Prostaglandin E2 signals through PTGER2 to regulate sclerostin expression

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Genetos, Damian C ^a   Yellowley, Clare E ^a   Loots, Gabriela G ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E2; SCLEROSTIN; SMALL INTERFERING RNA; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; BONE MORPHOGENETIC PROTEIN; CYCLOHEXIMIDE; DACTINOMYCIN; GLYCOPROTEIN; MYOGENIC FACTOR; PARATHYROID HORMONE; SIGNAL PEPTIDE;

ARTICLE; AXIN2 GENE; CONTROLLED STUDY; OSTEOBLAST; OSTEOCLAST; PROTEIN EXPRESSION; TCF3 GENE; ANIMAL; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CYCLIC AMP; CYCLOHEXIMIDE; DACTINOMYCIN; DINOPROSTONE; GENE EXPRESSION REGULATION; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MYOGENIC REGULATORY FACTORS; PARATHYROID HORMONE; RECEPTORS, PROSTAGLANDIN E, EP2 SUBTYPE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; WNT PROTEINS;

EID: 79952742823     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017772     Document Type: Article

References (69)

1. Feyen JH, Di Bon A, van der Plas A, Lowik CW, Nijweide PJ, (1985) Effects of exogenous prostanoids on the proliferation of osteoblast-like cells in vitro. Prostaglandins 30: 827-840.
2. Hakeda Y, Yoshino T, Natakani Y, Kurihara N, Maeda N, et al. (1986) Prostaglandin E2 stimulates DNA synthesis by a cyclic AMP-independent pathway in osteoblastic clone MC3T3-E1 cells. J Cell Physiol 128: 155-161.
3. Minamizaki T, Yoshiko Y, Kozai K, Aubin JE, Maeda N, (2009) EP2 and EP4 receptors differentially mediate MAPK pathways underlying anabolic actions of prostaglandin E2 on bone formation in rat calvaria cell cultures. Bone 44: 1177-1185.
4. Hakeda Y, Nakatani Y, Hiramatsu M, Kurihara N, Tsunoi M, et al. (1985) Inductive effects of prostaglandins on alkaline phosphatase in osteoblastic cells, clone MC3T3-E1. J Biochem 97: 97-104.
5. Flanagan AM, Chambers TJ, (1992) Stimulation of bone nodule formation in vitro by prostaglandins E1 and E2. Endocrinology 130: 443-448.
6. Klein-Nulend J, Burger EH, Semeins CM, Raisz LG, Pilbeam CC, (1997) Pulsating fluid flow stimulates prostaglandin release and inducible G/H synthase mRNA expression in primary mouse bone cells. J Bone Miner Res 12: 45-51.
7. Chen NX, Ryder KD, Pavalko FM, Turner CH, Burr DB, et al. (2000) Calcium regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am J Physiol 278: C989-997.
8. Wadhwa S, Godwin SL, Peterson DR, Epstein MA, Raisz LG, et al. (2002) Fluid flow induction of cyclo-oxygenase 2 gene expression in osteoblasts is dependent on an extracellular signal-regulated kinase signaling pathway. J Bone Miner Res 17: 266-274.
9. Pead MJ, Lanyon LE, (1989) Indomethacin modulation of load-related stimulation of new bone formation in vivo. Calcif Tissue Int 45: 34-40.
10. Forwood MR, (1996) Inducible cyclo-oxygenase (COX-2) mediates the induction of bone formation by mechanical loading in vivo. J Bone Miner Res 11: 1688-1693.
11. Jee WS, Ma YF, (1997) The in vivo anabolic actions of prostaglandins in bone. Bone 21: 297-304.
12. Gerstenfeld LC, Einhorn TA, (2004) COX inhibitors and their effects on bone healing. Expert Opin Drug Saf 3: 131-136.
13. Simon AM, Manigrasso MB, O'Connor JP, (2002) Cyclo-oxygenase 2 function is essential for bone fracture healing. J Bone Miner Res 17: 963-976.
14. Giannoudis PV, MacDonald DA, Matthews SJ, Smith RM, Furlong AJ, et al. (2000) Nonunion of the femoral diaphysis. The influence of reaming and non-steroidal anti-inflammatory drugs. J Bone Joint Surg Br 82: 655-658.
15. Burd TA, Hughes MS, Anglen JO, (2003) Heterotopic ossification prophylaxis with indomethacin increases the risk of long-bone nonunion. J Bone Joint Surg Br 85: 700-705.
16. Li M, Ke HZ, Qi H, Healy DR, Li Y, et al. (2003) A novel, non-prostanoid EP2 receptor-selective prostaglandin E2 agonist stimulates local bone formation and enhances fracture healing. J Bone Miner Res 18: 2033-2042.
17. Paralkar VM, Borovecki F, Ke HZ, Cameron KO, Lefker B, et al. (2003) An EP2 receptor-selective prostaglandin E2 agonist induces bone healing. Proc Natl Acad Sci U S A 100: 6736-6740.
18. Axelrad TW, Kakar S, Einhorn TA, (2007) New technologies for the enhancement of skeletal repair. Injury 38 (Suppl 1): S49-62.
19. Cameron KO, Lefker BA, Ke HZ, Li M, Zawistoski MP, et al. (2009) Discovery of CP-533536: an EP2 receptor selective prostaglandin E2 (PGE2) agonist that induces local bone formation. Bioorg Med Chem Lett 19: 2075-2078.
20. Bodine PV, Komm BS, (2006) Wnt signaling and osteoblastogenesis. Rev Endocr Metab Disord 7: 33-39.
21. Akiyama T, (2000) Wnt/beta-catenin signaling. Cytokine Growth Factor Rev 11: 273-282.
22. Nusse R, (1999) WNT targets. Repression and activation. Trends Genet 15: 1-3.
23. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, et al. (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513-523.
24. Little RD, Carulli JP, Del Mastro RG, Dupuis J, Osborne M, et al. (2002) A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am J Hum Genet 70: 11-19.
25. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, et al. (2002) Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 157: 303-314.
26. Holmen SL, Giambernardi TA, Zylstra CR, Buckner-Berghuis BD, Resau JH, et al. (2004) Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J Bone Miner Res 19: 2033-2040.
27. Sawakami K, Robling AG, Ai M, Pitner ND, Liu D, et al. (2006) The Wnt Co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem 281: 23698-23711.
28. Bodine PV, Zhao W, Kharode YP, Bex FJ, Lambert AJ, et al. (2004) The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol Endocrinol 18: 1222-1237.
29. Bodine PV, Billiard J, Moran RA, Ponce-de-Leon H, McLarney S, et al. (2005) The Wnt antagonist secreted frizzled-related protein-1 controls osteoblast and osteocyte apoptosis. J Cell Biochem 96: 1212-1230.
30. Balemans W, Van Den Ende J, Freire Paes-Alves A, Dikkers FG, Willems PJ, et al. (1999) Localization of the gene for sclerosteosis to the van Buchem disease-gene region on chromosome 17q12-q21. Am J Hum Genet 64: 1661-1669.
31. Balemans W, Ebeling M, Patel N, Van Hul E, Olson P, et al. (2001) Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum Mol Genet 10: 537-543.
32. Brunkow ME, Gardner JC, Van Ness J, Paeper BW, Kovacevich BR, et al. (2001) Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Hum Genet 68: 577-589.
33. Li X, Ominsky MS, Niu QT, Sun N, Daugherty B, et al. (2008) Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res 23: 860-869.
34. Winkler DG, Sutherland MK, Geoghegan JC, Yu C, Hayes T, et al. (2003) Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. Embo J 22: 6267-6276.
35. Loots GG, Kneissel M, Keller H, Baptist M, Chang J, et al. (2005) Genomic deletion of a long-range bone enhancer misregulates sclerostin in Van Buchem disease. Genome Res 15: 928-935.
36. Collette NM, Genetos DC, Murugesh D, Harland RM, Loots GG, (2010) Genetic evidence that SOST inhibits WNT signaling in the limb. Dev Biol 342: 169-179.
37. Kusu N, Laurikkala J, Imanishi M, Usui H, Konishi M, et al. (2003) Sclerostin is a novel secreted osteoclast-derived bone morphogenetic protein antagonist with unique ligand specificity. J Biol Chem 278: 24113-24117.
38. Li X, Zhang Y, Kang H, Liu W, Liu P, et al. (2005) Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem 280: 19883-19887.
39. Semenov M, Tamai K, He X, (2005) SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem 280: 26770-26775.
40. Ellies DL, Viviano B, McCarthy J, Rey JP, Itasaki N, et al. (2006) Bone density ligand, Sclerostin, directly interacts with LRP5 but not LRP5G171V to modulate Wnt activity. J Bone Miner Res 21: 1738-1749.
41. Semenov MV, He X, (2006) LRP5 mutations linked to high bone mass diseases cause reduced LRP5 binding and inhibition by SOST. J Biol Chem 281: 38276-38284.
42. Morvan F, Boulukos K, Clement-Lacroix P, Roman Roman S, Suc-Royer I, et al. (2006) Deletion of a single allele of the Dkk1 gene leads to an increase in bone formation and bone mass. J Bone Miner Res 21: 934-945.
43. Keller H, Kneissel M, (2005) SOST is a target gene for PTH in bone. Bone 37: 148-158.
44. Bellido T, Ali AA, Gubrij I, Plotkin LI, Fu Q, et al. (2005) Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 146: 4577-4583.
45. Leupin O, Kramer I, Collette NM, Loots GG, Natt F, et al. (2007) Control of the SOST bone enhancer by PTH using MEF2 transcription factors. J Bone Miner Res 22: 1957-1967.
46. Chyun YS, Raisz LG, (1984) Stimulation of bone formation by prostaglandin E2. Prostaglandins 27: 97-103.
47. Jorgensen HR, Svanholm H, Host A, (1988) Bone formation induced in an infant by systemic prostaglandin-E2 administration. Acta Orthop Scand 59: 464-466.
48. Holmen SL, Zylstra CR, Mukherjee A, Sigler RE, Faugere MC, et al. (2005) Essential role of beta-catenin in postnatal bone acquisition. J Biol Chem 280: 21162-21168.
49. Poole KE, van Bezooijen RL, Loveridge N, Hamersma H, Papapoulos SE, et al. (2005) Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. Faseb J 19: 1842-1844.
50. Papanicolaou SE, Phipps RJ, Fyhrie DP, Genetos DC, (2009) Modulation of sclerostin expression by mechanical loading and bone morphogenetic proteins in osteogenic cells. Biorheology 46: 389-399.
51. Genetos DC, Toupadakis CA, Raheja LF, Wong A, Papanicolaou SE, et al. (2010) Hypoxia decreases sclerostin expression and increases Wnt signaling in osteoblasts. J Cell Biochem 110: 457-467.
52. Sugimoto Y, Narumiya S, (2007) Prostaglandin E receptors. J Biol Chem 282: 11613-11617.
53. Kiriyama M, Ushikubi F, Kobayashi T, Hirata M, Sugimoto Y, et al. (1997) Ligand binding specificities of the eight types and subtypes of the mouse prostanoid receptors expressed in Chinese hamster ovary cells. Br J Pharmacol 122: 217-224.
54. Billot X, Chateauneuf A, Chauret N, Denis D, Greig G, et al. (2003) Discovery of a potent and selective agonist of the prostaglandin EP4 receptor. Bioorg Med Chem Lett 13: 1129-1132.
55. Kamiya N, Ye L, Kobayashi T, Mochida Y, Yamauchi M, et al. (2008) BMP signaling negatively regulates bone mass through sclerostin by inhibiting the canonical Wnt pathway. Development 135: 3801-3811.
56. Kawaguchi H, Raisz LG, Voznesensky OS, Alander CB, Hakeda Y, et al. (1994) Regulation of the two Prostaglandin G/H Synthases by parathyroid hormone, interleukin-1, cortisol, and prostaglandin E2 in cultured neonatal mouse calvariae. Endocrinology 135: 1157-1164.
57. Maciel FM, Sarrazin P, Morisset S, Lora M, Patry C, et al. (1997) Induction of cyclooxygenase-2 by parathyroid hormone in human osteoblasts in culture. J Rheumatol 24: 2429-2435.
58. Li X, Ominsky MS, Warmington KS, Morony S, Gong J, et al. (2009) Sclerostin antibody treatment increases bone formation, bone mass, and bone strength in a rat model of postmenopausal osteoporosis. J Bone Miner Res 24: 578-588.
59. Li X, Warmington KS, Niu QT, Asuncion FJ, Barrero M, et al. (2010) Inhibition of sclerostin by monoclonal antibody increases bone formation, bone mass and bone strength in aged male rats. J Bone Miner Res.
60. O'Brien CA, Plotkin LI, Galli C, Goellner JJ, Gortazar AR, et al. (2008) Control of bone mass and remodeling by PTH receptor signaling in osteocytes. PLoS ONE 3: e2942.
61. Suda M, Tanaka K, Natsui K, Usui T, Tanaka I, et al. (1996) Prostaglandin E receptor subtypes in mouse osteoblastic cell line. Endocrinology 137: 1698-1705.
62. Lee CM, Genetos DC, You Z, Yellowley CE, (2007) Hypoxia regulates PGE(2) release and EP1 receptor expression in osteoblastic cells. J Cell Physiol 212: 182-188.
63. Blackwell KA, Raisz LG, Pilbeam CC, (2010) Prostaglandins in bone: bad cop, good cop? Trends Endocrinol Metab 21: 294-301.
64. Wu H, Naya FJ, McKinsey TA, Mercer B, Shelton JM, et al. (2000) MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J 19: 1963-1973.
65. Blaeser F, Ho N, Prywes R, Chatila TA, (2000) Ca(2+)-dependent gene expression mediated by MEF2 transcription factors. J Biol Chem 275: 197-209.
66. Hamamura K, Liu Y, Yokota H, (2008) Microarray analysis of thapsigargin-induced stress to the endoplasmic reticulum of mouse osteoblasts. J Bone Miner Metab 26: 231-240.
67. Gardiner PJ, (1986) Characterization of prostanoid relaxant/inhibitory receptors (psi) using a highly selective agonist, TR4979. Br J Pharmacol 87: 45-56.
68. Partridge NC, Alcorn D, Michelangeli VP, Ryan G, Martin TJ, (1983) Morphological and biochemical characterization of four clonal osteogenic sarcoma cell lines of rat origin. Cancer Res 43: 4308-4314.
69. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.