BMP-2 induces ATF4 phosphorylation in chondrocytes through a COX-2/PGE2 dependent signaling pathway

Osteoarthritis and Cartilage

Volumn 22, Issue 3, 2014, Pages 481-489

  Li, T F ^a   Yukata, K ^b,c   Yin, G ^d   Sheu, T ^c   Maruyama, T ^c   Jonason, J H ^c   Hsu, W ^c   Zhang, X ^c   Xiao, G ^a   Konttinen, Y T ^e   Chen, D ^a   O'Keefe, R J ^c  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d NANJING MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

ATF4; BMP 2; Chondrocytes; COX 2

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BONE MORPHOGENETIC PROTEIN 2; CYCLOOXYGENASE 2; DOXYCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE 1; PROSTAGLANDIN E RECEPTOR; PROSTAGLANDIN E2; SMAD1 PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CARTILAGE CELL; CELL LYSATE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TIBIA FRACTURE; TRANSGENE; UPREGULATION; ANIMAL; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 2; CHONDROCYTES; CYCLOOXYGENASE 2; DINOPROSTONE; MICE; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84896736068     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2013.12.020     Document Type: Article

References (46)

1. Cao X., Chen D. The BMP signaling and invivo bone formation. Gene 2005, 357(1):1-8.
2. Miyazono K., Kamiya Y., Morikawa M. Bone morphogenetic protein receptors and signal transduction. JBiochem 2010, 147(1):35-51.
3. Lad S.P., Nathan J.K., Boakye M. Trends in the use of bone morphogenetic protein as a substitute to autologous iliac crest bone grafting for spinal fusion procedures in the United States. Spine 2011, 36(4):E274-E281.
4. Even J., Eskander M., Kang J. Bone morphogenetic protein in spine surgery: current and future uses. JAm Acad Orthop Surg 2012, 20(9):547-552.
5. Chrastil J., Patel A.A. Complications associated with posterior and transforaminal lumbar interbody fusion. JAm Acad Orthop Surg 2012, 20(5):283-291.
6. Argintar E., Edwards S., Delahay J. Bone morphogenetic proteins in orthopaedic trauma surgery. Injury 2011, 42(8):730-734.
7. Lee K.B., Taghavi C.E., Murray S.S., Song K.J., Keorochana G., Wang J.C. BMP induced inflammation. JOrthop Res 2012, 30(12):1985-1994.
8. Kimura N., Matsuo R., Shibuya H., Nakashima K., Taga T. BMP-2-induced apoptosis is mediated by activation of the TAK1-p38 kinase pathway that is negatively regulated by Smad6. JBiol Chem 2000, 275(23):17647-17652.
9. Shim J.H., Greenblatt M.B., Xie M., Schneider M.D., Zou W., Zhai B., et al. TAK1 is an essential regulator of BMP signalling in cartilage. EMBO J 2009, 28(14):2028-2041.
10. Gunnell L.M., Jonason J.H., Loiselle A.E., Kohn A., Schwarz E.M., Hilton M.J., et al. TAK1 regulates cartilage and joint development via the MAPK and BMP signaling pathways. JBone Min Res 2010, 25(8):1784-1797.
11. Li T.F., Gao L., Sheu T.J., Sampson E.R., Flick L.M., Konttinen Y.T., et al. Aberrant hypertrophy in Smad3-deficient murine chondrocytes is rescued by restoring transforming growth factor beta-activated kinase 1/activating transcription factor 2 signaling: a potential clinical implication for osteoarthritis. Arthritis Rheum 2010, 62(8):2359-2369.
12. Chikazu D., Li X., Kawaguchi H., Sakuma Y., Voznesensky O.S., Adams D.J., et al. Bone morphogenetic protein 2 induces cyclo-oxygenase 2 in osteoblasts via a Cbfal binding site: role in effects of bone morphogenetic protein 2 invitro and invivo. JBone Min Res 2002, 17(8):1430-1440.
13. Zhang X., Schwarz E.M., Young D.A., Puzas J.E., Rosier R.N., O'Keefe R.J. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. JClin Invest 2002, 109(11):1405-1415.
14. Sugimoto Y., Narumiya S. Prostaglandin E receptors. JBiol Chem 2007, 282(16):11613-11617.
15. Li T.F., Zuscik M.J., Ionescu A.M., Zhang X., Rosier R.N., Schwarz E.M., et al. PGE2 inhibits chondrocyte differentiation through PKA and PKC signaling. Exp Cell Res 2004, 300(1):159-169.
16. Arikawa T., Omura K., Morita I. Regulation of bone morphogenetic protein-2 expression by endogenous prostaglandin E2 in human mesenchymal stem cells. JCell Physiol 2004, 200(3):400-406.
17. Welting T.J., Caron M.M., Emans P.J., Janssen M.P., Sanen K., Coolsen M.M., et al. Inhibition of cyclooxygenase-2 impacts chondrocyte hypertrophic differentiation during endochondral ossification. Eur Cell Mater 2011, 22:420-436.
18. Xie C., Liang B., Xue M., Lin A.S., Loiselle A., Schwarz E.M., et al. Rescue of impaired fracture healing in COX-2-/- mice via activation of prostaglandin E2 receptor subtype 4. Am J Pathol 2009, 175(2):772-785.
19. Paralkar V.M., Borovecki F., Ke H.Z., Cameron K.O., Lefker B., Grasser W.A., et al. An EP2 receptor-selective prostaglandin E2 agonist induces bone healing. Proc Natl Acad Sci USA 2003, 100(11):6736-6740.
20. Tanaka M., Sakai A., Uchida S., Tanaka S., Nagashima M., Katayama T., et al. Prostaglandin E2 receptor (EP4) selective agonist (ONO-4819.CD) accelerates bone repair of femoral cortex after drill-hole injury associated with local upregulation of bone turnover in mature rats. Bone 2004, 34(6):940-948.
21. Zhang M., Ho H.C., Sheu T.J., Breyer M.D., Flick L.M., Jonason J.H., et al. EP1 (-/-) mice have enhanced osteoblast differentiation and accelerated fracture repair. JBone Min Res 2011, 26(4):792-802.
22. Desai S., April H., Nwaneshiudu C., Ashby B. Comparison of agonist-induced internalization of the human EP2 and EP4 prostaglandin receptors: role of the carboxyl terminus in EP4 receptor sequestration. Mol Pharmacol 2000, 58(6):1279-1286.
23. Fujino H., Xu W., Regan J.W. Prostaglandin E2 induced functional expression of early growth response factor-1 by EP4, but not EP2, prostanoid receptors via the phosphatidylinositol 3-kinase and extracellular signal-regulated kinases. JBiol Chem 2003, 278(14):12151-12156.
24. Jain S., Chakraborty G., Raja R., Kale S., Kundu G.C. Prostaglandin E2 regulates tumor angiogenesis in prostate cancer. Cancer Res 2008, 68(19):7750-7759.
25. Romeo Y., Zhang X., Roux P.P. Regulation and function of the RSK family of protein kinases. Biochem J 2012, 441(2):553-569.
26. Sassone-Corsi P., Mizzen C.A., Cheung P., Crosio C., Monaco L., Jacquot S., et al. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 1999, 285(5429):886-891.
27. Yang X., Matsuda K., Bialek P., Jacquot S., Masuoka H.C., Schinke T., et al. ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell 2004, 117(3):387-398.
28. Elefteriou F., Ahn J.D., Takeda S., Starbuck M., Yang X., Liu X., et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 2005, 434(7032):514-520.
29. Cao H., Yu S., Yao Z., Galson D.L., Jiang Y., Zhang X., et al. Activating transcription factor 4 regulates osteoclast differentiation in mice. JClin Invest 2010, 120(8):2755-2766.
30. Wang W., Lian N., Li L., Moss H.E., Wang W., Perrien D.S., et al. Atf4 regulates chondrocyte proliferation and differentiation during endochondral ossification by activating Ihh transcription. Development 2009, 136(24):4143-4153.
31. Wang W., Lian N., Ma Y., Li L., Gallant R.C., Elefteriou F., et al. Chondrocytic Atf4 regulates osteoblast differentiation and function via Ihh. Development 2012, 139(3):601-611.
32. Li T.F., Darowish M., Zuscik M.J., Chen D., Schwarz E.M., Rosier R.N., et al. Smad3-deficient chondrocytes have enhanced BMP signaling and accelerated differentiation. JBone Min Res 2006, 21(1):4-16.
33. Li T.F., Chen D., Wu Q., Chen M., Sheu T.J., Schwarz E.M., et al. Transforming growth factor-beta stimulates cyclin D1 expression through activation of beta-catenin signaling in chondrocytes. JBiol Chem 2006, 281(30):21296-21304.
34. Moutsatsos I.K., Turgeman G., Zhou S., Kurkalli B.G., Pelled G., Tzur L., et al. Exogenously regulated stem cell-mediated gene therapy for bone regeneration. Mol Ther 2001, 3(4):449-461.
35. Yi S.E., Daluiski A., Pederson R., Rosen V., Lyons K.M. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 2000, 127(3):621-630.
36. Guan Y., Zhang Y., Wu J., Qi Z., Yang G., Dou D., et al. Antihypertensive effects of selective prostaglandin E2 receptor subtype 1 targeting. JClin Invest 2007, 117(9):2496-2505.
37. Kennedy C.R., Zhang Y., Brandon S., Guan Y., Coffee K., Funk C.D., et al. Salt-sensitive hypertension and reduced fertility in mice lacking the prostaglandin EP2 receptor. Nat Med 1999, 5(2):217-220.
38. Dudas M., Sridurongrit S., Nagy A., Okazaki K., Kaartinen V. Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells. Mech Dev 2004, 121(2):173-182.
39. Mishina Y., Hanks M.C., Miura S., Tallquist M.D., Behringer R.R. Generation of Bmpr/Alk3 conditional knockout mice. Genesis 2002, 32(2):69-72.
40. Huang S., Tang B., Usoskin D., Lechleider R.J., Jamin S.P., Li C., et al. Conditional knockout of the Smad1 gene. Genesis 2002, 32(2):76-79.
41. Schneider A., Guan Y., Zhang Y., Magnuson M.A., Pettepher C., Loftin C.D., et al. Generation of a conditional allele of the mouse prostaglandin EP4 receptor. Genesis 2004, 40(1):7-14.
42. Xie M., Zhang D., Dyck J.R., Li Y., Zhang H., Morishima M., et al. Apivotal role for endogenous TGF-beta-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. Proc Natl Acad Sci USA 2006, 103(46):17378-17383.
43. Tsuji K., Bandyopadhyay A., Harfe B.D., Cox K., Kakar S., Gerstenfeld L., et al. BMP-2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet 2006, 38(12):1424-1429.
44. Tsuji K., Cox K., Bandyopadhyay A., Harfe B.D., Tabin C.J., Rosen V. BMP4 is dispensable for skeletogenesis and fracture-healing in the limb. JBone Jt Surg Am 2008, 90(Suppl 1):14-18.
45. Lau K.H., Kothari V., Das A., Zhang X.B., Baylink D.J. Cellular and molecular mechanisms of accelerated fracture healing by COX-2 gene therapy: studies in a mouse model of multiple fractures. Bone 2013, 53:369-381.
46. Naik A.A., Xie C., Zuscik M.J., Kingsley P., Schwarz E.M., Awad H., et al. Reduced COX-2 expression in aged mice is associated with impaired fracture healing. JBone Min Res 2009, 24(2):251-264.