and reporting of osteoarthritis: classification of osteoarthritis of the knee. Arthritis Rheum 1986, 29:1039-1049.
42. Francin PJ, Guillaume C, Humbert AC, Pottie P, Netter P, Mainard D, Presle N: Association between the chondrocyte phenotype and the expression of adipokines and their receptors: evidence for a role of leptin but not adiponectin in the expression of cartilage-specific markers. J Cell Physiol 2011, 226:2790-2797.
43. Janelle-Montcalm A, Boileau C, Poirier F, Pelletier JP, Guévremont M, Duval N, Martel-Pelletier J, Reboul P: Extracellular localization of galectin-3 has a deleterious role in joint tissues. Arthritis Res Ther 2007, 9:R20.
44. Cailotto F, Reboul P, Sebillaud S, Netter P, Jouzeau JY, Bianchi A: Calcium input potentiates the transforming growth factor (TGF)-β1-dependent signaling to promote the export of inorganic pyrophosphate by articular chondrocyte. J Biol Chem 2011, 286:19215-19228.
45. Utting JC, Robins SP, Brandao-Burch A, Orriss IR, Behar J, Arnett TR: Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp Cell Res 2006, 312:1693-1702.
46. Kiaer T, Pedersen NW, Kristensen KD, Starklint H: Intra-osseous pressure and oxygen tension in avascular necrosis and osteoarthritis of the hip. J Bone Joint Surg Br 1990, 72:1023-1030.
47. Akeno N, Czyzyk-Krzeska MF, Gross TS, Clemens TL: Hypoxia induces vascular endothelial growth factor gene transcription in human osteoblast-like cells through the hypoxia-inducible factor-2a. Endocrinology 2001, 142:959-962.
48. Guévremont M, Martel-Pelletier J, Massicotte F, Tardif G, Pelletier JP, Ranger P, Lajeunesse D, Reboul P: Human adult chondrocytes express hepatocyte growth factor (HGF) isoforms but not HGF: potential implication of osteoblasts on on the presence of HGF in cartilage. J Bone Min Res 2003, 18:1073-1081.
49. Sanchez C, Deberg MA, Bellahcène A, Castronovo V, Msika P, Delcour JP, Crielaard JM, Henrotin YE: Phenotypic characterization of osteoblasts from the sclerotic zones of osteoarthritic subchondral bone. Arthritis Rheum 2008, 58:442-455.
50. Jiang Y, Zheng W, Teegarden D: 1α, 25-Dihydroxyvitamin D regulates hypoxia-inducible factor-1α in untransformed and Harvey-ras transfected breast epithelial cells. Cancer Lett 2010, 298:159-166.
51. Chu DL, Li VW, Yu RM: Leptin: clue to poor appetite in oxygen-starved fish. Mol Cell Endocrinol 2010, 319:143-146.
52. Carlberg C, Campbell MJ: Vitamin D receptor signaling mechanisms: Integrated actions of a well-defined transcription factor. Steroids 2013, 78:127-136.
53. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G: Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000, 100:197-207.
54. Turner RT, Kalra SP, Wong CP, Philbrick KA, Lindenmaier LB, Boghossian S, Iwaniec UT: Peripheral leptin regulates bone formation. J Bone Miner Res 2013, 28:22-34.
55. James J, Steijn-Myagkaya GL: Death of osteocytes: electron microscopy after in vitro ischaemia. J Bone Joint Surg Br 1986, 68:620-624.
56. Catto M: Ischaemia of bone. J Clin Pathol Suppl (R Coll Pathol) 1977, 11:78-93.
57. Iwamoto I, Fujino T, Douchi T: The leptin receptor in human osteoblasts and the direct effect of leptin on bone metabolism. Gynecol Endocrinol 2004, 19:97-104.
58. Gordeladze JO, Drevon CA, Syversen U, Reseland JE: Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: Impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem 2002, 85:825-836.
59. White SJ, Taylor MJ, Hurt RT, Jensen MD, Poland GA: Leptin-based adjuvants: an innovative approach to improve vaccine response. Vaccine 2013, 31:1666-1672.